Oral administration of probiotic Lactobacillus paraplantarum BGCG11 attenuates diabetes-induced liver and kidney damage in rats

Journal of Functional Foods

Volumn 38, Issue , 2017, Pages 427-437

  Mihailović, Mirjana ^a   Živković, Milica ^a   Jovanović, Jelena Arambašić ^a   Tolinački, Maja ^a   Sinadinović, Marija ^a   Rajić, Jovana ^a   Uskoković, Aleksandra ^a   Dinić, Svetlana ^a   Grdović, Nevena ^a   Golić, Nataša ^a   Vidaković, Melita ^a  

^a UNIVERSITY OF BELGRADE   (Serbia)

Author keywords

Antidiabetic effect; Diabetes; Fibrosis; Inflammation; Lactobacillus paraplantarum BGCG11 probiotic; Oxidative stress

Indexed keywords

EID: 85029725408     PISSN: 17564646     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jff.2017.09.033     Document Type: Article

References (61)

1. Andersson, U., Bränning, C., Ahrné, S., Molin, G., Alenfall, J., Onning, G., Holm, C., Probiotics lower plasma glucose in the high-fat fed C57BL/6 J mouse. Beneficial Microbes 1:2 (2010), 189–196.
2. Aravindhan, V., Mohan, V., Arunkumar, N., Sandhya, S., Babu, S., Chronic endotoxemia in subjects with type-1 diabetes is seen much before the onset of microvascular complications. PLoS ONE, 10(9), 2015, e0137618.
3. Asemi, Z., Zare, Z., Shakeri, H., Sabihi, S.S., Esmaillzadeh, A., Effect of multispecies probiotic supplements on metabolic profiles, hs-CRP, and oxidative stress in patients with type 2 diabetes. Annals of Nutrition and Metabolism 63:1–2 (2013), 1–9.
4. Atanasova, E., Martinova, F., Jelev, D., Antonov, K., de Mey, C., Mateva, L., Krastev, Z., Alpha-2 macroglobulin is the simplest serum biomarker for liver fibrosis and fibrogenesis in chronic hepatitis C. MedInform 2 (2015), 153–164.
5. Balakumar, M., Prabhu, D., Sathishkumar, C., Prabu, P., Rokana, N., Kumar, R., Balasubramanyam, M., Improvement in glucose tolerance and insulin sensitivity by probiotic strains of Indian gut origin in high-fat diet-fed C57BL/6 J mice. European Journal of Nutrition, 2016 [Epub ahead of print].
6. Ban, C.R., Twigg, S.M., Fibrosis in diabetes complications: Pathogenic mechanisms and circulating and urinary markers. Vascular Health and Risk Management 4:3 (2008), 575–596.
7. Bermudez-Brito, M., Plaza-Díaz, J., Muñoz-Quezada, S., Gómez-Llorente, C., Gil, A., Probiotic mechanisms of action. Annals of Nutrition and Metabolism 61:2 (2012), 160–174.
8. Beutler, E., Catalase. Beutler, E., (eds.) Red cell metabolism, a manual of biochemical methods, 3rd ed., 1982, Grune and Stratton, New York, NY, USA, 105–116.
9. Bhatti, F., Mankhey, R.W., Asico, L., Quinn, M.T., Welch, W.J., Maric, C., Mechanisms of antioxidant and pro-oxidant effects of alpha-lipoic acid in the diabetic and nondiabetic kidney. Kidney International 67:4 (2005), 1371–1380.
10. Bogojević, D., Mihailović, M., Petrović, M., Dinić, S., Ivanović-Matić, S., Poznanović, G., Acute-phase-dependent binding affinity of C/EBPβ from the Nuclear Extract and Nuclear Matrix towards the Hormone Response Element of the α2-Macroglobulin Gene in Rat Hepatocytes. General Physiology and Biophysics 22 (2003), 279–285.
11. Cani, P., Neyrinck, N., Fava, F., Knauf, C., Burcelin, R.G., Tuohy, K.M., 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 50:11 (2007), 2374–2383.
