Skip to main content
Top
Published in: Nutrition Journal 1/2014

Open Access 01-12-2014 | Review

Gut microbiota, probiotics and diabetes

Authors: Aline Corado Gomes, Allain Amador Bueno, Rávila Graziany Machado de Souza, João Felipe Mota

Published in: Nutrition Journal | Issue 1/2014

Login to get access

Abstract

Diabetes is a condition of multifactorial origin, involving several molecular mechanisms related to the intestinal microbiota for its development. In type 2 diabetes, receptor activation and recognition by microorganisms from the intestinal lumen may trigger inflammatory responses, inducing the phosphorylation of serine residues in insulin receptor substrate-1, reducing insulin sensitivity. In type 1 diabetes, the lowered expression of adhesion proteins within the intestinal epithelium favours a greater immune response that may result in destruction of pancreatic β cells by CD8+ T-lymphocytes, and increased expression of interleukin-17, related to autoimmunity. Research in animal models and humans has hypothesized whether the administration of probiotics may improve the prognosis of diabetes through modulation of gut microbiota. We have shown in this review that a large body of evidence suggests probiotics reduce the inflammatory response and oxidative stress, as well as increase the expression of adhesion proteins within the intestinal epithelium, reducing intestinal permeability. Such effects increase insulin sensitivity and reduce autoimmune response. However, further investigations are required to clarify whether the administration of probiotics can be efficiently used for the prevention and management of diabetes.
Appendix
Available only for authorised users
Literature
1.
go back to reference WHO - World Health Organization: World Health Statistics WHO/FAO. 2012, Geneva: WHO WHO - World Health Organization: World Health Statistics WHO/FAO. 2012, Geneva: WHO
2.
go back to reference Cani PD, Daubioul CA, Reusens B, Remacle C, Catillon G, Delzenne NM: Involvement of endogenous glucagon-like peptide-1 amide on glycaemia-lowering effect of oligofructose in streptozotocin-treated rats. J Endocrinol. 2005, 185: 457-465.PubMed Cani PD, Daubioul CA, Reusens B, Remacle C, Catillon G, Delzenne NM: Involvement of endogenous glucagon-like peptide-1 amide on glycaemia-lowering effect of oligofructose in streptozotocin-treated rats. J Endocrinol. 2005, 185: 457-465.PubMed
3.
go back to reference Holmes E, Li JV, Athanasiou T, Ashrafian H, Nicholson JK: Understanding the role of gut microbiome-host metabolic signal disruption in health and disease. Trends Microbiol. 2011, 19: 349-359.PubMed Holmes E, Li JV, Athanasiou T, Ashrafian H, Nicholson JK: Understanding the role of gut microbiome-host metabolic signal disruption in health and disease. Trends Microbiol. 2011, 19: 349-359.PubMed
4.
go back to reference Larsen N, Vogensen FK, Berg FW, Nielsen DS, Andreasen AS, Pedersen BK, Al-Soud WA, Sørensen SJ, Hansen LH, Jakobsen M: Gut microbiota in human adults with type 2 diabetes differs from non-diabetic adults. PLoS One. 2010, 5: e9085-PubMedPubMedCentral Larsen N, Vogensen FK, Berg FW, Nielsen DS, Andreasen AS, Pedersen BK, Al-Soud WA, Sørensen SJ, Hansen LH, Jakobsen M: Gut microbiota in human adults with type 2 diabetes differs from non-diabetic adults. PLoS One. 2010, 5: e9085-PubMedPubMedCentral
5.
go back to reference Cani PD, Bibiloni R, Knauf C, Waget A, Neyrinck AM, Delzenne NM, Burcelin R: Changes in gut microbiota control metabolic endotoxemia-induced inflammation in high-fat diet-induced obesity and diabetes in mice. Diabetes. 2008, 57: 1470-1481.PubMed Cani PD, Bibiloni R, Knauf C, Waget A, Neyrinck AM, Delzenne NM, Burcelin R: Changes in gut microbiota control metabolic endotoxemia-induced inflammation in high-fat diet-induced obesity and diabetes in mice. Diabetes. 2008, 57: 1470-1481.PubMed
6.
go back to reference Secondulfo M, Lafusco D, Carratu R, de Magistris L, Sapone A, Generoso M, Mezzogiomo A, Sasso FC, Cartenì M, De Rosa R, Prisco F, Esposito V: Ultrastructural mucosal alterations and increased intestinal permeability in non-celiac, type I diabetic patients. Dig Liver Dis. 2004, 36: 35-45.PubMed Secondulfo M, Lafusco D, Carratu R, de Magistris L, Sapone A, Generoso M, Mezzogiomo A, Sasso FC, Cartenì M, De Rosa R, Prisco F, Esposito V: Ultrastructural mucosal alterations and increased intestinal permeability in non-celiac, type I diabetic patients. Dig Liver Dis. 2004, 36: 35-45.PubMed
7.
go back to reference Floch MH, Montrose DC: Use of probiotics in humans: an analysis of the literature. Gastroenterol Clin North Am. 2005, 34: 547-570.PubMed Floch MH, Montrose DC: Use of probiotics in humans: an analysis of the literature. Gastroenterol Clin North Am. 2005, 34: 547-570.PubMed
8.
go back to reference Moroti C, Souza Magri LF, Costa MR, Cavallini DC, Sivieri K: 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. 2012, 11: 29-PubMedPubMedCentral Moroti C, Souza Magri LF, Costa MR, Cavallini DC, Sivieri K: 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. 2012, 11: 29-PubMedPubMedCentral
9.
go back to reference Ejtahed HS, Mohtadi-Nia J, Homayouni-Rad A, Niafar M, Asghari-Jafarabadi M, Mofid V: Probiotic yogurt improves antioxidant status in type 2 diabetic patients. Nutrition. 2012, 28: 539-543.PubMed Ejtahed HS, Mohtadi-Nia J, Homayouni-Rad A, Niafar M, Asghari-Jafarabadi M, Mofid V: Probiotic yogurt improves antioxidant status in type 2 diabetic patients. Nutrition. 2012, 28: 539-543.PubMed
10.
go back to reference Andreasen AS, Larsen N, Pedersen-Skovsgaard T, Berg RM, Møller K, Svendsen KD, Jakobsen M, Pedersen BK: Effects of Lactobacillus acidophilus NCFM on insulin sensitivity and the systemic inflammatory response in human subjects. Br J Nut. 2010, 104: 1831-1838. Andreasen AS, Larsen N, Pedersen-Skovsgaard T, Berg RM, Møller K, Svendsen KD, Jakobsen M, Pedersen BK: Effects of Lactobacillus acidophilus NCFM on insulin sensitivity and the systemic inflammatory response in human subjects. Br J Nut. 2010, 104: 1831-1838.
11.
go back to reference Abdul-Ghani MA, Defronzo RA: Pathogenesis of insulin resistance in skeletal muscle. J Biomed Biotechnol. 2010, 2010: 476279-PubMedPubMedCentral Abdul-Ghani MA, Defronzo RA: Pathogenesis of insulin resistance in skeletal muscle. J Biomed Biotechnol. 2010, 2010: 476279-PubMedPubMedCentral
12.
go back to reference Ley RE, Turnbaugh PJ, Klein S, Gordon JI: Microbial ecology: Human gut microbes associated with obesity. Nature. 2006, 444: 1022-1023.PubMed Ley RE, Turnbaugh PJ, Klein S, Gordon JI: Microbial ecology: Human gut microbes associated with obesity. Nature. 2006, 444: 1022-1023.PubMed
13.
go back to reference Mackie RI, Sghir A, Gaskins HR: Developmental microbial ecology of the neonatal gastrointestinal tract. Am J Clin Nutr. 1999, 69: 1035S-1045S.PubMed Mackie RI, Sghir A, Gaskins HR: Developmental microbial ecology of the neonatal gastrointestinal tract. Am J Clin Nutr. 1999, 69: 1035S-1045S.PubMed
14.
go back to reference Zoetendal EG, Rajilic-Stojanovic M, Vos WM: High-throughput diversity and functionality analysis of the gastrointestinal tract microbiota. Gut. 2008, 57: 1605-1615.PubMed Zoetendal EG, Rajilic-Stojanovic M, Vos WM: High-throughput diversity and functionality analysis of the gastrointestinal tract microbiota. Gut. 2008, 57: 1605-1615.PubMed
15.
