Antiapoptotic effect of haem oxygenase-1 induced by nitric oxide in experimental solid tumour

British Journal of Cancer

Volumn 88, Issue 6, 2003, Pages 902-909

  Tanaka, S ^a   Akaike, T ^a   Fang, J ^a   Beppu, T ^a   Ogawa, M ^a   Tamura, F ^a   Miyamoto, Y ^a   Maeda, H ^a  

^a KUMAMOTO UNIV SCHOOL OF MEDICINE   (Japan)

Author keywords

Antiapoptosis; Haem oxygenase; Nitric oxide; Oxidative stress; Tumour growth

Indexed keywords

BILIRUBIN; CASPASE 3; CASPASE 3 INHIBITOR; HEME OXYGENASE 1; N ACETYL S NITROSOPENICILLAMINE; NITRIC OXIDE; PROPYLAMINE; PROTOPORPHYRIN TIN; PROTOPORPHYRIN ZINC;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL PROTECTION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INDUCTION; HEPATOMA CELL; MALE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; RAT; SOLID TUMOR; TUMOR BLOOD FLOW; TUMOR GROWTH; WESTERN BLOTTING;

ANIMALS; APOPTOSIS; BLOTTING, WESTERN; CARCINOMA, HEPATOCELLULAR; GENE EXPRESSION REGULATION; HEME OXYGENASE (DECYCLIZING); HEME OXYGENASE-1; HUMANS; LIVER NEOPLASMS; MALE; MEMBRANE PROTEINS; NEOPLASMS, EXPERIMENTAL; NITRIC OXIDE; OXIDATIVE STRESS; RATS; UP-REGULATION;

EID: 0037464355     PISSN: 00070920     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.bjc.6600830     Document Type: Article

References (44)

