Angiotensin-converting enzyme inhibition delays pulmonary vascular neointimal formation

American Journal of Respiratory and Critical Care Medicine

Volumn 158, Issue 3, 1998, Pages 939-950

  Okada, Kazushige ^a   Bernstein, Matthew L ^a   Zhang, Wei ^a   Schuster, Daniel P ^a   Botney, Mitchell D ^a,b  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b BARNES JEWISH HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOTENSIN RECEPTOR ANTAGONIST; DIPEPTIDYL CARBOXYPEPTIDASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTERY INTIMA PROLIFERATION; ARTICLE; ENZYME INHIBITION; GENE EXPRESSION; HYPERTROPHY; IN SITU HYBRIDIZATION; LUNG ARTERY PRESSURE; LUNG BLOOD FLOW; MALE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PULMONARY HYPERTENSION; RAT;

EID: 0031753080     PISSN: 1073449X     EISSN: None     Source Type: Journal    
DOI: 10.1164/ajrccm.158.3.9710007     Document Type: Article

References (80)

1. Heath, D., and J. E. Edwards. 1958. The pathology of hypertensive pulmonary vascular disease: a description of six grades of structural changes in the pulmonary arteries with special reference to congeital cardiac septal defects. Circulation 18:533-547.
2. Wagenvoort, C. A., and N. Wagenvoort. 1970. Primary pulmonary hypertension: a pathologic study of the lung vessels in 156 clinically diagnosed cases. Circulation 42:1163-1184.
3. Bjornsson, J., and W. D. Edwards. 1985. Primary pulmonary hypertension: a histopathologic study of 80 cases. Mayo Clin. Proc. 60:16-25.
4. Pietra, G. G., W. D. Edwards, J. M. Kay, S. Rich, J. Kernis, B. Schloo, S. M. Ayres, E. H. Bergofsky, B. H. Brundage, K. M. Detre, A. P. Fishman, R. M. Goldring, B. M. Groves, P. S. Levy, L. M. Reid, C. E. Vreim, and G. W. Williams. 1989. Histopathology of primary pulmonary hypertension: a qualitative and quantitative study of pulmonary blood vessels from 58 patients in the National Heart, Lung, and Blood Institute Primary Pulmonary Hypertension Registry. Circulation 80: 1198-1206.
5. Dresdale, D. T., M. Schultz, and R. H. Michtom. 1951. Primary pulmonary hypertension: I. Clinical and hemodynamic study. Am. J. Med. 11:686-705.
6. Wood, P. 1959. Pulmonary hypertension with special reference to the vasoconstrictive factor. Br. Heart J. 21:557-570.
7. Reid, L. 1990. Vascular remodeling. In A. P. Fishman, editor. The Pulmonary Circulation: Normal and Abnormal. University of Pennsylvania Press, Philadelphia. 259-282.
8. Botney, M. D., and R. P. Mecham. 1994. Cellular mechanisms of vascular remodeling in primary pulmonary hypertension. In J. Murray and J. Nadel, editors. Textbook of Pulmonary Medicine. W. B. Saunders, Philadelphia. 1994.
9. Botney, M. D., L. R. Kaiser, J. D. Cooper, R. P. Mecham, J. Roby, and W. C. Parks. 1992. Extracellular matrix protein gene expression in atherosclerotic pulmonary arteries. Am. J. Pathol. 140:357-364.
10. Botney, M. D., M. J. Liptay, L. R. Kaiser, J. D. Cooper, W. C. Parks, and R. P. Mecham. 1993. Active collagen synthesis by pulmonary arteries in human primary pulmonary hypertension. Am. J. Pathol. 143:121-129.
11. Liptay, M. J., W. C. Parks, R. P. Mecham, J. Roby, L. R. Kaiser, J. D. Cooper, and M. D. Botney. 1993. Neointimal macrophages co-localize with extracellular matrix gene expression in human atherosclerotic pulmonary arteries. J. Clin. Invest. 91:588-594.
12. Botney, M. D., L. Bahadori, and L. I. Gold. 1994. Vascular remodeling in primary pulmonary hypertension: potential role for transforming growth factor-β. Am. J. Pathol. 144:286-295.
13. Bahadori, L., J. Milder, L. I. Gold, and M. D. Botney. 1995. Active macrophage-associated TGF-β colocalizes with type I procollagen gene expression in atherosclerotic human hypertensive pulmonary arteries. Am. J. Pathol. 146:1140-1149.
