Advertisement

Pflügers Archiv

, Volume 446, Issue 1, pp 116–124 | Cite as

The induction of heat shock protein-72 attenuates cisplatin-induced acute renal failure in rats

  • Hua Zhou
  • Akihiko Kato
  • Hideo Yasuda
  • Mari Odamaki
  • Hideaki Itoh
  • Akira Hishida
Renal Function, Body Fluids

Abstract

Induction of heat shock proteins (HSPs) is thought to play a protective role in ischaemic acute renal failure (ARF). However the role of HSPs in nephrotoxic ARF is not well explored. The aim of this study was to clarify the effects of the induction of HSP70s on cisplatin (CDDP) (6 mg/kg i.v.)-induced ARF in rats. Uranyl acetate (UA) or sodium arsenite (SA) were administered i.v. 14 days or 1 day respectively before CDDP injection to induce HSPs. Serum creatinine (SCr), tubular damage score and the numbers of apoptotic (TUNEL-positive) cells were examined 5 days after CDDP injection. The expression of HSP72, B-cell lymphoma gene product-2 (Bcl-2) and Bax were evaluated by Western blot analysis. We also investigated the effect of co-administration of chelerythrine chloride (Chel), which inhibits the induction of HSPs, with SA on the expression of HSP72 and nephrotoxicity. Pretreatment with UA or SA significantly induced renal HSP72 expression. Both UA and SA attenuated the CDDP-induced increase in SCr and tubular damage scores. Co-administration of Chel with SA abolished the SA-induced increment of HSP72 and the beneficial effects of SA. The protective effects of the induction of HSP72 were associated with an increased renal Bcl-2/Bax ratio and the reduction of TUNEL-positive cells in the outer stripe of outer medulla. Our findings suggest that HSP72 attenuates CDDP-induced nephrotoxicity. The protective effects of HSP72 are associated with an increased Bcl-2/Bax ratio and less apoptosis.

Keywords

Cisplatin Acute renal failure HSP72 Apoptosis Bcl-2/Bax ratio Sodium arsenite Chelerythrine chloride 

Notes

Acknowledgements

We are grateful to the Nippon Kayaku (Tokyo, Japan) for kindly providing CDDP. Part of this work was presented at the World Congress of Nephrology (San Francisco, October 17-20, 2001). This work was supported by a research grant sponsored by the Ministry of Education, Science, Sports and Culture of Japan.

