Betulinic acid attenuates renal oxidative stress and inflammation in experimental model of murine polymicrobial sepsis

European Journal of Pharmaceutical Sciences

Volumn 70, Issue , 2015, Pages 12-21

  Lingaraju, Madhu Cholenahalli ^a   Pathak, Nitya Nand ^a   Begum, Jubeda ^a   Balaganur, Venkanna ^a   Ramachandra, Harish Darasaguppe ^a   Bhat, Rafia Ahmad ^a   Ram, Mahendra ^a   Singh, Vishakha ^a   Kandasamy, Kannan ^a   Kumar, Dhirendra ^a   Kumar, Dinesh ^a   Tandan, Surendra Kumar ^a  

^a INDIAN VETERINARY RESEARCH INSTITUTE   (India)

Author keywords

Cecal ligation and puncture; Cytokines; Inflammation; Oxidative stress; Septic kidney damage; Triterpenoid

Indexed keywords

BETULIC ACID; CATALASE; CREATININE; GELATINASE B; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 10; INTERLEUKIN 6; MALONALDEHYDE; NEUTROPHIL GELATINASE ASSOCIATED LIPOCALIN; NITRITE; SUPEROXIDE; SUPEROXIDE DISMUTASE; TUMOR NECROSIS FACTOR ALPHA; NONSTEROID ANTIINFLAMMATORY AGENT; TRITERPENE;

ACUTE KIDNEY FAILURE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CECAL LIGATION PUNCTURE; CONTROLLED STUDY; CREATININE BLOOD LEVEL; ENZYME ACTIVITY; HISTOPATHOLOGY; KIDNEY INJURY; LIGATION; LIPID PEROXIDATION; MALE; MOUSE; NEPHRITIS; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PUNCTURE; SEPSIS; SURVIVAL TIME; ACUTE KIDNEY INJURY; ANIMAL; COINFECTION; DISEASE MODEL; DRUG EFFECTS; INFLAMMATION; METABOLISM; PHYSIOLOGY;

ACUTE KIDNEY INJURY; ANIMALS; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; COINFECTION; DISEASE MODELS, ANIMAL; INFLAMMATION; MALE; MICE; OXIDATIVE STRESS; SEPSIS; TRITERPENES;

EID: 84961288986     PISSN: 09280987     EISSN: 18790720     Source Type: Journal    
DOI: 10.1016/j.ejps.2015.01.001     Document Type: Article

References (80)

