The development of cardiac fibrosis in low tissue factor mice is gender-dependent and is associated with differential regulation of urokinase plasminogen activator

Journal of Molecular and Cellular Cardiology

Volumn 42, Issue 3, 2007, Pages 559-571

  Davis, Darren R ^a   Wilson, Kate ^a   Sam, Melissa J ^a   Kennedy, Sean E ^a   Mackman, Nigel ^b   Charlesworth, John A ^a   Erlich, Jonathan H ^a  

^a UNIVERSITY OF NEW SOUTH WALES   (Australia)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

Cardiac fibrosis; Gender; MMP; TIMP; Tissue factor; Urokinase plasminogen activator

Indexed keywords

MESSENGER RNA; STROMELYSIN; THROMBOPLASTIN; TISSUE INHIBITOR OF METALLOPROTEINASE 1; UROKINASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; ENZYME LINKED IMMUNOSORBENT ASSAY; ENZYME REGULATION; FEMALE; HEART MUSCLE FIBROSIS; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEX DIFFERENCE; UPREGULATION; ZYMOGRAPHY;

ANIMALS; BIOLOGICAL MARKERS; DOWN-REGULATION; ENDOMYOCARDIAL FIBROSIS; FEMALE; HUMANS; IMMEDIATE-EARLY PROTEINS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MALE; MATRIX METALLOPROTEINASES; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; OXIDATIVE STRESS; RNA, MESSENGER; SEX CHARACTERISTICS; THROMBOPLASTIN; TISSUE INHIBITOR OF METALLOPROTEINASES; UP-REGULATION; URINARY PLASMINOGEN ACTIVATOR;

MURINAE; MUS;

EID: 33847392969     PISSN: 00222828     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2006.11.017     Document Type: Article

References (39)

