Heme oxygenase-1 is induced by thyroid hormone and involved in thyroid hormone preconditioning-induced protection against renal warm ischemia in rat

Molecular and Cellular Endocrinology

Volumn 339, Issue 1-2, 2011, Pages 54-62

  Li, Fei ^a   Lu, Shuyan ^a   Zhu, Ruixia ^a   Zhou, Zhongxin ^a   Ma, Lingdi ^a   Cai, Leiming ^a   Liu, Zhiyuan ^b  

^a THE AFFILIATED CHANGZHOU NO 2 PEOPLE S HOSPITAL OF NANJING MEDICAL UNIVERSITY   (China)

^b Wujin Hospital Affiliated with Jiangsu University   (China)

Author keywords

3,3 ,5 Triiodo l thyronine; Heat shock protein 32; Ischemia reperfusion; Kidney preconditioning; Oxidative stress

Indexed keywords

CREATININE; GLUTATHIONE; HEME OXYGENASE 1; LIOTHYRONINE; MALONALDEHYDE; NITROGEN; UREA;

ADULT ANIMAL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CREATININE BLOOD LEVEL; ENZYME INDUCTION; ISCHEMIC PRECONDITIONING; KIDNEY DYSFUNCTION; KIDNEY INJURY; KIDNEY ISCHEMIA; KIDNEY PARENCHYMA; MALE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; RENAL PROTECTION; REPERFUSION INJURY; SINGLE DRUG DOSE; THYROID HORMONE BLOOD LEVEL; UREA NITROGEN BLOOD LEVEL;

ANIMALS; GENE EXPRESSION; GLUTATHIONE; HEME OXYGENASE-1; KIDNEY; KIDNEY TUBULES; MALE; MALONDIALDEHYDE; OXIDATIVE STRESS; RATS; RATS, SPRAGUE-DAWLEY; REPERFUSION INJURY; TRIIODOTHYRONINE;

EID: 79958038489     PISSN: 03037207     EISSN: 18728057     Source Type: Journal    
DOI: 10.1016/j.mce.2011.03.019     Document Type: Article

References (45)

