The role of plasminogen, plasminogen activators, and matrix metalloproteinases in primate arterial smooth muscle cell migration

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 16, Issue 11, 1996, Pages 1373-1382

  Kenagy, R D ^a   Vergel, S ^a   Mattsson, E ^a   Bendeck, M ^b   Reidy, M A ^b   Clowes, A W ^a  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

Author keywords

matrix metalloproteinases; plasminogen; smooth muscle cell migration; tissue type plasminogen activator; urokinase

Indexed keywords

METALLOPROTEINASE; PLASMINOGEN; PLASMINOGEN ACTIVATOR; TISSUE PLASMINOGEN ACTIVATOR; UROKINASE;

ADOLESCENT; ANIMAL MODEL; ANIMAL TISSUE; AORTA; ARTICLE; ATHEROSCLEROSIS; BABOON; BLOOD VESSEL INJURY; CELL MIGRATION; EXPLANT; EXTRACELLULAR MATRIX; MALE; NONHUMAN; PRIORITY JOURNAL; VASCULAR SMOOTH MUSCLE;

EID: 0029911386     PISSN: 10795642     EISSN: None     Source Type: Journal    
DOI: 10.1161/01.ATV.16.11.1373     Document Type: Article

References (77)

1. Schwartz SM, Heimark RL, Majesky MW. Developmental mechanisms underlying pathology of arteries. Physiol Rev. 1990;70: 1177-1210.
2. Ross R. The pathogenesis of atherosclerosis: a perspective for the 1990s. Nature. 1993;362:801-809.
3. Ossowski L. Invasion of connective tissue by human carcinoma cell lines: requirement for urokinase, urokinase receptor, and interstitial collagenase. Cancer Res. 1992;52:6754-6760.
4. Stetler-Stevenson WG, Liotta LA, Kleiner DE Jr. Extracellular matrix 6: role of matrix metalloproteinases in tumor invasion and metastasis. FASEB J. 1993;7:1434-1441.
5. Kirchheimer JC, Remold HG. Endogenous receptor-bound urokinase mediates tissue invasion of human monocytes. J Immunol. 1989; 143:2634-2639.
6. Librach CL, Werb Z, Fitzgerald ML, Chiu K, Corwin NM, Esteves RA, Grobelny D, Galardy R, Damsky CH, Fisher SJ. 92-kD Type IV collagenase mediates invasion of human cytotrophoblasts. J Cell Biol. 1991;113:437-449.
7. Mignatti P, Tsuboi R, Robbins E, Rifkin DB. In vitro angiogenesis on the human amniotic membrane: requirement for basic fibroblast growth factor-induced proteinases. J Cell Biol. 1989;108:671-682.
8. Matrisian LM, Gaire M, Rodgers WH, Osteen KG. Metalloproteinase expression and hormonal regulation during tissue remodeling in the cycling human endometrium. Contrib Nephrol. 1994;107:94-100.
9. Talhouk RS, Bissell MJ, Werb Z. Coordinated expression of extracellular matrix-degrading proteinases and their inhibitors regulates mammary epithelial function during involution. J Cell Biol. 1992; 118:1271-1282.
10. Khokha R, Waterhouse P. The role of tissue inhibitor of metalloproteinase-1 in specific aspects of cancer progression and reproduction. J Neurooncol. 1994;18:123-127.
11. DeClerck YA, Yean T-D, Chan D, Shimada H, Langley KE. Inhibition of tumor invasion of smooth muscle cell layers by recombinant human metalloproteinase inhibitor. Cancer Res. 1991;51:2151-2157.
12. Kirchheimer JC, Binder BR, Remold HG. Matrix-bound plasminogen activator inhibitor type 1 inhibits the invasion of human monocytes into interstitial tissue. J Immunol. 1990;145:1518-1522.
13. Clowes AW, Clowes MM, Au YPT, Reidy MA, Belin D. Smooth muscle cells express urokinase during mitogenesis and tissue-type plasminogen activator during migration in injured rat carotid artery. Circ Res. 1990;67:61-67.
14. Zempo N, Kenagy RD, Au YPT, Bendeck M, Clowes MM, Reidy MA, Clowes AW. Matrix metalloproteinases of vascular wall cells are increased in balloon-injured rat carotid artery. J Vase Surg. 1994; 20:209-217.
15. Jackson CL, Raines EW, Ross R, Reidy MA. Role of endogenous platelet-derived growth factor in arterial smooth muscle cell migration after balloon catheter injury. Arterioscler Thromb. 1993;13: 1218-1226.
16. Bendeck MP, Zempo N, Clowes AW, Galardy RE, Reidy MA. Smooth muscle cell migration and matrix metalloproteinase expression after arterial injury in the rat. Circ Res. 1994;75:539-545.
