Dairy propionibacteria as human probiotics: A review of recent evidence
Fabien J. Cousin1,2,3, Denis D.G. Mater3, Benoît Foligne4 and Gwénaël Jan1,2*
INRA, UMR1253 Science et Technologie du Lait et de l’Œuf, F-35042 Rennes, France
2 AGROCAMPUS OUEST, UMR1253 Science et Technologie du Lait et de l’Œuf, F-35042 Rennes, France
3 CNIEL/Syndifrais, 42 rue de Châteaudun, F-75314 Paris 09, France
4 Institut Pasteur de Lille, Bactéries Lactiques & Immunité des Muqueuses, Centre d’Infection et d’Immunité de Lille, Unit 1019 – UMR 8204, Univ. Lille Nord de France, F-59019 Lille, France
* Corresponding author (通讯作者): email@example.com
Revised: 29 April 2010
Accepted: 29 April 2010
Probiotics have been the subject of intensive research, mainly focusing on bifidobacteria and lactic acid bacteria. However, there is evidence that dairy propionibacteria also display probiotic properties, which as yet have been underestimated. The aim of this paper is to review recent data which report probiotic characteristics of dairy propionibacteria and to distinctly organise them based on the experimental strategy employed: ranked from in vitro evidence to in vivo trials, which is a new approach. In addition to the selection criteria for probiotics in areas such as food safety, technological and digestive stress tolerance, many potential health benefits have been described which include modulation of microbiota and metabolic activity in the gut, modulation of intestinal motility and absorption, impact on intestinal inflammation, modulation of the immune system and potential modulation of risk factors for cancer development. The robust nature of dairy propionibacteria towards technological stresses should allow their future use in various fermented probiotic foods. Among the probiotic properties of dairy propionibacteria described in the literature, some of these properties are different from those reported for bifidobacteria and lactic acid bacteria. However, supplementation with dairy propionibacteria in randomised, placebo-controlled, double-blind human trials has mainly involved mixtures of propionibacteria with probiotic bacteria from other genera. Clinical studies involving the use of dairy propionibacteria alone are lacking. Such studies will allow the specifically observed health benefits to be attributed to dairy propionibacteria. This, in turn, will allow the investigation of the synergistic effects with other probiotic bacteria or beneficial food components.
Key words: probiotic / propionibacteria / Propionibacterium / short-chain fatty acid
关键字 : 益生性 / 丙酸菌 / 丙酸杆菌属 / 短链脂肪酸
© INRA, EDP Sciences, 2010
Propionibacteria were first described at the end of the 19th century by E. von Freudenreich and S. Orla-Jensen, studying propionic acid fermentation in Emmental cheese, leading to propose the genus Propionibacterium . Propionibacteria are firmicutes with a high G + C content, characterised as gram-positive, non-sporing, non-motile pleomorphic rods. They are anaerobic to aerotolerant and generally catalase positive. They grow optimally at 30 °C and are of neutral pH. Cells are hetero-fermentative and metabolise a variety of substrates such as carbohydrates (including glucose, galactose, fructose and lactose), alcohols (glycerol and erythritol) and organic acids (lactate and pyruvate). Propionibacteria present a particular central carbon metabolic pathway, propionic fermentation. This fermentation involves the Wood-Werkmann cycle  which produces propionate, acetate, succinate and carbon dioxide. The genus Propionibacterium is divided in two groups (Tab. I) based on habitat of origin: classical or dairy propionibacteria (mainly isolated from dairy products such as cheese) and cutaneous propionibacteria (typically found on skin). Recently, a new species, Propionibacterium acidifaciens, was isolated from human carious dentine . It was proposed as a member of the cutaneous group because it is closely related to Propionibacterium australiense. Dairy propionibacteria are commonly used as starter cultures in the dairy industry. Their main application is the ripening of Swiss-type cheeses, characterised by round “eyes”. In these cheeses, they play an important role in characteristic flavour and opening. Opening is due to the production of carbon dioxide. Flavour is linked to the production by dairy propionibacteria of volatiles, mainly propionate and acetate, and other compounds derived from amino acid and lipid catabolisms [19, 20, 74, 130–132].
Dairy and cutaneous Propionibacterium species.
Some strains of dairy propionibacteria are also used in probiotic preparations, alone or in combination with lactic acid bacteria and/or bifidobacteria. A probiotic is defined as “a live microorganism which, when administered in adequate amounts, confers a health benefit on the host” . An increasing number of reports on potential probiotic properties of propionibacteria have been published. However, there is far less literature on the probiotic properties of propionibacteria than on the lactobacilli and bifidobacteria. Two book chapters [53, 103] and two earlier reviews [84, 141] have reported on these potentialities. Recent evidence has been described in the literature but never reviewed. Moreover, no one has clearly sorted the probiotic characteristics described according to the level of evidence in the reports (in vitro, ex vivo, in vivo in animal models and in human beings). In addition, clinical studies have mainly reported on the use of dairy propionibacteria in complex bacterial mixtures and rarely with propionibacteria alone. This review provides an update on the probiotic potentialities of dairy propionibacteria and organises the potential health benefits according to the scientific level of the evidence. The paper only covers dairy propionibacteria, and only their probiotic potentialities in the gut. Uses as food preservatives and animal probiotics are not described here but have been extensively discussed in reports mentioned above. This paper includes six sections reviewing first selection criteria for using propionibacteria as probiotics, then probiotic potentialities of dairy propionibacteria that are suggested distinctly in vitro, ex vivo, in vivo in animal models and in human clinical study. In each section, we will successively evoke the impact of dairy propionibacteria on the gut microbiota (lowering pathogenic microorganisms and favouring beneficial ones), on different aspects of gut mucosa physiology and on the immune system. Finally, the production of others compounds related to propionibacteria and future trends in their further applications are discussed.
Selection of bacteria for probiotic application relies on criteria such as safety, technological and digestive stress survival, intestinal cell adhesion and human origin. The two last conditions are controversial and it is now recognised that they are not mandatory, although in some cases they may improve probiotic potential . These selection criteria are summarised in Table II.
Selection criteria for using dairy propionibacteria as probiotics.
The safety of dairy propionibacteria is evidenced by the widespread consumption of Swiss-type cheese. The highest rate of Emmental consumption is found in France, where per capita consumption averages 4 kg·year−1. Propionibacteria are present in Emmental in concentrations close to 109 bacteria per gram, and species Propionibacterium freudenreichii received the “Generally Recognised As Safe” (GRAS) . This opens the way to other applications such as probiotics, as discussed below. For example, one criterion studied for probiotic use is the absence of antibiotic resistance, because of the risk that any resistance will spread to intestinal microbiota. Dairy propionibacteria have natural resistance to few antibiotics and this resistance does not appear to be encoded by plasmids or other mobile genetic elements . In addition, dairy propionibacteria do not possess any known virulence factors, although some Propionibacterium thoenii and Propionibacterium jensenii strains have β-haemolytic activity . The European food safety authority has granted “Qualified presumption of safety” (QPS) status to species P. freudenreichii . No cytotoxic effect in mouse colonocytes  and no effect on the general health of rats [47, 71, 72] or infants  have been observed with strains of dairy propionibacteria. No indication of side effects from consuming dairy propionibacteria has been reported in any of the human trials reviewed here [7, 25, 26, 40–43, 55, 57–61, 64, 68–70, 89, 94, 96, 97, 103, 116, 119–122, 124, 128, 138, 139].
In addition to their tolerance to technological stresses (cheese making, encapsulation, freeze-drying etc.), dairy propionibacteria present good constitutive survival under digestive stress. In vitro, many studies have described their natural ability to survive low pH conditions and exposure to bile [46, 55, 79, 83, 127, 146, 151]. This tolerance is reinforced by a brief exposure to the same stress at a non-lethal level [54, 56, 78, 80]. Propionibacteria adapted in this way are able to survive pH values as low as two and bile salts’ concentrations higher than those reported in the human gut. The probiotic vector is also important for digestive stress tolerance. Propionibacteria in cheese had better tolerance to acid challenge than free cultures . A yoghurt-type fermented milk provided P. freudenreichii with a high tolerance towards acid challenge, bile salts challenge and a succession of the two . Survival during gastrointestinal transit has also been reported in vivo in rodents [47, 72, 107] and human beings [7, 55, 127]. A very high level of propionibacteria was detected in faeces but this concentration returned to the initial level a few days (or weeks) after consumption ceased.
Although controversial, another reported criterion for selecting probiotics is the ability to adhere to intestinal cells and/or mucosa. Dairy propionibacteria are able to adhere to immobilised mucus [105, 129, 134] and this adhesion was increased by the presence of other probiotic bacteria [12, 104]. The authors suggest that adhesion to mucus is the result of non-specific interactions, because adhesion to mucus and to bovine serum albumin was similar. Dairy propionibacteria also adhere in vitro to human intestinal epithelial cell lines [45, 77, 93]. Zarate et al.  demonstrated the adhesion of propionibacteria ex vivo to isolated mouse intestinal epithelial cells and in vivo by a plate count of the viable propionibacteria adhering to intestinal cells.
These properties of dairy propionibacteria − safety, gastrointestinal transit survival and adherence to intestinal cells and mucosa − offer good prospects for their use as human probiotics. Table III summarises promising properties further described below.
Useful characteristics for probiotic applications and beneficial effects reported for dairy propionibacteria.