1. Cao C., Wang S., Fan L., et al. Renal protection by ischemic preconditioning is associated with p50/p50 homodimers. Am. J. Nephrol. 2010, 31(1):1-8.
2. Chen X., Liu X., Wan X., et al. Ischemic preconditioning attenuates renal ischemia-reperfusion injury by inhibiting activation of ikkbeta and inflammatory response. Am. J. Nephrol. 2009, 30(3):287-294.
3. Choi A.M., Alam J. Heme oxygenase-1: function, regulation, and implication of a novel stress-inducible protein in oxidant-induced lung injury. Am. J. Respir. Cell Mol. Biol. 1996, 15(1):9-19.
4. Colville-Nash P.R., Qureshi S.S., Willis D., et al. Inhibition of inducible nitric oxide synthase by peroxisome proliferator-activated receptor agonists: correlation with induction of heme oxygenase 1. J. Immunol. 1998, 161(2):978-984.
5. Droge W. Free radicals in the physiological control of cell function. Physiol. Rev. 2002, 82(1):47-95.
6. Ferenbach D.A., Kluth D.C., Hughes J. Hemeoxygenase-1 and renal ischaemia-reperfusion injury. Nephron. Exp. Nephrol. 2010, 115(3):e33-e37.
7. Fernandez V., Videla L.A. Influence of hyperthyroidism on superoxide radical and hydrogen peroxide production by rat liver submitochondrial particles. Free Radic. Res. Commun. 1993, 18(6):329-335.
8. Fernandez V., Barrientos X., Kipreos K., et al. Superoxide radical generation, nadph oxidase activity, and cytochrome p-450 content of rat liver microsomal fractions in an experimental hyperthyroid state: relation to lipid peroxidation. Endocrinology 1985, 117(2):496-501.
9. Fernandez V., Cornejo P., Tapia G., et al. Influence of hyperthyroidism on the activity of liver nitric oxide synthase in the rat. Nitric Oxide 1997, 1(6):463-468.
10. Fernandez V., Tapia G., Varela P., et al. Thyroid hormone-induced oxidative stress in rodents and humans: a comparative view and relation to redox regulation of gene expression. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 2006, 142(3-4):231-239.
11. Fernandez V., Castillo I., Tapia G., et al. Thyroid hormone preconditioning: protection against ischemia-reperfusion liver injury in the rat. Hepatology 2007, 45(1):170-177.
12. Fernandez V., Tapia G., Varela P., et al. Causal role of oxidative stress in liver preconditioning by thyroid hormone in rats. Free Radic. Biol. Med. 2008, 44(9):1724-1731.
13. Fernandez V., Tapia G., Varela P., et al. Upregulation of liver inducible nitric oxide synthase following thyroid hormone preconditioning: suppression by n-acetylcysteine. Biol. Res. 2009, 42(4):487-495.
14. Franco-Gou R., Rosello-Catafau J., Casillas-Ramirez A., et al. How ischaemic preconditioning protects small liver grafts. J. Pathol. 2006, 208(1):62-73.
15. Fujii S., Sawa T., Ihara H., et al. The critical role of nitric oxide signaling, via protein s-guanylation and nitrated cyclic gmp, in the antioxidant adaptive response. J. Biol. Chem. 2010, 285(31):23970-23984.
16. Goligorsky M.S., Brodsky S.V., Noiri E. Nitric oxide in acute renal failure: nos versus nos. Kidney Int. 2002, 61(3):855-861.
17. Gozzelino R., Jeney V., Soares M.P. Mechanisms of cell protection by heme oxygenase-1. Annu. Rev. Pharmacol. Toxicol. 2010, 50:323-354.
18. Gurer A., Ozdogan M., Gomceli I., et al. Hyperbaric oxygenation attenuates renal ischemia-reperfusion injury in rats. Transplant. Proc. 2006, 38(10):3337-3340.
19. Huh K., Kwon T.H., Kim J.S., et al. Role of the hepatic xanthine oxidase in thyroid dysfunction: effect of thyroid hormones in oxidative stress in rat liver. Arch. Pharm. Res. 1998, 21(3):236-240.
20. Katori M., Busuttil R.W., Kupiec-Weglinski J.W. Heme oxygenase-1 system in organ transplantation. Transplantation 2002, 74(7):905-912.
21. Kurauchi Y., Hisatsune A., Isohama Y., et al. Nitric oxide-cyclic gmp signaling pathway limits inflammatory degeneration of midbrain dopaminergic neurons: Cell type-specific regulation of heme oxygenase-1 expression. Neuroscience 2009, 158(2):856-866.
22. Li C.Q., Kim M.Y., Godoy L.C., et al. Nitric oxide activation of keap1/nrf2 signaling in human colon carcinoma cells. Proc Natl Acad Sci U S A 2009, 106(34):14547-14551.
