Probiotics and Prebiotics for the Amelioration of Type 1 Diabetes: Present and Future Perspectives

Sidharth Prasad Mishra, Shaohua Wang, Ravinder Nagpal, Brandi Miller, Ria Singh, Subhash Taraphder, Hariom Yadav, Sidharth Prasad Mishra, Shaohua Wang, Ravinder Nagpal, Brandi Miller, Ria Singh, Subhash Taraphder, Hariom Yadav

Abstract

Type 1-diabetes (T1D) is an autoimmune disease characterized by immune-mediated destruction of pancreatic beta (β)-cells. Genetic and environmental interactions play an important role in immune system malfunction by priming an aggressive adaptive immune response against β-cells. The microbes inhabiting the human intestine closely interact with the enteric mucosal immune system. Gut microbiota colonization and immune system maturation occur in parallel during early years of life; hence, perturbations in the gut microbiota can impair the functions of immune cells and vice-versa. Abnormal gut microbiota perturbations (dysbiosis) are often detected in T1D subjects, particularly those diagnosed as multiple-autoantibody-positive as a result of an aggressive and adverse immunoresponse. The pathogenesis of T1D involves activation of self-reactive T-cells, resulting in the destruction of β-cells by CD8⁺ T-lymphocytes. It is also becoming clear that gut microbes interact closely with T-cells. The amelioration of gut dysbiosis using specific probiotics and prebiotics has been found to be associated with decline in the autoimmune response (with diminished inflammation) and gut integrity (through increased expression of tight-junction proteins in the intestinal epithelium). This review discusses the potential interactions between gut microbiota and immune mechanisms that are involved in the progression of T1D and contemplates the potential effects and prospects of gut microbiota modulators, including probiotic and prebiotic interventions, in the amelioration of T1D pathology, in both human and animal models.

Keywords: autoimmune; diabetes; diet; fiber; gut; microbiota; microflora; prebiotics; probiotics.

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1
Figure 1
Factors influencing the susceptibility of T1D. Abbreviations: HLA: Human leukocyte antigen; T1D: Type 1-Diabetes.
Figure 2
Figure 2
Mechanisms involved in the pathogenesis of T1D. APC: Antigen presenting cell; DCs: Dendritic cells; GALT: Gut Associated Lymphoid Tissue; MHC: Major Histocompatibility Complex; CD 8+ T-Cell: Cytotoxic T lymphocytes; CD4+ T-Cells: Helper T lymphocytes; T1D: Type-1-Diabetes.
Figure 3
Figure 3
Schematic representations of mechanisms of actions through which specific probiotic strains might help in the amelioration of T1D. Akt: protein kinase B; DCs: Dendritic cells; GLP-1: Glucagon-like peptide-1; NF-κB: Nuclear factor kappa-light-chain-enhancer of activated B-cells; IκBα: I kappa B kinase; IkkB: IκB kinase beta; IgA: Immunoglobulin A; Treg: T regulatory cell; Th2: T-helper cell 2.
Figure 4
Figure 4
Purported mechanism(s) of action through which prebiotics could manipulate gut microbiota as well as immune cells of T1D pathology. Akt: protein kinase B; DC: dendritic cell; GLP-1: glucagon-like peptide-1; GLP-2: glucagon-like peptide-2; IkkB: IκB kinase beta; IκBα: I kappa B kinase; NF-κB: Nuclear factor kappa-light-chain-enhancer of activated B-cells; SCFAs: short chain fatty acids; Th2: T-helper cell 2; Treg: T regulatory cell.

References

    1. Lamichhane S., Ahonen L., Dyrlund T.S., Siljander H., Hyoty H., Ilonen J., Toppari J., Veijola R., Hyotylainen T., Knip M., et al. A longitudinal plasma lipidomics dataset from children who developed islet autoimmunity and type 1 diabetes. Sci. Data. 2018;5:180250. doi: 10.1038/sdata.2018.250.
    1. Patterson C.C., Harjutsalo V., Rosenbauer J., Neu A., Cinek O., Skrivarhaug T., Rami-Merhar B., Soltesz G., Svensson J., Parslow R.C., et al. Trends and cyclical variation in the incidence of childhood type 1 diabetes in 26 European centres in the 25 year period 1989–2013: A multicentre prospective registration study. Diabetologia. 2018 doi: 10.1007/s00125-018-4763-3.
    1. Rewers M., Hyoty H., Lernmark A., Hagopian W., She J.X., Schatz D., Ziegler A.G., Toppari J., Akolkar B., Krischer J., et al. The Environmental Determinants of Diabetes in the Young (TEDDY) Study: 2018 Update. Curr. Diabetes Rep. 2018;18:136. doi: 10.1007/s11892-018-1113-2.
    1. Battaglia M., Atkinson M.A. The streetlight effect in type 1 diabetes. Diabetes. 2015;64:1081–1090. doi: 10.2337/db14-1208.
    1. Pociot F., Lernmark A. Genetic risk factors for type 1 diabetes. Lancet. 2016;387:2331–2339. doi: 10.1016/S0140-6736(16)30582-7.
    1. Rewers M., Ludvigsson J. Environmental risk factors for type 1 diabetes. Lancet. 2016;387:2340–2348. doi: 10.1016/S0140-6736(16)30507-4.
    1. Knip M., Simell O. Environmental triggers of type 1 diabetes. Cold Spring Harb. Perspect. Med. 2012;2:a007690. doi: 10.1101/cshperspect.a007690.