As regards modulation of gut microbiota, some authors have described a reduction in pathogen adhesion to immobilised mucus in the presence of P. freudenreichii subsp. shermanii JS, alone or in combination with other probiotic bacteria [11, 13–15, 95]. Collado et al.  showed that P. freudenreichii subsp. shermanii JS is able to aggregate with pathogenic bacteria. Myllyluoma et al.  described inhibition of Helicobacter pylori adhesion to a human intestinal epithelial cell line by P. freudenreichii subsp. shermanii JS alone. The authors observed the same inhibition with a combination with other probiotic bacteria. This combination also inhibited H. pylori-induced cell membrane leakage . A major advantage of dairy propionibacteria for microbiota modulation is their ability to enhance the growth of bifidobacteria [62, 93, 116, 146]. Two bifidogenic compounds have been already identified in vitro: 1,4-dihydroxy-2-naphthoic acid (DHNA)  and 2-amino-3-carboxy-1,4-naphthoquinone (ACNQ) [61, 92]. DHNA is a precursor of menaquinone (vitamin K2) biosynthesis in bacteria. Some DHNA is released from propionibacteria during growth . ACNQ stimulated the growth of bifidobacteria at an extremely low concentration (0.5 nM) and enhanced the activity of NADH peroxidase and NADH oxidase in bifidobacteria. ACNQ, which may derive from DHNA, is an electron acceptor of NAD(P)H diaphorase and an electron donor of NAD(P)H peroxidase in bifidobacteria [61, 89, 148, 149]. NAD(P)+ regeneration is thought to be responsible for the ability of propionibacteria to stimulate bifidobacteria growth via DHNA and ACNQ. It is also worth noting that propionate, the main end-product of propionibacteria fermentation, is considered to favour the growth of bifidobacteria ; a property used in bifidobacteria selective culture media .
As regards modulation of gut enzyme activity, some bacterial species including yoghurt starters are efficient in treating lactose intolerance by enhancing β-galactosidase activity in the intestine . Propionibacterium acidipropionici and P. freudenreichii have a high level of β-galactosidase activity at 37 °C  which was even improved in the presence of bile [151, 152], by permeabilisation of cells. The authors conclude that the environment in the human intestine may be adequate for β-galactosidase synthesis and activity. They also suggested that a fermented dairy product constitutes a good vector for high β-galactosidase activity. Moreover, the enzyme withstood the cooking temperature of Swiss-type cheeses and proved to be stable during storage at low temperatures.
Propionate was recently shown to enhance expression of epithelial calcium channel ECaC2, which is involved in the transcellular route of intestinal calcium absorption in Caco-2 cells . This would at least partly explain why propionate was shown to enhance calcium absorption from the human colon . Intestinal absorption of lipids may be modulated by the consumption of probiotics, including dairy propionibacteria. Somkuti and Johnson found evidence of adsorption of cholesterol to P. freudenreichii cells. This adsorption was mainly passive, as 70% of the cholesterol removed from the medium could be recovered by solvent extraction from washed cells . This suggests, however, that the presence of dairy propionibacteria in the gut may reduce the bioavailability of cholesterol.
Propionibacteria may contribute to reduction of risk factors for cancer development particularly through the ability to bind, in vitro, carcinogenic compounds like mycotoxins [22, 98] and especially aflatoxin B1 [24, 35–37, 39, 76], cyanotoxins such as microcystin-LR , plant lectins such as concanavilin A and jacalin , and also some heavy metals such as cadmium and lead [37, 50]. The organic toxins cited above are particularly associated with colorectal cancer. Heavy metals have many deleterious effects on human health including kidney or other cancers. These data suggest that dairy propionibacteria may help to reduce gut absorption of carcinogenic compounds and so limit the emergence or development of cancer. In addition, these bacteria may be used as detoxifying additives in food contaminated by high levels of this kind of carcinogenic compound which are very difficult to remove. Vorobjeva et al. [140–142] demonstrated the antimutagenic properties of dairy propionibacteria. P. freudenreichii subsp. shermanii prevented mutations caused by various mutagenic agents. The suggested active component is a cysteine synthase of 35 kg·mol−1, secreted into the extracellular environment . Another potential anti-cancer property is the ability of P. freudenreichii and P. acidipropionici to induce apoptosis of colorectal carcinoma cells owing to the action of short-chain fatty acids, especially propionate, on cancer cell mitochondria [52, 73]. These data suggest that the use of dairy propionibacteria could reduce the incidence of colon cancer or help to treat this cancer, which is the second most fatal cancer in Europe. In addition, P. freudenreichii and P. acidipropionici induced NKG2D ligand expression on various cancer cells and the authors speculate that the pro-apoptotic effect may also be mediated by this overexpression .
P. freudenreichii has been observed to modulate the immune system in vitro by inhibition of H. pylori-induced IL-8 and PGE2 release in human intestinal epithelial cells . These anti-inflammatory effects did not persist when P. freudenreichii subsp. shermanii JS was used in combination with Lactobacillus rhamnosus GG, L. rhamnosus LC-705 and B. breve Bbi99. The authors stress the importance of characterising the individual strains to improve the therapeutic response of probiotics used in combination. In addition, P. freudenreichii and P. acidipropionici induced NKG2D ligand MICA/B expression on human-activated T lymphocytes without affecting this expression on resting peripheral blood cells. This effect was also observed with propionate alone and to a lesser extent by acetate . Expression is stimulated by higher promoter activity due to a mechanism that depends on intracellular calcium. The authors suggest that preoperative treatment with cutaneous propionibacteria strains may produce beneficial immunostimulation and increased survival of patients with colorectal carcinoma. As regards cytokine production, P. freudenreichii subsp. shermanii JS was able to induce TNF-α and IL-10 production in human PBMCs . The anti-inflammatory actions of IL-10 could be helpful in the treatment of inflammatory conditions or diseases. Interestingly, P. freudenreichii subsp. shermanii JS induced the expression of IL-12 (pro-inflammatory cytokine) only weakly , suggesting useful implication to treat colitis as reported earlier . E. coli DH5α-induced IFN-γ production was also reduced when it was combined with P. freudenreichii subsp. shermanii JS .
P. freudenreichii enhanced iron absorption from the rat proximal colon ex vivo, via the production of short-chain fatty acids (SCFA), especially propionate . The authors suggest that this absorption may be enhanced in vivo by local production of SCFA. This suggests a positive effect of dairy propionibacteria on the bioavailability of dietary iron for uptake by the liver and spleen.
The ability of dairy propionibacteria to bind carcinogenic compounds like aflatoxin B1 has also been described ex vivo [24, 34, 35]. A mixture of P. freudenreichii subsp. shermanii JS and L. rhamnosus LC-705 was able to bind aflatoxin B1 and tissue uptake of this carcinogen was reduced when probiotic bacteria were present in a duodenal loop. Consequently, this probiotic mixture could delay, but not prevent, aflatoxin B1 absorption in duodenal loops. Hence, ingestion of dairy propionibacteria may limit bioavailability, absorption and metabolisation of these carcinogenic compounds and so decrease cancer emergence risk.
Sarkar and Misra [119, 120] showed a decline in the total number of faecal bacteria in rats fed a fermented milk containing Bifidobacterium bifidum, P. freudenreichii subsp. shermanii and either L. acidophilus or not. Especially, the number of coliforms was decreased, but an increase in the bifidobacteria population was observed. Perez-Chaia et al.  noticed a similar microbiota modulation in mice consuming P. acidipropionici, with fewer anaerobes and coliforms in the caecal content. Moreover, Alvarez et al.  reported that feeding a P. acidipropionici CRL 1198 supplement to mice prior to Salmonella typhimurium administration afforded a partial protection against the pathogen colonisation. Indeed, a decrease in tissue colonisation by S. typhimurium and an increase in the mice survival rate were observed. The P. freudenreichii component DHNA ingested by mice presenting a dextran sodium sulphate (DSS)-induced colitis led to a modulation of the microbiota, including a weaker drop in the Lactobacillus and Enterobacteriaceae intestinal populations caused by DSS . DHNA also increased intestinal bifidobacteria population in mice suffering from non-steroidal anti-inflammatory drug (NSAID)-induced colitis . Bifidobacterium is probably the most amply documented genus of the human microbiota studied for probiotic properties. Thus, stimulation of bifidobacteria growth by dairy propionibacteria therefore constitutes a key probiotic potential.
Metabolic activity of P. freudenreichii has been described in the gastrointestinal tract of human microbiota-associated rats . Transcriptional activity within the intestine was demonstrated by the presence of P. freudenreichii-specific transcarboxylase mRNA. Transcarboxylase is involved in propionic acid metabolism. Strain TL133 also increased the concentrations of acetate, propionate and butyrate in rat caecal contents . In another study, mice fed P. acidipropionici CRL 1198 showed increased β-galactosidase activity and enhanced propionic acid levels in the caecum . This strain also tends to reverse the hyperlipidemic effect of a high lipid diet . This effect can be attributed to modulation of liver metabolism by absorbed propionic acid but can also be linked to the cholesterol-binding activity described above . Hypolipidemic effects of dairy propionibacteria should be confirmed in human studies.
Many bacterial enzymes, including β-glucosidase, β-glucuronidase, azoreductase and urease, are involved in producing carcinogens within the gut. Many probiotic studies have monitored the activity of these faecal enzymes. A potential modulation of risk factors for carcinogenesis has been observed in animal models. In mice fed P. acidipropionici, β-glucuronidase activity was lower than in controls on a conventional diet . With a red cooked meat supplement, the β-glucuronidase activity increased in the control mice. In the faeces of propionibacteria-supplemented mice, β-glucuronidase activity increased much less than in the control at the beginning of the meat diet and decreased thereafter. Propionibacteria supplementation prevented the increase in β-glucuronidase activity with the red meat diet. The authors also describe a slight reduction in azoreductase and nitroreductase activity . Lan et al.  report that P. freudenreichii TL133 increased induction of apoptosis in colonic mucosal crypts of human microbiota-associated rats treated with the carcinogen 1,2-dimethylhydrazine (DMH). The administration of propionibacteria alone did not increase the number of apoptotic cells in healthy colonic mucosa. This study demonstrates the ability of P. freudenreichii to favour apoptotic depletion of damaged cells at an early stage of malignant cell transformation in rats.
