Divergent roles of matrix metalloproteinase 2 in pathogenesis of thoracic aortic aneurysm

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 35, Issue 4, 2015, Pages 888-898

  Shen, Mengcheng ^a,b   Lee, Jiwon ^a,b   Basu, Ratnadeep ^a,b   Sakamuri, Siva S V P ^a,b   Wang, Xiuhua ^a,b   Fan, Dong ^a,b   Kassiri, Zamaneh ^a,b  

^a UNIVERSITY OF ALBERTA   (Canada)

^b MAZANKOWSKI ALBERTA HEART INSTITUTE   (Canada)

Author keywords

aortic aneurysm, thoracic; matrix metalloproteinase 2

Indexed keywords

ANGIOTENSIN II; CALCIUM CHLORIDE; COLLAGEN TYPE 1; ELASTIN; GELATINASE A; GELATINASE B; HYPOXANTHINE PHOSPHORIBOSYLTRANSFERASE; SMAD2 PROTEIN; SMAD3 PROTEIN; TRANSFORMING GROWTH FACTOR BETA; COLLAGEN; MESSENGER RNA; MMP2 PROTEIN, MOUSE; SMAD2 PROTEIN, MOUSE; SMAD3 PROTEIN, MOUSE;

ABDOMINAL AORTA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AORTA WALL; ARTICLE; ASCENDING AORTA; COLLAGEN FIBER; CONTROLLED STUDY; HYPERTENSION; IN VITRO STUDY; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN DEGRADATION; SMOOTH MUSCLE FIBER; THORACIC AORTA; THORACIC AORTA ANEURYSM; VASODILATATION; ANIMAL; AORTIC ANEURYSM, THORACIC; C57BL MOUSE; CELL CULTURE; CHEMICALLY INDUCED; DEFICIENCY; DISEASE MODEL; ECHOGRAPHY; ENZYMOLOGY; GENETICS; GENOTYPE; LESIONS AND DEFECTS; METABOLISM; PATHOLOGY; PHENOTYPE; SIGNAL TRANSDUCTION; VASCULAR REMODELING; VASCULAR SMOOTH MUSCLE;

ANGIOTENSIN II; ANIMALS; AORTA, THORACIC; AORTIC ANEURYSM, THORACIC; CALCIUM CHLORIDE; CELLS, CULTURED; COLLAGEN; DILATATION, PATHOLOGIC; DISEASE MODELS, ANIMAL; ELASTIN; GENOTYPE; MALE; MATRIX METALLOPROTEINASE 2; MICE, INBRED C57BL; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; PHENOTYPE; RNA, MESSENGER; SIGNAL TRANSDUCTION; SMAD2 PROTEIN; SMAD3 PROTEIN; TRANSFORMING GROWTH FACTOR BETA; VASCULAR REMODELING;

EID: 84930243436     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.114.305115     Document Type: Article

References (69)

