Involvement of MMPs in the outward remodeling of collateral mesenteric arteries

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 293, Issue 4, 2007, Pages

  Haas, Tara L ^a   Doyle, Jennifer L ^a   Distasi, Matthew R ^b   Norton, Laura E ^b   Sheridan, Kevin M ^b   Unthank, Joseph L ^b  

^a YORK UNIVERSITY   (Canada)

^b INDIANA UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Collateral artery; Matrix metalloproteinase; Shear stress

Indexed keywords

DOXYCYCLINE; EARLY GROWTH RESPONSE FACTOR 1; GELATIN; GELATINASE A; GELATINASE B; MATRIX METALLOPROTEINASE; MATRIX METALLOPROTEINASE 14; MATRIX METALLOPROTEINASE INHIBITOR; PROTEIN C JUN;

ADAPTATION; ANIMAL TISSUE; ARTERY RESISTANCE; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; ENDOTHELIUM CELL; EXTRACELLULAR MATRIX; IMMUNOHISTOCHEMISTRY; MALE; MESENTERIC ARTERY; NONHUMAN; PRIORITY JOURNAL; RAT; SHEAR STRESS; UPREGULATION; VASCULARIZATION; VEIN GRAFT; ZYMOGRAPHY;

ANIMALS; ARTERIES; CELL PROLIFERATION; COLLATERAL CIRCULATION; DOXYCYCLINE; EARLY GROWTH RESPONSE PROTEIN 1; ENZYME ACTIVATION; EXTRACELLULAR MATRIX; ILEUM; LIGATION; MALE; MATRIX METALLOPROTEINASE 14; MATRIX METALLOPROTEINASE 2; MATRIX METALLOPROTEINASE 9; MATRIX METALLOPROTEINASES; MESENTERIC ARTERIES; MODELS, ANIMAL; PROTEASE INHIBITORS; PROTO-ONCOGENE PROTEINS C-JUN; RATS; RATS, WISTAR; SPLANCHNIC CIRCULATION; STRESS, MECHANICAL; TIME FACTORS; TUNICA INTIMA; UP-REGULATION;

EID: 35348973442     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00100.2007     Document Type: Article

References (60)