    1. Vatanen T., Franzosa E.A., Schwager R., Tripathi S., Arthur T.D., Vehik K., Lernmark A., Hagopian W.A., Rewers M.J., She J.X., et al. The human gut microbiome in early-onset type 1 diabetes from the TEDDY study. Nature. 2018;562:589–594. doi: 10.1038/s41586-018-0620-2.
    1. Jandhyala S.M., Talukdar R., Subramanyam C., Vuyyuru H., Sasikala M., Nageshwar Reddy D. Role of the normal gut microbiota. World J. Gastroenterol. 2015;21:8787–8803. doi: 10.3748/wjg.v21.i29.8787.
    1. Han H., Li Y., Fang J., Liu G., Yin J., Li T., Yin Y. Gut Microbiota and Type 1 Diabetes. Int. J. Mol. Sci. 2018;19:995. doi: 10.3390/ijms19040995.
    1. Schwiertz A., Taras D., Schafer K., Beijer S., Bos N.A., Donus C., Hardt P.D. Microbiota and SCFA in lean and overweight healthy subjects. Obesity (Silver Spring) 2010;18:190–195. doi: 10.1038/oby.2009.167.
    1. Moya-Perez A., Luczynski P., Renes I.B., Wang S., Borre Y., Anthony Ryan C., Knol J., Stanton C., Dinan T.G., Cryan J.F. Intervention strategies for cesarean section-induced alterations in the microbiota-gut-brain axis. Nutr. Rev. 2017;75:225–240. doi: 10.1093/nutrit/nuw069.
    1. Nagpal R., Tsuji H., Takahashi T., Kawashima K., Nagata S., Nomoto K., Yamashiro Y. Sensitive Quantitative Analysis of the Meconium Bacterial Microbiota in Healthy Term Infants Born Vaginally or by Cesarean Section. Front. Microbiol. 2016;7:1997. doi: 10.3389/fmicb.2016.01997.
    1. Nagpal R., Kurakawa T., Tsuji H., Takahashi T., Kawashima K., Nagata S., Nomoto K., Yamashiro Y. Evolution of gut Bifidobacterium population in healthy Japanese infants over the first three years of life: A quantitative assessment. Sci. Rep. 2017;7:10097. doi: 10.1038/s41598-017-10711-5.
    1. Nagpal R., Tsuji H., Takahashi T., Nomoto K., Kawashima K., Nagata S., Yamashiro Y. Gut dysbiosis following C-section instigates higher colonisation of toxigenic Clostridium perfringens in infants. Benef. Microbes. 2017;8:353–365. doi: 10.3920/BM2016.0216.
    1. Aw W., Fukuda S. Understanding the role of the gut ecosystem in diabetes mellitus. J. Diabetes Investig. 2018;9:5–12. doi: 10.1111/jdi.12673.
    1. Xie Z., Huang G., Wang Z., Luo S., Zheng P., Zhou Z. Epigenetic regulation of Toll-like receptors and its roles in type 1 diabetes. J. Mol. Med. 2018 doi: 10.1007/s00109-018-1660-7.
    1. Kim Y.K., Shin J.S., Nahm M.H. NOD-Like Receptors in Infection, Immunity, and Diseases. Yonsei Med. J. 2016;57:5–14. doi: 10.3349/ymj.2016.57.1.5.
    1. Priyadarshini M., Navarro G., Layden B.T. Gut Microbiota: FFAR Reaching Effects on Islets. Endocrinology. 2018;159:2495–2505. doi: 10.1210/en.2018-00296.
    1. Ang Z., Ding J.L. GPR41 and GPR43 in Obesity and Inflammation—Protective or Causative? Front. Immunol. 2016;7:28. doi: 10.3389/fimmu.2016.00028.
    1. Knip M., Honkanen J. Modulation of Type 1 Diabetes Risk by the Intestinal Microbiome. Curr. Diabetes Rep. 2017;17:105. doi: 10.1007/s11892-017-0933-9.
    1. Hill C., Guarner F., Reid G., Gibson G.R., Merenstein D.J., Pot B., Morelli L., Canani R.B., Flint H.J., Salminen S., et al. Expert consensus document. The International Scientific Association for Probiotics and Prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nat. Rev. Gastroenterol. Hepatol. 2014;11:506–514. doi: 10.1038/nrgastro.2014.66.
    1. Gibson G.R., Hutkins R., Sanders M.E., Prescott S.L., Reimer R.A., Salminen S.J., Scott K., Stanton C., Swanson K.S., Cani P.D., et al. Expert consensus document: The International Scientific Association for Probiotics and Prebiotics (ISAPP) consensus statement on the definition and scope of prebiotics. Nat. Rev. Gastroenterol. Hepatol. 2017;14:491–502. doi: 10.1038/nrgastro.2017.75.
    1. Zheng P., Li Z., Zhou Z. Gut microbiome in type 1 diabetes: A comprehensive review. Diabetes Metab. Res. Rev. 2018;34:e3043. doi: 10.1002/dmrr.3043.
    1. Yoo J.Y., Kim S.S. Probiotics and Prebiotics: Present Status and Future Perspectives on Metabolic Disorders. Nutrients. 2016;8:173. doi: 10.3390/nu8030173.
    1. Drexhage H.A., Dik W.A., Leenen P.J., Versnel M.A. The Immune Pathogenesis of Type 1 Diabetes: Not Only Thinking Outside the Cell but Also Outside the Islet and Out of the Box. Diabetes. 2016;65:2130–2133. doi: 10.2337/dbi16-0030.