As regards intestinal inflammation, in some studies, colonic infusion with P. acidipropionici  or oral supplementation with a milk whey culture of P. freudenreichii ET-3  reduced the severity of TNBS-induced colitis in rats. The healing of TNBS-induced colitis was also observed with oral administration of propionate . In therapeutic and preventive studies, DHNA improved the survival rate and histological damage scores of mice with DSS-induced colitis . DHNA attenuated colonic inflammation not only by balancing intestinal bacterial ecosystem but also by suppressing lymphocyte infiltration . Okada et al.  report that DHNA had an anti-inflammatory effect on NSAID-induced colitis in IL-10-knockout mice through increased numbers of Bifidobacteria and suppression of inflammatory cell infiltration.
As regards immunomodulation, Perez-Chaia et al.  observed an improvement in carbon clearance in mice fed with P. acidipropionici CRL 1198, indicating an enhanced phagocytic function of the reticuloendothelial system. Administration of this strain prior to S. typhimurium pathogen inoculation led to an increase in both anti-S. typhimurium IgA levels and numbers of cells producing the antibody . Moreover, P. acidipropionici enhanced the phagocytic activity of isolated mouse peritoneal macrophages , which was higher with mice fed propionibacteria than in the controls. The orally administered P. acidipropionici showed this immunostimulating activity with isolated cell wall but not with isolated peptidoglycan . Immune system modulation by dairy propionibacteria may be related to the chemical composition of the cell walls, particular molecules protruding from the surface. Oral treatment of mice with P. freudenreichii subsp. shermanii JS in combination with L. rhamnosus GG increased T-cell and B-cell proliferation after stimulation with concanavalin A (T-cell mitogen), and lipopolysaccharide (B-cell mitogen), respectively . The authors suggest that these results may indicate that the splenic lymphocytes acquired a higher tolerance to the cytotoxic effects of the mitogens. They suggest that they are related to the capacity of dairy propionibacteria to bind this lectin in vitro, as cited above. Another study showed a higher T-cell proliferation of splenic lymphocytes with P. jensenii 702 in mice receiving soluble Mycobacterium tuberculosis antigens . The strain has been patented as an adjuvant for oral vaccines [1, 2].
Many teams have studied the impact of dairy propionibacteria on the human microbiota. In several independent studies, ingestion of P. freudenreichii in the form of whey cultures, whether heat-inactivated [61, 121] or not , or as freeze-dried live bacteria forms [7, 116], resulted in a higher faecal bifidobacteria population in human beings. Sarkar and Misra [119, 120] showed that a fermented milk containing B. bifidum, P. freudenreichii subsp. shermanii and either L. acidophilus or not led to a decline in coliforms and to an increase in bifidobacteria in the faeces of infants receiving the product. Whey cultures with P. freudenreichii ET-3 also triggered a decrease in Clostridium perfringens  and Bacteroides populations . In children suffering from intestinal dysbacteriosis, consumption of a milk containing P. freudenreichii subsp. shermanii and L. acidophilus restored of the microbiota, thus shortening the convalescence period during antibiotherapy . Hatakka et al.  report that a cheese containing a mixture of probiotics (L. rhamnosus GG, L. rhamnosus LC705 and P. freudenreichii ssp. shermanii JS) reduced the risk of high yeast counts, especially Candida sp., in the mouth of elderly people. These authors also observed that probiotic intervention reduced the risk of hyposalivation and a dry mouth sensation and can therefore be considered beneficial to oral heath in general. In fact, the authors suggest that the absence of protective probiotics and increased hyposalivation might explain the enhanced Candida growth in the control group. A probiotic supplementation with L. rhamnosus GG, L. rhamnosus LC70, B. breve Bb99 and P. freudenreichii ssp. shermanii JS did not significantly reduce the frequency of new or aggravated symptoms caused by antibiotic treatment during H. pylori eradication , although this probiotic combination has exhibited promising anti-Helicobacter properties in vitro (see section above). However, taking total symptom severity into account, this study suggests improved tolerance of the anti-H. pylori treatment. The authors also show that the probiotic bacteria survived in the gastrointestinal tract despite the intensive antimicrobial therapy . A more recent study has confirmed that the same probiotic mixture counteracts the effects of antibiotic treatment against H. pylori . In particular, reduced H. pylori-induced inflammation of the gastric mucosa was observed . Altogether, these results strongly suggest that the tested probiotics, containing P. freudenreichii subsp. shermanii JS, may be helpful during the treatment of H. pylori infection.
Hojo et al.  report that a high faecal bifidobacteria level due to P. freudenreichii ET-3 supplementation was linked to an increased number of defecations in constipated female volunteers. Stool frequency was also significantly increased by administration of a P. freudenreichii culture in healthy human subjects  and in elderly subjects . In another study, elderly subjects receiving a L. rhamnosus and P. freudenreichii-supplemented juice also exhibited an increase in defecation frequency . This probiotic property is interesting because constipation is a common problem in elderly subjects. Another clinical study reported a limited effect on segmental colonic motility, including slower transit in the left colon . The authors suggested that propionibacteria may regulate transit when this one is disturbed.
The consumption of a juice supplemented with L. rhamnosus LC-705 and P. freudenreichii subsp. shermanii JS led to decreased faecal azoreductase activity in elderly subjects . The same probiotic combination was used in healthy men and led to a non-significant decrease in β-glucosidase activity of 10% and in urease activity of 13% . In irritable bowel syndrome patients, a probiotic mixture containing L. rhamnosus GG, L. rhamnosus LC-705, B. breve Bb99 and P. freudenreichii subsp. shermanii JS led to a decrease in β-glucuronidase activity in most people in the probiotic group . A clinical trial investigated the effect of a probiotic preparation containing L. rhamnosus LC-705 and P. freudenreichii subsp. shermanii JS on levels of aflatoxin B1 in human faecal samples. Following probiotic administration, there was a significant reduction in the faecal level of aflatoxin B1 and this decrease continued during the follow-up period . Another study with the same probiotic supplementation in young men from Southern China found an increase in urinary samples with negative aflatoxin B1-N7-guanine and a decrease in the concentration of urinary aflatoxin B1-N7-guanine in the probiotic group . Aflatoxin B1-N7-guanine is a marker for a biologically effective dose of aflatoxin. The probiotic supplementation thus reduced the organism’s exposure to this carcinogen.
A commercial preparation of bifidogenic growth stimulator (BGS), which is produced by P. freudenreichii ET-3, led to an improvement in the clinical activity scores of ulcerative colitis patients [89, 128]. Patients also showed a decrease in the endoscopic index and an improvement in serum haemoglobin and albumin concentrations . An increase in all SCFA concentrations was measured after BGS ingestion but this was significant only for butyrate . The authors suggest that BGS restores a healthy microbial balance, thus favouring beneficial competitive interactions which may prevent or treat ulcerative colitis.
Kekkonen et al.  report that a probiotic intervention with P. freudenreichii subsp. shermanii JS in healthy adults led to a reduction in the serum level of C-reactive protein (CRP) compared to a placebo control. CRP being a sensitive inflammation marker, this result confirms the anti-inflammatory potential of dairy propionibacteria. In a randomised, placebo-controlled, double-blind trial was performed in Helsinki on infants at high risk of allergy, a probiotic mixture containing L. rhamnosus GG, L. rhamnosus LC-705, B. breve Bb99 and P. freudenreichii subsp. shermanii JS was given daily for six months after birth and compared to a placebo [68–70]. Two years after birth, less antibiotic prescription and fewer respiratory infections were reported in the supplemented infant group, whatever the mode of delivery . In addition, less eczema and less atopic eczema were diagnosed in the treated group . Five years following birth, significant differences were detected among caesarean-delivered children: less IgE-associated disease occurred, particularly eczema, and less IgE sensitisation was detected . Thus, during the first stages of life, probiotic supplementation including propionibacteria seems to promote immune system maturation, preventing infections and allergies. In addition, such supplementation would further counteract disorders linked to caesarean delivery such as delayed colonisation of the gut by bifidobacteria and lactobacilli. Another randomised, placebo-controlled, double-blind trial tested the same probiotic mixture in infants with atopic eczema-dermatitis syndrome (AEDS) and suspected cow’s milk allergy (CMA). Soluble E-selectin and plasma IL-10 levels were higher after probiotic supplementation than after placebo treatment  and faecal IgA levels tended to be higher in the probiotic group . Another study showed that a mixture of P. freudenreichii subsp. shermanii JS, L. rhamnosus GG and LC-705 and B. breve Bbi99 increased IL-4 secretion and tended to stimulate IFN-γ secretion in PBMCs of infants with CMA . This may offer clinical benefits in the treatment of allergic diseases by immunologic means. Altogether, these clinical data indicate beneficial immunomodulation by a mixture of gram-positive bacteria including P. freudenreichii subsp. shermanii JS, with a reported anti-inflammatory effect of the latter. Further clinical data should pin down the role of dairy propionibacteria per se.
