, Volume 58, Issue 2, pp 207–227 | Cite as

Probiotic strains and mechanistic insights for the treatment of type 2 diabetes




The intestinal microbial composition appears to differ between healthy controls and individuals with Type 2 diabetes (T2D). This observation has led to the hypothesis that perturbations of the intestinal microbiota may contribute to the development of T2D. Manipulations of the intestinal microbiota may therefore provide a novel approach in the prevention and treatment of T2D. Indeed, fecal transplants have shown promising results in both animal models for obesity and T2D and in human clinical trials. To avoid possible complications associated with fecal transplants, probiotics are considered as a viable alternative therapy. An important, however often underappreciated, characteristic of probiotics is that individual strains may have different, even opposing, effects on the host. This strain specificity exists also within the same species. A comprehensive understanding of the underlying mechanisms at the strain level is therefore crucial for the selection of suitable probiotic strains.


The aim of this review is to discuss the mechanisms employed by specific probiotic strains of the Lactobacillus and the Bifidobacterium genuses, which showed efficacy in the treatment of obesity and T2D. Some probiotic strains employ recurring beneficial effects, including the production of anti-microbial lactic acid, while other strains display highly unique features, such as hydrolysis of tannins.


A major obstacle in the evaluation of probiotic strains lays in the great number of strains, differences in detection methodology and measured outcome parameters. The understanding of further research should be directed towards the development of standardized evaluation methods to facilitate the comparison of different studies.


Intestinal microbiota Probiotics Type 2 diabetes Obesity Strain-specificity 



angiopoietin-like protein


alanine amino transferase


aspartate aminotransferase


blood glucose at 120 min


bile salt hydrolase


body mass index


body weight




colony forming unit


C-type lectin receptor


c-reactive protein


cytosine-guanine dinucleotides


dendritic cell


dendritic cell specific intracellular adhesion molecule-3-grabbing non-integrin


diet-induced obesity


epithelial growth factor


epididymal fat


diet-induced obesity


Fasting blood glucose


fat mass


gamma-glutamyl transferase


gastrointestinal tract




hemoglobin A1c


high-fat diet


high-fructose diet


irritable bowl syndrome


intestinal endothelial cell






insulin resistance


Janus kinase 2


insulin resistance


lactic acid bacteria


liposaccharide-binding protein precursor


low density lipoprotein




lipteichoic acid


toll-like receptor


microorganism-associated molecular patterns




Metabolic Syndrome


non-alcoholic fatty liver disease


non-alcoholic steatohepatitis


not determined


natural killer cell


nucleotide-binding oligomerization domain-containing protein (NOD)-like receptors


not significant


oral glucose tolerance test


cyclin-dependent kinase inhibitor


plasminogen activator inhibitor-1


peroxisome proliferator-activated receptor-γ


pattern recognition receptors


reactive oxygen species


signal transducer and activator of transcription-1


short-chain fatty acids


surface layer protein


smooth muscle actin


superoxide dismutase




Type 2 diabetes


total cholesterol




tumor necrosis factor


zonula occludens-1


Compliance with ethical standards

Conflict of interest

The authors declare that they have no competing interests.


