Ameliorative effect of berberine against gentamicin-induced nephrotoxicity in rats via attenuation of oxidative stress, inflammation, apoptosis and mitochondrial dysfunction

Renal Failure

Volumn 38, Issue 6, 2016, Pages 996-1006

  Adil, Mohammad ^a   Kandhare, Amit D ^a   Dalvi, Gautami ^a   Ghosh, Pinaki ^a   Venkata, Shivakumar ^a   Raygude, Kiran S ^a   Bodhankar, Subhash L ^a  

^a BHARATI VIDYAPEETH DEEMED UNIVERSITY   (India)

Author keywords

Bcl 2; berberine; gentamicin; KIM 1; nephrotoxicity; NF KB; NGAL

Indexed keywords

BERBERINE; CREATININE; CYTOCHROME C OXIDASE; GENTAMICIN; GLUTATHIONE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; KIDNEY INJURY MOLECULE 1; MALONALDEHYDE; METHYLPREDNISOLONE; NEUTROPHIL GELATINASE ASSOCIATED LIPOCALIN; NITRIC OXIDE; PROTEIN BCL 2; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE; SUPEROXIDE DISMUTASE; UREA; ACUTE PHASE PROTEIN; ANTIINFECTIVE AGENT; CELL ADHESION MOLECULE; HAVCR1PROTEIN, RAT; LIPOCALIN; NEUTROPHIL GELATINASE-ASSOCIATED LIPOCALIN PROTEIN, RAT; ONCOPROTEIN;

ADULT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CONTROLLED STUDY; CREATININE BLOOD LEVEL; CREATININE CLEARANCE; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DOSE RESPONSE; DRUG EFFECT; DRUG MECHANISM; ENZYME ACTIVITY; GENE EXPRESSION; HISTOPATHOLOGY; INFLAMMATION; KIDNEY FUNCTION; KIDNEY MASS; MALE; NEPHROTOXICITY; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; RAT; RENAL PROTECTION; UREA NITROGEN BLOOD LEVEL; ANIMAL; BLOOD; DRUG EFFECTS; DRUG-RELATED SIDE EFFECTS AND ADVERSE REACTIONS; KIDNEY; KIDNEY FUNCTION TEST; METABOLISM; MITOCHONDRION; PATHOLOGY; RANDOMIZATION; SPRAGUE DAWLEY RAT;

ACUTE-PHASE PROTEINS; ANIMALS; ANTI-BACTERIAL AGENTS; APOPTOSIS; BERBERINE; BLOOD UREA NITROGEN; CELL ADHESION MOLECULES; CREATININE; DRUG-RELATED SIDE EFFECTS AND ADVERSE REACTIONS; GENTAMICINS; GLUTATHIONE; KIDNEY; KIDNEY FUNCTION TESTS; LIPOCALINS; MALE; MALONDIALDEHYDE; MITOCHONDRIA; OXIDATIVE STRESS; PROTO-ONCOGENE PROTEINS; RANDOM ALLOCATION; RATS; RATS, SPRAGUE-DAWLEY; SUPEROXIDE DISMUTASE;

EID: 84963997616     PISSN: 0886022X     EISSN: 15256049     Source Type: Journal    
DOI: 10.3109/0886022X.2016.1165120     Document Type: Article

References (81)