    1. Pushalkar S., Hundeyin M., Daley D., Zambirinis C.P., Kurz E., Mishra A., Mohan N., Aykut B., Usyk M., Torres L.E., et al. The Pancreatic Cancer Microbiome Promotes Oncogenesis by Induction of Innate and Adaptive Immune Suppression. Cancer Discov. 2018;8:403–416. doi: 10.1158/-17-1134.
    1. Paschou S.A., Papadopoulou-Marketou N., Chrousos G.P., Kanaka-Gantenbein C. On type 1 diabetes mellitus pathogenesis. Endocr. Connect. 2018;7:R38–R46. doi: 10.1530/EC-17-0347.
    1. Campbell-Thompson M., Fu A., Kaddis J.S., Wasserfall C., Schatz D.A., Pugliese A., Atkinson M.A. Insulitis and beta-Cell Mass in the Natural History of Type 1 Diabetes. Diabetes. 2016;65:719–731. doi: 10.2337/db15-0779.
    1. Clark M., Kroger C.J., Tisch R.M. Type 1 Diabetes: A Chronic Anti-Self-Inflammatory Response. Front. Immunol. 2017;8:1898. doi: 10.3389/fimmu.2017.01898.
    1. Burrack A.L., Martinov T., Fife B.T. T Cell-Mediated Beta Cell Destruction: Autoimmunity and Alloimmunity in the Context of Type 1 Diabetes. Front. Endocrinol. (Lausanne) 2017;8:343. doi: 10.3389/fendo.2017.00343.
    1. Cheung S.S., Ou D., Metzger D.L., Meloche M., Ao Z., Ng S.S., Owen D., Warnock G.L. B7-H4 expression in normal and diseased human islet beta cells. Pancreas. 2014;43:128–134. doi: 10.1097/MPA.0b013e31829695d2.
    1. Xiao L., Van’t Land B., van de Worp W., Stahl B., Folkerts G., Garssen J. Early-Life Nutritional Factors and Mucosal Immunity in the Development of Autoimmune Diabetes. Front. Immunol. 2017;8:1219. doi: 10.3389/fimmu.2017.01219.
    1. Winer D.A., Winer S., Dranse H.J., Lam T.K. Immunologic impact of the intestine in metabolic disease. J. Clin. Investig. 2017;127:33–42. doi: 10.1172/JCI88879.
    1. Li B., Selmi C., Tang R., Gershwin M.E., Ma X. The microbiome and autoimmunity: A paradigm from the gut-liver axis. Cell. Mol. Immunol. 2018;15:595–609. doi: 10.1038/cmi.2018.7.
    1. Jung C., Hugot J.P., Barreau F. Peyer’s Patches: The Immune Sensors of the Intestine. Int. J. Inflam. 2010;2010:823710. doi: 10.4061/2010/823710.
    1. Ermund A., Gustafsson J.K., Hansson G.C., Keita A.V. Mucus properties and goblet cell quantification in mouse, rat and human ileal Peyer’s patches. PLoS ONE. 2013;8:e83688. doi: 10.1371/journal.pone.0083688.
    1. Markov A.G., Falchuk E.L., Kruglova N.M., Radloff J., Amasheh S. Claudin expression in follicle-associated epithelium of rat Peyer’s patches defines a major restriction of the paracellular pathway. Acta Physiol. 2016;216:112–119. doi: 10.1111/apha.12559.
    1. Costa F.R., Francozo M.C., de Oliveira G.G., Ignacio A., Castoldi A., Zamboni D.S., Ramos S.G., Camara N.O., de Zoete M.R., Palm N.W., et al. Gut microbiota translocation to the pancreatic lymph nodes triggers NOD2 activation and contributes to T1D onset. J. Exp. Med. 2016;213:1223–1239. doi: 10.1084/jem.20150744.
    1. Pabst O., Mowat A.M. Oral tolerance to food protein. Mucosal Immunol. 2012;5:232–239. doi: 10.1038/mi.2012.4.
    1. Winer D.A., Luck H., Tsai S., Winer S. The Intestinal Immune System in Obesity and Insulin Resistance. Cell Metab. 2016;23:413–426. doi: 10.1016/j.cmet.2016.01.003.
    1. Maffeis C., Martina A., Corradi M., Quarella S., Nori N., Torriani S., Plebani M., Contreas G., Felis G.E. Association between intestinal permeability and faecal microbiota composition in Italian children with beta cell autoimmunity at risk for type 1 diabetes. Diabetes Metab. Res. Rev. 2016;32:700–709. doi: 10.1002/dmrr.2790.
    1. Shi G., Sun C., Gu W., Yang M., Zhang X., Zhai N., Lu Y., Zhang Z., Shou P., Zhang Z., et al. Free fatty acid receptor 2, a candidate target for type 1 diabetes, induces cell apoptosis through ERK signaling. J. Mol. Endocrinol. 2014;53:367–380. doi: 10.1530/JME-14-0065.
    1. Wen L., Ley R.E., Volchkov P.Y., Stranges P.B., Avanesyan L., Stonebraker A.C., Hu C., Wong F.S., Szot G.L., Bluestone J.A., et al. Innate immunity and intestinal microbiota in the development of Type 1 diabetes. Nature. 2008;455:1109–1113. doi: 10.1038/nature07336.