  1. 1.
    D.J. Pettitt, J. Talton, D. Dabelea et al., Prevalence of diabetes in U.S. youth in 2009: the SEARCH for diabetes in youth study. Diabetes. Care. 37, 402–408 (2014)PubMedPubMedCentralCrossRefGoogle Scholar
  2. 2.
    J.B. Tryggestad, S.M. Willi, Complications and comorbidities of T2DM in adolescents, findings from the TODAY clinical trial. J. Diabetes. Complicat. 29, 307–312 (2015)PubMedCrossRefGoogle Scholar
  3. 3.
    R.S. Weinstock, K.L. Drews, S. Caprio, N.I. Leibel, S.V. McKay, P.S. Zeitler, Metabolic syndrome is common and persistent in youth-onset type 2 diabetes, Results from the TODAY clinical trial. Obesity. 23, 1357–1361 (2015)PubMedPubMedCentralCrossRefGoogle Scholar
  4. 4.
    Z. Aziz, P. Absetz, J. Oldroyd, N.P. Pronk, B. Oldenburg, A systematic review of real-world diabetes prevention programs, learnings from the last 15 years. Implement. Sci. 10, 172 (2015)PubMedPubMedCentralCrossRefGoogle Scholar
  5. 5.
    W.L. Bennett, E.B. Bass, S. Bolen, Correction: Comparative effectiveness and safety of medications for type 2 diabetes. Ann. Intern. Med. 155, 67–68 (2011)PubMedCrossRefGoogle Scholar
  6. 6.
    S.J. Dunmore, J.E. Brown, The role of adipokines in beta-cell failure of type 2 diabetes. J. Endocrinol. 216, T37–T45 (2013)PubMedCrossRefGoogle Scholar
  7. 7.
    S.B. Dula, M. Jecmenica, R. Wu et al., Evidence that low-grade systemic inflammation can induce islet dysfunction as measured by impaired calcium handling. Cell. Calcium. 48, 133–142 (2010)PubMedPubMedCentralCrossRefGoogle Scholar
  8. 8.
    M. Mraz, M. Haluzik, The role of adipose tissue immune cells in obesity and low-grade inflammation. J. Endocrinol. 222, R113–R127 (2014)PubMedCrossRefGoogle Scholar
  9. 9.
    M. Remely, B. Hippe, J. Zanner, E. Aumueller, H. Brath, A.G. Haslberger Gut microbiota of obese, type 2 diabetic individuals is enriched in Faecalibacterium prausnitzii, Akkermansia muciniphila and Peptostreptococcus anaerobius after weight loss. Endocr. Metab. Immune. Disord. Drug. Targets. 16, 99–106 (2016)Google Scholar
  10. 10.
    M. Remely, E. Aumueller, D. Jahn, B. Hippe, H. Brath, A.G. Haslberger, Microbiota and epigenetic regulation of inflammatory mediators in type 2 diabetes and obesity. Benef. Microbes. 5, 33–43 (2014)PubMedCrossRefGoogle Scholar
  11. 11.
    P.D. Cani, J. Amar, M.A. Iglesias et al., Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes. 56, 1761–1772 (2007)PubMedCrossRefGoogle Scholar
  12. 12.
    S. de Kort, D. Keszthelyi, A.A. Masclee, Leaky gut and diabetes mellitus, what is the link? Obes. Rev. 12, 449–458 (2011)PubMedCrossRefGoogle Scholar
  13. 13.
    I.A. Kirpich, L.S. Marsano, C.J. McClain, Gut-liver axis, nutrition, and non-alcoholic fatty liver disease. Clin. Biochem. 48, 923–930 (2015)PubMedPubMedCentralCrossRefGoogle Scholar
  14. 14.
    A.M. Kabat, N. Srinivasan, K.J. Maloy, Modulation of immune development and function by intestinal microbiota. Trends. Immunol. 35, 507–517 (2014)PubMedCrossRefGoogle Scholar
  15. 15.
    S. Ding, P.K. Lund, Role of intestinal inflammation as an early event in obesity and insulin resistance. Curr. Opin. Clin. Nutr. Metab. Care. 14, 328–333 (2011)PubMedPubMedCentralCrossRefGoogle Scholar
  16. 16.
    P.D. Cani, R. Bibiloni, C. Knauf et al., Changes in gut microbiota control metabolic endotoxemia-induced inflammation in high-fat diet-induced obesity and diabetes in mice. Diabetes. 57, 1470–1481 (2008)PubMedCrossRefGoogle Scholar
  17. 17.
    C.B. de La Serre, C.L. Ellis, J. Lee, A.L. Hartman, J.C. Rutledge, H.E. Raybould, Propensity to high-fat diet-induced obesity in rats is associated with changes in the gut microbiota and gut inflammation. Am. J. Physiol. Gastrointest. Liver. Physiol. 299, G440–G448 (2010)CrossRefGoogle Scholar
  18. 18.
    N.N. Mehta, F.C. McGillicuddy, P.D. Anderson et al., Experimental endotoxemia induces adipose inflammation and insulin resistance in humans. Diabetes. 59, 172–181 (2010)PubMedCrossRefGoogle Scholar
  19. 19.
    M.A. Hildebrandt, C. Hoffmann, S.A. Sherrill-Mix et al., High-fat diet determines the composition of the murine gut microbiome independently of obesity. Gastroenterology. 137, 1716–1724, e1711-1712 (2009)PubMedPubMedCentralCrossRefGoogle Scholar
  20. 20.
    L. Geurts, V. Lazarevic, M. Derrien et al., Altered gut microbiota and endocannabinoid system tone in obese and diabetic leptin-resistant mice: impact on apelin regulation in adipose tissue. Front Microbiol. 2, 149 (2011)PubMedPubMedCentralCrossRefGoogle Scholar
  21. 21.
    P.J. Turnbaugh, M. Hamady, T. Yatsunenko et al., A core gut microbiome in obese and lean twins. Nature. 457, 480–484 (2009)PubMedCrossRefGoogle Scholar
  22. 22.
    R.E. Ley, P.J. Turnbaugh, S. Klein, J.I. Gordon, Microbial ecology: human gut microbes associated with obesity. Nature. 444, 1022–1023 (2006)PubMedCrossRefGoogle Scholar
  23. 23.
    X. Wu, C. Ma, L. Han et al., Molecular characterisation of the faecal microbiota in patients with type II diabetes. Curr. Microbiol. 61, 69–78 (2010)PubMedCrossRefGoogle Scholar
  24. 24.
    A. Schwiertz, D. Taras, K. Schafer et al., Microbiota and SCFA in lean and overweight healthy subjects. Obesity. 18, 190–195 (2010)PubMedCrossRefGoogle Scholar
  25. 25.
    F.H. Karlsson, V. Tremaroli, I. Nookaew et al., Gut metagenome in European women with normal, impaired and diabetic glucose control. Nature. 498, 99–103 (2013)PubMedCrossRefGoogle Scholar
  26. 26.
    E. Le Chatelier, T. Nielsen, J. Qin et al., Richness of human gut microbiome correlates with metabolic markers. Nature. 500, 541–546 (2013)PubMedCrossRefGoogle Scholar
  27. 27.
    B. Ruiz-Núñez, D.A. Dijck-Brouwer, F.A. Muskiet, The relation of saturated fatty acids with low-grade inflammation and cardiovascular disease. J. Nutr. Biochem. 36, 1–20 (2016)PubMedCrossRefGoogle Scholar
  28. 28.
    K.P. Karalis, P. Giannogonas, E. Kodela, Y. Koutmani, M. Zoumakis, T. Teli, Mechanisms of obesity and related pathology: linking immune responses to metabolic stress. FEBS. J. 276, 5747–5754 (2009)PubMedCrossRefGoogle Scholar
  29. 29.
    C.R. McGill, V.L. Fulgoni, L. Devareddy, Ten-year trends in fiber and whole grain intakes and food sources for the United States population: National Health and Nutrition Examination Survey 2001-2010. Nutrients. 7, 1119–1130 (2015)PubMedPubMedCentralCrossRefGoogle Scholar
  30. 30.
    S.L. Schnorr, M. Candela, S. Rampelli et al., Gut microbiome of the Hadza hunter-gatherers. Nat Commun. 5, 3654 (2014)PubMedPubMedCentralCrossRefGoogle Scholar
  31. 31.
    J.C. Clemente, E.C. Pehrsson, M.J. Blaser, et al., The microbiome of uncontacted Amerindians. Sci Adv. 1, e1500183 (2015)Google Scholar
  32. 32.
    J. Ou, F. Carbonero, E.G. Zoetendal et al., Diet, microbiota, and microbial metabolites in colon cancer risk in rural Africans and African Americans. Am. J. Clin. Nutr. 98, 111–120 (2013)PubMedPubMedCentralCrossRefGoogle Scholar
  33. 33.
    J.K. Nicholson, E. Holmes, J. Kinross et al., Host-gut microbiota metabolic interactions. Science 336, 1262–1267 (2012)PubMedCrossRefGoogle Scholar
  34. 34.
    D.R. Donohoe, N. Garge, X. Zhang et al., The microbiome and butyrate regulate energy metabolism and autophagy in the mammalian colon. Cell. Metab. 13, 517–526 (2011)PubMedPubMedCentralCrossRefGoogle Scholar
  35. 35.
    G. den Besten, K. van Eunen, A.K. Groen, K. Venema, D.J. Reijngoud, B.M. Bakker, The role of short-chain fatty acids in the interplay between diet, gut microbiota, and host energy metabolism. J. Lipid. Res. 54, 2325–2340 (2013)CrossRefGoogle Scholar
  36. 36.
    D.W. Russell, The enzymes, regulation, and genetics of bile acid synthesis. Annu. Rev. Biochem. 72, 137–174 (2003)PubMedCrossRefGoogle Scholar
  37. 37.
    L. Liu, L. Li, J. Min et al., Butyrate interferes with the differentiation and function of human monocyte-derived dendritic cells. Cell. Immunol. 277, 66–73 (2012)PubMedCrossRefGoogle Scholar
  38. 38.
    A.L. Millard, P.M. Mertes, D. Ittelet, F. Villard, P. Jeannesson, J. Bernard, Butyrate affects differentiation, maturation and function of human monocyte-derived dendritic cells and macrophages. Clin. Exp. Immunol. 130, 245–255 (2002)PubMedPubMedCentralCrossRefGoogle Scholar
