Allopurinol attenuates rhabdomyolysis-associated acute kidney injury: Renal and muscular protection

Free Radical Biology and Medicine

Volumn 101, Issue , 2016, Pages 176-189

  Gois, Pedro H F ^a   Canale, Daniele ^a   Volpini, Rildo A ^a   Ferreira, Daniela ^a   Veras, Mariana M ^a   Andrade Oliveira, Vinicius ^a   Câmara, Niels O S ^a   Shimizu, Maria H M ^a   Seguro, Antonio C ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Acute kidney injury; Allopurinol; Glycerol; Inflammasome; Oxidative stress; Rhabdomyolysis

Indexed keywords

ALLOPURINOL; GLYCEROL; ICOSANOID; INFLAMMASOME; REACTIVE OXYGEN METABOLITE; 8-EPI-PROSTAGLANDIN F2ALPHA; PROSTAGLANDIN F2 ALPHA; SCAVENGER;

ACUTE KIDNEY FAILURE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; DRUG EFFICACY; KIDNEY BLOOD FLOW; KIDNEY FUNCTION; MALE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN ISOLATION; RAT; RENAL PROTECTION; RHABDOMYOLYSIS; VASOCONSTRICTION; ANALOGS AND DERIVATIVES; ANIMAL; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; CHEMICALLY INDUCED; COMPLICATION; DRUG EFFECTS; EPITHELIUM CELL; KIDNEY TUBULE; METABOLISM; MUSCLE CELL; OXIDATION REDUCTION REACTION; PATHOLOGY; SKELETAL MUSCLE; WISTAR RAT;

ACUTE KIDNEY INJURY; ALLOPURINOL; ANIMALS; APOPTOSIS; DINOPROST; EPITHELIAL CELLS; FREE RADICAL SCAVENGERS; GLYCEROL; KIDNEY TUBULES; MALE; MUSCLE CELLS; MUSCLE, SKELETAL; OXIDATION-REDUCTION; OXIDATIVE STRESS; RATS; RATS, WISTAR; REACTIVE OXYGEN SPECIES; RHABDOMYOLYSIS;

EID: 84992584899     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2016.10.012     Document Type: Article

References (69)