1. C.Salgado, F.Hernandes, J.Novoa. Glomerular nephrotoxicity of amino nucleosides. Toxicol Appl Pharmacol. 2007;223:86–98.
2. J.M.Lopez-Novoa, Y.Quiros, L.Vicente, A.I.Morales, F.J.Lopez-Hernandez New insights into the mechanism of aminoglycoside nephrotoxicity: An integrative point of view. Kidney Int. 2011;79:33–45.
3. R.P.Wedeen, V.Batuman, C.Cheeks, E.Marquet, H.Sobel Transport of gentamicin in rat proximal tubule. Lab Invest. 1983;48:212–223.
4. R.Baliga, N.Ueda, P.D.Walker, S.V.Shah Oxidant mechanisms in toxic acute renal failure. Drug Metab Rev. 1999;31:971–997.
5. P.Balakumar, A.Rohilla, A.Thangathirupathi Gentamicin-induced nephrotoxicity: Do we have a promising therapeutic approach to blunt it? Pharmacol Res. 2010;62:179–186.
6. J.M.Weinberg, P.G.Harding, H.D.Humes Mechanisms of gentamicin-induced dysfunction of renal cortical mitochondria. II. Effects on mitochondrial monovalent cation transport. Arch Biochem Biophys. 1980;205:232–239.
7. T.Finkel Oxygen radicals and signaling. Curr Opin Cell Biol. 1998;10:248–253.
8. G.Bledsoe, S.Crickman, J.Mao,. Kallikrein/kinin protects against gentamicin-induced nephrotoxicity by inhibition of inflammation and apoptosis. Nephrol Dial Transplant. 2006;21:624–633.
9. A.D.Kandhare, K.S.Raygude, P.Ghosh, T.P.Gosavi, S.L.Bodhankar Patentability of animal models: India and the Globe. Inter J Pharm Bio Arc. 2011;2:1024–1032.
10. K.Fukuda, Y.Hibiya, M.Mutoh, M.Koshiji, S.Akao, H.Fujiwara Inhibition by berberine of cyclooxygenase-2 transcriptional activity in human colon cancer cells. J Ethnopharmacol. 1999;66:227–233.
11. W.Kong, J.Wei, P.Abidi,. Berberine is a novel cholesterol-lowering drug working through a unique mechanism distinct from statins. Nat Med. 2004;10:1344–1351.
12. P.R.Vuddanda, S.Chakraborty, S.Singh Berberine: A potential phytochemical with multispectrum therapeutic activities. Expert Opin Invest Drugs. 2010;19:1297–1307.
13. S.Lee, H.-J.Lim, J.-H.Park, K.-S.Lee, Y.Jang, H.-Y.Park Berberine-induced LDLR up-regulation involves JNK pathway. Biochem Biophys Res Commun. 2007;362:853–857.
14. E.W.Holy, A.Akhmedov, T.F.Lüscher, F.C.Tanner Berberine, a natural lipid-lowering drug, exerts prothrombotic effects on vascular cells. J Mol Cell Cardiol. 2009;46:234–240.
15. A.Visnagri, A.D.Kandhare, S.L.Bodhankar Renoprotective effect of berberine via intonation on apoptosis and mitochondrial-dependent pathway in renal ischemia reperfusion-induced mutilation. Ren Fail. 2015;37:482–493.
16. F.-M.Wang, Y.-J.Yang, L.-L.Ma, X.-J.Tian, Y.-Q.He Berberine ameliorates renal interstitial fibrosis induced by unilateral ureteral obstruction in rats. Nephrology. 2014;19:542–551.
17. Z.Guo, H.Sun, H.Zhang, Y.Zhang Anti-hypertensive and renoprotective effects of berberine in spontaneously hypertensive rats. Clin Exp Hypertens. 2015;37:332–339.
18. B.D.Sahu, S.Tatireddy, M.Koneru,. Naringin ameliorates gentamicin-induced nephrotoxicity and associated mitochondrial dysfunction, apoptosis and inflammation in rats: Possible mechanism of nephroprotection. Toxicol Appl Pharmacol. 2014;277:8–20.
19. R.M.Kakalij, C.P.Alla, R.P.Kshirsagar, B.H.Kumar, S.S.Mutha, P.V.Diwan Ameliorative effect of Elaeocarpus ganitrus on gentamicin-induced nephrotoxicity in rats. Indian J Pharmacol. 2014;46:298–302.
