Arterial enlargement in response to high flow requires early expression of matrix metalloproteinases to degrade extracellular matrix

Experimental and Molecular Pathology

Volumn 73, Issue 2, 2002, Pages 142-153

  Sho, Eiketsu ^a,b   Sho, Mien ^a,b   Singh, Tej M ^a   Nanjo, Hiroshi ^b   Komatsu, Masayo ^b   Xu, Chengpei ^a   Masuda, Hirotake ^b   Zarins, Christopher K ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b AKITA UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

Blood flow; Egr 1; Endothelial cell; Extracellular matrix; Matrix metalloproteinase; Smooth muscle cell; TGF 1; Wall shear stress

Indexed keywords

CANCER GROWTH FACTOR BETA1; GELATINASE A; GELATINASE B; INTERSTITIAL COLLAGENASE; MATRIX METALLOPROTEINASE; MESSENGER RNA; TISSUE INHIBITOR OF METALLOPROTEINASE 2; TRANSCRIPTION FACTOR EGR 1; TRANSFORMING GROWTH FACTOR; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTERIOVENOUS FISTULA; ARTICLE; BLOOD FLOW; CAROTID ARTERY; CELL PROLIFERATION; CONTROLLED STUDY; ENDOTHELIUM CELL; EXTRACELLULAR MATRIX; JAPAN; JUGULAR VEIN; MALE; MOLECULAR BIOLOGY; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; RABBIT; REGULATORY MECHANISM; SHEAR STRESS; SMOOTH MUSCLE FIBER;

ORYCTOLAGUS CUNICULUS;

EID: 0036385662     PISSN: 00144800     EISSN: None     Source Type: Journal    
DOI: 10.1006/exmp.2002.2457     Document Type: Article

References (45)