  39. 39.
    H. Ohira, Y. Fujioka, C. Katagiri et al., Butyrate attenuates inflammation and lipolysis generated by the interaction of adipocytes and macrophages. J. Atheroscler. Thromb. 20, 425–442 (2013)PubMedCrossRefGoogle Scholar
  40. 40.
    S.H. Al-Lahham, H. Roelofsen, M. Priebe et al., Regulation of adipokine production in human adipose tissue by propionic acid. Eur. J. Clin. Invest. 40, 401–407 (2010)PubMedCrossRefGoogle Scholar
  41. 41.
    P.J. Turnbaugh, F. Backhed, L. Fulton, J.L.Gordon, Diet-induced obesity is linked to marked but reversible alterations in the mouse distal gut microbiome. Cell Host Microbe 17, 213–223 (2008)PubMedPubMedCentralCrossRefGoogle Scholar
  42. 42.
    T.J. Borody, S. Paramsothy, G. Agrawal, Fecal microbiota transplantation: indications, methods, evidence, and future directions. Curr. Gastroenterol. Rep. 15, 337 (2013)PubMedPubMedCentralCrossRefGoogle Scholar
  43. 43.
    A. Vrieze, E. Van Nood, F. Holleman et al., Transfer of intestinal microbiota from lean donors increases insulin sensitivity in individuals with metabolic syndrome. Gastroenterology. 143, 913–916, e917 (2012)PubMedCrossRefGoogle Scholar
  44. 44.
    M.B. Smith, C. Kelly, E.J. Alm, Policy: How to regulate faecal transplants. Nature. 506, 290–291 (2014)PubMedCrossRefGoogle Scholar
  45. 45.
    A. Kazerouni, J. Burgess, L.J. Burns, L.M. Wein, Optimal screening and donor management in a public stool bank. Microbiome. 3, 75 (2015)PubMedPubMedCentralCrossRefGoogle Scholar
  46. 46.
    J. Alard, V. Lehrter, M. Rhimi et al., Beneficial metabolic effects of selected probiotics on diet-induced obesity and insulin resistance in mice are associated with improvement of dysbiotic gut microbiota. Environ. Microbiol. 18, 1484–1497 (2015)CrossRefGoogle Scholar
  47. 47.
    J. Wang, H. Tang, C. Zhang et al., Modulation of gut microbiota during probiotic-mediated attenuation of metabolic syndrome in high fat diet-fed mice. ISME. J. 9, 1–15 (2015)PubMedCrossRefGoogle Scholar
  48. 48.
    C. Ferrario, V. Taverniti, C. Milani et al., Modulation of fecal Clostridiales bacteria and butyrate by probiotic intervention with Lactobacillus paracasei DG varies among healthy adults. J. Nutr. 144, 1787–1796 (2014)PubMedCrossRefGoogle Scholar
  49. 49.
    H. Zhang, H. Wang, M. Shepherd et al., Probiotics and virulent human rotavirus modulate the transplanted human gut microbiota in gnotobiotic pigs. Gut Pathog. 6, 39 (2014)PubMedPubMedCentralCrossRefGoogle Scholar
  50. 50.
    A.D. Kostic, D. Gevers, C.S. Pedamallu et al., Genomic analysis identifies association of Fusobacterium with colorectal carcinoma. Genome. Res. 22, 292–298 (2012)PubMedPubMedCentralCrossRefGoogle Scholar
  51. 51.
    J.C. Arthur, R.Z. Gharaibeh, J.M. Uronis et al., VSL#3 probiotic modifies mucosal microbial composition but does not reduce colitis-associated colorectal cancer. Sci. Rep. 3, 2868 (2013)PubMedPubMedCentralCrossRefGoogle Scholar
  52. 52.
    S.R. Yoo, Y.J. Kim, D.Y. Park et al., Probiotics L. plantarum and L. curvatus in combination alter hepatic lipid metabolism and suppress diet-inducedobesity. Obesity. 21, 2571–2578 (2013)PubMedCrossRefGoogle Scholar
  53. 53.
    L.K. Stenman, A. Waget, C. Garret, P. Klopp, R. Burcelin, S. Lahtinen, Potential probiotic Bifidobacterium animalis ssp. lactis 420 prevents weight gain and glucose intolerance in diet-induced obese mice. Benef. Microbes. 5, 437–445 (2014)PubMedCrossRefGoogle Scholar
  54. 54.
    A. Everard, C. Belzer, L. Geurts et al., Cross-talk between Akkermansia muciniphila and intestinal epithelium controls diet-induced obesity. Proc. Natl. Acad. Sci. U S A. 110, 9066–9071 (2013)PubMedPubMedCentralCrossRefGoogle Scholar
  55. 55.
    J. Sun, N.J. Buys, Glucose- and glycaemic factor-lowering effects of probiotics on diabetes: a meta-analysis of randomised placebo-controlled trials. Br. J. Nutr. 115, 1167–1177 (2016)PubMedCrossRefGoogle Scholar
  56. 56.
    C. Moroti, L.F. Souza Magri, M. de Rezende Costa, D.C. Cavallini, K. Sivieri, Effect of the consumption of a new symbiotic shake on glycemia and cholesterol levels in elderly people with type 2 diabetes mellitus. Lipids. Health. Dis. 11, 29 (2012)PubMedPubMedCentralCrossRefGoogle Scholar
  57. 57.
    A. Bayat, F. Azizi-Soleiman, M. Heidari-Beni et al., Effect of Cucurbita ficifolia and probiotic yogurt consumption on blood glucose, lipid profile, and inflammatory marker in Type 2 diabetes. Int. J. Prev. Med. 7, 30 (2016)PubMedPubMedCentralCrossRefGoogle Scholar
  58. 58.
    Z. Asemi, A. Khorrami-Rad, S.A. Alizadeh, H. Shakeri, A. Esmaillzadeh, Effects of synbiotic food consumption on metabolic status of diabetic patients: a double-blind randomized cross-over controlled clinical trial. Clin. Nutr. 33, 198–203 (2014)PubMedCrossRefGoogle Scholar
  59. 59.
    H. Yadav, S. Jain, P.R. Sinha, Oral administration of dahi containing probiotic Lactobacillus acidophilus and Lactobacillus casei delayed the progression of streptozotocin-induced diabetes in rats. J. Dairy. Res. 75, 189–195 (2008)PubMedCrossRefGoogle Scholar
  60. 60.
    N. Dolatkhah, M. Hajifaraji, F. Abbasalizadeh, N. Aghamohammadzadeh, Y. Mehrabi, M.M. Abbasi, Is there a value for probiotic supplements in gestational diabetes mellitus? A randomized clinical trial. J. Health. Popul. Nutr. 33, 25 (2015)PubMedPubMedCentralCrossRefGoogle Scholar
  61. 61.
    P. Morteau Evidence of probiotic strain specificity makes extrapolation of results impossible from a strain to another, even from the same species. AGH. 1, 1–3 (2011)Google Scholar
  62. 62.
    P. Ducrotte, P. Sawant, V. Jayanthi, Clinical trial: Lactobacillus plantarum 299v (DSM 9843) improves symptoms of irritable bowel syndrome. World. J. Gastroenterol. 18, 4012–4018 (2012)PubMedPubMedCentralCrossRefGoogle Scholar
  63. 63.
    K. Niedzielin, H. Kordecki, B. Birkenfeld, A controlled, double-blind, randomized study on the efficacy of Lactobacillus plantarum 299V in patients with irritable bowel syndrome. Eur. J. Gastroenterol. Hepatol. 13, 1143–1147 (2001)PubMedCrossRefGoogle Scholar
  64. 64.
    S.C. Ligaarden, L. Axelsson, K. Naterstad, S. Lydersen, P.G. Farup, A candidate probiotic with unfavourable effects in subjects with irritable bowel syndrome: a randomised controlled trial. BMC. Gastroenterol. 10, 16 (2010)PubMedPubMedCentralCrossRefGoogle Scholar
  65. 65.
    K. Yoshimura, T. Matsui, K. Itoh, Prevention of Escherichia coli O157:H7 infection in gnotobiotic mice associated with Bifidobacterium strains. Antonie. Van. Leeuwenhoek. 97, 107–117 (2010)PubMedCrossRefGoogle Scholar
  66. 66.
    Y.N. Yin, Q.F. Yu, N. Fu, X.W. Liu, F.G. Lu, Effects of four Bifidobacteria on obesity in high-fat diet induced rats. World. J. Gastroenterol. 16, 3394–3401 (2010)PubMedPubMedCentralCrossRefGoogle Scholar
  67. 67.
    M.C. Dao, A. Everard, J. Aron-Wisnewsky et al., Akkermansia muciniphila and improved metabolic health during a dietary intervention in obesity: relationship with gut microbiome richness and ecology. Gut. 65, 426–436 (2016)PubMedCrossRefGoogle Scholar
  68. 68.
    M. Remely, B. Hippe, I. Geretschlaeger, S. Stegmayer, I. Hoefinger, A. Haslberger, Increased gut microbiota diversity and abundance of Faecalibacterium prausnitzii and Akkermansia after fasting: a pilot study. Wien. Klin. Wochenschr. 127, 394–398 (2015)PubMedPubMedCentralCrossRefGoogle Scholar
  69. 69.
    S. Zhao, W. Liu, J. Wang et al., Akkermansia muciniphila improves metabolic profiles by reducing inflammation in chow diet-fed mice. J. Mol. Endocrinol. 58, 1–14 (2017)PubMedCrossRefGoogle Scholar
  70. 70.
    H. Plovier, A. Everard, C. Druart et al., A purified membrane protein from Akkermansia muciniphila or the pasteurized bacterium improves metabolism in obese and diabetic mice. Nat. Med. 23, 107–113 (2017)PubMedCrossRefGoogle Scholar
  71. 71.
    R.C. Inglin, M.J. Stevens, L. Meile, C. Lacroix, High-throughput screening assays for antibacterial and antifungal activities of Lactobacillus species. J. Microbiol. Methods. 114, 26–29 (2015)PubMedCrossRefGoogle Scholar