12. Chen, J., Cui, W., Zhan, Q., Jia, Y., Sun, Y., Weng, L., Yang, B., Low molecular weight fucoidan ameliorates diabetic nephropathy via inhibiting epithelial-mesenchymal transition and fibrotic processes. American Journal of Translational Research 7:9 (2015), 1553–1563.
13. Dolpady, J., Sorini, C., Di Pietro, C., Cosorich, I., Ferrarese, R., Saita, D., Falcone, M., Oral Probiotic VSL#3 Prevents Autoimmune Diabetes by Modulating Microbiota and Promoting Indoleamine 2,3-Dioxygenase-Enriched Tolerogenic Intestinal Environment. Journal of Diabetes Research, 2016, 2016, 7569431.
14. Drabkin, D., Austin, H., Spectrophotometric studies preparations from washed blood cells. Journal of Biological Chemistry 112 (1935), 51–55.
15. Ejtahed, H.S., Mohtadi-Nia, J., Homayouni-Rad, A., Niafar, M., Asghari-Jafarabadi, M., Mofid, V., Probiotic yogurt improves antioxidant status in type 2 diabetic patients. Nutrition 28 (2012), 539–543.
16. Gambal, D., Simple, rapid procedure for isolating serum albumin. Biochimica et Biophysica Acta 251 (1971), 54–56.
17. Geier, M.S., Butler, R.N., Giffard, P.M., Howarth, G.S., Lactobacillus fermentum BR11, a potential new probiotic, alleviates symptoms of colitis induced by dextran sulphate sodium (DSS) in rats. International Journal of Food Microbiology 114:3 (2007), 267–274.
18. Gomes, A.C., Bueno, A.A., Machado de Souza, R.G., Mota, J.F., Gut microbiota, probiotics and diabetes. Nutrition Journal, 13, 2014, 60.
19. Gómez-Llorente, C., Muñoz, S., Gil, A., Role of Toll-like receptors in the development of immunotolerance mediated by probiotics. The Proceedings of the Nutrition Society 69 (2010), 381–389.
20. Gooding, J.M., Yap, K.L., Ikura, M., The cadherin-catenin complex as a focal point of cell adhesion and signalling: New insights from three-dimensional structures. BioEssays 26:5 (2004), 497–511.
21. Gruys, E., Toussaint, M.J.M., Niewold, T.A., Koopmans, S.J., Acute phase reaction and acute phase proteins. Journal of Zheijang University SCIENCE B 6:11 (2005), 1045–1056.
22. Habig, W.H., Pubst, M.J., Jakoby, W.B., Glutathione S-transferase. Journal of Biological Chemistry 249 (1974), 7130–7139.
23. Hsu, M.J., Lee, S.S., Lin, W.W., Polysaccharide purified from Ganoderma lucidum inhibits spontaneous and Fas-mediated apoptosis in human neutrophils through activation of the phosphatidylinositol 3 kinase/Akt signaling pathway. Journal of Leukocyte Biology 72:1 (2002), 207–216.
24. Huebschmann, A.G., Regensteiner, J.G., Vlassara, H., Reusch, J.E., Diabetes and advanced glycoxidation end products. Diabetes Care 29:6 (2006), 1420–1432.
25. Kalluri, R., Neilson, E.G., Epithelial-mesenchymal transition and its implications for fibrosis. Journal of Clinical Investigation 112:12 (2003), 1776–1784.
26. Karunakaran, U., Jeoung, N.H., O-GlcNAc modification: Friend or foe in diabetic cardiovascular disease. Korean Diabetes Journal 34:4 (2010), 211–219.
27. Kellow, N.J., Coughlan, M.T., Savige, G.S., Reid, C.M., Effect of dietary prebiotic supplementation on advanced glycation, insulin resistance and inflammatory biomarkers in adults with pre-diabetes: A study protocol for a double-blind placebo-controlled randomised crossover clinical trial. BMC Endocrine Disorders, 14(55), 2014.
28. Kullisaar, T., Songisepp, E., Mikelsaar, M., Zilmer, K., Vihalemm, T., Zilmer, M., Antioxidative probiotic fermented goats’ milk decreases oxidative stress-mediated atherogenicity in human subjects. British Journal of Nutrition 90 (2003), 449–456.
