Inducible nitric oxide synthase expression in smooth muscle cells and macrophages of human transplant coronary artery disease

Circulation

Volumn 97, Issue 23, 1998, Pages 2338-2345

  Ravalli, Stefano ^a   Albala, Arline ^a   Ming, Ming ^a   Szabolcs, Matthias ^a   Barbone, Alessandro ^a   Michler, Robert E ^a   Cannon, Paul J ^a,b  

^a New York Presbyterian Columbia University Medical Center   (United States)

^b Columbia University ^*  (United States)

Author keywords

Arteriosclerosis; Endothelium derived factors; Transplantation

Indexed keywords

NITRIC OXIDE SYNTHASE;

ADULT; ARTICLE; CHILD; CLINICAL ARTICLE; CORONARY ARTERY DISEASE; ENZYME INDUCTION; ENZYME LOCALIZATION; FEMALE; HUMAN; IMMUNOHISTOCHEMISTRY; MACROPHAGE; MALE; PATHOPHYSIOLOGY; PRIORITY JOURNAL; VASCULAR SMOOTH MUSCLE;

EID: 0032537571     PISSN: 00097322     EISSN: None     Source Type: Journal    
DOI: 10.1161/01.CIR.97.23.2338     Document Type: Article

References (50)

1. Hosenpud JD, Novick RJ, Bennett LE, Keck BM, Fiol B, Daily OP. The registry of the International Society for Heart and Lung Transplantation: thirteenth official report - 1996. J Heart Lung Transplant. 1996;15:655-674.
2. Salomon RN, Hughes CW, Schoen FJ, Payne DD, Pober JS, Libby P. Human coronary transplantation-associated arteriosclerosis: evidence for a chronic immune reaction to activated graft endothelial cells. Am J Pathol. 1991;138:791-798.
3. Rose ML. Role of antibody and indirect antigen presentation in transplant-associated coronary artery vasculopathy. J Heart Lung Transplant. 1996;15:342-349.
4. Johnson MR. Transplant coronary disease: nonimmunologic risk factors. J Heart Lung Transplant. 1992;11:S124-S132.
5. Park JW, Merz M, Braun P, Vermeltfoort M. Lipid disorder and transplant coronary artery disease in long-term survivors of heart transplantation. J Heart Lung Transplant. 1996;15:572-579.
6. Sasagury S, Eishi Y, Tsukada T, Sunamori M, Suzuki A, Numano F, Hatakeyama S, Hosoda Y. Role of smooth muscle cells and macrophages in cardiac allograft arteriosclerosis in rabbits. J Heart Transplant. 1990:9:18-24.
7. Forstermann U, Schmidt HHW, Pollock JS, Sheng H, Mitchell JA, Warner TD, Nakane M, Murad F. Isoforms of nitric oxide synthase: characterization and purification from different cell types. Biochem Pharmacol. 1991;42:1848-1857.
8. Moncada S, Palmer RMJ, Higgs A. Nitric oxide: physiology, pathophysiology and pharmacology. Pharmacol Rev. 1991;43:109-142.
9. Nathan C. Nitric oxide as a secretory product of mammalian cells. FASEB J. 1992;6:3051-3064.
10. Waldman SA, Murad F. Biochemical mechanisms underlying vascular smooth muscle relaxation: the guanylate cyclase-cyclic GMP system. J Cardovasc Pharmacol. 1988;12:S115-S118.
11. Radomski MW, Palmer RMJ, Moncada S. The role of nitric oxide and cGMP in platelet adhesion to vascular endothelium. Biochem Biophys Res Commun. 1987;148:1482-1489.
12. Garg UC, Hassid A. Nitric oxide-generating vasodilators and 8-bromo-cyclic guanosine monophosphate inhibit mitogenesis and proliferation of cultured rat vascular smooth muscle cells. J Clin Invest. 1989;83:1774-1777.
13. Beckman JS, Beckman TW, Chen J, Marshall PA, Freeman BA. Apparent hydroxyl radical production by peroxynitrite: implications for endothelial injury from nitric oxide and superoxide. Proc Natl Acad Sci U S A. 1990;87:1620-1624.
14. Hogg N, Darley-Usman VM, Wilson MT, Moncada S. Production of hydroxyl radicals from the simultaneous generation of superoxide and nitric oxide. Biochem J. 1992;281:419-424.
15. Langrehr JM, Hoffman RA, Lancaster JR, Simmons RL. Nitric oxide: a new endogenous immunomodulator. Transplantation. 1993;55:1205-1212.
16. 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.
