Cyclic GMP-Dependent protein kinase regulates vascular smooth muscle cell phenotype

Journal of Vascular Research

Volumn 34, Issue 4, 1997, Pages 245-259

  Boerth, Nancy J ^a   Dey, Nupur B ^a   Cornwell, Trudy L ^a   Lincoln, Thomas M ^a  

^a University of Alabama at Birmingham   (United States)

Author keywords

cGMP; Contraction; Differentiation; Migration; Morphology; Nitric oxide; Phosphorylation; Proliferation; Smooth muscle

Indexed keywords

CYCLIC GMP DEPENDENT PROTEIN KINASE; NITRIC OXIDE;

ANIMAL TISSUE; AORTA; ARTERY INJURY; ARTERY INTIMA PROLIFERATION; ARTICLE; CONTROLLED STUDY; MODULATION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REGULATORY MECHANISM; VASCULAR SMOOTH MUSCLE;

EID: 0030842912     PISSN: 10181172     EISSN: 14230135     Source Type: Journal    
DOI: 10.1159/000159231     Document Type: Article

References (82)

1. Schwartz SM, O’brien ER, deBlois D, Giachclli CM: Relevance of smooth muscle cell replication and development to vascular disease: in Schwartz SM, Mccham RP (eds): The Vascular Smooth Muscle Cell, San Diego, Academic Press, 1995, pp 81-139.
2. Ross R: Growth regulatory mechanisms and formation of the lesions of atherosclerosis, Ann NY Acad Sci 1995;748:1-4.
3. Mosse PR, Campbell GR, Wang ZL, Campbell JH: Smooth muscle phenotypic expression in human carotid arteries, I, Comparison of cells from diffuse intimai thickenings adjacent to atheromatous plaques with those of the media, Lab Invest 1985;53:556-562.
4. Fingerle J, Johnson R, Clowes AW, Majcsky MW, Reidv MA: Role of platelets in smooth muscle cell proliferation and migration after vascular injury in rat carotid artery, Proc Natl Acad Sci USA 1989;86:8412-8416.
5. Schwartz SM, Heimark RL, Majesky MW: Developmental mechanisms underlying pathology of arteries, Physiol Rev 1990:70:1177-1209.
6. Ferns GA, Stewart-Lee AL, Anggard EE: Arterial responses to mechanical injury: Balloon catheter de-endothelialization, Atherosclerosis 1992;92:89-104.
7. Ross R: The pathogenesis of atherosclerosis: A perspective for the 1990s, Nature 1993:362: 801-809.
8. Fritz KE, Jarmoiych J, Daoud AS: Association of DNA synthesis and apparent dedifferentiation of aortic smooth muscle cells in vitro, Exp Mol Pathol 1970;12:354-362.
9. Barja F, Cougglin C, Belin D, Gabbiani G: Action isoform synthesis and mRNA levels in quiescent and proliferating rat aortic smooth muscle cells in vivo and in vitro, Lab Invest 1986:64:5-15.
10. Glukhova MA, Kabakov AE, Frid MG, Omas-kv OI, Belkin AM, Mukhin DN, Orekhov AN, Kotcliansky VE, Smirnov VN: Modulation of human aorta smooth muscle cell phenotype: A study of muscle-specific variants of vinculin, caldcsmon and actin expression, Proc Natl Acad Sci USA 1988:85:9542-9546.
11. Majesky MW, Giachelli CM, Reidy MA, Schwartz SM: Rat carotid neointimal smooth muscle cells rc-cxpress a developmcntally regulated phenotype during repair of arterial injury, CircRes 1992;71:759-768.
12. Campbell JH, Campbell GR: Smooth muscle cell phenotype changes in arterial wall homeostasis: Implication for the pathogenesis of atherosclerosis, Exp Mol Pathol 1985:42:136-162.
13. Gown AM, Tsukada T, Ross R: Human atherosclerosis, II, Immunocytochcmical analysis of the cellular composition of human atherosclerotic lesions, Am J Pathol 1986:125:191-207.
