Abstract
Nitric oxide (NO) synthase induction in vascular smooth muscle cells may play a role in local vascular injury associated with atherosclerosis or postangioplasty restenosis by inhibiting smooth muscle cell proliferation and contraction, as well as by preventing leukocyte and platelet adhesion. The expression of inducible NO synthase is increased in balloon‐injured arteries of experimental animals or in human atherosclerotic lesions. Replacement therapy with NO donors or NO synthase gene transfer may improve the clinical course of atherosclerosis or restenosis.
Keywords: nitric oxide, vascular smooth muscle, atherosclerosis, restenosis, gene transfer
Full Text
The Full Text of this article is available as a PDF (482.2 KB).
References
- 1. Moncada S, Palmer RMJ, Higgs EA: Nitric oxide: Physiology, pathophysiology and pharmacology. Phannacol Rev 1991; 43: 109–140 [PubMed] [Google Scholar]
- 2. Nathan C, Xie Q: Regulation of biosynthesis of nitric oxide. J Biol Chem 1994; 269: 13725–13728 [PubMed] [Google Scholar]
- 3. Shindo T, Ikeda U, Ohkawa F, Takahashi M, Funayama H, Nishinaga M, Kawahara Y, Yokoyama M, Shimada K: Nitric oxide synthesis in rat cardiac myocytes and fibroblasts. Life Sciences 1994; 55: 1101–1108 [DOI] [PubMed] [Google Scholar]
- 4. Koide M, Kawahara Y, Tsuda T, Yokoyama M: Cylokine‐induced expression of an inducible type of nitric oxide synthase gene in cultured vascular smooth muscle cells. FEBS Lett 1993; 318: 213–217 [DOI] [PubMed] [Google Scholar]
- 5. Dinerman JL, Lowenstein CJ, Snyder SH: Molecular mechanisms of nitric oxide regulation. Circ Res 1993; 73: 217–222 [DOI] [PubMed] [Google Scholar]
- 6. Tanner FC, Boulanger CM, Lüscher TF: Endotheliun‐derived nitricoxide, endothelin, and platelet vessel wall interaction: Alterations in hypercholesterolemia and atherosclerosis. Semin Thromb Hemost 1993; 19: 167–175 [DOI] [PubMed] [Google Scholar]
- 7. Wennnialm A: Endothelial nitric oxide and cardiovascular disease. J Intern Med 1994; 235: 317–327 [DOI] [PubMed] [Google Scholar]
- 8. Warren JB, Pons F. Brady AJB: Nitric oxide biology: Implications for cardiovascular therapeutics. Canliovasc Res 1994; 28: 25–3() [DOI] [PubMed] [Google Scholar]
- 9. Mclntyre M, Dominiczak AF: Nitric oxide and cardiovascular disease. Postgrad Med J 1997; 73: 63–643 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 10. Ikeda U, Kanbe T, Nakayama I, Kawahara Y, Yokoyama M, Shimada K: Aldosterone inhibits nitric oxide synthesis in rat vascular smooth muscle cells induced by interleukin‐1β. Eur J Pharmacol 1995; 290: 69–73 [DOI] [PubMed] [Google Scholar]
- 11. French JF, Lambert LE, Dage RC: Nitric oxide synthase inhibitors interleukin‐1 β‐induced depression of vascular smooth muscle. J Pharmacol Exp Thier 1991; 259: 260–264 [PubMed] [Google Scholar]
- 12. Takizawa S, Ozaki H, Karaki H: Interleukin‐1β‐induced, nitric oxide‐dependent and ‐independent inhibition of vascular smooth muscle contraction. Eur J Pharmacol 1997; 330: 143–150 [DOI] [PubMed] [Google Scholar]
- 13. Moritoki H, Takeuchi S, Hisayama T, Kondoh W: Nitric oxide synthase responsible for L‐arginine‐induced relaxation of rat aortic rings in vitro may be an inducible type. Br J Pharmacol 1992; 107: 361–366 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 14. Karaki H, Sato K, Ozaki H, Murakami K: Effects of sodium nitroprusside on cytosolic calcium level in vascular smooth muscle. Eur J Pharmacol 1988; 156: 259–266 [DOI] [PubMed] [Google Scholar]
