Lactobacillus helveticus and Lactobacillus plantarum modulate renal antioxidant status in a rat model of fructose-induced metabolic syndrome
Keywords:dietary fructose, renal antioxidant status, antioxidant enzymes, Lactobacillus helveticus, Lactobacillus plantarum.
- Dietary high-fructose causes metabolic disorder and augments the risk of chronic kidney diseases most probably due to oxidative stress.
- Renal superoxide dismutases are suppressed while catalase is upregulated in fructose-fed rats.
- Lactobacillus helveticus and Lactobacillus plantarum alleviate dietary fructose-induced changes in biochemical markers of blood and renal antioxidant enzymes.
- Lactobacillus helveticus and Lactobacillus plantarum might have a positive influence on renal antioxidant capacity in the dietary fructose-induced metabolic disorder.
Abstract: High dietary fructose intake causes a metabolic disorder and augments the risk of chronic kidney disease most likely due to oxidative stress. Probiotics could have antioxidant, antiinflammatory and immunoregulatory properties. The present study examined the influence of Lactobacillus helveticus and Lactobacillus plantarum supplementation on dietary fructose-induced metabolic changes and renal antioxidant/oxidant status of rats. Male Wistar rats were divided into four groups as follows: control; fructose; fructose plus L. helveticus; fructose plus L. plantarum. Fructose was given to the rats as a 20% solution in drinking water for 15 weeks. The probiotic supplementation was applied by gastric gavage once a day for six weeks. Several metabolic parameters in the plasma, gene and protein expressions of the main antioxidant enzymes in renal tissues of rats were measured. Dietary fructose-induced elevations in plasma insulin, triglyceride, VLDL, creatinine as well as renal urea levels were alleviated after treatment with L. helveticus and L. plantarum. Moreover, L. helveticus and L. plantarum supplementation recovered the changes in renal protein expression level of SOD1, SOD2 and CAT. In conclusion, supplementation with L. helveticus and L. plantarum has an improving effect on specific metabolic parameters and renal antioxidative enzymes in a fructose-induced metabolic disorder.
Received: January 23, 2019; Revised: February 20, 2019; Accepted: February 21, 2019; Published online: February 26, 2019
How to cite this article: Korkmaz OA, Sadi G, Kocabas A, Yildirim OG, Sumlu E, Koca HB, Nalbantoglu B, Pektas MB, Akar F. Lactobacillus helveticus and Lactobacillus plantarum modulate renal antioxidant status in a rat model of fructose-induced metabolic syndrome. Arch Biol Sci. 2019;71(2):265-73.
Prasad K, Dhar I. Oxidative stress as a mechanism of added sugar-induced cardiovascular disease. Int J Angiol. 2014;23:217-26.
Hannou SA, Haslam DE, McKeown NM, Herman MA. Fructose metabolism and metabolic disease. J Clin Invest. 2018;128:545-55.
Akar F, Uludağ O, Aydın A, Aytekin YA, Elbeg S, Tuzcu M, Sahin K. High-fructose corn syrup causes vascular dysfunction associated with metabolic disturbance in rats: protective effect of resveratrol. Food Chem Toxicol. 2012;50:2135-41.
Babacanoglu C, Yildirim N, Sadi G, Pektas MB, Akar F. Resveratrol prevents high-fructose corn syrup-induced vascular insulin resistance and dysfunction in rats. Food Chem Toxicol. 2013;60:160-7.
Sadi G, Ergin V, Yilmaz G, Pektas MB, Yildirim OG, Menevse A, Akar F. High-fructose corn syrup-induced hepatic dysfunction in rats: improving effect of resveratrol. Eur J Nutr. 2015;54(6):895-904.
Pektas MB, Yücel G, Koca H, Sadi G, Yıldırım O, Öztürk G, Akar F. Dietary fructose-induced hepatic injury in male and female rats: influence of resveratrol. Drug Res. (Stuttg). 2017;67:103-10.
Pektas MB, Koca HB, Sadi G, Akar F. Dietary fructose activates insulin signaling and inflammation in adipose tissue: modulatory role of resveratrol. Biomed Res Int. 2016;2016:8014252.