14. Benditt EP, Benditt JM: Evidence for a monoclonal origin of human atherosclerotic plaques, Proc Natl Acad Sci USA 1973:70:1753-1756.
15. Pearson TA, Solez K, Dillman J, Heptinstal R: Monoclonal characteristics of organising arterial thrombi: Significance in the origin and growth of human atherosclerotic plaques, Lancet 1979;i:7-11.
16. Thomas WA, Reiner JM, Janakidevi K, Flo-ricntin RA, Lee KT: Population dynamics of arterial cells during athcrogencsis, X, Study of monotypism in atherosclerotic lesions of black woman heterozygous for glucose-6-phosphate dehydrogenase (G-6-PD), Exp Mol Pathol 1979;31:367-386.
17. ChaMIey-Campbell J, Campbell GR, Ross R: Phenotype-dependent response of cultured aortic smooth muscle cells to scrum mitogens, J Cell Biol 1981;89:379-383.
18. Hedin U, Sjolund M, Hultgardh-Nilsson A, Thyberg J: Changes in expression and organization of smooth muscle-specific a-actin during fibroncctin-mediatcd modulation of arterial smooth muscle cell phenotype, Differentiation 1990;44:222-231.
19. Thyberg J, Hedin U, Sjolund M, Palmberg L, Bottger BA: Regulation of differentiated properties and proliferation of arterial smooth muscle cells, Arteriosclerosis 1990:10:966-990.
20. ChaMIey-Campbell J, Campbell GR, Ross R: The smooth muscle cell in culture, Physiol Rev 1979:59:1-61.
21. Garg UC, Hassid A: Nitric oxide-generating vasodilators and 8-bromo-cyclic guanosinc monophosphate inhibit mitogenesis and proliferation of cultured rat vascular smooth muscle cells, J Clin Invest 1989:83:1774-1777.
22. 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.
23. Nakaki T, Nakayanta M, Kato R: Inhibition by nitric oxide and nitric oxide-producing vasodilators of DNA synthesis in vascular smooth muscle cells, Eur J Pharmacol 1990:189:347-353.
24. Cook JP, Singer AH, Tsao P, Zera P, Rowan RA, Billingham ME: Antiatherogenic effects of ¿-arginine in the hypercholestérolémie rabbit, J Clin Invest 1992:90:1168-1172.
25. McNamara DB, Bedi B, Aurora H, Tena L, Ignarro LJ, Kadowitz PJ, Akers DL: J-Arginine inhibits balloon catheter-induced intimai hyperplasia, Biochem Biophys Res Commun 1993:193:291-296.
26. Davies MJ, Kim JH, Dalen H, Makhoul RG, Svcndsen E, Hagen PO: Reduction of experimental vein graft intimai hyperplasia and preservation of nitric oxide-mediated relaxation by the nitric oxide precursor Jarginine, Surgery 1994:116:557-568.
27. Cayatte AJ, Palacino JJ, Horten K, Cohen RA: Chronic inhibition of nitric oxide production accelerates neointima formation and impairs endothelial function in hypercholestérolémie rabbits, Artcriosclcr Thromb 1994; 14:753-759.
28. Gordon D, Reidy MA, Benditi EP, Schwartz SM: Cell proliferation in human coronary arteries, Proc Natl Acad Sci USA 1990:87:4600-4604.
29. Katsuda S, Coltrerà MD, Ross R, Gown AM: Human atherosclerosis, IV, Immunocytochem-ical analysis of cell activation and proliferation in lesions of young adults, Am J Pathol 1993; 142:1787-1793.
30. Ignarro LJ, Kadowitz P: The pharmacological and physiological role of cyclic GMP in vascular smooth muscle relaxation, Annu Rev Phar-macol Toxicol 1985;25:171-191.
