Epoxyeicosatrienoic acids prevent cisplatin-induced renal apoptosis through a p38 mitogen-activated protein kinase-regulated mitochondrial pathway

Molecular Pharmacology

Volumn 84, Issue 6, 2013, Pages 925-934

  Liu, Yingmei ^a   Lu, Xiaodan ^a   Nguyen, Sinh ^a   Olson, Jean L ^a   Webb, Heather K ^b   Kroetz, Deanna L ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b Arête Therapeutics   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1 ADAMANTAN 1 YL 3 (1 METHYLSULFONYL PIPERIDIN 4 YLUREA); AR 9273; CASPASE 3; CISPLATIN; CYTOCHROME C; EPOXYICOSATRIENOIC ACID; HYDROLASE INHIBITOR; MITOGEN ACTIVATED PROTEIN KINASE P38; PROTEIN BAX; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CELL MIGRATION; CELL PROTECTION; CONTROLLED STUDY; DRUG CYTOTOXICITY; DRUG MECHANISM; ENZYME ACTIVATION; ENZYME INHIBITION; IN VITRO STUDY; IN VIVO STUDY; LLC PK1 CELL; MALE; MOUSE; NEPHROTOXICITY; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN INDUCTION; RENAL PROTECTION; SIGNAL TRANSDUCTION;

8,11,14-EICOSATRIENOIC ACID; ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; CASPASE 3; CELL LINE; CISPLATIN; ENZYME ACTIVATION; EPOXIDE HYDROLASES; EPOXY COMPOUNDS; KIDNEY; KIDNEY TUBULES, PROXIMAL; MALE; MICE; MICE, INBRED C57BL; MITOCHONDRIA; P38 MITOGEN-ACTIVATED PROTEIN KINASES; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION; SUPEROXIDE DISMUTASE; SWINE;

EID: 84888868447     PISSN: 0026895X     EISSN: 15210111     Source Type: Journal    
DOI: 10.1124/mol.113.088302     Document Type: Article

References (52)

