Smooth Muscle Cell Expression of Extracellular Matrix Genes After Arterial Injury

Overview

Journal Am J Pathol

Publisher Elsevier

Specialty Pathology

Date 1994 Jun 1

PMID 8203472

Citations 47

Authors

S T Nikkari

H T Jarvelainen

T N Wight

M Ferguson

A W Clowes

Affiliations

Soon will be listed here.

Abstract

Accumulation of extracellular matrix (ECM) after arterial injury is an important event in the development of intimal thickening and is modulated by heparin. To investigate the regulation of matrix protein expression, we have analyzed messenger RNA levels by Northern blotting for various ECM proteins in the rat carotid artery balloon injury model. RNA was extracted from normal arteries and from intima-medial preparations at 2 days, 1 week, 2 weeks, and 4 weeks after balloon injury of arteries in animals receiving either saline or heparin infusion. Transcripts for the heparan sulfate proteoglycans perlecan, syndecan, and ryudocan; the chondroitin sulfate proteoglycan versican; the dermatan sulfate proteoglycan biglycan; type I procollagen; and tropoelastin all were increased on Northern blots beginning at 1 week after injury. By in situ hybridization, the transcripts for elastin nd biglycan were primarily localized to smooth muscle cells in the intima and were diminished by heparin in proportion to the decrease in intimal mass. Other matrix genes (perlecan, ryudocan) were expressed in the intima and media and were not affected by heparin. The results support the conclusion that ECM gene expression is a relatively late event in the response of the carotid artery, and that some of the genes are expressed only in the intima whereas others are expressed in both the intima and media.

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References

Schonherr E, Jarvelainen H, Sandell L, Wight T . Effects of platelet-derived growth factor and transforming growth factor-beta 1 on the synthesis of a large versican-like chondroitin sulfate proteoglycan by arterial smooth muscle cells. J Biol Chem. 1991; 266(26):17640-7. View

Au Y, Montgomery K, Clowes A . Heparin inhibits collagenase gene expression mediated by phorbol ester-responsive element in primate arterial smooth muscle cells. Circ Res. 1992; 70(5):1062-9. DOI: 10.1161/01.res.70.5.1062. View

Miano J, Vlasic N, Tota R, Stemerman M . Smooth muscle cell immediate-early gene and growth factor activation follows vascular injury. A putative in vivo mechanism for autocrine growth. Arterioscler Thromb. 1993; 13(2):211-9. DOI: 10.1161/01.atv.13.2.211. View

Mutoh S, Clowes M, Clowes A . Heparin increased cell membrane-associated heparan sulfate proteoglycan in balloon-injured rat carotid artery. J Vasc Res. 1993; 30(3):161-8. DOI: 10.1159/000158991. View

Saksela O, Moscatelli D, Sommer A, Rifkin D . Endothelial cell-derived heparan sulfate binds basic fibroblast growth factor and protects it from proteolytic degradation. J Cell Biol. 1988; 107(2):743-51. PMC: 2115214. DOI: 10.1083/jcb.107.2.743. View

Majesky M, Giachelli C, Reidy M, Schwartz S . Rat carotid neointimal smooth muscle cells reexpress a developmentally regulated mRNA phenotype during repair of arterial injury. Circ Res. 1992; 71(4):759-68. DOI: 10.1161/01.res.71.4.759. View

Botney M, Kaiser L, Cooper J, Mecham R, Parghi D, Roby J . Extracellular matrix protein gene expression in atherosclerotic hypertensive pulmonary arteries. Am J Pathol. 1992; 140(2):357-64. PMC: 1886436. View

Castellot Jr J, Wright T, Karnovsky M . Regulation of vascular smooth muscle cell growth by heparin and heparan sulfates. Semin Thromb Hemost. 1987; 13(4):489-503. DOI: 10.1055/s-2007-1003525. View

Gavriel P, Kagan H . Inhibition by heparin of the oxidation of lysine in collagen by lysyl oxidase. Biochemistry. 1988; 27(8):2811-5. DOI: 10.1021/bi00408a022. View

10.

Wilcox J, Smith K, Williams L, Schwartz S, Gordon D . Platelet-derived growth factor mRNA detection in human atherosclerotic plaques by in situ hybridization. J Clin Invest. 1988; 82(3):1134-43. PMC: 303629. DOI: 10.1172/JCI113671. View

11.

Lark M, Yeo T, Mar H, Lara S, Hellstrom I, Hellstrom K . Arterial chondroitin sulfate proteoglycan: localization with a monoclonal antibody. J Histochem Cytochem. 1988; 36(10):1211-21. DOI: 10.1177/36.10.3047228. View

12.

Fisher L, Termine J, Young M . Deduced protein sequence of bone small proteoglycan I (biglycan) shows homology with proteoglycan II (decorin) and several nonconnective tissue proteins in a variety of species. J Biol Chem. 1989; 264(8):4571-6. View

13.

Flaumenhaft R, Moscatelli D, Rifkin D . Heparin and heparan sulfate increase the radius of diffusion and action of basic fibroblast growth factor. J Cell Biol. 1990; 111(4):1651-9. PMC: 2116237. DOI: 10.1083/jcb.111.4.1651. View

14.

Clowes A, Clowes M, Gown A, Wight T . Localization of proteoheparan sulfate in rat aorta. Histochemistry. 1984; 80(4):379-84. DOI: 10.1007/BF00495421. View

15.

Murdoch A, Dodge G, Cohen I, Tuan R, Iozzo R . Primary structure of the human heparan sulfate proteoglycan from basement membrane (HSPG2/perlecan). A chimeric molecule with multiple domains homologous to the low density lipoprotein receptor, laminin, neural cell adhesion molecules, and epidermal.... J Biol Chem. 1992; 267(12):8544-57. View

16.

Kojima T, Shworak N, Rosenberg R . Molecular cloning and expression of two distinct cDNA-encoding heparan sulfate proteoglycan core proteins from a rat endothelial cell line. J Biol Chem. 1992; 267(7):4870-7. View

17.

Asundi V, STAHL R, Teichman L, Chernousov M, Cowan K, Carey D . Regulated expression of syndecan in vascular smooth muscle cells and cloning of rat syndecan core protein cDNA. J Biol Chem. 1992; 267(22):15729-36. View

18.

Haudenschild C . Pathobiology of restenosis after angioplasty. Am J Med. 1993; 94(4A):40S-44S. View

19.

Clowes A, Reidy M, Clowes M . Mechanisms of stenosis after arterial injury. Lab Invest. 1983; 49(2):208-15. View

20.

Tso J, Sun X, Kao T, Reece K, Wu R . Isolation and characterization of rat and human glyceraldehyde-3-phosphate dehydrogenase cDNAs: genomic complexity and molecular evolution of the gene. Nucleic Acids Res. 1985; 13(7):2485-502. PMC: 341170. DOI: 10.1093/nar/13.7.2485. View