go back to reference Wells JM, Rossi O, Meijerink M, van Baarlen P: Epithelial crosstalk at the microbiota-mucosal interface. Proc Natl Acad Sci. 2011, 108: 4607-4614.PubMed Wells JM, Rossi O, Meijerink M, van Baarlen P: Epithelial crosstalk at the microbiota-mucosal interface. Proc Natl Acad Sci. 2011, 108: 4607-4614.PubMed
16.
go back to reference De La Serre CB, Ellis CL, Lee J, van Baarlen P: 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. 2010, 299: G440-G448.PubMedPubMedCentral De La Serre CB, Ellis CL, Lee J, van Baarlen P: 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. 2010, 299: G440-G448.PubMedPubMedCentral
17.
go back to reference Kankaanpää PE, Salminen SJ, Isolauri E, Lee YK: The influence of polyunsaturated fatty acids on probiotic growth and adhesion. FEMS Microbiol Lett. 2001, 194: 149-153.PubMed Kankaanpää PE, Salminen SJ, Isolauri E, Lee YK: The influence of polyunsaturated fatty acids on probiotic growth and adhesion. FEMS Microbiol Lett. 2001, 194: 149-153.PubMed
18.
go back to reference Roberfroid MB: Prebiotics: the concept revisited. J Nutr. 2007, 137: 830S-837S.PubMed Roberfroid MB: Prebiotics: the concept revisited. J Nutr. 2007, 137: 830S-837S.PubMed
19.
go back to reference Shoaf K, Mulvey GL, Armstrong GD, Hutkins RW: Prebiotic galactooligosaccharides reduce adherence of enteropathogenic Escherichia coli to tissue culture cells. Infect Immun. 2006, 74: 6920-6928.PubMedPubMedCentral Shoaf K, Mulvey GL, Armstrong GD, Hutkins RW: Prebiotic galactooligosaccharides reduce adherence of enteropathogenic Escherichia coli to tissue culture cells. Infect Immun. 2006, 74: 6920-6928.PubMedPubMedCentral
20.
go back to reference Gee JM, Johnson IT: Polyphenolic compounds: interactions with the gut and implications for human health. Curr Med Chem. 2001, 8: 1245-1255.PubMed Gee JM, Johnson IT: Polyphenolic compounds: interactions with the gut and implications for human health. Curr Med Chem. 2001, 8: 1245-1255.PubMed
21.
go back to reference Serino M, Luche E, Chabo C, Amar J, Burcelin R: Intestinal microflora and metabolic diseases. Diabetes Metab. 2009, 35: 262-272.PubMed Serino M, Luche E, Chabo C, Amar J, Burcelin R: Intestinal microflora and metabolic diseases. Diabetes Metab. 2009, 35: 262-272.PubMed
22.
go back to reference Cani PD, Amar J, Iglesias MA, Poggi M, Knauf C, Bastelica D, Neyrinck AM, Fava F, Tuohy KM, Chabo C, Waget A, Delmée E, Cousin B, Sulpice T, Chamontin B, Ferrières J, Tanti JF, Gibson GR, Casteilla L, Delzenne NM, Alessi MC, Burcelin R: Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes. 2007, 56: 1761-1772.PubMed Cani PD, Amar J, Iglesias MA, Poggi M, Knauf C, Bastelica D, Neyrinck AM, Fava F, Tuohy KM, Chabo C, Waget A, Delmée E, Cousin B, Sulpice T, Chamontin B, Ferrières J, Tanti JF, Gibson GR, Casteilla L, Delzenne NM, Alessi MC, Burcelin R: Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes. 2007, 56: 1761-1772.PubMed
23.
go back to reference Brownleea IA, Knighta J, Dettmarb PW, Pearson JP: Action of reactive oxygen species on colonic mucus secretions. Free Radic Biol Med. 2007, 43: 800-808. Brownleea IA, Knighta J, Dettmarb PW, Pearson JP: Action of reactive oxygen species on colonic mucus secretions. Free Radic Biol Med. 2007, 43: 800-808.
24.
go back to reference Hall DM, Buettner GR, Oberley LW, Xu L, Matthes RD, Gisolfi CV: Mechanisms of circulatory and intestinal barrier dysfunction during whole body hyperthermia. Am J Physiol Heart Circ Physiol. 2001, 280: H509-H521.PubMed Hall DM, Buettner GR, Oberley LW, Xu L, Matthes RD, Gisolfi CV: Mechanisms of circulatory and intestinal barrier dysfunction during whole body hyperthermia. Am J Physiol Heart Circ Physiol. 2001, 280: H509-H521.PubMed
25.
go back to reference Muccioli GG, Naslain D, Bäckhed F, Reigstad CS, Lambert DM, Delzenne NM, Cani PD: The endocannabinoid system links gut microbiota to adipogenesis. Mol Syst Biol. 2010, 6: 392-405.PubMedPubMedCentral Muccioli GG, Naslain D, Bäckhed F, Reigstad CS, Lambert DM, Delzenne NM, Cani PD: The endocannabinoid system links gut microbiota to adipogenesis. Mol Syst Biol. 2010, 6: 392-405.PubMedPubMedCentral
26.
go back to reference Furet JP, Kong LC, Tap J, Poitou C, Basdevant A, Bouillot JL, Mariat D, Corthier G, Doré J, Henegar C, Rizkalla S, Clément K: Differential adaptation of human gut microbiota to bariatric surgery-induced weight loss: links with metabolic and low-grade inflammation markers. Diabetes. 2010, 59: 3049-3057.PubMedPubMedCentral Furet JP, Kong LC, Tap J, Poitou C, Basdevant A, Bouillot JL, Mariat D, Corthier G, Doré J, Henegar C, Rizkalla S, Clément K: Differential adaptation of human gut microbiota to bariatric surgery-induced weight loss: links with metabolic and low-grade inflammation markers. Diabetes. 2010, 59: 3049-3057.PubMedPubMedCentral
27.
go back to reference O’Mahony D, Murphy S, Boileau T, Park J, O'Brien F, Groeger D, Konieczna P, Ziegler M, Scully P, Shanahan F, Kiely B, O'Mahony L: Bifidobacterium animalis AHC7 protects against pathogen-induced NF-kappaB activation in vivo. BMC Immunol. 2010, 11: 63-PubMedPubMedCentral O’Mahony D, Murphy S, Boileau T, Park J, O'Brien F, Groeger D, Konieczna P, Ziegler M, Scully P, Shanahan F, Kiely B, O'Mahony L: Bifidobacterium animalis AHC7 protects against pathogen-induced NF-kappaB activation in vivo. BMC Immunol. 2010, 11: 63-PubMedPubMedCentral
28.
go back to reference Mehta NN, McGillicuddy FC, Anderson PD, Hinkle CC, Shah R, Pruscino L, Tabita-Martinez J, Sellers KF, Rickels MR, Reilly MP: Experimental endotoxemia induces adipose inflammation and insulin resistance in humans. Diabetes. 2010, 59: 172-181.PubMed Mehta NN, McGillicuddy FC, Anderson PD, Hinkle CC, Shah R, Pruscino L, Tabita-Martinez J, Sellers KF, Rickels MR, Reilly MP: Experimental endotoxemia induces adipose inflammation and insulin resistance in humans. Diabetes. 2010, 59: 172-181.PubMed
29.
go back to reference Creely SJ, McTernan PG, Kusminski CM, Fisher FM, Da Silva NF, Khanolkar M, Evans M, Harte AL, Kumar S: Lipopolysaccharide activates an innate immune system response in human adipose tissue in obesity and type 2 diabetes. Am J Physiol Endocrinol Metab. 2007, 292: E740-E747.PubMed Creely SJ, McTernan PG, Kusminski CM, Fisher FM, Da Silva NF, Khanolkar M, Evans M, Harte AL, Kumar S: Lipopolysaccharide activates an innate immune system response in human adipose tissue in obesity and type 2 diabetes. Am J Physiol Endocrinol Metab. 2007, 292: E740-E747.PubMed
30.
