Matrix metalloproteinases: Control of vascular function and their potential role in preeclampsia

Frontiers in Bioscience

Volumn 12, Issue 7, 2007, Pages 2484-2493

  Lalu, Manoj Mathew ^a   Xu, Han ^a   Davidge, Sandra Thomas ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

Endothelial dysfunction; Endothelium; Matrix metalloproteinase; Oxidative stress; Preeclampsia; Tissue inhibitors of matrix metalloproteinases; Vascular dysfunction

Indexed keywords

MATRIX METALLOPROTEINASE;

ENZYMOLOGY; FEMALE; HUMAN; PATHOPHYSIOLOGY; PHYSIOLOGY; PREECLAMPSIA; PREGNANCY; REVIEW; VASOCONSTRICTION; VASODILATATION;

FEMALE; HUMANS; MATRIX METALLOPROTEINASES; PRE-ECLAMPSIA; PREGNANCY; VASOCONSTRICTION; VASODILATION;

EID: 34948871223     PISSN: 27686701     EISSN: 27686698     Source Type: Journal    
DOI: 10.2741/2249     Document Type: Review

References (75)

1. ACOG practice bulletin. Diagnosis and management of preeclampsia and eclampsia. Number 33, January 2002. Obstet Gynecol 99(1), 159-67 (2002)
2. MacKay, A. P., C. J. Berg & H. K. Atrash: Pregnancyrelated mortality from preeclampsia and eclampsia. Obstet Gynecol 97(4), 533-8 (2001)
3. Moodley, J.: Maternal deaths associated with hypertensive disorders of pregnancy: a population-based study. Hypertens Pregnancy 23(3), 247-56 (2004) (Pubitemid 39552297)
4. Ray, J. G., M. J. Vermeulen, M. J. Schull & D. A. Redelmeier: Cardiovascular health after maternal placental syndromes (CHAMPS): population-based retrospective cohort study. Lancet 366(9499), 1797-803 (2005) (Pubitemid 41642644)
5. Thadhani, R., M. J. Stampfer, D. J. Hunter, J. E. Manson, C. G. Solomon & G. C. Curhan: High body mass index and hypercholesterolemia: risk of hypertensive disorders of pregnancy. Obstet Gynecol 94(4), 543-50 (1999) (Pubitemid 29460937)
6. Ness, R. B., N. Markovic, D. Bass, G. Harger & J. M. Roberts: Family history of hypertension, heart disease, and stroke among women who develop hypertension in pregnancy. Obstet Gynecol 102(6), 1366-71 (2003) (Pubitemid 37518420)
7. Dunne, F., P. Brydon, K. Smith & H. Gee: Pregnancy in women with Type 2 diabetes: 12 years outcome data 1990-2002. Diabet Med 20(9), 734-8 (2003) (Pubitemid 41701467)
8. Caritis, S., B. Sibai, J. Hauth, M. Lindheimer, P. Van Dorsten, M. Klebanoff, E. Thom, M. Landon, R. Paul, M. Miodovnik, P. Meis, G. Thurnau, M. Dombrowski, D. McNellis & J. Roberts: Predictors of pre-eclampsia in women at high risk. National Institute of Child Health and Human Development Network of Maternal-Fetal Medicine Units. Am J Obstet Gynecol 179(4), 946-51 (1998)
9. Roberts, J. M. & H. S. Gammill: Preeclampsia: recent insights. Hypertension 46(6), 1243-9 (2005) (Pubitemid 43189714)
10. Delemarre, F. M., E. A. Steegers, P. A. van Dop & P. A. de Jong: Angiotensin sensitivity test revisited. Hypertens Pregnancy 19(3), 289-98 (2000)
11. Galis, Z. S. & J. J. Khatri: Matrix metalloproteinases in vascular remodeling and atherogenesis: the good, the bad, and the ugly. Circ Res 90(3), 251-262 (2002) (Pubitemid 34633925)
12. Sawicki, G., E. Salas, J. Murat, H. Miszta-Lane & M. W. Radomski: Release of gelatinase A during platelet activation mediates aggregation. Nature 386, 616-619 (1997) (Pubitemid 27175428)
13. Dubois, B., S. Starckx, A. Pagenstecher, J. Oord, B. Arnold & G. Opdenakker: Gelatinase B deficiency protects against endotoxin shock. Eur J Immunol 32(8), 2163-71. (2002) (Pubitemid 34965879)
14. Lalu, M. M., E. Pasini, C. J. Schulze, M. Ferrari-Vivaldi, G. Ferrari-Vivaldi, T. Bachetti & R. Schulz: Ischaemia-reperfusion injury activates matrix metalloproteinases in the human heart. Eur Heart J 26(1), 27-35 (2005) (Pubitemid 40221120)