17. Worrall NK, Lazenby WD, Misko TP, Lin TS, Rodi CP, Manning PT, Tilton RG, Williamson JR, Ferguson TB. Modulation of in vivo alloreactivity by inhibition of inducible nitric oxide synthase. J Exp Med. 1995;181:63-70.
18. Lewis NP, Tsao PS, Rickenbacher PR, Xue C, Johns RA, Haywood GA, von der Leyen H, Trindade PT, Cooke JP, Hunt SA, Billingham ME, Valantine HA, Fowler MB. Induction of nitric oxide synthase in the human cardiac allograft is associated with contractile dysfunction of the left ventricle. Circulation. 1996;93:720-729.
19. Szabolcs M, Michler RE, Yang X, Aji W, Roy D, Athan E, Sciacca RR, Minanov OP, Cannon PJ. Apoptosis of cardiac myocytes during cardiac allograft rejection: relation to induction of nitric oxide synthase. Circulation. 1996;94:1665-1673.
20. Buttery LDK, Springall DR, Chester AH, Evans TJ, Standfield N, Parums DV, Yacoub MH, Polak JM. Inducible nitric oxide synthase is present within human atherosclerotic lesions and promotes the formation and activity of peroxynitrite. Lab Invest. 1996;75:77-85.
21. Russell ME, Wallace AF, Wyner LR, Newell JB, Karnovsky MJ. Upregulation and modulation of inducible nitric oxide synthase in rat cardiac allografts with chronic rejection and transplant arteriosclerosis. Circulation. 1995;92:457-464.
22. Akyurek LM, Fellstrom BC, Yan Z, Hansson GK, Funa K, Larsson E. Inducible and endothelial nitric oxide synthase expression during development of transplant arteriosclerosis in rat aortic allografts. Am J Pathol. 1996;149:1981-1990.
23. Lafond-Walker A, Chen C, Augustine S, Wu T, Hruban RH, Lowenstein CJ. Inducible nitric oxide synthase expression in coronary arteries of transplanted human hearts with accelerated graft arteriosclerosis. Am J Pathol. 1997;151:919-925.
24. Nicholson S, Bonecini M, Lapa J, Nathan C, Xie Q, Mumford R, Weidner JR, Calaycay J, Geng J, Boechat N, Linhares C, Rom W, Ho JL. Inducible nitric oxide synthase in pulmonary alveolar macrophages from patients with tuberculosis. J Exp Med. 1996;183:2293-2302.
25. 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.
26. de Beider A, Radomski M, Hancock V, Brown A, Moncada S, Martin J. Megakaryocytes from patients with coronary atherosclerosis express the inducible nitric oxide synthase. Arterioscler Thromb Vasc Biol. 1995;15:637-641.
27. Padgett EL, Pruett SB. Evaluation of nitric oxide production by human monocyte-derived macrophages. Biochem Biophys Res Commun. 1992;186:775-787.
28. Kolb JP, Paul-Eugene N, Damais C, Yamaoka K, Drapier JC, Dugas B. Interleukin-4 stimulates cGMP production by IFN-γ-activated human monocytes: involvement of the nitric oxide synthase pathway. J Biol Chem. 1994;269:9811-9816.
29. Spitsin SV, Koprowski H, Michaels FH. Characterization and functional analysis of the human inducible nitric oxide synthase gene promoter. Mol Med. 1996;2:226-235.
30. Russell ME, Wallace AF, Hancock WW, Sayegh MH, Adams DH, Sibinga NES, Wyner LR, Karnovsky MJ. Upregulation of cytokines associated with macrophage activation in the Lewis to F344 rat chronic cardiac rejection model. Transplantation. 1995;59:572-578.
31. Clausell N, Molossi S, Rabinovitch M. Increased interleukin-1β and fibronectin expression are early features of the development of the post-cardiac transplant coronary arteriopathy in piglets. Am J Pathol. 1993;142:1772-1786.
32. Larsen CP. Alexander DZ, Hollenbaugh D, Elwood ET, Ritchie SC, Aruffo A, Hendrix R, Pearson TC. CD40-gp39 interactions play a critical role during allograft rejection: suppression of allograft rejection by blockade of the CD40-gp39 pathway. Transplantation. 1996;61:4-9.
33. Yellin MJ, Szabolcs M, Han A, Michler RE, Cannon PJ, Chess L. CD40L+CD4+ T cells and CD40+ target cells are present in atherosclerosis and transplant coronary artery disease. Circulation. 1996;94(suppl I):I-1. Abstract.