17. Zempo N, Koyama N, Kenagy RD, Lea H L, Clowes AW. Regulation of vascular smooth muscle cell migration and proliferation in vitro and in injured rat arteries by a synthetic matrix metalloproteinase inhibitor. Arterioscler Thromb Vasc Biol. 1996;16:28-33.
18. Carmeliet P, Stassen JM, De Mol M, Declercq C, Bouche A, Collen D. Arterial neointima formation after trauma in mice with inactivation of the t-PA, u-PA or PAI-1 genes. Fibrinolysis. 1994;8:280a. Abstract.
19. MERCATOR Study Group. Does the new angiotensin converting enzyme inhibitor cilazapril prevent restenosis after percutaneous transluminal coronary angioplasty? Results of the MERCATOR study: a multicenter, randomized, double-blind placebo-controlled trial. Circulation. 1992;86:100-110.
20. Pepine CJ. Angiotensin converting enzyme inhibition and coronary artery disease. J Hypertens. 1994;12:565-571.
21. Powell JS, Clozel JP, Muller RKM, Kuhn H, Hefti F, Hosang M, Baumgartner HR. Inhibitors of angiotensin-converting enzyme prevent myointimal proliferation after vascular injury. Science. 1989; 245:186-188.
22. Hanson SR, Powell JS, Dodson T, Lumsden A, Kelly AB, Anderson JS, Clowes AW, Harker LA. Effects of angiotensin converting enzyme inhibition with cilazapril on intimal hyperplasia in injured arteries and vascular grafts in the baboon. Hypertension. 1991;18(suppl II):II-70-II-76.
23. Clowes AW, Clowes MM. Kinetics of cellular proliferation after arterial injury, II: inhibition of smooth muscle growth by heparin. Lab Invest. 1985;52:611-616.
24. Clowes AW, Clowes MM, Kirkman TR, Jackson CL, Au YPT, Kenagy R. Heparin inhibits the expression of tissue-type plasminogen activator by smooth muscle cells in injured rat carotid artery. Cric Res. 1992;70:1128-1136.
25. Geary RL, Koyama N, Wang TW, Vergel S, Clowes AW. Failure of heparin to inhibit intimai hyperplasia in injured baboon arteries: the role of heparin-sensitive and insensitive pathways in the stimulation of smooth muscle cell migration and proliferation. Circulation. 1995; 91:2972-2981.
26. 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.
27. Schneiderman J, Sawdey MS, Keeton MR, Bordin GM, Bernstein EF, Dilley RB, Loskutoff DJ. Increased type 1 plasminogen activator inhibitor gene expression in atherosclerotic human arteries. Proc Natl Acad Sci U S A. 1992;89:6998-7002.
28. Irizarry E, Newman KM, Gandhi RH, Nackman GB, Halpern V, Wishner S, Scholes JV, Tilson MD. Demonstration of interstitial collagenase in abdominal aortic aneurysm disease. J Surg Res. 1993; 54:571-574.
29. Vine N, Powell JT. Metalloproteinases in degenerative aortic disease. Clin Sci. 1991;81:233-239.
30. Brown DL, Hibbs MS, Kearney 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.
31. Henney AM, Wakeley PR, Davies MJ, Foster K, Hembry R, Murphy G, Humphries S. Localization of stromelysin gene expression in atherosclerotic plaques by in situ hybridization. Proc Natl Acad Sci U S A. 1991;88:8154-8158.
32. Davies B, Brown PD, East N, Crimmin MJ, Balkwill FR. A synthetic matrix metalloproteinase inhibitor decreases tumor burden and prolongs survival of mice bearing human ovarian carcinoma xenografts. Cancer Res. 1993;53:2087-2091.
33. McMurray HF, Parrott DP, Bowyer DE. A standardised method of culturing aortic explants, suitable for the study of factors affecting the phenotypic modulation, migration and proliferation of aortic smooth muscle cells. Atherosclerosis. 1991;86:227-237.
34. Clowes AW, Reidy MA, Clowes MM. Kinetics of cellular proliferation after arterial injury, I: smooth muscle growth in the absence of endothelium. Lab Invest. 1983;49:327-333.
35. Grondahl-Hansen J, Agerlin N, Munkholm-Larsen P, Bach F, Nielsen LS, Dombernowsky P, Dano K. Sensitive and specific enzyme-linked immunosorbert assay for urokinase-type plasminogen activator and its application to plasma from patients with breast cancer. J Lab Clin Med. 1988;111:42-51.