    1. Scott N.A., Andrusaite A., Andersen P., Lawson M., Alcon-Giner C., Leclaire C., Caim S., Le Gall G., Shaw T., Connolly J.P.R., et al. Antibiotics induce sustained dysregulation of intestinal T cell immunity by perturbing macrophage homeostasis. Sci. Transl. Med. 2018;10 doi: 10.1126/scitranslmed.aao4755.
    1. Tanca A., Palomba A., Fraumene C., Manghina V., Silverman M., Uzzau S. Clostridial Butyrate Biosynthesis Enzymes Are Significantly Depleted in the Gut Microbiota of Nonobese Diabetic Mice. mSphere. 2018;3 doi: 10.1128/mSphere.00492-18.
    1. Karumuthil-Melethil S., Sofi M.H., Gudi R., Johnson B.M., Perez N., Vasu C. TLR2- and Dectin 1-associated innate immune response modulates T-cell response to pancreatic beta-cell antigen and prevents type 1 diabetes. Diabetes. 2015;64:1341–1357. doi: 10.2337/db14-1145.
    1. Devaraj S., Dasu M.R., Rockwood J., Winter W., Griffen S.C., Jialal I. Increased toll-like receptor (TLR) 2 and TLR4 expression in monocytes from patients with type 1 diabetes: Further evidence of a proinflammatory state. J. Clin. Endocrinol. Metab. 2008;93:578–583. doi: 10.1210/jc.2007-2185.
    1. Shibasaki S., Imagawa A., Tauriainen S., Iino M., Oikarinen M., Abiru H., Tamaki K., Seino H., Nishi K., Takase I., et al. Expression of toll-like receptors in the pancreas of recent-onset fulminant type 1 diabetes. Endocr. J. 2010;57:211–219. doi: 10.1507/endocrj.K09E-291.
    1. Zipris D., Lien E., Xie J.X., Greiner D.L., Mordes J.P., Rossini A.A. TLR Activation Synergizes with Kilham Rat Virus Infection to Induce Diabetes in BBDR Rats. J. Immunol. 2004;174:131–142. doi: 10.4049/jimmunol.174.1.131.
    1. Assmann T.S., Brondani Lde A., Boucas A.P., Canani L.H., Crispim D. Toll-like receptor 3 (TLR3) and the development of type 1 diabetes mellitus. Arch. Endocrinol. Metab. 2015;59:4–12. doi: 10.1590/2359-3997000000003.
    1. Tan J.K., McKenzie C., Marino E., Macia L., Mackay C.R. Metabolite-Sensing G Protein-Coupled Receptors-Facilitators of Diet-Related Immune Regulation. Annu. Rev. Immunol. 2017;35:371–402. doi: 10.1146/annurev-immunol-051116-052235.
    1. Zhang X.S., Li J., Krautkramer K.A., Badri M., Battaglia T., Borbet T.C., Koh H., Ng S., Sibley R.A., Li Y., et al. Antibiotic-induced acceleration of type 1 diabetes alters maturation of innate intestinal immunity. eLife. 2018;7 doi: 10.7554/eLife.37816.
    1. Brown A.J., Goldsworthy S.M., Barnes A.A., Eilert M.M., Tcheang L., Daniels D., Muir A.I., Wigglesworth M.J., Kinghorn I., Fraser N.J., et al. The Orphan G protein-coupled receptors GPR41 and GPR43 are activated by propionate and other short chain carboxylic acids. J. Biol. Chem. 2003;278:11312–11319. doi: 10.1074/jbc.M211609200.
    1. Bhutia Y.D., Ganapathy V. Short, but Smart: SCFAs Train T Cells in the Gut to Fight Autoimmunity in the Brain. Immunity. 2015;43:629–631. doi: 10.1016/j.immuni.2015.09.014.
    1. Sun J., Furio L., Mecheri R., van der Does A.M., Lundeberg E., Saveanu L., Chen Y., van Endert P., Agerberth B., Diana J. Pancreatic beta-Cells Limit Autoimmune Diabetes via an Immunoregulatory Antimicrobial Peptide Expressed under the Influence of the Gut Microbiota. Immunity. 2015;43:304–317. doi: 10.1016/j.immuni.2015.07.013.
    1. Ohira H., Tsutsui W., Fujioka Y. Are Short Chain Fatty Acids in Gut Microbiota Defensive Players for Inflammation and Atherosclerosis? J. Atheroscler. Thromb. 2017;24:660–672. doi: 10.5551/jat.RV17006.
    1. Galderisi A., Pirillo P., Moret V., Stocchero M., Gucciardi A., Perilongo G., Moretti C., Monciotti C., Giordano G., Baraldi E. Metabolomics reveals new metabolic perturbations in children with type 1 diabetes. Pediatr. Diabetes. 2018;19:59–67. doi: 10.1111/pedi.12524.
    1. Paun A., Yau C., Danska J.S. The Influence of the Microbiome on Type 1 Diabetes. J. Immunol. 2017;198:590–595. doi: 10.4049/jimmunol.1601519.
    1. Lin L., Zhang J. Role of intestinal microbiota and metabolites on gut homeostasis and human diseases. BMC Immunol. 2017;18:2. doi: 10.1186/s12865-016-0187-3.
    1. Chen Y.G., Mathews C.E., Driver J.P. The Role of NOD Mice in Type 1 Diabetes Research: Lessons from the Past and Recommendations for the Future. Front. Endocrinol. (Lausanne) 2018;9:51. doi: 10.3389/fendo.2018.00051.