14. Schuster, D. P., E. C. Crouch, W. C. Parks, T. Johnson, and M. D. Botney. 1996. Angiotensin converting enzyme expression in primary pulmonary hypertension. Am. J. Respir. Crit. Care Med. 154:1087-1091.
15. Giaid, A., M. Yanagisawa, and D. Langleben. 1993. Expression of endothelin-1 in the lungs of patients with pulmonary hypertension. N. Engl. J. Med. 328:1732-1739.
16. Kerr, J. S., D. J. Riley, M. M. Frank, R. L. Trelstad, and H. M. Frankel. 1984. Reduction of chronic hypoxic pulmonary hypertension in the rat by beta-aminopropionitrile. J. Appl. Physiol. 57:1760-1766.
17. Kerr, J. S., C. L. Ruppert, C. A. Tozzi, J. A. Neubauer, H. M. Frenkel, S. Y. Yu, and D. J. Riley. 1987. Reduction of chronic hypoxic pulmonary hypertension in the rat by an inhibitor of collagen production. Am. Rev. Respir. Dis. 135:300-306.
18. Poiani, G. J., C. A. Tozzi, J. K. Choe, S. E. Yohn, and D. A. Riley. 1990. An antifibrotic agent reduces blood pressure in established pulmonary hypertension in the rat. J. Appl. Physiol. 68:1542-1547.
19. Tanaka, Y., D. P. Schuster, E. C. Davis, G. A. Patterson, and M. D. Botney. 1986. The role of vascular injury and hemodynamics in pulmonary artery remodeling. J. Clin. Invest. 98:434-442.
20. Okada, K., Y. Tanaka, M. Bernstein, W. Zhang, G. A. Patterson, and M. D. Botney. 1997. Pulmonary hemodynamics modify the rat pulmonary artery response to injury: a neointimal model of pulmonary hypertension: Am. J. Pathol. 151:1019-1025.
21. Morrell, N. W., E. N. Atochina, K. G. Morris, S. M. Danilov, and K. R. Stenmark. 1995. Angiotensin converting enzyme expression is increased in small pulmonary arteries of rats with hypoxia-induced pulmonary hypertension. J. Clin. Invest. 96:1823-1833.
22. Molteni, A., W. F. Ward, C. Ts'ao, and N. H. Solliday. 1985. Monocrotaline-induced pulmonary fibrosis in rats: amelioration by captopril and penicillamine. Proc. Soc. Exp. Biol. Med. 180:112-120.
23. Molteni, A., W. F. Ward, C. H. Ts'ao, and N. H. Solliday. 1986. Monocrotaline-induced cardiopulmonary damage in rats: amelioration by the angiotensin-converting enzyme inhibitor CL242817. Proc. Soc. Exp. Biol. Med. 182:483-493.
24. Morrell, N. W., K. G. Morris, and K. R. Stenmark. 1995. Role of angiotensin-converting enzyme and angiotensin II in development of hypoxic pulmonary hypertension. Am. J. Physiol. 269:H1186-H1194.
25. Nong, Z., J. M. Stassen, L. Moons, D. Collen, and S. Janssens. 1996. Inhibition of tissue angiotensin-converting enzyme with quinapril reduces hypoxic pulmonary hypertension and pulmonary vascular remodeling. Circulation 94:1941-1947.
26. Powell, J. S., J. P. Clozel, R. K. M. Muller, H. Kuhn, F. Hefti, M. Hosang, and H. R. Baumgartner. 1989. Inhibition of angiotensin-converting enzyme prevent myointimal proliferation after vascular injury. Science 245:186-188.
27. Farhy, R. D., O. A. Carretero, K.-L. Ho, and A. G. Scicli. 1993. Role of kinins and nitric oxide and the effects of angiotensin converting enzyme inhibitors on neointima formation. Circ. Res. 72:1202-1210.
28. Rakugi, H., D. S. Wang, V. J. Dzau, and R. E. Pratt. 1994. Potential importance of tissue angiotensin-converting enzyme inhibition in preventing neointima formation. Circulation 90:449-455.
29. Schoental, R., and M. A. Head. 1995. Pathological changes in rats as a result of treatment with monocrotaline. Br. J. Cancer 9:229-237.