1. Asanuma K, Magid R, Johnson C, Nerem RM, Galis ZS. Uniaxial strain upregulates matrix-degrading enzymes produced by human vascular smooth muscle cells. Am J Physiol Heart Circ Physiol 284: H1778-H1784, 2003.
2. Bakker EN, Pistea A, Spaan JA, Rolf T, de Vries CJ, van Rooijen N, Candi E, VanBavel E. Flow-dependent remodeling of small arteries in mice deficient for tissue-type transglutaminase: possible compensation by macrophage-derived factor XIII. Circ Res 99: 86-92, 2006.
3. Belkin AM, Zemskov EA, Hang J, Akimov SS, Sikora S, Strongin AY. Cell-surface-associated tissue transglutaminase is a target of MMP-2 proteolysis. Biochemistry 43: 11760-11769, 2004.
4. Bendeck MP, Irvin C, Reidy MA. Inhibition of matrix metalloproteinase activity inhibits smooth muscle cell migration but not neointimal thickening after arterial injury. Circ Res 78: 38-43, 1996.
5. Berceli SA, Jiang Z, Klingman NV, Schultz GS, Keith Ozaki C. Early differential MMP-2 and -9 dynamics during flow-induced arterial and vein graft adaptations. J Surg Res 134: 327-334, 2006.
6. Brownlee RD, Langille BL. Arterial adaptations to altered blood flow. Can J Physiol Pharmacol 69: 978-983, 1991.
7. Buus CL, Pourageaud F, Fazzi GE, Janssen G, Mulvany MJ, De Mey JGR. Smooth muscle cell changes during flow-related remodeling of rat mesenteric resistance arteries. Circ Res 89: 180-186, 2001.
8. Cai W, Vosschulte R, Afsah-Hedjri A, Koltai S, Kocsis E, Scholz D, Kostin S, Schaper W, Schaper J. Altered balance between extracellular proteolysis and antiproteolysis is associated with adaptive coronary arteriogenesis. J Mol Cell Cardiol 32: 997-1011, 2000.
9. Cai WJ, Koltai S, Kocsis E, Scholz D, Kostin S, Luo X, Schaper W, Schaper J. Remodeling of the adventitia during coronary arteriogenesis. Am J Physiol Heart Circ Physiol 284: H31-H40, 2003.
10. Cai WJ, Kocsis E, Wu X, Rodriguez M, Luo X, Schaper W, Schaper J. Remodeling of the vascular tunica media is essential for development of collateral vessels in the canine heart. Mol Cell Biochem 264: 201-210, 2004.
11. Deindl E, Ziegelhoffer T, Kanse SM, Fernandez B, Neubauer E, Carmeliet P, Preissner KT, Schaper W. Receptor-independent role of the urokinase-type plasminogen activator during arteriogenesis (Abstract). FASEB J 17: 1174-1176, 2003.
12. 2 production by non-small cell lung cancer cells regulates matrix metalloproteinase-2 and CD44 in cyclooxygenase-2-dependent invasion. J Biol Chem 277: 50828-50833, 2002.
13. Franco C, Ho B, Mulholland D, Hou G, Islam M, Donaldson K, Bendeck MP. Doxycycline alters vascular smooth muscle cell adhesion, migration, and reorganization of fibrillar collagen matrices. Am J Pathol 168: 1697-1709, 2006.
14. Garanich JS, Pahakis M, Tarbell JM. Shear stress inhibits smooth muscle cell migration via nitric oxide-mediated downregulation of matrix metalloproteinase-2 activity. Am J Physiol Heart Circ Physiol 288: H2244-H2252, 2005.
15. Haas TL, Davis SJ, Madri JA. 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, 1998.
16. Haas TL, Stitelman D, Davis SJ, Apte SS, Madri JA. Egr-1 mediates extracellular matrix-driven transcription of membrane type 1 matrix metalloproteinase in endothelium. J Biol Chem 274: 22679-22685, 1999.
17. Heil M, Ziegelhoeffer T, Pipp F, Kostin S, Martin S, Clauss M, Schaper W. Blood monocyte concentration is critical for enhancement of collateral artery growth. Am J Physiol Heart Circ Physiol 283: H2411-H2419, 2002.
18. Heil M, Ziegelhoeffer T, Wagner S, Fernandez B, Helisch A, Martin S, Tribulova S, Kuziel WA, Bachmann G, Schaper W. Collateral artery growth (arteriogenesis) after experimental arterial occlusion is impaired in mice lacking CC-chemokine receptor-2. Circ Res 94: 671-677, 2004.
19. Heil M, Schaper W. Influence of mechanical, cellular, and molecular factors on collateral artery growth (arteriogenesis). Circ Res 95: 449-458, 2004.