20. A.D.Kandhare, V.Shivakumar, A.Rajmane, P.Ghosh, S.L.Bodhankar Evaluation of the neuroprotective effect of chrysin via modulation of endogenous biomarkers in a rat model of spinal cord injury. J Nat Med. 2014;68:586–603.
21. M.Adil, A.Visnagri, V.S.Kumar, A.D.Kandhare, P.Ghosh, S.L.Bodhankar Protective effect of naringin on sodium arsenite induced testicular toxicity via modulation of biochernical perturbations in experimental rats. Pharmacologia. 2014;5:222–234.
22. S.L.Badole, S.M.Chaudhari, G.B.Jangam, A.D.Kandhare, S.L.Bodhankar Cardioprotective activity of Pongamia pinnata in streptozotocin-nicotinamide induced diabetic rats. Biomed Res Int. 2015;2015:403291.
23. A.E.Ghule, A.D.Kandhare, S.S.Jadhav, A.A.Zanwar, S.L.Bodhankar Omega-3-fatty acid adds to the protective effect of flax lignan concentrate in pressure overload-induced myocardial hypertrophy in rats via modulation of oxidative stress and apoptosis. Int Immunopharmacol. 2015;28:751–763.
24. V.Honmore, A.Kandhare, A.A.Zanwar, S.Rojatkar, S.Bodhankar, A.Natu Artemisia pallens alleviates acetaminophen induced toxicity via modulation of endogenous biomarkers. Pharm Biol. 2015;53:571–581.
25. H.Kamble, A.D.Kandhare, S.L.Bodhankar, V.Mohan, P.A.Thakurdesai Effect of low molecular weight galactomannans from fenugreek seeds on animal models of diabetes mellitus. Biomed Aging Pathol. 2013;3:145–151.
26. A.D.Kandhare, J.Alam, M.V.Patil, A.Sinha, S.L.Bodhankar Wound healing potential of naringin ointment formulation via regulating the expression of inflammatory, apoptotic and growth mediators in experimental rats. Pharm Biol. 2016;54:419–432.
27. S.Ketkar, A.Rathore, A.D.Kandhare,. Alleviating exercise-induced muscular stress using neat and processed bee pollen: oxidative markers, mitochondrial enzymes, and myostatin expression in rats. Integr Med Res. 2015;4:147–160.
28. A.D.Kandhare, S.L.Bodhankar, V.Mohan, P.A.Thakurdesai Effect of glycosides based standardized fenugreek seed extract in bleomycin-induced pulmonary fibrosis in rats: Decisive role of Bax, Nrf2, NF-kappaB, Muc5ac, TNF-alpha and IL-1beta. Chem Biol Interact. 2015;237:151–165.
29. A.D.Kandhare, P.Ghosh, S.L.Bodhankar Naringin, a flavanone glycoside, promotes angiogenesis and inhibits endothelial apoptosis through modulation of inflammatory and growth factor expression in diabetic foot ulcer in rats. Chem Biol Interact. 2014;219:101–112.
30. A.Visnagri, A.D.Kandhare, S.Chakravarty, P.Ghosh, S.L.Bodhankar Hesperidin, a flavanoglycone attenuates experimental diabetic neuropathy via modulation of cellular and biochemical marker to improve nerve functions. Pharm Biol. 2014;52:814–828.
31. A.D.Kandhare, S.L.Bodhankar, V.Mohan, P.A.Thakurdesai Prophylactic efficacy and possible mechanisms of oligosaccharides based standardized fenugreek seed extract on high-fat diet-induced insulin resistance in C57BL/6 mice. J App Pharma Sci. 2015;5:035–045.
32. A.D.Kandhare, P.Ghosh, A.E.Ghule, S.L.Bodhankar Elucidation of molecular mechanism involved in neuroprotective effect of Coenzyme Q10 in alcohol-induced neuropathic pain. Fundam Clin Pharmacol. 2013;27:603–622.
33. A.Visnagri, A.D.Kandhare, P.Ghosh, S.L.Bodhankar Endothelin receptor blocker bosentan inhibits hypertensive cardiac fibrosis in pressure overload-induced cardiac hypertrophy in rats. Cardiovasc Endocrinol. 2013;2:85–97.