    1. Abdelazez A., Abdelmotaal H., Evivie S.E., Melak S., Jia F.F., Khoso M.H., Zhu Z.T., Zhang L.J., Sami R., Meng X.C. Screening Potential Probiotic Characteristics of Lactobacillus brevis Strains In Vitro and Intervention Effect on Type I Diabetes In Vivo. Biomed. Res. Int. 2018;2018:7356173. doi: 10.1155/2018/7356173.
    1. Yadav R., Khan S.H., Mada S.B., Meena S., Kapila R., Kapila S. Consumption of Probiotic Lactobacillus fermentum MTCC: 5898-Fermented Milk Attenuates Dyslipidemia, Oxidative Stress, and Inflammation in Male Rats Fed on Cholesterol-Enriched Diet. Probiotics Antimicrob. Proteins. 2018 doi: 10.1007/s12602-018-9429-4.
    1. Raafat K., Wurglics M., Schubert-Zsilavecz M. Prunella vulgaris L. active components and their hypoglycemic and antinociceptive effects in alloxan-induced diabetic mice. Biomed. Pharmacother. 2016;84:1008–1018. doi: 10.1016/j.biopha.2016.09.095.
    1. Lau K., Benitez P., Ardissone A., Wilson T.D., Collins E.L., Lorca G., Li N., Sankar D., Wasserfall C., Neu J., et al. Inhibition of type 1 diabetes correlated to a Lactobacillus johnsonii N6.2-mediated Th17 bias. J. Immunol. 2011;186:3538–3546. doi: 10.4049/jimmunol.1001864.
    1. Sarmiento J., Wallis R.H., Ning T., Marandi L., Chao G., Veillette A., Lernmark A., Paterson A.D., Poussier P. A functional polymorphism of Ptpn22 is associated with type 1 diabetes in the BioBreeding rat. J. Immunol. 2015;194:615–629. doi: 10.4049/jimmunol.1302689.
    1. de Oliveira G.L.V., Leite A.Z., Higuchi B.S., Gonzaga M.I., Mariano V.S. Intestinal dysbiosis and probiotic applications in autoimmune diseases. Immunology. 2017;152:1–12. doi: 10.1111/imm.12765.
    1. Nagpal R., Wang S., Ahmadi S., Hayes J., Gagliano J., Subashchandrabose S., Kitzman D.W., Becton T., Read R., Yadav H. Human-origin probiotic cocktail increases short-chain fatty acid production via modulation of mice and human gut microbiome. Sci. Rep. 2018;8:12649. doi: 10.1038/s41598-018-30114-4.
    1. Marino E., Richards J.L., McLeod K.H., Stanley D., Yap Y.A., Knight J., McKenzie C., Kranich J., Oliveira A.C., Rossello F.J., et al. Gut microbial metabolites limit the frequency of autoimmune T cells and protect against type 1 diabetes. Nat. Immunol. 2017;18:552–562. doi: 10.1038/ni.3713.
    1. Psichas A., Sleeth M.L., Murphy K.G., Brooks L., Bewick G.A., Hanyaloglu A.C., Ghatei M.A., Bloom S.R., Frost G. The short chain fatty acid propionate stimulates GLP-1 and PYY secretion via free fatty acid receptor 2 in rodents. Int. J. Obes. (London) 2015;39:424–429. doi: 10.1038/ijo.2014.153.
    1. Christiansen C.B., Gabe M.B.N., Svendsen B., Dragsted L.O., Rosenkilde M.M., Holst J.J. The impact of short-chain fatty acids on GLP-1 and PYY secretion from the isolated perfused rat colon. Am. J. Physiol. Gastrointest. Liver Physiol. 2018;315:G53–G65. doi: 10.1152/ajpgi.00346.2017.
    1. Le T.K., Hosaka T., Nguyen T.T., Kassu A., Dang T.O., Tran H.B., Pham T.P., Tran Q.B., Le T.H., Pham X.D. Bifidobacterium species lower serum glucose, increase expressions of insulin signaling proteins, and improve adipokine profile in diabetic mice. Biomed. Res. 2015;36:63–70. doi: 10.2220/biomedres.36.63.
    1. Dolpady J., Sorini C., Di Pietro C., Cosorich I., Ferrarese R., Saita D., Clementi M., Canducci F., Falcone M. Oral Probiotic VSL#3 Prevents Autoimmune Diabetes by Modulating Microbiota and Promoting Indoleamine 2,3-Dioxygenase-Enriched Tolerogenic Intestinal Environment. J. Diabetes Res. 2016;2016:7569431. doi: 10.1155/2016/7569431.
    1. Zhang J., Motyl K.J., Irwin R., MacDougald O.A., Britton R.A., McCabe L.R. Loss of Bone and Wnt10b Expression in Male Type 1 Diabetic Mice Is Blocked by the Probiotic Lactobacillus reuteri. Endocrinology. 2015;156:3169–3182. doi: 10.1210/EN.2015-1308.
    1. Mauvais F.X., Diana J., van Endert P. Beta cell antigens in type 1 diabetes: Triggers in pathogenesis and therapeutic targets. F1000Res. 2016;5 doi: 10.12688/f1000research.7411.1.
    1. Takiishi T., Korf H., Van Belle T.L., Robert S., Grieco F.A., Caluwaerts S., Galleri L., Spagnuolo I., Steidler L., Van Huynegem K., et al. Reversal of autoimmune diabetes by restoration of antigen-specific tolerance using genetically modified Lactococcus lactis in mice. J. Clin. Investig. 2012;122:1717–1725. doi: 10.1172/JCI60530.