30. Sugita, T., K. R. Stenmark, J. Wagner, P. M. Henson, J. E. Henson, T. M. Hyers, and J. T. Reeves. 1983. Abnormal alveolar cells in monocrotaline induced pulmonary hypertension. Exp. Lung Res. 5:201-215.
31. Todorovich-Hunter, L., D. J. Johnson, P. Ranger, F. W. Keeley, and M. Rabinovitch. 1988. Altered elastin and collagen synthesis associated with progressive pulmonary hypertension induced by monocrotaline: a biochemical and ultrastructural study. Lab. Invest. 58:184-195.
32. Tanaka, Y., M. L. Bernstein, R. P. Mecham, G. A. Patterson, J. D. Cooper, and M. D. Botney. 1996. Site-specific responses to monocrotaline-induced vascular injury: evidence for two distinct mechanisms of remodeling. Am. J. Respir. Cell Mol. Biol. 15:390-397.
33. Cushman, D. W., and H. S. Cheung. 1971. Spectrophotometric assay and properties of the angiotensin-converting enzyme of rabbit lung. Biochem. Pharmacol. 20:1637-1648.
34. Chomczynski, P., and N. Sacchi. 1987. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chlorophorm extraction. Anal. Biochem. 162:156-159.
35. Cassis, L. A., P. E. Rippetoe, E. E. Soltis, D. J. Painter, R. Fitz, and M. N. Gillespie. 1992. Angiotensin II and monocrotaline-induced pulmonary hypertension: effect of losartan (DuP 753), a nonpeptide angiotensin type I receptor antagonist. J. Pharmacol. Exp. Ther. 262:1168-1172.
36. Dubey, R. K., E. K. Jackson, and T. F. Luscher. 1995. Nitric oxide inhibits angiotensin II-induced migration of rat aortic smooth muscle cell: role of cyclic-nucleotides and angiotensin 1 receptors. J. Clin. Invest. 96:141-149.
37. Matsusaka, T., and I. Ichikawa. 1997. Biological functions of angiotensin and its receptors. Annu. Rev. Physiol. 59:395-412.
38. Gibbons, G. H., R. E. Pratt, and V. J. Dzau. 1992. Vascular smooth muscle cell hypertrophy versus hyperplasia: autocrine transforming growth factor expression determines growth response to angiotensin II. J. Clin. Invest. 90:456-461.
39. Crawford, D. C. A. V. Chobanian, and P. Brecher. 1994. Angiotensin II induces fibronectin expression associated with cardiac fibrosis in the rat. Circ. Res. 74:727-739.
40. Kagami, S., W. A. Border, D. E. Miller, and N. A. Noble. 1994. Angiotensin II stimulates extracellular matrix protein synthesis through induction of transforming growth factor-β expression in rat glomerular mesangial cells. J. Clin. Invest. 93:2431-2437.
41. Linz, W., G. Wiemer, P. Gohlke, T. Unger, and B. A. Scholkens. 1995. Contribution of kinins to the cardiovascular actions of angiotensin-converting enzyme inhibitors. Pharmacol. Rev. 47:25-49.
42. Nolly, H., O. A. Carretero, and A. G. Scicli. 1993. Kallikrein release by vascular tissue. Am. J. Physiol. 265:H1209-H1214.
43. Chao, J., J. V. Simson, P. Chung, L.-M. Chrn, and L. Chao. 1993. Regulation of kininogen gene expression and localization in the lung after monocrotaline-induced pulmonary hypertension in rats. Proc. Soc. Exp. Biol. Med. 203:243-250.
44. Goldstein, R. H., and P. Polgar. 1982. The effect and interaction of bradykinin and prostaglandins on protein and collagen production by lung fibroblasts. J. Biol. Chem. 257:8630-8633.
45. 9-bradykinin. J. Biol. Chem. 259:9263.
46. Nakajima, M., H. G. Hutchinson, M. Fujinaga, W. Hayashida, R. Morishita, L. Zhang, M. Horiuchi, R. E. Pratt, and V. J. Dzau. 1995. The angiotensin II type 2 (AT2) receptor antagonizes the growth effects of the ATI receptor: gain-of-function study using gene transfer. Proc. Natl. Acad. Sci. U.S.A. 92:10663-10667.
47. Stoll, M., U. M. Steckelings, M. Paul, S. P. Bottari, R. Metzger, and T. Unger. 1995. The angiotensin AT2-receptor mediates inhibition of cell proliferation in coronary endothelial cells. J. Clin. Invest. 95:651-657.