29. Lowry, O.H., Rosebrough, N.L., Farr, A.L., Randall, R.I., Protein measurement with Folin phenol reagent. Journal of Biological Chemistry 193 (1951), 265–275.
30. Lu, Y.C., Yin, L.T., Chang, W.T., Huang, J.S., Effect of Lactobacillus reuteri GMNL-263 treatment on renal fibrosis in diabetic rats. Journal of Bioscience and Bioengineering 110 (2010), 709–715.
31. Maritim, A.C., Sanders, R.A., Watkins, J.B., Diabetes, oxidative stress, and antioxidants: A review. Journal of Biochemical and Molecular Toxicology 17:1 (2003), 24–38.
32. Matsuzaki, T., Nagata, Y., Kado, S., Uchida, K., Prevention of onset in an insulin-dependent diabetes mellitus model, NOD mice, by oral feeding of Lactobacillus casei. APMIS 105 (1997), 643–649.
33. Matsuzaki, T., Yamazaki, R., Hashimoto, S., Yokokura, T., Antidiabetic effects of an oral administration of Lactobacillus casei in a non-insulindependent diabetes mellitus (NIDDM) model using KK-Ay mice. Endocrine Journal 44:3 (1997), 357–365.
34. Matsuzawa, A., Ichijo, H., Molecular mechanisms of the decision between life and death: Regulation of apoptosis by apoptosis signal-regulating kinase 1. Journal of Biochemistry 130:1 (2001), 1–8.
35. Miraghajani, M., Dehsoukhteh, S.S., Rafe, N., Hamedani, S.G., Sabihi, S., Ghiasvand, R., Potential mechanisms linking probiotics to diabetes: A narrative review of the literature. Sao Paulo Medical Journal 135:2 (2017), 169–178.
36. Misra, H.P., Fridovich, I., The role of superoxide anion in the autooxidation of epinephrine and simple assay for superoxide dismutase. Journal of Biological Chemistry 247 (1972), 3170–3175.
37. Mohamed, J., Nazratun Nafizah, A.H., Zariyantey, A.H., Budin, S.B., Mechanisms of diabetes-induced liver damage: The role of oxidative stress and inflammation. Sultan Qaboos University Medical Journal 16:2 (2016), 132–141.
38. Mukherjee, P.K., Maiti, K., Mukherjee, K., Houghton, P.J., Leads from Indian medicinal plants with hypoglycemic potentials. Journal of Ethnopharmacology 106:1 (2006), 1–28.
39. Nikolic, M., López, P., Strahinic, I., Suárez, A., Kojic, M., Fernández-García, M., Ruas-Madiedo, P., Characterisation of the exopolysaccharide (EPS)-producing Lactobacillus paraplantarum BGCG11 and its non-EPS producing derivative strains as potential probiotics. International Journal of Food Microbiology 158:2 (2012), 155–162.
40. Nuñez, G., Benedict, M.A., Hu, Y., Inohara, N., Caspases: The proteases of the apoptotic pathway. Oncogene 17:25 (1998), 3237–3245.
41. Parker, K.M., England, J.D., DaCosta, J., Hess, E.L., Goldstein, D.E., Improved colorimetric assay for glycosylated haemoglobin. Clinical Chemistry 27 (1981), 669–672.
42. Petrides, A.S., Liver disease and diabetes mellitus. Diabetes Reviews 2 (1994), 2–18.
43. Ruan, Y., Sun, J., He, J., Chen, F., Chen, R., Chen, H., Effect of probiotics on glycemic control: A systematic review and meta-analysis of randomized, controlled trials. PLoS ONE, 10(7), 2015, e0132121.
44. Sáez-Lara, M.J., Robles-Sanchez, C., Ruiz-Ojeda, F.J., Plaza-Diaz, J., Gil, A., Effects of probiotics and synbiotics on obesity, insulin resistance syndrome, type 2 diabetes and non-alcoholic fatty liver disease: A review of human clinical trials. International Journal of Molecular Sciences, 17(6), 2016.
45. Sánchez-Valle, V., Chávez-Tapia, N.C., Uribe, M., Méndez-Sánchez, N., Role of oxidative stress and molecular changes in liver fibrosis: A review. Current Medicinal Chemistry 19:28 (2012), 4850–4860.