References

  1. 1.
    Abe T, Gotoh S, Higashi K (1999) Higher induction of heat shock protein 72 by heat stress in cisplatin-resistant than in cisplatin-sensitive cancer cells. Biochim Biophys Acta Gene Struct Expr 1445:123–133CrossRefGoogle Scholar
  2. 2.
    Basu A, Akkaraju GR (1999) Regulation of caspase activation and cis-diamminedichloroplatinum(II)-induced cell death by protein kinase C. Biochemistry 38:4245–4251CrossRefPubMedGoogle Scholar
  3. 3.
    Beck FX, Neuhofer W, Müller E (2000) Molecular chaperones in the kidney: distribution, putative roles, and regulation. Am J Physiol 279:F203–F215Google Scholar
  4. 4.
    Beere HM, Wolf BB, Cain K, Mosser DD, Mahboubi A, Kuwana T, Tailor P, Morimoto RI, Cohen GM, Green DR (2000) Heat-shock protein 70 inhibits apoptosis by preventing recruitment of procaspase-9 to the Apaf-1 apoptosome. Nat Cell Biol 2:469–475CrossRefPubMedGoogle Scholar
  5. 5.
    Bidmon B, Endemann M, Muller T, Arbeiter K, Herkner K, Aufricht C (2000) Heat shock protein-70 repairs proximal tubule structure after renal ischemia. Kidney Int 58:2400–2407PubMedGoogle Scholar
  6. 6.
    Brown IR, Rush SJ (1984) Induction of a 'stress' protein in intact mammalian organs after the intravenous administration of sodium arsenite. Biochem Biophys Res Commun 120:150–155PubMedGoogle Scholar
  7. 7.
    Bull JM, Strebel FR, Sunderland BA, Bulger RE, Edwards M, Siddik ZH, Newman RA (1988) O-(Beta-hydroxyethyl)-rutoside-mediated protection of renal injury associated with cis-diamminedichloroplatinum (II)/hyperthermia treatment. Cancer Res 48:2239–2244PubMedGoogle Scholar
  8. 8.
    Buzzard KA, Giaccia AJ, Killender M, Anderson RL (1998) Heat shock protein 72 modulates pathways of stress-induced apoptosis. J Biol Chem 273:17147–17153CrossRefPubMedGoogle Scholar
  9. 9.
    Chao DT, Korsmeyer SJ (1998) BCL-2 family: regulators of cell death. Annu Rev Immunol 16:395–419PubMedGoogle Scholar
  10. 10.
    Chen HW, Hsu C, Lue SI, Yang RC (2000) Attenuation of sepsis-induced apoptosis by heat shock pretreatment in rats. Cell Stress Chaperones 5:188–195PubMedGoogle Scholar
  11. 11.
    Emami A, Schwartz JH, Borkan SC (1991) Transient ischemia or heat stress induces a cytoprotectant protein in rat kidney. Am J Physiol 260:F479–F485PubMedGoogle Scholar
  12. 12.
    Garrett SH, Belcastrp M, Sens MA, Somji S, Sens DA (2001) Acute exposure to arsenite induces metallothionein isoform-specific gene expression in human proximal tubule cells. J Toxicol Environ Health A 64:343–355CrossRefPubMedGoogle Scholar
  13. 13.
    Gordon SA, Hoffman RA, Simmons RL, Ford HR (1997) Induction of heat shock protein 70 protects thymocytes against radiation-induced apoptosis. Arch Surg 132:1277–1282PubMedGoogle Scholar
  14. 14.
    Jaattela M, Wissing D, Kokholm K, Kallunki T, Egeblad M (1998) Hsp70 exerts its anti-apoptotic function downstream of caspase-3-like proteases. EMBO J 17:6124–6134PubMedGoogle Scholar
  15. 15.
    Kelly KJ, Baird NR, Greene AL (2001) Induction of stress response proteins and experimental renal ischemia/reperfusion. Kidney Int 59:1798–1802CrossRefPubMedGoogle Scholar
  16. 16.
    Komatsuda A, Wakui H, Satoh K, Yasuda T, Imai H, Nakamoto Y, Miura AB, Tashima M (1993) Altered localization of 73-kilodalton heat-shock protein in rat kidneys with gentamicin-induced acute tubular injury. Lab Invest 68:687–695PubMedGoogle Scholar
  17. 17.
    Komatsuda A, Wakui H, Ohtani H, Imai H, Miura AB, Itoh H (1999) Intracellular localization of HSP73 and HSP90 in rat kidneys with acute lysosomal thesaurismosis. Pathol Int 49:513–518CrossRefPubMedGoogle Scholar
  18. 18.
