Platelet-derived growth factor stimulates heme oxygenase-1 gene expression and carbon monoxide production in vascular smooth muscle cells

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 19, Issue 11, 1999, Pages 2666-2672

  Durante, William ^a,b   Peyton, Kelly J ^a   Schafer, Andrew I ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b MICHAEL E DEBAKEY VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Carbon monoxide; Heme oxygenase; Platelet derived growth factor

Indexed keywords

CARBON MONOXIDE; CYCLOHEXIMIDE; DACTINOMYCIN; HEME OXYGENASE; PLATELET DERIVED GROWTH FACTOR RECEPTOR; REACTIVE OXYGEN METABOLITE;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; GENE EXPRESSION REGULATION; GENE INDUCTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; RAT; VASCULAR SMOOTH MUSCLE;

EID: 0032725611     PISSN: 10795642     EISSN: None     Source Type: Journal    
DOI: 10.1161/01.ATV.19.11.2666     Document Type: Article

References (57)

1. Tenhunen R, Marver HS, Schmidt R. The enzymatic conversion of heme to bilirubin by microsomal heme oxygenase. Proc Natl Acad Sci U S A. 1968;244:6388-6394.
2. Maines MD, Trakshel GM, Kutty RK. Characterization of two constitutive forms of rat liver microsomal heme oxygenase: only one molecular species of the enzyme is inducible. J Biol Chem. 1986;261:411-419.
3. Trakshel GM, Maines MD. Multiplicity of heme oxygenase isozymes: HO-1 and HO-2 are different molecular species in rat and rabbit. J Biol Chem. 1989;264:1323-1328.
4. Maines MD. Heme oxygenase: function, multiplicity, regulatory mechanisms, and clinical applications. FASEB J. 1988;2:2557-2568.
5. Keyse SM, Applegate LA, Tromvoukis Y, Terrell RM. Oxidative stress leads to the transcriptional activation of the human heme oxygenase gene in cultured skin fibroblasts. Mol Cell Biol. 1990;10:4967-4969.
6. Vile GF, Basu-Modak S, Waltner C, Tyrell RM. Heme oxygenase 1 mediates an adaptive response to oxidative stress in human skin fibroblasts. Proc Natl Acad Sci U S A. 1994;91:2607-2610.
7. 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.
8. Durante W, Kroll MH, Christodoulides N, Peyton KJ, Schafer AI. Nitric oxide induces heme oxygenase expression and carbon monoxide production in vascular smooth muscle cells. Circ Res. 1997;80:557-564.
9. McCoubrey WK Jr, 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.
10. Maines MD, Mayer RD, Ewing JF, McCoubrey WK Jr. Induction of kidney heme oxygenase-1 (HSP32) mRNA and protein by ischemia/reperfusion: possible role of heme as both a promoter of tissue damage and regulator of HSP32. J Pharmacol Exp Ther. 1993;264:457-462.
11. Maulik N, Engelman DT, Watanabe M, Engelman RM, Rousou JA, Flack JE III, Deaton DW, Gorbunov NV, Elsayed NM, Kagan VE, Das DK. Nitric oxide/carbon monoxide: a molecular switch for myocardial preservation during ischemia. Circulation. 1996;94(suppl II):II-393-II-406.
12. Abraham NG, Lavrovsky Y, Schwartzman ML, Stoltz RA, Levere RD, Gerritsen ME, Shibahara S, Kappas A. Transfection of human heme oxygenase gene into rabbit coronary microvessels endothelial cells: protective effect against heme and hemoglobin toxicity. Proc Natl Acad Sci U S A. 1995;92:6798-6802.
13. Stocker R, Yamamoto Y, McDonagh AF, Gazer AN, Ames BN. Bilirubin is an antioxidant of possible physiologic importance. Science. 1987;235:1043-1046.
14. Llesuy SF, Tomaro ML. Heme oxygenase and oxidative stress: evidence of involvement of bilirubin as physiological protector against oxidative damage. Biochim Biophys Acta. 1994;1223:9-14.