1. Batchu SN, Lee SB, Qadhi RS, Chaudhary KR, El-Sikhry H, Kodela R, Falck JR, and Seubert JM (2011) Cardioprotective effect of a dual acting epoxyeicosatrienoic acid analogue towards ischaemia reperfusion injury. Br J Pharmacol 162:897-907.
2. Bodiga S, Zhang R, Jacobs DE, Larsen BT, Tampo A, Manthati VL, Kwok WM, Zeldin DC, Falck JR, and Gutterman DD et al. (2009) Protective actions of epoxyeicosatrienoic acid: dual targeting of cardiovascular PI3K and KATP channels. J Mol Cell Cardiol 46:978-988.
3. Burger H, Nooter K, Boersma AW, Kortland CJ, and Stoter G (1997) Lack of correlation between cisplatin-induced apoptosis, p53 status and expression of Bcl-2 family proteins in testicular germ cell tumour cell lines. Int J Cancer 73:592-599.
4. Chen C, Li G, Liao W, Wu J, Liu L, Ma D, Zhou J, Elbekai RH, Edin ML, and Zeldin DC et al. (2009) Selective inhibitors of CYP2J2 related to terfenadine exhibit strong activity against human cancers in vitro and in vivo. J Pharmacol Exp Ther 329:908-918.
5. Chen C, Wei X, Rao X, Wu J, Yang S, Chen F, Ma D, Zhou J, Dackor RT, and Zeldin DC et al. (2011) Cytochrome P450 2J2 is highly expressed in hematologic malignant diseases and promotes tumor cell growth. J Pharmacol Exp Ther 336:344-355.
6. Cummings BS and Schnellmann RG (2002) Cisplatin-induced renal cell apoptosis: caspase 3-dependent and -independent pathways. J Pharmacol Exp Ther 302:8-17.
7. Dhanasekaran A, Gruenloh SK, Buonaccorsi JN, Zhang R, Gross GJ, Falck JR, Patel PK, Jacobs ER, and Medhora M (2008) Multiple antiapoptotic targets of the PI3K/ Akt survival pathway are activated by epoxyeicosatrienoic acids to protect cardiomyocytes from hypoxia/anoxia. Am J Physiol Heart Circ Physiol 294:H724-H735.
8. El-Beshbishy HA, Bahashwan SA, Aly HA, and Fakher HA (2011) Abrogation of cisplatin-induced nephrotoxicity in mice by alpha lipoic acid through ameliorating oxidative stress and enhancing gene expression of antioxidant enzymes. Eur J Pharmacol 668:278-284.
9. Gordon JA and Gattone VH, 2nd (1986) Mitochondrial alterations in cisplatin-induced acute renal failure. Am J Physiol 250:F991-F998.
10. Hanigan MH and Devarajan P (2003) Cisplatin nephrotoxicity: molecular mechanisms. Cancer Ther 1:47-61.
11. Hsu YT, Wolter KG, and Youle RJ (1997) Cytosol-to-membrane redistribution of Bax and Bcl-X(L) during apoptosis. Proc Natl Acad Sci USA 94:3668-3672.
12. Huang Q, Dunn RT, 2nd, Jayadev S, DiSorbo O, Pack FD, Farr SB, Stoll RE, and Blanchard KT (2001) Assessment of cisplatin-induced nephrotoxicity by microarray technology. Toxicol Sci 63:196-207.
13. Jiang JG, Chen CL, Card JW, Yang S, Chen JX, Fu XN, Ning YG, Xiao X, Zeldin DC, and Wang DW (2005) Cytochrome P450 2J2 promotes the neoplastic phenotype of carcinoma cells and is up-regulated in human tumors. Cancer Res 65:4707-4715.
14. Khan MA, Liu J, Kumar G, Skapek SX, Falck JR, and Imig JD (2013) Novel orally active epoxyeicosatrienoic acid (EET) analogs attenuate cisplatin nephrotoxicity. FASEB J 27:2946-2956.
15. Kaushal GP, Kaushal V, Hong X, and Shah SV (2001) Role and regulation of activation of caspases in cisplatin-induced injury to renal tubular epithelial cells. Kidney Int 60:1726-1736.
16. Korbakis D and Scorilas A (2012) Quantitative expression analysis of the apoptosis-related genes BCL2, BAX and BCL2L12 in gastric adenocarcinoma cells following treatment with the anticancer drugs cisplatin, etoposide and taxol. Tumour Biol 33:865-875.
17. Kroetz DL and Zeldin DC (2002) Cytochrome P450 pathways of arachidonic acid metabolism. Curr Opin Lipidol 13:273-283.
18. Kyriakis JM and Avruch J (2001) Mammalian mitogen-activated protein kinase signal transduction pathways activated by stress and inflammation. Physiol Rev 81:807-869.
19. Lee RH, Song JM, Park MY, Kang SK, Kim YK, and Jung JS (2001) Cisplatin-induced apoptosis by translocation of endogenous Bax in mouse collecting duct cells. Biochem Pharmacol 62:1013-1023.
20. Li P, Nijhawan D, Budihardjo I, Srinivasula SM, Ahmad M, Alnemri ES, and Wang X (1997) Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell 91:479-489.
21. Liu L, Chen C, Gong W, Li Y, Edin ML, Zeldin DC, and Wang DW (2011) Epoxyeicosatrienoic acids attenuate reactive oxygen species level, mitochondrial dysfunction, caspase activation, and apoptosis in carcinoma cells treated with arsenic trioxide. J Pharmacol Exp Ther 339:451-463.
22. Liu X, Kim CN, Yang J, Jemmerson R, and Wang X (1996) Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome c. Cell 86: 147-157.
23. Liu Y, Webb HK, Fukushima H, Micheli J, Markova S, Olson JL, and Kroetz DL (2012) Attenuation of cisplatin-induced renal injury by inhibition of soluble epoxide hydrolase involves nuclear factor κB signaling. J Pharmacol Exp Ther 341: 725-734.
24. Ma J, Zhang L, Han W, Shen T, Ma C, Liu Y, Nie X, Liu M, Ran Y, and Zhu D (2012) Activation of JNK/c-Jun is required for the proliferation, survival, and angiogenesis induced by EET in pulmonary artery endothelial cells. J Lipid Res 53: 1093-1105.
25. Ma J, Zhang L, Li S, Liu S, Ma C, Li W, Falck JR, Manthati VL, Reddy DS, and Medhora M et al. (2010) 8,9-Epoxyeicosatrienoic acid analog protects pulmonary artery smooth muscle cells from apoptosis via ROCK pathway. Exp Cell Res 316:2340-2353.
