Lipid lowering promotes accumulation of mature smooth muscle cells expressing smooth muscle myosin heavy chain isoforms in rabbit atheroma

Circulation Research

Volumn 83, Issue 10, 1998, Pages 1015-1026

  Aikawa, Masanori ^a   Rabkin, Elena ^a   Voglic, Sami J ^a   Shing, Helen ^a   Nagai, Ryozo ^b   Schoen, Frederick J ^a   Libby, Peter ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b GUNMA UNIVERSITY   (Japan)

Author keywords

Atherosclerosis; Hypercholesterolemia; Lipid lowering; Smooth muscle cell differentiation

Indexed keywords

ALPHA ACTIN; CHOLESTEROL; GELATINASE B; MYOSIN HEAVY CHAIN; STROMELYSIN; TRIACYLGLYCEROL;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AORTA INJURY; ARTICLE; ATHEROMA; CHOLESTEROL INTAKE; CONTROLLED STUDY; HYPERCHOLESTEROLEMIA; HYPOCHOLESTEROLEMIA; MALE; NONHUMAN; PRIORITY JOURNAL; RABBIT; SMOOTH MUSCLE FIBER;

EID: 0032538870     PISSN: 00097330     EISSN: None     Source Type: Journal    
DOI: 10.1161/01.RES.83.10.1015     Document Type: Article

References (52)

