Heme oxygenase-1 is a cGMP-inducible endothelial protein and mediates the cytoprotective action of nitric oxide

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 20, Issue 5, 2000, Pages 1209-1215

  Polte, Tobias ^b   Abate, Aida ^b   Dennery, Phyllis A ^a   Schröder, Henning ^a,b  

^a MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

CGMP; Cytoprotection; Endothelial cells; Heme oxygenase 1; Nitric oxide

Indexed keywords

1H 1,2,4 OXADIAZOLO[4,3 A]QUINOXALIN 1 ONE; 8 BROMO CYCLIC GMP; ANTISENSE OLIGONUCLEOTIDE; ATRIAL NATRIURETIC FACTOR; CYCLIC GMP; DIBUTYRYLCYTIDINE 3',5' PHOSPHATE; GUANYLATE CYCLASE ACTIVATOR; GUANYLATE CYCLASE INHIBITOR; HEME OXYGENASE; HEME OXYGENASE INHIBITOR; LINSIDOMINE; MOLSIDOMINE; N ACETYL S NITROSOPENICILLAMINE; NITRIC OXIDE; NITRIC OXIDE DONOR; OLIGODEOXYNUCLEOTIDE PHOSPHOROTHIOATE; PROTOPORPHYRIN TIN; SCAVENGER; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANTIINFLAMMATORY ACTIVITY; ANTIOXIDANT ACTIVITY; ARTICLE; CATTLE; CELL PROTECTION; CELL VIABILITY; CONTROLLED STUDY; CYTOTOXICITY; ENDOTHELIUM CELL; ENZYME ACTIVITY; GENE TARGETING; NONHUMAN; PRIORITY JOURNAL; PROTEIN INDUCTION; PULMONARY ARTERY; SECOND MESSENGER; WESTERN BLOTTING;

EID: 0034063564     PISSN: 10795642     EISSN: None     Source Type: Journal    
DOI: 10.1161/01.ATV.20.5.1209     Document Type: Article

References (50)