Many other properties of dairy propionibacteria can be regarded as beneficial . They secrete bacteriocins , anti-fungal compounds  and anti-viral compounds [16, 32, 33, 112–115] and are therefore used as food preservatives. Propionate, being an SCFA, has been investigated for its health effects. In particular, preliminary in vitro investigations suggest that propionate has a role inducing apoptosis of gastric cancer cells  and in preventing colon cancer cell colonisation . In vivo, propionate increased secretion of intestinal mucus in rats  and human colorectal calcium absorption . The suggested beneficial effects of propionate suggest similar properties for dairy propionibacteria, mediated by their metabolism end-products. As an example, induction of the satietogen peptide PYY by SCFAs having been reported , Ruijschop et al.  tested a dairy product fermented by lactic acid bacteria and propionibacteria in a human study. After consumption of this product, subjects felt significantly fuller, were less hungry and had less desire to eat . However, the authors report no effect on ad libitum food consumption. Also of health interest is the capacity of dairy propionibacteria to improve the nutritional quality of fermented products by synthesising vitamins, trehalose and conjugated linoleic acid (CLA). Dairy propionibacteria synthesise vitamin B8 (biotin), B9 (folic acid) and B12 (cobalamin) . Folic acid has been described as an agent for colorectal cancer prevention but this claim is controversial . Trehalose has been observed to reduce the level of enterohaemorrhagic Escherichia coli O157:H7 in ruminants because this sugar can be used by commensal E. coli but not by the O157:H7 strain . The broad spectrum of biological effects reported for conjugated linoleic acids [10, 144] includes the anticarcinogenic properties of rumenic acid, the cis-9,trans-11 stereoisomer of CLA [75, 82]. P. freudenreichii has been shown to convert linoleic acid to rumenic acid [86, 110, 111, 136, 145] and the corresponding mechanisms have been identified . As the authors of that study suggest, rumenic acid formation in the human gut could promote health.
The technological qualities of dairy propionibacteria constitute a key advantage for their uses as probiotics. They survive the technological stresses imposed during freeze-drying, spray-drying, reconstitution in milk, cheese making and storage at low temperatures. Dairy propionibacteria ferment a wide range of carbohydrate substrates. Such remarkable adaptability, robustness and versatility are consistent with the occurrence of propionibacteria in various niches and should allow their growth and/or viability in a variety of probiotic vectors.
Most of the clinical studies have been conducted using mixtures of bacteria from different genera. The development of a pure culture of dairy propionibacteria in a food grade vector will make it possible to pin down their specific probiotic potential in human beings. However, synergistic effect between different probiotics should also be investigated in the different fields of beneficial activity. In addition, complex interactions between ingested probiotics and the complex gut microbiota should be taken into consideration. In this context, the ability of dairy propionibacteria to modulate this microbiota, beyond the propionibacteria population itself, is of particular interest.
Probiotic properties “in general”, including bifidobacteria and lactobacilli, differ from a species to another and are strain-dependent. It is therefore necessary to screen a large number of dairy propionibacteria in order to select strains with the best potentialities for dedicated applications. In this context, such approach to study immunomodulation of a large set of diverse single propionibacteria both in vitro (PBMC) and in vivo (experimental colitis and infectious mice models) have already been initiated and developed (Deutsch/Foligné et al., personal communication) and should fill some gaps soon. Besides classical screening methods, the first dairy Propionibacterium genome from a P. freudenreichii subsp. shermanii strain is expected to be available soon. Genomic data will allow new mechanistic investigations of its probiotic potential .
In conclusion, although more experimental data are available concerning probiotic applications of bifidobacteria and lactobacilli, dairy propionibacteria also deserve attention. Indeed, there is now specific promising evidence from dairy propionibacteria regarding beneficial modulation of colon microbiota and carcinogenesis together with anti-inflammatory and immune properties. Future works should focus on the development of molecular tools and appropriate delivery vectors as well as on selecting the best strains. Progress on these aspects will allow specific clinical studies. These in turn should lead to a better understanding and exploitation of the beneficial effects of dairy propionibacteria in the different compartments of the gastrointestinal tract.
Individual probiotics demonstrate unique, specific biological effects. Knowledge of the specific effects of each probiotic strain will allow the development of probiotic mixtures adapted to particular cases or pathologies. Selecting (mixtures of) probiotics for use in disease(s) treatment will be guided by improved knowledge on action mechanisms based on established experimental models from in vitro to clinic. Knowledge of probiotic mechanisms may allow us to select the strain(s) with the best possible expected biological outcome. However, bench-to-bedside clinical trials will remain necessary to validate the chosen strain selection strategy. It will also confirm the physiological effectiveness of the proposed mechanisms in, for example, a wider population of patients suffering immune disorders, such as Inflammatory Bowel Diseases (IBD) and Irritable Bowel Syndrome (IBS), as well as other gastrointestinal infection diseases, cancers and allergies.
The authors thank Hariet Coleman for revising and correcting the English language. This work was financially supported by the Science Committee of Syndifrais and the Centre National Interprofessionnel de l’Économie Laitière (CNIEL). F.C. received a grant from CNIEL.
- Adams M.C., Huang Y., Probiotic Propionibacterium jensenii 702, Patent WO2004001022-A1, 2003. (In the text)
- Adams M.C., Huang Y., Probiotic Propionibacterium, Patent US 07427397, 2008. (In the text)
- Adams M.C., Lean M.L., Hitchick N.C., Beagley K.W., The efficacy of Propionibacterium jensenii 702 to stimulate a cell-mediated response to orally administered soluble Mycobacterium tuberculosis antigens using a mouse model, Lait 85 (2005) 75–84. [CrossRef] [EDP Sciences] (In the text)
- Alvarez S., Medicini M., Vintini E., Oliver G., De Ruiz Holgado A.P., Perdigon G., Effect of the oral administration of Propionibacterium acidi-propionici on IgA levels and on the prevention of enteric infection in mice, Microbiol. Alim. Nut. 14 (1996) 237–243. (In the text)
- Andresen L., Hansen K.A., Jensen H., Pedersen S.F., Stougaard P., Hansen H.R., Jurlander J., Skov S., Propionic acid secreted from propionibacteria induces NKG2D ligand expression on human-activated T lymphocytes and cancer cells, J. Immunol. 183 (2009) 897–906. [CrossRef] [PubMed] (In the text)
- Anonymous, Scientific opinion of the panel on biological hazards on a request from EFSA on the maintenance of the QPS list of microorganisms intentionally added to food or feed, EFSA Journal 923 (2008) 1–48. (In the text)
- Bouglé D., Roland N., Lebeurrier F., Arhan P., Effect of propionibacteria supplementation on fecal bifidobacteria and segmental colonic transit time in healthy human subjects, Scand. J. Gastroenterol. 34 (1999) 144–148. [CrossRef] [PubMed] (In the text)
- Bouglé D., Vaghefi-Vaezzadeh N., Roland N., Bouvard G., Arhan P., Bureau F., Neuville D., Maubois J.-L., Influence of short-chain fatty acids on iron absorption by proximal colon, Scand. J. Gastroenterol. 37 (2002) 1008–1011. [CrossRef] [PubMed] (In the text)
- Cherbut C., Ferrier L., Roze C., Anini Y., Blottière H., Lecannu G., Galimiche J.P., Short-chain fatty acids modify colonic motility through nerves and polypeptide YY release in the rat, Am. J. Physiol. Gastrointest. Liver Physiol. 275 (1998) G1415–G1422. (In the text)
- Churruca I., Fernandez-Quintela A., Portillo M.P., Conjugated linoleic acid isomers: differences in metabolism and biological effects, Biofactors 35 (2009) 105–111. [CrossRef] [PubMed] (In the text)