Pektas MB, Sadi G, Akar F.Long-term dietary fructose causes gender-different metabolic and vascular dysfunction in rats: modulatory effects of resveratrol. Cell Physiol Biochem. 2015;37:1407-20.
Yildirim OG, Sumlu E, Aslan E, Koca HB, Pektas MB, Sadi G, Akar F. High-fructose in drinking water initiates activation of inflammatory cytokines and testicular degeneration in rat. Toxicol Mech Methods. 2018;DOI: 10.1080/15376516.2018.1543745.
Prince PD, Lanzi CR, Toblli JE, Elesgaray R, Oteiza PI, Fraga CG, Galleano M. Dietary (–)-epicatechin mitigates oxidative stress, NO metabolism alterations, and inflammation in renal cortex from fructose-fed rats. Free Radic Biol Med. 2016;90:35-46.
Palanisamy N, Viswanathan P, Anuradha CV. Effect of Genistein, a soy isoflavone, on whole body insulin sensitivity and renal damage induced by a high-fructose diet. Ren Fail. 2008;30:645-54.
Nasri R, Abdelhedi O, Jemil I, Daoued I, Hamden K, Kallel C, Elfeki A, Lamri-Senhadji M, Boualga A, Nasri M, Karra-Châabouni M. Ameliorating effects of goby fish protein hydrolysates on high-fat-high-fructose diet-induced hyperglycemia, oxidative stress and deterioration of kidney function in rats. Chem Biol Interact. 2015;242:71-80.
Wang W, Ding X-Q, Gu T-T, Song L, Li J-M, Xue Q-C, Kong L-D. Pterostilbene and allopurinol reduce fructose-induced podocyte oxidative stress and inflammation via microRNA-377. Free Radic Biol Med. 2015;83:214-26.
Qiao Y, Xu L, Tao X, Yin L, QiY, Xu Y, Han X, Tang Z, Ma X, Liu K, Peng J. Protective effects of dioscin against fructose-induced renal damage via adjusting Sirt3-mediated oxidative stress, fibrosis, lipid metabolism and inflammation. Toxicol Lett. 2018;284:37-45.
Chaudhary K, Malhotra K, Sowers J, Aroor A. Uric Acid - key ingredient in the recipe for cardiorenal metabolic syndrome. Cardiorenal Med. 2013;3:208-20.
Johnson RJ, Nakagawa T, Sanchez-Lozada LG, Shafiu M, Sundaram S, Le M, Ishimoto T, Sautin YY, Lanaspa MA. Sugar, uric acid, and the etiology of diabetes and obesity. Diabetes. 2013;62:3307-15.
Wang J, Tang H, Zhang C, Zhao Y, Derrien M, Rocher E, van-Hylckama Vlieg JE, Strissel K, Zhao L, Obin M, Shen J. Modulation of gut microbiota during probiotic-mediated attenuation of metabolic syndrome in high fat diet-fed mice. ISME J. 2015;9:1-15.
Rad AH, Abbasalizadeh S, Vazifekhah S, Abbasalizadeh F, Hassanalilou T, Bastani P, Ejtahed H-S, Soroush A-R, Javadi M, Mortazavian AM, Khalili L. The future of diabetes management by healthy probiotic microorganisms. Curr Diabetes Rev. 2017;13:582-9.
Plaza-Díaz J, Ruiz-Ojeda FJ, Vilchez-Padial LM, Gil A. Evidence of the anti-inflammatory effects of probiotics and synbiotics in intestinal chronic diseases. Nutrients. 2017;9(6):555.
Wang Y, Wu Y, Wang Y, XuH, Mei X, Yu D, Wang Y, Li W. Antioxidant properties of probiotic bacteria. Nutrients. 2017;9(5):521.
Zielińska D, Kolożyn-Krajewska D. Food-origin lactic acid bacteria may exhibit probiotic properties: review. Biomed Res Int. 2018;2018:5063185.