1. H.E. Aebi Catalase H.U. Bergmeyer, J. Bergmeyer, M. Graßl, Methods of Enzymatic Analysis vol. III, third ed. 1983 Verlag Chemie Weinheim 273 286
2. S. Alakurtti, T. Makela, S. Koskimies, and J. YliKauhaluoma Pharmacological properties of the ubiquitous natural product betulin Eur. J. Pharm. Sci. 29 2006 1 13
3. J. Albert, A. Radomski, A. Soop, A. Sollevi, C. Frostell, and M.W. Radomski Differential release of matrix metalloproteinase-9 and nitric oxide following infusion of endotoxin to human volunteers Acta Anaesthesiol. Scand. 47 2003 407 410
4. S.M. Bagshaw, S. Uchino, R. Bellomo, H. Morimatsu, S. Morgera, M. Schetz, I. Tan, C. Bouman, E. Macedo, N. Gibney, A. Tolwani, H.M. Oudemans-van Straaten, C. Ronco, and J.A. Kellum Septic acute kidney injury in critically ill patients: clinical characteristics and outcomes Clin. J. Am. Soc. Nephrol. 2 2007 431 439
5. K. Bian, K. Davis, J. Kuret, L. Binder, and F. Murad Nitrotyrosine formation with endotoxin-induced kidney injury detected by immunohistochemistry Am. J. Physiol. 277 1999 33 40
6. K.A. Brown, S.D. Brain, J.D. Pearson, J.D. Edgeworth, S.M. Lewis, and D.F. Treacher Neutrophils in development of multiple organ failure in sepsis Lancet 368 2006 157 169
7. B. Brune, J. Zhou, and A. von Knethen Nitric oxide, oxidative stress, and apoptosis Kidney Int. Suppl. 63 2003 22 24
8. P.K. Chatterjee, M.M. Yeboah, O. Dowling, X.Y. Xue, S.R. Powell, Y. Al-Abeb, and C.N. Metz Nicotinic acetylcholine receptor agonists attenuate septic acute kidney injury in mice by suppressing inflammation and proteasome activity PLoS ONE 7 2012 35361
9. L.S. Chawla, M.G. Seneff, D.R. Nelson, M. Williams, H. Levy, P.L. Kimmel, and W.L. Macias Elevated plasma concentrations of IL-6 and elevated APACHE II score predict acute kidney injury in patients with severe sepsis Clin. J. Am. Soc. Nephrol. 2 2007 22 30
10. E. Cho, J.H. Lee, H.J. Lim, S.W. Oh, S.K. Jo, W.Y. Cho, H.K. Kim, and S.Y. Lee Soluble CD25 is increased in patients with sepsis-induced acute kidney injury Nephrology (Carlton) 19 2014 318 324
11. J. Cohen, and J. Carlet INTERSEPT: an international, multicenter, placebo-controlled trial of monoclonal antibody to human tumor necrosis factor-alpha in patients with sepsis. International Sepsis Trial Study Group Crit. Care Med. 24 1996 1431 1440
12. P.N. Cunningham, H.M. Dyanov, P. Park, J. Wang, K.A. Newell, and R.J. Quigg Acute renal failure in endotoxemia is caused by TNF acting directly on TNF receptor-1 in kidney J. Immunol. 168 2002 5817 5823
13. J. Deng, Y. Kohda, H. Chiao, Y. Wang, X. Hu, S.M. Hewitt, T. Miyaji, P. McLeroy, B. Nibhanupudy, S. Li, and R.A. Star Interleukin-10 inhibits ischemic and cisplatin-induced acute renal injury Kidney Int. 60 2001 2118 2128
14. P. Dennen, C. Altmann, J. Kaufman, C.L. Klein, A. Andres-Hernando, N.H. Ahuja, C.L. Edelstein, M.A. Cadnapaphornchai, A. Keniston, and S. Faubel Urine interleukin-6 is an early biomarker of acute kidney injury in children undergoing cardiac surgery Crit. Care 14 2010 181
15. P. Devarajan Emerging biomarkers of acute kidney injury Contrib. Nephrol. 156 2007 203 212
16. K. Doi, A. Leelahavanichkul, P.S. Yuen, and R.A. Star Animal models of sepsis and sepsis-induced kidney injury J. Clin. Invest. 119 2009 2868 2878
