Amelioration of lipopolysaccharide-induced acute kidney injury by erythropoietin: Involvement of mitochondria-regulated apoptosis

Toxicology

Volumn 318, Issue 1, 2014, Pages 13-21

  Stoyanoff, Tania R ^a   Todaro, Juan S ^a   Aguirre, María V ^a   Zimmermann, María C ^a,b   Brandan, Nora C ^a,b  

^a UNIVERSIDAD NACIONAL DEL NORDESTE   (Argentina)

^b Facultad de Ciencias Naturales e Instituto M Lillo   (Argentina)

Author keywords

Apoptosis; Cytochrome c; EPO R; Erythropoietin; LPS induced AKI; Renoprotection

Indexed keywords

CASPASE 3; CYTOCHROME C; ERYTHROPOIETIN RECEPTOR; LIPOPOLYSACCHARIDE; PROTEIN BAX; PROTEIN BCL XL; RECOMBINANT ERYTHROPOIETIN;

ACUTE KIDNEY FAILURE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CONTROLLED STUDY; CYTOSOL; EXPERIMENTAL RENAL FAILURE; GENE OVEREXPRESSION; HISTOPATHOLOGY; IMMUNOHISTOCHEMISTRY; KIDNEY FUNCTION; KIDNEY INTERSTITIUM; LIPOPOLYSACCHARIDE INDUCED ACUTE KIDNEY INJURY; MALE; MITOCHONDRION; MOUSE; NICK END LABELING; NONHUMAN; PRIORITY JOURNAL; PROTEIN SECRETION; REGULATORY MECHANISM; RENAL PROTECTION; WESTERN BLOTTING;

APOPTOSIS; CYTOCHROME C; EPO-R; ERYTHROPOIETIN; LPS-INDUCED AKI; RENOPROTECTION;

ACUTE KIDNEY INJURY; ANIMALS; APOPTOSIS; CRYOPROTECTIVE AGENTS; DISEASE MODELS, ANIMAL; ERYTHROPOIETIN; HUMANS; KIDNEY; LIPOPOLYSACCHARIDES; MALE; MICE; MICE, INBRED BALB C; MITOCHONDRIA; RECEPTORS, ERYTHROPOIETIN;

EID: 84895797635     PISSN: 0300483X     EISSN: 18793185     Source Type: Journal    
DOI: 10.1016/j.tox.2014.01.011     Document Type: Article

References (42)

