Hypoxic regulation of inducible nitric oxide synthase via hypoxia inducible factor-1 in cardiac myocytes

Circulation Research

Volumn 86, Issue 3, 2000, Pages 319-325

  Jung, Frank ^a   Palmer, Lisa A ^a   Zhou, Nan ^a   Johns, Roger A ^a,b  

^a UNIVERSITY OF VIRGINIA HEALTH SYSTEM   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Heart; Hypoxia; Hypoxia inducible factor 1; Inducible nitric oxide synthase

Indexed keywords

HYPOXIA INDUCIBLE FACTOR 1; INTERLEUKIN 1BETA; NITRIC OXIDE SYNTHASE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL HYPOXIA; CONTROLLED STUDY; ENZYME REGULATION; GENE EXPRESSION REGULATION; HEART MUSCLE CELL; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; RAT;

EID: 0033976342     PISSN: 00097330     EISSN: None     Source Type: Journal    
DOI: 10.1161/01.RES.86.3.319     Document Type: Article

References (50)

1. Moncada S, Palmer RM, Higgs EA. Nitric oxide: physiology, pathophysiology, and pharmacology. Pharmacol Rev. 1991;43:109-142.
2. Balligand JL, Cannon PJ. Nitric oxide synthases and cardiac muscle: autocrine and paracrine influences. Arterioscler Thromb Vasc Biol. 1997; 17:1846-1858.
3. Bredt DS, Snyder SH. Nitric oxide: a physiologic messenger molecule. Annu Rev Biochem. 1994;63:175-195.
4. Ungureanu-Longrois D, Balligand JL, Kelly RA, Smith TW. Myocardial contractile dysfunction in the systemic inflammatory response syndrome: role of a cytokine-inducible nitric oxide synthase in cardiac myocytes. J Mol Cell Cardiol. 1995;27:155-167.
5. Ikeda U, Shimida K. Nitric oxide and cardiac failure. Clin Cardiol. 1997;20:837-841.
6. Dudek RR, Wildhirt S, Conforto A, Pinto V, Suzuki H, Winder S, Bing RJ. Inducible nitric oxide synthase activity in myocardium after myocardial infarction in rabbit. Biochem Biophvs Res Commun. 1994;205:1671-1680.
7. Wildhirt SM, Suzuki H, Horstman D, Weismuller S, Dudek RR, Akiyama K, Reichart B. Selective modulation of inducible nitric oxide synthase isozyme in myocardial infarction. Circulation. 1997;96:1616-1623.
8. Yang X, Chowdhury N, Cai B, Brett J, Marboe C, Sciacca RR, Michler RE, Cannon PJ. Induction of myocardial nitric oxide synthase by cardiac allograft rejection. J Clin Invest. 1994;94:714-721.
9. Haywood GA, Tsao PS, von der Leyen HE, Mann MJ, Keeling PJ, Trindade PT, Lewis NP, Byrne CD, Rickenbacher PR, Bishopric NH, Cooke JP, McKenna WJ, Fowler MB. Expression of inducible nitric oxide synthase in human heart failure. Circulation. 1996;93:1087-1094.
10. Balligand JL, Ungureanu D, Kelly RA, Kobzik L, Pimental D, Michel T, Smith TW. Abnormal contractile function due to induction of nitric oxide synthesis in rat cardiac myocytes follows exposure to activated macrophage-conditioned medium. J Clin Invest. 1993;91:2314-2319.
11. Depre C, Vanoverschelde JL, Goudemant JF, Mottet I, Hue L. Protection against ischemic injury by nonvasoactive concentrations of nitric oxide synthase inhibitors in the perfused rabbit heart. Circulation. 1995;92: 1911-1918.
12. Balligand JL, Ungureanu-Longrois D, Simmons WW, Pimentai D, Malinski TA, Kapturczak M, Taha Z, Lowenstein CJ, Davidoff AJ, Kelly RA. Cytokine-inducible nitric oxide synthase (iNOS) expression in cardiac myocytes: characterization and regulation of iNOS expression and detection of iNOS activity in single cardiac myocytes in vitro. J Biol Chem. 1994;269:27580-27588.