  72. 72.
    R.J. Siezen, V.A. Tzeneva, A. Castioni et al., Phenotypic and genomic diversity of Lactobacillus plantarum strains isolated from various environmental niches. Environ. Microbiol. 12, 758–773 (2010)PubMedCrossRefGoogle Scholar
  73. 73.
    O. Pepe, G. Blaiotta, M. Anastasio, G. Moschetti, D. Ercolini, F. Villani, Technological and molecular diversity of Lactobacillus plantarum strains isolated from naturally fermented sourdoughs. Syst. Appl. Microbiol. 27, 443–453 (2004)PubMedCrossRefGoogle Scholar
  74. 74.
    R.J. Siezen, J.E. van Hylckama Vlieg, Genomic diversity and versatility of Lactobacillus plantarum, a natural metabolic engineer. Microb. Cell. Fact. 10(Suppl 1), S3 (2011)PubMedPubMedCentralCrossRefGoogle Scholar
  75. 75.
    U. Andersson, C. Branning, S. Ahrne et al., Probiotics lower plasma glucose in the high-fat fed C57BL/6J mouse. Benef Microbes. 1, 189–196 (2010)PubMedCrossRefGoogle Scholar
  76. 76.
    C.C. Wu, W.L. Weng, W.L. Lai et al., Effect of Lactobacillus plantarum Strain K21 on High-Fat Diet-Fed Obese Mice. Evid. Based. Complement. Alternat. Med. 2015, 391767 (2015)PubMedPubMedCentralGoogle Scholar
  77. 77.
    J. Karczewski, F.J. Troost, I. Konings et al., Regulation of human epithelial tight junction proteins by Lactobacillus plantarum in vivo and protective effects on the epithelial barrier. Am. J. Physiol. Gastrointest. Liver. Physiol. 298, G851–G859 (2010)PubMedCrossRefGoogle Scholar
  78. 78.
    W. Bejar, K. Hamden, R. Ben Salah, H. Chouayekh, Lactobacillus plantarum TN627 significantly reduces complications of alloxan-induced diabetes in rats. Anaerobe. 24, 4–11 (2013)PubMedCrossRefGoogle Scholar
  79. 79.
    H.Y. Huang, M. Korivi, C.H. Tsai, J.H. Yang, Y.C. Tsai, Supplementation of Lactobacillus plantarum K68 and Fruit-Vegetable Ferment along with High Fat-Fructose Diet Attenuates Metabolic Syndrome in Rats with Insulin Resistance. Evid. Based. Complement. Alternat. Med. 2013, 943020 (2013)PubMedPubMedCentralGoogle Scholar
  80. 80.
    K. Lee, K. Paek, H.Y. Lee, J.H. Park, Y. Lee, Antiobesity effect of trans-10,cis-12-conjugated linoleic acid-producing Lactobacillus plantarum PL62 on diet-induced obese mice. J. Appl. Microbiol. 103, 1140–1146 (2007)PubMedCrossRefGoogle Scholar
  81. 81.
    T.D. Nguyen, J.H. Kang, M.S. Lee, Characterization of Lactobacillus plantarum PH04, a potential probiotic bacterium with cholesterol-lowering effects. Int. J. Food. Microbiol. 113, 358–361 (2007)PubMedCrossRefGoogle Scholar
  82. 82.
    C. Li, S.P. Nie, K.X. Zhu, Q. Ding, T. Xiong, M.Y. Xie, Lactobacillus plantarum NCU116 improves liver function, oxidative stress and lipid metabolism in rats with high fat diet induced non-alcoholic fatty liver disease. Food Funct. 5, 3216–3223 (2014)PubMedCrossRefGoogle Scholar
  83. 83.
    C. Li, Q. Ding, S.P. Nie, Y.S. Zhang, T. Xiong, M.Y. Xie, Carrot juice fermented with Lactobacillus plantarum NCU116 ameliorates type 2 diabetes in rats. J. Agric. Food. Chem. 62, 11884–11891 (2014)PubMedCrossRefGoogle Scholar
  84. 84.
    X. Li, N. Wang, B. Yin et al., Effects of Lactobacillus plantarum CCFM0236 on hyperglycaemia and insulin resistance in high-fat and streptozotocin-induced type 2 diabetic mice. J. Appl. Microbiol. 121, 1727–1736 (2016)PubMedCrossRefGoogle Scholar
  85. 85.
    M. Hariri, R. Salehi, A. Feizi, M. Mirlohi, R. Ghiasvand, N. Habibi, A randomized, double-blind, placebo-controlled, clinical trial on probiotic soy milk and soy milk: effects on epigenetics and oxidative stress in patients with type II diabetes. Genes Nutr. 10, 52 (2015)PubMedPubMedCentralCrossRefGoogle Scholar
  86. 86.
    A.R. Desai, N.P. Shah, I.B. Powell, Discrimination of dairy industry isolates of the Lactobacillus casei group. J. Dairy. Sci. 89, 3345–3351 (2006)PubMedCrossRefGoogle Scholar
  87. 87.
    S. Coudeyras, H. Marchandin, C. Fajon, C. Forestier, Taxonomic and strain-specific identification of the probiotic strain Lactobacillus rhamnosus 35 within the Lactobacillus casei group. Appl. Environ. Microbiol. 74, 2679–2689 (2008)PubMedPubMedCentralCrossRefGoogle Scholar
  88. 88.
    H. Toh, K. Oshima, A. Nakano et al., Genomic adaptation of the Lactobacillus casei group. PLoS. ONE. 8, e75073 (2013)PubMedPubMedCentralCrossRefGoogle Scholar
  89. 89.
    Y. Ritze, G. Bardos, A. Claus et al., Lactobacillus rhamnosus GG protects against non-alcoholic fatty liver disease in mice. PLoS. ONE. 9, e80169 (2014)PubMedPubMedCentralCrossRefGoogle Scholar
  90. 90.
    K. Honda, M. Moto, N. Uchida, F. He, N. Hashizume, Anti-diabetic effects of lactic acid bacteria in normal and type 2 diabetic mice. J. Clin. Biochem. Nutr. 51, 96–101 (2012)PubMedPubMedCentralCrossRefGoogle Scholar
  91. 91.
    M. Tabuchi, M. Ozaki, A. Tamura et al., Antidiabetic effect of Lactobacillus GG in streptozotocin-induced diabetic rats. Biosci. Biotechnol. Biochem. 67, 1421–1424 (2003)PubMedCrossRefGoogle Scholar
  92. 92.
    P. Vajro, C. Mandato, M.R. Licenziati et al., Effects of Lactobacillus rhamnosus strain GG in pediatric obesity-related liver disease. J. Pediatr. Gastroenterol. Nutr. 52, 740–743 (2011)PubMedCrossRefGoogle Scholar
  93. 93.
    J. Plaza-Diaz, C. Gomez-Llorente, F. Abadia-Molina et al., Effects of Lactobacillus paracasei CNCM I-4034, Bifidobacterium breve CNCM I-4035 and Lactobacillus rhamnosus CNCM I-4036 on hepatic steatosis in Zucker rats. PLoS. ONE. 9, e98401 (2014)PubMedPubMedCentralCrossRefGoogle Scholar
  94. 94.
    J.A. Marazza, J.G. LeBlanc, G.S. de Giori, M.S. Garro, Soymilk fermented with Lactobacillus rhamnosus CRL981 ameliorates hyperglycemia, lipid profiles and increases antioxidant enzyme activities in diabetic mice. J Funct Food. 5, 1848–1853 (2013)CrossRefGoogle Scholar
  95. 95.
    H.Y. Lee, J.H. Park, S.H. Seok et al., Human originated bacteria, Lactobacillus rhamnosus PL60, produce conjugated linoleic acid and show anti-obesity effects in diet-induced obese mice. Biochim. Biophys. Acta. 736-744, 2006 (1761)Google Scholar
  96. 96.
    M. Sanchez, C. Darimont, V. Drapeau et al., Effect of Lactobacillus rhamnosus CGMCC1.3724 supplementation on weight loss and maintenance in obese men and women. Br. J. Nutr. 111, 1507–1519 (2014)PubMedCrossRefGoogle Scholar
  97. 97.
    P. Chen, Q. Zhang, H. Dang et al., Antidiabetic effect of Lactobacillus casei CCFM0412 on mice with type 2 diabetes induced by a high-fat diet and streptozotocin. Nutrition. 30, 1061–1068 (2014)PubMedCrossRefGoogle Scholar
  98. 98.
    M. Tanida, K. Imanishi, H. Akashi et al., Injection of Lactobacillus casei strain Shirota affects autonomic nerve activities in a tissue-specific manner, and regulates glucose and lipid metabolism in rats. J. Diabetes Investig. 5, 153–161 (2014)PubMedCrossRefGoogle Scholar
  99. 99.
    G. Karimi, M.R. Sabran, R. Jamaluddin et al., The anti-obesity effects of Lactobacillus casei strain Shirota versus Orlistat on high fat diet-induced obese rats. Food Nutr. Res. 59, 29273 (2015)PubMedCrossRefGoogle Scholar
  100. 100.
    I.N. Nunez, C.M. Galdeano, M. de LeBlanc Ade, G. Perdigon, Evaluation of immune response, microbiota, and blood markers after probiotic bacteria administration in obese mice induced by a high-fat diet. Nutrition. 30, 1423–1432 (2014)PubMedCrossRefGoogle Scholar
  101. 101.
    C.J. Hulston, A.A. Churnside, M.C. Venables, Probiotic supplementation prevents high-fat, overfeeding-induced insulin resistance in human subjects. Br. J. Nutr. 113, 596–602 (2015)PubMedPubMedCentralCrossRefGoogle Scholar
  102. 102.
    P. Tian, B. Li, C. He et al., Antidiabetic (type 2) effects of Lactobacillus G15 and Q14 in rats through regulation of intestinal permeability and microbiota. Food Funct. 7, 3789–3797 (2016)PubMedCrossRefGoogle Scholar
  103. 103.
    C.H. Chiu, T.Y. Lu, Y.Y. Tseng, T.M. Pan, The effects of Lactobacillus-fermented milk on lipid metabolism in hamsters fed on high-cholesterol diet. Appl. Microbiol. Biotechnol. 71, 238–245 (2006)PubMedCrossRefGoogle Scholar
  104. 104.