- Collado M.C., Jalonen L., Meriluoto J., Salminen S., Protection mechanism of probiotic combination against human pathogens: in vitro adhesion to human intestinal mucus, Asia Pac. J. Clin. Nutr. 15 (2006) 570–575. [PubMed] (In the text)
- Collado M.C., Meriluoto J., Salminen S., Development of new probiotics by strain combinations: Is it possible to improve the adhesion to intestinal mucus?, J. Dairy Sci. 90 (2007) 2710–2716. [CrossRef] [PubMed] (In the text)
- Collado M.C., Meriluoto J., Salminen S., In vitro analysis of probiotic strain combinations to inhibit pathogen adhesion to human intestinal mucus, Food Res. Int. 40 (2007) 629–636. [CrossRef] (In the text)
- Collado M.C., Meriluoto J., Salminen S., Role of commercial probiotic strains against human pathogen adhesion to intestinal mucus, Lett. Appl. Microbiol. 45 (2007) 454–460. [CrossRef] [PubMed] (In the text)
- Collado M.C., Meriluoto J., Salminen S., Adhesion and aggregation properties of probiotic and pathogen strains, Eur. Food Res. Technol. 226 (2008) 1065–1073. [CrossRef] (In the text)
- Cutting W., Read G., Cords H., Preliminary studies on the chemical nature of propionin, Stanford. Med. Bull. 20 (1962) 156–162. [PubMed] (In the text)
- de Vaux A., Morrison M., Hutkins R.W., Displacement of Escherichia coli O157:H7 from rumen medium containing prebiotic sugars, Appl. Environ. Microbiol. 68 (2002) 519–524. [CrossRef] [PubMed] (In the text)
- de Vrese M., Stegelmann A., Richter B., Fenselau S., Laue C., Schrezenmeir J., Probiotics – compensation for lactase insufficiency, Am. J. Clin. Nutr. 73 (2001) 421S–429S. [PubMed] (In the text)
- Dherbecourt J., Falentin H., Jardin J., Maillard M.B., Bagliniere F., Barloy-Hubler F., Thierry A., Identification of a secreted lipolytic esterase in Propionibacterium freudenreichii, a ripening process bacterium involved in Emmental cheese lipolysis, Appl. Environ. Microbiol. 76 (2010) 1181–1188. [CrossRef] [PubMed] (In the text)
- Dherbecourt J., Maillard M.B., Catheline D., Thierry A., Production of branched-chain aroma compounds by Propionibacterium freudenreichii: links with the biosynthesis of membrane fatty acids, J. Appl. Microbiol. 105 (2008) 977–985. [CrossRef] [PubMed] (In the text)
- Downes J., Wade W.G., Propionibacterium acidifaciens sp. nov., isolated from the human mouth, Int. J. Syst. Evol. Microbiol. 59 (2009) 2778–2781. [CrossRef] [PubMed] (In the text)
- El-Nezami H.S., Chrevatidis A., Auriola S., Salminen S., Mykkanen H., Removal of common Fusarium toxins in vitro by strains of Lactobacillus and Propionibacterium , Food Addit. Contam. 19 (2002) 680–686. [CrossRef] [PubMed] (In the text)
- El-Nezami H., Kankaanpaa P., Salminen S., Ahokas J., Ability of dairy strains of lactic acid bacteria to bind a common food carcinogen, aflatoxin B-1, Food Chem. Toxicol. 36 (1998) 321–326. [CrossRef] [PubMed] (In the text)
- El-Nezami H., Mykkanen H., Kankaanpaa P., Salminen S., Ahokas J., Ability of Lactobacillus and Propionibacterium strains to remove aflatoxin B-1 from the chicken duodenum, J. Food Prot. 63 (2000) 549–552. [PubMed] (In the text)
- El-Nezami H., Mykkanen H., Kankaanpaa P., Suomalainen T., Salminen S., Ahokas J., Ability of a mixture of Lactobacillus and Propionibacterium to influence the faecal aflatoxin content in healthy Egyptian volunteers: a pilot clinical study, Biosci. Microflora 19 (2000) 41–45. (In the text)
- El-Nezami H.S., Polychronaki N.N., Ma J., Zhu H.L., Ling W.H., Salminen E.K., Juvonen R.O., Salminen S.J., Poussa T., Mykkanen H.M., Probiotic supplementation reduces a biomarker for increased risk of liver cancer in young men from Southern China, Am. J. Clin. Nutr. 83 (2006) 1199–1203. [PubMed] (In the text)
- Emenaker N.J., Basson M.D., Short chain fatty acids inhibit human (SW1116) colon cancer cell invasion by reducing urokinase plasminogen activator activity and stimulating TIMP-1 and TIMP-2 activities, rather than via MMP modulation, J. Surg. Res. 76 (1998) 41–46. [CrossRef] [PubMed] (In the text)
- FAO, WHO, Probiotics in food: health and nutritional properties and guidelines for evaluation, FAO Food Nutr. Pap., 2006. (In the text)
- Foligné B., Nutten S., Grangette C., Dennin V., Goudercourt D., Poiret S., Dewulf J., Brassart D., Mercenier A., Pot B., Correlation between in vitro and in vivo immunomodulatory properties of lactic acid bacteria, World J. Gastroenterol. 13 (2007) 236–243. [PubMed] (In the text)
- Fukushima A., Aizaki Y., Sakuma K., Short-chain fatty acids induce intestinal transient receptor potential vanilloid type 6 expression in rats and Caco-2 cells, J. Nutr. 139 (2009) 20–25. [PubMed] (In the text)
- Furuichi K., Hojo K., Katakura Y., Ninomiya K., Shioya S., Aerobic culture of Propionibacterium freudenreichii ET-3 can increase production ratio of 1, 4-dihydroxy-2-naphthoic acid to menaquinone, J. Biosci. Bioeng. 101 (2006) 464–470. [CrossRef] [PubMed] (In the text)
- Furusawa E., Furusawa S., Cutting W., Action mechanism of propionin against intracellular vaccinia multiplication and comparison with other agents, Med. Pharmacol. Exp. Int. J. Exp. Med. 12 (1965) 259–265. [PubMed] (In the text)
- Furusawa E., Ramanathan S., Furusawa S., Woo Y.K., Cutting W., Antiviral activity of higher plants and propionin on lymphocytic choriomeningitis infection, Proc. Soc. Exp. Biol. Med. 125 (1967) 234–239. [PubMed] (In the text)
- Gratz S., El-Nezami H., Mykkanen H., Probiotic bacteria retard the ex vivo absorption of aflatoxin B-1 from chick duodenum, Toxicology 191 (2003) 50. (In the text)
- Gratz S., Mykkanen H., El-Nezami H., Aflatoxin B-1 binding by a mixture of Lactobacillus and Propionibacterium: in vitro versus ex vivo, J. Food Prot. 68 (2005) 2470–2474. [PubMed] (In the text)
- Gratz S., Mykkanen H., Ouwehand A.C., Juvonen R., Salminen S., El-Nezami H., Intestinal mucus alters the ability of probiotic bacteria to bind aflatoxin B-1 in vitro, Appl. Environ. Microbiol. 70 (2004) 6306–6308. [CrossRef] [PubMed]
- Halttunen T., Collado M.C., El-Nezami H., Meriluoto J., Salminen S., Combining strains of lactic acid bacteria may reduce their toxin and heavy metal removal efficiency from aqueous solution, Lett. Appl. Microbiol. 46 (2008) 160–165. [CrossRef] [PubMed] (In the text)
- Hartemink R., Rombouts F.M., Comparison of media for the detection of bifidobacteria, lactobacilli and total anaerobes from faecal samples, J. Microbiol. Methods 36 (1999) 181–192. [CrossRef] [PubMed] (In the text)
- Haskard C.A., El-Nezami H.S., Kankaanpaa P.E., Salminen S., Ahokas J.T., Surface binding of aflatoxin B-1 by lactic acid bacteria, Appl. Environ. Microbiol. 67 (2001) 3086–3091. [CrossRef] [PubMed] (In the text)
- Hatakka K., AholaA.J., Yli-Knuuttila H., Richardson M., Poussa T., Meurman J.H., Korpela R., Probiotics reduce the prevalence of oral Candida in the elderly – a randomized controlled trial, J. Dent. Res. 86 (2007) 125–130. [CrossRef] [PubMed] (In the text)
- Hatakka K., Holma R., El-Nezami H., Suomalainen T., Kuisma M., Saxelin M., Polussa T., Mykkänen H., Korpela R., The influence of Lactobacillus rhamnosus LC705 together with Propionibacterium freudenreichii ssp. shermanii JS on potentially carcinogenic bacterial activity in human colon, Int. J. Food Microbiol. 128 (2008) 406–410. [CrossRef] [PubMed] (In the text)
- Hervé C., Fondrevez M., Cheron A., Barloy-Hubler F., Jan G., Transcarboxylase mRNA: a marker which evidences P. freudenreichii survival and metabolic activity during its transit in the human gut, Int. J. Food Microbiol. 113 (2007) 303–314. [CrossRef] [PubMed] (In the text)
- Hojo K., Yoda N., Tsuchita H., Ohtsu T., Seki K., Taketomo N., Murayama T., Iino H., Effect of ingested culture of Propionibacterium freudenreichii ET-3 on fecal microflora and stool frequency in healthy females, Biosci. Microflora 21 (2002) 115–120. (In the text)
- Holo H., Faye T., Brede D.A., Nilsen T., Odegard I., Langsrud T., Brendehaug J., Nes I.F., Bacteriocins of propionic acid bacteria, Lait 82 (2002) 59–68. [CrossRef] [EDP Sciences] (In the text)
- Huang Y., Adams M.C., An in vitro model for investigating intestinal adhesion of potential dairy propionibacteria probiotic strains using cell line C2BBe1, Lett. Appl. Microbiol. 36 (2003) 213–216. [CrossRef] [PubMed] (In the text)
- Huang Y., Adams M.C., In vitro assessment of the upper gastrointestinal tolerance of potential probiotic dairy propionibacteria, Int. J. Food Microbiol. 91 (2004) 253–260. [CrossRef] [PubMed] (In the text)
- Huang Y., Kotula L., Adams M.C., The in vivo assessment of safety and gastrointestinal survival of an orally administered novel probiotic, Propionibacterium jensenii 702, in a male Wistar rat model, Food Chem. Toxicol. 41 (2003) 1781–1787. [CrossRef] [PubMed] (In the text)