34. A.D.Kandhare, M.V.Patil, S.L.Bodhankar l-Arginine attenuates the ethylene glycol induced urolithiasis in ininephrectomized hypertensive rats: Role of KIM-1, NGAL, and NOs. Ren Fail. 2015;37:709–721.
35. A.A.Abdelsameea, A.M.Mohamed, M.G.Amer, S.M.Attia Cilostazol attenuates gentamicin-induced nephrotoxicity in rats. Exp Toxicol Pathol. 2016;68:247–253.
36. D.H.El-Kashef, A.E.El-Kenawi, G.M.Suddek, H.A.Salem Protective effect of allicin against gentamicin-induced nephrotoxicity in rats. Int Immunopharmacol. 2015;29:679–686.
37. S.H.Bekheet, E.A.Awadalla, M.M.Salman, M.K.Hassan Prevention of hepatic and renal toxicity with bradykinin potentiating factor (BPF) isolated from Egyptian scorpion venom (Buthus occitanus) in gentamicin treated rats. Tissue Cell. 2013;45:89–94.
38. U.M.Aswar, A.D.Kandhare, V.Mohan, P.A.Thakurdesai Anti-allergic effect of intranasal administration of type-A procyanidin polyphenols based standardized extract of cinnamon bark in ovalbumin sensitized BALB/c mice. Phytother Res. 2015;29:423–433.
39. N.V.Bhilare, S.S.Dhaneshwar, A.J.Sinha, A.D.Kandhare, S.L.Bodhankar Novel thioester prodrug of N-acetylcysteine for odor masking and bio availability enhancement. Curr Drug Deliv. 2015;4:4.
40. S.T.Devkar, A.D.Kandhare, B.D.Sloley, et al. Evaluation of the bioavailability of major withanolides of Withania somnifera using an in vitro absorption model system. J Adv Pharm Technol Res. 2015;6:159–164.
41. D.Ragab, D.M.Abdallah, H.S.El-Abhar Cilostazol renoprotective effect: Modulation of PPAR-gamma, NGAL, KIM-1 and IL-18 underlies its novel effect in a model of ischemia-reperfusion. PLoS One. 2014;9:e95313.
42. T.P.Gosavi, A.D.Kandhare, P.Ghosh, S.L.Bodhankar Anticonvulsant activity of Argentum metallicum, a homeopathic preparation. Pharm Lett. 2012;4:626–637.
43. S.Goswami, A.Kandhare, A.A.Zanwar,. Oral l-glutamine administration attenuated cutaneous wound healing in Wistar rats. Int Wound J. 2016;13:116–124.
44. V.S.Honmore, A.D.Kandhare, P.P.Kadam,. Isolates of Alpinia officinarum Hance as COX-2 inhibitors: Evidence from anti-inflammatory, antioxidant and molecular docking studies. Int Immunopharmacol. 2016;33:8–17.
45. A.D.Kandhare, S.L.Bodhankar, V.Mohan, P.A.Thakurdesai Acute and repeated doses (28 days) oral toxicity study of glycosides based standardized fenugreek seed extract in laboratory mice. Regul Toxicol Pharmacol. 2015;72:323–334.
46. A.D.Kandhare, S.L.Bodhankar, V.Singh, V.Mohan, P.A.Thakurdesai Anti-asthmatic effects of type-A procyanidine polyphenols from cinnamon bark in ovalbumin-induced airway hyperresponsiveness in laboratory animals. Biomed Aging Pathol. 2013;3:23–30.
47. A.Visnagri, A.D.Kandhare, V.Shiva Kumar,. Elucidation of ameliorative effect of Co-enzyme Q10 in streptozotocin-induced diabetic neuropathic perturbation by modulation of electrophysiological, biochemical and behavioral markers. Biomed Aging Pathol. 2012;2:157–172.
48. S.Samarghandian, M.Azimi-Nezhad, H.Mehrad-Majd, S.R.Mirhafez Thymoquinone ameliorates acute renal failure in gentamicin-treated adult male rats. Pharmacology. 2015;96:112–117.
49. J.D.Erusalimsky, S.Moncada Nitric oxide and mitochondrial signaling: From physiology to pathophysiology. Arterioscl Thromb Vasc Biol. 2007;27:2524–2531.