    M.C. Cheng, T.Y. Tsai, T.M. Pan, Anti-obesity activity of the water extract of Lactobacillus paracasei subsp. paracasei NTU 101 fermented soy milk products. Food Funct. 6, 3522–3530 (2015)PubMedCrossRefGoogle Scholar
  105. 105.
    J.H. Kang, S.I. Yun, M.H. Park, J.H. Park, S.Y. Jeong, H.O. Park, Anti-obesity effect of Lactobacillus gasseri BNR17 in high-sucrose diet-induced obese mice. PLoS. ONE. 8, e54617 (2013)PubMedPubMedCentralCrossRefGoogle Scholar
  106. 106.
    M. Miyoshi, A. Ogawa, S. Higurashi, Y. Kadooka, Anti-obesity effect of Lactobacillus gasseri SBT2055 accompanied by inhibition of pro-inflammatory gene expression in the visceral adipose tissue in diet-induced obese mice. Eur. J. Nutr. 53, 599–606 (2014)PubMedCrossRefGoogle Scholar
  107. 107.
    S.I. Yun, H.O. Park, J.H. Kang, Effect of Lactobacillus gasseri BNR17 on blood glucose levels and body weight in a mouse model of type 2 diabetes. J. Appl. Microbiol. 107, 1681–1686 (2009)PubMedCrossRefGoogle Scholar
  108. 108.
    Y. Kadooka, M. Sato, K. Imaizumi et al., Regulation of abdominal adiposity by probiotics (Lactobacillus gasseri SBT2055) in adults with obese tendencies in a randomized controlled trial. Eur. J. Clin. Nutr. 64, 636–643 (2010)PubMedCrossRefGoogle Scholar
  109. 109.
    A. Ogawa, T. Kobayashi, F. Sakai, Y. Kadooka, Y. Kawasaki, Lactobacillus gasseri SBT2055 suppresses fatty acid release through enlargement of fat emulsion size in vitro and promotes fecal fat excretion in healthy Japanese subjects. Lipids. Health. Dis. 14, 20 (2015)PubMedPubMedCentralCrossRefGoogle Scholar
  110. 110.
    P.L. Oh, A.K. Benson, D.A. Peterson et al., Diversification of the gut symbiont Lactobacillus reuteri as a result of host-driven evolution. ISME. J. 4, 377–387 (2010)PubMedCrossRefGoogle Scholar
  111. 111.
    S.A. Frese, A.K. Benson, G.W. Tannock et al., The evolution of host specialization in the vertebrate gut symbiont Lactobacillus reuteri. PLoS. Genet. 7, e1001314 (2011)PubMedPubMedCentralCrossRefGoogle Scholar
  112. 112.
    R. Mobini, V. Tremaroli, M. Ståhlman et al., Metabolic effects of Lactobacillus reuteri DSM 17938 in Patients with Type 2 Diabetes: A Randomized Controlled Trial. Diabetes. Obes. Metab. 19, 579–589 (2016)CrossRefGoogle Scholar
  113. 113.
    Y.C. Lu, L.T. Yin, W.T. Chang, J.S. Huang, Effect of Lactobacillus reuteri GMNL-263 treatment on renal fibrosis in diabetic rats. J. Biosci. Bioeng. 110, 709–715 (2010)PubMedCrossRefGoogle Scholar
  114. 114.
    F.C. Hsieh, C.L. Lee, C.Y. Chai, W.T. Chen, Y.C. Lu, C.S. Wu, Oral administration of Lactobacillus reuteri GMNL-263 improves insulin resistance and ameliorates hepatic steatosis in high fructose-fed rats. Nutr. Metab. 10, 35 (2013)CrossRefGoogle Scholar
  115. 115.
    T. Poutahidis, M. Kleinewietfeld, C. Smillie et al., Microbial reprogramming inhibits Western diet-associated obesity. PLoS. ONE. 8, e68596 (2013)PubMedPubMedCentralCrossRefGoogle Scholar
  116. 116.
    J.W. Anderson, S.E. Gilliland, Effect of fermented milk (yogurt) containing Lactobacillus acidophilus L1 on serum cholesterol in hypercholesterolemic humans. J. Am. Coll. Nutr. 18, 43–50 (1999)PubMedCrossRefGoogle Scholar
  117. 117.
    A.S. Andreasen, N. Larsen, T. Pedersen-Skovsgaard et al., Effects of Lactobacillus acidophilus NCFM on insulin sensitivity and the systemic inflammatory response in human subjects. Br. J. Nutr. 104, 1831–1838 (2010)PubMedCrossRefGoogle Scholar
  118. 118.
    F. Turroni, D. van Sinderen, M. Ventura, Genomics and ecological overview of the genus Bifidobacterium. Int. J. Food. Microbiol. 149, 37–44 (2011)PubMedCrossRefGoogle Scholar
  119. 119.
    M. Arumugam, J. Raes, E. Pelletier et al., Enterotypes of the human gut microbiome. Nature. 473, 174–180 (2011)PubMedPubMedCentralCrossRefGoogle Scholar
  120. 120.
    S.H. Duncan, H.J. Flint, Probiotics and prebiotics and health in ageing populations. Maturitas. 75, 44–50 (2013)PubMedCrossRefGoogle Scholar
  121. 121.
    J. Amar, C. Chabo, A. Waget et al., Intestinal mucosal adherence and translocation of commensal bacteria at the early onset of type 2 diabetes: molecular mechanisms and probiotic treatment. EMBO. Mol. Med. 3, 559–572 (2011)PubMedPubMedCentralCrossRefGoogle Scholar
  122. 122.
    L.J. Bernini, A.N. Simao, D.F. Alfieri et al., Beneficial effects of Bifidobacterium lactis on lipid profile and cytokines in patients with metabolic syndrome: A randomized trial. Effects of probiotics on metabolic syndrome. Nutrition. 32, 716–719 (2016)PubMedCrossRefGoogle Scholar
  123. 123.
    S. Kondo, J.Z. Xiao, T. Satoh et al., Antiobesity effects of Bifidobacterium breve strain B-3 supplementation in a mouse model with high-fat diet-induced obesity. Biosci. Biotechnol. Biochem. 74, 1656–1661 (2010)PubMedCrossRefGoogle Scholar
  124. 124.
    S. Kondo, A. Kamei, J.Z. Xiao, K. Iwatsuki, K. Abe, Bifidobacterium breve B-3 exerts metabolic syndrome-suppressing effects in the liver of diet-induced obese mice: a DNA microarray analysis. Benef. Microbes. 4, 247–251 (2013)PubMedCrossRefGoogle Scholar
  125. 125.
    J. Minami, S. Kondo, N. Yanagisawa et al., Oral administration of Bifidobacterium breve B-3 modifies metabolic functions in adults with obese tendencies in a randomised controlled trial. J. Nutr. Sci. 4, e17 (2015)PubMedPubMedCentralCrossRefGoogle Scholar
  126. 126.
    J.Z. Xiao, S. Kondo, N. Takahashi et al., Effects of milk products fermented by Bifidobacterium longum on blood lipids in rats and healthy adult male volunteers. J. Dairy. Sci. 86, 2452–2461 (2003)PubMedCrossRefGoogle Scholar
  127. 127.
    A. Reichold, S.A. Brenner, A. Spruss, K. Förster-Fromme, I. Bergheim, S.C. Bischoff, Bifidobacterium adolescentis protects from the development of nonalcoholic steatohepatitis in a mouse model. J. Nutr. Biochem. 25, 118–125 (2014)PubMedCrossRefGoogle Scholar
  128. 128.
    M.J. Medellin-Pena, M.W. Griffiths, Effect of molecules secreted by Lactobacillus acidophilus strain La-5 on Escherichia coli O157:H7 colonization. Appl. Environ. Microbiol. 75, 1165–1172 (2009)PubMedCrossRefGoogle Scholar
  129. 129.
    M.A. Riley, J.E. Wertz, Bacteriocin diversity: ecological and evolutionary perspectives. Biochimie. 84, 357–364 (2002)PubMedCrossRefGoogle Scholar
  130. 130.
    J.M. Bates, J. Akerlund, E. Mittge, K. Guillemin, Intestinal alkaline phosphatase detoxifies lipopolysaccharide and prevents inflammation in zebrafish in response to the gut microbiota. Cell. Host. Microbe. 2, 371–382 (2007)PubMedPubMedCentralCrossRefGoogle Scholar
  131. 131.
    E. Cario, Bacterial interactions with cells of the intestinal mucosa: Toll-like receptors and NOD2. Gut. 54, 1182–1193 (2005)PubMedPubMedCentralCrossRefGoogle Scholar
  132. 132.
    D. Artis, Epithelial-cell recognition of commensal bacteria and maintenance of immune homeostasis in the gut. Nat. Rev. Immunol. 8, 411–420 (2008)PubMedCrossRefGoogle Scholar
  133. 133.
    J. Lee, J.H. Mo, C. Shen, A.N. Rucker, E. Raz, Toll-like receptor signaling in intestinal epithelial cells contributes to colonic homoeostasis. Curr. Opin. Gastroenterol. 23, 27–31 (2007)PubMedCrossRefGoogle Scholar
  134. 134.
    M. Rescigno, M. Urbano, B. Valzasina et al., Dendritic cells express tight junction proteins and penetrate gut epithelial monolayers to sample bacteria. Nat. Immunol. 2, 361–367 (2001)PubMedCrossRefGoogle Scholar
  135. 135.
    R. Medzhitov, Recognition of microorganisms and activation of the immune response. Nature 449, 819–826 (2007)PubMedCrossRefGoogle Scholar
  136. 136.
    S.I. Gringhuis, J. den Dunnen, M. Litjens, B. van Het Hof, Y. van Kooyk, T.B. Geijtenbeek, C-type lectin DC-SIGN modulates Toll-like receptor signaling via Raf-1 kinase-dependent acetylation of transcription factor NF-kappaB. Immunity. 26, 605–616 (2007)PubMedCrossRefGoogle Scholar
  137. 137.
    W. Strober, P.J. Murray, A. Kitani, T. Watanabe, Signalling pathways and molecular interactions of NOD1 and NOD2. Nat. Rev. Immunol. 6, 9–20 (2006)PubMedCrossRefGoogle Scholar
  138. 138.
    G. Melmed, L.S. Thomas, N. Lee et al., Human intestinal epithelial cells are broadly unresponsive to Toll-like receptor 2-dependent bacterial ligands: implications for host-microbial interactions in the gut. J. Immunol. 170, 1406–1415 (2003)PubMedCrossRefGoogle Scholar