- Hubner R.A., Houlston R.S., Folate and colorectal cancer prevention, Br. J. Cancer 100 (2009) 233–239. [CrossRef] [PubMed] (In the text)
- Hugenholtz J., Hunik J., Santos H., Smid E., Nutraceutical production by propionibacteria, Lait 82 (2002) 103–112. [CrossRef] [EDP Sciences] (In the text)
- Ibrahim F., Halttunen T., Tahvonen R., Salminen S., Probiotic bacteria as potential detoxification tools: assessing their heavy metal binding isotherms, Can. J. Microbiol. 52 (2006) 877–885. [CrossRef] [PubMed] (In the text)
- Isawa K., Hojo K., Yoda N., Kamiyama T., Makino S., Saito M., Sugano H., Mizoguchi C., Kurama S., Shibasaki M., Endo N., Sato Y., Isolation and identification of a new bifidogenic growth stimulator produced by Propionibacterium freudenreichii ET-3, Biosci. Biotechnol. Biochem. 66 (2002) 679–681. [CrossRef] [PubMed] (In the text)
- Jan G., Belzacq A.S., Haouzi D., Rouault A., Metivier D., Kroemer G., Brenner C., Propionibacteria induce apoptosis of colorectal carcinoma cells via short-chain fatty acids acting on mitochondria, Cell Death Differ. 9 (2002) 179–188. [CrossRef] [MathSciNet] [PubMed] (In the text)
- Jan G., Lan A., Leverrier P., Dairy propionibacteria as probiotics, in: Saarela M. (Ed.), Functional dairy products, vol. 2, Woodhead Publishing Ltd, Cambridge, UK, 2007, pp. 165–194. (In the text)
- Jan G., Leverrier P., Pichereau V., Boyaval P., Changes in protein synthesis and morphology during acid adaptation of Propionibacterium freudenreichii, Appl. Environ. Microbiol. 67 (2001) 2029–2036. [CrossRef] [PubMed] (In the text)
- Jan G., Leverrier P., Proudy I., Roland N., Survival and beneficial effects of propionibacteria in the human gut: in vivo and in vitro investigations, Lait 82 (2002) 131–144. [CrossRef] [EDP Sciences] (In the text)
- Jan G., Rouault A., Maubois J.L., Acid stress susceptibility and acid adaptation of Propionibacterium freudenreichii subsp. shermanii, Lait 80 (2000) 325–336. [CrossRef] [EDP Sciences] [MathSciNet] (In the text)
- Kajander K., Hatakka K., Poussa T., Markkila M., Korpela R., A probiotic mixture alleviates symptoms in irritable bowel syndrome patients: a controlled 6-month intervention, Aliment. Pharmacol. Ther. 22 (2005) 387–394. [CrossRef] [PubMed] (In the text)
- Kajander K., Korpela R., Clinical studies on alleviating the symptoms of irritable bowel syndrome with a probiotic combination, Asia Pac. J. Clin. Nutr. 15 (2006) 576–580. [PubMed] (In the text)
- Kajander K., Krogius-Kurikka L., Rinttila T., Karjalainen H., Palva A., Korpela R., Effects of multispecies probiotic supplementation on intestinal microbiota in irritable bowel syndrome, Aliment. Pharmacol. Ther. 26 (2007) 463–473. [CrossRef] [PubMed] (In the text)
- Kajander K., Myllyluoma E., Rajilic-Stojanovic M., Kyronpalo S., Rasmussen M., Jarvenpaa S., Zoetendal E.G., De Vos W.M., Vapaatalo H., Korpela R., Clinical trial: multispecies probiotic supplementation alleviates the symptoms of irritable bowel syndrome and stabilizes intestinal microbiota, Aliment. Pharmacol. Ther. 27 (2008) 48–57. [CrossRef] [PubMed] (In the text)
- Kaneko T., A novel bifidogenic growth stimulator produced by Propionibacterium freudenreichii, Biosci. Microflora 18 (1999) 73–80. (In the text)
- Kaneko T., Mori H., Iwata M., Meguro S., Growth stimulator for bifidobacteria produced by Propionibacterium freudenreichii and several intestinal bacteria, J. Dairy Sci. 77 (1994) 393–404. [CrossRef] [PubMed] (In the text)
- Kekkonen R.A., Kajasto E., Miettinen M., Veckman V., Korpela R., Julkunen I., Probiotic Leuconostoc mesenteroides ssp. cremoris and Streptococcus thermophilus induce IL-12 and IFN-gamma production, World J. Gastroenterol. 14 (2008) 1192–1203. [CrossRef] [PubMed] (In the text)
- Kekkonen R.A., Lummela N., Karjalainen H., Latvala S., Tynkkynen S., Jarvenpaa S., Kautiainen H., Julkunen I., Vapaatalo H., Korpela R., Probiotic intervention has strain-specific anti-inflammatory effects in healthy adults, World J. Gastroenterol. 14 (2008) 2029–2036. [CrossRef] [PubMed] (In the text)
- Kirjavainen P.V., El-Nezami H.S., Salminen S.J., Ahokas J.T., Wright P.F.A., Effects of orally administered viable Lactobacillus rhamnosus GG and Propionibacterium freudenreichii subsp. shermanii JS on mouse lymphocyte proliferation, Clin. Diagn. Lab. Immunol. 6 (1999) 799–802. [PubMed] (In the text)
- Klaenhammer T.R., Barrangou R., Buck B.L., Azcarate-Peril M.A., Altermann E., Genomic features of lactic acid bacteria effecting bioprocessing and health, FEMS Microbiol. Rev. 29 (2005) 393–409. [CrossRef] [PubMed] (In the text)
- Kouya T., Misawa K., Horiuchi M., Nakayama E., Deguchi H., Tanaka T., Taniguchi M., Production of extracellular bifidogenic growth stimulator by anaerobic and aerobic cultivations of several propionibacterial strains, J. Biosci. Bioeng. 103 (2007) 464–471. [CrossRef] [PubMed] (In the text)
- Kuitunen M., Kukkonen K., Juntunen-Backman K., Korpela R., Poussa T., Tuure T., Haahtela T., Savilahti E., Probiotics prevent IgE-associated allergy until age 5 years in cesarean-delivered children but not in the total cohort, J. Allergy Clin. Immunol. 123 (2009) 335–341. [CrossRef] [PubMed] (In the text)
- Kukkonen K., Savilahti E., Haahtela T., Juntunen-Backman K., Korpela R., Poussa T., Tuure T., Kuitunen M., Probiotics and prebiotic galacto-oligosaccharides in the prevention of allergic diseases: a randomized, double-blind, placebo-controlled trial, J. Allergy Clin. Immunol. 119 (2007) 192–198. [CrossRef] [PubMed] (In the text)
- Kukkonen K., Savilahti E., Haahtela T., Juntunen-Backman K., Korpela R., Poussa T., Tuure T., Kuitunen M., Long-term safety and impact on infection rates of postnatal probiotic and prebiotic (synbiotic) treatment: randomized, double-blind, placebo-controlled trial, Pediatrics 122 (2008) 8–12. [CrossRef] [PubMed] (In the text)
- Lan A., Bruneau A., Bensaada M., Philippe C., Bellaud P., Rabot S., Jan G., Increased induction of apoptosis by Propionibacterium freudenreichii TL133 in colonic mucosal crypts of human microbiota-associated rats treated with 1, 2-dimethylhydrazine, Br. J. Nutr. 100 (2008) 1251–1259. [CrossRef] [MathSciNet] [PubMed] (In the text)
- Lan A., Bruneau A., Philippe C., Rochet V., Rouault A., Herve C., Roland N., Rabot S., Jan G., Survival and metabolic activity of selected strains of Propionibacterium freudenreichii in the gastrointestinal tract of human microbiota-associated rats, Br. J. Nutr. 97 (2007) 714–724. [CrossRef] [PubMed] (In the text)
- Lan A., Lagadic-Gossmann D., Lemaire C., Brenner C., Jan G., Acidic extracellular pH shifts colorectal cancer cell death from apoptosis to necrosis upon exposure to propionate and acetate, major end-products of the human probiotic propionibacteria, Apoptosis 12 (2007) 573–591. [CrossRef] [PubMed] (In the text)
- Langsrud T., Reinbold G.W., Flavor development and microbiology of Swiss cheese. A review. III. Ripening and flavor production, J. Milk Food Technol. 36 (1973) 593–609. (In the text)
- Lavillonniere F., Chajes V., Martin J.C., Sebedio J.L., Lhuillery C., Bougnoux P., Dietary purified cis-9, trans-11 conjugated linoleic acid isomer has anticarcinogenic properties in chemically induced mammary tumors in rats, Nutr. Cancer 45 (2003) 190–194. [CrossRef] [PubMed] (In the text)
- Lee Y.K., El-Nezami H., Haskard C.A., Gratz S., Puong K.Y., Salminen S., Mykkanen H., Kinetics of adsorption and desorption of aflatoxin B-1 by viable and nonviable bacteria, J. Food Prot. 66 (2003) 426–430. [PubMed] (In the text)
- Lehto E.M., Salminen S., Adhesion of two Lactobacillus strains, one Lactococcus and one Propionibacterium strain to cultured human intestinal Caco-2 cell line, Biosci. Microflora 16 (1997) 13–17. (In the text)
- Leverrier P., Dimova D., Pichereau V., Auffray Y., Boyaval P., Jan G.L., Susceptibility and adaptive response to bile salts in Propionibacterium freudenreichii: physiological and proteomic analysis, Appl. Environ. Microbiol. 69 (2003) 3809–3818. [CrossRef] [PubMed] (In the text)
- Leverrier P., Fremont Y., Rouault A., Boyaval P., Jan G., In vitro tolerance to digestive stresses of propionibacteria: influence of food matrices, Food Microbiol. 22 (2005) 11–18. [CrossRef] (In the text)
- Leverrier P., Vissers J.P.C., Rouault A., Boyaval P., Jan G., Mass spectrometry proteomic analysis of stress adaptation reveals both common and distinct response pathways in Propionibacterium freudenreichii, Arch. Microbiol. 181 (2004) 215–230. [CrossRef] [PubMed] (In the text)