1. [1] Zager, R.A., Rhabdomyolysis and myohemoglobinuric acute renal failure. Kidney Int. 49 (1996), 314–326.
2. [2] Rosa, N.G., Silva, G., Teixeira, A., Rodrigues, F., Araújo, J.A., Rhabdomyolysis. Acta Med. Port. 18 (2005), 271–281.
3. [3] Rizzi, D., Basile, C., Di Maggio, A., et al. Clinical spectrum of accidental hemlock poisoning: neurotoxic manifestations, rhabdomyolysis and acute tubular necrosis. Nephrol. Dial. Transpl. 6 (1991), 939–943.
4. [4] Korrapati, M.C., Shaner, B.E., Schnellmann, R.G., Recovery from glycerol-induced acute kidney injury is accelerated by suramin. J. Pharmacol. Exp. Ther. 341 (2012), 126–136.
5. [5] Graves, E.J., Gillum, B.S., Detailed diagnoses and procedures, National Hospital Discharge Survey, 1995. Vital. Health Stat. 13 (1997), 1–146.
6. [6] Rodríguez, E., Soler, M.J., Rap, O., Barrios, C., Orfila, M.A., Pascual, J., Risk factors for acute kidney injury in severe rhabdomyolysis. PLoS One, 8, 2013, e82992.
7. [7] George, J., Struthers, A.D., Role of urate, xanthine oxidase and the effects of allopurinol in vascular oxidative stress. Vasc. Health Risk Manag. 5 (2009), 265–272.
8. [8] Ibrahim, B., Stoward, P.J., The histochemical localization of xanthine oxidase. Histochem. J. 10 (1978), 615–617.
9. [9] Glantzounis, G.K., Tsimoyiannis, E.C., Kappas, A.M., Galaris, D.A., Uric acid and oxidative stress. Curr. Pharm. Des. 11 (2005), 4145–4151.
10. [10] Hellsten, Y., Ahlborg, G., Jensen-Urstad, M., Sjödin, B., Indication of in vivo xanthine oxidase activity in human skeletal muscle during exercise. Acta Physiol. Scand. 134 (1988), 159–160.
11. [11] Gomez-Cabrera, M.C., Ferrando, B., Brioche, T., Sanchis-Gomar, F., Viña, J., Exercise and antioxidant supplements in the elderly. J. Sport Health Sci. 2 (2013), 94–100.
12. [12] Johnson, R.J., Nakagawa, T., Jalal, D., Sánchez-Lozada, L.G., Kang, D.H., Ritz, E., Uric acid and chronic kidney disease: which is chasing which?. Nephrol. Dial. Transpl. 28 (2013), 2221–2228.
13. [13] Carnovale, C., Venegoni, M., Clementi, E., Allopurinol overuse in asymptomatic hyperuricemia: a teachable moment. JAMA Intern. Med. 174 (2014), 1031–1032.
14. [14] Khosla, U.M., Zharikov, S., Finch, J.L., et al. Hyperuricemia induces endothelial dysfunction. Kidney Int. 67 (2005), 1739–1742.
15. [15] Sánchez-Lozada, L.G., Soto, V., Tapia, E., et al. Role of oxidative stress in the renal abnormalities induced by experimental hyperuricemia. Am. J. Physiol. Ren. Physiol. 295 (2008), F1134–F1141.
16. [16] Mazzali, M., Hughes, J., Kim, Y.G., et al. Elevated uric acid increases blood pressure in the rat by a novel crystal-independent mechanism. Hypertension 38 (2001), 1101–1106.
17. [17] Sapalidis, K., Papavramidis, T.S., Gialamas, E., Deligiannidis, N., Tzioufa, V., Papavramidis, S., The role of allopurinol's timing in the ischemia reperfusion injury of small intestine. J. Emerg. Trauma Shock 6 (2013), 203–208.
18. [18] Mao, X., Wang, T., Liu, Y., et al. N-acetylcysteine and allopurinol confer synergy in attenuating myocardial ischemia injury via restoring HIF-1α/HO-1 signaling in diabetic rats. PLoS One, 8, 2013, e68949.
19. [19] Keel, C.E., Wang, Z., Colli, J., Grossman, L., Majid, D., Lee, B.R., Protective effects of reducing renal ischemia-reperfusion injury during renal hilar clamping: use of allopurinol as a nephroprotective agent. Urology, 81, 2013 (210.e5-10).
20. [20] Castelli, P., Condemi, A.M., Brambillasca, C., et al. Improvement of cardiac function by allopurinol in patients undergoing cardiac surgery. J. Cardiovasc. Pharmacol. 25 (1995), 119–125.
21. [21] Guan, W., Osanai, T., Kamada, T., et al. Effect of allopurinol pretreatment on free radical generation after primary coronary angioplasty for acute myocardial infarction. J. Cardiovasc. Pharmacol. 41 (2003), 699–705.
22. [22] Erol, T., Tekin, A., Katırcıbaşı, M.T., et al. Efficacy of allopurinol pretreatment for prevention of contrast-induced nephropathy: a randomized controlled trial. Int. J. Cardiol. 167 (2013), 1396–1399.
23. [23] de Jesus Soares, T., Volpini, R.A., Francescato, H.D., Costa, R.S., da Silva, C.G., Coimbra, T.M., Effects of resveratrol on glycerol-induced renal injury. Life Sci. 81 (2007), 647–656.