1. Pawlinski R., Pedersen B., Erlich J., and Mackman N. Role of tissue factor in haemostasis, thrombosis, angiogenesis and inflammation: lessons from low tissue factor mice. Thromb. Haemost. 92 3 (2004) 444-450
2. Carmeliet P., Mackman N., Moons L., Luther T., Gressens P., Van Vlaenderen I., et al. Role of tissue factor in embryonic blood vessel development. Nature 383 6595 (1996) 73-75
3. Parry G.C., Erlich J.H., Carmeliet P., Luther T., and Mackman N. Low levels of tissue factor are compatible with development and hemostasis in mice. J. Clin. Invest. 101 3 (1998) 560-569
4. Pawlinski R., Fernandes A., Kehrle B., Pedersen B., Parry G., Erlich J., et al. Tissue factor deficiency causes cardiac fibrosis and left ventricular dysfunction. Proc. Natl. Acad. Sci. U. S. A. 99 24 (2002) 15333-15338
5. Weber K.T., Brilla C.G., Campbell S.E., Zhou G., Matsubara L., and Guarda E. Pathologic hypertrophy with fibrosis: the structural basis for myocardial failure. Blood Pressure 1 2 (1992) 75-85
6. Vanhoutte D., Schellings M., Pinto Y., and Heymans S. Relevance of matrix metalloproteinases and their inhibitors after myocardial infarction: a temporal and spatial window. Cardiovasc. Res. 69 3 (2006) 604-613
7. Ollivier V., Chabbat J., Herbert J.M., Hakim J., and de Prost D. Vascular endothelial growth factor production by fibroblasts in response to factor VIIa binding to tissue factor involves thrombin and factor Xa. Arterioscler. Thromb. Vasc. Biol. 20 5 (2000) 1374-1381
8. Zhang J., Ding J., Zhang X., Shao X., and Hao Z. Regulation of vascular endothelial growth factor (VEGF) production and angiogenesis by tissue factor (TF) in SGC-7901 gastric cancer cells. Cancer Biol. Ther. 4 7 (2005) 769-772
9. Abe K., Shoji M., Chen J., Bierhaus A., Danave I., Micko C., et al. Regulation of vascular endothelial growth factor production and angiogenesis by the cytoplasmic tail of tissue factor. Proc. Natl. Acad. Sci. U. S. A. 96 15 (1999) 8663-8668
10. Clauss M., Weich H., Breier G., Knies U., Rockl W., Waltenberger J., et al. The vascular endothelial growth factor receptor Flt-1 mediates biological activities. Implications for a functional role of placenta growth factor in monocyte activation and chemotaxis. J. Biol. Chem. 271 30 (1996) 17629-17634
11. Wang H., and Keiser J.A. Vascular endothelial growth factor upregulates the expression of matrix metalloproteinases in vascular smooth muscle cells: role of flt-1. Circ. Res. 83 8 (1998) 832-840
12. Lamoreaux W.J., Fitzgerald M.E., Reiner A., Hasty K.A., and Charles S.T. Vascular endothelial growth factor increases release of gelatinase A and decreases release of tissue inhibitor of metalloproteinases by microvascular endothelial cells in vitro. Microvasc. Res. 55 1 (1998) 29-42
13. Duhamel-Clerin E., Orvain C., Lanza F., Cazenave J.P., and Klein-Soyer C. Thrombin receptor-mediated increase of two matrix metalloproteinases, MMP-1 and MMP-3, in human endothelial cells. Arterioscler. Thromb. Vasc. Biol. 17 10 (1997) 1931-1938
14. Zucker S., Mirza H., Conner C.E., Lorenz A.F., Drews M.H., Bahou W.F., et al. Vascular endothelial growth factor induces tissue factor and matrix metalloproteinase production in endothelial cells: conversion of prothrombin to thrombin results in progelatinase A activation and cell proliferation. Int. J. Cancer 75 5 (1998) 780-786
15. Chambers R.C., Leoni P., Blanc-Brude O.P., Wembridge D.E., and Laurent G.J. Thrombin is a potent inducer of connective tissue growth factor production via proteolytic activation of protease-activated receptor-1. J. Biol. Chem. 275 45 (2000) 35584-35591
16. Chen M.M., Lam A., Abraham J.A., Schreiner G.F., and Joly A.H. CTGF expression is induced by TGF-beta in cardiac fibroblasts and cardiac myocytes: a potential role in heart fibrosis. J. Mol. Cell. Cardiol. 32 10 (2000) 1805-1819
17. Takeshita K., Hayashi M., Iino S., Kondo T., Inden Y., Iwase M., et al. Increased expression of plasminogen activator inhibitor-1 in cardiomyocytes contributes to cardiac fibrosis after myocardial infarction. Am. J. Pathol. 164 2 (2004) 449-456
18. He C.J., Rondeau E., Medcalf R.L., Lacave R., Schleuning W.D., and Sraer J.D. Thrombin increases proliferation and decreases fibrinolytic activity of kidney glomerular epithelial cells. J. Cell. Physiol. 146 1 (1991) 131-140
19. Carmeliet P., and Collen D. Development and disease in proteinase-deficient mice: role of the plasminogen, matrix metalloproteinase and coagulation system. Thromb. Res. 91 6 (1998) 255-285