31. Furchgott RF: Studies on relaxation of rabbit aorta by sodium nitrate: The basis for the proposal that the acid-activatable inhibitory factor from bovine retractor penis is inorganic nitrate and the endothelium-derived relaxing factor is nitric oxide; in Vanhoutte P (ed): Mechanisms of Vasodilation, New York, Raven, 1988, vol 4, pp 401-414.
32. Hofmann F, Dostmann W, Kcilbach A, Land-graff W: Structure and physiological role of cGMP-dependent protein kinase, Biochim Biophys Acta 1992; 1135:51-60.
33. Lincoln TM, Cornwell TL: Intracellular cyclic GMP receptor proteins, FASEB J 1993:7:328-338.
34. 2+ by atriopeptin and 8-bromo-cyclic GMP is mediated by cyclic GMP-dependent protein kinase, J Biol Chem 1989;264:1146-1155.
35. 2+ by cAMP in vascular smooth muscle cells, Am J Physiol 1990:258:C399-C407.
36. Cornwell TL, Soff GA, Traynor AE, Lincoln TM: Regulation of the expression of cyclic GMP-dependent protein kinase by cell density in vascular smooth muscle cells, J Vase Res 1994;31:330-337.
37. Chomczynski P, Sacchi N: Single-step method of RNA isolation by acid guanidinium thiocya-nate-phcnol-chloroform extraction, Anal Bio-chent 1987;162:156-159.
38. Wemet W, Flockerzi V, Hofmann F: The cDNAs of the two isoforms of bovine cGMP-dcpendent protein kinase, FEBS Lett 1989; 251:191-196.
39. Boerth NJ, Lincoln TM: Expression of the catalytic domain of cyclic GMP-dependent protein kinase in a baculovirus system, FEBS Lett 1994;342:255-260.
40. Kelly CA, Sellers JR., Goldsmith PK, Adelstcin RS: Smooth muscle myosin is composed of homodimcric heavy chains, J Biol Chem 1992; 267:2127-2130.
41. Winder SJ, Sutherland C, Walsh MP: Biochemical and functional characterization of smooth muscle calponin, Adv Exp Med Biol 1991;304:37-51.
42. Colbran JL, Francis SH, Leach AB, Thomas MK, Jiang H, McAllister LM, Corbin JD: A phenylalanine in peptide substrates provides for selectivity between cGMP-dependent and cAMP-dependent protein kinases, J Biol Chem 1992;267:9589-9594.
43. Sckhar KR, Hatchett RJ, Shabb JB, Francis SH, Wells JN, Corbin JD: Relaxation of pig coronary arteries by new and potent cGMP analogs that selectively activate type la compared to type Iß cGMP-dependent protein kinase, Mol Pharmacol 1992;42:103-108.
44. Ueki N, Sobue K, Kanda K, Hada T, Higashi-no K: Expression of high and low molecular weight caldesmons during phenotypic modulation of smooth muscle cells, Proc Natl Acad Sci USA 1987:84:9094-9053.
45. Kawamoto S, Adelstcin RS: Characterization of myosin heavy chains in cultured aorta smooth muscle cells: A comparative study, J Biol Chem 1987;262:7282-7288.
46. Tachas G, Campbell JH, Campbell GR: Genes expressed during vascular smooth muscle phenotype modulation, Ann NY Acad Sci 1990; 598:540-543.
47. Glukhova MA, Frid G, Koteliansky VE: Developmental changes in expression of contractile and cytoskeletal proteins in human aortic smooth muscle, J Biol Chem 1990:265:13042-13046.
48. Frid MG, Printesva OY, Chiavcgato A, Faggin E, Scatena M, Koteliansky VE, Pauletto P, Glukhova MA, Sartore S: Myosin heavy chain isoform composition and distribution in developing and adult human aortic smooth muscle, J Vase Res 1993:30:279-292.
49. Kocher O, Gabbiani F, Gabbiani G, Reidy MA, Cokay MS, Peters H, Hüttner I: Phenotypic features of smooth muscle cells during the evolution of experimental carotid artery intimai thickening: Biochemical and morphologic studies, Lab Invest 1991:65:459-470.