15. Gross, J. & C. Lapiere: Collagenolytic activity in amphibian tissues: a tissue culture assay. Proc Natl Acad Sci USA 54, 1197-1204 (1962)
16. Woessner, J. F., Jr.: MMPs and TIMPs-an historical perspective. Mol Biotechnol 22(1), 33-49 (2002)
17. Nagase, H. & J. F. Woessner, Jr.: Matrix metalloproteinases. J Biol Chem 274(31), 21491-4 (1999)
18. Visse, R. & H. Nagase: Matrix metalloproteinases and tissue inhibitors of metalloproteinases: structure, function, and biochemistry. Circ Res 92(8), 827-39 (2003) (Pubitemid 36542523)
19. Morgunova, E., A. Tuuttila, U. Bergmann, M. Isupov, Y. Lindqvist, G. Schneider & K. Tryggvason: Structure of human pro-matrix metalloproteinase-2: activation mechanism revealed. Science 284(5420), 1667-70 (1999) (Pubitemid 29291376)
20. Van Wart, H. E. & H. Birkedal-Hansen: The cysteine switch: a principle of regulation of metalloproteinase activity with potential applicability to the entire matrix metalloproteinase gene family. Proc Natl Acad Sci USA 87(14), 5578-82 (1990)
21. Gomis-Ruth, F. X., K. Maskos, M. Betz, A. Bergner, R. Huber, K. Suzuki, N. Yoshida, H. Nagase, K. Brew, G. P. Bourenkov, H. Bartunik & W. Bode: Mechanism of inhibition of the human matrix metalloproteinase stromelysin-1 by TIMP-1. Nature 389(6646), 77-81 (1997) (Pubitemid 27387694)
22. Kassiri, Z., G. Y. Oudit, O. Sanchez, F. Dawood, F. F. Mohammed, R. K. Nuttall, D. R. Edwards, P. P. Liu, P. H. Backx & R. Khokha: Combination of tumor necrosis factor-alpha ablation and matrix metalloproteinase inhibition prevents heart failure after pressure overload in tissue inhibitor of metalloproteinase-3 knock-out mice. Circ Res 97(4), 380-90 (2005) (Pubitemid 41216143)
23. Johnson, J. L., A. H. Baker, K. Oka, L. Chan, A. C. Newby, C. L. Jackson & S. J. George: Suppression of atherosclerotic plaque progression and instability by tissue inhibitor of metalloproteinase-2: involvement of macrophage migration and apoptosis. Circulation 113(20), 2435-44 (2006) (Pubitemid 43948051)
24. Nagase, H.: Activation mechanisms of matrix metalloproteinases. Biol Chem 378(3-4), 151-60. (1997) (Pubitemid 27230597)
25. Strongin, A. Y., I. Collier, G. Bannikov, B. L. Marmer, G. A. Grant & G. I. Goldberg: Mechanism of cell surface activation of 72-kDa type IV collagenase. Isolation of the activated form of the membrane metalloprotease. J Biol Chem 270(10), 5331-8 (1995)
26. Lijnen, H. R.: Plasmin and matrix metalloproteinases in vascular remodeling. Thromb Haemost 86(1), 324-33 (2001) (Pubitemid 32663963)
27. Pei, D. & S. J. Weiss: Furin-dependent intracellular activation of the human stromelysin-3 zymogen. Nature 375(6528), 244-7 (1995)
28. Kang, T., H. Nagase & D. Pei: Activation of membrane-type matrix metalloproteinase 3 zymogen by the proprotein convertase furin in the trans-Golgi network. Cancer Res 62(3), 675-81 (2002) (Pubitemid 34126940)
29. Rajagopalan, S., X. P. Meng, S. Ramasamy, D. G. Harrison & Z. S. Galis: Reactive oxygen species produced by macrophage-derived foam cells regulate the activity of vascular matrix metalloproteinases in vitro. Implications for atherosclerotic plaque stability. J Clin Invest 98(11), 2572-2579 (1996) (Pubitemid 26415078)
30. Okamoto, T., T. Akaike, T. Sawa, Y. Miyamoto, A. van der Vliet & H. Maeda: Activation of matrix metalloproteinases by peroxynitrite-induced protein S-glutathiolation via disulfide S-oxide formation. J Biol Chem 276, 29596-29602 (2001)