36. Stephens R, Leung K-C, Pollanen J, Salonen E-M, Vaheri A. Microplate immunocapture assay for plasminogen activators and their specific inhibitors. J Immunol Methods. 1987;105:245-251.
37. Dean DD, Schwartz Z, Muniz OE, Gomez R, Swain LD, Howell DS, Boyan BD. Matrix vesicles are enriched in metalloproteinases that degrade proteoglycans. Calcif Tissue Int. 1992;50:342-349.
38. Kenagy RD, Nikkari ST, Welgus HG, Clowes AW. Heparin inhibits the induction of three matrix metalloproteinases (stromelysin, 92-kD gelatinase, and collagenase) in primate arterial smooth muscle cells. J Clin Invest. 1994;93:1987-1993.
39. r 72,000 type IV collagenase and interstitial collagenase in human tumorigenic cell lines. Cancer Res. 1990;50:6184-6191.
40. Overall CM, Wrana JL, Sodek J. Independent regulation of collagenase, 72-kDa progelatinase, and metalloproteinase inhibitor expression in human fibroblasts by transforming growth factor-B. J Biol Chem. 1989;264:1860-1869.
41. Hipps DS, Hembry RM, Docherty AJP, Reynolds JJ, Murphy G. Purification and characterisation of human 72-kDa gelatinase (type IV collagenase): use of immunolocalisation to demonstrate the noncoordinate regulation of the 72-kDa and 95-kDa gelatinases by human fibroblasts. Biol Chem Hoppe Seyler. 1991;372:287-296.
42. Ossowski L, Quigley JP, Reich E. Plasminogen, a necessary factor for cell migration in vitro. In: Proteases and Biological Control. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory; 1975:1-901.
43. Clowes AW, Schwartz SM. Significance of quiescent smooth muscle migration in the injured rat carotid artery. Circ Res. 1985;56:139-145.
44. Majack RA, Clowes AW. Inhibition of vascular smooth muscle cell migration by heparin-like glycosaminoglycans. J Cell Physiol. 1984; 118:253-256.
45. Fingerle J, Faulmüller A, Müller G, Bowen-Pope DF, Clowes MM, Reidy MA, Clowes AW. Pituitary factors in blood plasma are necessary for smooth muscle cell proliferation in response to injury in vivo. Arterioscler Thromb. 1992;12:1488-1495.
46. Kenagy RD, Hart C, Clowes AW. Role for growth factors and proteinases in the migration of smooth muscle cells through native extracellular matrix in vitro. FASEB J. 1993;7:A637. Abstract.
47. Jackson CL, Reidy MA. Basic fibroblast growth factor: its role in the control of smooth muscle cell migration. Am J Pathol. 1993;143: 1024-1031.
48. Fibbi G, Ziehe M, Morbidelli L, Magnelli L, DelRosso M. Interaction of urokinase with specific receptors stimulates mobilization of bovine adrenal capillary endothelial cells. Exp Cell Res. 1988;179:385-395.
49. Odekon LE, Sato Y, Rifkin DB. Urokinase-type plasminogen activator mediates basic fibroblast growth factor-induced bovine endothelial cell migration independent of its proteolytic activity. J Cell Physiol. 1992;150:258-263.
50. Inyang AL, Tobelem G. Tissue-plasminogen activator stimulates endothelial cell migration in wound assays. Biochem Biophys Res Commun. 1990;171:1326-1332.
51. De Petro G, Copeta A, Barlati S. Urokinase-type and tissue-type plasminogen activators as growth factors of human fibroblasts. Exp Cell Res. 1994;213:286-294.
52. Kirchheimer JC, Wojta J, Hienert G, Christ G, Heger ME, Pfluger H, Binder BR. Effect of urokinase on the proliferation of primary cultures of human prostatic cells. Thromb Res. 1987;48:291-298.
53. He C, Rebibou J, Peraldi M, Meulders Q, Rondeau E. Growth factor-like effect of urokinase type plasminogen activator in human renal cells. Biochem Biophys Res Commun. 1991;176:1408-1416.
54. Herbert JM, Lamarche I, Prabonnaud V, Dol F. Tissue-type plasminogen activator is a potent mitogen for human aortic smooth muscle Cells. J Biol Chem. 1994;269:3076-3080.
55. Gold LI, Schwimmer R, Quigley JP. Human plasma fibronectin as a substrate for human urokinase. Biochem J. 1989;262:529-534.
56. Reith A, Rucklidge GJ. Invasion of brain tissue by primary glioma: evidence for the involvement of urokinase-type plasminogen activator as an activator of type IV collagenase. Biochem Biophys Res Commun. 1992;186:348-354.