50. K.S.Raygude, A.D.Kandhare, P.Ghosh, A.E.Ghule, S.L.Bodhankar Evaluation of ameliorative effect of quercetin in experimental model of alcoholic neuropathy in rats. Inflammopharmacology. 2012;20:331–341.
51. K.Y.Saraswathi, A.P.Muthal, A.Kandhare, S.Rojatkar, S.L.Bodhankar Study of methanolic extract of Artemisia pallens wall on endurance of laboratory animals. Pharmacologia. 2014;5:298–309.
52. A.Sarkar, A.Sengupta, A.Mukhrjee,. Antiulcer potential of morin in acetic acid-induced gastric ulcer via modulation of endogenous biomarkers in laboratory animals. Pharmacologia. 2015;6:273–281.
53. A.D.Kandhare, P.Ghosh, A.E.Ghule, G.N.Zambare, S.L.Bodhankar Protective effect of Phyllanthus amarus by modulation of endogenous biomarkers and DNA damage in acetic acid induced ulcerative colitis: Role of phyllanthin and hypophyllanthin. Apollo Med. 2013;10:87–97.
54. J.S.Christo, A.M.Rodrigues, M.G.Mouro,. Nitric oxide (NO) is associated with gentamicin (GENTA) nephrotoxicity and the renal function recovery after suspension of GENTA treatment in rats. Nitric Oxide. 2011;24:77–83.
55. B.H.Ali, M.Al Za'abi, G.Blunden, A.Nemmar Experimental gentamicin nephrotoxicity and agents that modify it: A mini-review of recent research. Basic Clin Pharmacol Toxicol. 2011;109:225–232.
56. R.Che, Y.Yuan, S.Huang, A.Zhang Mitochondrial dysfunction in the pathophysiology of renal diseases. Am J Physiol Renal Physiol. 2014;306:F367–F378.
57. A.I.Morales, D.Detaille, M.Prieto,. Metformin prevents experimental gentamicin-induced nephropathy by a mitochondria-dependent pathway. Kidney Int. 2010;77:861–869.
58. C.F.SimmonsJr, R.T.Bogusky, H.D.Humes Inhibitory effects of gentamicin on renal mitochondrial oxidative phosphorylation. J Pharmacol Exp Ther. 1980;214:709–715.
59. L.Ferreira, Y.Quiros, S.M.Sancho-Martinez, et al. Urinary levels of regenerating islet-derived protein III β and gelsolin differentiate gentamicin from cisplatin-induced acute kidney injury in rats. Kidney Int. 2011;79:518–528.
60. T.Ichimura, E.J.Asseldonk, B.D.Humphreys, L.Gunaratnam, J.S.Duffield, J.V.Bonventre Kidney injury molecule-1 is a phosphatidylserine receptor that confers a phagocytic phenotype on epithelial cells. J Clin Invest. 2008;118:1657–1668.
61. K.Mori, K.Nakao Neutrophil gelatinase-associated lipocalin as the real-time indicator of active kidney damage. Kidney Int. 2007;71:967–970.
62. W.K.Han, V.Bailly, R.Abichandani, R.Thadhani, J.V.Bonventre Kidney Injury Molecule-1 (KIM-1): A novel biomarker for human renal proximal tubule injury. Kidney Int. 2002;62:237–244.
63. K.Mori, H.T.Lee, D.Rapoport,. Endocytic delivery of lipocalin-siderophore-iron complex rescues the kidney from ischemia-reperfusion injury. J Clin Invest. 2005;115:610–621.
64. Q.H.Luo, M.L.Chen, F.J.Sun,. KIM-1 and NGAL as biomarkers of nephrotoxicity induced by gentamicin in rats. Mol Cell Biochem. 2014;397:53–60.
65. Y.Zhou, V.S.Vaidya, R.P.Brown,. Comparison of kidney injury molecule-1 and other nephrotoxicity biomarkers in urine and kidney following acute exposure to gentamicin, mercury, and chromium. Toxicol Sci. 2008;101:159–170.
66. D.Bolignano, V.Donato, G.Coppolino,. Neutrophil gelatinase-associated lipocalin (NGAL) as a marker of kidney damage. Am J Kidney Dis. 2008;52:595–605.