46. Schleicher, E.D., Wagner, E., Nerlich, A.G., Increased accumulation of the glycoxidation product Nε-(carboxymethyl)lysine in human tissues in diabetes and aging. Journal of Clinical Investigation 99:3 (1997), 457–468.
47. Schroeder-Gloeckler, J.M., Rahman, S.M., Janssen, R.C., Qiao, L., Shao, J., Roper, M., Friedman, J.E., CCAAT/enhancer-binding protein beta deletion reduces adiposity, hepatic steatosis, and diabetes in Lepr(db/db) mice. Journal of Biological Chemistry 282:21 (2007), 15717–15729.
48. Singh, N.P., McCoy, M.T., Tice, R.R., Schneider, E.L., A simple technique for quantitation of low levels of DNA damage in individual cells. Experimental Cell Research 175 (1988), 184–191.
49. Tabuchi, M., Ozaki, M., Tamura, A., Yamada, N., Antidiabetic effect of Lactobacillus GG in streptozotocin-induced diabetic rats. Bioscience, Biotechnology, and Biochemistry 67:6 (2003), 1421–1424.
50. Takada, T., Kodera, Y., Matsubara, M., Kawashima, Y., Maeda, T., Shichiri, M., Serum monomeric alpha2-macroglobulin as a clinical biomarker in diabetes. Atherosclerosis 228:1 (2013), 270–276.
51. Towbin, H., Staehelin, T., Gordon, J., Electrophoretic transfer of proteins from polyacrilamifostinede gels to nitrocellulose sheets: Procedure and some applications. Proceedings of the National Academy of Sciences of the United States of America 76 (1979), 4350–4354.
52. 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. Journal of Functional Foods 18:A (2015), 473–486.
53. Wells, L., Vosseller, K., Hart, G.W., A role for N-acetylglucosamine as a nutrient sensor and mediator of insulin resistance. Cellular and Molecular Life Sciences 60:2 (2003), 222–228.
54. Yadav, H., Jain, S., Sinha, P.R., Antidiabetic effect of probiotic dahi containing Lactobacillus acidophilus and Lactobacillus casei in high fructose fed rats. Nutrition 23:1 (2007), 62–68.
55. Yadav, H., Jain, S., Sinha, P.R., Oral administration of dahi containing probiotic Lactobacillus acidophilus and Lactobacillus casei delayed the progression of streptozotocin-induced diabetes in rats. Journal of Dairy Research 75:2 (2008), 189–195.
56. Yadav, H., Lee, J.H., Lloyd, J., Walter, P.G., Rane, S.G., Beneficial metabolic effects of a probiotic via butyrate-induced GLP-1 hormone secretion. Journal of Biological Chemistry 288:35 (2013), 25088–25097.
57. Yan, F., Cao, H., Cover, I.T., Whitehead, R., Washington, M.K., Polk, D.B., Soluble proteins produced by probiotic bacteria regulate intestinal epithelial cell survival and growth. Gastroenterology 132:2 (2007), 562–575.
58. Yu, F., Lu, Z., Chen, B., Wu, X., Dong, P., Zheng, J., Salvianolic acid B-induced microRNA-152 inhibits liver fibrosis by attenuating DNMT1-mediated Patched1 methylation. Journal of Cellular and Molecular Medicine 19:11 (2015), 2617–2632.
59. Zador, I.Z., Hsieh, C.C., Papaconstantinou, J., Renal CCAAT/enhancer-binding proteins in experimental diabetes mellitus. Nephron 79:3 (1998), 312–316.
60. Ziegler, A.G., Schmid, S., Huber, D., Hummel, M., Bonifacio, E., Early infant feeding and risk of developing type 1 diabetes-associated autoantibodies. JAMA 290:13 (2003), 1721–1728.
61. Zirker, L., The relationship between gut microbiota and CKD: Why use prebiotics in CKD patients?. Renal Nutrition Forum 33 (2014), 1–7.