go back to reference Dixon AN, Valsamakis G, Hanif MW, Field A, Boutsiadis A, Harte A, McTernan PG, Barnett AH, Kumar S: Effect of the orlistat on serum endotoxin lipopolysaccharide and adipocytokines in South Asian individuals with impaired glucose tolerance. Int J Clin Pract. 2008, 62: 1124-1129.PubMed Dixon AN, Valsamakis G, Hanif MW, Field A, Boutsiadis A, Harte A, McTernan PG, Barnett AH, Kumar S: Effect of the orlistat on serum endotoxin lipopolysaccharide and adipocytokines in South Asian individuals with impaired glucose tolerance. Int J Clin Pract. 2008, 62: 1124-1129.PubMed
31.
go back to reference Al-Attas OS, Al-Daghri NM, Al-Rubeaan K, da Silva NF, Sabico SL, Kumar S, McTernan PG, Harte AL: Changes in endotoxin levels in T2DM subjects on anti-diabetic therapies. Cardiovasc Diabetol. 2009, 8: 20-PubMedPubMedCentral Al-Attas OS, Al-Daghri NM, Al-Rubeaan K, da Silva NF, Sabico SL, Kumar S, McTernan PG, Harte AL: Changes in endotoxin levels in T2DM subjects on anti-diabetic therapies. Cardiovasc Diabetol. 2009, 8: 20-PubMedPubMedCentral
32.
go back to reference Ghanim H, Abuaysheh S, Sia CL, Korzeniewski K, Chaudhuri A, Fernandez-Real JM, Dandona P: Increase in plasma endotoxin concentrations and the expression of Toll-like receptors and suppressor of cytokine signaling-3 in mononuclear cells after a high-fat, high-carbohydrate meal: implications for insulin resistance. Diabetes Care. 2009, 32: 2281-2287.PubMedPubMedCentral Ghanim H, Abuaysheh S, Sia CL, Korzeniewski K, Chaudhuri A, Fernandez-Real JM, Dandona P: Increase in plasma endotoxin concentrations and the expression of Toll-like receptors and suppressor of cytokine signaling-3 in mononuclear cells after a high-fat, high-carbohydrate meal: implications for insulin resistance. Diabetes Care. 2009, 32: 2281-2287.PubMedPubMedCentral
33.
go back to reference Pussinen PJ, Havulinna AS, Lehto M, Sundvall J, Salomaa V: Endotoxemia is associated with an increased risk of incident diabetes. Diabetes Care. 2011, 34: 392-397.PubMedPubMedCentral Pussinen PJ, Havulinna AS, Lehto M, Sundvall J, Salomaa V: Endotoxemia is associated with an increased risk of incident diabetes. Diabetes Care. 2011, 34: 392-397.PubMedPubMedCentral
34.
go back to reference Amar J, Chabo C, Waget A, Klopp P, Vachoux C, Bermúdez-Humarán LG, Smirnova N, Bergé M, Sulpice T, Lahtinen S, Ouwehand A, Langella P, Rautonen N, Sansonetti PJ, Burcelin R: Intestinal mucosal adherence and translocation of commensal bacteria at the early onset of type 2 diabetes: molecular mechanisms and probiotic treatment. EMBO Mol Med. 2011, 3: 559-572.PubMedPubMedCentral Amar J, Chabo C, Waget A, Klopp P, Vachoux C, Bermúdez-Humarán LG, Smirnova N, Bergé M, Sulpice T, Lahtinen S, Ouwehand A, Langella P, Rautonen N, Sansonetti PJ, Burcelin R: Intestinal mucosal adherence and translocation of commensal bacteria at the early onset of type 2 diabetes: molecular mechanisms and probiotic treatment. EMBO Mol Med. 2011, 3: 559-572.PubMedPubMedCentral
35.
go back to reference Amar J, Serino M, Lange C, Chabo C, Iacovoni J, Mondot S, Lepage P, Klopp C, Mariette J, Bouchez O, Perez L, Courtney M, Marre M, Klopp P, Lantieri O, Doré J, Charles M, Balkau B, Burcelin R, D.E.S.I.R. Study Group: Involvement of tissue bacteria in the onset of diabetes in humans: evidence for a concept. Diabetologia. 2011, 54: 3055-3061.PubMed Amar J, Serino M, Lange C, Chabo C, Iacovoni J, Mondot S, Lepage P, Klopp C, Mariette J, Bouchez O, Perez L, Courtney M, Marre M, Klopp P, Lantieri O, Doré J, Charles M, Balkau B, Burcelin R, D.E.S.I.R. Study Group: Involvement of tissue bacteria in the onset of diabetes in humans: evidence for a concept. Diabetologia. 2011, 54: 3055-3061.PubMed
36.
go back to reference Medzhitov R: Origin and physiological roles of inflammation. Nature. 2008, 454: 428-435.PubMed Medzhitov R: Origin and physiological roles of inflammation. Nature. 2008, 454: 428-435.PubMed
37.
go back to reference Hirabara SM, Gorjão R, Vinolo MA, Rodrigues AC, Nachbar RT, Curi R: Molecular targets related to inflammation and insulin resistance and potential interventions. J Biomed Biotechnol. 2012, 2012: 1-16. Hirabara SM, Gorjão R, Vinolo MA, Rodrigues AC, Nachbar RT, Curi R: Molecular targets related to inflammation and insulin resistance and potential interventions. J Biomed Biotechnol. 2012, 2012: 1-16.
38.
go back to reference Cristofaro P, Opal SM: Role of Toll-like receptors in infection and immunity: clinical implications. Drugs. 2006, 66: 15-29.PubMed Cristofaro P, Opal SM: Role of Toll-like receptors in infection and immunity: clinical implications. Drugs. 2006, 66: 15-29.PubMed
39.
go back to reference Kumar H, Kawai T, Akira S: Toll-like receptors and innate immunity. Biochem Biophys Res Commun. 2009, 388: 621-625.PubMed Kumar H, Kawai T, Akira S: Toll-like receptors and innate immunity. Biochem Biophys Res Commun. 2009, 388: 621-625.PubMed
40.
go back to reference Drewe J, Beglinger C, Fricker G: Effect of ischemia on intestinal permeability of lipopolysaccharides. Eur J Clin Invest. 2001, 31: 138-144.PubMed Drewe J, Beglinger C, Fricker G: Effect of ischemia on intestinal permeability of lipopolysaccharides. Eur J Clin Invest. 2001, 31: 138-144.PubMed
41.
go back to reference Neal MD, Leaphart C, Levy R, Prince J, Billiar TR, Watkins S, Li J, Cetin S, Ford H, Schreiber A, Hackam DJ: Enterocyte TLR4 mediates phagocytosis and translocation of bacteria across the intestinal barrier. J Immunol. 2006, 176: 3070-3079.PubMed Neal MD, Leaphart C, Levy R, Prince J, Billiar TR, Watkins S, Li J, Cetin S, Ford H, Schreiber A, Hackam DJ: Enterocyte TLR4 mediates phagocytosis and translocation of bacteria across the intestinal barrier. J Immunol. 2006, 176: 3070-3079.PubMed
42.
go back to reference Spruss A, Kanuri G, Wagnerberger S, Haub S, Bischoff SC, Bergheim I: Toll-like receptor 4 is involved in the development of fructose-induced hepatic steatosis in mice. Hepatology. 2009, 50: 1094-1104.PubMed Spruss A, Kanuri G, Wagnerberger S, Haub S, Bischoff SC, Bergheim I: Toll-like receptor 4 is involved in the development of fructose-induced hepatic steatosis in mice. Hepatology. 2009, 50: 1094-1104.PubMed
43.
go back to reference Cani PD, Delzenne NM: Gut microflora as a target for energy and metabolic homeostasis. Curr Opin Clin Nutr Metab Care. 2007, 10: 729-734.PubMed Cani PD, Delzenne NM: Gut microflora as a target for energy and metabolic homeostasis. Curr Opin Clin Nutr Metab Care. 2007, 10: 729-734.PubMed
44.
go back to reference Akashi-Takamura S, Miyake K: TLR accessory molecules. Curr Opin Immunol. 2008, 20: 420-425.PubMed Akashi-Takamura S, Miyake K: TLR accessory molecules. Curr Opin Immunol. 2008, 20: 420-425.PubMed
45.
go back to reference Sugita H, Kaneki M, Tokunaga E, Sugita M, Koike C, Yasuhara S, Tompkins RG, Martyn JA: Inducible nitric oxide synthase plays a role in LPS-induced hyperglycemia and insulin resistance. Am J Physiol. 2002, 282: E386-E394. Sugita H, Kaneki M, Tokunaga E, Sugita M, Koike C, Yasuhara S, Tompkins RG, Martyn JA: Inducible nitric oxide synthase plays a role in LPS-induced hyperglycemia and insulin resistance. Am J Physiol. 2002, 282: E386-E394.