  139. 139.
    E.C. Lavelle, C. Murphy, L.A. O’Neill, E.M. Creagh, The role of TLRs, NLRs, and RLRs in mucosal innate immunity and homeostasis. Mucosal Immunol. 3, 17–28 (2010)PubMedCrossRefGoogle Scholar
  140. 140.
    R.D. Fusunyan, N.N. Nanthakumar, M.E. Baldeon, W.A. Walker, Evidence for an innate immune response in the immature human intestine: toll-like receptors on fetal enterocytes. Pediatr. Res. 49, 589–593 (2001)PubMedCrossRefGoogle Scholar
  141. 141.
    A.T. Gewirtz, T.A. Navas, S. Lyons, P.J. Godowski, J.L. Madara, Cutting edge: bacterial flagellin activates basolaterally expressed TLR5 to induce epithelial proinflammatory gene expression. J. Immunol. 167, 1882–1885 (2001)PubMedCrossRefGoogle Scholar
  142. 142.
    M.T. Abreu, Toll-like receptor signalling in the intestinal epithelium: how bacterial recognition shapes intestinal function. Nat. Rev. Immunol. 10, 131–144 (2010)PubMedCrossRefGoogle Scholar
  143. 143.
    R. McClure, P. Massari, TLR-Dependent human mucosal epithelial cell responses to microbial pathogens. Front. Immunol. 5, 386 (2014)PubMedPubMedCentralCrossRefGoogle Scholar
  144. 144.
    K. Gao, C. Wang, L. Liu et al., Immunomodulation and signaling mechanism of Lactobacillus rhamnosus GG and its components on porcine intestinal epithelial cells stimulated by lipopolysaccharide. J. Microbiol. Immunol. Infect. S1684-1182, 00748–3 (2015)Google Scholar
  145. 145.
    N.J. Nilsen, S. Deininger, U. Nonstad et al., Cellular trafficking of lipoteichoic acid and Toll-like receptor 2 in relation to signaling: role of CD14 and CD36. J. Leukoc. Biol. 84, 280–291 (2008)PubMedPubMedCentralCrossRefGoogle Scholar
  146. 146.
    I.J. Claes, M.E. Segers, T.L. Verhoeven et al., Lipoteichoic acid is an important microbe-associated molecular pattern of Lactobacillus rhamnosus GG. Microb. Cell. Fact. 11, 161 (2012)PubMedPubMedCentralCrossRefGoogle Scholar
  147. 147.
    R. Sengupta, E. Altermann, R.C. Anderson, W.C. McNabb, P.J. Moughan, N.C. Roy, The role of cell surface architecture of lactobacilli in host-microbe interactions in the gastrointestinal tract. Mediators. Inflamm. 2013, 237921 (2013)PubMedPubMedCentralCrossRefGoogle Scholar
  148. 148.
    W. Wang, S. Uzzau, S.E. Goldblum, A. Fasano, Human zonulin, a potential modulator of intestinal tight junctions. J. Cell. Sci. 113, 4435–4440 (2000)PubMedGoogle Scholar
  149. 149.
    M. Furuse, H. Sasaki, K. Fujimoto, S. Tsukita, A single gene product, claudin-1 or -2, reconstitutes tight junction strands and recruits occludin in fibroblasts. J. Cell. Biol. 143, 391–401 (1998)PubMedPubMedCentralCrossRefGoogle Scholar
  150. 150.
    M.S. Balda, J.A. Whitney, C. Flores, S. González, M. Cereijido, K. Matter, Functional dissociation of paracellular permeability and transepithelial electrical resistance and disruption of the apical-basolateral intramembrane diffusion barrier by expression of a mutant tight junction membrane protein. J. Cell. Biol. 134, 1031–1049 (1996)PubMedCrossRefGoogle Scholar
  151. 151.
    R.M. Patel, L.S. Myers, A.R. Kurundkar, A. Maheshwari, A. Nusrat, P.W. Lin, Probiotic bacteria induce maturation of intestinal claudin 3 expression and barrier function. Am. J. Pathol. 180, 626–635 (2012)PubMedPubMedCentralCrossRefGoogle Scholar
  152. 152.
    R.C. Anderson, A.L. Cookson, W.C. McNabb et al., Lactobacillus plantarum MB452 enhances the function of the intestinal barrier by increasing the expression levels of genes involved in tight junction formation. BMC. Microbiol. 10, 316 (2012)CrossRefGoogle Scholar
  153. 153.
    J.B. Ewaschuk, H. Diaz, L. Meddings et al., Secreted bioactive factors from Bifidobacterium infantis enhance epithelial cell barrier function. Am. J. Physiol. Gastrointest. Liver. Physiol. 295, G1025–G1034 (2008)PubMedCrossRefGoogle Scholar
  154. 154.
    D. Ghadimi, M. de Vrese, K.J. Heller, J. Schrezenmeir, Lactic acid bacteria enhance autophagic ability of mononuclear phagocytes by increasing Th1 autophagy-promoting cytokine (IFN-gamma) and nitric oxide (NO) levels and reducing Th2 autophagy-restraining cytokines (IL-4 and IL-13) in response to Mycobacterium tuberculosis antigen. Int. Immunopharmacol. 10, 694–706 (2010)PubMedCrossRefGoogle Scholar
  155. 155.
    D. Fayol-Messaoudi, C.N. Berger, M.H. Coconnier-Polter, V. Liévin-Le Moal, A.L. Servin, pH-, Lactic acid-, and non-lactic acid-dependent activities of probiotic Lactobacilli against Salmonella enterica Serovar Typhimurium. Appl. Environ. Microbiol. 71, 6008–6013 (2005)PubMedPubMedCentralCrossRefGoogle Scholar
  156. 156.
    P.A. Maragkoudakis, W. Chingwaru, L. Gradisnik, E. Tsakalidou, A. Cencic, Lactic acid bacteria efficiently protect human and animal intestinal epithelial and immune cells from enteric virus infection. Int. J. Food. Microbiol. 141(Suppl 1), S91–S97 (2014)Google Scholar
  157. 157.
    F. Atassi, A.L. Servin, Individual and co-operative roles of lactic acid and hydrogen peroxide in the killing activity of enteric strain Lactobacillus johnsonii NCC933 and vaginal strain Lactobacillus gasseri KS120.1 against enteric, uropathogenic and vaginosis-associated pathogens. FEMS. Microbiol. Lett. 304, 29–38 (2010)PubMedCrossRefGoogle Scholar
  158. 158.
    I. Reveron, H. Rodriguez, G. Campos et al., Tannic acid-dependent modulation of selected Lactobacillus plantarum traits linked to gastrointestinal survival. PLoS. ONE. 8, e66473 (2013)PubMedPubMedCentralCrossRefGoogle Scholar
  159. 159.
    Y. Nishitani, E. Sasaki, T. Fujisawa, R. Osawa, Genotypic analyses of lactobacilli with a range of tannase activities isolated from human feces and fermented foods. Syst. Appl. Microbiol. 27, 109–117 (2004)PubMedCrossRefGoogle Scholar
  160. 160.
    N. Jimenez, J.A. Curiel, I. Reveron, B. de Las Rivas, R. Munoz, Uncovering the Lactobacillus plantarum WCFS1 gallate decarboxylase involved in tannin degradation. Appl. Environ. Microbiol. 79, 4253–4263 (2013)PubMedPubMedCentralCrossRefGoogle Scholar
  161. 161.
    P. van Baarlen, F.J. Troost, S. van Hemert et al., Differential NF-kappaB pathways induction by Lactobacillus plantarum in the duodenum of healthy humans correlating with immune tolerance. Proc. Natl. Acad. Sci. U S A. 106, 2371–2376 (2009)PubMedPubMedCentralCrossRefGoogle Scholar
  162. 162.
    H. van Bokhorst-van de Veen, I.C. Lee, M.L. Marco, M. Wels, P.A. Bron, M. Kleerebezem, Modulation of Lactobacillus plantarum gastrointestinal robustness by fermentation conditions enables identification of bacterial robustness markers. PLoS. ONE. 7, e39053 (2012)PubMedPubMedCentralCrossRefGoogle Scholar
  163. 163.
    M.T. Liong, N.P. Shah, Acid and bile tolerance and cholesterol removal ability of lactobacilli strains. J. Dairy. Sci. 88, 55–66 (2005)PubMedCrossRefGoogle Scholar
  164. 164.
    M.L. Jones, C. Tomaro-Duchesneau, C.J. Martoni, S. Prakash, Cholesterol lowering with bile salt hydrolase-active probiotic bacteria, mechanism of action, clinical evidence, and future direction for heart health applications. Expert. Opin. Biol. Ther. 13, 631–642 (2013)PubMedCrossRefGoogle Scholar
  165. 165.
    D.O. Noh, S.E. Gilliland, Influence of bile on cellular integrity and beta-galactosidase activity of Lactobacillus acidophilus. J. Dairy. Sci. 76, 1253–1259 (1993)PubMedCrossRefGoogle Scholar
  166. 166.
    Y.K. Nakamura, S.T. Omaye, Metabolic diseases and pro- and prebiotics: Mechanistic insights. Nutr. Metab. 9, 60 (2012)CrossRefGoogle Scholar
  167. 167.
    S. Toomey, J. McMonagle, H.M. Roche, Conjugated linoleic acid: a functional nutrient in the different pathophysiological components of the metabolic syndrome? Curr. Opin. Clin. Nutr. Metab. Care. 9, 740–747 (2006)PubMedCrossRefGoogle Scholar
  168. 168.
    HosonoA. Usman, Bile tolerance, taurocholate deconjugation, and binding of cholesterol by Lactobacillus gasseri strains. J. Dairy. Sci. 82, 243–248 (1999)PubMedCrossRefGoogle Scholar
  169. 169.