24. [24] Kim, J.H., Lee, S.S., Jung, M.H., et al. N-acetylcysteine attenuates glycerol-induced acute kidney injury by regulating MAPKs and Bcl-2 family proteins. Nephrol. Dial. Transpl. 25 (2010), 1435–1443.
25. [25] Homsi, E., de Brito, S.M., Janino, P., Silymarin exacerbates p53-mediated tubular apoptosis in glycerol-induced acute kidney injury in rats. Ren. Fail. 32 (2010), 623–632.
26. [26] Bosch, X., Poch, E., Grau, J.M., Rhabdomyolysis and acute kidney injury. N. Engl. J. Med. 361 (2009), 62–72.
27. [27] Sharma, V., McNeill, J.H., To scale or not to scale: the principles of dose extrapolation. Br. J. Pharmacol. 157 (2009), 907–921.
28. [28] McCormack, M.C., Kwon, E., Eberlin, K.R., et al. Development of reproducible histologic injury severity scores: skeletal muscle reperfusion injury. Surgery 143 (2008), 126–133.
29. [29] Hori, K., Tsujii, M., lino, T., et al. Protective effect of edaravone for tourniquet-induced ischemia-reperfusion injury on skeletal muscle in murine hindlimb. BMC Musculoskelet. Disord., 14, 2013, 113.
30. [30] Livak, K.J., Schmittgen, T.D., Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T))method. Methods 25 (2001), 402–408.
31. [31] Thiel, G., Wilson, D.R., Arce, M.L., Oken, D.E., Glycerol induced hemoglobinuric acute renal failure in the rat. II. The experimental model, predisposing factors, and pathophysiologic features. Nephron 4 (1967), 276–297.
32. [32] Salahudeen, A.K., Wang, C., Bigler, S.A., Dai, Z., Tachikawa, H., Synergistic renal protection by combining alkaline-diuresis with lipid peroxidation inhibitors in rhabdomyolysis: possible interaction between oxidant and non-oxidant mechanisms. Nephrol. Dial. Transpl. 11 (1996), 635–642.
33. [33] Abul-Ezz, S.R., Walker, P.D., Shah, S.V., Role of glutathione in an animal model of myoglobinuric acute renal failure. Proc. Natl. Acad. Sci. USA 88 (1991), 9833–9837.
34. [34] Homsi, E., Mota da Silva, S. Jr., Machado de Brito, S., Bouçada Inácio Peixoto, E., Butori Lopes, de Faria, J., Janino, P., p53-Mediated oxidative stress and tubular injury in rats with glycerol-induced acute kidney injury. Am. J. Nephrol. 33 (2011), 49–59.
35. [35] Moore, K.P., Holt, S.G., Patel, R.P., et al. A causative role for redox cycling of myoglobin and its inhibition by alkalinization in the pathogenesis and treatment of rhabdomyolysis-induced renal failure. J. Biol. Chem. 273 (1998), 31731–31737.
36. [36] Zager, R.A., Heme protein induced tubular cytoresistance: expression at the plasma membrane level. Kidney Int. 47 (1995), 1336–1345.
37. [37] Zager, R.A., Burkhart, K.M., Conrad, D.S., Gmur, D.J., Iron, heme oxygenase, and glutathione: effects on myohemoglobinuric proximal tubular injury. Kidney Int. 48 (1995), 1624–1634.
38. [38] Forman, H.J., Augusto, O., Brigelius-Flohe, R., et al. Even free radicals should follow some rules: a guide to free radical research terminology and methodology. Free Radic. Biol. Med. 78 (2015), 233–235.
39. [39] Miriyala, S., Spasojevic, I., Tovmasyan, A., et al. Manganese superoxide dismutase, MnSOD and its mimics. Biochim. Biophys. Acta 1822 (2012), 794–814.
40. [40] Wei, Q., Hill, W.D., Su, Y., Huang, S., Dong, Z., Heme oxygenase-1 induction contributes to renoprotection by G-CSF during rhabdomyolysis-associated acute kidney injury. Am. J. Physiol. Ren. Physiol. 301 (2011), F162–F170.
41. [41] Nath, K.A., Balla, G., Vercellotti, G.M., et al. Induction of heme oxygenase is a rapid, protective response in rhabdomyolysis in the rat. J. Clin. Investig. 90 (1992), 267–270.
42. [42] Hsu, C.H., Kurtz, T.W., Waldinger, T.P., Cardiac output and renal blood flow in glycerol-induced acute renal failure in the rat. Circ. Res 40 (1977), 178–182.
43. [43] Taber, D.F., Morrow, J.D., Roberts, L.J. 2nd, A nomenclature system for the isoprostanes. Prostaglandins 53 (1997), 63–67.
44. [44] Morrow, J.D., Hill, K.E., Burk, R.F., Nammour, T.M., Badr, K.F., Roberts, L.J., A series of prostaglandin F2-like compounds are produced in vivo in humans by a non-cyclooxygenase, free radical-catalyzed mechanism. Proc. Natl. Acad. Sci. USA 87 (1990), 9383–9387.
45. [45] Badr, K.F., Abi-Antoun, T.E., Isoprostanes and the kidney. Antioxid. Redox Signal 7 (2005), 236–243.
46. [46] Skinner, K.A., White, C.R., Patel, R., et al. Nitrosation of uric acid by peroxynitrite. Formation of a vasoactive nitric oxide donor. J. Biol. Chem. 273 (1998), 24491–24497.