46.
go back to reference Stamler JS, Toone EJ, Lipton SA, Sucher NJ: (S)NO signals: translocation, regulation, and a consensus motif. Neuron. 1997, 18: 691-696.PubMed Stamler JS, Toone EJ, Lipton SA, Sucher NJ: (S)NO signals: translocation, regulation, and a consensus motif. Neuron. 1997, 18: 691-696.PubMed
47.
go back to reference Shinozaki S, Choi CS, Shimizu N, Yamada M, Kim M, Zhang T, Shiota G, Dong HH, Kim YB, Kaneki M: Liver-specific inducible nitric-oxide synthase expression is sufficient to cause hepatic insulin resistance and mild hyperglycemia in mice. J Biol Chem. 2011, 286: 34959-34975.PubMedPubMedCentral Shinozaki S, Choi CS, Shimizu N, Yamada M, Kim M, Zhang T, Shiota G, Dong HH, Kim YB, Kaneki M: Liver-specific inducible nitric-oxide synthase expression is sufficient to cause hepatic insulin resistance and mild hyperglycemia in mice. J Biol Chem. 2011, 286: 34959-34975.PubMedPubMedCentral
48.
go back to reference Ovadia H, Haim Y, Nov O, Almog O, Kovsan J, Bashan N, Benhar M, Rudich A: Increased adipocyte S-nitrosylation targets anti-lipolytic action of insulin: relevance to adipose tissue dysfunction in obesity. J Biol Chem. 2011, 286: 30433-30443.PubMedPubMedCentral Ovadia H, Haim Y, Nov O, Almog O, Kovsan J, Bashan N, Benhar M, Rudich A: Increased adipocyte S-nitrosylation targets anti-lipolytic action of insulin: relevance to adipose tissue dysfunction in obesity. J Biol Chem. 2011, 286: 30433-30443.PubMedPubMedCentral
50.
go back to reference Konner A, Bruning J: Toll-like receptors: linking inflammation to metabolism. Trends Endocrinol Metab. 2011, 22: 16-23.PubMed Konner A, Bruning J: Toll-like receptors: linking inflammation to metabolism. Trends Endocrinol Metab. 2011, 22: 16-23.PubMed
51.
go back to reference Hiratani K, Haruta T, Tani A, Kawahara J, Usui I, Kobayashi M: Roles of mTOR and JNK in serine phosphorylation, translocation, and degradation of IRS-1. Biochem Biophys Res Commun. 2005, 335: 836-842.PubMed Hiratani K, Haruta T, Tani A, Kawahara J, Usui I, Kobayashi M: Roles of mTOR and JNK in serine phosphorylation, translocation, and degradation of IRS-1. Biochem Biophys Res Commun. 2005, 335: 836-842.PubMed
52.
go back to reference Saltiel AR, Kahn CR: Insulin signalling and the regulation of glucose and lipid metabolism. Nature. 2001, 414: 799-806.PubMed Saltiel AR, Kahn CR: Insulin signalling and the regulation of glucose and lipid metabolism. Nature. 2001, 414: 799-806.PubMed
53.
go back to reference Bluestone JA, Herold K, Eisenbarth G: Genetics, pathogenesis and clinical interventions in type 1 diabetes. Nature. 2010, 464: 1293-1300.PubMed Bluestone JA, Herold K, Eisenbarth G: Genetics, pathogenesis and clinical interventions in type 1 diabetes. Nature. 2010, 464: 1293-1300.PubMed
54.
go back to reference Dabelea DRA, Bell RB, D’Agostino J, Bell RA, D'Agostino RB, Imperatore G, Johansen JM, Linder B, Liu LL, Loots B, Marcovina S, Mayer-Davis EJ, Pettitt DJ, Waitzfelder B: Incidence of diabetes in youth in the United States. JAMA. 2007, 297: 2716-2724.PubMed Dabelea DRA, Bell RB, D’Agostino J, Bell RA, D'Agostino RB, Imperatore G, Johansen JM, Linder B, Liu LL, Loots B, Marcovina S, Mayer-Davis EJ, Pettitt DJ, Waitzfelder B: Incidence of diabetes in youth in the United States. JAMA. 2007, 297: 2716-2724.PubMed
55.
go back to reference Chervonsky AV: Influence of microbial environment on autoimmunity. Nat Immunol. 2010, 11: 28-35.PubMed Chervonsky AV: Influence of microbial environment on autoimmunity. Nat Immunol. 2010, 11: 28-35.PubMed
56.
go back to reference Anderson MS, Bluestone JA: The NOD mouse: a model of immune dysregulation. Annu Rev Immunol. 2005, 23: 447-485.PubMed Anderson MS, Bluestone JA: The NOD mouse: a model of immune dysregulation. Annu Rev Immunol. 2005, 23: 447-485.PubMed
57.
go back to reference Ohland CL, Macnaughton WK: Probiotic bacteria and intestinal epithelial barrier function. Am J Physiol Gastrointest Liver Physiol. 2010, 298: G807-G819.PubMed Ohland CL, Macnaughton WK: Probiotic bacteria and intestinal epithelial barrier function. Am J Physiol Gastrointest Liver Physiol. 2010, 298: G807-G819.PubMed
58.
go back to reference Atkinson MA, Chervonsky A: Does the gut microbiota have a role in type 1 diabetes? Early evidence from humans and animal models of the disease. Diabetologia. 2012, 55: 2868-28677.PubMedPubMedCentral Atkinson MA, Chervonsky A: Does the gut microbiota have a role in type 1 diabetes? Early evidence from humans and animal models of the disease. Diabetologia. 2012, 55: 2868-28677.PubMedPubMedCentral
59.
go back to reference Vehik K, Dabelea D: The changing epidemiology of type 1 diabetes: why is it going through the roof?. Diabetes Metab Res Rev. 2011, 27: 3-13.PubMed Vehik K, Dabelea D: The changing epidemiology of type 1 diabetes: why is it going through the roof?. Diabetes Metab Res Rev. 2011, 27: 3-13.PubMed
60.
go back to reference Neu J, Reverte CM, Mackey AD, Liboni K, Tuhacek-Tenace LM, Hatch M, Li N, Caicedo RA, Schatz DA, Atkinson M: Changes in intestinal morphology and permeability in the biobreeding rat before the onset of type 1 diabetes. J Pediatr Gastroenterol Nutr. 2005, 40: 589-595.PubMed Neu J, Reverte CM, Mackey AD, Liboni K, Tuhacek-Tenace LM, Hatch M, Li N, Caicedo RA, Schatz DA, Atkinson M: Changes in intestinal morphology and permeability in the biobreeding rat before the onset of type 1 diabetes. J Pediatr Gastroenterol Nutr. 2005, 40: 589-595.PubMed
61.
go back to reference Lam YY, Ha CWY, Campbell CR, Mitchell AJ, Dinudom A, Oscarsson J, Cook DI, Hunt NH, Caterson ID, Holmes AJ, Storlien LH: Increased Gut Permeability and Microbiota Change Associate with Mesenteric Fat Inflammation and Metabolic Dysfunction in Diet-Induced Obese Mice. Plos One. 2012, 7: 34233- Lam YY, Ha CWY, Campbell CR, Mitchell AJ, Dinudom A, Oscarsson J, Cook DI, Hunt NH, Caterson ID, Holmes AJ, Storlien LH: Increased Gut Permeability and Microbiota Change Associate with Mesenteric Fat Inflammation and Metabolic Dysfunction in Diet-Induced Obese Mice. Plos One. 2012, 7: 34233-
62.
go back to reference Neu J, Lorca G, Kingma SDK, Triplett EW: The Intestinal Microbiome: Relationship to Type 1. Diabetes. 2010, 39: 563-571. Neu J, Lorca G, Kingma SDK, Triplett EW: The Intestinal Microbiome: Relationship to Type 1. Diabetes. 2010, 39: 563-571.