- Lind H., Sjogren J., Gohil S., Kenne L., Schnurer J., Broberg A., Antifungal compounds from cultures of dairy propionibacteria type strains, FEMS Microbiol. Lett. 271 (2007) 310–315. [CrossRef] [PubMed] (In the text)
- Lock A.L., Corl B.A., Barbano D.M., Bauman D.E., Ip C., The anticarcinogenic effect of trans-11 18: One is dependent on its conversion to cis-9, trans-11 CLA by Delta 9-desaturase in rats, J. Nutr. 134 (2004) 2698–2704. [PubMed] (In the text)
- Mantere-Alhonen S., On the survival of a Propionibacterium freudenreichii culture during in vitro gastric digestion, Meijeritieteellinen Aikakauskirja 41 (1983) 19–23. (In the text)
- Mantere-Alhonen S., Propionibacteria used as probiotics – a review, Lait 75 (1995) 447–452. [CrossRef] [EDP Sciences] (In the text)
- Matthews G.M., Howarth G.S., Butler R.N., Short-chain fatty acid modulation of apoptosis in the Kato III human gastric carcinoma cell line, Cancer Biol. Ther. 6 (2007) 1051–1057. [CrossRef] [PubMed] (In the text)
- McIntosh F.M., Shingfield K.J., Devillard E., Russell W.R., Wallace R.J., Mechanism of conjugated linoleic acid and vaccenic acid formation in human faecal suspensions and pure cultures of intestinal bacteria, Microbiology 155 (2009) 285–294. [CrossRef] [PubMed] (In the text)
- Meile L., Le Blay G., Thierry A., Safety assessment of dairy microorganisms: Propionibacterium and Bifidobacterium, Int. J. Food Microbiol. 126 (2008) 316–320. [CrossRef] [PubMed] (In the text)
- Michel C., Roland N., Lecannu G., Hervé C., Avice J.C., Rival M., Cherbut C., Colonic infusion with Propionibacterium acidipropionici reduces severity of chemically-induced colitis in rats, Lait 85 (2005) 99–111. [CrossRef] [EDP Sciences] (In the text)
- Mitsuyama K., Masuda J., Yamasaki H., Kuwaki K., Kitazaki S., Koga H., Uchida M., Sata M., Treatment of ulcerative colitis with milk whey culture with Propionibacterium freudenreichii, J. Intest. Microbiol. 21 (2007) 143–147. (In the text)
- Mogensen G., Salminen S., O’Brien J., Ouwehand A., Holzapfel W., Shortt C., Fonden R., Miller G., Donohue D., Playne M., Crittenden R., Salvadori B., Zink R., Inventory of microorganisms with a documented history of use in food, Bulletin of the IDF (2002) 10–19. (In the text)
- Morata de Ambrosini V., Gonzalez S., Perdigon G., De Ruiz Holgado A.P., Oliver G., Immunostimulating activity of cell walls from lactic acid bacteria and related species, Food Agric. Immunol. 10 (1998) 183–191. [CrossRef] (In the text)
- Mori H., Sato Y., Taketomo N., Kamiyama T., Yoshiyama Y., Meguro S., Sato H., Kaneko T., Isolation and structural identification of bifidogenic growth stimulator produced by Propionibacterium freudenreichii , J. Dairy Sci. 80 (1997) 1959–1964. [CrossRef] [PubMed] (In the text)
- Moussavi M., Adams M.C., An in vitro study on bacterial growth interactions and intestinal epithelial cell adhesion characteristics of probiotic combinations, Curr. Microbiol. 60 (2010) 327–335. [CrossRef] [PubMed] (In the text)
- Myllyluoma E., Ahlroos T., Veijola L., Rautelin H., Tynkkynen S., Korpela R., Effects of anti-Helicobacter pylori treatment and probiotic supplementation on intestinal microbiota, Int. J. Antimicrob. Agents 29 (2007) 66–72. [CrossRef] [PubMed] (In the text)
- Myllyluoma E., Ahonen A.M., Korpela R., Vapaatalo H., Kankuri E., Effects of multispecies probiotic combination on Helicobacter pylori infection in vitro, Clin. Vaccine Immunol. 15 (2008) 1472–1482. [CrossRef] [PubMed] (In the text)
- Myllyluoma E., Kajander K., Mikkola H., Kyronpalo S., Rasmussen M., Kankuri E., Sipponen P., Vapaatalo H., Korpela R., Probiotic intervention decreases serum gastrin-17 in Helicobacter pylori infection, Digest. Liver Dis. 39 (2007) 516–523. [CrossRef] (In the text)
- Myllyluoma E., Veijola L., Ahlroos T., Tynkkynen S., Kankuri E., Vapaatalo H., Rautelin H., Korpela R., Probiotic supplementation improves tolerance to Helicobacter pylori eradication therapy – a placebo-controlled, double-blind randomized pilot study, Aliment. Pharmacol. Ther. 21 (2005) 1263–1272. [CrossRef] [PubMed] (In the text)
- Niderkorn V., Boudra H., Morgavi D.P., Binding of Fusarium mycotoxins by fermentative bacteria in vitro, J. Appl. Microbiol. 101 (2006) 849–856. [CrossRef] [PubMed] (In the text)
- Okada Y., Hokari R., Kato S., Mataki N., Okudaira K., Takebayashi K., Matsunaga H., Tsuzuki Y., Komoto S., Watanabe C., Kawaguchi A., Nagao S., Itoh K., Miura S., 1.4-dihydroxy-2-naphthoic acid (DHNA) shows anti-inflammatory effect on NSAID-induced colitis in IL-10-knockout mice through suppression of inflammatory cell infiltration and increased number of Genus Bifidobacterium, Gastroenterology 130 (2006) A313. (In the text)
- Okada Y., Tsuzuki Y., Miyazaki J., Matsuzaki K., Hokari R., Komoto S., Kato S., Kato S., Kawaguchi A., Nagao S., Itoh K., Watanabe T., Miura S., Propionibacterium freudenreichii component 1.4-dihydroxy-2-naphthoic acid (DHNA) attenuates dextran sodium sulphate induced colitis by modulation of bacterial flora and lymphocyte homing, Gut 55 (2006) 681–688. [CrossRef] [PubMed] (In the text)
- Orla-Jensen O., Die hauptlinien des natürlichen bakteriensystems, The main lines of the natural bacterial system, Zentralbl. Bakteriol. 22 (1909) 305–346. (In the text)
- Ouwehand A.C., Lagstrom H., Suomalainen T., Salminen S., Effect of probiotics on constipation, fecal azoreductase activity and fecal mucin content in the elderly, Ann. Nutr. Metab. 46 (2002) 159–162. [CrossRef] [PubMed] (In the text)
- Ouwehand A.C., Salminen S., von Wright A., Ouwehand A., The probiotic potential of propionibacteria, in: Lactic acid bacteria: Microbiology and functional aspects, 3rd edition, revised and expanded, Marcel Dekker Inc., New York, USA, 2004, pp. 159–174. (In the text)
- Ouwehand A.C., Suomalainen T., Tolkko S., Salminen S., In vitro adhesion of propionic acid bacteria to human intestinal mucus, Lait 82 (2002) 123–130. [CrossRef] [EDP Sciences] (In the text)
- Ouwehand A.C., Tolkko S., Kulmala J., Salminen S., Salminen E., Adhesion of inactivated probiotic strains to intestinal mucus, Lett. Appl. Microbiol. 31 (2000) 82–86. [CrossRef] [PubMed] (In the text)
- Perez-Chaia A., Nader de Macias M.E., Oliver G., Propionibacteria in the gut: effect on some metabolic activities of the host, Lait 75 (1995) 435–445. [CrossRef] [EDP Sciences] (In the text)
- Perez-Chaia A., Zarate G., Dairy propionibacteria from milk or cheese diets remain viable and enhance propionic acid production in the mouse cecum, Lait 85 (2005) 85–98. [CrossRef] [EDP Sciences] (In the text)
- Perez-Chaia A., Zarate G., Oliver G., The probiotic properties of propionibacteria, Lait 79 (1999) 175–185. [CrossRef] [EDP Sciences] (In the text)
- Pohjavuori E., Viljanen M., Korpela R., Kuitunen M., Tiittanen M., Vaarala O., Savilahti E., Lactobacillus GG effect in increasing IFN-gamma production in infants with cow’s milk allergy, J. Allergy Clin. Immunol. 114 (2004) 131–136. [CrossRef] [PubMed] (In the text)
- Rainio A., Vahvaselka M., Suomalainen T., Laakso S., Reduction of linoleic acid inhibition in production of conjugated linoleic acid by Propionibacterium freudenreichii ssp. shermanii, Can. J. Microbiol. 47 (2001) 735–740. [CrossRef] [PubMed] (In the text)
- Rainio A., Vahvaselka M., Suomalainen T., Laakso S., Production of conjugated linoleic acid by Propionibacterium freudenreichii ssp. shermanii , Lait 82 (2002) 91–101. [CrossRef] [EDP Sciences] (In the text)
- Ramanathan S., Furusawa E., Read G., Cutting W., Isolation and activity of propionin A an antiviral polypeptide from propionibacteria, Chemotherapy 10 (1965) 197–198. [CrossRef] [PubMed] (In the text)
- Ramanathan S., Furusawa E., Yee H., Cutting W.C., Propionin B an anti viralprinciple of propionibacteria, Chemotherapy 19 (1973) 16–21. [CrossRef] [PubMed]
- Ramanathan S., Olynec C., Cutting W., Antiviral principles of Propionibacteria-isolation, activity of Propionins B, C, Proc. Soc. Exp. Biol. Med. 129 (1968) 73–77. [PubMed]
- Ramanathan S., Read G., Cutting W., Purification of propionin, an antiviral agent from propionibacteria, Proc. Soc. Exp. Biol. Med. 123 (1966) 271–273. [PubMed] (In the text)
- Roland N., Bouglé D., Lebeurrier F., Arhan P., Maubois J.-L., Propionibacterium freudenreichii stimulates the growth of Bifidobacterium bifidum in vitro and increases fecal bifidobacteria in healthy human volunteers, Int. Dairy J. 8 (1998) 587–588. (In the text)
- Ruijschop R.M.A.J., Boelrijk A.E.M., Giffel M.C.T., Satiety effects of a dairy beverage fermented with propionic acid bacteria, Int. Dairy J. 18 (2008) 945–950. [CrossRef] (In the text)