31. Okamoto, T., T. Akaike, T. Nagano, S. Miyajima, M. Suga, M. Ando, K. Ichimori & H. Maeda: Activation of human neutrophil procollagenase by nitrogen dioxide and peroxynitrite: a novel mechanism for procollagenase activation involving nitric oxide. Arch Biochem Biophys 342(2), 261-274 (1997) (Pubitemid 27251247)
32. Okamoto, T., T. Akuta, F. Tamura, A. van der Vliet & T. Akaike: Molecular mechanism for activation and regulation of matrix metalloproteinases during bacterial infections and respiratory inflammation. Biol Chem 385(11), 997-1006 (2004) (Pubitemid 39600307)
33. Tsukimori, K., K. Fukushima, A. Tsushima & H. Nakano: Generation of reactive oxygen species by neutrophils and endothelial cell injury in normal and preeclamptic pregnancies. Hypertension 46(4), 696-700 (2005) (Pubitemid 43186740)
34. Roggensack, A. M., Y. Zhang & S. T. Davidge: Evidence for peroxynitrite formation in the vasculature of women with preeclampsia. Hypertension 33(1), 83-9 (1999) (Pubitemid 29061846)
35. Manabe, S., Z. Gu & S. A. Lipton: Activation of matrix metalloproteinase-9 via neuronal nitric oxide synthase contributes to NMDA-induced retinal ganglion cell death. Invest Ophthalmol Vis Sci 46(12), 4747-53 (2005) (Pubitemid 44264580)
36. Sinha, I., K. K. Hannawa, G. Ailawadi, D. T. Woodrum, J. W. Ford, P. K. Henke, J. C. Stanley, M. J. Eagleton & G. R. Upchurch, Jr.: The nitric oxide donor DETA-NONOate decreases matrix metalloproteinase-9 expression and activity in rat aortic smooth muscle and abdominal aortic explants. Ann Vasc Surg 20(1), 92-8 (2006) (Pubitemid 43029864)
37. McCawley, L. J. & L. M. Matrisian: Matrix metalloproteinases: they're not just for matrix anymore! Curr Opin Cell Biol 13(5), 534-40 (2001) (Pubitemid 32817010)
38. Schonbeck, U., F. Mach & P. Libby: Generation of biologically active IL-1 beta by matrix metalloproteinases: a novel caspase-1-independent pathway of IL-1 beta processing. J Immunol 161(7), 3340-6 (1998)
39. Haro, H., H. C. Crawford, B. Fingleton, K. Shinomiya, D. M. Spengler & L. M. Matrisian: Matrix metalloproteinase-7-dependent release of tumor necrosis factor-alpha in a model of herniated disc resorption. J Clin Invest 105(2), 143-50 (2000) (Pubitemid 30054353)
40. McQuibban, G. A., J. H. Gong, E. M. Tam, C. A. McCulloch, I. Clark-Lewis & C. M. Overall: Inflammation dampened by gelatinase A cleavage of monocyte chemoattractant protein-3. Science 289(5482), 1202-1206 (2000) (Pubitemid 30650734)
41. Sellers, A., J. J. Reynolds & M. C. Meikle: Neutral metallo-proteinases of rabbit bone. Separation in latent forms of distinct enzymes that when activated degrade collagen, gelatin and proteoglycans. Biochem J 171(2), 493-6 (1978) (Pubitemid 8332729)
42. Harris, E. D., Jr. & S. M. Krane: An endopeptidase from rheumatoid synovial tissue culture. Biochim Biophys Acta 258(2), 566-76 (1972)
43. Collier, I. E., P. A. Krasnov, A. Y. Strongin, H. Birkedal-Hansen & G. I. Goldberg: Alanine scanning mutagenesis and functional analysis of the fibronectin-like collagen-binding domain from human 92-kDa type IV collagenase. J Biol Chem 267(10), 6776-81 (1992)
44. Fernandez-Patron, C., M. W. Radomski & S. M. Davidge: Vascular matrix metalloproteinase-2 cleaves big endothelin-1 yielding a novel vasoconstrictor. Circ Res 85, 906-911 (1999) (Pubitemid 29534165)
45. Xu, D., N. Emoto, A. Giaid, C. Slaughter, S. Kaw, D. deWit & M. Yanagisawa: ECE-1: a membrane-bound metalloprotease that catalyzes the proteolytic activation of big endothelin-1. Cell 78(3), 473-85 (1994) (Pubitemid 24250811)