63.
go back to reference Tiittanen M, Huupponen JT, Knip M, Vaarala O: Insulin treatment in patients with type 1 diabetes induces upregulation of regulatory T-cell markers in peripheral blood mononuclear cells stimulated with insulin in vitro. Diabetes. 2006, 55: 3446-3454.PubMed Tiittanen M, Huupponen JT, Knip M, Vaarala O: Insulin treatment in patients with type 1 diabetes induces upregulation of regulatory T-cell markers in peripheral blood mononuclear cells stimulated with insulin in vitro. Diabetes. 2006, 55: 3446-3454.PubMed
64.
go back to reference Vaarala O, Atkinson M, Neu J: The “perfect storm” for type 1 diabetes: the complex interplay between intestinal microbiota, gut permeability, and mucosal immunity. Diabetes. 2008, 57: 2555-2562.PubMedPubMedCentral Vaarala O, Atkinson M, Neu J: The “perfect storm” for type 1 diabetes: the complex interplay between intestinal microbiota, gut permeability, and mucosal immunity. Diabetes. 2008, 57: 2555-2562.PubMedPubMedCentral
65.
go back to reference Vaarala O, Knip M, Paronen J, Hämäläinen AM, Muona P, Väätäinen M, Ilonen J, Simell O, Akerblom HK: Cow’s milk formula feeding induces primary immunization to insulin in infants at genetic risk for type 1 diabetes. Diabetes. 1999, 48: 1389-1394.PubMed Vaarala O, Knip M, Paronen J, Hämäläinen AM, Muona P, Väätäinen M, Ilonen J, Simell O, Akerblom HK: Cow’s milk formula feeding induces primary immunization to insulin in infants at genetic risk for type 1 diabetes. Diabetes. 1999, 48: 1389-1394.PubMed
66.
go back to reference Proal AD, Albert PJ, Marshall T: Autoimmune disease in the era of the metagenome. Autoimmun Rev. 2009, 8: 677-681.PubMed Proal AD, Albert PJ, Marshall T: Autoimmune disease in the era of the metagenome. Autoimmun Rev. 2009, 8: 677-681.PubMed
67.
go back to reference Murri M, Leiva I, Gomez-Zumaquero JM, Tinahones FJ, Cardona F, Soriguer F, Queipo-Ortuño MI: Gut microbiota in children with type 1 diabetes differs from that in healthy children: a case–control study. BMC Med. 2013, 11: 46-PubMedPubMedCentral Murri M, Leiva I, Gomez-Zumaquero JM, Tinahones FJ, Cardona F, Soriguer F, Queipo-Ortuño MI: Gut microbiota in children with type 1 diabetes differs from that in healthy children: a case–control study. BMC Med. 2013, 11: 46-PubMedPubMedCentral
68.
go back to reference Goffau M, Luopajärvi K, Knip M, Ilonen J, Ruohtula T, Härkönen T, Orivuori L, Hakala S, Welling GW, Harmsen HJ, Vaarala O: Fecal microbiota composition differs between children with beta-cell autoimmunity and those without. Diabetes. 2013, 62: 1238-1244.PubMedPubMedCentral Goffau M, Luopajärvi K, Knip M, Ilonen J, Ruohtula T, Härkönen T, Orivuori L, Hakala S, Welling GW, Harmsen HJ, Vaarala O: Fecal microbiota composition differs between children with beta-cell autoimmunity and those without. Diabetes. 2013, 62: 1238-1244.PubMedPubMedCentral
69.
go back to reference Bosi E, Molteni L, Radaelli MG, Fermo I, Bazzigaluppi E, Piemonti L, Pastore MR, Paroni R: Increased intestinal permeability precedes clinical onset of type 1 diabetes. Diabetologia. 2006, 49: 2824-2827.PubMed Bosi E, Molteni L, Radaelli MG, Fermo I, Bazzigaluppi E, Piemonti L, Pastore MR, Paroni R: Increased intestinal permeability precedes clinical onset of type 1 diabetes. Diabetologia. 2006, 49: 2824-2827.PubMed
70.
go back to reference Brugman S, Klatter FA, Visser JT, Wildeboer-Veloo AC, Harmsen HJ, Rozing J, Bos NA: Antibiotic treatment partially protects against type 1 diabetes in the bio-breeding diabetes-prone rat. Is the gut flora involved in the development of type 1 diabetes?. Diabetologia. 2006, 49: 2105-2108.PubMed Brugman S, Klatter FA, Visser JT, Wildeboer-Veloo AC, Harmsen HJ, Rozing J, Bos NA: Antibiotic treatment partially protects against type 1 diabetes in the bio-breeding diabetes-prone rat. Is the gut flora involved in the development of type 1 diabetes?. Diabetologia. 2006, 49: 2105-2108.PubMed
71.
go back to reference Roesch LFW, Lorca GL, Casella G, Wildeboer-Veloo AC, Harmsen HJ, Rozing J, Bos NA: Culture-independent identification of gut bacteria correlated with the onset of diabetes in a rat model. Isme J. 2009, 3: 536-548.PubMedPubMedCentral Roesch LFW, Lorca GL, Casella G, Wildeboer-Veloo AC, Harmsen HJ, Rozing J, Bos NA: Culture-independent identification of gut bacteria correlated with the onset of diabetes in a rat model. Isme J. 2009, 3: 536-548.PubMedPubMedCentral
72.
go back to reference Cerf-Bensussan N, Gaboriau-Routhiau V: The immune system and the gut microbiota: friends or foes?. Nat Rev Immunol. 2010, 10: 735-744.PubMed Cerf-Bensussan N, Gaboriau-Routhiau V: The immune system and the gut microbiota: friends or foes?. Nat Rev Immunol. 2010, 10: 735-744.PubMed
73.
go back to reference Giongo A, Gano KA, Crabb DB, Mukherjee N, Novelo LL, Casella G, Drew JC, Ilonen J, Knip M, Hyöty H, Veijola R, Simell T, Simell O, Neu J, Wasserfall CH, Schatz D, Atkinson MA, Triplett EW: Toward defining the autoimmune microbiome for type 1 diabetes. ISME J. 2011, 5: 82-91.PubMed Giongo A, Gano KA, Crabb DB, Mukherjee N, Novelo LL, Casella G, Drew JC, Ilonen J, Knip M, Hyöty H, Veijola R, Simell T, Simell O, Neu J, Wasserfall CH, Schatz D, Atkinson MA, Triplett EW: Toward defining the autoimmune microbiome for type 1 diabetes. ISME J. 2011, 5: 82-91.PubMed
74.
go back to reference Brown CT, Davis-Richardson AG, Giongo A, Mukherjee N, Novelo LL, Casella G, Drew JC, Ilonen J, Knip M, Hyöty H, Veijola R, Simell T, Simell O, Neu J, Wasserfall CH, Schatz D, Atkinson MA, Triplett EW: Gut microbiome metagenomics analysis suggests a functional model for the development of autoimmunity for type 1 diabetes. Plos One. 2011, 6: e25792-PubMedPubMedCentral Brown CT, Davis-Richardson AG, Giongo A, Mukherjee N, Novelo LL, Casella G, Drew JC, Ilonen J, Knip M, Hyöty H, Veijola R, Simell T, Simell O, Neu J, Wasserfall CH, Schatz D, Atkinson MA, Triplett EW: Gut microbiome metagenomics analysis suggests a functional model for the development of autoimmunity for type 1 diabetes. Plos One. 2011, 6: e25792-PubMedPubMedCentral
75.
go back to reference Louis P, Flint HJ: Diversity, metabolism and microbial ecology of butyrate-producing bacteria from the human large intestine. Fems Microbiology Letters. 2009, 294: 1-8.PubMed Louis P, Flint HJ: Diversity, metabolism and microbial ecology of butyrate-producing bacteria from the human large intestine. Fems Microbiology Letters. 2009, 294: 1-8.PubMed
76.
go back to reference Lewis K, Lutgendorff F, Phan V, Söderholm JD, Sherman PM, McKay DM: Enhanced Translocation of Bacteria Across Metabolically Stressed Epithelia is Reduced by Butyrate. Inflammatory Bowel Diseases. 2010, 16: 1138-1148.PubMed Lewis K, Lutgendorff F, Phan V, Söderholm JD, Sherman PM, McKay DM: Enhanced Translocation of Bacteria Across Metabolically Stressed Epithelia is Reduced by Butyrate. Inflammatory Bowel Diseases. 2010, 16: 1138-1148.PubMed
77.
go back to reference Paassen BN, Vincent A, Puiman PJ, van der Sluis M, Bouma J, Boehm G, van Goudoever JB, van Seuningen I, Renes IB: The regulation of intestinal mucin MUC2 expression by short-chain fatty acids: implications for epithelial protection. Biochem J. 2009, 420: 211-219. Paassen BN, Vincent A, Puiman PJ, van der Sluis M, Bouma J, Boehm G, van Goudoever JB, van Seuningen I, Renes IB: The regulation of intestinal mucin MUC2 expression by short-chain fatty acids: implications for epithelial protection. Biochem J. 2009, 420: 211-219.
