Influence of GABA and GABA-producing Lactobacillus brevis DPC 6108 on the development of diabetes in a streptozotocin rat model

Beneficial Microbes

Volumn 7, Issue 3, 2016, Pages 409-420

  Marques, T M ^a,b,c   Patterson, E ^a,b,c   Wall, R ^a,b   O'Sullivan, O ^a,b   Fitzgerald, G F ^a,c   Cotter, P D ^a,b   Dinan, T G ^a,c   Cryan, J F ^a   Ross, R P ^a   Stanton, C ^a,b  

^a UNIVERSITY COLLEGE CORK   (Ireland)

^b TEAGASC FOOD RESEARCH CENTRE   (Ireland)

^c UNIVERSITY COLLEGE CORK   (Ireland)

Author keywords

Probiotic; Streptozotocin; Type 1 diabetes; aminobutyric acid

Indexed keywords

4 AMINOBUTYRIC ACID; C PEPTIDE; CHOLESTEROL; GASTRIC INHIBITORY POLYPEPTIDE; GLUCAGON LIKE PEPTIDE 1; GLUCOSE; INSULIN; LEPTIN; PEPTIDE YY; PROBIOTIC AGENT; TRIACYLGLYCEROL; ANTIDIABETIC AGENT; ANTINEOPLASTIC ANTIBIOTIC; PLACEBO;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL STRAIN; CONTROLLED STUDY; DIET SUPPLEMENTATION; FECES ANALYSIS; GLUCOSE BLOOD LEVEL; HYPERGLYCEMIA; INSULIN BLOOD LEVEL; INSULIN DEPENDENT DIABETES MELLITUS; INTESTINE FLORA; LACTOBACILLUS BREVIS; MALE; MICROBIAL DIVERSITY; NONHUMAN; RAT; SPECIES COMPOSITION; STREPTOZOTOCIN-INDUCED DIABETES MELLITUS; THERAPY EFFECT; WEIGHT REDUCTION; ANIMAL; DIABETES MELLITUS, EXPERIMENTAL; METABOLISM; SPRAGUE DAWLEY RAT; TREATMENT OUTCOME;

ANIMALS; ANTIBIOTICS, ANTINEOPLASTIC; DIABETES MELLITUS, EXPERIMENTAL; GAMMA-AMINOBUTYRIC ACID; HYPOGLYCEMIC AGENTS; LACTOBACILLUS BREVIS; PLACEBOS; PROBIOTICS; RATS, SPRAGUE-DAWLEY; TREATMENT OUTCOME;

EID: 84971645676     PISSN: 18762883     EISSN: 18762891     Source Type: Journal    
DOI: 10.3920/BM2015.0154     Document Type: Article

References (53)