Huang H-Y, Korivi M, Tsai C-H, Yang J-H, Tsai Y-C. Supplementation of Lactobacillus plantarum K68 and fruit-vegetable ferment along with high fat-fructose diet attenuates metabolic syndrome in rats with insulin resistance. Evid Based Complement Alternat Med. 2013;2013:943020.
Park D-Y, Ahn Y-T, Huh C-S, McGregor RA, Choi M-S. Dual probiotic strains suppress high fructose-induced metabolic syndrome. World J Gastroenterol. 2013;19(2):274-83.
Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951;193:265-75.
Zhang D-M, Jiao R-Q, Kong L-D. High dietary fructose: direct or indirect dangerous factors disturbing tissue and organ functions. Nutrients. 2017;9(4):335.
Della Corte KW, Perrar I, Penczynski KJ, Schwingshackl L, Herder C, Buyken AE. Effect of dietary sugar intake on biomarkers of subclinical inflammation: a systematic review and meta-analysis of intervention studies. Nutrients. 2018;10(5):606.
Andersson U, Bränning C, Ahrné S, Molin G, Alenfall J, Önning G, Nyman M, Holm C. Probiotics lower plasma glucose in the high-fat fed C57BL/6J mouse. Benef Microbes. 2010;1:189-96.
Choi I-D, Kim S-H, Jeong J-W, Lee DE, Huh C-S, Hong SS, Sim J-H, Ahn Y-T. Triglyceride-lowering effects of two probiotics, Lactobacillus plantarum KY1032 and Lactobacillus curvatus HY7601, in a rat model of high-fat diet-induced hypertriglyceridemia. J Microbiol Biotechnol. 2016;26:483-7.
Martinic A, Barouei J, Bendiks Z, Mishchuk D, Heeney DD, Martin R, Marco ML, Slupsky CM. Supplementation of Lactobacillus plantarum improves markers of metabolic dysfunction induced by a high fat diet. J Proteome Res. 2018;17:2790-802.
Yakovlieva M, Tacheva T, Mihaylova S, Tropcheva R, Trifonova K, Toleкova A, Danova S, Vlaykova T. Influence of Lactobacillus brevis 15 and Lactobacillus plantarum 13 on blood glucose and body weight in rats after high-fructose diet. Benef Microbes. 2015;6:505-12.
Ahn HY, Kim M, Chae JS, Ahn Y-T, Sim J-H, Choi I-D, Lee S-H, Lee JH. Supplementation with two probiotic strains, Lactobacillus curvatus HY7601 and Lactobacillus plantarum KY1032, reduces fasting triglycerides and enhances apolipoprotein A-V levels in non-diabetic subjects with hypertriglyceridemia. Atherosclerosis. 2015;241:649-56.
Zubiría MG, Gambaro SE, Rey MA, Carasi P, Serradell M de L.Á, Giovambattista A. Deleterious metabolic effects of high fructose intake: the preventive effect of Lactobacillus kefiri administration. Nutrients. 2017;9:470.
Dabla PK. Renal function in diabetic nephropathy. World J Diabetes. 2010;1:48-56.
Aoyama M, Isshiki K, Kume S, Chin-Kanasaki M, Araki H, Araki S-I, Koya D, Haneda M, Kashiwagi A, Maegawa H, Uzu T. Fructose induces tubulointerstitial injury in the kidney of mice. Biochem Biophy Res Commun. 2012;419:244-9.
Sasikumar P, Gomathi S, Anbazhagan K, Abhishek A, Paul E, Vasudevan V, Sasikumar S, Selvam GS. Recombinant Lactobacillus plantarum expressing and secreting heterologous oxalate decarboxylase prevents renal calcium oxalate stone deposition in experimental rats. J Biomed Sci. 2014;21:86.
Cioffi F, Senese R, Lasala P, Ziello A, Mazzoli A, Crescenzo R, Liverini G, Lanni A, Goglia F, Iossa S. Fructose-rich diet affects mitochondrial DNA damage and repair in rats. Nutrients. 2017;9(4)323.