- 15. Provost P, Tremblay J, Merhi Y: The antiadhesive and antithrombotic effects of the nitric oxide donor SIN‐1 are combined with a decreased vasoconstriction in a porcine model of balloon angioplasty. Aneriosler Thromb Vasc Biol 1997; 17: 1806–1812 [DOI] [PubMed] [Google Scholar]
- 16. Yan Z, Yokota T, Zhang W, Hansson GK: Expression of inducible nitric oxide synthase inhibits platelet adhesion and restores blood flow in the injured artery. Circ Res 1996; 79: 38–44 [DOI] [PubMed] [Google Scholar]
- 17. Garg UC, Hassid A: Nitric oxide‐generating vasodilators and 8‐bromo‐cyclic GMP inhibit mitogenesis and proliferation of cultured rat vascular smooth muscle cells. J Clin Invest 1989; 83: 1774–1777 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 18. Kariya K, Kawahara Y, Araki S, Fukuzaki H, Takai Y: Antiproliferative action of cyclic GMP‐elevating vasodilators in cultured rabbit aortic smooth muscle cells. Atherosclerosis 1989; 80: 143–147 [DOI] [PubMed] [Google Scholar]
- 19. Garg UC, Hassid A: Nitric oxide‐generating vasodilators inhibit mitogenesis and proliferation of BALB/c 3T3 fibroblasts by a cGMP‐independent mechanism. Biochem Biophys Res Commun 1990; l71: 474–479 [DOI] [PubMed] [Google Scholar]
- 20. Kullo IJ, Schwartz RS, Pompili VJ, Tsutsui M, Milstien S, Fitzpatrick LA, Katusic ZS, O'Brien T: Expression and function of recombinant endothelial NO synthase in coronary artery smooth muscle cells. Arterioscler Thromb Vasc Biol 1997; 17: 2405–2412 [DOI] [PubMed] [Google Scholar]
- 21. Merhi Y, Lacoste LL, Lam JYT: Neutrophil implications in platelet deposition and vasoconstriction after deep arterial injury by angioplasty in pigs. Circulation 1994; 90: 997–1002 [DOI] [PubMed] [Google Scholar]
- 22. Provost P, Lam JYT, Lacoste L, Merhi Y, Waters D: Endotheliumderived nitric oxide attenuates neutrophil adhesion to endothelium under arterial flow conditions. Arteriosder Thromb 1994; 14: 331–335 [DOI] [PubMed] [Google Scholar]
- 23. Bath PMW, Hasall DG, Glaswin AM, Palmer RMJ, Martin JF: Nitric oxide and prostacyclin: Divergence of inhibitory effects on monocyte chemotaxis and adhesion to endothelium in vitro. Arteriosder Thromb 1991; 11: 254–260 [DOI] [PubMed] [Google Scholar]
- 24. Siegfried MR, Carey C, Ma XI, Lefer AM: Beneficial effects of SPM‐5185, a cystein‐containing NO donor, in myocardial ischemia‐reperfusion. Am J Physiol 1992; 263: H771–H777 [DOI] [PubMed] [Google Scholar]
- 25. Takahashi M, Ikeda U, Masuyama J, Funayama H, Kano S, Shimada K: Nitric oxide attenuates adhesion molecule expression in human endothelial cells. Cytokine 1996; 8: 817–821 [DOI] [PubMed] [Google Scholar]
- 26. De Caterina R, Libby P, Peng HB, Thannickal VJ, Rajavashisth TB, Gimbrone MAA, Shin WS, Liao JK: Nitric oxide decreases cytokine‐induced endothelial activation. J Clin Invest 1995; 96: 60–68 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 27. Kubes P, Suzuki M, Granger DN: Nitric oxide: An endogenous modulator of leukocyte adhesion. Proc Natl Acad Sci USA 1992; 88: 4651–1655 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 28. Nguyen BL, Sitoh M, Ware JA: Interaciton of nitric oxide and cGMP with signal transduction in activated platelets. Am J Physiol 1991; 261: H1043–H1052 [DOI] [PubMed] [Google Scholar]