1. Akaike T, Inoue K, Okamoto T, Nishino H, Otagiri M, Fujii S, Maeda H (1997) Nanomolar quantification and identification of various nitrosothiols by high performance liquid chromatography coupled with flow reactors of metals and Griess reagent. J Biochem 122: 459-466
2. Bastian NR, Yim CY, Hibbs Jr JB, Samlowski WE (1994) Induction of iron-derived EPR signals in murine cancers by nitric oxide. Evidence for multiple intracellular targets. J Biol Chem 269: 5127-5131
3. Bouton C, Demple B (2000) Nitric oxide-inducible expression of haem oxygenase-1 in human cells. J Biol Chem 275: 32688-32693
4. Buttke TM, Sandstrom PA (1994) Oxidative stress as a mediator of apoptosis. Immunol Today 15: 7-10
5. Dennery PA, Sridhar KJ, Lee CS, Wong HE, Shokoohi V, Rodgers PA, Spitz DR (1997) Haem oxygenase-mediated resistance to oxygen toxicity in hamster fibroblasts. J Biol Chem 272: 14937-14942
6. Doi K, Akaike T, Fujii S, Tanaka S, Ikebe N, Beppu T, Shibahara S, Ogawa M, Maeda H (1999) Induction of haem oxygenase-1 nitric oxide and ischaemia in experimental solid tumours and implications for tumour growth. Br J Cancer 80: 1945-1954
7. Doi K, Akaike T, Horie H, Noguchi Y, Fujii S, Beppu T, Ogawa M, Maeda H (1996) Excessive production of nitric oxide in rat solid tumour and its implication in rapid tumour growth. Cancer 77: 1598-1604
8. Dore S, Takahashi M, Ferris CD, Zakhary R, Hester LD, Guastella D, Snyder SH (1999) Bilirubin, formed by activation of haem oxygenase-2, protects neurons against oxidative stress injury. Proc Natl Acad Sci USA 96: 2445-2450
9. Drummond GS, Kappas A (1981) Prevention of neonatal hyperbilirubinemia by tin protoporphyrin IX, a potent competitive inhibitor of haem oxidation. Proc Natl Acad Sci USA 78: 6466-6470
10. Elbashir SM, Harborth J, Lendeckel W, Yalcin A, Weber K, Tuschl T (2001) Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Nature 411: 494-498
11. Enari M, Talanian RV, Wong WW, Nagata S (1996) Sequential activation of ICE-like and CPP32-like proteases during Fas-mediated apoptosis. Nature 380: 723-726
12. Foresti R, Motterlini R (1999) The haem oxygenase pathway and its interaction with nitric oxide in the control of cellular homeostasis. Free Radicals Res 31: 459-475
13. Gourley GR (1997) Bilirubin metabolism and kernicterus. Adv Pediatr 44: 173-229
14. Hancock WW, Buelow R, Sayegh MH, Turka LA (1998) Antibody-induced transplant arteriosclerosis is prevented by graft expression of antioxidant and anti-apoptotic genes. Nat Med 4: 1392-1396
15. 1-protease inhibitor on hepatic ischemia-reperfusion injury. J Pharmacol Exp Ther 295: 904-911
16. Jenkins DC, Charles IG, Thomsen LL, Moss DW, Holmes LS, Baylis SA, Rhodes P, Wetmore K, Emson PC, Moncada S (1995) Role of nitric oxide in tumour growth. Proc Natl Acad Sci USA 92: 4392-4396
17. Keyse SM, Tyrrell RM (1989) Haem oxygenase is the major 32-kDa stress protein induced in human skin fibroblasts by UVA radiation, hydrogen peroxide, and sodium arsenite. Proc Natl Acad Sci USA 86: 99-103
18. Kim YM, Bergonia H, Lancaster Jr JR (1995) Nitrogen oxide-induced autoprotection in isolated rat hepatocytes. FEBS Lett 374: 228-232
19. Kimura M, Matsumura Y, Konno T, Miyauchi Y, Maeda H (1990) Enzymatic removal of bilirubin toxicity by bilirubin oxidase in vitro and excretion of degradation products in vivo. Proc Soc Exp Biol Med 195: 64-69
20. Lutton JD, Abraham NG, Drummond GS, Levere RD, Kappas A (1997) Zinc porphyrins: potent inhibitors of hematopoiesis in animal and human bone marrow. Proc Natl Acad Sci USA 94: 1432-1436
21. Maines MD (1997) The haem oxygenase system: a regulator of second messenger gases. Annu Rev Pharmacol Toxicol 37: 517-554
22. Mannick JB, Asano K, Izumi K, Kieff E, Stamler JS (1994) Nitric oxide produced by human B lymphocytes inhibits apoptosis and Epstein-Barr virus reactivation. Cell 79: 1137-1146
23. Minetti M, Mallozzi C, Di Stasi AM, Pietraforte D (1998) Bilirubin is an effective antioxidant of peroxynitrite-mediated protein oxidation in human blood plasma. Arch Biochem Biophys 352: 165-174