34. Clausell N, Butany J, Molossi S, Lonn E, Gladstone P, Rabinovitch M, Daly PA. Abnormalities in intramyocardial arteries detected in cardiac transplant biopsy specimens and lack of correlation with abnormal intracoronary ultrasound or endothelial dysfunction in large epicardial coronary arteries. J Am Coll Cardiol. 1995;26:110-119.
35. de Graaf JC, Banga JD, Moncada S, Palmer RMJ, de Groot PG, Sixma JJ. Nitric oxide functions as an inhibitor of platelet adhesion under flow conditions. Circulation. 1992;85:2284-2290.
36. De Caterina R, Libby P, Peng HB, Thannickal VJ, Rajavashisth TB, Gimbrone MA, Shin WS, Liao JK. Nitric oxide decreases cytokine-induced endothelial activation. J Clin Invest. 1995;96:60-68.
37. Zeiher AM, Fisslthaler B, Schray-Utz B, Busse R. Nitric oxide modulates the expression of monocyte chemoattractant protein 1 in cultured human endothelial cells. Circ Res. 1995;76:980-986.
38. Naruse K, Shimizu K, Muramatsu M, Toki Y, Miyazaki Y, Okumura K, Hashimoto H, Ito T. Long-term inhibition of NO synthesis promotes atherosclerosis in the hypercholesterolemic rabbit thoracic aorta. Arterioscler Thromb. 1994;14:746-752.
39. Cayatte AJ, Palacino JJ, Horten K, Cohen RA. Chronic inhibition of nitric oxide production accelerates neointima formation and impairs endothelial function in hypercholesterolemic rabbits. Arterioscler Thromb. 1994;14:753-759.
40. Aji W, Ravalli S, Szabolcs M, Jiang X, Sciacca RR, Michler RE, Cannon PJ. L-Arginine prevents xanthoma development and inhibits atherosclerosis in LDL receptor knockout mice. Circulation. 1997;95:430-437.
41. Cooke JP, Singer AH, Tsao P, Zera P, Rowan RA, Billingham ME. Antiatherogenic effects of L-arginine in the hypercholesterolemic rabbit. J Clin Invest. 1992;90:1168-1172.
42. Lou H, Kodama T, Wang YN, Katz N, Ramwell P, Foegh ML. L-Arginine prevents heart transplant arteriosclerosis by modulating the vascular cell proliferative response to insulin-like growth factor-1 and interleukin-6. J Heart Lung Transplant. 1996;15:1248-1257.
43. Fukuo K, Hata S, Suhara T, Nakahashi T, Shinto Y, Tsujimoto Y, Morimoto S, Ogihara T. Nitric oxide induces upregulation of Fas and apoptosis in vascular smooth muscle. Hypertension. 1996;27:823-826.
44. Albina JE, Cui S, Mateo RB, Reichner JS. Nitric oxide-mediated apoptosis in murine peritoneal macrophages. J Immunol. 1993;150:5080-5085.
45. Koglin J, Glysing-Jensen T, Mudgett JS, Russell ME. Exacerbated transplant arteriosclerosis in iNOS-deficient mice: iNOS protects against immune-mediated intimal thickening. Circulation. 1997;96(suppl I):I-171. Abstract.
46. Beckman JS, Ischiropoulos H, Zhu L, van der Woerd M, Smith C, Chen J, Harrison J, Martin JC, Tsai M. Kinetics of superoxide dismutase and iron catalyzed nitration of phenolics by peroxynitrite. Arch Biochem Biophys. 1992;298:438-445.
47. Beckman JS, Ye YZ, Anderson PG, Chen J, Accavitti MA, Tarpey MM, White CR. Extensive nitration of protein tyrosines in human atherosclerosis detected by immunohistochemistry. Biol Chem Hoppe Seyler. 1994;375:81-88.
48. Radi R, Beckman JS, Bush KM, Freeman BA. Peroxynitrite-induced membrane lipid peroxidation: the cytotoxic potential of superoxide and nitric oxide. Arch Biochem Biophys. 1991;288:481-487.
49. Darley-Usmar VM, Hogg N, O'Leary VJ, Moncada S. The simultaneous generation of superoxide and nitric oxide can initiate lipid peroxidation in human low density lipoprotein. Free Radic Res Commun. 1992;17:9-20.
50. Marui N, Offerman MK, Swerlick R, Kunsch C, Rosen CA, Ahmad M, Alexander RW, Medford RM. Vascular cell adhesion molecule-1 (VCAM-1) gene transcription and expression are regulated through an antioxidant-sensitive mechanism in human vascular endothelial cells. J Clin Invest. 1993;92:1866-1874.