1. Owens GK. Regulation of differentiation of vascular smooth muscle cells. Physiol Rev. 1995;75:487-517.
2. Nagai R, Larson DT, Periasamy M. Characterization of a mammalian smooth muscle myosin heavy chain cDNA clone and its expression in various smooth muscle types. Proc Natl Acad Sci U S A. 1988;85:1047-1051.
3. Nagai R, Kuro-o M, Babij P, Periasamy M. Identification of two types of smooth muscle myosin heavy chain isoforms by cDNA cloning and immunoblot analysis. J Biol Chem. 1989;264:9734-9737.
4. Miano JM, Cserjesi P, Ligon KL, Periasamy M, Olson EN. Smooth muscle myosin heavy chain exclusively marks the smooth muscle lineage during mouse embryogenesis. Circ Res. 1994;75:803-812.
5. Kuro-o M, Nagai R, Tsuchimochi H, Katoh H, Yazaki Y, Ohkubo A, Takaku F. Developmentally regulated expression of vascular smooth muscle myosin heavy chain isoforms. J Biol Chem. 1989;264:18272-18275.
6. Aikawa M, Sivam PN, Kuro-o M, Kimura K, Nakahara K, Takewaki S, Ueda M, Yamaguchi H, Yazaki Y, Nagai R. Human smooth muscle myosin heavy chain isoforms as molecular markers for vascular development and atherosclerosis. Circ Res. 1993;73:1000-1012.
7. Holycross BJ, Blank RS, Thompson MM, Peach MJ, Owens GK. Platelet-derived growth factor-BB-induced suppression of smooth muscle cell differentiation. Circ Res. 1992;71:1525-1532.
8. Okamoto E, Imataka K, Fujii J, Kuro-o M, Nakahara K, Nishimura H, Yazaki Y, Nagai R. Heterogeneity in smooth muscle cell population accumulating in the neointima and the media of poststenotic dilatation of the rabbit carotid artery. Biochem Biophys Res Commun. 1992;185: 459-464.
9. Okamoto E, Suzuki T, Aikawa M, Imataka K, Fujii J, Kuro-o M, Nakahara K, Hasegawa K, Yazaki Y, Nagai R. Diversity of the synthetic-state smooth muscle cells proliferating in mechanically and hemodynamically injured rabbit arteries. Lab Invest. 1996;74: 120-128.
10. Aikawa M, Sakomura Y, Ueda M, Kimura K, Manabe I, Ishiwata S, Komiyama N, Yamaguchi H, Yazaki Y, Nagai R. Redifferentiation of smooth muscle cells after coronary angioplasty determined via myosin heavy chain expression. Circulation. 1997;96:82-90.
11. Kuro-o 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.
12. Kawamoto S, Adelstein RS. Chicken nonmuscle myosin heavy chains: differential expression of two mRNAs and evidence for two different polypeptides. J Cell Biol. 1991;112:915-924.
13. Simons M, Wang M, McBride OW, Kawamoto S, Yamanaka K, Gdula D, Adelstein RS, Weir L. Human nonmuscle myosin heavy chains are encoded by two genes located on different chromosomes. Circ Res. 1991;69:530-539.
14. De Leon H, Scott NA, Martin F, Simonet L, Bernstein KE, Wilcox JN. Expression of nonmuscle myosin heavy chain-B isoform in the vessel wall of porcine coronary arteries after balloon angioplasty. Circ Res. 1997;80:514-519.
15. Suzuki J, Isobe M, Aikawa M, Kawauchi M, Shiojima I, Kobayashi N, Tojo A, Kimura K, Nishikawa T, Sakai T, Sekiguchi M, Yazaki Y, Nagai R. Nonmuscle and smooth muscle myosin heavy chain expression in rejected cardiac allografts: a study in rat and monkey models. Circulation. 1996;94:1118-1124.
16. Hiroi J, Kimura K, Aikawa M, Tojo A, Suzuki Y, Nagamatsu T, Omata M, Yazaki Y, Nagai R. Expression of a nonmuscle myosin heavy chain in glomerular cells differentiates various types of glomerular disease in rats. Kidney Int. 1996;49:1231-1241.
17. Frid MG, Printesva OY, Chiavegato 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 Vasc Res. 1993;30:279-292.
18. Henney AM, Wakeley PR, Davies MJ, Foster K, Murphy G, Humphries S. Localization of stromelysin gene expression in atherosclerotic plaque by in situ hybridization. Proc Natl Acad Sci U S A. 1991;88:8154-8158.
19. Galis ZS, Sukhova GK, Lark MW, Libby P. Increased expression of matrix metalloproteinases and matrix degrading activity in vulnerable regions of human atherosclerotic plaques. J Clin Invest. 1994;94:2493-2503.
20. Brown DL, Hibbs MS, Keaney M, Loushin C, Isner JM. Identification of 92-kD gelatinase in human coronary atherosclerotic lesions: association of active enzyme synthesis with unstable angina. Circulation. 1995;91: 2125-2131.
21. Nikkari ST, O'Brien KD, Ferguson M, Hatsukami T, Welgus HG, Alpers CE, Clowes AW. Interstitial collagenase (MMP-1) expression in human carotid atherosclerosis. Circulation. 1995;92:1393-1398.
22. Sacks FM, Pfeffer MA, Moye LA, Rouleau JL, Rutherford JD, Cole TG, Brown L, Wanica JW, Arnold JMO, Wun CC, Davis BR, Braunwald E. The effect of pravastatin on coronary events after myocardial infarction in patients with average cholesterol levels. N Engl J Med. 1996;335: 1001-1009.
23. 4S Group. Randomized trial of cholesterol lowering in 4444 patients with coronary heart disease: the Scandinavian Simvastatin Survival Study (4S). Lancet. 1994;344:1383-1389.
24. Shepherd J, Cobbe SM, Ford I, Isles CG, Lorimer AR, MacFarlane PW, McKillip JH, Packard CJ. Prevention of coronary heart disease with pravastatin in men with hypercholesterolemia. N Engl J Med. 1995;333: 1301-1307.
25. Armstrong ML, Megan MB. Lipid depletion in atheromatous coronary arteries in rhesus monkeys after regression diet. Circ Res. 1972;30:675-680.
26. Armstrong ML, Megan MB. Arterial fibrous proteins in cynomolgus monkeys after atherogenic and regression diets. Circ Res. 1975;36: 256-261.
27. Small DM, Bond MG, Waugh D, Prack M, Sawyer JK. Physicochemical and histological changes in the arterial wall of non-human primates during progression and regression of atherosclerosis. J Clin Invest. 1984; 73:1590-1605.
