Prevention of hypoxia-induced pulmonary hypertension by enhancement of endogenous heme oxygenase-1 in the rat

Circulation Research

Volumn 86, Issue 12, 2000, Pages 1224-1229

  Christou, Helen ^a   Morita, Toshisuke ^a   Hsieh, Chung Ming ^b   Koike, Hideo ^a   Arkonac, Burak ^b   Perrella, Mark A ^b   Kourembanas, Stella ^a,c  

^a HARVARD MEDICAL SCHOOL   (United States)

^b HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^c BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

Gene expression; Hypoxia; Vascular remodeling

Indexed keywords

HEME OXYGENASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CATALYSIS; CONTROLLED STUDY; ENZYME ANALYSIS; ENZYME INDUCTION; HYPOXIA; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PULMONARY HYPERTENSION; RAT; VASODILATATION;

EID: 0034705371     PISSN: 00097330     EISSN: None     Source Type: Journal    
DOI: 10.1161/01.RES.86.12.1224     Document Type: Article

References (35)

1. Marks GS, Brien JF, Nakatsu K, McLaughlin BE. Does carbon monoxide have a physiological function? Trends Pharmacol Sci. 1991;12:185-188.
2. Shibahara S, Muller R, Taguchi H, Yoshida T. Cloning and expression of cDNA for rat heme oxygenase. Proc Natl Acad Sci U S A. 1985;82: 7865-7869.
3. Trakshel GM, Kutty RK, Maines MD. Purification and characterization of the major constitutive form of testicular heme oxygenase. J Biol Chem. 1986;261:11131-11137.
4. McCoubrey WK, Huang TJ, Maines MD. Isolation and characterization of a cDNA from the rat brain that encodes hemoprotein heme oxygenase-3. Eur J Biochem. 1997;247:725-732.
5. Verma A, Hirsch DJ, Glatt CE, Ronnett GV, Snyder SH. Carbon monoxide: a putative neural messenger. Science. 1993;259:381-384.
6. Monta T, Perrella MA, Lee M-E, Kourembanas S. Smooth muscle cell-derived carbon monoxide is a regulator of vascular cGMP. Proc Natl Acad Sci U S A. 1995;92:1475-1479.
7. Ramos KS, Lin H, McGrath JJ. Modulation of cyclic monophosphate levels in cultured aortic smooth muscle cells by carbon monoxide. Biochem Pharmacol. 1989;38:1368-1370.
8. Vedernikov YP, Graser T, Vanin AF. Similar endothelium-independent arterial relaxation by carbon monoxide and nitric oxide. Biomed Biochim Acta. 1989;48:601-603.
9. Monta T, Kourembanas S. Endothelial cell expression of vasoconstrictors and growth factors is regulated by smooth muscle cell-derived carbon monoxide. J Clin Invest. 1995;96:2676-2682.
10. Morita T, Mitsialis SA, Koike H, Liu Y, Kourembanas S. Carbon monoxide controls the proliferation of hypoxic vascular smooth muscle cells. J Biol Chem. 1997;272:32804-32809.
11. Shibahara S. Regulation of heme oxygenase gene expression. Semin Hematol. 1988;25:370-376.
12. Maines MD. Heme oxygenase: function, multiplicity, regulatory mechanisms, and clinical applications. FASEB J. 1988;2:2557-2568.
13. Rodgers PA, Stevenson DK. Developmental biology of heme oxygenase. Clin Perinatol. 1990;17:275-291.
14. Stocker R, Yamamoto Y, McDonagh AF, Glazer AN, Ames BN. Bilirubin is an antioxidant of possible physiological importance. Science. 1987;235:1043-1046.
15. Elton TS, Oparil S, Taylor GR, Hicks PH, Yang RH, Jin H, Chen YF. Normobaric hypoxia stimulates endothelin-1 gene expression in the rat. Am J Physiol. 1992;263:R1260-R1264.