46. Fernandez-Patron, C., K. G. Stewart, Y. Zhang, E. Koivunen, M. W. Radomski & S. T. Davidge: Vascular matrix metalloproteinase-2-dependent cleavage of calcitonin gene-related peptide promotes vasoconstriction. Circ Res 87(8), 670-676 (2000)
47. Koivunen, E., W. Arap, H. Valtanen, A. Rainisalo, O. P. Medina, P. Heikkila, C. Kantor, C. G. Gahmberg, T. Salo, Y. T. Konttinen, T. Sorsa, E. Ruoslahti & R. Pasqualini: Tumor targeting with a selective gelatinase inhibitor. Nat Biotechnol 17(8), 768-74 (1999) (Pubitemid 29365104)
48. Martinez, A., H. R. Oh, E. J. Unsworth, C. Bregonzio, J. M. Saavedra, W. G. Stetler-Stevenson & F. Cuttitta: Matrix metalloproteinase-2 cleavage of adrenomedullin produces a vasoconstrictor out of a vasodilator. Biochem J 383 (Pt. 3), 413-8 (2004) (Pubitemid 39546110)
49. Schiff, E., S. A. Friedman, B. M. Sibai, L. Kao & S. Schifter: Plasma and placental calcitonin gene-related peptide in pregnancies complicated by severe preeclampsia. Am J Obstet Gynecol 173(5), 1405-9 (1995)
50. Minegishi, T., M. Nakamura, K. Abe, M. Tano, A. Andoh, M. Yoshida, T. Takagi, T. Nishikimi, M. Kojima & K. Kangawa: Adrenomedullin and atrial natriuretic peptide concentrations in normal pregnancy and pre-eclampsia. Mol Hum Reprod 5(8), 767-70 (1999) (Pubitemid 29366875)
51. Davis, M. J. & M. A. Hill: Signaling mechanisms underlying the vascular myogenic response. Physiol Rev 79(2), 387-423 (1999) (Pubitemid 29210926)
52. Lucchesi, P. A., A. Sabri, S. Belmadani & K. Matrougui: Involvement of metalloproteinases 2/9 in epidermal growth factor receptor transactivation in pressureinduced myogenic tone in mouse mesenteric resistance arteries. Circulation 110(23), 3587-93 (2004) (Pubitemid 39612575)
53. Kalmes, A., G. Daum & A. W. Clowes: EGFR transactivation in the regulation of SMC function. Ann N Y Acad Sci 947, 42-54; discussion 54-5 (2001)
54. Cipolla, M. J., N. DeLance & L. Vitullo: Pregnancy prevents hypertensive remodeling of cerebral arteries: a potential role in the development of eclampsia. Hypertension 47(3), 619-26 (2006) (Pubitemid 43843886)
55. Merchant, S. J. & S. T. Davidge: The role of matrix metalloproteinases in vascular function: implications for normal pregnancy and pre-eclampsia. BJOG 111(9), 931-9 (2004) (Pubitemid 39223042)
56. Woessner, J. F., Jr. & C. J. Taplin: Purification and properties of a small latent matrix metalloproteinase of the rat uterus. J Biol Chem 263(32), 16918-25 (1988) (Pubitemid 18268875)
57. Hao, L., M. Du, A. Lopez-Campistrous & C. Fernandez-Patron: Agonist-induced activation of matrix metalloproteinase-7 promotes vasoconstriction through the epidermal growth factor-receptor pathway. Circ Res 94(1), 68-76 (2004) (Pubitemid 38064100)
58. Hao, L., T. Nishimura, H. Wo & C. Fernandez-Patron: Vascular responses to alpha1-adrenergic receptors in small rat mesenteric arteries depend on mitochondrial reactive oxygen species. Arterioscler Thromb Vasc Biol 26(4), 819-25 (2006) (Pubitemid 43732157)
59. Lalu, M. M., R. Chowdhury, J. Cena, A. Lam & R. Schulz: Matrix metalloproteinases contribute to endotoxin and interleukin-1beta induced vascular dysfunction. Brit J Pharmacol (2006 (in press))
60. Chew, D. K., M. S. Conte & R. A. Khalil: Matrix metalloproteinase- specific inhibition of Ca2+ entry mechanisms of vascular contraction. J Vasc Surg 40(5), 1001-10 (2004) (Pubitemid 39535233)
61. Fernandez-Patron, C., M. W. Radomski & S. T. Davidge: Role of matrix metalloproteinase-2 in thrombininduced vasorelaxation of rat mesenteric arteries. Am J Physiol 278 (5), H1473-H1479 (2000) (Pubitemid 30395557)