17. B. Dubois, S. Starckx, A. Pagenstecher, J. Oord, B. Arnold, and G. Opdenakker Gelatinase B deficiency protects against endotoxin shock Eur. J. Immunol. 32 2002 2163 2171
18. E. Ekşioʇlu-Demiralp, E.R. Kardaş, S. Ozgül, T. Yaʇci, H. Bilgin, O. Sehirli, F. Ercan, and G. Sener Betulinic acid protects against ischemia/reperfusion-induced renal damage and inhibits leukocyte apoptosis Phytother. Res. 24 2010 325 332
19. D.F. Fiorentino, A. Zlotnik, T.R. Mosmann, M. Howard, K.W. Moore, and A. O'Garra IL-10 acts on the antigen-presenting cell to inhibit cytokine production by Th1 cells J. Immunol. 147 1991 385 422
20. S. Fontanay, M. Grare, J. Mayer, C. Finance, and R.E. Duval Ursolic, oleanolic and betulinic acids: antibacterial spectra and selectivity indexes J. Ethnopharmacol. 120 2008 272 276
21. J.J. Friedewald, and H. Rabb Inflammatory cells in ischemic acute renal failure Kidney Int. 66 2004 486 491
22. G. Friedman, S. Jankowski, A. Marchant, M. Goldman, R.J. Kahn, and J.L. Vincent Blood interleukin 10 levels parallel the severity of septic shock J. Crit. Care 12 1997 183 187
23. H.F. Galley Bench-to-bedside review: targeting antioxidants to mitochondria in sepsis Crit. Care 14 2010 230
24. L.C. Green, D.A. Wagner, J. Gloglowski, P.L. Skipper, J.S. Wishnok, and S.R. Tannenbaum Analysis of nitrate, nitrite and [15N] nitrate in biological fluids and quantification of cytokines J. Immunol. Methods 284 2004 99 106
25. B. Hauser, H. Bracht, M. Matejovic, P. Radermacher, and B. Venkatesh Nitric oxide synthase inhibition in sepsis? Lessons learned from large-animal studies Anesth. Analg. 101 2005 488 498
26. S. Heemskerk, P. Pickkers, M.P. Bouw, A. Draisma, J.G. van der Hoeven, W.H. Peters, P. Smits, F.G. Russel, and R. Masereeuw Upregulation of renal inducible nitric oxide synthase during human endotoxemia and sepsis is associated with proximal tubule injury Clin. J. Am. Soc. Nephrol. 1 2006 853 862
27. S. Heemskerk, R. Masereeuw, F.G. Russel, and P. Pickkers Selective iNOS inhibition for the treatment of sepsis-induced acute kidney injury Nat. Rev. Nephrol. 5 2009 629 640
28. A. Hegde, H. Zhang, S.M. Moochhala, and M. Bhatia Neurokinin-1 receptor antagonist treatment protects mice against lung injury in polymicrobial sepsis J. Leukoc. Biol. 82 2007 678 685
29. S.M. Hollenberg, M. Broussard, J. Osman, and J.E. Parrillo Increased microvascular reactivity and improved mortality in septic mice lacking inducible nitric oxide synthase Cir. Res. 86 2000 774 778
30. Y. Kadoi, and F. Goto Selective inducible nitric oxide inhibition can restore hemodynamics, but does not improve neurological dysfunction in experimentally-induced septic shock in rats Anesth. Analg. 99 2004 212 220
31. K. Kapoor, S. Basu, B.K. Das, and B.D. Bhatia Lipid peroxidation and antioxidants in neonatal septicemia J. Trop. Pediatr. 52 2006 372 375
32. K.C. Kim, and C.H. Lee MAP kinase activation is required for the MMP-9 induction by TNF-stimulation Arch. Pharm. Res. 28 2005 1257 1262
33. N.T. Le, M. Xue, L.A. Castelnoble, and C.J. Jackson The dual personalities of matrix metalloproteinases in inflammation Front. Biosci. 12 2007 1475 1487