    1. Pearson J.A., Wong F.S., Wen L. The importance of the Non Obese Diabetic (NOD) mouse model in autoimmune diabetes. J. Autoimmun. 2016;66:76–88. doi: 10.1016/j.jaut.2015.08.019.
    1. Wei S.-H., Chen Y.-P., Chen M.-J. Selecting probiotics with the abilities of enhancing GLP-1 to mitigate the progression of type 1 diabetes in vitro and in vivo. J. Funct. Foods. 2015;18:473–486. doi: 10.1016/j.jff.2015.08.016.
    1. Calcinaro F., Dionisi S., Marinaro M., Candeloro P., Bonato V., Marzotti S., Corneli R.B., Ferretti E., Gulino A., Grasso F., et al. Oral probiotic administration induces interleukin-10 production and prevents spontaneous autoimmune diabetes in the non-obese diabetic mouse. Diabetologia. 2005;48:1565–1575. doi: 10.1007/s00125-005-1831-2.
    1. Blankenhorn E.P., Cort L., Greiner D.L., Guberski D.L., Mordes J.P. Virus-induced autoimmune diabetes in the LEW.1WR1 rat requires Iddm14 and a genetic locus proximal to the major histocompatibility complex. Diabetes. 2009;58:2930–2938. doi: 10.2337/db09-0387.
    1. Alkanani A.K., Hara N., Gianani R., Zipris D. Kilham Rat Virus-induced type 1 diabetes involves beta cell infection and intra-islet JAK-STAT activation prior to insulitis. Virology. 2014;468-470:19–27. doi: 10.1016/j.virol.2014.07.041.
    1. Valladares R., Sankar D., Li N., Williams E., Lai K.K., Abdelgeliel A.S., Gonzalez C.F., Wasserfall C.H., Larkin J., Schatz D., et al. Lactobacillus johnsonii N6.2 mitigates the development of type 1 diabetes in BB-DP rats. PLoS ONE. 2010;5:e10507. doi: 10.1371/journal.pone.0010507.
    1. Yadav R., Dey D.K., Vij R., Meena S., Kapila R., Kapila S. Evaluation of anti-diabetic attributes of Lactobacillus rhamnosus MTCC: 5957, Lactobacillus rhamnosus MTCC: 5897 and Lactobacillus fermentum MTCC: 5898 in streptozotocin induced diabetic rats. Microb. Pathog. 2018;125:454–462. doi: 10.1016/j.micpath.2018.10.015.
    1. Bejar W., Hamden K., Ben Salah R., Chouayekh H. Lactobacillus plantarum TN627 significantly reduces complications of alloxan-induced diabetes in rats. Anaerobe. 2013;24:4–11. doi: 10.1016/j.anaerobe.2013.08.006.
    1. Uusitalo U., Liu X., Yang J., Aronsson C.A., Hummel S., Butterworth M., Lernmark A., Rewers M., Hagopian W., She J.X., et al. Association of Early Exposure of Probiotics and Islet Autoimmunity in the TEDDY Study. JAMA Pediatr. 2016;170:20–28. doi: 10.1001/jamapediatrics.2015.2757.
    1. Marcial G.E., Ford A.L., Haller M.J., Gezan S.A., Harrison N.A., Cai D., Meyer J.L., Perry D.J., Atkinson M.A., Wasserfall C.H., et al. Lactobacillus johnsonii N6.2 Modulates the Host Immune Responses: A Double-Blind, Randomized Trial in Healthy Adults. Front. Immunol. 2017;8:655. doi: 10.3389/fimmu.2017.00655.
    1. Weir G.C., Bonner-Weir S. Dreams for Type 1 Diabetes: Shutting Off Autoimmunity and Stimulating β-Cell Regeneration. Endocrinology. 2010;151:2971–2973. doi: 10.1210/en.2010-0538.
    1. Yadav H., Lee J.-H., Lloyd J., Walter P., Rane S.G. Beneficial Metabolic Effects of a Probiotic via Butyrate-induced GLP-1 Hormone Secretion. J. Biol. Chem. 2013;288:25088–25097. doi: 10.1074/jbc.M113.452516.
    1. Burrows M.P., Volchkov P., Kobayashi K.S., Chervonsky A.V. Microbiota regulates type 1 diabetes through Toll-like receptors. Proc. Natl. Acad. Sci. USA. 2015;112:9973–9977. doi: 10.1073/pnas.1508740112.
    1. Groele L., Szajewska H., Szypowska A. Effects of Lactobacillus rhamnosus GG and Bifidobacterium lactis Bb12 on beta-cell function in children with newly diagnosed type 1 diabetes: Protocol of a randomised controlled trial. BMJ Open. 2017;7:e017178. doi: 10.1136/bmjopen-2017-017178.
    1. Ahola A.J., Harjutsalo V., Forsblom C., Freese R., Makimattila S., Groop P.H. The Self-reported Use of Probiotics is Associated with Better Glycaemic Control and Lower Odds of Metabolic Syndrome and its Components in Type 1 Diabetes. J. Probiotics Health. 2017;05 doi: 10.4172/2329-8901.1000188.
    1. Yang J., Tamura R.N., Uusitalo U.M., Aronsson C.A., Silvis K., Riikonen A., Frank N., Joslowski G., Winkler C., Norris J.M., et al. Vitamin D and probiotics supplement use in young children with genetic risk for type 1 diabetes. Eur. J. Clin. Nutr. 2017;71:1449–1454. doi: 10.1038/ejcn.2017.140.