57. Keski-Oja J, Lohi J, Tuuttila A, Tryggvason K, Vartio T. Proteolytic processing of the 72,000-Da type IV collagenase by urokinase plasminogen activator. Exp Cell Res. 1992;202:471-476.
58. Smith EB, Crosbie L. Does lipoprotein(a) (Lp(a)) compete with plasminogen in human atherosclerotic lesions and thrombi? Atherosclerosis. 1991;89:127-136.
59. Ossowski L. In vivo invasion of modified chorioallantoic membrane by tumor cells: the role of cell surface-bound urokinase. J Cell Biol. 1988;107:2437-2445.
60. Ellis V, Pyke C, Eriksen J, Solberg H, Dano K. The urokinase receptor: involvement in cell surface proteolysis and cancer invasion. Ann N Y Acad Sci. 1992;667:13-31.
61. Blasi F, Conese M, Moller LB, Pedersen N, Cavallaro U, Cubellis MV, Fazioli F, Hernandez-Marrero L, Limongi P, Munoz-Canoves P, et al. The urokinase receptor: structure, regulation and inhibitor-mediated internalization. Fibrinolysis. 1994;8(suppl 1):182-188.
62. Beebe DP, Miles LA, Plow EF. A linear amino acid sequence involved in the interaction of t-PA with its endothelial cell receptor. Blood. 1989;74:2034-2037.
63. Felez J, Chanquia CJ, Levin EG, Miles LA, Plow EF. Binding of tissue plasminogen activator to human monocytes and monocytoid cells. Blood. 1991;78:2318-2327.
64. Plow EF, Miles LA. Plasminogen receptors in the mediation of pericellular proteolysis. Cell Differ Dev. 1990;32:293-298.
65. Manchanda N, Schwartz BS. Single chain urokinase: augmentation of enzymatic activity upon binding to monocytes. J Biol Chem. 1991;266:14580-14584.
66. Reuning U, Bang NU. Regulation of the urokinase-type plasminogen activator receptor on vascular smooth muscle cells is under the control of thrombin and other mitogens. Arterioscler Thromb. 1992;12: 1161-1170.
67. Okada SS, Tomaszewski JE, Barnathan ES. Migrating vascular smooth muscle cells polarize cell surface urokinase receptors after injury in vitro. Exp Cell Res. 1995;217:180-187.
68. Southgate KM, Davies M, Booth RFG, Newby AC. Involvement of extracellular-matrix-degrading metalloproteinases in rabbit aortic smooth-muscle cell proliferation. Biochem J. 1992; 288:93-99.
69. Gonias SL. a2-Macroglobulin: a protein at the interface of fibrinolysis and cellular growth regulation. Exp Hematol. 1992;20: 302-311.
70. Srinivas S, Sironmani TA, Shanmugam G. Dimethyl sulfoxide inhibits the expression of early growth-response genes and arrests fibroblasts at quiescence. Exp Cell Res. 1991;196:279-286.
71. Pauly RR, Passaniti A, Bilato C, Monticone R, Cheng L, Papadopoulos N, Gluzband YA, Smith L, Weinstein C, Lakatta EG, Crow MT. Migration of cultured vascular smooth muscle cells through a basement membrane barrier requires type IV collagenase activity and is inhibited by cellular differentiation. Circ Res. 1994;75:41-54.
72. Nagase H, Ogata Y, Suzuki K, Enghild JJ, Salvesen G. Substrate specificities and activation mechanisms of matrix metalloproteinases. Biochem Soc Trans. 1991;19:715-718.
73. Nagase H, Enghild JJ, Suzuki K, Salveson G. Stepwise activation mechanisms of the precursor of matrix metallo proteinase 3 (stromelysin) by proteinases and (4-aminophenyl)mercuric acetate. Biochemistry. 1990;29:5783-5789.
74. Murphy G, Atkinson S, Ward R, Gavrilovic J, Reynolds JJ. The role of plasminogen activators in the regulation of connective tissue metalloproteinases. Ann N Y Acad Sci. 1992;667:1-12.
75. Wong AP, Cortez SL, Baricos WH. Role of plasmin and gelatinase in extracellular matrix degradation by cultured rat mesangial cells. Am J Physiol Renal (Fluid Electrolyte Physiol). 1992;263: F1112-F1118.
76. Sato H, Takino T, Okada Y, Cao J, Shinagawa A, Yamamoto E, Seiki M. A matrix metalloproteinase expressed on the surface of invasive tumour cells. Nature. 1994;370:61-65.
77. Desrochers PE, Jeffrey JJ, Weiss SJ. Interstitial collagenase (matrix metalloproteinase-1) expresses serpinase activity. J Clin Invest. 1991; 87:2258-2265.