48. Yamada, T., M. Horiuchi, and V. J. Dzau. 1996. Angiotensin 11 type 2 receptor mediates programmed cell death. Proc. Natl. Acad. Sci. U.S.A. 93:156-160.
49. Rahinovitch, M., M. Mullen, H. C. Rosenberg, K. Maruyama, H. O'Brodovich, and P. M. Olley. 1988. Angiotensin II prevents hypoxic pulmonary hypertension and vascular changes in rat. Am. J. Physiol. 254: H500-H508.
50. Fishel, R. S., V. Thourani, S. J. Eisenberg, S. Y. Shai, M. A. Corson, E. G. Nabel, K. E. Bernstein, and B. C. Berk. 1995. Fibroblast growth factor stimulates angiotensin converting enzyme expression in vascular smooth muscle cells. J. Clin. Invest. 95:377-387.
51. Kawaguchi, H., H. Sawa, and H. Yasuda. 1990. Endothelin stimulates angiotensin I to angiotensin II conversion in cultured pulmonary artery endothelial cells. J. Mol. Cell. Cardiol. 22:839-842.
52. Wang, D. H., R. L. Prewitt, and S. J. Beebe. 1995. Regulation of PDGF-α: a possible mechanism for angiotensin II-induced vascular growth. Am. J. Physiol. 269:H356-H364.
53. Weber, H., D. S. Taylor, and C. J. Molloy. 1994. Angiotensin II induces delayed mitogenesis and cellular proliferation in rat aortic smooth muscle cells: correlation with the expression of specific endogenous growth factors and reversal by suramin. J. Clin. Invent. 93:788-798.
54. Vaughan, D. E., S. A. Lazos, and K. Tong. 1995. Angiotensin II regulates the expression of plasminogen activator inhibitor-1 in cultured endothelial cells: a potential link between the renin-angiotensin system and thrombosis. J. Clin. Invest. 95:995-1001.
55. Delafontaine, P., and H. Lou. 1993. Angiotensin II regulates insulin-like growth factor-I gene expression in vascular smooth muscle cells. J. Biol. Chem. 268:16866-16870.
56. Lemire, J. M., C. W. Covin, S. White, C. M. Giachelli, and S. M. Schwartz. 1994. Characterization of cloned aortic smooth muscle cells from young rats. Am. J. Pathol. 144:1068-1081.
57. Frid M, G., E. P. Moiseeva, and K. R. Stenmark. 1994. Multiple phenotypically distinct smooth muscle cell populations exist in the adult and developing bovine pulmonary arterial media in vivo. Circ. Res. 75:669-681.
58. Clowes, A. W., and M. J. Karnovsky. 1977. Suppression by heparin of smooth muscle cell proliferation in injured arteries. Nature 265:625-626.
59. Guyton, J. R., R. D. Rosenberg, A. W. Clowes, and M. J. Karnovsky. 1980. Inhibition of rat arterial smooth muscle cell proliferation by heparin: I. In vivo studies with anticoagulant and nonanticoagulant heparin. Circ. Res. 46:625-634.
60. Clowes, A. W., and M. M. Clowes. 1986. Kinetics of cellular proliferation after arterial injury: IV. Heparin inhibits rat smooth muscle mitogenesis and migration. Circ. Res. 58:839-845.
61. Snow, A. D., R. P. Bolender, T. N. Wight, and A. W. Clowes. 1990. Heparin modulates the composition of the extracellular matrix domain surrounding arterial smooth muscle cells. Am. J. Pathol. 137:313-330.
62. Clowes, A. W., M. M. Clowes, A. M. Gown, and T. N. Wight. 1984. Localization of proteoheparan sulfate in rat aorta. Histochemistry 80:379-384.
63. Castellot, J. J., L. V. Favreau, M. J. Karnovsky, and R. D. Rosenberg. 1982. Inhibition of vascular smooth muscle cell growth by endothelial cell-derived heparin. J. Biol. Chem. 257:11256-11260.
64. Castellot, J. J., M. L. Addonizio, R. Rosenberg, and M. J. Karnovsky. 1981. Cultured endothelial cells produces a heparinlike inhibitor of smooth muscle cell growth. J. Cell Biol. 90:372-379.