Girard A, Madani S, Boukortt F, Cherkaoui-Malki M, Belleville J, Prost J. Fructose-enriched diet modifies antioxidant status and lipid metabolism in spontaneously hypertensive rats. Nutrition. 2006;22:758-66.
Francini F, Castro MC, Schinella G, García ME, Maiztegui B, Raschia MA, Gagliardino JJ, Massa ML. Changes induced by a fructose-rich diet on hepatic metabolism and the antioxidant system. Life Sci. 2010;86:965-71.
Taleb-Dida N, Krouf D, Bouchenak M. Globularia alypum aqueous extract decreases hypertriglyceridemia and ameliorates oxidative status of the muscle, kidney, and heart in rats fed a high-fructose diet. Nutr Res. 2011;31:488-95.
Ali Hussei S, M Abd El-O, S Hemdan H. Protective effect of L-carnitine on metabolic disorders, oxidative stress, antioxidant status and inflammation in a rat model of insulin resistance. Int J Biol Chem. 2014;8:21-36.
Abdel-Kawi SH, Hassanin KMA, Hashem KS. The effect of high dietary fructose on the kidney of adult albino rats and the role of curcumin supplementation: A biochemical and histological study. Beni-Suef Univ J Basic Appl Sci. 2016;5:52-60.
Rajasekar P, Viswanathan P, Anuradha CV. Renoprotective action of L-carnitine in fructose-induced metabolic syndrome. Diabetes Obes Metab. 2008;10:171-80.
Sivakumar AS, Viswanathan P, Anuradha CV. Dose-dependent effect of galangin on fructose-mediated insulin resistance and oxidative events in rat kidney. Redox Rep. 2010;15:224-32.
Nogales F, Ojeda ML, del Valle PM, Serrano A, Murillo ML, Carreras Sánchez, O. Metabolic syndrome and selenium during gestation and lactation. Eur J Nutr. 2017;56:819-30.
Demirtas CY, Pasaoglu OT, Bircan FS, Kantar S, Turkozkan N. The investigation of melatonin effect on liver antioxidant and oxidant levels in fructose-mediated metabolic syndrome model. Eur Rev Med Pharmacol Sci. 2015;19:1915-21.
Sadi G, Şahin G, Bostancı A. Modulation of renal insulin signaling pathway and antioxidant enzymes with streptozotocin-induced diabetes: effects of resveratrol. Medicina (B. Aires). 2019;55(1):3.
Sadi G, Sadi Ö.Antioxidants and regulation of antioxidant enzymes by cellular redox status. Turkish J Sci Rev. 2010;3:95-107.
Aluwong T, Ayo J, Kpukple A, Oladipo O. Amelioration of hyperglycaemia, oxidative stress and dyslipidaemia in alloxan-induced diabetic wistar rats treated with probiotic and vitamin C. Nutrients. 2016;8(5):151.
Kleniewska P, Hoffmann A, Pniewska E, Pawliczak R. The influence of probiotic Lactobacillus casei in combination with prebiotic inulin on the antioxidant capacity of human plasma. Oxid Med Cell Longev. 2016;2016:1340903.
Kleniewska P, Pawliczak R. Influence of synbiotics on selected oxidative stress parameters. Oxid Med Cell Longev. 2017;2017:9315375.
Majlesi M, Shekarforoush SS, Ghaisari HR, Nazifi S, Sajedianfard J, Eskandari MH. Effect of probiotic Bacillus coagulans and Lactobacillus plantarum on alleviation of mercury toxicity in rat. Probiotics Antimicrob Proteins. 2017;9:300-9.
Wang AN, Yi XW, Yu HF, Dong B, Qiao SY. Free radical scavenging activity of Lactobacillus fermentum in vitro and its antioxidative effect on growing-finishing pigs. J Appl Microbiol. 2009;107:1140-8.
Aluwong T, Kawu M, Raji M, Dzenda T, Govwang F, Sinkalu V, Ayo J. Effect of yeast probiotic on growth, antioxidant enzyme activities and malondialdehyde concentration of broiler chickens. Antioxidants (Basel). 2013;2(4):326-39.
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(5):539-43.