1. Moncada S, Palmer RMJ, Higgs EA. Nitric oxide: physiology, pathophysiology and pharmacology. Pharmocol Rev. 1991;43:109-142.
2. Wink DA, Hanbauer I, Krishna MC, DeGraff W, Gamson J, Mitchell JB. Nitric oxide protects against cellular damage and cytotoxicity from reactive oxygen species. Proc Natl Acad Sci U S A. 1993;90:9813-9817.
3. Motterlini R, Foresti R, Intaglietta M, Winslow RM. NO-mediated activation of heme oxygenase: endogenous cytoprotection against oxidative stress to endothelium. Am J Physiol. 1996;270:H107-H114.
4. Polte T, Oberle S, Schröder H. Nitric oxide protects endothelial cells from tumor necrosis factor-α-mediated cytotoxicity: possible involvement of cyclic GMP. FEBS Lett. 1997;409:46-48.
5. Polte T, Schröder H. Cyclic AMP mediates endothelial protection by nitric oxide. Biochem Biophys Res Commun. 1998;251:460-465.
6. Beckman JS, Koppenol WH. Nitric oxide, superoxide, and peroxynitrite: the good, the bad, and the ugly. Am J Physiol. 1996;271:C1424-C1437.
7. Dimmeler S, Haendeler J, Nehls M, Zeiher AM. Suppression of apoptosis by nitric oxide via inhibition of interleukin-1beta-converting enzyme (ICE)-like and cysteine protease protein (CPP)-32-like proteases. J Exp Med. 1997;185: 601-607.
8. Kim YM, Talanian RV, Billiar TR. Nitric oxide inhibits apoptosis by preventing increases in caspase-3-like activity via two distinct mechanisms. J Biol Chem. 1997;272:31138-31148.
9. Shen YH, Wang XL, Wilcken DEL. Nitric oxide induces and inhibits apoptosis through different pathways. FEBS Lett. 1998;433:125-131.
10. Genaro AM, Hortelano S, Alvarez A, Martinez C, Bosca L. Splenic B lymphocyte programmed cell death is prevented by nitric oxide release through mechanisms involving sustained Bcl-2 levels. J Clin Invest. 1995; 95:1884-1890.
11. Sciorati C, Rovere P, Ferrarini M, Heltai S, Manfredi AA, Clementi E. Autocrine nitric oxide modulates CD95-induced apoptosis in gammadelta T lymphocytes. J Biol Chem. 1997;272:23211-23215.
12. Moro MA, FernandezTome P, Leza JC, Lorenzo P, Lizasoain I. Neuronal death induced by SIN-1 in the presence of superoxide dismutase: protection by cyclic GMP. Neuropharmacology. 1998;37:1071-1079.
13. Thippeswamy T, Morris R. Cyclic guanosine 3′,5′-monophosphate-mediated neuroprotection by nitric oxide in dissociated cultures of rat dorsal root ganglion neurones. Brain Res. 1997;774:116-122.
14. Pantazis NJ, West JR, Dai D. The nitric oxide-cyclic GMP pathway plays an essential role in both promoting cell survival of cerebellar granule cells in culture and protecting the cells against ethanol neurotoxicity. J Neurochem. 1998;70:1826-1838.
15. Estevez AG, Spear N, Thompson JA, Cornwell RL, Radi R, Barbeito L, Beckman JS. Nitric oxide-dependent production of cGMP supports the survival of rat embryonic motor neurons cultured with brain-derived neurotrophic factor. J Neurosci. 1998;18:3708-3714.
16. Oberle S, Schröder H. Ferritin may mediate SIN-1-induced protection against oxidative stress. Nitric Oxide. 1997;1:308-314.
17. Kim YM, Bergoma H, Lancaster JR Jr. Nitrogen oxide-induced autoprotection in isolated rat hepatocytes. FEBS Lett. 1995;374:228-232.
18. Maines MD. The heme oxygenase system: a regulator of second messenger gases. Annu Rev Pharmacol Toxicol. 1997;37:517-554.
19. Platt JL, Nath KA. Heme oxygenase: protective gene or Trojan horse. Nat Med. 1998;4:1364-1365.
20. Willis D, Moore AR, Frederick R, Willoughby DA. Heme oxygenase: a novel target for the modulation of the anti-inflammatory response. Nat Med. 1996;2:87-90.
21. Hancock WW, Buelow R, Sayegh MH, Turka LA. Antibody-induced transplant arteriosclerosis is prevented by graft expression of anti-oxidant and anti-apoptotic genes. Nat Med. 1998;4:1392-1396.
22. Soares MP, Lin Y, Anrather J, Csizmadia E, Takigami K, Sato K, Grey ST, Colvin RB, Choi AM, Poss KD, Bach FH. Expression of heme oxygenase-1 can determine cardiac xenograft survival. Nat Med. 1998;4:1073-1077.
23. Ye J, Laychock SG. A protective role for heme oxygenase expression in pancreatic islets exposed to interleukin-1 beta. Endocrinology. 1998;139:4155-4163.
24. Yachie A, Niida Y, Wada T, Igarashi N, Kaneda H, Toma T, Ohta K, Kasahara Y, Koizumi S. Oxidative stress causes enhanced endothelial cell injury in human heme oxygenase-1 deficiency. J Clin Invest. 1999;103:129-135.
25. Yee EL, Pitt BR, Billiar TR, Kim YM. Effect of nitric oxide on heme metabolism in pulmonary artery endothelial cells. Am J Physiol. 1996;271: L512-L518.
26. Durante W, Kroll MH, Christodoulides N, Peyton KJ, Schafer AI. Nitric oxide induces heme oxygenase-1 gene expression and carbon monoxide production in vascular smooth muscle cells. Circ Res. 1997;80:557-564.
27. Durante W, Christodoulides N, Cheng K, Peyton KJ, Sunahara RK, Schafer AI. cAMP induces heme oxygenase 1 gene expression and carbon monoxide production in vascular smooth muscle. Am J Physiol. 1997;273:H317-H323.
