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

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Abstract

Introduction

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.

Purpose

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.

Conclusion

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.

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Abbreviations

ANGPTL:

angiopoietin-like protein

ALT:

alanine amino transferase

AST:

aspartate aminotransferase

BG(120) :

blood glucose at 120 min

BSH:

bile salt hydrolase

BMI:

body mass index

BW:

body weight

CAT:

catalase

CFU:

colony forming unit

CLR:

C-type lectin receptor

CRP:

c-reactive protein

CpG:

cytosine-guanine dinucleotides

DC:

dendritic cell

DC-SIGN:

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

DIO:

diet-induced obesity

EGF:

epithelial growth factor

EPI:

epididymal fat

DIO:

diet-induced obesity

FBG:

Fasting blood glucose

FM:

fat mass

GGT:

gamma-glutamyl transferase

GI:

gastrointestinal tract

GSH:

glutathione

HbA1c :

hemoglobin A1c

HFD:

high-fat diet

HfrD:

high-fructose diet

IBS:

irritable bowl syndrome

IEC:

intestinal endothelial cell

IL:

interleukin

INF:

interferon

IR:

insulin resistance

JAK2:

Janus kinase 2

IR:

insulin resistance

LAB:

lactic acid bacteria

LBP:

liposaccharide-binding protein precursor

LDL:

low density lipoprotein

LPS:

Lipopolysaccharides

LTA:

lipteichoic acid

LTR:

toll-like receptor

MAMPs:

microorganism-associated molecular patterns

MDA:

malondialdehyde

MetS:

Metabolic Syndrome

NAFLD:

non-alcoholic fatty liver disease

NASH:

non-alcoholic steatohepatitis

ND:

not determined

NK:

natural killer cell

NRL:

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

NS:

not significant

OGTT:

oral glucose tolerance test

P21:

cyclin-dependent kinase inhibitor

PAI-1:

plasminogen activator inhibitor-1

PPAR- γ:

peroxisome proliferator-activated receptor-γ

PRRs:

pattern recognition receptors

ROS:

reactive oxygen species

STAT:

signal transducer and activator of transcription-1

SCFAs:

short-chain fatty acids

Slp:

surface layer protein

SMA:

smooth muscle actin

SOD:

superoxide dismutase

STZ:

streptozotocin

T2D:

Type 2 diabetes

TC:

total cholesterol

TG:

triglycerides

TNF:

tumor necrosis factor

ZO-1:

zonula occludens-1

References

  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)

    Article  PubMed  PubMed Central  Google Scholar 

  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)

    Article  PubMed  Google Scholar 

  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)

    Article  PubMed  PubMed Central  Google Scholar 

  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)

    Article  PubMed  PubMed Central  Google Scholar 

  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)

    Article  PubMed  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  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)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. M. Mraz, M. Haluzik, The role of adipose tissue immune cells in obesity and low-grade inflammation. J. Endocrinol. 222, R113–R127 (2014)

    Article  CAS  PubMed  Google Scholar 

  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)

  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)

    Article  CAS  PubMed  Google Scholar 

  11. P.D. Cani, J. Amar, M.A. Iglesias et al., Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes. 56, 1761–1772 (2007)

    Article  CAS  PubMed  Google Scholar 

  12. S. de Kort, D. Keszthelyi, A.A. Masclee, Leaky gut and diabetes mellitus, what is the link? Obes. Rev. 12, 449–458 (2011)

    Article  PubMed  CAS  Google Scholar 

  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)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. A.M. Kabat, N. Srinivasan, K.J. Maloy, Modulation of immune development and function by intestinal microbiota. Trends. Immunol. 35, 507–517 (2014)

    Article  CAS  PubMed  Google Scholar 

  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)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  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)

    Article  CAS  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  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)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. P.J. Turnbaugh, M. Hamady, T. Yatsunenko et al., A core gut microbiome in obese and lean twins. Nature. 457, 480–484 (2009)

    Article  CAS  PubMed  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  24. A. Schwiertz, D. Taras, K. Schafer et al., Microbiota and SCFA in lean and overweight healthy subjects. Obesity. 18, 190–195 (2010)