47. [47] Kuzkaya, N., Weissmann, N., Harrison, D.G., Dikalov, S., Interactions of peroxynitrite with uric acid in the presence of ascorbate and thiols: implications for uncoupling endothelial nitric oxide synthase. Biochem. Pharmacol. 70 (2005), 343–354.
48. [48] Sautin, Y.Y., Nakagawa, T., Zharikov, S., Johnson, R.J., Adverse effects of the classic antioxidant uric acid in adipocytes: nadph oxidase-mediated oxidative/nitrosative stress. Am. J. Physiol. Cell Physiol. 293 (2007), C584–C596.
49. [49] Feig, D.I., et al. Serum uric acid: a risk factor and a target for treatment?. J. Am. Soc. Nephrol. 17 (2006), S69–S73.
50. [50] Tan, S., Gelman, S., Wheat, J.K., Parks, D.A., Circulating xanthine oxidase in human ischemia reperfusion. South Med. J. 88 (1995), 479–482.
51. [51] Yokoyama, Y., Beckman, J.S., Beckman, T.K., et al. Circulating xanthine oxidase: potential mediator of ischemic injury. Am. J. Physiol. 258 (1990), G564–G570.
52. [52] Brown, J.M., Terada, L.S., Grosso, M.A., et al. Xanthine oxidase produces hydrogen peroxide which contributes to reperfusion injury of ischemic, isolated, perfused rat hearts. J. Clin. Investig. 81 (1988), 1297–1301.
53. [53] Pacher, P., Nivorozhkin, A., Szabó, C., Therapeutic effects of xanthine oxidase inhibitors: renaissance half a century after the discovery of allopurinol. Pharmacol. Rev. 58 (2006), 87–114.
54. [54] Homsi, E., Janino, P., de Faria, J.B., Role of caspases on cell death, inflammation, and cell cycle in glycerol-induced acute renal failure. Kidney Int. 69 (2006), 1385–1392.
55. [55] Homsi, E., Andreazzi, D.D., Faria, J.B., Janino, P., TNF-α-mediated cardiorenal injury after rhabdomyolysis in rats. Am. J. Physiol. Ren. Physiol. 308 (2015), F1259–F1267.
56. [56] Wilson, H.M., Walbaum, D., Rees, A.J., Macrophages and the kidney. Curr. Opin. Nephrol. Hypertens. 13 (2004), 285–290.
57. [57] Belliere, J., Casemayou, A., Ducasse, L., et al. Specific macrophage subtypes influence the progression of rhabdomyolysis-induced kidney injury. J. Am. Soc. Nephrol. 26 (2015), 1363–1377.
58. [58] Komada, T., Usui, F., Kawashima, A., et al. Role of NLRP3 inflammasomes for rhabdomyolysis-induced acute kidney injury. Sci. Rep., 5, 2015, 10901.
59. [59] Lin, P.Y., Lin, C.C., Liu, H.C., et al. Rasburicase improves hyperuricemia in patients with acute kidney injury secondary to rhabdomyolysis caused by ecstasy intoxication and exertional heat stroke. Pedia. Crit. Care Med. 12 (2011), e424–e427.
60. [60] Price, P.M., Safirstein, R.L., Megyesi, J., The cell cycle and acute kidney injury. Kidney Int. 76 (2009), 604–613.
61. [61] Gartel, A.L., Radhakrishnan, S.K., Lost in transcription: p21 repression, mechanisms, and consequences. Cancer Res. 65 (2005), 3980–3985.
62. [62] Xiong, Y., Zhang, H., Beach, D., D type cyclins associate with multiple protein kinases and the DNA replication and repair factor PCNA. Cell 71 (1992), 505–514.
63. [63] Prelich, G., Stillman, B., Coordinated leading and lagging strand synthesis during SV40 DNA replication in vitro requires PCNA. Cell 53 (1988), 117–126.
64. [64] Prelich, G., Kostura, M., Marshak, D.R., Mathews, M.B., Stillman, B., The cell-cycle regulated proliferating cell nuclear antigen is required for SV40 DNA replication in vitro. Nature 326 (1987), 471–475.
65. [65] Prelich, G., Tan, C.K., Kostura, M., et al. Functional identity of proliferating cell nuclear antigen and a DNA polymerase-delta auxiliary protein. Nature 326 (1987), 517–520.
66. [66] Megyesi, J., Udvarhelyi, N., Safirstein, R.L., Price, P.M., The p53-independent activation of transcription of p21 WAF1/CIP1/SDI1 after acute renal failure. Am. J. Physiol. 271 (1996), F1211–F1216.
67. [67] Megyesi, J., Safirstein, R.L., Price, P.M., Induction of p21WAF1/CIP1/SDI1 in kidney tubule cells affects the course of cisplatin-induced acute renal failure. J. Clin. Invesitig. 101 (1998), 777–782.
68. [68] Gómez-Cabrera, M.C., Pallardó, F.V., Sastre, J., Viña, J., García-del-Moral, L., Allopurinol and markers of muscle damage among participants in the Tour de France. JAMA 289 (2003), 2503–2504.
69. [69] Sanchis-Gomar, F., Pareja-Galeano, H., Gomez-Cabrera, M.C., et al. Allopurinol prevents cardiac and skeletal muscle damage in professional soccer players. Scand. J. Med Sci. Sports 25 (2015), e110–e115.