    1. Carlson J.L., Erickson J.M., Lloyd B.B., Slavin J.L. Health Effects and Sources of Prebiotic Dietary Fiber. Curr. Dev. Nutr. 2018;2:nzy005. doi: 10.1093/cdn/nzy005.
    1. Wilson B., Whelan K. Prebiotic inulin-type fructans and galacto-oligosaccharides: Definition, specificity, function, and application in gastrointestinal disorders. J. Gastroenterol. Hepatol. 2017;32(Suppl. 1):64–68. doi: 10.1111/jgh.13700.
    1. Shokryazdan P., Faseleh Jahromi M., Navidshad B., Liang J.B. Effects of prebiotics on immune system and cytokine expression. Med. Microbiol. Immunol. 2017;206:1–9. doi: 10.1007/s00430-016-0481-y.
    1. Kaji I., Karaki S., Tanaka R., Kuwahara A. Density distribution of free fatty acid receptor 2 (FFA2)-expressing and GLP-1-producing enteroendocrine L cells in human and rat lower intestine, and increased cell numbers after ingestion of fructo-oligosaccharide. J. Mol. Histol. 2011;42:27–38. doi: 10.1007/s10735-010-9304-4.
    1. den Besten G., van Eunen K., Groen A.K., Venema K., Reijngoud D.J., Bakker B.M. The role of short-chain fatty acids in the interplay between diet, gut microbiota, and host energy metabolism. J. Lipid Res. 2013;54:2325–2340. doi: 10.1194/jlr.R036012.
    1. Fukuda S., Toh H., Hase K., Oshima K., Nakanishi Y., Yoshimura K., Tobe T., Clarke J.M., Topping D.L., Suzuki T., et al. Bifidobacteria can protect from enteropathogenic infection through production of acetate. Nature. 2011;469:543–547. doi: 10.1038/nature09646.
    1. Chen K., Chen H., Faas M.M., de Haan B.J., Li J., Xiao P., Zhang H., Diana J., de Vos P., Sun J. Specific inulin-type fructan fibers protect against autoimmune diabetes by modulating gut immunity, barrier function, and microbiota homeostasis. Mol. Nutr. Food Res. 2017;61 doi: 10.1002/mnfr.201601006.
    1. Woting A., Pfeiffer N., Hanske L., Loh G., Klaus S., Blaut M. Alleviation of high fat diet-induced obesity by oligofructose in gnotobiotic mice is independent of presence of Bifidobacterium longum. Mol. Nutr. Food Res. 2015;59:2267–2278. doi: 10.1002/mnfr.201500249.
    1. Cani P.D., Neyrinck A.M., Fava F., Knauf C., Burcelin R.G., Tuohy K.M., Gibson G.R., Delzenne N.M. Selective increases of bifidobacteria in gut microflora improve high-fat-diet-induced diabetes in mice through a mechanism associated with endotoxaemia. Diabetologia. 2007;50:2374–2383. doi: 10.1007/s00125-007-0791-0.
    1. Xiao L., Van’t Land B., Engen P.A., Naqib A., Green S.J., Nato A., Leusink-Muis T., Garssen J., Keshavarzian A., Stahl B., et al. Human milk oligosaccharides protect against the development of autoimmune diabetes in NOD-mice. Sci. Rep. 2018;8:3829. doi: 10.1038/s41598-018-22052-y.
    1. Bach Knudsen K.E., Laerke H.N., Hedemann M.S., Nielsen T.S., Ingerslev A.K., Gundelund Nielsen D.S., Theil P.K., Purup S., Hald S., Schioldan A.G., et al. Impact of Diet-Modulated Butyrate Production on Intestinal Barrier Function and Inflammation. Nutrients. 2018;10:1499. doi: 10.3390/nu10101499.
    1. Koh G.Y., Rowling M.J., Schalinske K.L., Grapentine K., Loo Y.T. Consumption of Dietary Resistant Starch Partially Corrected the Growth Pattern Despite Hyperglycemia and Compromised Kidney Function in Streptozotocin-Induced Diabetic Rats. J. Agric. Food Chem. 2016;64:7540–7545. doi: 10.1021/acs.jafc.6b03808.
    1. Crookshank J.A., Patrick C., Wang G.S., Noel J.A., Scott F.W. Gut immune deficits in LEW.1AR1-iddm rats partially overcome by feeding a diabetes-protective diet. Immunology. 2015;145:417–428. doi: 10.1111/imm.12457.
    1. Gorelick J., Yarmolinsky L., Budovsky A., Khalfin B., Klein J.D., Pinchasov Y., Bushuev M.A., Rudchenko T., Ben-Shabat S. The Impact of Diet Wheat Source on the Onset of Type 1 Diabetes Mellitus-Lessons Learned from the Non-Obese Diabetic (NOD) Mouse Model. Nutrients. 2017;9:482. doi: 10.3390/nu9050482.
    1. Stenman L.K., Waget A., Garret C., Briand F., Burcelin R., Sulpice T., Lahtinen S. Probiotic B420 and prebiotic polydextrose improve efficacy of antidiabetic drugs in mice. Diabetol. Metab. Syndr. 2015;7:75. doi: 10.1186/s13098-015-0075-7.