15. Vile GF, Tyrell RM. Oxidative stress resulting from ultraviolet A irradiation of human skin fibroblasts leads to a heme oxygenase-dependent increase of ferritin. J Biol Chem. 1993;268:14678-14681.
16. Durante W, Schafer AI. Carbon monoxide and vascular cell function. Int J Mol Med. 1998;2:255-262.
17. Graser T, Vedernikov YP, Li DS. Study on the mechanism of carbon monoxide induced endothelium-independent relaxation in the porcine coronary artery and vein. Biomed Biochim Acta. 1990;49:293-296.
18. Vedernikov GP, Graser T, Vanin AF. Similar endothelium-independent arterial relaxation by carbon monoxide and nitric oxide. Biomed Biochim Acta.
19. Furchgott RF, Jothianandan D. Endothelium-dependent and independent vasodilation involving cyclic GMP: relaxation induced by nitric oxide, carbon monoxide, and light. Blood Vessels. 1991;28:52-61.
20. Wang R, Wang ZZ, Wu L. Carbon monoxide-induced vasorelaxation and the underlying mechanisms. Br J Pharmacol. 1997;121:927-934.
21. Levere RD, Martasek P, Escalante B, Schwartzman ML, Abraham NG. Effect of heme arginate administration on blood pressure in spontaneously hypertensive rats. J Clin Invest. 1990;86:213-219.
22. Johnson RA, Lavesa M, Askari B, Abraham NG, Nasjletti A. A heme oxygenase product, presumably carbon monoxide, mediates a vasodepressor function in rats. Hypertension. 1995;25:166-169.
23. Morita 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.
24. Morita T, Mitsialis SA, Hoike H, Liu Y, Kourembanas S. Carbon monoxide controls the proliferation of hypoxic smooth muscle cells. J Biol Chem. 1997;272:32804-32809.
25. Wagner CT, Durante W, Christodoulides N, Hellums JD, Schafer AI. Hemodynamic forces induce the expression of heme oxygenase in cultured vascular smooth muscle cells. J Clin Invest. 1997;100:589-596.
26. Brune B, Ullrich V. Inhibition of platelet aggregation by carbon monoxide is mediated by the activation of guanylate cyclase. Mol Pharmacol. 1987;32:497-504.
27. Morita T, Perella MA, Lee ME, 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.
28. Christodoulides N, Durante W, Kroll MH, Schafer AI. Vascular smooth muscle cell heme oxygenases generate guanylyl cyclase-stimulatory carbon monoxide. Circulation. 1995;91:2306-2309.
29. Yet S-F, Pellacani A, Patterson C, Tan L, Folta SC, Foster L, Lee W-S, Hsieh C-M, Perella MA. Induction of heme oxygenase-1 expression in vascular smooth muscle cells: a link to endotoxin shock. J Biol Chem. 1997;272:4295-4301.
30. Ross R, Raines EW, Bowen-Pope DF. The biology of platelet-derived growth factor. Cell. 1988;46:155-169.
31. Majesky MW, Reidy MA, Bowen-Pope DF, Hart CE, Wilcox JN, Schwartz SM. PDGF ligand and receptor gene expression during repair of arterial injury. J Cell Biol. 1990;111:2149-2158.
32. Schwartz SM, Heimark RL, Majesky MW. Developmental mechanisms underlying pathology of arteries. Physiol Rev. 1990;70:1177-1209.
33. Berk BC, Alexander RW, Brock TA, Gimbrone MA Jr, Webb RC. Vasoconstriction: a new activity for platelet-derived growth factor. Science. 1986;232:87-90.
34. BB in vascular smooth muscle cells. Eur J Pharmacol. 1992;216:379-383.
35. Durante W, Schini VB, Kroll MH, Catovsky S, Scott-Burden T, White G, Vanhoutte PM, Schafer AI. Platelets inhibit the induction of nitric oxide synthesis by interleukin-1β in vascular smooth muscle cells. Blood. 1994;83:1831-1838.
36. Durante W, Kroll MH, Orloff GJ, Cunningham JM, Scott-Burden T, Vanhoutte PM, Schafer AI. Hemostatic proteins regulate interleukin-1β stimulated inducible nitric oxide synthase expression in cultured vascular smooth muscle cells. Biochem Pharmacol. 1996;51:847-853.