34. A. Leelahavanichkul, H. Yasuda, K. Doi, X. Hu, H. Zhou, P.S. Yuen, and R.A. Star Methyl-2-acetamidoacrylate, an ethyl pyruvate analog, decreases sepsis-induced acute kidney injury in mice Am. J. Physiol. Renal. Physiol. 295 2008 1825 1835
35. P. Lentini, M. de Cal, A. Clementi, A. Angela D'Angelo, and C. Ronco Sepsis and AKI in ICU patients: the role of plasma biomarkers Crit. Care Res. Pract. 2012 2012 856401
36. W.J. Liaw, T.H. Chen, Z.Z. Lai, S.J. Chen, A. Chen, C. Tzao, J.Y. Wu, and C.C. Wu Effects of a membrane-permeable radical scavenger, tempol, on intraperitoneal sepsis-induced organ injury in rats Shock 23 2005 88 96
37. T.A. Libermann, and D. Baltimore Activation of interleukin-6 gene expression through the NF-kappa B transcription factor Mol. Cell. Biol. 10 1990 2327 2334
38. M.C. Lingaraju, N.N. Pathak, J. Begum, V. Balaganur, R.A. Bhat, H.D. Ramachandra, A. Ayanur, M. Ram, V. Singh, D. Kumar, D. Kumar, and S.K. Tandan Betulinic acid attenuates lung injury by modulation of inflammatory cytokine response in experimentally-induced polymicrobial sepsis in mice Cytokine 71 2015 101 108
39. O.H. Lowry, N.J. Rosbrough, A.L. Farr, and R.J. Randall Protein measurement with the follin phenol reagent J. Biol. Chem. 193 1951 265
40. M. Madesh, and K.A. Balasubramanian Microtitre plate assay for superoxide dismutase using MTT reduction by superoxide Indian J. Biochem. Biophys. 35 1998 184 188
41. H. Maurya, V. Mangal, S. Gandhi, K. Prabhu, and K. Ponnudurai Prophylactic antioxidant potential of gallic acid in murine model of sepsis Int. J. Inflam. 2014 2014 580320
42. S. Miwa, F.L. Muller, and K.B. Beckman The Basics of Oxidative Biochemistry in Oxidative Stress in Aging S. Miwa, F.L. Muller, K.B. Beckman, 2008 Humana Press, Springer p. 14 (Chapter 2)
43. T. Miyaji, X. Hu, P.S. Yuen, Y. Muramatsu, S. Iyer, S.M. Hewitt, and R.A. Star Ethyl pyruvate decreases sepsis-induced acute renal failure and multiple organ damage in aged mice Kidney Int. 64 2003 1620 1631
44. D. Muhl, G. Woth, L. Drenkovics, A. Varga, S. Ghosh, C. Csontos, L. Bogár, G. Wéber, and J. Lantos Comparison of oxidative stress & leukocyte activation in patients with severe sepsis & burn injury Indian J. Med. Res. 134 2011 69 78
45. R. Murugan, V. Karajala-Subramanyam, M. Lee, S. Yende, L. Kong, M. Carter, D.C. Angus, and J.A. Kellum Acute kidney injury in non-severe pneumonia is associated with an increased immune response and lower survival Kidney Int. 77 2010 527 535
46. M.A. Nader, and H.N. Baraka Effect of betulinic acid on neutrophil recruitment and inflammatory mediator expression in lipopolysaccharide-induced lung inflammation in rats Eur. J. Pharm. Sci. 46 2012 106 113
47. Y. Nechemia-Arbely, D. Barkan, G. Pizov, A. Shriki, S. Rose-John, E. Galun, and J.H. Axelrod IL-6/IL-6R axis plays a critical role in acute kidney injury J. Am. Soc. Nephrol. 19 2008 1106 1115
48. A. Oberholzer, C. Oberholzer, and L. Moldawer Interleukin-10: a complex role in the pathogenesis of sepsis syndromes and its potential as an anti-inflammatory drug Crit. Care Med. 30 2002 58 63
49. Ogura, Y., Jesmin, S., Yamaguchi, N., Oki, M., Shimojo, N., Islam, M.M., Khatun, T., Kamiyama, J., Sakuramoto, H., Hagiya, K., Kawano, S., Mizutani, T., 2014. Potential amelioration of upregulated renal HIF-1alpha-endothelin-1 system by landiolol hydrochloride in a rat model of endotoxaemia. Life Sci. (in press), doi: http://dx.doi.org/10.1016/j.lfs.2014.05.007.