28. Kaplan JR, Manuck SB, Adams MR, Williams JK, Register TC, Clarkson TB. Plaque changes and arterial enlargement in atherosclerotic monkeys after manipulation of diet and social environment. Arterioscler Thromb. 1993;13:254-263.
29. Shiomi M, Itoh T, Tsukada T, Yata T, Watanabe Y, Tsujita Y, Fukami M, Fukushige J, Hosokawa T, Tamura A. Reduction of serum cholesterol levels alters lesional composition of atherosclerotic plaques: effect of pravastatin sodium on atherosclerosis in mature WHHL rabbits. Arterioscler Thromb Vasc Biol. 1995;15:1938-1944.
30. Aikawa M, Rabkin E, Okada Y, Voglic SJ, Clinton SK, Brinckerhoff CE, Sukhova GK, Libby P. Lipid lowering by diet reduces matrix metelloproteinase activity and increases collagen content of rabbit atheroma: a potential mechanism of lesion stabilization. Circulation. 1998;97: 2433-2444.
31. Galis ZS, Sukhova GK, Kranzhofer R, Clark S, Libby P. Macrophage foam cells from experimental atheroma constitutively produce matrix-degrading proteinases. Proc Natl Acad Sci U S A. 1995;92:402-406.
32. Lee RT, Schoen FJ, Loree ML, Lark MW, Libby P. Circumferential stress and matrix metalloproteinase-1 in human coronary atherosclerosis. Implications for plaque rupture. Arterioscler Thromb Vasc Biol. 1996;16: 1070-1073.
33. Heinz N, Sive HL, Roeder RG. Regulation of human histone gene expression: kinetics of accumulation and changes in the rate of synthesis and in the half-lives of individual histone mRNAs during the HeLa cell cycle. Mol Cel Biol. 1983;3:539-550.
34. Alison M, Chaudry Z, Baker J, Lauder I. Liver regeneration: a comparison of in situ hybridization for histone mRNA with bromodeoxyuridine labeling for the detection of S-phase cells. J Histochem Cytochem. 1994;42:1603-1608.
35. Babij P, Kawamoto S, White S, Adelstein RS, Periasamy M. Differential expression of SM1 and SM2 myosin isoforms in cultured vascular smooth muscle. Am J Physiol. 1992;262:C6007-C6013.
36. Zanellato AM, Borrione AC, Tonello M, Scannapieco G, Pauletto P, Sartore S. Myosin isoform expression and smooth muscle cell heterogeneity in normal and atherosclerotic rabbit aorta. Arteriosclerosis. 1990; 10:996-1009.
37. Ross R, Masuda J, Raines EW, Gown AM, Katsuda S, Sasahara M, Maiden LT, Masuko H, Sato H. Localization of PDGF-B protein in macrophages in all phases of atherogenesis. Science. 1990;248: 1009-1012.
38. Uchida K, Sasahara M, Morigami N, Hazama F, Kinoshita M. Expression of platelet-derived growth factor B-chain in neointimal smooth muscle cells of balloon injured rabbit femoral arteries. Atherosclerosis. 1996; 124:9-23.
39. Kim HS, Aikawa M, Kimura K, Kuro-o M, Nakahara K, Suzuki T, Katoh H, Okamoto E, Yazaki Y, Nagai R. Ductus arteriosus: advanced differentiation of smooth muscle cells demonstrated by myosin heavy chain isoform expression in rabbits. Circulation. 1993;88(Part 1):1804-1810.
40. Kimura K, Nagai R, Sakai T, Aikawa M, Kuro-o M, Kobayashi N, Shirato I, Inagami T, Oshi M, Suzuki N, Oba S, Mise N, Tojo A, Hirata Y, Goto A, Yazaki Y, Omata M. Diversity and variability of smooth muscle phenotypes of renal arterioles as revealed by myosin isoform expression. Kidney Int. 1995;48:372-382.
41. Chamley-Campbell J, Campbell GR, Ross R. The smooth muscle cell in culture. Physiol Rev. 1979;59:1-61.
42. Katoh Y, Loukianov E, Kopras E, Zilberman A, Periasamy M. Identification of functional promotor elements in the rabbit smooth muscle myosin heavy chain gene. 1994;48:30538-30545.
43. Watanabe M, Sakomura Y, Kurabayashi M, Manabe I, Aikawa M, Kuro-o M, Suzuki T, Yazaki Y, Nagai R. Structure and characterization of the 5′-flanking region of the mouse smooth muscle myosin heavy chain (SM1/2) gene. Circ Res. 1996;78:978-989.
44. Manabe I, Kurabayashi M, Shimomura Y, Kuro-o M, Watanabe N, Watanabe M, Aikawa M, Suzuki T, Yazaki Y, Nagai R. Isolation of the embryonic form of smooth muscle myosin heavy chain (SMemb/ NMHC-B) gene and characterization of its 5′-flanking region. Biochem Biophys Res Commun. 1997;239:598-605.
45. Madsen CS, Hershey JC, Hautmann MB, White SL, Owens GK. Expression of the smooth muscle myosin heavy chain gene is regulated by a negative-acting GC-rich element located between two positive-acting serum responsive factor-binding elements. J Biol Chem. 1997;272: 6332-6340.
46. Zilberman A, Dave V, Miano J, Olson EN, Periasamy M. Evolutionarily conserved promotor region containing CArG*-like element is crucial for smooth muscle myosin heavy chain gene expression. Circ Res. 1998;82: 566-575.
47. Madsen CS, Regan CP, Hungerford JE, White SL, Manabe I, Owens GK. Smooth muscle-specific expression of the smooth muscle myosin heavy chain in transgenic mice requires 5′-flanking and first intronic DNA sequence. Circ Res. 1998;82:908-917.
48. Benditt EP, Benditt JM. Evidence for a monoclonal origin of human atherosclerotic plaques. Proc Natl Acad Sci U S A. 1973;70: 1753-1756.
49. Murry CE, Gipaya CT, Bartosek T, Benditt EP, Schwartz SM. Monoclonality of smooth muscle cells in human atherosclerosis. Am J Pathol. 1997;151:697-706.
50. Schwartz SM, deBlois D, O'Brien ERM. The intima: soil for atherosclerosis and restenosis. Circ Res. 1995;77:445-465.
51. Gordon D, Reidy MA, Benditt EP, Schwartz SM. Cell proliferation in human coronary arteries. Proc Natl Acad Sci U S A. 1990;87: 4600-4604.
52. Kockx MM, DeMeyer GRY, Buyssens N, Knappen MWM, Herman AG. Cell composition, replication, and apoptosis in atherosclerotic plaque after 6 months of cholesterol withdrawal. Circ Res. 1998;83: 378-387.