28. Dimmeler S, Zeiher AM. Nitric oxide and apoptosis: another paradigm for the double-edged role of nitric oxide. Nitric Oxide. 1997;1:275-281.
29. Nishikawa M, Takeda K, Sato EF, Kuroki T, Inoue M. Nitric oxide regulates energy metabolism and Bcl-2 expression in intestinal epithelial cells. Am J Physiol. 1998;274:G797-G801.
30. Dennery PA, Sridhar KJ, Lee CS, Wong HE, Shokoohi V, Rodgers PA, Spitz DR. Heme oxygenase-mediated resistance to oxygen toxicity in hamster fibroblasts. J Biol Chem. 1997;272:14937-14942.
31. Oberle S, Polte T, Abate A, Podhaisky H-P, Schröder H. Aspirin increases ferritin synthesis in endothelial cells: a novel antioxidant pathway. Circ Res. 1998;82:1016-1020.
32. Flick DA, Gifford GE. Comparison of in vitro cell cytotoxic assays for tumor necrosis factor. J Immunol Methods. 1984;68:167-175.
33. Wink DA, Cook JA, Pacelli R, DeGraff W, Gamson J, Liebmann J, Krishna MC, Mitchell JB. The effect of various nitric oxide-donor agents on hydrogen peroxide-mediated toxicity: a direct correlation between nitric oxide formation and protection. Arch Biochem Biophys. 1996;331:241-248.
34. Schuger L, Varani J, Marks RM, Kunkel SL, Johnson KJ, Ward PA. Cytotoxicity of tumor necrosis factor-α for human umbilical endothelial cells. Lab Invest. 1989;61:62-68.
35. Goossens V, Grooten J, De Vos K, Fiers W. Direct evidence for tumor necrosis factor-induced mitochondrial reactive oxygen intermediates and their involvement in cytotoxicity. Proc Natl Acad Sci U S A. 1995;92: 8115-8119.
36. Schröder H, Warren S, Bargetzi MJ, Torti SV, Torti FM. N-Acetyl-L-cysteine protects endothelial cells but not L929 tumor cells from tumor necrosis factor-α-mediated cytotoxicity. Naunyn Schmiedebergs Arch Pharmacol. 1993;347:664-666.
37. Feelisch M, Stamler JS. Donors of nitrogen oxides. In: Feelisch M, Stamler JS, eds. Methods in Nitric Oxide Research. Chichester, NY: John Wiley & Sons Inc; 1996:71-115.
38. Singh RJ, Hogg N, Joseph J, Konorev E, Kalyanaraman B. The peroxynitrite generator, SIN-1, becomes a nitric oxide donor in the presence of electron acceptors. Arch Biochem Biophys. 1999;361:331-339.
39. Akaike T, Maeda H. Quantitation of nitric oxide using 2-pheny1,4,5,5-tetramethylimidazoline-1-oxyl 3-oxide (PTIO). Methods Enzymol. 1996;268: 211-221.
40. Moro MA, Russel RJ, Cellek S, Lizasoain I, Su Y, Darley-Usmar VM, Radomski MW, Moncada S. cGMP mediates the vascular and platelet actions of nitric oxide: confirmation using an inhibitor of the soluble guanylyl cyclase. Proc Natl Acad Sci U S A. 1996;93:1480-1485.
41. Immenschuh S, Hinke V, Ohlmann A, Gifhorn-Katz S, Katz N, Jungermann K, Kietzmann T. Transcriptional activation of the haem oxygenase-1 gene by cGMP via a cAMP response element activator protein-1 element in primary cultures of rat hepatocytes. Biochem J. 1998;334:141-146.
42. Schröder H, Ney P, Woditsch I, Schrör K. Cyclic GMP mediates SIN-1-induced inhibition of human polymorphonuclear leukocytes. Eur J Pharmacol. 1990;182:211-218.
43. Takahashi K, Hara E, Ogawa K, Kimura D, Fujita H, Shibahara S. Possible implications of the induction of human heme oxygenase-1 by nitric oxide donors. J Biochem (Tokyo). 1997;121:1162-1168.
44. Leitman DC, Agnost VL, Catalano RM, Schröder H, Waldman SA, Bennett BM, Tuan JJ, Murad F. Atrial natriuretic peptide, oxytocin, and vasopressin increase guanosine 3′,5′-monophosphate in LLC-PK1 kidney epithelial cells. Endocrinology. 1988;122:1478-1485.
45. Schröder H, Leitman DC, Bennett BM, Waldman SA, Murad F. Glyceryl trinitrate-induced desensitization of guanylate cyclase in cultured rat lung fibroblasts. J Pharmacol Exp Ther. 1988;245:413-418.
46. Cedidi C, Meyer M, Kuse ER, Schulz-Knappe P, Ringe B, Frei U, Pichlmayr R, Forssmann WG. Urodilatin: a new approach for the treatment of therapy-resistant acute renal failure after liver transplantation. Eur J Clin Invest. 1994;24:632-639.
47. Gianello P, Carlier M, Jamart J, Hulhoven R, Bernheim J, Bernard A, Ketelslegers JM, Squifflet JP. Effect of 1-28 alpha-h atrial natriuretic peptide on acute renal failure in cadaveric renal transplantation. Clin Transplant. 1995;9:481-489.
48. Immenschuh S, Kietzmann T, Hinke V, Wiederhold M, Katz N, Muller-Eberhard U. The rat heme oxygenase-1 gene is transcriptionally induced via the protein kinase a signaling pathway in rat hepatocyte cultures. Mol Pharmacol. 1998;53:483-491.
49. Pilz RB, Suhasini M, Idriss S, Meinkoth JL, Boss GR. Nitric oxide and cGMP analogs activate transcription from AP-1-responsive promoters in mammalian cells. FASEB J. 1995;9:552-558.
50. Alam J, Den Z. Distal AP-1 binding sites mediate basal level enhancement and TPA induction of the mouse heme oxygenase-1 gene. J Biol Chem. 1992;267:21894-21900.