    1. Prud’homme G.J., Glinka Y., Kurt M., Liu W., Wang Q. The anti-aging protein Klotho is induced by GABA therapy and exerts protective and stimulatory effects on pancreatic beta cells. Biochem. Biophys. Res. Commun. 2017;493:1542–1547. doi: 10.1016/j.bbrc.2017.10.029.
    1. Ho J., Reimer R.A., Doulla M., Huang C. Effect of prebiotic intake on gut microbiota, intestinal permeability and glycemic control in children with type 1 diabetes: Study protocol for a randomized controlled trial. Trials. 2016;17:347. doi: 10.1186/s13063-016-1486-y.
    1. Beretta M.V., Bernaud F.R., Nascimento C., Steemburgo T., Rodrigues T.C. Higher fiber intake is associated with lower blood pressure levels in patients with type 1 diabetes. Arch. Endocrinol. Metab. 2018;62:47–54. doi: 10.20945/2359-3997000000008.
    1. Bernaud F.S., Beretta M.V., do Nascimento C., Escobar F., Gross J.L., Azevedo M.J., Rodrigues T.C. Fiber intake and inflammation in type 1 diabetes. Diabetol. Metab. Syndr. 2014;6:66. doi: 10.1186/1758-5996-6-66.
    1. Biester T., Aschemeier B., Fath M., Frey M., Scheerer M.F., Kordonouri O., Danne T. Effects of dapagliflozin on insulin-requirement, glucose excretion and ss-hydroxybutyrate levels are not related to baseline HbA1c in youth with type 1 diabetes. Diabetes Obes. Metab. 2017;19:1635–1639. doi: 10.1111/dom.12975.
    1. Singh R.K., Chang H.W., Yan D., Lee K.M., Ucmak D., Wong K., Abrouk M., Farahnik B., Nakamura M., Zhu T.H., et al. Influence of diet on the gut microbiome and implications for human health. J. Transl. Med. 2017;15:73. doi: 10.1186/s12967-017-1175-y.
    1. Uusitalo U., Lee H.S., Andren Aronsson C., Vehik K., Yang J., Hummel S., Silvis K., Lernmark A., Rewers M., Hagopian W., et al. Early Infant Diet and Islet Autoimmunity in the TEDDY Study. Diabetes Care. 2018;41:522–530. doi: 10.2337/dc17-1983.
    1. Falony G., Lazidou K., Verschaeren A., Weckx S., Maes D., De Vuyst L. In vitro kinetic analysis of fermentation of prebiotic inulin-type fructans by Bifidobacterium species reveals four different phenotypes. Appl. Environ. Microbiol. 2009;75:454–461. doi: 10.1128/AEM.01488-08.
    1. Brugman S., Ikeda-Ohtsubo W., Braber S., Folkerts G., Pieterse C.M.J., Bakker P. A Comparative Review on Microbiota Manipulation: Lessons From Fish, Plants, Livestock, and Human Research. Front. Nutr. 2018;5:80. doi: 10.3389/fnut.2018.00080.
    1. Lund-Blix N.A., Dydensborg Sander S., Stordal K., Nybo Andersen A.M., Ronningen K.S., Joner G., Skrivarhaug T., Njolstad P.R., Husby S., Stene L.C. Infant Feeding and Risk of Type 1 Diabetes in Two Large Scandinavian Birth Cohorts. Diabetes Care. 2017;40:920–927. doi: 10.2337/dc17-0016.
    1. Niinisto S., Takkinen H.M., Erlund I., Ahonen S., Toppari J., Ilonen J., Veijola R., Knip M., Vaarala O., Virtanen S.M. Fatty acid status in infancy is associated with the risk of type 1 diabetes-associated autoimmunity. Diabetologia. 2017;60:1223–1233. doi: 10.1007/s00125-017-4280-9.
    1. Lamb M.M., Miller M., Seifert J.A., Frederiksen B., Kroehl M., Rewers M., Norris J.M. The effect of childhood cow’s milk intake and HLA-DR genotype on risk of islet autoimmunity and type 1 diabetes: The Diabetes Autoimmunity Study in the Young. Pediatr. Diabetes. 2015;16:31–38. doi: 10.1111/pedi.12115.
    1. Takeshima S., Matsumoto Y., Chen J., Yoshida T., Mukoyama H., Aida Y. Evidence for cattle major histocompatibility complex (BoLA) class II DQA1 gene heterozygote advantage against clinical mastitis caused by Streptococci and Escherichia species. Tissue Antigens. 2008;72:525–531. doi: 10.1111/j.1399-0039.2008.01140.x.
    1. Hanninen A., Toivonen R., Poysti S., Belzer C., Plovier H., Ouwerkerk J.P., Emani R., Cani P.D., De Vos W.M. Akkermansia muciniphila induces gut microbiota remodelling and controls islet autoimmunity in NOD mice. Gut. 2018;67:1445–1453. doi: 10.1136/gutjnl-2017-314508.
    1. Weir G.C., Bonner-Weir S. GABA Signaling Stimulates beta Cell Regeneration in Diabetic Mice. Cell. 2017;168:7–9. doi: 10.1016/j.cell.2016.12.006.
    1. Kanikarla-Marie P., Jain S.K. Hyperketonemia (acetoacetate) upregulates NADPH oxidase 4 and elevates oxidative stress, ICAM-1, and monocyte adhesivity in endothelial cells. Cell. Physiol. Biochem. 2015;35:364–373. doi: 10.1159/000369702.

Source: PubMed

Patrocinadores y Colaboradores

Condiciones médicas

Intervenciones de drogas

3
Suscribir