37. Durante W, Schini VB, Catovsky S, Kroll MH, Vanhoutte PM, Schafer AI. Plasmin potentiates the induction of nitric oxide synthase by interleukin-1β in vascular smooth muscle. Am J Physiol. 1993;264: H617-H624.
38. Chirgwin JM, Pryzbla AE, MacDonald RJ, Rutter WJ. Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease. Biochemistry. 1979;18:5294-5299.
39. Smith PK, Krohn RI, Hermanson GI, Mallia AK, Gartner FH, Provenzano MD, Fujimoto EK, Goeke NM, Olson BJ, Klenk DC. Measurement of protein using bicinchoninic acid. Anal Biochem. 1885;150:76-85.
40. Zulueta JJ, Sawhney R, Yu FS, Cote CC, Hassoun PM. Intracellular generation of reactive oxygen species in endothelial cells exposed to anoxia-reoxygenation. Am J Physiol. 1997;272:L897-L902.
41. 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.
42. Kerr LD, Holt JT, Matrisian LM. Growth factors regulate transin gene expression by c-fos dependent and c-fos independent pathways. Science. 1988;242:1424-1427.
43. Franchimont N, Durante D, Rydziel S, Canalis E. Platelet-derived growth factor induces interleukin-6 transcription in osteoblasts through activator-1 complex and activating transcription factor-2. J Biol Chem. 1999;274:6783-6789.
44. Elbirt KK, Whitmarsh AJ, Davis RJ, Bonkovsky HL. Mechanism of sodium arsenite-mediated induction of heme oxygenase-1 in hepatoma cells: role of mitogen-activated protein kinases. J Biol Chem. 1998;273:8922-8931.
45. Camhi SL, Alam J, Wiegand GW, Choi AM. Transcriptional activation of the HO-1 gene by lipopolysaccharide is mediated by 5′ distal enhancers: role of reactive oxygen intermediates and AP-1. Am J Respir Cell Mol Biol. 1998;18:226-234.
46. 2 for platelet-derived growth factor signal transduction. Science. 1995;270:296-299.
47. Marumo T, Schini-Kerth VB, Fisslthaler B, Busse R. Platelet-derived growth factor-stimulated superoxide anion production modulates activation of transcription factor NF-κB and expression of monocyte chemoattractant protein 1 in human aortic smooth muscle cells. Circulation. 1997;96:2361-2367.
48. Keyse SM, Tyrrell RM. Heme 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. 1989;86:99-103.
49. Sen CK, Packer L. Antioxidant and redox regulation of gene transcription. FASEB J. 1996;10:709-720.
50. 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.
51. Neuzil J, Stocker R. Free and albumin-bound bilirubin are efficient co-antioxidants for α-tocopherol, inhibiting plasma and low density lipid peroxidation. J Biol Chem. 1994;269:16712-16719.
52. Schwertner HA, Jackson WG, Tolan G. Association of low serum concentration of bilirubin with increased risk of coronary artery disease. Clin Chem. 1994;40:18-23.
53. Hopkins PN, Wu LL, Hunt SC, James EC, Vincent GM, Williams RR. Higher serum bilirubin is associated with decreased risk for early familial coronary artery disease. Arterioscler Thromb Vasc Biol. 1996;16:250-255.
54. Groves HM, Kinlough-Rathbone RL, Mustard JF. Development of nonthrombogenicity of injured rabbit aortas despite inhibition of platelet adherence. Arteriosclerosis. 1986;6:189-195.
55. Wilentz JR, Sanborn TA, Haudenschild CC, Valeri CR, Ryan TJ. Platelet accumulation in experimental angioplasty: time course and relation to vascular injury. Circulation. 1987;75:636-642.
56. Motterlini R, Gonzalez A, Foresti R, Clark JE, Green CJ, Winslow RM. Heme oxygenase-1 derived carbon monoxide contributes to the suppression of acute hypertensive responses in vivo. Circ Res. 1998;83:568-577.
57. Pannen BHJ, Kohler N, Hole B, Bauer M, Clemons MG, Geiger KK. Protective role of endogenous carbon monoxide in hepatic microcirculatory dysfunction after hemorrhagic shock in rats. J Clin Invest. 1988;102:1220-1228.