1. Adeghate, E. and Ponery, A.S., 2002. GABA in the endocrine pancreas:cellular localization and function in normal and diabetic rats. Tissue Cell 34: 1-6.
2. Altschul, S.F., Gish, W., Miller, W., Myers, E.W. and Lipman, D.J., 1990. Basic local alignment search tool. Journal of Molecular Biology 215: 403-410.
3. Atkinson, M.A. and Eisenbarth, G.S., 2001. Type 1 diabetes: new perspectives on disease pathogenesis and treatment. The Lancet 358: 221-229.
4. Bailey, S.J., Ravier, M.A. and Rutter, G.A., 2007. Glucose-dependent regulation of gamma-aminobutyric acid (GABA A) receptor expression in mouse pancreatic islet alpha-cells. Diabetes 56:320-327.
5. Bansal, P., Wang, S., Liu, S., Xiang, Y.Y., Lu, W.Y. and Wang, Q., 2011. GABA coordinates with insulin in regulating secretory function in pancreatic INS-1 beta-cells. PLoS One 6: e26225.
6. Barrett, E., Ross, R.P., O'Toole, P.W., Fitzgerald, G.F. and Stanton, C., 2012. gamma-Aminobutyric acid production by culturable bacteria from the human intestine. Journal of Applied Microbiology 113:411-417.
7. Bonaventura, M.M., Catalano, P.N., Chamson-Reig, A., Arany, E., Hill, D., Bettler, B., Saravia, F., Libertun, C. and Lux-Lantos, V.A., 2008. GABAB receptors and glucose homeostasis: evaluation in GABAB receptor knockout mice. American Journal of Physiology - Endocrinology and Metabolism 294: E157-E167.
8. Brown, C.T., Davis-Richardson, A.G., Giongo, A., Gano, K.A., Crabb, D.B., Mukherjee, N., Casella, G., Drew, J.C., Ilonen, J., Knip, M., Hyoty, H., Veijola, R., Simell, T., Simell, O., Neu, J., Wasserfall, C.H., Schatz, D., Atkinson, M.A. and Triplett, E.W., 2011. Gut microbiome metagenomics analysis suggests a functional model for the development of autoimmunity for type 1 diabetes. PLoS ONE 6: e25792.
9. Cani, P.D., 2012. Crosstalk between the gut microbiota and the endocannabinoid system: impact on the gut barrier function and the adipose tissue. Clinical Microbiology and Infection 18: 50-53.
10. Caporaso, J.G., Bittinger, K., Bushman, F.D., DeSantis, T.Z., Andersen, G.L. and Knight, R., 2010a. PyNAST: a flexible tool for aligning sequences to a template alignment. Bioinformatics 26: 266-267.
11. Caporaso, J.G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F.D., Costello, E.K., Fierer, N., Pena, A.G., Goodrich, J.K., Gordon, J.I., Huttley, G.A., Kelley, S.T., Knights, D., Koenig, J.E., Ley, R.E., Lozupone, C.A., McDonald, D., Muegge, B.D., Pirrung, M., Reeder, J., Sevinsky, J.R., Turnbaugh, P.J., Walters, W.A., Widmann, J., Yatsunenko, T., Zaneveld, J. and Knight, R., 2010b. QIIME allows analysis of high-throughput community sequencing data. Nature Methods 7: 335-336.
12. Cotter, P.D., Gahan, C.G. and Hill, C., 2001. A glutamate decarboxylase system protects Listeria monocytogenes in gastric fluid. Molecular Microbiology 40: 465-475.
13. Cryan, J.F. and Dinan, T.G., 2012. Mind-altering microorganisms:the impact of the gut microbiota on brain and behaviour. Nature Reviews Neuroscience 13: 701-712.
14. Dallman, M.F. and Bhatnagar, S., 2011. Chronic Stress and energy balance: role of the hypothalamo-pituitary-adrenal axis. Comprehensive Physiology. DOI: http://dx.doi.org/10.1002/cphy.cp070410.
15. Davari, S., Talaei, S.A., Alaei, H. and Salami, M., 2013. Probiotics treatment improves diabetes-induced impairment of synaptic activity and cognitive function: behavioral and electrophysiological proofs for microbiome-gut-brain axis. Neuroscience 240: 287-296.
16. De Goffau, M.C., Luopajarvi, K., Knip, M., Ilonen, J., Ruohtula, T., Harkonen, T., Orivuori, L., Hakala, S., Welling, G.W., Harmsen, H.J. and Vaarala, O., 2013. Fecal microbiota composition differs between children with beta-cell autoimmunity and those without. Diabetes 62: 1238-1244.
17. Dong, H., Kumar, M., Zhang, Y., Gyulkhandanyan, A., Xiang, Y.Y., Ye, B., Perrella, J., Hyder, A., Zhang, N., Wheeler, M., Lu, W.Y. and Wang, Q., 2006. Gamma-aminobutyric acid up- and downregulates insulin secretion from beta cells in concert with changes in glucose concentration. Diabetologia 49: 697-705.
18. El-Salhy, M., 2001. Gastric emptying in an animal model of human diabetes type 1: relation to endocrine cells. Acta Diabetologica 38: 139-144.