- 29. Radomski MW, Rees DD, Dutra A, Moncada S: S‐Nitroso‐glutathione inhibits platelet activation in vitro and in vivo. Br J Pharmacol 1992; 107: 745–749 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 30. Langford EJ, Brown AS, Wainwright RJ, de Belder BA, Thomas MR, Smith RE, Radomski MW, Martin JF, Moncada S: Inhibition of platelet activity by S‐nitorosoglutathione during coronary angioplasty. Lancet 1994; 344: 1458–0‐I460 [DOI] [PubMed] [Google Scholar]
- 31. Horstrup K, Jablonka B, Honig LP, Just M, Kochsiek K, Walter U: Phosphorylation of focal adhesion vasodilator‐stimulated phosphoprotein at Ser 157 in intact human platelets correlates with fibrinogen receptor inhibition. EurJ Biochem 1994; 225: 21–27 [DOI] [PubMed] [Google Scholar]
- 32. Oslen SB, Tang DB, Jackson MR, Gomez ER, Ayala B, Alving BM: Enhancement of platelet deposition by cross‐linked hemoglobin in a rat carotid endarterectomy model. Circulation 1996; 93: 327–332 [DOI] [PubMed] [Google Scholar]
- 33. Ikeda U, Kurosaki K, Ohya K, Shimada K: Adenosine stimulates nitric oxide synthesis in vascular smooth muscle cells. Cardiovasc Res 1997; 35: 168–174 [DOI] [PubMed] [Google Scholar]
- 34. Ikeda U, Kanbe T, Shimada K: Adrenomedullin increases inducible nitric oxide synthase in rat vascular smooth muscle cells stimulated with interleukin‐1. Hypertension 1996; 27: 1240–1244 [DOI] [PubMed] [Google Scholar]
- 35. Nakayama I, Kawahara Y, Tsuda T, Okuda M, Yokoyama M: Angiotensin II inhibits cytokine‐stimulated inducible nitric oxide synthase expression in vascular smooth muscle cells. J Biol Chem 1994; 269: 11628–11633. [PubMed] [Google Scholar]
- 36. Scott‐Burden T, Schini VB, Elizondo E, Junquero DC, Vanhoutte PM: Platelet‐derived growth factor suppresses and fibroblast growth factor enhances cytoki ne‐induced production of nitric oxide by cultured smooth muscle cells. Circ Res 1992; 71: 1088–1100 [DOI] [PubMed] [Google Scholar]
- 37. Ikeda U, Yamamoto K, Maeda Y, Shimpo M, Kanbe T, Shimada K: Endothelin‐1 inhibits nitric oxide synthesis in vascular smooth muscle cells. Hypertension 1997; 24: 65–69 [DOI] [PubMed] [Google Scholar]
- 38. Hansson GK, Geng Y, Holm J, Hardhammar P, Wennmalm A, Jennische E: Arterial smooth muscle cells express nitric oxide syn thase in response to endothelial injury. J Exp Med 1994; 180: 733–738 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 39. Buttery LD, Springall DR, Chester AH, Evans TJ, Standfield EN, 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 [PubMed] [Google Scholar]
- 40. Joly GA, Schini VB, Vanhoutte PM: Balloon injury and interleukin‐ 1 β induce nitric oxide synthase activity in rat carotid arteries. Circ Res 1992; 71: 331–338 [DOI] [PubMed] [Google Scholar]
- 41. Bosnians JM, Bull H, Vrints CJ, Kockx MM, Herman AG: Balloon angioplasty and induction of non‐endothelial nitric oxide synthase in rabbit carotid arteries. Eur J Pharmacol 1996; 310: 163–174 [DOI] [PubMed] [Google Scholar]