13. Pinsky DJ, Cai B, Yang X, Rodriguez C, Sciacca RR, Cannon PJ. The lethal effects of cytokine-induced nitric oxide on cardiac myocytes are blocked by nitric oxide synthase antagonism or transforming growth factor beta. J Clin Invest. 1995;95:677-685.
14. Takano H, Manchikalapudi S, Tang XL, Qiu Y, Rizvi A, Jadoon AK, Zhang Q, Bolli R. Nitric oxide synthase is the mediator of late preconditioning against myocardial infarction in conscious rabbits. Circulation. 1998;98:441-449.
15. Imagawa J, Yellon DM, Baxter GF. Pharmacological evidence that induciblc nitric oxide synthase is a mediator of delayed preconditioning. Br J Pharmacol. 1999;126:701-708.
16. Kitakaze M, Node K, Komamura K, Minamino T, Inoue M, Hori M, Kamada T. Evidence for nitric oxide generation in the cardiomyocytes: its augmentation by hypoxia. J Mol Cell Cardiol. 1995;27:2149-2154.
17. Schulz R, Panas DL, Catena R, Moncada S, Olley PM, Lopaschuk GD. The role of nitric oxide in cardiac depression induced by interleukin-1 beta and tumour necrosis factor-alpha. Br J Pharmacol. 1995;114:27-34.
18. Tsujino M, Hirata Y, Imai T, Kanno K, Eguchi S, Ito H, Marumo F. Induction of nitric oxide synthase gene by interleukin-1 beta in cultured rat cardiocytes. Circulation. 1994;90:375-383.
19. Kinugawa KI, Kohmoto O, Yao A, Serizawa T, Takahashi T. Cardiac inducible nitric oxide synthase negatively modulates myocardial function in cultured rat myocytes. Am J Physiol. 1997;272(1 pt 2):H35-H47.
20. Kinugawa K, Shimizu T, Yao A, Kohmoto O, Serizawa T, Takahashi T. Transcriptional regulation of inducible nitric oxide synthase in cultured neonatal rat cardiac myocytes. Circ Res. 1997;81:911-921.
21. Kacimi R, Long CS, Karliner JS. Chronic hypoxia modulates the interleukin-1beta-stimulated inducible nitric oxide synthase pathway in cardiac myocytes. Circulation. 1997;96:1937-1943.
22. Melillo G, Musso T, Sica A, Taylor LS, Cox GW, Varesio L. A hypoxiaresponsive element mediates a novel pathway of activation of the inducible nitric oxide synthase promoter. J Exp Med. 1995;182:1683-1693.
23. Palmer LA, Semenza GL, Stoler MH, Johns RA. Hypoxia induces type II NOS gene expression in pulmonary artery endothelial cells via HIF-1. Am J Physiol. 1998;274(2 pt 1):L212-L219.
24. Le Cras TD, Xue C, Rengasamy A, Johns RA. Chronic hypoxia upregulates endothelial and inducible NO synthase gene and protein expression in rat lung. Am J Physiol. 1996;270(1 pt 1):L164-L170.
25. Xue C, Rengasamy A, Le Cras TD, Koberna PA, Dailey GC, Johns RA. Distribution of NOS in normoxic vs hypoxic rat lung: upregulation of NOS by chronic hypoxia. Am J Physiol. 1994;267(6 pt 1):L667-L678.
26. Levy AP, Levy NS, Wegner S, Goldberg MA. Transcriptional regulation of the rat vascular endothelial growth factor gene by hypoxia. J Biol Chem. 1995;270:13333-13340.
27. Kourembanas S, Marsden PA, McQuillan LP, Faller DV. Hypoxia induces endothelin gene expression and secretion in cultured human endothelium. J Clin Invest. 1991;88:1054-1057.
28. Kourembanas S, Hannan RL, Faller DV. Oxygen tension regulates the expression of the platelet-derived growth factor-B chain gene in human endothelial cells. J Clin Invest. 1990;86:670-674.
29. Semenza GL, Nejfelt MK, Chi SM, Antonarakis SE. Hypoxia-inducible nuclear factors bind to an enhancer element located 3′ to the human erythropoietin gene. Proc Natl Acad Sci U S A. 1991;88:5680-5684.
30. Wang GL, Semenza GL. Characterization of hypoxia-inducible factor 1 and regulation of DNA binding activity by hypoxia. J Biol Chem. 1993; 268:21513-21518.