20. Herzog S, Sager H, Khmelevski E, Deylig A, Ito WD. Collateral arteries grow from preexisting anastomoses in the rat hindlimb. Am J Physiol Heart Circ Physiol 283: H2012-H2020, 2002.
21. Husain S, Jafri F, Crosson CE. Acute effects of PGF2 on MMP-2 secretion from human ciliary muscle cells: a PKC- and ERK-dependent process. Invest Ophthalmol Vis Sci 46: 1706-1713, 2005.
22. Hyre CE, Unthank JL, Dalsing MC. Direct in vivo measurement of flow-dependent nitric oxide production in mesenteric resistance arteries. J Vasc Surg 27: 726-732, 1998.
23. Ispanovic E, Haas T. JNK and PI3K differentially regulate MMP-2 and MT1-MMP mRNA and protein in response to actin cytoskeleton reorganization in endothelial cells. Am J Physiol Cell Physiol 291: C579-C588, 2006.
24. Itoh Y, Seiki M. MT1-MMP: a potent modifier of pericellular microenvironment. J Cell Physiol 206: 1-8, 2006.
25. Jackson ZS, Dajnowiec D, Gotlieb AI, Langille BL. Partial off-loading of longitudinal tension induces arterial tortuosity. Arterioscler Thromb Vasc Biol 25: 957-962, 2005.
26. Johnson C, Sung HJ, Lessner SM, Fini ME, Galis ZS. Matrix metalloproteinase-9 is required for adequate angiogenic revascularization of ischemic tissues: potential role in capillary branching. Circ Res 94: 262-268, 2004.
27. Kamiya A, Togawa T. Adaptive regulation of wall shear-stress to flow change in the canine carotid artery. Am J Physiol Heart Circ Physiol 239: H14-H21, 1980.
28. Kleiner DE, Stetler-Stevenson WG. Quantitative zymography: detection of picogram quantities of gelatinases. Anal Biochem 218: 325-329, 1994.
29. Lee CZ, Xu B, Hashimoto T, McCulloch CE, Yang GY, Young WL. Doxycycline suppresses cerebral matrix metalloproteinase-9 and angiogenesis induced by focal hyperstimulation of vascular endothelial growth factor in a mouse model. Stroke 35: 1715-1719, 2004.
30. Lee CZ, Yao JS, Huang Y, Zhai W, Liu W, Guglielmo BJ, Lin E, Yang GY, Young WL. Dose-response effect of tetracyclines on cerebral matrix metalloproteinase-9 after vascular endothelial growth factor hyperstimulation. J Cereb Blood Flow Metab 26: 1157-1164, 2006.
31. Lehoux S, Tedgui A. Cellular mechanics and gene expression in blood vessels. J Biomech 36: 631-643, 2003.
32. Liu J, Xiong W, Baca-Regen L, Nagase H, Baxter BT. Mechanism of inhibition of matrix metalloproteinase-2 expression by doxycycline in human aortic smooth muscle cells. J Vasc Surg 38: 1376 -1383, 2003.
33. Longland CJ. The collateral circulation of the limb - Arris and Gale Lecture delivered at the Royal College of Surgeons of England on 4th February 1953. Ann R Coll Surg Engl 13: 161-176, 1953.
34. Masuda H, Kawamura K, Tohda K, Shozawa T, Sageshima M, Kamiya A. Increase in endothelial-cell density before artery enlargement in flow-loaded canine carotid-artery. Arteriosclerosis 9: 812-823, 1989.
35. Matsunaga T, Weihrauch DW, Moniz MC, Tessmer J, Warltier DC, Chilian WM. Angiostatin inhibits coronary angiogenesis during impaired production of nitric oxide. Circulation 105: 2185-2191, 2002.
36. Milkiewicz M, Kelland C, Colgan S, Haas TL. Nitric oxide and p38 MAP kinase mediate shear stress-dependent inhibition of MMP-2 production in microvascular endothelial cells. J Cell Physiol 208: 229-237, 2006.
37. Oh J, Takahashi R, Adachi E, Kondo S, Kuratomi S, Noma A, Alexander DB, Motoda H, Okada A, Seiki M, Itoh T, Itohara S, Takahashi C, Noda M. Mutations in two matrix metalloproteinase genes, MMP-2 and MT1-MMP, are synthetic lethal in mice. Oncogene 23: 5041-5048, 2004.
38. Pan MR, Hung WC. Nonsteroidal anti-inflammatory drugs inhibit matrix metalloproteinase-2 via suppression of the ERK/Sp1-mediated transcription. J Biol Chem 277: 32775-32780, 2002.
39. Petrinec D, Liao S, Holmes DR, Reilly JM, Parks WC, Thompson RW. Doxycycline inhibition of aneurysmal degeneration in an elastaseinduced rat model of abdominal aortic aneurysm: preservation of aortic elastin associated with suppressed production of 92 kD gelatinase. J Vasc Surg 23: 336-346, 1996.