1. Abdelrahman M., Sharples E.J., McDonald M.C., Collin M., Patel N.S.A., Yaqoob M.M., Thiemermann C. Erythropoietin attenuates the tissue injury associated with hemorrhagic shock and myocardial ischemia. Shock 2004, 22:63-69.
2. Aoshiba K., Onizawa S., Tsuji T., Nagai A. Therapeutic effects of erythropoietin in murine models of endotoxin shock. Crit. Care Med. 2009, 37:889-898.
3. Aquino-Esperanza J.A., Aguirre M.V., Aispuru G.R., Lettieri C.N., Juaristi J.A., Alvarez M.A., Brandan N.C. In vivo 5-flourouracil-induced apoptosis on murine thymocytes: Involvement of FAS, Bax and Caspase 3. Cell Biol. Toxicol. 2008, 24:411-422.
4. Balestra G.M., Legrand M., Ince C. Microcirculation and mitochondria in sepsis: getting out of breath. Curr. Opin. Anaesthesiol. 2009, 22:84-90.
5. Brines M. The therapeutic potential of erythropoiesis-stimulating agents for tissue protection: A tale of two receptors. Blood Purif. 2010, 29:86-92.
6. Brines M., Cerami A. Erythropoietin-mediated tissue protection: reducing collateral damage from the primary injury response. J. Intern. Med. 2008, 264:405-432.
7. Brines M., Grasso G., Fiordaliso F., Sfacteria A., Ghezzi P., Fratelli M., Latini R., Xie Q.W., Smart J., Su-Rick C.J., Pobre E., Diaz D., Gomez D., Hand C., Coleman T., Cerami A. Erythropoietin mediates tissue protection through an erythropoietin and common β-subunit heteroreceptor. Proc. Natl. Acad. Sci. 2004, 101:14907-14912.
8. Chong Z.Z., Kang J.Q., Maiese K. Erythropoietin: cytoprotection in vascular and neuronal cells. Curr. Drug Targets Cardiovasc. Haematol. Disord. 2003, 3:141-154.
9. Cunningham P.N., Dyanov H.M., Park P., Wang J., Newell K.A., Quigg R.J. Acute renal failure in endotoxemia is caused by TNF acting directly on TNF receptor-1 in kidney. J. Immunol. 2002, 168:5817-5823.
10. De Beuf A., Verhulst A., Helbert M., Spaepen G., De Broe M.E., Ysebaert D.K., D́haese P.C. Tubular erythropoietin receptor expression mediates erythropoietin-induced renoprotection. Open Hematol. J. 2009, 3:1-10.
11. de Seigneux S., Ponte B., Weiss L., Pugin J., Romand J.A., Martin P.Y., Saudan P. Epoetin administrated after cardiac surgery: effects on renal function and inflammation in a randomized controlled study. BMC Nephrol. 2012, 13:132.
12. Doi K., Leelahavanichkul A., Yuen P.S., Star R.A. Animal models of sepsis and sepsis-induced kidney injury. J. Clin. Invest. 2009, 119:2868-2878.
13. Duranton C., Rubera I., L'hoste S., Cougnon M., Poujeol P., Barhanin J., Tauc M. KCNQ1 K+ channels are involved in lipopolysaccharide-induced apoptosis of distal kidney cells. Cell Physiol. Biochem. 2010, 25:367-378.
14. Esposito C., Pertile E., Grosjean F., Castoldi F., Diliberto R., Serpieri N., Arra M., Villa L., Mangione F., Esposito V., Migotto C., Valentino R., Dal Canton A. The improvement of ischemia/reperfusion injury by erythropoietin is not mediated through bone marrow cell recruitment in rats. Transplant Proc. 2009, 41:1113-1115.
15. Frede S., Fandrey J., Pagel H., Hellwig T., Jelkmann W. Erythropoietin gene expression is suppressed after lipopolysaccharide or interleukin-1 beta injections in rats. Am. J. Physiol. 1997, 273:1067-1071.
16. Jelkmann W., Wagner K. Beneficial and ominous aspects of the pleiotropic action of erythropoietin. Ann. Hematol. 2004, 83:673-686.
17. Jelkmann W. Erythropoietin after a century of research: younger than ever. Eur. J. Haematol. 2007, 78:183-205.
18. Kong D., Zhuo L., Gao C., Shi S., Wang N., Huang Z., Li W., Hao L. Erythropoietin protects against cisplatin-induced nephrotoxicity by attenuating endoplasmic reticulum stress-induced apoptosis. J. Nephrol. 2013, 26:219-227.
19. Langford M.P., McGee D.J., Ta K.H., Redens T.B., Texada D.E. Multiple caspases mediate acute renal cell apoptosis induced by bacterial cell wall components. Renal Fail. 2011, 33:192-206.
20. Legrand M., Bezemer R., Kandil A., Demirci C., Payen D., Ince C. The role of renal hypoperfusion in development of renal microcirculatory dysfunction in endotoxemic rats. Intensive Care Med. 2011, 37:1534-1542.
21. Martinou J.C., Green D.R. Breaking the mitocondrial barrier. Nat. Rev. Mol. Cell Biol. 2001, 2:63-67.