78.
go back to reference Wen L, Ley RE, Volchkov PY, Avanesyan L, Stonebraker AC, Hu C, Wong FS, Szot GL, Bluestone JA, Gordon JI, Chervonsky AV: Innate immunity and intestinal microbiota in the development of type 1 diabetes. Nature. 2008, 455: 1109-1113.PubMedPubMedCentral Wen L, Ley RE, Volchkov PY, Avanesyan L, Stonebraker AC, Hu C, Wong FS, Szot GL, Bluestone JA, Gordon JI, Chervonsky AV: Innate immunity and intestinal microbiota in the development of type 1 diabetes. Nature. 2008, 455: 1109-1113.PubMedPubMedCentral
79.
go back to reference Hara N, Alkanani AK, Ir D, Robertson CE, Wagner BD, Frank DN, Zipris D: Prevention of virus-induced type 1 diabetes with antibiotic therapy. J Immunol. 2012, 15: 3805-3814. Hara N, Alkanani AK, Ir D, Robertson CE, Wagner BD, Frank DN, Zipris D: Prevention of virus-induced type 1 diabetes with antibiotic therapy. J Immunol. 2012, 15: 3805-3814.
80.
go back to reference Thomas HE, McKenzie MD, Angstetra E, Campbell PD, Kay TW: Beta cell apoptosis in diabetes. Apoptosis. 2009, 14: 1389-1404.PubMed Thomas HE, McKenzie MD, Angstetra E, Campbell PD, Kay TW: Beta cell apoptosis in diabetes. Apoptosis. 2009, 14: 1389-1404.PubMed
81.
go back to reference Seewaldt S, Thomas HE, Ejrnaes M, Christen U, Wolfe T, Rodrigo E, Coon B, Michelsen B, Kay TW, von Herrath MG: Virus-induced autoimmune diabetes: most beta-cells die through inflammatory cytokines and not perforin from autoreactive (anti-viral) cytotoxic T-lymphocytes. Diabetes. 2000, 49: 1801-1809.PubMed Seewaldt S, Thomas HE, Ejrnaes M, Christen U, Wolfe T, Rodrigo E, Coon B, Michelsen B, Kay TW, von Herrath MG: Virus-induced autoimmune diabetes: most beta-cells die through inflammatory cytokines and not perforin from autoreactive (anti-viral) cytotoxic T-lymphocytes. Diabetes. 2000, 49: 1801-1809.PubMed
82.
go back to reference Foulis AK, Farquharson MA, Hardman R: Aberrant expression of class II major histocompatibility complex molecules by B cells and hyperexpression of class I major histocompatibility complex molecules by insulin containing islets in type 1 (insulin-dependent) diabetes mellitus. Diabetologia. 1987, 30: 333-343.PubMed Foulis AK, Farquharson MA, Hardman R: Aberrant expression of class II major histocompatibility complex molecules by B cells and hyperexpression of class I major histocompatibility complex molecules by insulin containing islets in type 1 (insulin-dependent) diabetes mellitus. Diabetologia. 1987, 30: 333-343.PubMed
83.
go back to reference Itoh N, Hanafusa T, Miyazaki A, Miyagawa J, Yamagata K, Yamamoto K, Waguri M, Imagawa A, Tamura S, Inada M, Kawata S, Tarui S, Kono N, Matsuzawa Y: Mononuclear cell infiltration and its relation to the expression of major histocompatibility complex antigens and adhesion molecules in pancreas biopsy specimens from newly diagnosed insulin-dependent diabetes mellitus patients. J Clin Invest. 1993, 92: 2313-2322.PubMedPubMedCentral Itoh N, Hanafusa T, Miyazaki A, Miyagawa J, Yamagata K, Yamamoto K, Waguri M, Imagawa A, Tamura S, Inada M, Kawata S, Tarui S, Kono N, Matsuzawa Y: Mononuclear cell infiltration and its relation to the expression of major histocompatibility complex antigens and adhesion molecules in pancreas biopsy specimens from newly diagnosed insulin-dependent diabetes mellitus patients. J Clin Invest. 1993, 92: 2313-2322.PubMedPubMedCentral
84.
go back to reference Round JL, Mazmanian SK: Inducible Foxp3+ regulatory T-cell development by a commensal bacterium of the intestinal microbiota. Proc Natl Acad Sci. 2010, 107: 12204-12209.PubMedPubMedCentral Round JL, Mazmanian SK: Inducible Foxp3+ regulatory T-cell development by a commensal bacterium of the intestinal microbiota. Proc Natl Acad Sci. 2010, 107: 12204-12209.PubMedPubMedCentral
85.
go back to reference Serreze DV, Post CM, Chapman HD, Johnson EA, Lu B, Rothman PB: Interferon-gamma receptor signaling is dispensable in the development of autoimmune type 1 diabetes in NOD mice. Diabetes. 2000, 49: 2007-2011.PubMed Serreze DV, Post CM, Chapman HD, Johnson EA, Lu B, Rothman PB: Interferon-gamma receptor signaling is dispensable in the development of autoimmune type 1 diabetes in NOD mice. Diabetes. 2000, 49: 2007-2011.PubMed
86.
go back to reference Geuking MB, Cahen zli J, Lawson MA: Intestinal bacterial colonization induces mutualistic regulatory T cell responses. Immunity. 2011, 34: 794-806.PubMed Geuking MB, Cahen zli J, Lawson MA: Intestinal bacterial colonization induces mutualistic regulatory T cell responses. Immunity. 2011, 34: 794-806.PubMed
87.
go back to reference Kriegel MA, Sefik E, Hill JA, Wu HJ, Benoist C, Mathis D: Naturally transmitted segmented filamentous bacteria segregate with diabetes protection in nonobese diabetic mice. Proc Natl Acad. 2011, 108: 11548-11553. Kriegel MA, Sefik E, Hill JA, Wu HJ, Benoist C, Mathis D: Naturally transmitted segmented filamentous bacteria segregate with diabetes protection in nonobese diabetic mice. Proc Natl Acad. 2011, 108: 11548-11553.
88.
go back to reference Mazmanian SK, Round JL, Kasper DL: A microbial symbiosis fact or prevents intestinal inflammatory disease. Nature. 2008, 453: 620-625.PubMed Mazmanian SK, Round JL, Kasper DL: A microbial symbiosis fact or prevents intestinal inflammatory disease. Nature. 2008, 453: 620-625.PubMed
90.
go back to reference WHO - World Health Organization: Joint WHO/FAO Expert Consultation on Geneva. Evaluation of Health and Nutritional Properties of Probiotics in Food Including Powder Milk with Live Lactic Acid Bacteria. 2001, Cordoba, Argentina: WHO WHO - World Health Organization: Joint WHO/FAO Expert Consultation on Geneva. Evaluation of Health and Nutritional Properties of Probiotics in Food Including Powder Milk with Live Lactic Acid Bacteria. 2001, Cordoba, Argentina: WHO
91.
go back to reference Gill H, Prasad J: Probiotics, immunomodulation, and health benefits. Adv Exp Med Bio. 2008, 606: 423-454. Gill H, Prasad J: Probiotics, immunomodulation, and health benefits. Adv Exp Med Bio. 2008, 606: 423-454.
92.
go back to reference Prasad J, Gill HS, Smart JB, Gopal PK: Selection and characterization of Lactobacillus and Bifidobacterium strains for use as probiotics. Int Dairy J. 1998, 8: 993-1002. Prasad J, Gill HS, Smart JB, Gopal PK: Selection and characterization of Lactobacillus and Bifidobacterium strains for use as probiotics. Int Dairy J. 1998, 8: 993-1002.