50. Takahashi K, Nadal-Ginard B: Molecular cloning and sequence analysis of smooth muscle calponin, J Biol Chem 1991:266:13284-13288.
51. Shanahan CM, Weissberg PC, Metcalfe JC: Isolation of gene markers of differentiated and proliferating vascular smooth muscle cells, Circ Res 1993;73:193-204.
52. Rovner AS, Murphy RA, Owens GK: Expression of smooth muscle and nonmuscle myosin heavy chains in cultured vascular smooth muscle cells, J Biol Chem 1986;261:14740-14745.
53. Rovner AS, Thompson MM, Murphy RA: Two different heavy chains are found in smooth muscle myosin, Am J Physiol 1986:250:C861-C870.
54. Miaño J, Cscrjesi P, Ligón K, Periasamy M, Olsor, EN: Smooth muscle myosin heavy chain exclusively marks the smooth muscle lineage during mouse embrvogencsis, Circ Res 1994; 75:803-812.
55. Periasamy M, Nagai R: Molecular basis of smooth muscle contractility-Myosin heavy chains: Gene structure and expression; in Schwartz SM, Méchant PP (eds): The Vascular Smocth Muscle Cell, San Diego, Academic Press, 1995, pp 189-211.
56. Kuro-o M, Nagai R, Tsuchimochi H, Katoh H, Yazaki Y, Ohkubo A, Takaku F: Developmen-tally regulated expression of vascular smooth muscle myosin heavy chain isoforms, J Biol Cheni 1989;264:18272-18275.
57. Kuroo M, Nagai R, Nakahara K, Katoh H, Tsai RC, Tsuchimochi H, Yazaki Y, Ohkubo A, Takaku F: cDNA cloning of a myosin heavy chain isoform in embryonic smooth muscle and its expression during vascular development and in arteriosclerosis, J Biol Chem 1991; 266:3768-3773.
58. Sartore S, Scatena M, Chiavegato A, Faggin E, Giurialo L, Paulctto P: Myosin isoform expression in smooth muscle cells during physiological and pathological vascular remodeling, J Vase Res 1994;31:61-81.
59. Gimona M, Hersog M, Vandederckhove J, Small J V: Smooth muscle specific expression of calponin, FEBS Lett 1990;274:159-162.
60. Draeger A, Gimona M, Stuckert A, Celis JE, Small JV; Calponin: Developmental isoforms and a low molecular weight variant, FEBS Lett 1991:291:24-28.
61. Blank RS, Owens GK: Platelet-derived growth factor regulates actin isoform expression and growth state in cultured rat aortic smooth muscle cells, J Cell Physiol 1990;142:635-642.
62. Cornwell TL, Arnold E, Bocrth NJ, Lincoln TM: Inhibition of smooth muscle cell growth by nitric oxide and activation of c.AMP-depen-dent protein kinase by cGMP, Am J Physiol 1994;267:C1405-C1413.
63. Lincoln TM, Cornwell TL, Komalavilas P, MacMillan-Crow LA, Boerth NJ: The nitric oxide-cyclic GMP signaling system; in Barany M (ed): Biochemistry of Smooth Muscle Contraction, San Diego, Academic Press, 1996, pp 257-268.
64. Blank RS, Swartz EA, Thompson MM, Olson EN, Owens GK: A retinoic acid-induced clonal cell line derived from multipotential P19 embryonal carcinoma cells express smooth muscle characteristics, Circ Res 1995;76:742-749.
65. Miano JM, Topouzis S, Majesky MW, Olson EN: Retinoid receptor expression and all trans retinoic acid-mediated growth inhibition in vascular smooth muscle cells, Circulation 1996;93:1886-1895.
66. Reusch P, Wagdy M, Rcusch R, Wilson E, Ives HE: Mechanical strain increases smooth muscle and decreases nonmuscle myosin expression in rat vascular smooth muscle cells, Circ Res 1996;79:1046-1053.