22. Mitra A., Bansal S., Wang W., Falk S., Zolty E., Schrier R.W. Erythropoietin ameliorates renal dysfunction during endotoxaemia. Nephrol. Dial. Transpl. 2007, 22:2349-2353.
23. Mohamed H.E., El-Swefy S.E., Mohamed R.H., Ghanim A.M.H. Effect of erythropoietin therapy on the progression of cisplatin induced renal injury in rats. Exp. Toxicol. Pathol. 2013, 65:197-203.
24. Moore E.M., Bellomo R., Nichol A.D. Erythropoietin as a novel brain and kidney protective agent. Anaesth. Intensive Care 2011, 39:356-372.
25. Nagai A., Nakagawa E., Choi H.B., Hatori K., Kobayashi S., Kim S.U. Erythropoietin and erythropoietin receptors in human CNS neurons, astrocytes, microglia, and oligodendrocytes grown in culture. J. Neuropathol. Exp. Neurol. 2001, 60:386-392.
26. Nakazawa Y., Nishino T., Obata Y., Nakazawa M., Furusu A., Abe K., Miyazaki M., Koji T., Kohno S. Recombinant human erythropoietin attenuates renal tubulointerstitial injury in murine adriamycin-induced nephropathy. J. Nephrol. 2013, 26:527-533.
27. Pallet N., Bouvier N., Legendre C., Beaune P., Thervet E., Choukroun G. Antiapoptotic properties of recombinant human erythropoietin protects against tubular cyclosporine toxicity. Pharmacol. Res. 2010, 61:71-75.
28. Parson M.J., Green D.R. Mitochondria in cell death. Essays Biochem. 2010, 47:99-114.
29. Pessoa de Souza A.C., Volpini R.A., Shimizu M.H., Sanches T.R., Camara N.O., Semedo P., Rodrigues C.E., Seguro A.C., Andrade L. Erythropoietin prevents sepsis-related acute kidney injury in rats by inhibiting NF-κB and upregulating endothelial nitric oxide synthase. Am. J. Physiol. Renal Physiol. 2012, 302:1045-1054.
30. Salahudeen A.K., Haider N., Jenkins J., Joshi M., Patel H., Huang H., Yang M., Zhe H. Antiapoptotic properties of erythropoiesis-stimulating proteins in models of cisplatin-induced acute kidney injury. Am. J. Physiol. Renal Physiol. 2008, 294:1354-1365.
31. Schrier R.W., Wang W. Acute renal failure and sepsis. N. Engl. J. Med. 2004, 351:159-169.
32. Sharples E.J., Patel N., Brown P., Stewart K., Motha-Philipe H., Sheaff M., Kieswich J., Allen D., Harwood S., Raftery M., Thiemermann C., Yagoob M.M. Erythropoietin protects the kidney against the injury and dysfunction caused by ischemia-reperfusion. J. Am. Sol. Nephrol. 2004, 15:2115-2124.
33. Song Y.R., Lee T., You S.J., Chin H.J., Chae D.W., Lim C., Park K.H., Han S., Kim J.H., Na K.Y. Prevention of acute kidney injury by erythropoietin in patients undergoing coronary artery bypass grafting: a pilot study. Am. J. Nephrol. 2009, 30:253-260.
34. Stoyanoff T.R., Todaro J.S., Aguirre M.V., Brandan N.C. Cell stress, hypoxic response and apoptosis in murine adriamycin-induced nephropathy. J. Pharmacol. Toxicol. 2012, 7:344-358.
35. Vesey D.A., Cheung C., Pat B., Endre Z., Gobé G., Johnson D.W. Erythropoietin protects against ischaemic acute renal injury. Nephrol. Dial. Transpl. 2004, 19:348-355.
36. Wan L., Bellomo R., Di Giantomasso D., Ronco C. The pathogenesis of septic acute renal failure. Curr. Opin. Crit. Care 2003, 9:496-502.
37. Wang W., Faubel S., Ljubanovic D., Mitra A., Falk S.A., Kim J., Tao Y., Soloviev A., Reznikov L.L., Dinarello C.A., Schrier R.W., Edelstein C.L. Endotoxemic acute renal failure is attenuated in caspase-1-deficient mice. Am. J. Physiol. Renal Physiol. 2005, 288:997-1004.
38. Wang W., Zhang J. Protective effect of erythropoietin against aristolochic acid-induced apoptosis in renal tubular epithelial cells. Eur. J. Pharmacol. 2008, 588:135-140.
39. Westenfelder C., Biddle D.L., Baranowski R.L. Human, rat, and mouse kidney cells express functional erythropoietin receptors. Kidney Int. 1999, 55:808-820.
40. Wu L., Gokden N., Mayeux P.R. Evidence for the role of reactive nitrogen species in polymicrobial sepsis-induced renal peritubular capillary dysfunction and tubular injury. J. Am. Soc. Nephrol. 2007, 18:1807-1815.
41. Wu X., Guo R., Wang Y., Cunningham P.N. The role of ICAM-1 in endotoxin-induced acute renal failure. Am. J. Physiol. Renal Physiol. 2007, 293:1262-1271.
42. Yang C.W., Li C., Jung J.Y., Shin S.J., Choi B.S., Lim S.W., Sun B.K., Kim Y.S., Kim J., Chang Y.S., Bang B.K. Preconditioning with erythropoietin protects against subsequent ischemia-reperfusion injury in rat kidney. FASEB J. 2003, 17:1754-1755.