93.
go back to reference Hummel S, Veltman K, Cichon C, Sonnenborn U, Schmidt MA: Differential Targeting of the E-Cadherin/β-Catenin Complex by Gram-Positive Probiotic Lactobacilli Improves Epithelial Barrier Function. Appl Environ Microbiol. 2012, 78: 1140-1147.PubMedPubMedCentral Hummel S, Veltman K, Cichon C, Sonnenborn U, Schmidt MA: Differential Targeting of the E-Cadherin/β-Catenin Complex by Gram-Positive Probiotic Lactobacilli Improves Epithelial Barrier Function. Appl Environ Microbiol. 2012, 78: 1140-1147.PubMedPubMedCentral
94.
go back to reference Singh R, Lei P, Andreadis ST: PKC-δ binds to E-cadherin and mediates EGF-induced cell scattering. Exp Cell Res. 2009, 315: 2899-2913.PubMed Singh R, Lei P, Andreadis ST: PKC-δ binds to E-cadherin and mediates EGF-induced cell scattering. Exp Cell Res. 2009, 315: 2899-2913.PubMed
95.
go back to reference Gooding JM, Yap KL, Ikura M: The cadherin-catenin complex as a focal point of cell adhesion and signalling: new insights from three-dimensional structures. BioEssays. 2004, 26: 497-511.PubMed Gooding JM, Yap KL, Ikura M: The cadherin-catenin complex as a focal point of cell adhesion and signalling: new insights from three-dimensional structures. BioEssays. 2004, 26: 497-511.PubMed
96.
go back to reference Kingma SDK, Li N, Sun F, Valladares RB, Neu J, Lorca GL: Lactobacillus johnsonii N6.2 Stimulates the Innate Immune Response through Toll-Like Receptor 9 in Caco-2 Cells and Increases Intestinal Crypt Paneth Cell Number in BioBreeding Diabetes-Prone Rats. J Nutr. 2011, 141: 1023-1028.PubMed Kingma SDK, Li N, Sun F, Valladares RB, Neu J, Lorca GL: Lactobacillus johnsonii N6.2 Stimulates the Innate Immune Response through Toll-Like Receptor 9 in Caco-2 Cells and Increases Intestinal Crypt Paneth Cell Number in BioBreeding Diabetes-Prone Rats. J Nutr. 2011, 141: 1023-1028.PubMed
97.
go back to reference Jabri B, Ebert E: Human CD8+ intraepithelial lymphocytes: a unique model to study the regulation of effector cytotoxic T lymphocytes in tissue. Immunol Rev. 2007, 215: 202-214.PubMed Jabri B, Ebert E: Human CD8+ intraepithelial lymphocytes: a unique model to study the regulation of effector cytotoxic T lymphocytes in tissue. Immunol Rev. 2007, 215: 202-214.PubMed
98.
go back to reference Valladares R, Sankar D, Li N, Williams E, Lai KK, Abdelgeliel AS, Gonzalez CF, Wasserfall CH, Larkin J, Schatz D, Atkinson MA, Triplett EW, Neu J, Lorca GL: Lactobacillus johnsonii N6.2 Mitigates the Development of Type 1 Diabetes in BB-DP Rats. Plos One. 2010, 5: e10507-PubMedPubMedCentral Valladares R, Sankar D, Li N, Williams E, Lai KK, Abdelgeliel AS, Gonzalez CF, Wasserfall CH, Larkin J, Schatz D, Atkinson MA, Triplett EW, Neu J, Lorca GL: Lactobacillus johnsonii N6.2 Mitigates the Development of Type 1 Diabetes in BB-DP Rats. Plos One. 2010, 5: e10507-PubMedPubMedCentral
99.
go back to reference Lau K, Benitez P, Ardissone A, Wilson TD, Collins EL, Lorca G, Li N, Sankar D, Wasserfall C, Neu J, Atkinson MA, Shatz D, Triplett EW, Larkin J: Inhibition of Type 1 Diabetes Correlated to a Lactobacillus johnsonii N6.2-Mediated Th17 Bias. J Immunol. 2011, 186: 3538-3546.PubMed Lau K, Benitez P, Ardissone A, Wilson TD, Collins EL, Lorca G, Li N, Sankar D, Wasserfall C, Neu J, Atkinson MA, Shatz D, Triplett EW, Larkin J: Inhibition of Type 1 Diabetes Correlated to a Lactobacillus johnsonii N6.2-Mediated Th17 Bias. J Immunol. 2011, 186: 3538-3546.PubMed
100.
go back to reference Ivanov II, Frutos Rde L, Manel N, Yoshinaga K, Rifkin DB, Sartor RB, Finlay BB, Littman DR: Specific microbiota direct the differentiation of IL-17-producing T-helper cells in the mucosa of the small intestine. Cell Host Microbe. 2008, 4: 337-349.PubMedPubMedCentral Ivanov II, Frutos Rde L, Manel N, Yoshinaga K, Rifkin DB, Sartor RB, Finlay BB, Littman DR: Specific microbiota direct the differentiation of IL-17-producing T-helper cells in the mucosa of the small intestine. Cell Host Microbe. 2008, 4: 337-349.PubMedPubMedCentral
101.
go back to reference Martin-Orozco N, Chung Y, Chang SH, Wang YH, Dong C: Th17 cells promote pancreatic inflammation but only induce diabetes efficiently in lymphopenic hosts after conversion into Th1 cells. Eur J Immunol. 2009, 39: 216-224.PubMedPubMedCentral Martin-Orozco N, Chung Y, Chang SH, Wang YH, Dong C: Th17 cells promote pancreatic inflammation but only induce diabetes efficiently in lymphopenic hosts after conversion into Th1 cells. Eur J Immunol. 2009, 39: 216-224.PubMedPubMedCentral
102.
go back to reference Yadav H, Jain S, Sinha PR: Antidiabetic effect of probiotic dahi containing Lactobacillus acidophilus and Lactobacillus casei in high fructose fed rats. Nutrition. 2007, 23: 62-68.PubMed Yadav H, Jain S, Sinha PR: Antidiabetic effect of probiotic dahi containing Lactobacillus acidophilus and Lactobacillus casei in high fructose fed rats. Nutrition. 2007, 23: 62-68.PubMed
103.
go back to reference Andersson U, Bränning C, Ahrné S, Molin G, Alenfall J, Onning G, Nyman M, Holm C: Probiotics lower plasma glucose in the high-fat fed C57BL/6J mouse. Benef Microbes. 2010, 1: 189-196.PubMed Andersson U, Bränning C, Ahrné S, Molin G, Alenfall J, Onning G, Nyman M, Holm C: Probiotics lower plasma glucose in the high-fat fed C57BL/6J mouse. Benef Microbes. 2010, 1: 189-196.PubMed
104.
go back to reference Mencarelli A, Cipriani S, Renga B, Bruno A, D'Amore C, Distrutti E, Fiorucci S: VSL#3 Resets Insulin Signaling and Protects against NASH and Atherosclerosis in a Model of Genetic Dyslipidemia and Intestinal Inflammation. Plos One. 2012, 7: e45425-PubMedPubMedCentral Mencarelli A, Cipriani S, Renga B, Bruno A, D'Amore C, Distrutti E, Fiorucci S: VSL#3 Resets Insulin Signaling and Protects against NASH and Atherosclerosis in a Model of Genetic Dyslipidemia and Intestinal Inflammation. Plos One. 2012, 7: e45425-PubMedPubMedCentral
105.
go back to reference Ma X, Hua J, Li Z: Probiotics improve high fat diet-induced hepatic steatosis and insulin resistance by increasing hepatic NKT cells. J Hepatol. 2008, 49: 821-830.PubMedPubMedCentral Ma X, Hua J, Li Z: Probiotics improve high fat diet-induced hepatic steatosis and insulin resistance by increasing hepatic NKT cells. J Hepatol. 2008, 49: 821-830.PubMedPubMedCentral
106.