65. Fritze, L. M. S., C. F. Reilly, and R. D. Rosenberg. 1985. An antiproliferative heparan sulfate species produced by pustconfluent smooth muscle cells. J. Cell Biol. 100:1041-1049.
66. Benitz, W. E., R. T. Kelley, C. M. Anderson, D. E. Lorant, and M. Bernfield. 1990. Endothelial heparan sulfate proteoglycan: I. Inhibitory effects on smooth muscle cell proliferation. Am. J. Respir. Cell Mol. Biol. 2:13-24.
67. Pukac, L. A., J. J. Castellot, T. J. Wright, B. L. Caleb, and M. J. Karnovsky. 1990. Heparin inhibits c-fos and c-myc mRNA expression in vascular smooth muscle cells. Cell Regul. 1:435-443.
68. San, A. J., M. J. Karnovsky, M. E. Ottlinger, R. Schillig, and L. A. Pukac. 1993. Isolation of heparin-insensitive aortic smooth muscle cells: growth and differentiation. Arterioscler. Thromb. 13:748-757.
69. Barzu, T., J. M. Herbert, A. Desmouliere, P. Carayon, and M. Pascal. 1994. Characterization of rat aortic smooth muscle cells resistant to the antiproliferative activity of heparin following long-term heparin treatment. J. Cell. Physiol. 160:239-248.
70. Caleb, B. L., M. Hardenbrook, V. Cherington, and J. J. Castellot. 1996. Isolation of vascular smooth muscle cell cultures with altered responsiveness to the antiproliferative effect of heparin. J. Cell. Physiol. 167: 185-195.
71. Chan. P., M. Patel, L. Betteridge, E. Munro, M. Schachter, J. Wolfe, and P. Sever. 1993. Abnormal growth regulation of vascular smooth muscle cells by heparin in patients with restenosis. Lancet 341:341-342.
72. Albert, M. A., T. A. Pressly, V. Mukerji, C. R. Lambert, and B. Mukerji. 1992. Short- and long-term hemodynamic effects of captopril in patients with pulmonary hypertension and selected connective tissue disease. Chest 102:1407-1412.
73. Escudero, J., J. Navarro, A. Padua, L. Betancourt, and G. Nava. 1987. Hemodynamic changes with enalapril in pulmonary arterial hypertension secondary to congenital heart disease. Chest 91:351-355.
74. Stumpe, K. O., K. Schmengler, L. Bette, A. Overlack, and R. Kolloch. 1986. Persistent hemodynamic and clinical improvement after captopril in patients with pulmonary hypertension. Herz. 11:217-225.
75. Leier, C. V., D. Bambach, S. Nelson, J. B. Hermiller, P. Huss, R. D. Magorien, and D. V. Unverferth. 1983. Captopril in primary pulmonary hypertension. Circulation 67:155-161.
76. Rich, S., B. H. Brundage, and P. S. Levy. 1985. The effect of vasodilator therapy on the clinical outcome of patients with primary pulmonary hypertension. Circulation 71:1141-1196.
77. Weir, E. K. 1990. Acute vasodilator testing and pharmacological treatment of primary pulmonary hypertension. In A. P. Fishman, editor. The Pulmonary Circulation: Normal and Abnormal. University of Pennsylvania Press, Philadelphia. 259-282.
78. Jones, D. K., T. W. Higginhottam, and J. Wallwork. 1987. Treatment of primary pulmonary hypertension with intravenous epoprostenol (prostacyclin). Br. Heart J. 57:270-278.
79. Rubin, L. J., J. Mendoza, M. Hood, M. McGoon, R. Barst, W. B. Williams, J. H. Diehl, J. Crow, and W. Long. 1990. Treatment of primary pulmonary hypertension with continuous intravenous prostacyclin (epoprostenol). Ann. Intern. Med. 112:485-491.
80. Barst, R. J., L. J. Rubin, W. A. Long, M. D. McGoon, S. Rich, D. B. Badesch, B. M. Groves, V. F. Tapson, R. C. Bourge, B. H. Brundage, S. K. Koerner, D. Langlehen, C. A. Keller, S. Murali, B. F. Uretsky, L. M. Clayton, M. M. Jobsis, S. E. Blackburn, D. Shortino, and J. W. Crow. 1996. A comparison of continuous intravenous epoprostenol (prostacyclin) with conventional therapy for primary pulmonary hypertension. N. Engl. J. Med. 334:296-301.