19. Erdö, S.L., 1992. Non-neuronal GABA systems: an overview. In: Erdö, S.L. (ed.) GABA outside the CNS. Springer, Berlin, Germany, pp. 97-110.
20. Feingold, K.R., 1989. Importance of small intestine in diabetic hypercholesterolemia. Diabetes 38: 141-145.
21. Frank, D.N., Robertson, C.E., Hamm, C.M., Kpadeh, Z., Zhang, T.Y., Chen, H.Y., Zhu, W., Sartor, R.B., Boedeker, E.C., Harpaz, N., Pace, N.R. and Li, E., 2011. Disease phenotype and genotype are associated with shifts in intestinal-associated microbiota in inflammatory bowel diseases. Inflammatory Bowel Diseases 17: 179-184.
22. German, J.P., Thaler, J.P., Wisse, B.E., Oh, I.S., Sarruf, D.A., Matsen, M.E., Fischer, J.D., Taborsky, G.J., Jr., Schwartz, M.W. and Morton, G.J., 2011. Leptin activates a novel CNS mechanism for insulinindependent normalization of severe diabetic hyperglycemia. Endocrinology 152: 394-404.
23. Giongo, A., Gano, K.A., Crabb, D.B., Mukherjee, N., Novelo, L.L., Casella, G., Drew, J.C., Ilonen, J., Knip, M., Hyoty, H., Veijola, R., Simell, T., Simell, O., Neu, J., Wasserfall, C.H., Schatz, D., Atkinson, M.A. and Triplett, E.W., 2011. Toward defining the autoimmune microbiome for type 1 diabetes. ISME Journal 5: 82-91.
24. Gleeson, A., Owens, D., Collins, P., Johnson, A. and Tomkin, G.H., 2000. The relationship between cholesterol absorption and intestinal cholesterol synthesis in the diabetic rat model. International Journal of Experimental Diabetes Research 1: 203-210.
25. Graessler, J., Qin, Y., Zhong, H., Zhang, J., Licinio, J., Wong, M.L., Xu, A., Chavakis, T., Bornstein, A.B., Ehrhart-Bornstein, M., Lamounier-Zepter, V., Lohmann, T., Wolf, T. and Bornstein, S.R., 2013. Metagenomic sequencing of the human gut microbiome before and after bariatric surgery in obese patients with type 2 diabetes: correlation with inflammatory and metabolic parameters. Pharmacogenomics Journal 13: 514-522.
26. Jung, I.L. and Kim, I.G., 2003. Polyamines and glutamate decarboxylasebased acid resistance in Escherichia coli. Journal of Biological Chemistry 278: 22846-22852.
27. Karlsson, C.L., Onnerfalt, J., Xu, J., Molin, G., Ahrne, S. and Thorngren-Jerneck, K., 2012. The microbiota of the gut in preschool children with normal and excessive body weight. Obesity 20: 2257-2261.
28. Lam, Y.Y., Mitchell, A.J., Holmes, A.J., Denyer, G.S., Gummesson, A., Caterson, I.D., Hunt, N.H. and Storlien, L.H., 2011. Role of the gut in visceral fat inflammation and metabolic disorders. Obesity 19: 2113-2120.
29. Lin, C.H., Lin, C.C., Shibu, M.A., Liu, C.S., Kuo, C.H., Tsai, F.J., Tsai, C.H., Hsieh, C.H., Chen, Y.H. and Huang, C.Y., 2014. Oral Lactobacillus reuteri GMN-32 treatment reduces blood glucose concentrations and promotes cardiac function in rats with streptozotocin-induced diabetes mellitus. British Journal of Nutrition 111: 598-605.
30. Lyte, M., 2011. Probiotics function mechanistically as delivery vehicles for neuroactive compounds: microbial endocrinology in the design and use of probiotics. Bioessays 33: 574-581.
31. Magoc, T. and Salzberg, S.L., 2011. FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27:2957-2963.
32. Murri, M., Leiva, I., Gomez-Zumaquero, J.M., Tinahones, F.J., Cardona, F., Soriguer, F. and Queipo-Ortuno, M.I., 2013. Gut microbiota in children with type 1 diabetes differs from that in healthy children:a case-control study. BMC Medicine 11: 46.
33. Nakagawa, T., Yokozawa, T., Kim, H.J. and Shibahara, N., 2005. Protective effects of gamma-aminobutyric acid in rats with streptozotocin-induced diabetes. Journal of Nutritional Science and Vitaminology 51: 278-282.
34. Park, K.B. and Oh, S.H., 2007. Production of yogurt with enhanced levels of gamma-aminobutyric acid and valuable nutrients using lactic acid bacteria and germinated soybean extract. Bioresource Technology 98: 1675-1679.
35. Patterson, E., Marques, T.M., O'Sullivan, O., Fitzgerald, P., Fitzgerald, G.F., Cotter, P.D., Dinan, T.G., Cryan, J.F., Stanton, C. and Ross, R.P., 2015. Streptozotocin-induced type-1-diabetes disease onset in Sprague-Dawley rats is associated with an altered intestinal microbiota composition and decreased diversity. Microbiology 161: 182-193.