    Article  PubMed  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  26. E. Le Chatelier, T. Nielsen, J. Qin et al., Richness of human gut microbiome correlates with metabolic markers. Nature. 500, 541–546 (2013)

    Article  PubMed  CAS  Google Scholar 

  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)

    Article  PubMed  CAS  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  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)

    Article  PubMed  PubMed Central  Google Scholar 

  30. S.L. Schnorr, M. Candela, S. Rampelli et al., Gut microbiome of the Hadza hunter-gatherers. Nat Commun. 5, 3654 (2014)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. J.C. Clemente, E.C. Pehrsson, M.J. Blaser, et al., The microbiome of uncontacted Amerindians. Sci Adv. 1, e1500183 (2015)

  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)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. J.K. Nicholson, E. Holmes, J. Kinross et al., Host-gut microbiota metabolic interactions. Science 336, 1262–1267 (2012)

    Article  CAS  PubMed  Google Scholar 

  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)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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)

    Article  CAS  Google Scholar 

  36. D.W. Russell, The enzymes, regulation, and genetics of bile acid synthesis. Annu. Rev. Biochem. 72, 137–174 (2003)

    Article  CAS  PubMed  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  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)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  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)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. T.J. Borody, S. Paramsothy, G. Agrawal, Fecal microbiota transplantation: indications, methods, evidence, and future directions. Curr. Gastroenterol. Rep. 15, 337 (2013)

    Article  PubMed  PubMed Central  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  44. M.B. Smith, C. Kelly, E.J. Alm, Policy: How to regulate faecal transplants. Nature. 506, 290–291 (2014)

    Article  PubMed  Google Scholar 

  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)

    Article  PubMed  PubMed Central  Google Scholar 

  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)

    Article  CAS  Google Scholar 

  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)

    Article  PubMed  CAS  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  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)

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  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)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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)

    Article  PubMed  PubMed Central  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  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)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  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)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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)

    Article  PubMed  PubMed Central  Google Scholar 

  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)

    Article  PubMed  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  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)

    Article  PubMed  PubMed Central  Google Scholar 

  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)

  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)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  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)

    Article  PubMed  PubMed Central  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  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)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  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)

    Article  PubMed  PubMed Central  Google Scholar 

  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)

    Article  PubMed  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  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)

    Article  PubMed  PubMed Central  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  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)

    PubMed  PubMed Central  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  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)

    PubMed  PubMed Central  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  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)

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  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)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. H. Toh, K. Oshima, A. Nakano et al., Genomic adaptation of the Lactobacillus casei group. PLoS. ONE. 8, e75073 (2013)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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)

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  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)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  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)

    Article  PubMed  Google Scholar 

  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)

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  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)

    Article  CAS  Google Scholar 

  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. 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)

    Article  CAS  PubMed  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  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)

    Article  PubMed  Google Scholar 

  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)

    Article  PubMed  CAS  Google Scholar 

  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)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  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)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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)

    Article  PubMed  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  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)

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  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)

    Article  PubMed  Google Scholar 

  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)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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)

    Article  CAS  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  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)

    Article  CAS  Google Scholar 

  115. T. Poutahidis, M. Kleinewietfeld, C. Smillie et al., Microbial reprogramming inhibits Western diet-associated obesity. PLoS. ONE. 8, e68596 (2013)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  118. F. Turroni, D. van Sinderen, M. Ventura, Genomics and ecological overview of the genus Bifidobacterium. Int. J. Food. Microbiol. 149, 37–44 (2011)

    Article  CAS  PubMed  Google Scholar 

  119. M. Arumugam, J. Raes, E. Pelletier et al., Enterotypes of the human gut microbiome. Nature. 473, 174–180 (2011)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  120. S.H. Duncan, H.J. Flint, Probiotics and prebiotics and health in ageing populations. Maturitas. 75, 44–50 (2013)

    Article  CAS  PubMed  Google Scholar 

  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)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  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)

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  129. M.A. Riley, J.E. Wertz, Bacteriocin diversity: ecological and evolutionary perspectives. Biochimie. 84, 357–364 (2002)