26. Marino JP, Jr (2009) Soluble epoxide hydrolase, a target with multiple opportunities for cardiovascular drug discovery. Curr Top Med Chem 9 :452-463.
27. Morin C, Sirois M, Echavé V, Albadine R, and Rousseau E (2010) 17,18-epoxyeicosatetraenoic acid targets PPARγ and p38 mitogen-activated protein kinase to mediate its anti-inflammatory effects in the lung: role of soluble epoxide hydrolase. Am J Respir Cell Mol Biol 43:564-575.
28. Pabla N and Dong Z (2008) Cisplatin nephrotoxicity: mechanisms and renoprotective strategies. Kidney Int 73:994-1007.
29. Pabla N and Dong Z (2012) Curtailing side effects in chemotherapy: a tale of PKCδ in cisplatin treatment. Oncotarget 3:107-111.
30. Pabla N, Murphy RF, Liu K, and Dong Z (2009) The copper transporter Ctr1 contributes to cisplatin uptake by renal tubular cells during cisplatin nephrotoxicity. Am J Physiol Renal Physiol 296:F505-F511.
31. Park MS, De Leon M, and Devarajan P (2002) Cisplatin induces apoptosis in LLCPK1 cells via activation of mitochondrial pathways. J Am Soc Nephrol 13:858-865.
32. Raingeaud J, Gupta S, Rogers JS, Dickens M, Han J, Ulevitch RJ, and Davis RJ (1995) Pro-inflammatory cytokines and environmental stress cause p38 mitogen-activated protein kinase activation by dual phosphorylation on tyrosine and threonine. J Biol Chem 270:7420-7426.
33. Ramesh G and Reeves WB (2002) TNF-α mediates chemokine and cytokine expression and renal injury in cisplatin nephrotoxicity. J Clin Invest 110:835-842.
34. Ramesh G and Reeves WB (2003) TNFR2-mediated apoptosis and necrosis in cisplatin-induced acute renal failure. Am J Physiol Renal Physiol 285:F610-F618.
35. Ramesh G and Reeves WB (2005) p38 MAP kinase inhibition ameliorates cisplatin nephrotoxicity in mice. Am J Physiol Renal Physiol 289:F166-F174.
36. Reed JC (2002) Apoptosis-based therapies. Nat Rev Drug Discov 1:111-121.
37. Reed JC, Doctor K, Rojas A, Zapata JM, Stehlik C, Fiorentino L, Damiano J, Roth W, Matsuzawa S, and Newman R et al.; RIKEN GER Group;; GSL Members (2003) Comparative analysis of apoptosis and inflammation genes of mice and humans. Genome Res 13 (6B):1376-1388.
38. Samali A, Zhivotovsky B, Jones D, Nagata S, and Orrenius S (1999) Apoptosis: cell death defined by caspase activation. Cell Death Differ 6:495-496.
39. Segreto HR, Oshima CT, Franco MF, Silva MR, Egami MI, Teixeira VP, and Segreto RA (2011) Phosphorylation and cytoplasmic localization of MAPK p38 during apoptosis signaling in bone marrow granulocytes of mice irradiated in vivo and the role of amifostine in reducing these effects. Acta Histochem 113:300-307.
40. Seth R, Yang C, Kaushal V, Shah SV, and Kaushal GP (2005) p53-dependent caspase-2 activation in mitochondrial release of apoptosis-inducing factor and its role in renal tubular epithelial cell injury. J Biol Chem 280:31230-31239.
41. Spector AA, Fang X, Snyder GD, and Weintraub NL (2004) Epoxyeicosatrienoic acids (EETs): metabolism and biochemical function. Prog Lipid Res 43:55-90.
42. Tsuruya K, Ninomiya T, Tokumoto M, Hirakawa M, Masutani K, Taniguchi M, Fukuda K, Kanai H, Kishihara K, and Hirakata H et al. (2003) Direct involvement of the receptor-mediated apoptotic pathways in cisplatin-induced renal tubular cell death. Kidney Int 63:72-82.
43. Wang YX, Ulu A, Zhang LN, and Hammock B (2010) Soluble epoxide hydrolase in atherosclerosis. Curr Atheroscler Rep 12:174-183.
44. Wei Q, Dong G, Franklin J, and Dong Z (2007) The pathological role of Bax in cisplatin nephrotoxicity. Kidney Int 72:53-62.
45. Wolter KG, Hsu YT, Smith CL, Nechushtan A, Xi XG, and Youle RJ (1997) Movement of Bax from the cytosol to mitochondria during apoptosis. J Cell Biol 139: 1281-1292.
46. Wood CD, Thornton TM, Sabio G, Davis RA, and Rincon M (2009) Nuclear localization of p38 MAPK in response to DNA damage. Int J Biol Sci 5:428-437.
47. Yang S, Lin L, Chen JX, Lee CR, Seubert JM, Wang Y, Wang H, Chao ZR, Tao DD, and Gong JP et al. (2007) Cytochrome P-450 epoxygenases protect endothelial cells from apoptosis induced by tumor necrosis factor-α via MAPK and PI3K/Akt signaling pathways. Am J Physiol Heart Circ Physiol 293:H142-H151.
48. Yao X, Panichpisal K, Kurtzman N, and Nugent K (2007) Cisplatin nephrotoxicity: a review. Am J Med Sci 334:115-124.
49. Zhan Y, van de Water B, Wang Y, and Stevens JL (1999) The roles of caspase-3 and bcl-2 in chemically-induced apoptosis but not necrosis of renal epithelial cells. Oncogene 18:6505-6512.
50. Zhang B, Ramesh G, Norbury CC, and Reeves WB (2007) Cisplatin-induced nephrotoxicity is mediated by tumor necrosis factor-alpha produced by renal parenchymal cells. Kidney Int 72:37-44.
51. Zhao G, Tu L, Li X, Yang S, Chen C, Xu X, Wang P, and Wang DW (2012) Delivery of AAV2-CYP2J2 protects remnant kidney in the 5/6-nephrectomized rat via inhibition of apoptosis and fibrosis. Hum Gene Ther 23:688-699.
52. Zhivotovsky B, Samali A, Gahm A, and Orrenius S (1999) Caspases: their intracellular localization and translocation during apoptosis. Cell Death Differ 6: 644-651.