    F. Sakai, T. Hosoya, A. Ono-Ohmachi et al., Lactobacillus gasseri SBT2055 induces TGF-beta expression in dendritic cells and activates TLR2 signal to produce IgA in the small intestine. PLoS. ONE. 9, e105370 (2014)PubMedPubMedCentralCrossRefGoogle Scholar
  170. 170.
    H. Dong, I. Rowland, K.M. Tuohy, L.V. Thomas, P. Yaqoob, Selective effects of Lactobacillus casei Shirota on T cell activation, natural killer cell activity and cytokine production. Clin. Exp. Immunol. 161, 378–388 (2010)PubMedPubMedCentralGoogle Scholar
  171. 171.
    K. Takeda, T. Suzuki, S.I. Shimada, K. Shida, M. Nanno, K. Okumura, Interleukin-12 is involved in the enhancement of human natural killer cell activity by Lactobacillus casei Shirota. Clin. Exp. Immunol. 146, 109–115 (2006)PubMedPubMedCentralCrossRefGoogle Scholar
  172. 172.
    K.A. Baken, J. Ezendam, E.R. Gremmer et al., Evaluation of immunomodulation by Lactobacillus casei Shirota: immune function, autoimmunity and gene expression. Int. J. Food. Microbiol. 112, 8–18 (2006)PubMedCrossRefGoogle Scholar
  173. 173.
    K. Shida, T. Suzuki, J. Kiyoshima-Shibata, S. Shimada, M. Nanno, Essential roles of monocytes in stimulating human peripheral blood mononuclear cells with Lactobacillus casei to produce cytokines and augment natural killer cell activity. Clin. Vaccine. Immunol. 13, 997–1003 (2006)PubMedPubMedCentralCrossRefGoogle Scholar
  174. 174.
    P. Gourbeyre, S. Denery, M. Bodinier, Probiotics, prebiotics, and synbiotics: impact on the gut immune system and allergic reactions. J. Leukoc. Biol. 89, 685–695 (2011)PubMedCrossRefGoogle Scholar
  175. 175.
    E. Yasuda, M. Serata, T. Sako, Suppressive effect on activation of macrophages by Lactobacillus casei strain Shirota genes determining the synthesis of cell wall-associated polysaccharides. Appl. Environ. Microbiol. 74, 4746–4755 (2008)PubMedPubMedCentralCrossRefGoogle Scholar
  176. 176.
    T. Watanabe, H. Nishio, T. Tanigawa et al., Probiotic Lactobacillus casei strain Shirota prevents indomethacin-induced small intestinal injury: involvement of lactic acid. Am. J. Physiol. Gastrointest. Liver. Physiol. 297, G506–G513 (2009)PubMedCrossRefGoogle Scholar
  177. 177.
    E.M. Tuomola, A.C. Ouwehand, S.J. Salminen, The effect of probiotic bacteria on the adhesion of pathogens to human intestinal mucus. FEMS. Immunol. Med. Microbiol. 26, 137–142 (1999)PubMedCrossRefGoogle Scholar
  178. 178.
    J. Reunanen, I. von Ossowski, A.P. Hendrickx, A. Palva, W.M. de Vos, Characterization of the SpaCBA pilus fibers in the probiotic Lactobacillus rhamnosus GG. Appl. Environ. Microbiol. 78, 2337–2344 (2012)PubMedPubMedCentralCrossRefGoogle Scholar
  179. 179.
    S. Lebeer, I. Claes, H.L. Tytgat et al., Functional analysis of Lactobacillus rhamnosus GG pili in relation to adhesion and immunomodulatory interactions with intestinal epithelial cells. Appl. Environ. Microbiol. 78, 185–193 (2012)PubMedPubMedCentralCrossRefGoogle Scholar
  180. 180.
    M. Kankainen, L. Paulin, S. Tynkkynen et al., Comparative genomic analysis of Lactobacillus rhamnosus GG reveals pili containing a human- mucus binding protein. Proc. Natl. Acad. Sci. U S A. 106, 17193–17198 (2009)PubMedPubMedCentralCrossRefGoogle Scholar
  181. 181.
    P. Tripathi, A. Beaussart, D. Alsteens et al., Adhesion and nanomechanics of pili from the probiotic Lactobacillus rhamnosus GG. ACS. Nano. 7, 3685–3697 (2013)PubMedCrossRefGoogle Scholar
  182. 182.
    B.R. Goldin, S.L. Gorbach, M. Saxelin, S. Barakat, L. Gualtieri, S. Salminen, Survival of Lactobacillus species (strain GG) in human gastrointestinal tract. Dig. Dis. Sci. 37, 121–128 (1992)PubMedCrossRefGoogle Scholar
  183. 183.
    F. Yan, L. Liu, P.J. Dempsey et al., A Lactobacillus rhamnosus GG-derived soluble protein, p40, stimulates ligand release from intestinal epithelial cells to transactivate epidermal growth factor receptor. J. Biol. Chem. 288, 30742–30751 (2013)PubMedPubMedCentralCrossRefGoogle Scholar
  184. 184.
    L. Wang, H. Cao, L. Liu et al., Activation of epidermal growth factor receptor mediates mucin production stimulated byp40, a Lactobacillus rhamnosus GG-derived protein. J. Biol. Chem. 289, 20234–20244 (2014)PubMedPubMedCentralCrossRefGoogle Scholar
  185. 185.
    D. Srutkova, M. Schwarzer, T. Hudcovic et al., Bifidobacterium longum CCM 7952 Promotes Epithelial Barrier Function and Prevents Acute DSS-Induced Colitis in Strictly Strain-Specific Manner. PLoS. ONE. 10, e0134050 (2015)PubMedPubMedCentralCrossRefGoogle Scholar
  186. 186.
    R. Mennigen, K. Nolte, E. Rijcken et al., Probiotic mixture VSL#3 protects the epithelial barrier by maintaining tight junction protein expression and preventing apoptosis in a murine model of colitis. Am. J. Physiol. Gastrointest. Liver. Physiol. 296, G1140–G1149 (2009)PubMedCrossRefGoogle Scholar
  187. 187.
    H. Hemmi, O. Takeuchi, T. Kawai et al., A Toll-like receptor recognizes bacterial DNA. Nature. 408, 740–745 (2000)PubMedCrossRefGoogle Scholar
  188. 188.
    J. Lee, J.H. Mo, K. Katakura et al., Maintenance of colonic homeostasis by distinctive apical TLR9 signalling in intestinal epithelial cells. Nat. Cell. Biol. 8, 1327–1336 (2006)PubMedCrossRefGoogle Scholar
  189. 189.
    I.D. Iliev, H. Kitazawa, T. Shimosato et al., Strong immunostimulation in murine immune cells by Lactobacillus rhamnosus GG DNA containing novel oligodeoxynucleotide pattern. Cell. Microbiol. 7, 403–414 (2005)PubMedCrossRefGoogle Scholar
  190. 190.
    U. Hynönen, A. Palva, Lactobacillus surface layer proteins: structure, function and applications. Appl. Microbiol. Biotechnol. 97, 5225–5243 (2013)PubMedPubMedCentralCrossRefGoogle Scholar
  191. 191.
    B. Johnson, K. Selle, S. O’Flaherty, Y.J. Goh, T. Klaenhammer, Identification of extracellular surface-layer associated proteins in Lactobacillus acidophilus NCFM. Microbiology. 159, 2269–2282 (2013)PubMedPubMedCentralCrossRefGoogle Scholar
  192. 192.
    Y.J. Goh, M.A. Azcárate-Peril, S. O’Flaherty et al., Development and application of a upp-based counterselective gene replacement system for the study of the S-layer protein SlpX of Lactobacillus acidophilus NCFM. Appl. Environ. Microbiol. 75, 3093–3105 (2009)PubMedPubMedCentralCrossRefGoogle Scholar
  193. 193.
    G. Zoumpopoulou, E. Tsakalidou, J. Dewulf, B. Pot, C. Grangette, Differential crosstalk between epithelial cells, dendritic cells and bacteria in a co-culture model. Int. J. Food. Microbiol. 131, 40–51 (2009)PubMedCrossRefGoogle Scholar
  194. 194.
    B. Foligne, S. Nutten, C. Grangette et al., Correlation between in vitro and in vivo immunomodulatory properties of lactic acid bacteria. World. J. Gastroenterol. 13, 236–243 (2007)PubMedPubMedCentralCrossRefGoogle Scholar
  195. 195.
    S.R. Konstantinov, H. Smidt, W.M. de Vos et al., S layer protein A of Lactobacillus acidophilus NCFM regulates immature dendritic cell and T cell functions. Proc. Natl. Acad. Sci. U S A. 105, 19474–19479 (2008)PubMedPubMedCentralCrossRefGoogle Scholar
  196. 196.
    Y.L. Lightfoot, K. Selle, T. Yang et al., SIGNR3-dependent immune regulation by Lactobacillus acidophilus surface layer protein A in colitis. EMBO. J. 34, 881–895 (2015)PubMedPubMedCentralCrossRefGoogle Scholar
  197. 197.
    H. Bischoff, The mechanism of alpha-glucosidase inhibition in the management of diabetes. Clin. Invest. Med. 18, 303–311 (1995)PubMedGoogle Scholar
  198. 198.
    M. Bermudez-Brito, S. Muñoz-Quezada, C. Gomez-Llorente et al., Cell-free culture supernatant of Bifidobacterium breve CNCM I-4035 decreases pro-inflammatory cytokines in human dendritic cells challenged with Salmonella typhi through TLR activation. PLoS. ONE. 8, e59370 (2013)PubMedPubMedCentralCrossRefGoogle Scholar
  199. 199.
    S.J. Aujla, P.J. Dubin, J.K. Kolls, Th17 cells and mucosal host defense. Semin. Immunol. 19, 377–382 (2007)PubMedPubMedCentralCrossRefGoogle Scholar
  200. 200.
    Y. Hiramatsu, T. Satho, K. Irie et al., Differences in TLR9-dependent inhibitory effects of H(2)O(2)-induced IL-8 secretion and NF-kappa B/I kappa B-alpha system activation by genomic DNA from five Lactobacillus species. Microbes. Infect. 15, 96–104 (2013)PubMedCrossRefGoogle Scholar
  201. 201.