31. Wang GL, Semenza GL. Purification and characterization of hypoxia-inducible factor 1. J Biol Chem. 1995;270:1230-1237.
32. 2 tension. Proc Natl Acad Sci U S A. 1995;92:5510-5514.
33. Wang GL, Semenza GL. General involvement of hypoxia-inducible factor 1 in transcriptional response to hypoxia. Proc Natl Acad Sci U S A. 1993;90:4304-4308.
34. Forsythe JA, Jiang BH, Iyer NV, Agani F, Leung SW, Koos RD, Semenza GL. Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1. Mol Cell Biol. 1996;16:4604-4613.
35. Liu Y, Cox SR, Morita T, Kourembanas S. Hypoxia regulates vascular endothelial growth factor gene expression in endothelial cells: identification of a 5′ enhancer. Circ Res. 1995;77:638-643.
36. Semenza GL, Jiang BH, Leung SW, Passantino R, Concordet JP, Maire P, Giallongo A. Hypoxia response elements in the aldolase A, enolase 1, and lactate dehydrogenase A gene promoters contain essential binding sites for hypoxia-inducible factor 1. J Biol Chem. 1996;271:32529-32537.
37. Semenza GL, Roth PH, Fang HM, Wang GL. Transcriptional regulation of genes encoding glycolytic enzymes by hypoxia-inducible factor 1. J Biol Chem. 1994;269:23757-23763.
38. Firth JD, Ebert BL, Pugh CW, Ratcliffe PJ. Oxygen-regulated control elements in the phosphoglycerate kinase 1 and lactate dehydrogenase A genes: similarities with the erythropoietin 3′ enhancer. Proc Natl Acad Sci U S A. 1994;91:6496-6500.
39. Firth JD, Ebert BL, Ratcliffe PJ. Hypoxic regulation of lactate dehydrogenase A: interaction between hypoxia-inducible factor 1 and cAMP response elements. J Biol Chem. 1995;270:21021-21027.
40. Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970;227:680-685.
41. German CM, Moffat LF, Howard BH. Recombinant genomes which express chloramphenicol acetyltransferase in mammalian cells. Mol Cell Biol. 1982;2:1044-1051.
42. Stoler MH. In situ hybridization. Clin Lab Med. 1990;10:215-236.
43. Stoler MH Tissue in situ hybridization. In: Henry JB, ed. Clinical Diagnosis and Management by Laboratory Methods. 19th ed. Philadelphia, Pa: WB Saunders; 1996:1400-1412.
44. Muhl H, Pfeilschifter J. Amplification of nitric oxide synthase expression by nitric oxide in interleukin 1 beta-stimulated rat mesangial cells. J Clin Invest. 1995;95:1941-1946.
45. Marczin N, Papapetropoulos A, Catravas JD. Tyrosine kinase inhibitors suppress endotoxin- and IL-1 beta-induced NO synthesis in aortic smooth muscle cells. Am J Physiol. 1993;265(3 pt 2):H1014-H1018.
46. Wiener CM Booth G, Semenza GL. In vivo expression of mRNAs encoding hypoxia-inducible factor 1. Biochem Biophys Res Commun. 1996;225:485-488.
47. Huang LE, Arany Z, Livingston DM, Bunn HF. Activation of hypoxia-inducible transcription factor depends primarily upon redox-sensitive stabilization of its alpha subunit. J Biol Chem. 1996;271: 32253-32259.
48. Semenza GL, Dureza RC, Traystman MD, Gearhart JD, Antonarakis SE. Human erythropoietin gene expression in transgenic mice: multiple transcription initiation sites and cis-acting regulatory elements. Mol Cell Biol. 1990;10:930-938.
49. Niwa M, Kawai Y, Nakamura N, Futaki S. The structure of the promoter region for rat inducible nitric oxide synthase gene. Life Sci. 1997;61: 45-49.
50. Friedlander RM, Gagliardini V, Rotello RJ, Yuan J. Functional role of interleukin 1 beta (IL-1 beta) in IL-1 beta-converting enzyme-mediated apoptosis. J Exp Med. 1996;184:717-724.