62. Jeyabalan, A., J. Novak, L. A. Danielson, L. J. Kerchner, S. L. Opett & K. P. Conrad: Essential role for vascular gelatinase activity in relaxin-induced renal vasodilation, hyperfiltration, and reduced myogenic reactivity of small arteries. Circ Res 93(12), 1249-57 (2003) (Pubitemid 37543066)
63. Kelly, B. A., B. C. Bond & L. Poston: Aortic adaptation to pregnancy: elevated expression of matrix metalloproteinases-2 and-3 in rat gestation. Mol Hum Reprod 10(5), 331-7 (2004) (Pubitemid 38714364)
64. Kelly, B. A., B. C. Bond & L. Poston: Gestational profile of matrix metalloproteinases in rat uterine artery. Mol Hum Reprod 9(6), 351-8 (2003) (Pubitemid 36748840)
65. Narumiya, H., Y. Zhang, C. Fernandez-Patron, L. J. Guilbert & S. T. Davidge: Matrix metalloproteinase-2 is elevated in the plasma of women with preeclampsia. Hypertens Pregnancy 20(2), 185-94 (2001) (Pubitemid 33032126)
66. Robbesyn, F., N. Auge, C. Vindis, A. V. Cantero, R. Barbaras, A. Negre-Salvayre & R. Salvayre: High-density lipoproteins prevent the oxidized low-density lipoproteininduced epidermal [corrected] growth factor receptor activation and subsequent matrix metalloproteinase-2 upregulation. Arterioscler Thromb Vasc Biol 25(6), 1206-12 (2005) (Pubitemid 40776610)
67. Myers, J. E., S. J. Merchant, M. Macleod, G. J. Mires, P. N. Baker & S. T. Davidge: MMP-2 levels are elevated in the plasma of women who subsequently develop preeclampsia. Hypertens Pregnancy 24(2), 103-15 (2005) (Pubitemid 40911348)
68. Myers, J., G. Mires, M. Macleod & P. Baker: In preeclampsia, the circulating factors capable of altering in vitro endothelial function precede clinical disease. Hypertension 45(2), 258-63 (2005) (Pubitemid 40179969)
69. Lehoux, S., C. A. Lemarie, B. Esposito, H. R. Lijnen & A. Tedgui: Pressure-induced matrix metalloproteinase-9 contributes to early hypertensive remodeling. Circulation 109(8), 1041-7 (2004) (Pubitemid 38282859)
70. Kolben, M., A. Lopens, J. Blaser, K. Ulm, M. Schmitt, K. T. Schneider & H. Tschesche: Proteases and their inhibitors are indicative in gestational disease. Eur J Obstet Gynecol Reprod Biol 68(1-2), 59-65 (1996) (Pubitemid 26292792)
71. Ahmed, S. H., L. L. Clark, W. R. Pennington, C. S. Webb, D. D. Bonnema, A. H. Leonardi, C. D. McClure, F. G. Spinale & M. R. Zile: Matrix metalloproteinases/tissue inhibitors of metalloproteinases: relationship between changes in proteolytic determinants of matrix composition and structural, functional, and clinical manifestations of hypertensive heart disease. Circulation 113(17), 2089-96 (2006)
72. Tayebjee, M. H., S. K. Nadar, R. J. MacFadyen & G. Y. Lip: Tissue inhibitor of metalloproteinase-1 and matrix metalloproteinase-9 levels in patients with hypertension Relationship to tissue Doppler indices of diastolic relaxation. Am J Hypertens 17(9), 770-4 (2004) (Pubitemid 39201091)
73. Merchant, S. J., H. Narumiya, Y. Zhang, L. J. Guilbert & S. T. Davidge: The effects of preeclampsia and oxygen environment on endothelial release of matrix metalloproteinase-2. Hypertens Pregnancy 23(1), 47-60 (2004) (Pubitemid 38445552)
74. Vatten, L. J., P. R. Romundstad, T. L. Holmen, C. C. Hsieh, D. Trichopoulos & S. O. Stuver: Intrauterine exposure to preeclampsia and adolescent blood pressure, body size, and age at menarche in female offspring. Obstet Gynecol 101(3), 529-33 (2003) (Pubitemid 36288494)
75. Lalu, M. M. & S. T. Davidge: Plasma of preeclamptic women increases matrix metalloproteinase-2 activity and decreases expression of matrix metalloproteinase inhibitors in endothelial cells. Can J Cardiol 21 (C), 62C (2005)