    D. Ghadimi, M. Vrese, K.J. Heller, J. Schrezenmeir, Effect of natural commensal-origin DNA on toll-like receptor 9 (TLR9) signaling cascade, chemokine IL-8 expression, and barrier integritiy of polarized intestinal epithelial cells. Inflamm. Bowel. Dis. 16, 410–427 (2010)PubMedCrossRefGoogle Scholar
  202. 202.
    E.A. Eloe-Fadrosh, A. Brady, J. Crabtree et al., Functional dynamics of the gut microbiome in elderly people during probiotic consumption. MBio. 6, e00231–15 (2015)PubMedPubMedCentralCrossRefGoogle Scholar
  203. 203.
    C. Hou, H. Liu, J. Zhang et al., Intestinal microbiota succession and immunomodulatory consequences after introduction of Lactobacillus reuteri I5007 in neonatal piglets. PLoS. ONE. 10, e0119505 (2015)PubMedPubMedCentralCrossRefGoogle Scholar
  204. 204.
    N. Larsen, F.K. Vogensen, R.J. Gøbel et al., Effect of Lactobacillus salivarius Ls-33 on fecal microbiota in obese adolescents. Clin. Nutr. 32, 935–940 (2013)PubMedCrossRefGoogle Scholar
  205. 205.
    A. Belenguer, S.H. Duncan, A.G. Calder et al., Two routes of metabolic cross-feeding between Bifidobacterium adolescentis and butyrate-producing anaerobes from the human gut. Appl. Environ. Microbiol. 72, 3593–3599 (2006)PubMedPubMedCentralCrossRefGoogle Scholar
  206. 206.
    G. Falony, A. Vlachou, K. Verbrugghe, L. De Vuyst, Cross-feeding between Bifidobacterium longum BB536 and acetate-converting, butyrate-producing colon bacteria during growth on oligofructose. Appl. Environ. Microbiol. 72, 7835–7841 (2006)PubMedPubMedCentralCrossRefGoogle Scholar
  207. 207.
    S.H. Duncan, P. Louis, H.J. Flint, Lactate-utilizing bacteria, isolated from human feces, that produce butyrate as a major fermentation product. Appl. Environ. Microbiol. 70, 5810–5817 (2004)PubMedPubMedCentralCrossRefGoogle Scholar
  208. 208.
    M.J. Cox, Y.J. Huang, K.E. Fujimura et al., Lactobacillus casei abundance is associated with profound shifts in the infant gut microbiome. PLoS. ONE. 5, e8745 (2010)PubMedPubMedCentralCrossRefGoogle Scholar
  209. 209.
    K. Forslund, F. Hildebrand, T. Nielsen et al., Disentangling type 2 diabetes and metformin treatment signatures in the human gut microbiota. Nature. 528, 262–266 (2015)PubMedPubMedCentralCrossRefGoogle Scholar
  210. 210.
    H. Wu, E. Esteve, V. Tremaroli et al., Metformin alters the gut microbiome of individuals with treatment-naive type 2 diabetes, contributing to the therapeutic effects of the drug. Nat. Med. 23, 850–858 (2017)PubMedCrossRefGoogle Scholar
  211. 211.
    N.R. Shin, J.C. Lee, H.Y. Lee et al., An increase in the Akkermansia spp. population induced by metformin treatment improves glucose homeostasis in diet-induced obese mice. Gut 63, 727–735 (2014)PubMedCrossRefGoogle Scholar
  212. 212.
    H. Lee, G. Ko, Effect of metformin on metabolic improvement and gut microbiota. Appl. Environ. Microbiol. 80, 5935–5943 (2014)PubMedPubMedCentralCrossRefGoogle Scholar
  213. 213.
    J. de la Cuesta-Zuluaga, N.T. Mueller, V. Corrales-Agudelo et al., Metformin Is Associated With Higher Relative Abundance of Mucin-Degrading Akkermansia muciniphila and Several Short-Chain Fatty Acid-Producing Microbiota in the Gut. Diabetes. Care. 40, 54–62 (2017)PubMedCrossRefGoogle Scholar
  214. 214.
    J. Qin, Y. Li, Z. Cai et al., A metagenome-wide association study of gut microbiota in type 2 diabetes. Nature. 490, 55–60 (2012)PubMedCrossRefGoogle Scholar
  215. 215.
    M. Juntunen, P.V. Kirjavainen, A.C. Ouwehand, S.J. Salminen, E. Isolauri, Adherence of probiotic bacteria to human intestinal mucus in healthy infants and during rotavirus infection. Clin. Diagn. Lab. Immunol. 8, 293–296 (2001)PubMedPubMedCentralGoogle Scholar
  216. 216.
    Y.T. Tsai, P.C. Cheng, C.K. Fan, T.M. Pan, Time-dependent persistence of enhanced immune response by a potential probiotic strain Lactobacillus paracasei subsp. paracasei NTU 101. Int. J. Food. Microbiol. 128, 219–225 (2008)PubMedCrossRefGoogle Scholar
  217. 217.
    M. Schultz, C. Göttl, R.J. Young, P. Iwen, J.A. Vanderhoof, Administration of oral probiotic bacteria to pregnant women causes temporary infantile colonization. J. Pediatr. Gastroenterol. Nutr. 38, 293–297 (2004)PubMedCrossRefGoogle Scholar
  218. 218.
    P. Toivanen, J. Vaahtovuo, E. Eerola, Influence of major histocompatibility complex on bacterial composition of fecal flora. Infect. Immun. 69, 2372–2377 (2001)PubMedPubMedCentralCrossRefGoogle Scholar
  219. 219.
    M. van den Nieuwboer, R.J. Brummer, F. Guarner, L. Morelli, M. Cabana, E. Claassen, Safety of probiotics and synbiotics in children under 18 years of age. Benef. Microbes. 6, 615–630 (2015)PubMedCrossRefGoogle Scholar
  220. 220.
    L. Brunkwall, M. Orho-Melander, The gut microbiome as a target for prevention and treatment of hyperglycaemia in type 2 diabetes: from current human evidence to future possibilities. Diabetologia. 60, 943–951 (2017)PubMedPubMedCentralCrossRefGoogle Scholar
  221. 221.
    F.J. Cousin, S.M. Lynch, H.M. Harris et al., Detection and genomic characterization of motility in Lactobacillus curvatus: confirmation of motility in a species outside the Lactobacillus salivarius clade. Appl. Environ. Microbiol. 81, 1297–1308 (2015)PubMedGoogle Scholar
  222. 222.
    F. Turroni, E. Foroni, F. Serafini et al., Ability of Bifidobacterium breve to grow on different types of milk: exploring the metabolism of milk through genome analysis. Appl. Environ. Microbiol. 77, 7408–7417 (2011)PubMedPubMedCentralCrossRefGoogle Scholar
  223. 223.
    S.W. Kim, K.Y. Park, B. Kim, E. Kim, C.K. Hyun, Lactobacillus rhamnosus GG improves insulin sensitivity and reduces adiposity in high-fat diet-fed mice through enhancement of adiponectin production. Biochem. Biophys. Res. Commun. 431, 258–263 (2013)PubMedCrossRefGoogle Scholar
  224. 224.
    R. Luoto, M. Kalliomaki, K. Laitinen, E. Isolauri, The impact of perinatal probiotic intervention on the development of overweight and obesity: follow-up study from birth to 10 years. Int. J. Obes. 34, 1531–1537 (2010)CrossRefGoogle Scholar
  225. 225.
    I. Novotny Nunez, C. Maldonado Galdeano, A. de Moreno de LeBlanc, G. Perdigon, Lactobacillus casei CRL 431 administration decreases inflammatory cytokines in a diet-induced obese mouse model. Nutrition. 31, 1000–1007 (2013)CrossRefGoogle Scholar
  226. 226.
    L. Aronsson, Y. Huang, P. Parini et al., Decreased fat storage by Lactobacillus paracasei is associated with increased levels of angiopoietin-like 4 protein (ANGPTL4). PLoS. ONE. 5, e13087 (2010)PubMedPubMedCentralCrossRefGoogle Scholar
  227. 227.
    H. Fazeli, J. Moshtaghian, M. Mirlohi, M. Shirzadi, Reduction in lipid serum parameter by incorporation of a native strain of Lactobacillus plantarum A7 in mice. IJDLD. 9, 1–7 (2010)Google Scholar
  228. 228.
    T. Sakai, T. Taki, A. Nakamoto et al., Lactobacillus plantarum OLL2712 regulates glucose metabolism in C57BL/6 mice fed a high-fat diet. J. Nutr. Sci. Vitaminol. 59, 144–147 (2013)PubMedCrossRefGoogle Scholar
  229. 229.
    J.E. Park, S.H. Oh, Y.S. Cha, Lactobacillus plantarum LG42 isolated from gajami sik-hae decreases body and fat pad weights in diet-induced obese mice. J. Appl. Microbiol. 116, 145–156 (2014)PubMedCrossRefGoogle Scholar
  230. 230.
    R. Ben Salah, I. Trabelsi, K. Hamden, H. Chouayekh, S. Bejar, Lactobacillus plantarum TN8 exhibits protective effects on lipid, hepatic and renal profiles in obese rat. Anaerobe. 23, 55–61 (2013)PubMedCrossRefGoogle Scholar
  231. 231.
    T. Okubo, N. Takemura, A. Yoshida, K. Sonoyama, KK/Ta Mice Administered Lactobacillus plantarum Strain No. 14 Have Lower Adiposity and Higher Insulin Sensitivity. Biosci. Microbiota. Food Health. 32, 93–100 (2013)PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2017

Authors and Affiliations

  1. 1.Department of MedicineDivision of Metabolism, Endocrinology and Nutrition, University of WashingtonSeattleUSA
  2. 2.Center for Integrative Brain Research, Seattle Children’s Hospital & Research InstituteSeattleUSA
  3. 3.Pediatric Endocrinology, Seattle Children’s Hospital & Research InstituteSeattleUSA

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