go back to reference Calcinaro F, Dionisi S, Marinaro M, Candeloro P, Bonato V, Marzotti S, Corneli RB, Ferretti E, Gulino A, Grasso F, De Simone C, Di Mario U, Falorni A, Boirivant M, Dotta F: Oral probiotic administration induces interleukin-10 production and prevents spontaneous autoimmune diabetes in the non-obese diabetic mouse. Diabetologia. 2005, 48: 1565-1575.PubMed Calcinaro F, Dionisi S, Marinaro M, Candeloro P, Bonato V, Marzotti S, Corneli RB, Ferretti E, Gulino A, Grasso F, De Simone C, Di Mario U, Falorni A, Boirivant M, Dotta F: Oral probiotic administration induces interleukin-10 production and prevents spontaneous autoimmune diabetes in the non-obese diabetic mouse. Diabetologia. 2005, 48: 1565-1575.PubMed
107.
go back to reference Moore KW, de Waal MR, Coffman RL, O'Garra A: Interleukin-10 and the interleukin-10 receptor. Annu Rev Immunol. 2001, 19: 683-765.PubMed Moore KW, de Waal MR, Coffman RL, O'Garra A: Interleukin-10 and the interleukin-10 receptor. Annu Rev Immunol. 2001, 19: 683-765.PubMed
108.
go back to reference Ohkawara S, Furuya H, Nagashima K, Asanuma N, Hino T: Oral administration of butyrivibrio fibrisolvens, a butyrate-producing bacterium, decreases the formation of aberrant crypt foci in the colon and rectum of mice. J Nutr. 2005, 135: 2878-2883.PubMed Ohkawara S, Furuya H, Nagashima K, Asanuma N, Hino T: Oral administration of butyrivibrio fibrisolvens, a butyrate-producing bacterium, decreases the formation of aberrant crypt foci in the colon and rectum of mice. J Nutr. 2005, 135: 2878-2883.PubMed
109.
go back to reference Yadav H, Jain S, Sinha PR: The Effect of Probiotic Dahi Containing Lactobacillus acidophilus and Lactobacillus casei on Gastropathic Consequences in Diabetic Rats. J Med Food. 2008, 11: 62-68.PubMed Yadav H, Jain S, Sinha PR: The Effect of Probiotic Dahi Containing Lactobacillus acidophilus and Lactobacillus casei on Gastropathic Consequences in Diabetic Rats. J Med Food. 2008, 11: 62-68.PubMed
110.
go back to reference Yadav H, Jain S, Sinha PR: Oral administration of dahi containing probiotic Lactobacillus acidophilus and Lactobacillus casei delayed the progression of streptozotocin-induced diabetes in rats. J Dairy Res. 2008, 75: 189-195.PubMed Yadav H, Jain S, Sinha PR: Oral administration of dahi containing probiotic Lactobacillus acidophilus and Lactobacillus casei delayed the progression of streptozotocin-induced diabetes in rats. J Dairy Res. 2008, 75: 189-195.PubMed
111.
go back to reference Lu YC, Yin LT, Chang WT, Huang JS: Effect of Lactobacillus reuteri GMNL-263 treatment on renal fibrosis in diabetic rats. J Biosci Bioeng. 2010, 110: 709-715.PubMed Lu YC, Yin LT, Chang WT, Huang JS: Effect of Lactobacillus reuteri GMNL-263 treatment on renal fibrosis in diabetic rats. J Biosci Bioeng. 2010, 110: 709-715.PubMed
112.
go back to reference Chen J, Wang R, Li XF, Wang RL: Bifidobacterium adolescentis supplementation ameliorates visceral fat accumulation and insulin sensitivity in an experimental model of the metabolic syndrome. Br J Nutr. 2012, 10: 1429-1434. Chen J, Wang R, Li XF, Wang RL: Bifidobacterium adolescentis supplementation ameliorates visceral fat accumulation and insulin sensitivity in an experimental model of the metabolic syndrome. Br J Nutr. 2012, 10: 1429-1434.
113.
go back to reference Drucker DJ: Glucagon-like peptides: regulators of cell proliferation, differentiation, and apoptosis. Mol Endocrinol Rev. 2003, 17: 161-171. Drucker DJ: Glucagon-like peptides: regulators of cell proliferation, differentiation, and apoptosis. Mol Endocrinol Rev. 2003, 17: 161-171.
114.
go back to reference Lee SK, Yang KM, Cheon JH, Kim TI, Kim WH: Anti-inflammatory mechanism of Lactobacillus rhamnosus GG in lipopolysaccharide- stimulated HT-29 cell. Korean J Gastroenterol. 2012, 60: 86-93.PubMed Lee SK, Yang KM, Cheon JH, Kim TI, Kim WH: Anti-inflammatory mechanism of Lactobacillus rhamnosus GG in lipopolysaccharide- stimulated HT-29 cell. Korean J Gastroenterol. 2012, 60: 86-93.PubMed
115.
go back to reference Cani PD, Delzenne NM: The role of the gut microbiota in energy metabolism and metabolic disease. Curr Pharm Des. 2009, 15: 1546-1558.PubMed Cani PD, Delzenne NM: The role of the gut microbiota in energy metabolism and metabolic disease. Curr Pharm Des. 2009, 15: 1546-1558.PubMed
116.
go back to reference Marik E: Colonic flora, Probiotics, Obesity and Diabetes. Front Endocrinol. 2012, 3: 87- Marik E: Colonic flora, Probiotics, Obesity and Diabetes. Front Endocrinol. 2012, 3: 87-
117.
go back to reference Luoto R, Laitinen K, Nermes M, Isolauri E: Impact of maternal probiotic-supplemented dietary counselling on pregnancy outcome and prenatal and postnatal growth: a double-blind, placebo-controlled study. Br J Nutr. 2010, 103: 1792-1799.PubMed Luoto R, Laitinen K, Nermes M, Isolauri E: Impact of maternal probiotic-supplemented dietary counselling on pregnancy outcome and prenatal and postnatal growth: a double-blind, placebo-controlled study. Br J Nutr. 2010, 103: 1792-1799.PubMed
118.
go back to reference Laitinen K, Poussa T, Isolauri E: Probiotics and dietary counselling contribute to glucose regulation during and after pregnancy: a randomised controlled trial. Br J Nutr. 2009, 101: 1679-1687.PubMed Laitinen K, Poussa T, Isolauri E: Probiotics and dietary counselling contribute to glucose regulation during and after pregnancy: a randomised controlled trial. Br J Nutr. 2009, 101: 1679-1687.PubMed
119.
go back to reference Karczewski J, Troost FJ, Konings I, Dekker J, Kleerebezem M, Brummer RJ, Wells JM: 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. 2010, 298: G851-G859.PubMed Karczewski J, Troost FJ, Konings I, Dekker J, Kleerebezem M, Brummer RJ, Wells JM: 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. 2010, 298: G851-G859.PubMed
120.
go back to reference Walsh-Reitz MM, Huang EF, Musch MW, Chang EB, Martin TE, Kartha S, Toback FG: AMP-18 protects barrier function of colonic epithelial cells: role of tight junction proteins. Am J Physiol Gastrointest Liver Physiol. 2005, 289: G163-G171.PubMedPubMedCentral Walsh-Reitz MM, Huang EF, Musch MW, Chang EB, Martin TE, Kartha S, Toback FG: AMP-18 protects barrier function of colonic epithelial cells: role of tight junction proteins. Am J Physiol Gastrointest Liver Physiol. 2005, 289: G163-G171.PubMedPubMedCentral
121.
go back to reference Mikelsaar M, Zilmer M: Lactobacillus fermentum ME-3—an antimicrobial and antioxidative probiotic. Microb Ecol Health Dis. 2009, 21: 1-27.PubMedPubMedCentral Mikelsaar M, Zilmer M: Lactobacillus fermentum ME-3—an antimicrobial and antioxidative probiotic. Microb Ecol Health Dis. 2009, 21: 1-27.PubMedPubMedCentral
Metadata
Title
Gut microbiota, probiotics and diabetes
Authors
Aline Corado Gomes
Allain Amador Bueno
Rávila Graziany Machado de Souza
João Felipe Mota
Publication date
01-12-2014
Publisher
BioMed Central
Published in
Nutrition Journal / Issue 1/2014
Electronic ISSN: 1475-2891
DOI
https://doi.org/10.1186/1475-2891-13-60

Other articles of this Issue 1/2014

Nutrition Journal 1/2014 Go to the issue
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discuss last year's major advances in heart failure and cardiomyopathies.