67. Hassid A, Arabshahi H, Bourcier T, Dhaunsi GS, Matthews C: Nitric oxide selectively amplifies FGF-2 mitogenesis in primary rat aortic smooth muscle cells, Am J Physiol 1994:267: H1040-H1048.
68. Murphy-Uilrich JE, Pallerò MA, Bocrth NJ, Greenwood JA, Lincoln TM, Cornwell TL: Cyclic GMP-dependent protein kinase is required for thrombospondin and tcnascin-mcdiatcd focal adhesion disassembly, J Cell Sci 1996:109: 2499-2508.
69. Dubey RK, Jackson EK, Luscher TF: Nitric oxide inhibits angiotensin 11-mediatcd migration of rat aortic smooth muscle cells, J Clin Invest 1995;96:141-149.
70. Jiang H, Colbran JL, Francis SH, Corbin JD: Direct evidence for cross-activation of cGMP-dependent protein kinase by cAMP in pig coronary arteries, J Biol Chem 1992:267:1015-1019.
71. Soff G, Cornwell TM, Cundiff DI., Wade EL, Lincoln TM: Smooth muscle cell expression of type 1 cyclic GMP-dependcnt protein kinase is suppressed by continuous exposure to nitrova-sodilators, theophylline, cyclic GMP, and cyclic AMP, J Clin Invest, in revision.
72. Beasley D, McGuiggin ME: Interleukin 1 activates soluble guanvlate cyclase in human vascular smooth muscle cells through a novel nitric oxide-independent pathway, J Exp Med 1994;179:71-80.
73. Beasley D, Eldridgc M: Interleukin Ip and tumor necrosis factor a synergistically induce nitric oxide synthase in rat vascular smooth muscle cells, Am J Phvsiol 1994:266:R1197-R1203.
74. Beasley D, McGuiggin ME: Interleukin 1 induces prostacyclin-dependent increases in cyclic AMP production and does not affect cyclic GMP production in human vascular smooth muscle cells, Cytokine 1995:7:417-426.
75. Janiak P, Villeneuve N, Pillon A, Jacquemin C, Vilaine JP: Interleukin lß aggravated the neointima formation after injury despite inducing nitric oxide synthase in rat carotid artery, FASEBJ 1996; 10:A619.
76. Farhy RD, Carretero O.A, Ho KL, Scicli AG: Role of kinins and nitric oxide in the effects of angiotensin converting enzyme inhibitors on neointima formation, Circ Res 1993:72:1202-1210.
77. Soyombo AA, Angelini GD, Newby AC: Neointima formation is promoted by surgical preparation and inhibited by cyclic nucleotides in human saphenous vein organ cultures, J Thorac Cardiovase Surg 1995:109:2-12.
78. Wolf YG, Rasmussen LM, Sherman Y, Bunden» WP, Hye RJ: Nitroglycerine decreases medial smooth muscle cell proliferation after arterial balloon injury, J Vase Surg 1995:21: 499-504.
79. Sek, J, Nishio M, Kalo Y, Motoyama Y, Yoshi-da K: FK.409, a new nitric oxide donor, suppresses smooth muscle proliferation in the rat model of balloon angioplasty, Atherosclerosis 1995:117:97-106.
80. De Meyer GR, Bult H, Ustuncs L, Kockx MM, Feclisch M, Herman AG: Effect of nitric oxide donors on neointima formation and vascular reactivity in the collared carotid artery of rabbits J Cardiovasc Pharmacol 1995;26:272-279.
81. van der Leven HE, Gibbons GH, Morishita R, Lewis NP, Zhang L, Nakayima M, Kaneda Y, Cooke JP, Dzau VJ: Gene therapy inhibits ncomtimal vascular lesion, In vivo transfer of endothelial nitric oxide synthase gene, Proc Natl Acad Sci USA 1995:92:1137-1141.
82. Pollman MJ, Yamada T, Horiuchi M, Gibbons GH: Vasoactive substances regulate vascular smooth muscle cell apoptosis, Countervailing influences of nitric oxide and angiotensin II, Circ Res 1996:79:748-756.