1. Kamiya, A., and Togawa, T. (1980). Adaptive regulation of wall shear stress to flow change in the canine carotid artery. Am. J. Physiol. 239, H14-H21.
2. Zarins, C. K., Zatina, M. A., Giddens, D. P., Ku, D. N., and Glagoy, S. (1987). Shear stress regulation of artery lumen diameter in experimental atherogenesis. J. Vasc. Surg. 5, 413-420.
3. Masuda, H., Bassiouny, H., Glagoy, S., and Zarins, C. K. (1989). Artery wall restructuring in response to increased flow. Surg. Forum 45, 285-286.
4. Tohda, K., Masuda, H., Kawamura, K., and Shozawa, T. (1992). Difference in dilation between endothelium preserved and desquamated segments in flow loaded rat common carotid artery. Arterioscler. Thromb. 12, 519-528.
5. Masuda, H., Kawamura, K., Sugiyama, T., and Kamiya, A. (1993). Effects of endothelial denudation in flow-induced arterial dilation. Frontiers Med. Biol. Eng. 5, 55-62.
6. Langille, B. L., and O'Donnell, F. (1986). Reductions in arterial diameter produced by chronic decreases in blood flow are endothelium-dependent. Science 231, 405-407.
7. Masuda, H., Kawamura, K., Tohda, K., Shozawa, T., Sageshima, M., and Kamiya, A. (1989). Increase in endothelial cell density before artery enlargement in flow-loaded canine carotid artery. Arteriosclerosis 9, 812-823.
8. Masuda, H., Zhuang, Y.-J., Singh, T. M., Kawamura, K., Murakami, M., Zarins, C. K., and Glagov, S. (1999). Adaptive remodeling of internal elastic lamina and endothelial lining during flow induced arterial enlargement. Arterioscler. Thromb. Vasc. Biol. 19, 2298-2307.
9. Murphy, G., Stanton, H., Cowell, S., Butler, G., Knauper, V., Atkinson, S., and Gavrilovic, J. (1999). Mechanisms for pro matrix metalloproteinase activation. APMIS 107, 38-44.
10. Birkedal-Hansen, H., Moor, W. G. I., Bodden, M. K., Windsor, L. J., Birkedal-Hanse, B., De Carlo, A., and Engler, J. A. (1993). Matrix metalloproteinases: A review. Crit. Rev. Oral Biol. Med. 4, 197-250.
11. Haas, T. L., and Madri, J. A. (1999). Extracellular matrix-driven matrix metalloproteinase production in endothelial cells. Trends Cardiovasc. Med. 9, 70-77.
12. Koyama, N., Koshikawa, T., Morisaki, N., Saito, Y., and Yoshida, S. (1990). Bifunctional effects of transforming growth factor-β on migration of cultured rat aortic smooth muscle cell. Biochem. Biophys. Res. Commun. 169, 725-729.
13. Cucina, A., Srerpetti, A. V., Borrelli, V., Pagliei, S., Cavallaro, A., and D'Angelo, L. S. (1998). Shear stress induces transforming growth factor-beta 1 release by arterial endothelial cells. Surgery 123, 212-217.
14. Ohno, M., Cooke, J. P., Dzau, V. J., and Gibbons, G. H. (1995). Fluid shear stress induces endothelial transforming growth factor beta-1 transcription and production: Modulation by potassium channel blockade. J. Clin. Invest. 95, 1363-1369.
15. O'Callaghan, C. J., and Williams, B. (2000). Mechanical strain-induced extracellular matrix production by human vascular smooth muscle cells - Role of TGF-β1. Hypertension 36, 319-324.
16. Overall, C. M., Wrana, J. L., and Sodek, J. (1989). Independent regulation of collagenase, 72 kD progelatinase and metalloendoproteinase inhibitor expression in human fibroblasts by transforming growth factor-[beta]. J. Biol. Chem. 264, 1860-1869.
17. Marti, H. P., Lee, L., Kashgarian, M., and Lovett, D. H. (1994). Transforming growth factor-[beta]1 stimulates glomerular mesangial cell synthesis of the 72-kD type IV collagenase. Am. J. Pathol. 144, 82-94.
18. Salo, T., Lyons, J. G., Rahemtulla, F., Birkedal-Hansen, H., and Larjava, H. (1991). Transforming growth factor-[beta] up-regulates type IV collagenase expression in cultured human keratinocytes. J. Biol. Chem. 266, 11436-11441.
19. Xie, B., Bucana, C. D., and Fidler, I. J. (1994). Density-dependent induction of 92-kD type IV collagenase activity in cultures of A431 human epidermoid carcinoma cells. Am. J. Pathol. 144, 1058-1067.
20. Gashler, A., and Sukhatme, V. P. (1995). Early growth response protein 1 (Egr-1): Prototype of a zinc-finger family of transcription factors. Prog. Nucleic Acid Res. Mol. Biol. 50, 191-224.
21. Khachigian, L. M., and Collins, T. (1997). Inducible expression of Egr-1-dependent genes: A paradigm of transcriptional activation in vascular endothelium. Circ. Res. 81, 457-461.
22. Khachigian, L. M., Lindner, V., Williams, A. J., and Collins, T. (1996). Egr-1-induced endothelial gene expression: A common theme in vascular injury. Science 271, 1427-1431.
23. Haas, T. L., Stitelman, D., Davis, S. J., Apte, S. S., and Madri, J. A. (1999). Egr-1 mediates extracellular matrix-driven transcription of membrane type 1 matrix metalloproteinase in endothelium. J. Biol. Chem. 274, 22679-22685.