23. Li Volti G., Sorrenti V., Murabito P., et al. Pharmacological induction of heme oxygenase-1 inhibits inos and oxidative stress in renal ischemia-reperfusion injury. Transplant. Proc. 2007, 39(10):2986-2991.
24. Mishra J., Mori K., Ma Q., et al. Amelioration of ischemic acute renal injury by neutrophil gelatinase-associated lipocalin. J. Am. Soc. Nephrol. 2004, 15(12):3073-3082.
25. Pacher P., Beckman J.S., Liaudet L. Nitric oxide and peroxynitrite in health and disease. Physiol. Rev. 2007, 87(1):315-424.
26. Pamplona A., Ferreira A., Balla J., et al. Heme oxygenase-1 and carbon monoxide suppress the pathogenesis of experimental cerebral malaria. Nat. Med. 2007, 13(6):703-710.
27. Pantos C.I., Malliopoulou V.A., Mourouzis I.S., et al. Long-term thyroxine administration increases heat stress protein-70 mrna expression and attenuates p38 map kinase activity in response to ischaemia. J. Endocrinol. 2001, 170(1):207-215.
28. Pantos C.I., Malliopoulou V.A., Mourouzis I.S., et al. Long-term thyroxine administration protects the heart in a pattern similar to ischemic preconditioning. Thyroid 2002, 12(4):325-329.
29. Pantos C., Malliopoulou V., Mourouzis I., et al. Thyroxine pretreatment increases basal myocardial heat-shock protein 27 expression and accelerates translocation and phosphorylation of this protein upon ischaemia. Eur. J. Pharmacol. 2003, 478(1):53-60.
30. Pantos C., Malliopoulou V., Paizis I., et al. Thyroid hormone and cardioprotection: study of p38 mapk and jnks during ischaemia and at reperfusion in isolated rat heart. Mol. Cell. Biochem. 2003, 242(1-2):173-180.
31. Pantos C., Malliopoulou V., Mourouzis I., et al. Hyperthyroid hearts display a phenotype of cardioprotection against ischemic stress: a possible involvement of heat shock protein 70. Horm. Metab. Res. 2006, 38(5):308-313.
32. Platt J.L., Nath K.A. Heme oxygenase: protective gene or trojan horse. Nat. Med. 1998, 4(12):1364-1365.
33. Redaelli C.A., Tian Y.H., Schaffner T., et al. Extended preservation of rat liver graft by induction of heme oxygenase-1. Hepatology 2002, 35(5):1082-1092.
34. Sikorski E.M., Hock T., Hill-Kapturczak N., et al. The story so far: molecular regulation of the heme oxygenase-1 gene in renal injury. Am. J. Physiol. Renal. Physiol. 2004, 286(3):F425-F441.
35. Soares M.P., Bach F.H. Heme oxygenase-1 in organ transplantation. Front. Biosci. 2007, 12:4932-4945.
36. Tapia G., Fernandez V., Pino C., et al. The acute-phase response of the liver in relation to thyroid hormone-induced redox signaling. Free Radic. Biol. Med. 2006, 40(9):1628-1635.
37. Tapia G., Santibanez C., Farias J., et al. Kupffer-cell activity is essential for thyroid hormone rat liver preconditioning. Mol. Cell. Endocrinol. 2010, 323(2):292-297.
38. Trushin S.A., Pennington K.N., Carmona E.M., et al. Protein kinase calpha (pkcalpha) acts upstream of pkctheta to activate ikappab kinase and nf-kappab in t lymphocytes. Mol. Cell. Biol. 2003, 23(19):7068-7081.
39. Venditti P., Di Meo S. Thyroid hormone-induced oxidative stress. Cell. Mol. Life Sci. 2006, 63(4):414-434.
40. Videla L.A. Energy metabolism, thyroid calorigenesis, and oxidative stress: functional and cytotoxic consequences. Redox Rep. 2000, 5(5):265-275.
41. Wagner M., Cadetg P., Ruf R., et al. Heme oxygenase-1 attenuates ischemia/reperfusion-induced apoptosis and improves survival in rat renal allografts. Kidney Int. 2003, 63(4):1564-1573.
42. Wang W.P., Guo X., Koo M.W., et al. Protective role of heme oxygenase-1 on trinitrobenzene sulfonic acid-induced colitis in rats. Am. J. Physiol. Gastrointest. Liver Physiol. 2001, 281(2):G586-G594.
43. Yamashita J., Ogata M., Itoh M., et al. Role of nitric oxide in the renal protective effects of ischemic preconditioning. J. Cardiovasc. Pharmacol. 2003, 42(3):419-427.
44. Yeo P.P., Lewis M., Evered D.C. Radioimmunoassay of free thyroid hormone concentrations in the investigation of thyroid disease. Clin. Endocrinol. (Oxf.) 1977, 6(2):159-165.
45. Zeynalov E., Shah Z.A., Li R.C., et al. Heme oxygenase 1 is associated with ischemic preconditioning-induced protection against brain ischemia. Neurobiol. Dis. 2009, 35(2):264-269.