50. G.P. Otto, M. Busch, M. Sossdorf, and R.A. Claus Impact of sepsis-associated cytokine storm on plasma NGAL during acute kidney injury in a model of polymicrobial sepsis Crit Care 17 2013 419
51. E. Ozbek Induction of oxidative stress in kidney Int. J. Nephrol. 2012 2012 465897 10.1155/2012/465897
52. E. Pathak, L.A. MacMillan-Crow, and P.R. Mayeux Role of mitochondrial oxidants in an in vitro model of sepsis-induced renal injury J. Pharmacol. Exp. Ther. 340 2012 192 201
53. J. Pugin, M.C. Widmer, S. Kossodo, C.M. Liang, H.L. Preas 2nd, and A.F. Suffredini Human neutrophils secrete gelatinase B in vitro and in vivo in response to endotoxin and proinflammatory mediators Am. J. Respir. Cell Mol. Biol. 20 1999 458 464
54. S.U. Rehman Lead-induced regional lipid peroxidation in brain Toxicol. Lett. 21 1984 333
55. J.W. Rhee, K.W. Lee, D. Kim, Y. Lee, O.H. Jeon, H.J. Kwon, and D.S. Kim NF-κB-dependent regulation of matrix metalloproteinase-9 gene expression by lipopolysaccharide in a macrophage cell line RAW 264.7 J. Biochem. Mol. Biol. 40 2007 88 94
56. P.A. Riley Free radicals in biology: oxidative stress and the effects of ionizing radiation Int. J. Radiat. Biol. 65 1994 27 33
57. D. Rittirsch, M.S. Huber-Lang, M.A. Flierl, and P.A. Ward Immunodesign of experimental sepsis by cecal ligation and puncture Nat. Protoc. 4 2009 31
58. M. Rodriguez, L. Cabal-Hierro, M.T. Carcedo, J.M. Iglesias, N. Artime, B.G. Darnay, and P.S. Lazo NF-kappaB signal triggering and termination by tumor necrosis factor receptor 2 J. Biol. Chem. 286 2011 22814 22824
59. R.W. Schrier Cancer therapy and renal injury J. Clin. Invest. 110 2002 743 745
60. E.M. Simmons, J. Himmelfarb, M.T. Sezer, G.M. Chertow, R.L. Mehta, E.P. Paganini, S. Soroko, S. Freedman, K. Becker, D. Spratt, Y. Shyr, and T.A. Ikizler Plasma cytokine levels predict mortality in patients with acute renal failure Kidney Int. 65 2004 1357 1365
61. W.S. Speidl, W.G. Toller, C. Kaun, T.W. Weiss, S. Pfaffenberger, S.P. Kastl, A. Furnkranz, G. Maurer, K. Huber, H. Metzler, and J. Wojta Catecholamines potentiate LPS-induced expression of MMP-1 and MMP-9 in human monocytes and in the human monocytic cell line U937: possible implications for peri-operative plaque instability FASEB J. 18 2004 603 605
62. Y. Takada, and B.B. Aggarwal Betulinic acid suppresses carcinogen-induced NFkappa B activation through inhibition of I kappa B alpha kinase and p65 phosphorylation: abrogation of cyclooxygenase-2 and matrix metalloprotease-9 J. Immunol. 171 2003 3278 3286
63. T.K. Tan, G. Zheng, T.T. Hsu, S.R. Lee, J. Zhang, Y. Zhao, X. Tian, Y. Wang, Y.M. Wang, Q. Cao, Y. Wang, V.W. Lee, C. Wang, D. Zheng, S.I. Alexander, E. Thompson, and D.C. Harris Matrix metalloproteinase-9 of tubular and macrophage origin contributes to the pathogenesis of renal fibrosis via macrophage recruitment through osteopontin cleavage Lab. Invest. 93 2013 434 449
64. L. Tarhan, and M.N. Tuzmen Some properties of Cu, Zn-superoxide dismutase from sheep erythrocyte Turk. J. Chem. 24 2000 109