67. V.S.Vaidya, J.S.Ozer, F.Dieterle,. Kidney injury molecule-1 outperforms traditional biomarkers of kidney injury in preclinical biomarker qualification studies. Nat Biotechnol. 2010;28:478–485.
68. E.H.Bae, I.J.Kim, S.Y.Joo,. Renoprotective effects of the direct renin inhibitor aliskiren on gentamicin-induced nephrotoxicity in rats. J Renin Angiotensin Aldosterone Syst. 2014;15:348–361.
69. Y.C.Chen, C.H.Chen, Y.H.Hsu,. Leptin reduces gentamicin-induced apoptosis in rat renal tubular cells via the PI3K-Akt signaling pathway. Eur J Pharmacol. 2011;658:213–218.
70. M.K.Pandey, B.Sung, A.B.Kunnumakkara, G.Sethi, M.M.Chaturvedi, B.B.Aggarwal Berberine modifies cysteine 179 of IkappaBalpha kinase, suppresses nuclear factor-kappaB-regulated antiapoptotic gene products, and potentiates apoptosis. Cancer Res. 2008;68:5370–5379.
71. H.Servais, Y.Jossin, F.Van Bambeke, P.M.Tulkens, M.P.Mingeot-Leclercq Gentamicin causes apoptosis at low concentrations in renal LLC-PK1 cells subjected to electroporation. Antimicrob Agents Chemother. 2006;50:1213–1221.
72. A.D.Kandhare, V.S.Kumar, M.Adil, A.R.Rajmane, P.Ghosh, S.L.Bodhankar Investigation of gastro protective activity of Xanthium strumarium L. by modulation of cellular and biochemical marker. Orient Pharm Exp Med. 2012;12:287–299.
73. A.D.Kandhare, K.S.Raygude, P.Ghosh, S.L.Bodhankar The ameliorative effect of fisetin, a bioflavonoid, on ethanol-induced and pylorus ligation-induced gastric ulcer in rats. Inter J Green Pharm. 2011;5:236–243.
74. A.D.Kandhare, K.S.Raygude, P.Ghosh, A.E.Ghule, S.L.Bodhankar Neuroprotective effect of naringin by modulation of endogenous biomarkers in streptozotocin induced painful diabetic neuropathy. Fitoterapia. 2012;83:650–659.
75. A.D.Kandhare, K.S.Raygude, P.Ghosh, A.E.Ghule, S.L.Bodhankar Therapeutic role of curcumin in prevention of biochemical and behavioral aberration induced by alcoholic neuropathy in laboratory animals. Neurosci Lett. 2012;511:18–22.
76. V.S.Kumar, A.R.Rajmane, M.Adil, A.D.Kandhare, P.Ghosh, S.L.Bodhankar Naringin ameliorates acetic acid induced colitis through modulation of endogenous oxido-nitrosative balance and DNA damage in rats. J Biomed Res. 2014;28:132–145.
77. K.S.Raygude, A.D.Kandhare, P.Ghosh, S.L.Bodhankar Anticonvulsant effect of fisetin by modulation of endogenous biomarkers. Biomed Prev Nutr. 2012;2:215–222.
78. A.P.Sarkate, P.R.Murumkar, D.K.Lokwani,. Design of selective TACE inhibitors using molecular docking studies: Synthesis and preliminary evaluation of anti-inflammatory and TACE inhibitory activity. SAR QSAR Environ Res. 2015;26:905–923.
79. Y.Kalkan, K.A.Kapakin, A.Kara,. Protective effect of Panax ginseng against serum biochemical changes and apoptosis in kidney of rats treated with gentamicin sulphate. J Mol Histol. 2012;43:603–613.
80. A.Patil, A.Guru, A.Mukhrjee,. Elucidation of gastro-protective activity of Morin in pylorus ligation induced gastric ulcer via modulation of oxidative stress. Pharm Lett. 2015;7:131–139.
81. W.Yu, M.Sheng, R.Xu,. Berberine protects human renal proximal tubular cells from hypoxia/reoxygenation injury via inhibiting endoplasmic reticulum and mitochondrial stress pathways. J Transl Med. 2013;11:24.