- Sanders M.E., Probiotics: definition, sources, selection, and uses, Clin. Infect. Dis. 46 (2008) S58–S61. [CrossRef] [PubMed] (In the text)
- Sarkar S., Misra A.K., Effect of feeding Propiono-Acido-Bifido (PAB) milk on the nutritional status and excretory pattern in rats and infants, Milchwissenschaft 53 (1998) 666–668. (In the text)
- Sarkar S., Misra A.K., Effect of feeding dietetic yoghurt on the nutritional status and excretory pattern in rats and infants, Egypt. J. Dairy Sci. 30 (2002) 63–73. (In the text)
- Satomi K., Kurihara H., Isawa K., Mori H., Kaneko T., Effects of culture-powder of Propionibacterium freudenreichii ET-3 on fecal microflora of normal adults, Biosci. Microflora 18 (1999) 27–30. (In the text)
- Seki K., Nakao H., Umino H., Isshiki H., Yoda N., Tachihara R., Ohuchi T., Saruta H., Suzuki K., Mitsuoka T., Effects of fermented milk whey containing novel bifidogenic growth stimulator produced by Propionibacterium on fecal bacteria, putrefactive metabolite, defecation frequency and fecal properties in senile volunteers needed serious nursing-care taking enteral nutrition by tube feeding, J. Intest. Microbiol. 18 (2004) 107–115. (In the text)
- Shimotoyodome A., Meguro S., Hase T., Tokimitsu I., Sakata T., Short chain fatty acids but not lactate or succinate stimulate mucus release in the rat colon, Comp. Biochem. Physiol., Part A Mol. Integr. Physiol. 125 (2000) 525–531. [CrossRef] [PubMed] (In the text)
- Sidorchuk I.I., Bondarenko V.M., Selection of a biologically active mutant of Propionibacterium shermanii and the possibility of its use in complex therapy of enteral dysbacteriosis, J. Hyg. Epidemiol. Microbiol. Immunol. (Prague) 28 (1984) 331–338. (In the text)
- Somkuti G.A., Johnson T.L., Cholesterol uptake by Propionibacterium freudenreichii, Curr. Microbiol. 20 (1990) 305–309. [CrossRef] (In the text)
- Stackebrandt E., Schumann P., Schaal K.P., Weiss N., Propionimicrobium gen. nov., a new genus to accommodate Propionibacterium lymphophilum (Torrey 1916) Johnson and Cummins 1972, 1057(AL) as Propionimicrobium lymphophilum comb. nov., Int. J. Syst. Evol. Microbiol. 52 (2002) 1925–1927. [CrossRef] [PubMed] (In the text)
- Suomalainen T., Sigvart-Mattila P., Matto J., Tynkkynen S., In vitro and in vivo gastrointestinal survival, antibiotic susceptibility and genetic identification of Propionibacterium freudenreichii ssp. shermanii JS, Int. Dairy J. 18 (2008) 271–278. [CrossRef] (In the text)
- Suzuki A., Mitsuyama K., Koga H., Tomiyasu N., Masuda J., Takaki K., Tsuruta O., Toyonaga A., Sata M., Bifidogenic growth stimulator for the treatment of active ulcerative colitis: a pilot study, Nutrition 22 (2006) 76–81. [CrossRef] [PubMed] (In the text)
- Thiel A., Eikmanns B., Salminen S., Ouwehand A.C., In vitro adhesion of propionibacteria to human intestinal mucus, Ital. J. Food Sci. 16 (2004) 245–253. (In the text)
- Thierry A., Maillard M.B., Hervé C., Richoux R., Lortal S., Varied volatile compounds are produced by Propionibacterium freudenreichii in Emmental cheese, Food Chem. 87 (2004) 439–446. [CrossRef] (In the text)
- Thierry A., Maillard M.B., Yvon M., Conversion of L-leucine to isovaleric acid by Propionibacterium freudenreichii TL 34 and ITGP23, Appl. Environ. Microbiol. 68 (2002) 608–615. [CrossRef] [PubMed]
- Thierry A., Richoux R., Kerjean J.R., Isovaleric acid is mainly produced by Propionibacterium freudenreichii in Swiss cheese, Int. Dairy J. 14 (2004) 801–807. [CrossRef] (In the text)
- Trinidad T.P., Wolever T.M.S., Thompson L.U., Effects of calcium concentration, acetate, and propionate on calcium absorption in the human distal colon, Nutrition 15 (1999) 529–533. [CrossRef] [PubMed] (In the text)
- Tuomola E.M., Ouwehand A.C., Salminen S.J., Human ileostomy glycoproteins as a model for small intestinal mucus to investigate adhesion of probiotics, Lett. Appl. Microbiol. 28 (1999) 159–163. [CrossRef] [PubMed] (In the text)
- Uchida M., Mogami O., Milk whey culture with Propionibacterium freudenreichii ET-3 is effective on the colitis induced by 2, 4, 6-trinitrobenzene sulfonic acid in rats, J. Pharmacol. Sci. 99 (2005) 329–334. [CrossRef] [PubMed] (In the text)
- Vahvaselka M., Laakso S., Production of cis-9,trans-11-conjugated linoleic acid in camelina meal and okara by an oat-assisted microbial process, J. Agric. Food Chem. 58 (2010) 2479–2482. [CrossRef] [PubMed] (In the text)
- Vesterlund S., Karp M., Salminen S., Ouwehand A.C., Staphylococcus aureus adheres to human intestinal mucus but can be displaced by certain lactic acid bacteria, Microbiology 152 (2006) 1819–1826. [CrossRef] [PubMed] (In the text)
- Viljanen M., Kuitunen M., Haahtela T., Juntunen-Backman K., Korpela R., Savilahti E., Probiotic effects on faecal inflammatory markers and on faecal IgA in food allergic atopic eczema/dermatitis syndrome infants, Pediatr. Allergy Immunol. 16 (2005) 65–71. [CrossRef] [PubMed] (In the text)
- Viljanen M., Pohjavuori E., Haahtela T., Korpela R., Kuitunen M., Sarnesto A., Vaarala O., Savilahti E., Induction of inflammation as a possible mechanism of probiotic effect in atopic eczema-dermatitis syndrome, J. Allergy Clin. Immunol. 115 (2005) 1254–1259. [CrossRef] [PubMed] (In the text)
- Vorobjeva L.I., Iljasova O.V., Khodjaev E.Y., Ponomareva G.M., Varioukhina S.Y., Inhibition of induced mutagenesis in Salmonella typhimurium by the protein of Propionibacterium freudenreichii subsp. shermanii, Anaerobe 7 (2001) 37–44. [CrossRef] (In the text)
- Vorobjeva L.I., Khodjaev E.Y., Cherdinceva T.A., Antimutagenic and reactivative activities of dairy propionibacteria, Lait 75 (1995) 473–487. [CrossRef] [EDP Sciences] (In the text)
- Vorobjeva L.I., Khodjaev E.Y., Vorobjeva N.V., Propionic acid bacteria as probiotics, Microb. Ecol. Health Dis. 20 (2008) 109–112. [CrossRef] (In the text)
- Vorobjeva L., Leverrier P., Zinchenko A., Boyaval P., Khodjaev E., Varioukhina S., Ponomareva G., Gordeeva E., Jan G., Anti-stress activity of Propionibacterium freudenreichii: identification of a reactivative protein, Antonie van Leeuwenhoek. Int. J. Gen. Mol. Microbiol. 85 (2004) 53–62. [CrossRef] (In the text)
- Wahle K.W.J., Heys S.D., Rotondo D., Conjugated linoleic acids: Are they beneficial or detrimental to health?, Prog. Lipid Res. 43 (2004) 553–587. [CrossRef] [PubMed] (In the text)
- Wang L.M., Lv J.P., Chu Z.Q., Cui Y.Y., Ren X.H., Production of conjugated linoleic acid by Propionibacterium freudenreichii, Food Chem. 103 (2007) 313–318. [CrossRef] (In the text)
- Warminska-Radyko I., Laniewska-Moroz L., Babuchowski A., Possibilities for stimulation of Bifidobacterium growth by propionibacteria, Lait 82 (2002) 113–121. [CrossRef] [EDP Sciences] (In the text)
- Wood H.G., Eastbrook R.W., Srera P., Metabolic cycles in the fermentation of propionic acid bacteria, in: Current topics in cellular regulation, Academic press, New York, USA, 1981, pp. 255–287. [PubMed] (In the text)
- Yamazaki S., Kano K., Ikeda T., Isawa K., Kaneko T., Mechanistic study on the roles of a bifidogenetic growth stimulator based on physicochemical characterization, BBA-Gen. Subjects 1425 (1998) 516–526. [CrossRef] (In the text)
- Yamazaki S., Kano K., Ikeda T., Isawa K., Kaneko T., Role of 2-amino-3-carboxy-1, 4-naphthoquinone, a strong growth stimulator for bifidobacteria, as an electron transfer mediator for NAD(P)(+) regeneration in Bifidobacterium longum, BBA-Gen. Subjects 1428 (1999) 241–250. [CrossRef] (In the text)
- Yokota A., Tamura T., Takeuchi M., Weiss N., Stackebrandt E., Transfer of Propionibacterium innocuum Pitcher and Collins 1991 to Propioniferax gen. nov., as Propioniferax innocua comb. nov., Int. J. Syst. Bacteriol. 44 (1994) 579–582. [CrossRef] [PubMed] (In the text)
- Zarate G., Chaia A.P., Gonzalez S., Oliver G., Viability and beta-galactosidase activity of dairy propionibacteria subjected to digestion by artificial gastric and intestinal fluids, J. Food Prot. 63 (2000) 1214–1221. [PubMed] (In the text)
- Zarate G., Chaia A.P., Oliver G., Some characteristics of practical relevance of the beta-galactosidase from potential probiotic strains of Propionibacterium acidipropionici, Anaerobe 8 (2002) 259–267. [CrossRef] (In the text)
- Zarate G., De Ambrosini V.I.M., Chaia A.P., Gonzalez S.N., Adhesion of dairy propionibacteria to intestinal epithelial tissue in vitro and in vivo, J. Food Prot. 65 (2002) 534–539. [PubMed] (In the text)
- Zarate G., Perez Chaia A., Dairy bacteria remove in vitro dietary lectins with toxic effects on colonic cells, J. Appl. Microbiol. 106 (2009) 1050–1057. [CrossRef] [PubMed] (In the text)