16. Morrell NW, Danilov SM, Satyan KB, Morris KG, Stenmark KR. Right ventricular angiotensin converting enzyme activity and expression is increased during hypoxic pulmonary hypertension. Cardiovasc Res. 1997;34:393-403.
17. Le Cras TD, Tyler RC, Horan MP, Morris KG, Tuder RM, McMurtry IF, Johns RA, Abman SH. Effects of chronic hypoxia and altered hemodynamics on endothelial nitric oxide synthase expression in the adult rat lung. J Clin Invest. 1998;101:795-801.
18. 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:L667-L678.
19. Christou H, Yoshida A, Arthur V, Morita T, Kourembanas S. Increased vascular endothelial growth factor production in the lungs of rats with hypoxia-induced pulmonary hypertension. Am J Respir Cell Mol Biol. 1998;18:768-776.
20. Chomczynski P, Sacchi N. Single-step method of RNA isolation by guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem. 1987;162:156-159.
21. 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.
22. Shi C, Lee W-S, Russell ME, Zhang D, Fletcher DL, Newell JB, Haber E. Hypercholesterolemia exacerbates transplant arteriosclerosis via increased neointimal smooth muscle cell accumulation: studies in apolipoprotein E knockout mice. Circulation. 1997;96:2722-2728.
23. Christou H, Adatia I, Van Marter LJ, Kane JW, Thompson JE, Stark AR, Wessel DL, Kourembanas S. Effect of inhaled nitric oxide on endothelin-1 and cyclic guanosine 5′-monophosphate plasma concentrations in newborn infants with persistent pulmonary hypertension. J Pediatr. 1997;130:603-611.
24. Kappas A, Maines MD. Tin: a potent inducer of heme oxygenase in kidney. Science. 1976;192:60-62.
25. Sunderman FWJ, Reid MC, Bibeau LM, Linden JV. Nickel induction of microsomal heme oxygenase activity in rodents. Toxicol Appl Pharmacol. 1983;68:87-95.
26. Sunderman FWJ. Metal induction of heme oxygenase. Ann N Y Acad Sci. 1987;514:65-80.
27. Jones RC, Reid LM. Structural basis of pulmonary hypertension. Curr Pulmonol. 1987;8:175-210.
28. Kourembanas S, Morita T, Liu Y, Christou H. Mechanisms by which oxygen regulates gene expression and cell-cell interaction in the vasculature. Kidney Int. 1997;51:438-443.
29. 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.
30. McQuillan LP, Leung GK, Marsden PA, Kostyk SK, Kourembanas S. Hypoxia inhibits expression of eNOS via transcriptional and posttranscriptional mechanisms. Am J Physiol. 1994;267:H1921-H1927.
31. Sacerdoti D, Escalante B, Abraham NG, McGiff JC, Levere RD, Schwartzman ML. Treatment with tin prevents the development of hypertension in spontaneously hypertensive rats. Science. 1989;243:388-390.
32. Liu Y, Christou H, Morita T, Laughner E. Semenza GL, Kourembanas S. Carbon monoxide and nitric oxide suppress the hypoxic induction of vascular endothelial growth factor gene via the 5′ enhancer. J Biol Chem. 1998;273:15257-15262.
33. Vosatka RJ, Kashyap S, Trifiletti RR. Arginine deficiency accompanies persistent pulmonary hypertension of the newborn. Biol Neonate. 1994; 66:65-70.
34. Dollberg S, Warner BW, Myatt L. Urinary nitrite and nitrate concentrations in patients with idiopathic persistent pulmonary hypertension of the newborn and effect of extracorporeal membrane oxygenation. Pediatr Res. 1995;37:31-34.
35. Sogawa K, Numayama-Tsuruta K, Ema M, Abe M, Abe H, Fujii-Kuriyama Y. Inhibition of hypoxia-inducible factor 1 activity by nitric oxide donors in hypoxia. Proc Natl Acad Sci U S A. 1998;95:7368-7373.