24. Zhuang, Y.-J., Singh, T. M., Zarins, C. K., and Masuda, H. (1998). Sequential increases and decreases in blood flow stimulate progressive Intimal thickening. Eur. J. Vasc. Endovasc. Surg. 16(4), 301-310.
25. Tronc, F., Mallat, Z., Lehoux, S., Wassef, M., Esposito, B., and Tedgui, A. (2000). Role of matrix metalloproteinases in blood flow-induced arterial enlargement - Interaction with NO. Arterioscler. Thromb. Vasc. Biol. 20, e120-e126.
26. Jackson, C. J., and Nguyen, M. (1997). Human microvascular endothelial cells differ from macrovascular endothelial cells in their expression of matrix metalloproteinases. Int. J. Biochem. Cell. Biol. 29, 1167-1177.
27. Bendeck, M. P., Zempo, N., Clowes, A. W., Galardy, R. E., and Reidy, M. A. (1994). Smooth muscle cell migration and matrix metalloproteinase expression after arterial injury in the rat. Circ. Res. 75, 539-545.
28. Brown, L. C., Messick, F. C., Kok, M. P., Hamilton, I. G., and Girard, P. R. (1995). Fluid flow stimulates metalloproteinase production and deposition into the extracellular matrix of endothelial cells. FASEB J. 9, A617.
29. Haas, T. L., Davis, S. J., and Madri, J. A. (1998). Three-dimensional type I collagen lattices induce coordinate expression of matrix metalloproteinases MT1-MMP and MMP-2 in microvascular endothelial cells. J. Biol. Chem. 273, 3604-3610.
30. Tokuraku, M., Sato, H., Murakami, S., Okada, Y., Watanabe, Y., and Seiki, M. (1995). Activation of the precursor of gelatinase A72 kDa type IV collagenase/MMP-2 in lung carcinomas correlates with the expression of membrane-type matrix metalloproteinase (MT-MMP) and with lymph node metastasis. Int. J. Cancer 64, 355-359.
31. Haas, T. L., Davis, S. J., and Madri, J. A. (1998). Three-dimensional type I collagen lattices induce coordinate expression of matrix metalloproteinases MT1-MMP and MMP-2 in microvascular endothelial cells. J. Biol. Chem. 273, 3604-3610.
32. Nguyen, M., Arkell, J., and Jackson, C. J. (2000). Three-dimensional collagen matrices induce delayed but sustained activation of gelatinase A in human endothelial cells via MT1-MMP. Int. J. Biochem. Cell. Biol. 32, 621-631.
33. Haas, T. L., and Madri, J. A. (1999). Extracellular matrix-driven matrix metalloproteinase production in endothelial cell: Implications for angiogenesis. Trends Cardiovasc. Med. 9, 70-77.
34. Silverman, E. S., and Collins, T. (1999). Pathways of Egr-1-mediated gene transcription on vascular biology. Am. J. Pathol. 154, 665-670.
35. Haas, T. L., Stitelman, D., Davis, S. J., Apte, S. S., and Madri, J. A. (1999). Egr-1 mediates extracellular matrix-driven transcription of membrane type 1 matrix metalloproteinase in endothelium. J. Biol. Chem. 274, 22679-22685.
36. Pepper, M. S., Belin, D., Montesano, R., Orci, L., and Vassalli, J. D. (1990). Transforming growth factor-β1 modulates basic fibroblast growth factor-induced proteolytic and angiogenic properties of endothelial cells in vitro. J. Cell. Biol. 111, 743-755.
37. Pepper, M. S., Vassalli, J. D., Orci, L., and Montesano, R. (1993). Biphasic effect of transforming growth factor-β1 on in vitro angiogenesis. Exp. Cell Res. 204, 356-363.
38. Ohno, M., Cooke, J. P., Dzau, V. J., and Gibbons, G. H. (1995). Fluid shear stress induces endothelial transforming growth factor beta-1 transcription and production. J. Clin. Invest. 99, 1363-1369.
39. Cucina, A., Sterpetti, A. V., Borrelli, V., Pagliei, S., Carvallaro, A., and D'Angelo, L. S. (1998). Shear stress induces transforming growth factor-beta release by arterial endothelial cells. Surgery 123, 212-217.
40. Roberts, A. B., Hline, U. I., Flanders, K. C., and Sporn, M. B. (1990). Transforming growth factor-b: Major role in regulation of extracellular matrix. Ann. N.Y. Acad. Sci. 580, 225-230.
41. Kerr, L. D., Miller, D. B., and Matrisian, L. M. (1990). TGF-β1 inhibition of transin/stromelysin gene expression is mediated through a Fos binding sequence. Cell 61, 267-278.
42. Matrisian, L. M., Ganser, G. L., Kerr, L. D., Pelton, R. W., and Wood, L. D. (1992). Negative regulation of gene expression by TGF-β. Mol. Reprod. Dev. 32, 111-120.
43. Mauviel, A., Chen, Y. Q., Dong, W., Evans, C. H., and Uitto, J. (1993). Transcriptional interactions of transforming growth factor-β with proinflammatory cytokines. Curr. Biol. 3, 822-831.
44. Overall, C. M., Wrana, J. L., and Sodek, J. (1991). Transcriptional and post-transcriptional regulation of 72-Kda gelatinase/type IV collagenase by transforming growth factor-β1 in human fibroblasts. Comparisons with collagenase and tissue inhibitor of matrix metalloproteinase gene expression. J. Biol. Chem. 266, 14064-14071.
45. Puyraimond, A., Weitzman, J. B., Babiole, E., and Menashi, S. (1999). Examining the relationship between the gelatinolytic balance and the invasive capacity of endothelial cells. J. Cell Sci. 112, 1283-1290.