- 42. Wilcox JN, Subramanian RR, Sundell CL, Tracey WR, Pollock JS, Harrison DG, Marsden PA: Expression of multiple isoforms of nitric oxide synthase in normal and atherosclerotic vessels. Arterioscler Thromb Vasc Biol 1997; 17: 2479–2488 [DOI] [PubMed] [Google Scholar]
- 43. Ikeda U, Maeda Y, Funayama H, Hojo Y, Ikeda M, Minota S, Kano S, Shimada K: Monocyte‐vascular smooth muscle cell interaction enhances nitric oxide production. Cardiovas Res 1998; 37: 820–825 [DOI] [PubMed] [Google Scholar]
- 44. Nunokawa Y, Ishida N, Tanaka S: Promoter analysis of human inducible nitric oxide synthase gene associated with cardiovascular homeostasis. Biochem Biophys Res Commun 1994; 200: 802–807 [DOI] [PubMed] [Google Scholar]
- 45. 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 [DOI] [PubMed] [Google Scholar]
- 46. 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 [DOI] [PubMed] [Google Scholar]
- 47. Tarry WC, Makhoul RG: L‐arginine improves endothelium‐dependent vasorelaxation and reduces intimal hyperplasia after balloon angioplasty. Arterioscler Thromb 1994; 14: 938–943 [DOI] [PubMed] [Google Scholar]
- 48. Ooboshi H, Chu Y, Rios CD, Faraci FM, Davidson BL, Heistad DD: Altered vascular function after adenovirus‐mediated overexpression of endothelial nitric oxide synthase. Am J Physiol 1997; 273: H265–H270 [DOI] [PubMed] [Google Scholar]
- 49. McNamara DB, Bedi B, Aurora H, Tena L, Ignarro LJ, Kadowitz PJ, Akers DL: L‐arginine inhibits balloon catheter‐induced intimal hyperplasia. Biochem Biophys Res Commun 1993; 193: 291–296 [DOI] [PubMed] [Google Scholar]
- 50. 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 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 51. Tzeng E, Shears LL II, Robbins PD, Pitt BR, Geller DA, Watkins SC, Simmons RL, Billiar TR: Vascular gene transfer of the human inducible nitric oxide synthase: Characterization of activity and effects on myointimal hyperplasia. Mol Med 1996; 2: 211–225 [PMC free article] [PubMed] [Google Scholar]
- 52. von der Leyen HE, Gibbons GH, Morishita R, Lewis NP, Zhang L, Nakajima M, Kaneda Y, Cooke JP, Dzau VJ: Gene therapy inhibiting neointimal vascular lesion: in vivo transfer of endothelial cell nitric oxide synthase gene. Proc Natl Acad Sci USA 1995; 92: 1137–1141 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 53. Maeda Y, Ikeda U, Ishibashi S, Shimpo M, Shimada K, Ozawa K: Transfer of endothelial constitutive nitric oxide synthase gene into vascular structure using adeno‐associated virus vectors (abstr). Jpn Circ J 1997; 61: 590–591 [Google Scholar]
- 54. Cable DG, O'Brien T, Kullo I, Schwartz RS, Schaff HV, Pompili VJ: Expression and function of a recombinant endothelial nitric oxide synthase gene in porcine coronary arteries. Cardiovasc Res 1997; 35: 553–559 [DOI] [PubMed] [Google Scholar]
- 55. Kullo IJ, Mozes G, Schwartz RS, Gloviczki P, Crotty TB, Barber DA, Katusic ZS, O'Brien T: Adventitial gene transfer of recombinant endothelial nitric oxide synthase to rabbit carotid arteries alters vascular reactivity. Circulation 1997; 96: 2254–2261 [DOI] [PubMed] [Google Scholar]
- 56. Cable DG, O'Brien T, Schaff HV, Pompili VJ: Recombinant endothelial nitric oxide synthase‐transduced human saphenous veins: Gene therapy to augment nitric oxide production in bypass conduits. Circulation 1997; 96: II‐173–II‐178 [PubMed] [Google Scholar]