24. Mitani K, Fujita H, Fukuda Y, Kappas A, Sassa S (1993) The role of inorganic metals and metalloporphyrins in the induction of haem oxygenase and heat-shock protein 70 in human hepatoma cells. Biochem J 290: 819-825
25. Motterlini R, Foresti R, Bassi R, Calabrese V, Clark JE, Green CJ (2000) Endothelial haem oxygenase-1 induction by hypoxia. Modulation by inducible nitric-oxide synthase and S-nitrosothiols. J Biol Chem 275: 13613-13620
26. Ogura T, DeGeorge G, Tatemichi M, Esumi H (1998) Suppression of anti-microtubule agent-induced apoptosis by nitric oxide: possible mechanism of a new drug resistance. Jpn J Cancer Res 89: 199-205
27. Ohta K, Araki N, Shibata M, Hamada J, Komatsumoto S, Shimazu K, Fukuuchi Y (1994) A novel in vivo assay system for consecutive measurement of brain nitric oxide production combined with the microdialysis technique. Neurosci Lett 176: 165-168
28. Otterbein LE, Mantell LL, Choi AM (1999) Carbon monoxide provides protection against hyperoxic lung injury. Am J Physiol 276: L688-L694
29. Petrache I, Otterbein LE, Alam J, Wiegand GW, Choi AM (2000) Haem oxygenase-1 inhibits TNF-α-induced apoptosis in cultured fibroblasts. Am J Physiol 278: L312-L319
30. Sahoo SK, Sawa T, Fang J, Tanaka S, Miyamoto Y, Akaike T, Maeda H (2002) Pegylated zinc protoporphyrin: a water-soluble heme oxygenase inhibitor with tumour-targeting capacity. Bioconjug Chem 13: 1031-1038
31. Schlesinger MJ (1990) Heat shock proteins. J Biol Chem 265: 12111-12114
32. Shibahara S, Muller RM, Taguchi H (1987) Transcriptional control of rat haem oxygenase by heat shock. J Biol Chem 262: 12889-12892
33. Soares MP, Lin Y, Anrather J, Csizmadia E, Takigami K, Sato K, Grey ST, Colvin RB, Choi AM, Poss KD, Bach FH (1998) Expression of haem oxygenase-1 can determine cardiac xenograft survival. Nat Med 4: 1073-1077
34. Suematsu M, Kashiwagi S, Sano T, Goda N, Shinoda Y, Ishimura Y (1994) Carbon monoxide as an endogenous modulator of hepatic vascular perfusion. Biochem Biophys Res Commun 205: 1333-1337
35. Suttner DM, Dennery PA (1999) Reversal of HO-1 related cytoprotection with increased expression is due to reactive iron. FASEB J 13: 1800-1809
36. Suttner DM, Sridhar K, Lee CS, Tomura T, Hansen TN, Dennery PA (1999) Protective effects of transient HO-1 overexpression on susceptibility to oxygen toxicity in lung cells. Am J Physiol 276: L443-L451
37. Tenhunen R, Marver HS, Schmid R (1968) The enzymatic conversion of haem to bilirubin by microsomal haem oxygenase. Proc Natl Acad Sci USA 61: 748-755
38. Tenhunen R, Marver HS, Schmid R (1970) The enzymatic catabolism of hemoglobin: stimulation of microsomal haem oxygenase by hemin. J Lab Clin Med 75: 410-421
39. ω-nitro-L-arginine, and the haemoxygenase inhibitor, zinc protoporphyrin IX, on tumour blood flow. Int J Radiat Oncol Biol Phys 42: 849-853
40. Workman P, Twentyman P, Balkwill F, Balmain A, Chaplin D, Double J, Embleton J, Newell D, Raymond R, Stables J, Stephens T, Wallace J (1998) United Kingdom Co-ordinating Committee on Cancer Research (UKCCCR) guidelines for the welfare of animals in experimental neoplasia (Second Edition). Br J Cancer 77: 1-10
41. Wu J, Akaike T, Maeda H (1998) Modulation of enhanced vascular permeability in tumours by a bradykinin antagonist, a cyclooxygenase inhibitor, and a nitric oxide scavenger. Cancer Res 58: 159-165
42. Xu Q, Hu Y, Kleindienst R, Wick G (1997) Nitric oxide induces heat-shock protein 70 expression in vascular smooth muscle cells via activation of heat shock factor 1. J Clin Invest 100: 1089-1097
43. Yang G, Nguyen X, Ou J, Rekulapelli P, Stevenson DK, Dennery PA (2001) Unique effects of zinc protoporphyrin on HO-1 induction and apoptosis. Blood 97: 1306-1313
44. Zakhary R, Gaine SP, Dinerman JL, Ruat M, Flavahan NA, Snyder SH (1996) Haem oxygenase 2: endothelial and neuronal localization and role in endothelium-dependent relaxation. Proc Natl Acad Sci USA 93: 795-798