    Article  CAS  PubMed  Google Scholar 

  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)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  131. E. Cario, Bacterial interactions with cells of the intestinal mucosa: Toll-like receptors and NOD2. Gut. 54, 1182–1193 (2005)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  132. D. Artis, Epithelial-cell recognition of commensal bacteria and maintenance of immune homeostasis in the gut. Nat. Rev. Immunol. 8, 411–420 (2008)

    Article  CAS  PubMed  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  135. R. Medzhitov, Recognition of microorganisms and activation of the immune response. Nature 449, 819–826 (2007)

    Article  CAS  PubMed  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  143. R. McClure, P. Massari, TLR-Dependent human mucosal epithelial cell responses to microbial pathogens. Front. Immunol. 5, 386 (2014)

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  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. 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)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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)

    Article  PubMed  PubMed Central  Google Scholar 

  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)

    CAS  PubMed  Google Scholar 

  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)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  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)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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)

    Article  CAS  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  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)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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. 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)

    Article  CAS  PubMed  Google Scholar 

  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)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  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)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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)

    Article  PubMed  PubMed Central  Google Scholar 

  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)

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  166. Y.K. Nakamura, S.T. Omaye, Metabolic diseases and pro- and prebiotics: Mechanistic insights. Nutr. Metab. 9, 60 (2012)

    Article  CAS  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  168. HosonoA. Usman, Bile tolerance, taurocholate deconjugation, and binding of cholesterol by Lactobacillus gasseri strains. J. Dairy. Sci. 82, 243–248 (1999)

    Article  CAS  PubMed  Google Scholar 

  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)

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  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)

    CAS  PubMed  PubMed Central  Google Scholar 

  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)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  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)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  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)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  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)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  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)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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)

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  187. H. Hemmi, O. Takeuchi, T. Kawai et al., A Toll-like receptor recognizes bacterial DNA. Nature. 408, 740–745 (2000)

    Article  CAS  PubMed  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  190. U. Hynönen, A. Palva, Lactobacillus surface layer proteins: structure, function and applications. Appl. Microbiol. Biotechnol. 97, 5225–5243 (2013)

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  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)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  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)

    Article  PubMed  PubMed Central  Google Scholar 

  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)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  197. H. Bischoff, The mechanism of alpha-glucosidase inhibition in the management of diabetes. Clin. Invest. Med. 18, 303–311 (1995)

    CAS  PubMed  Google Scholar 

  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)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  199. S.J. Aujla, P.J. Dubin, J.K. Kolls, Th17 cells and mucosal host defense. Semin. Immunol. 19, 377–382 (2007)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  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)

    Article  PubMed  Google Scholar 

  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)

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  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)

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  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)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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)

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  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)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  212. H. Lee, G. Ko, Effect of metformin on metabolic improvement and gut microbiota. Appl. Environ. Microbiol. 80, 5935–5943 (2014)

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  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)

    Article  PubMed  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  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)

    CAS  PubMed  PubMed Central  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  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)

    Article  PubMed  Google Scholar 

  218. P. Toivanen, J. Vaahtovuo, E. Eerola, Influence of major histocompatibility complex on bacterial composition of fecal flora. Infect. Immun. 69, 2372–2377 (2001)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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)

    Article  PubMed  Google Scholar 

  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)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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)

    CAS  PubMed  Google Scholar 

  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)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  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)

    Article  CAS  Google Scholar 

  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)

    Article  CAS  Google Scholar 

  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)

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  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)

    CAS  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  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)

    Article  PubMed  CAS  Google Scholar 

  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)

    Article  PubMed  PubMed Central  Google Scholar 

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Authors and Affiliations

  1. Department of Medicine, Division of Metabolism, Endocrinology and Nutrition, University of Washington, Seattle, WA, 98109, USA

    Christiane S. Hampe

  2. Center for Integrative Brain Research, Seattle Children’s Hospital & Research Institute, Seattle, WA, 98101, USA

    Christian L. Roth

  3. Pediatric Endocrinology, Seattle Children’s Hospital & Research Institute, Seattle, WA, 98101, USA

    Christian L. Roth

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Hampe, C.S., Roth, C.L. Probiotic strains and mechanistic insights for the treatment of type 2 diabetes. Endocrine 58, 207–227 (2017). https://doi.org/10.1007/s12020-017-1433-z

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