20. Breckon J.J., Papaioannou S., Kon L.W., Tumber A., Hembry R.M., Murphy G., et al. Stromelysin (MMP-3) synthesis is up-regulated in estrogen-deficient mouse osteoblasts in vivo and in vitro. J. Bone Miner. Res. 14 11 (1999) 1880-1890
21. Jones C.B., Sane D.C., and Herrington D.M. Matrix metalloproteinases: a review of their structure and role in acute coronary syndrome. Cardiovasc. Res. 59 4 (2003) 812-823
22. Lockwood C.J., Krikun G., Aigner S., and Schatz F. Effects of thrombin on steroid-modulated cultured endometrial stromal cell fibrinolytic potential. J. Clin. Endocrinol. Metab. 81 1 (1996) 107-112
23. Szotowski B., Goldin-Lang P., Antoniak S., Bogdanov V.Y., Pathirana D., Pauschinger M., et al. Alterations in myocardial tissue factor expression and cellular localization in dilated cardiomyopathy. J. Am. Coll. Cardiol. 45 7 (2005) 1081-1089
24. Malarstig A., Tenno T., Jossan S., Aberg M., and Siegbahn A. A quantitative real-time PCR method for tissue factor mRNA. Thromb. Res. 112 3 (2003) 175-183
25. Li Y.Y., McTiernan C.F., and Feldman A.M. Interplay of matrix metalloproteinases, tissue inhibitors of metalloproteinases and their regulators in cardiac matrix remodelling. Cardiovasc. Res. 46 2 (2000) 214-224
26. Du X.J. Gender modulates cardiac phenotype development in genetically modified mice. Cardiovasc. Res. 63 3 (2004) 510-519
27. Chang W.Y., Wilson M.J., Birch L., and Prins G.S. Neonatal estrogen stimulates proliferation of periductal fibroblasts and alters the extracellular matrix composition in the rat prostate. Endocrinology 140 1 (1999) 405-415
28. Heymans S., Luttun A., Nuyens D., Theilmeier G., Creemers E., Moons L., et al. Inhibition of plasminogen activators or matrix metalloproteinases prevents cardiac rupture but impairs therapeutic angiogenesis and causes cardiac failure. Nat. Med. 5 10 (1999) 1135-1142
29. Heymans S., Lupu F., Terclavers S., Vanwetswinkel B., Herbert J.M., Baker A., et al. Loss or inhibition of uPA or MMP-9 attenuates LV remodelling and dysfunction after acute pressure overload in mice. Am. J. Pathol. 166 1 (2005) 15-25
30. Heymans S., Pauschinger M., De Palma A., Kallwellis-Opara A., Rutschow S., Swinnen M., et al. Inhibition of urokinase-type plasminogen activator or matrix metalloproteinases prevents cardiac injury and dysfunction during viral myocarditis. Circulation 114 6 (2006) 565-573
31. Moriwaki H., Stempien-Otero A., Kremen M., Cozen A.E., and Dichek D.A. Overexpression of urokinase by macrophages or deficiency of plasminogen activator inhibitor type 1 causes cardiac fibrosis in mice. Circ. Res. 95 6 (2004) 637-644
32. Stempien-Otero A., Plawman A., Meznarich J., Dyamenahalli T., Otsuka G., and Dichek D.A. Mechanisms of cardiac fibrosis induced by urokinase plasminogen activator. J. Biol. Chem. 281 22 (2006) 15345-15351
33. Campbell S.E., Janicki J.S., Matsubara B.B., and Weber K.T. Myocardial fibrosis in the rat with mineralocorticoid excess. Prevention of scarring by amiloride. Am. J. Hypertens 6 6 Pt. 1 (1993) 487-495
34. Gaertner R., Jacob M.P., Prunier F., Angles-Cano E., Mercadier J.J., and Michel J.B. The plasminogen-MMP system is more activated in the scar than in viable myocardium 3 months post-MI in the rat. J. Mol. Cell. Cardiol. 38 1 (2005) 193-204
35. Spinale F.G., Coker M.L., Heung L.J., Bond B.R., Gunasinghe H.R., Etoh T., et al. A matrix metalloproteinase induction/activation system exists in the human left ventricular myocardium and is upregulated in heart failure. Circulation 102 16 (2000) 1944-1949
36. Peterson J.T., Li H., Dillon L., and Bryant J.W. Evolution of matrix metalloproteinase and tissue inhibitor expression during heart failure progression in the infarcted rat. Cardiovasc. Res. 46 2 (2000) 307-315
37. Sakata Y., Yamamoto K., Mano T., Nishikawa N., Yoshida J., Hori M., et al. Activation of matrix metalloproteinases precedes left ventricular remodelling in hypertensive heart failure rats: its inhibition as a primary effect of Angiotensin-converting enzyme inhibitor. Circulation 109 17 (2004) 2143-2149
38. Pedersen B., Holscher T., Sato Y., Pawlinski R., and Mackman N. A balance between tissue factor and tissue factor pathway inhibitor is required for embryonic development and hemostasis in adult mice. Blood 105 7 (2005) 2777-2782
39. Spinale F.G. Matrix metalloproteinases: regulation and dysregulation in the failing heart. Circ. Res. 90 5 (2002) 520-530