65. L. Teng, M. Yu, J.M. Li, H. Tang, J. Yu, L.H. Mo, J. Jin, and X.Z. Liu Matrix metalloproteinase-9 as new biomarkers of severity in multiple organ dysfunction syndrome caused by trauma and infection Mol. Cell. Biochem. 360 2012 271 277
66. V.S. Vaidya, K. Shankar, E.A. Lock, D. Dixon, and H.M. Mehendale Molecular mechanisms of renal tissue repair in survival from acute renal tubule necrosis: role of ERK1/2 pathway Toxicol. Pathol. 31 2003 604 618
67. T. van der Poll, J. Jansen, M. Levi, H. ten Cate, J.W. ten Cate, and S.J. van Deventer Regulation of interleukin-10 release by tumor necrosis factor in humans and chimpanzees J. Exp. Med. 180 1994 1985 1988
68. V. Viji, A. Helen, and V.R. Luxmi Betulinic acid inhibits endotoxin-stimulated phosphorylation cascade and pro-inflammatory prostaglandin E2 production in human peripheral blood mononuclear cells Br. J. Pharmacol. 162 2011 1291 1303
69. H.D. Wang, P.J. Pagano, Y. Du, A.J. Cayatte, M.T. Quinn, P. Brecher, and R.A. Cohen Superoxide anion from the adventitia of the rat thoracic aorta inactivates nitric oxide Circ. Res. 82 1998 810 818
70. R.L. Warner, N. Bhagavathula, K.C. Nerusu, H. Lateef, E. Younkin, K.J. Johnson, and J. Varani Matrix metalloproteinases in acute inflammation: induction of MMP-3 and MMP-9 in fibroblasts and epithelial cells following exposure to pro-inflammatory mediators in vitro Exp. Mol. Pathol. 76 2004 189 195
71. M.S. Wolin, M. Ahmad, and S.A. Gupte The sources of oxidative stress in the vessel wall Kidney Int. 67 2005 1659 1661
72. L. Wu, and P.R. Mayeux Effects of the inducible nitric oxide synthase inhibitor L-N6-(1-iminoethyl)-lysine on microcirculation and reactive nitrogen species generation in the kidney following lipopolysaccharide administration in mice J. Pharmacol. Exp. Ther. 320 2007 1061 1067
73. C.C. Wu, C.W. Chiao, G. Hsiao, A. Chen, and M.H. Yen Melatonin prevents endotoxin-induced circulatory failure in rats J. Pineal Res. 3 2001 147 156
74. L. Wu, N. Gokden, and P.R. Mayeux Evidence for the role of reactive nitrogen species in polymicrobial sepsis-induced renal peritubular capillary dysfunction and tubular injury J. Am. Soc. Nephrol. 18 2007 1807 1815
75. Y.-W. Xie, and M.S. Wolin Role of nitric oxide and its interaction with superoxide in the suppression of cardiac muscle mitochondrial respiration: involvement in response to hypoxia/ reoxygenation Circulation 94 1996 2580 2586
76. K. Yamamoto, T. Shimokawa, H. Yi, K. Isobe, T. Kojima, D.J. Loskutoff, and H. Saito Aging accelerates endotoxin-induced thrombosis: Increased responses of plasminogen activator inhibitor-1 and lipopolysaccharide signaling with aging Am. J. Pathol. 161 2002 1805 1814
77. C.L. Yeh, C.S. Hsu, S.L. Yeh, and W.J. Chen Dietary glutamine supplementation modulates Th1/Th2 cytokine and interleukin-6 expressions in septic mice Cytokine 31 2005 329 334
78. A. Zarjou, and A. Agarwal Sepsis and acute kidney injury J. Am. Soc. Nephrol. 6 2011 999 1006
79. C. Zhang, L.M. Walker, and P.R. Mayeux Role of nitric oxide in lipopolysaccharide-induced oxidant stress in the rat kidney Biochem. Pharmacol. 59 2000 203 209
80. X. Zhou, M.S. Fragala, J.E. McElhaney, and G.A. Kuchel Conceptual and methodological issues relevant to cytokine and inflammatory marker measurements in clinical research Curr. Opin. Clin. Nutr. Metab. Care 13 2010 541 547