40. Pourageaud F, De Mey JG. Structural properties of rat mesenteric small arteries after 4-wk exposure to elevated or reduced blood flow. Am J Physiol Heart Circ Physiol 273: H1699-H1706, 1997.
41. Prager GW, Breuss JM, Steurer S, Mihaly J, Binder BR. Vascular endothelial growth factor (VEGF) induces rapid prourokinase (pro-uPA) activation on the surface of endothelial cells. Blood 103: 955-962, 2004.
42. Prior BM, Yang HT, Terjung RL. What makes vessels grow with exercise training? J Appl Physiol 97: 1119-1128, 2004.
43. Schaper W. New paradigms for collateral vessel growth. Basic Res Cardiol 88: 193-198, 1993.
44. Sho E, Sho M, Singh TM, Nanjo H, Komatsu M, Xu C, Masuda H, Zarins CK. Arterial enlargement in response to high flow requires early expression of matrix metalloproteinases to degrade extracellular matrix. Exp Mol Pathol 73: 142-153, 2002.
45. Skalak TC, Price RJ. The role of mechanical stresses in microvascular remodeling. Microcirculation 3: 143-165, 1996.
46. Stepp DW, Pollock DM, Frisbee JC. Low-flow vascular remodeling in the metabolic syndrome X. Am J Physiol Heart Circ Physiol 286: H964-H970, 2004.
47. Sun D, Liu H, Yan C, Jacobson A, Ojaimi C, Huang A, Kaley G. COX-2 contributes to the maintenance of flow-induced dilation in arterioles of eNOS-knockout mice. Am J Physiol Heart Circ Physiol 291: H1429-H1435, 2006.
48. Takahashi Y, Kawahara F, Noguchi M, Miwa K, Sato H, Seiki M, Inoue H, Tanabe T, Yoshimoto T. Activation of matrix metalloproteinase-2 in human breast cancer cells overexpressing cyclooxygenase-1 or -2. FEBS Lett 460: 145-148, 1999.
49. Tang GL, Chang DS, Sarkar R, Wang R, Messina LM. The effect of gradual or acute arterial occlusion on skeletal muscle blood flow, arteriogenesis, and inflammation in rat hindlimb ischemia. J Vasc Surg 41: 312-320, 2005.
50. Thompson RW, Baxter BT. MMP inhibition in abdominal aortic aneurysms: rationale for a prospective randomized clinical trial. Ann NY Acad Sci 878: 159-178, 1999.
51. Tronc F, Mallat Z, Lehoux S, Wassef M, Esposito B, Tedgui A. Role of matrix metalloproteinases in blood flow-induced arterial enlargement: interaction with NO. Arterioscler Thromb Vasc Biol 20: E120-E126, 2000.
52. Tulis DA, Unthank JL, Prewitt RL. Flow-induced arterial remodeling in rat mesenteric vasculature. Am J Physiol Heart Circ Physiol 274: H874-H882, 1998.
53. Tuttle JL, Hahn TL, Sanders BM, Witzmann FA, Miller SJ, Dalsing MC, Unthank JL. Impaired collateral development in mature rats. Am J Physiol Heart Circ Physiol 283: H146-H155, 2002.
54. Tuttle JL, Nachreiner RD, Bhuller AS, Condict KW, Connors BA, Herring BP, Dalsing MC, Unthank JL. Shear level influences resistance artery remodeling: wall dimensions, cell density, and eNOS expression. Am J Physiol Heart Circ Physiol 281: H1380-H1389, 2001.
55. Unthank JL, Nixon JC, Burkhart HM, Fath SW, Dalsing MC. Early collateral and microvascular adaptations to intestinal artery occlusion in rat. Am J Physiol Heart Circ Physiol 271: H914-H923, 1996.
56. Unthank JL, Sheridan KM, Dalsing MC. Collateral growth in the peripheral circulation: a review. Vasc Endovascular Surg 38: 291-313, 2004.
57. Unthank JL, Fath SW, Burkhart HM, Miller SC, Dalsing MC. Wall remodeling during luminal expansion of mesenteric arterial collaterals in the rat. Circ Res 79: 1015-1023, 1996.
58. Yetik-Anacak G, Catravas JD. Nitric oxide and the endothelium: history and impact on cardiovascular disease. Vasc Pharmacol 45: 268-276, 2006.
59. Yun S, Dardik A, Haga M, Yamashita A, Yamaguchi S, Koh Y, Madri JA, Sumpio BE. Transcription factor Sp1 phosphorylation induced by shear stress inhibits membrane type 1-matrix metalloproteinase expression in endothelium. J Biol Chem 277: 34808-34814, 2002.
60. Zarins CK, Zatina MA, Giddens DP, Ku DN, Glagov S. Shear-stress regulation of artery lumen diameter in experimental atherogenesis. J Vasc Surg 5: 413-420, 1987.