    Komatsuda A, Wakui H, Oyama Y, Imai H, Miura AB, Itoh H, Tashima Y (1999) Overexpression of the human 72 kDa heat shock protein in renal tubular cells confers resistance against oxidative injury and cisplatin toxicity. Nephrol Dial Transplant 14:1385–1390CrossRefPubMedGoogle Scholar
  19. 19.
    Li CY, Lee JS, Ko YG, Kim JI, Seo JS (2000) Heat shock protein 70 inhibits apoptosis downstream of cytochrome c release and upstream of caspase-3 activation. J Biol Chem 275:25665–25671CrossRefPubMedGoogle Scholar
  20. 20.
    Matsumoto H, Hayashi S, Shioura H, Ohtsubo T, Kitai R, Ohnishi K, Hayashi N, Ohnishi T, Kano E (1998) Suppression of heat-induced HSF activation by CDDP in human glioblastoma cells. Int J Radiat Oncol Biol Phys 41:915–920CrossRefPubMedGoogle Scholar
  21. 21.
    Meldrum KK, Meldrum DR, Sezen SF, Crone JK, Burnett AL (2001) Heat shock prevents simulated ischemia-induced apoptosis in renal tubular cells via a PKC-dependent mechanism. Am J Physiol 281:R359–R364Google Scholar
  22. 22.
    Meng X, Brown JM, Ao L, Nordeen SK, Franklin W, Harken AH, Banerjee A (1996) Endotoxin induces cardiac HSP70 and resistance to endotoxemic myocardial depression in rats. Am J Physiol 271:C1316–C1324PubMedGoogle Scholar
  23. 23.
    Miyaji T, Kato A, Yasuda H, Hishida A (2001) Role of the increase in p21 in cisplatin-induced acute renal failure in rats. J Am Soc Nephrol 12:900–908PubMedGoogle Scholar
  24. 24.
    Mizuno S, Fujita K, Furuy R, Hishid A, Ito H, Tashim Y, Kumagai H (1997) Association of HSP73 with the acquired resistance to uranyl acetate-induced acute renal failure. Toxicology 117:183–191CrossRefPubMedGoogle Scholar
  25. 25.
    Morita K, Wakui H, Komatsuda A, Ohtani H, Miura AB, Itoh H, Tashima Y (1995) Induction of heat-shock proteins HSP73 and HSP90 in rat kidneys after ischemia. Ren Fail 17:405–419PubMedGoogle Scholar
  26. 26.
    Mosser DD, Caron AW, Bourget L, Denis-Larose C, Massie B (1997) Role of the human heat shock protein hsp70 in protection against stress-induced apoptosis. Mol Cell Biol 17:5317–5327PubMedGoogle Scholar
  27. 27.
    Müller E, Neuhofer W, Burger-Kentischer A, Ohno A, Thurau K, Beck F (1998) Effects of long-term changes in medullary osmolality on heat shock proteins HSp25, HSP60, HSP72 and HSP73 in the rat kidney. Pflugers Arch 435:705–712PubMedGoogle Scholar
  28. 28.
    Nakajima T, Miyaji T, Kato A, Ikegaya N, Yamamoto T, Hishida A (1996) Uninephrectomy reduces apoptotic cell death and enhances renal tubular cell regeneration in ischemic ARF in rats. Am J Physiol 271:F846–F853PubMedGoogle Scholar
  29. 29.
    Nakamura S, Tatuno I, Noguchi Y, Kitagawa M, Kohn LD, Saito Y, Hirai A (1999) 73-kDa heat shock cognate protein interacts directly with P27Kip1, a cyclin-dependent kinase inhibitor, during G1/S transition. Biochem Biophys Res Commun 257:340–343CrossRefPubMedGoogle Scholar
  30. 30.
    Richards EH, Hickey E, Weber L, Master JR (1996) Effect of overexpression of the small heat shock protein HSP27 on the heat and drug sensitivities of human testis tumor cells. Cancer Res 56:2446–2451PubMedGoogle Scholar
  31. 31.
    Sano K, Fujigaki Y, Miyaji T, Ikegaya N, Ohishi K, Yonemura K, Hishida A (2000) Role of apoptosis in uranyl acetate (UA)-induced acute renal failure and acquired resistance to uranyl acetate. Kidney Int 57:1560–1570CrossRefPubMedGoogle Scholar
  32. 32.
    Satoh K, Wakui H, Komatsuda A, Nakamoto Y, Miura AB, Itoh H, Tashima Y (1994) Induction and altered localization of 90-kDa heat-shock protein in rat kidneys with cisplatin-induced acute renal failure. Renal Fail 16:313–323Google Scholar
  33. 33.