36. Qin, J., Li, Y., Cai, Z., Li, S., Zhu, J., Zhang, F., Liang, S., Zhang, W., Guan, Y., Shen, D., Peng, Y., Zhang, D., Jie, Z., Wu, W., Qin, Y., Xue, W., Li, J., Han, L., Lu, D., Wu, P., Dai, Y., Sun, X., Li, Z., Tang, A., Zhong, S., Li, X., Chen, W., Xu, R., Wang, M., Feng, Q., Gong, M., Yu, J., Zhang, Y., Zhang, M., Hansen, T., Sanchez, G., Raes, J., Falony, G., Okuda, S., Almeida, M., LeChatelier, E., Renault, P., Pons, N., Batto, J.M., Zhang, Z., Chen, H., Yang, R., Zheng, W., Li, S., Yang, H., Wang, J., Ehrlich, S.D., Nielsen, R., Pedersen, O., Kristiansen, K. and Wang, J., 2012. A metagenome-wide association study of gut microbiota in type 2 diabetes. Nature 490: 55-60.
37. Quast, C., Pruesse, E., Yilmaz, P., Gerken, J., Schweer, T., Yarza, P., Peplies, J. and Glockner, F.O., 2013. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Research 41: D590-596.
38. Sanders, J.W., Leenhouts, K., Burghoorn, J., Brands, J.R., Venema, G. and Kok, J., 1998. A chloride-inducible acid resistance mechanism in Lactococcus lactis and its regulation. Molecular Microbiology 27: 299-310.
39. Saudek, C.D. and Young, N.L., 1981. Cholesterol metabolism in diabetes mellitus: the role of diet. Diabetes 30: 76-81.
40. Seo, M.J., Nam, Y.D., Lee, S.Y., Park, S.L., Sung-Hun, Y. and Lim, S.I., 2013. Expression and characterization of a glutamate decarboxylase from Lactobacillus brevis 877G producing gamma-aminobutyric acid. Bioscience Biotechnology and Biochemistry 77: 853-856.
41. Sindelar, D.K., Havel, P.J., Seeley, R.J., Wilkinson, C.W., Woods, S.C. and Schwartz, M.W., 1999. Low plasma leptin levels contribute to diabetic hyperphagia in rats. Diabetes 48: 1275-1280.
42. Sipols, A.J., Baskin, D.G. and Schwartz, M.W., 1995. Effect of intracerebroventricular insulin infusion on diabetic hyperphagia and hypothalamic neuropeptide gene expression. Diabetes 44: 147-151.
43. Soltani, N., Qiu, H., Aleksic, M., Glinka, Y., Zhao, F., Liu, R., Li, Y., Zhang, N., Chakrabarti, R., Ng, T., Jin, T., Zhang, H., Lu, W.Y., Feng, Z.P., Prud'homme, G.J. and Wang, Q., 2011. GABA exerts protective and regenerative effects on islet beta cells and reverses diabetes. Proceedings of the National Academy of Sciences of the USA 108: 11692-11697.
44. Tabuchi, M., Ozaki, M., Tamura, A., Yamada, N., Ishida, T., Hosoda, M. and Hosono, A., 2003. Antidiabetic effect of Lactobacillus GG in streptozotocin-induced diabetic rats. Bioscience, Biotechnology and Biochemistry 67: 1421-1424.
45. Tamura, S. and Shimomura, I., 2005. Contribution of adipose tissue and de novo lipogenesis to nonalcoholic fatty liver disease. Journal of Clinical Investigation 115: 1139-1142.
46. Tian, J., Dang, H., Chen, Z., Guan, A., Jin, Y., Atkinson, M.A. and Kaufman, D.L., 2013. γ-aminobutyric acid regulates both the survival and replication of human β-cells. Diabetes 62: 3760-3765.
47. Tian, J., Dang, H. and Kaufman, D.L., 2011a. Combining antigen-based therapy with GABA treatment synergistically prolongs survival of transplanted ss-cells in diabetic NOD mice. PLoS ONE 6: e25337.
48. Tian, J., Dang, H.N., Yong, J., Chui, W.S., Dizon, M.P., Yaw, C.K. and Kaufman, D.L., 2011b. Oral treatment with gamma-aminobutyric acid improves glucose tolerance and insulin sensitivity by inhibiting inflammation in high fat diet-fed mice. PLoS ONE 6: e25338.
49. Vazquez-Baeza, Y., Pirrung, M., Gonzalez, A. and Knight, R., 2013. EMPeror: a tool for visualizing high-throughput microbial community data. Gigascience 2: 16.
50. Wu, K.K. and Huan, Y., 2008. Streptozotocin-induced diabetic models in mice and rats. Current Protocols in Pharmacology 40: 5.47.1-5.47.14.
51. Yadav, H., Jain, S. and Sinha, P.R., 2008. Oral administration of dahi containing probiotic Lactobacillus acidophilus and Lactobacillus casei delayed the progression of streptozotocin-induced diabetes in rats. Journal of Dairy Research 75: 189-195.
52. Zarfeshani, A., Khaza'ai, H., Ali, R.M., Hambali, Z., Wahle, K. and Mutalib, M., 2011. Effect of Lactobacillus casei on the production of pro-inflammatory markers in streptozotocin-induced diabetic rats. Probiotics and Antimicrobial Proteins 3: 168-174.
53. Zhang, X., Shen, D., Fang, Z., Jie, Z., Qiu, X., Zhang, C., Chen, Y. and Ji, L., 2013. Human gut microbiota changes reveal the progression of glucose intolerance. PLoS ONE 8: e71108.