    Sardana MK, Drummond GS, Sassa S, Kappas A (1981) The potent heme oxygenase inducing action of arsenic and parasiticidal arsenicals. Pharmacology 23:247–251PubMedGoogle Scholar
  34. 34.
    Stokes KY, Abdih HK, Kelly CJ, Redmond HP, Bouchier-Hayes DJ (1996) Thermotolerance attenuates ischemia-reperfusion induced renal injury and increased expression of ICAM-1. Transplantation 62:1143–1149PubMedGoogle Scholar
  35. 35.
    Tsuruma T, Yagihashi A, Matsuno T, Zou XM, Asanuma K, Sasaki K, Hirata K (1996) The heat-shock protein 70 family reduces ischemia/reperfusion injury in small intestine. Transplant Proc 28:2629–2630PubMedGoogle Scholar
  36. 36.
    Turman MA, Rosenfeld SL (1999) Heat shock protein 70 overexpression protects LLC-PK1 tubular cells from heat shock but not hypoxia. Kidney Int 55:189–197CrossRefPubMedGoogle Scholar
  37. 37.
    Van Why SK, Hildebrandt F, Ardito T, Mann AS, Siegel NJ, Kashgarian M (1992) Induction and intracellular localization of HSP-72 after renal ischemia. Am J Physiol 263:F769–F775PubMedGoogle Scholar
  38. 38.
    Wakui H, Komatsuda A, Miura AB (1995) Heat-shock proteins in animal models for acute renal failure. Ren Fail 17:641–649PubMedGoogle Scholar
  39. 39.
    Wang HG, Reed JC (1998) Mechanisms of Bcl-2 protein function. Histol Histopathol 13:521–530PubMedGoogle Scholar
  40. 40.
    Wang Y, Knowlton AA, Christensen TG, Shih T, Borkan SC (1999) Prior heat stress inhibits apoptosis in adenosine triphosphate-depleted renal tubular cells. Kidney Int 55:2224–2235CrossRefPubMedGoogle Scholar
  41. 41.
    Welch WJ (1992) Mammalian stress response: cell physiology, structure/function of stress proteins, and implications for medicine and disease. Physiol Rev 72:1063–1081PubMedGoogle Scholar
  42. 42.
    Wondergem J, Bulger RE, Strebel FR, Newman RA, Travis EL, Stephens LC, Bull JM (1988) Effect of cis-diamminedichloroplatinum (II) combined with whole body hyperthermia on renal injury. Cancer Res 48:440–446PubMedGoogle Scholar
  43. 43.
    Yamashita N, Hoshida S, Nishida M, Igarashi J, Aoki K, Hori M, Kuzuya T, Tada M (1997) Time course of tolerance to ischemia-reperfusion injury and induction of heat shock protein 72 by heat stress in the rat heart. J Mol Cell Cardiol 29:1815–1821CrossRefPubMedGoogle Scholar
  44. 44.
    Yang CW, Kim BS, Kim J, Ahn HJ, Park JH, Jin DC, Kim YS, Bang BK (2001) Preconditioning with sodium arsenite inhibits apoptotic cell death in rat kidney with ischemia/reperfusion or cyclosporine-induced injuries. Exp Nephrol 9:284–294CrossRefPubMedGoogle Scholar
  45. 45.
    Yuan CM, Bohen EM, Musio F, Carome MA (1996) Sublethal heat shock and cyclosporine exposure produce tolerance against subsequent cyclosporine toxicity. Am J Physiol 271:F571–F578PubMedGoogle Scholar
  46. 46.
    Zhou H, Miyaji T, Kato A, Fujigaki Y, Sano K, Hishida A (1999) The attenuation of cisplatin-induced acute renal failure is associated with the less apoptotic cell death. J Lab Clin Med 34:649–658Google Scholar
  47. 47.
    Zhou H, Kato A, Miyaji T, Fujigaki Y, Sano K, Hishida A (2000) Glycine attenuates apoptotic cell death in uranyl acetate-induced acute renal failure in rats. Clin Exp Nephrol 4:24–28Google Scholar

Copyright information

© Springer-Verlag  2003

Authors and Affiliations

  • Hua Zhou
    • 1
  • Akihiko Kato
    • 1
  • Hideo Yasuda
    • 1
  • Mari Odamaki
    • 1
  • Hideaki Itoh
    • 2
  • Akira Hishida
    • 1
  1. 1.First Department of MedicineHamamatsu University School of MedicineHamamatsuJapan
  2. 2.Second Department of BiochemistryAkita University School of MedicineAkitaJapan

Personalised recommendations