1. Best VA, Price JF, Fowkes FG. Persistent increase in the incidence of abdominal aortic aneurysm in Scotland, 1981-2000. Br J Surg. 2003:90:1510-1515.
2. Filipovic M, Goldacre MJ, Roberts SE, Yeates D, Duncan ME, Cook-Mozaffari P. Trends in mortality and hospital admission rates for abdominal aortic aneurysm in England and Wales, 1979-1999. Br J Surg. 2005:92:968-975.
3. Lindsay ME, Dietz HC. Lessons on the pathogenesis of aneurysm from heritable conditions. Nature. 2011;473:308-316. doi: 10.1038/ nature10145.
4. National Center for Injury Prevention and Control. WISQRS Leading Causes of Death Reports, 1999-2006. http://webappa.cdc.gov/sasweb/ ncipc/leadcaus10.html.
5. Propanolol Aneurysm Trial Investigators. Propranolol for small abdominal aortic aneurysms: results of a randomized trial. J Vasc Surg. 2002:35:72-79.
6. Hackam DG, Thiruchelvam D, Redelmeier DA. Angiotensinconverting enzyme inhibitors and aortic rupture: A populationbased case-control study. Lancet. 2006;368:659-665. doi: 10.1016/ S0140-6736(06)69250-7.
7. Brooke BS, Habashi JP, Judge DP, Patel N, Loeys B, Dietz HC 3rd. Angiotensin II blockade and aortic-root dilation in Marfan's syndrome. N Engl J Med. 2008;358:2787-2795. doi: 10.1056/NEJMoa0706585.
8. Sweeting MJ, Thompson SG, Brown LC, Greenhalgh RM, Powell JT. Use of angiotensin converting enzyme inhibitors is associated with increased growth rate of abdominal aortic aneurysms. J Vasc Surg. 2010;52:1-4. doi: 10.1016/j.jvs.2010.02.264.
9. Ahimastos AA, Aggarwal A, D'Orsa KM, Formosa MF, White AJ, Savarirayan R, Dart AM, Kingwell BA. Effect of perindopril on large artery stiffness and aortic root diameter in patients with Marfan syndrome: A randomized controlled trial. JAMA. 2007;298:1539-1547. doi: 10.1001/ jama.298.13.1539.
10. Ferguson CD, Clancy P, Bourke B, Walker PJ, Dear A, Buckenham T, Norman P, Golledge J. Association of statin prescription with small abdominal aortic aneurysm progression. Am Heart J. 2010;159:307-313. doi: 10.1016/j.ahj.2009.11.016.
11. Diehm N, Becker G, Katzen B, Benenati J, Kovacs M, Dick F. Statins are associated with decreased mortality in abdominal, but not in thoracic aortic aneurysm patients undergoing endovascular repair: propensity score-adjusted analysis. VASA. 2008;37:241-249. doi: 10.1024/0301-1526.37.3.241.
12. Ruddy JM, Jones JA, Spinale FG, Ikonomidis JS. Regional heterogeneity within the aorta: relevance to aneurysm disease. J Thorac Cardiovasc Surg. 2008;136:1123-1130. doi: 10.1016/j.jtcvs.2008.06.027.
13. Golledge J, Norman PE. Current status of medical management for abdominal aortic aneurysm. Atherosclerosis. 2011;217:57-63.
14. Nordon IM, Hinchliffe RJ, Loftus IM, Thompson MM. Pathophysiology and epidemiology of abdominal aortic aneurysms. Nat Rev Cardiol. 2011;8:92-102. doi: 10.1038/nrcardio.2010.180.
15. Ruddy JM, Jones JA, Ikonomidis JS. Pathophysiology of thoracic aortic aneurysm (TAA): is it not one uniform aorta? Role of embryologic origin. Prog Cardiovasc Dis. 2013;56:68-73. doi: 10.1016/j.pcad.2013.04.002.
16. Moore L, Fan D, Basu R, Kandalam V, Kassiri Z. Tissue inhibitor of metalloproteinases (TIMPs) in heart failure. Heart Fail Rev. 2012;17:693-706. doi: 10.1007/s10741-011-9266-y.
17. Okada Y, Morodomi T, Enghild JJ, Suzuki K, Yasui A, Nakanishi I, Salvesen G, Nagase H. Matrix metalloproteinase 2 from human rheumatoid synovial fibroblasts. Purification and activation of the precursor and enzymic properties. Eur J Biochem. 1990;194:721-730.
18. Ikonomidis JS, Jones JA, Barbour JR, Stroud RE, Clark LL, Kaplan BS, Zeeshan A, Bavaria JE, Gorman JH, Spinale FG, Gorman RC. Expression of matrix metalloproteinases and endogenous inhibitors within ascending aortic aneurysms of patients with Marfan syndrome. Circulation. 2006:114:I365-I370.
19. Crowther M, Brindle NP, Sayers R, Bell PR, Thompson MM. Aneurysmal smooth muscle cells exhibit increased matrix metalloproteinase-2 production in vitro. Ann N Y Acad Sci. 1996;800:283-285.
20. Crowther M, Goodall S, Jones JL, Bell PR, Thompson MM. Localization of matrix metalloproteinase 2 within the aneurysmal and normal aortic wall. Br J Surg. 2000;87:1391-1400. doi: 10.1046/j.1365-2168.2000.01554.x.
21. Goodall S, Crowther M, Hemingway DM, Bell PR, Thompson MM. Ubiquitous elevation of matrix metalloproteinase-2 expression in the vasculature of patients with abdominal aneurysms. Circulation. 2001;104:304-309.
22. Davis V, Persidskaia R, Baca-Regen L, Itoh Y, Nagase H, Persidsky Y, Ghorpade A, Baxter BT. Matrix metalloproteinase-2 production and its binding to the matrix are increased in abdominal aortic aneurysms. Arterioscler Thromb Vasc Biol. 1998;18:1625-1633.
23. Jones JA, Stroud RE, O'Quinn EC, Black LE, Barth JL, Elefteriades JA, Bavaria JE, Gorman JH 3rd, Gorman RC, Spinale FG, Ikonomidis JS. Selective microRNA suppression in human thoracic aneurysms: relationship of miR-29a to aortic size and proteolytic induction. Circ Cardiovasc Genet. 2011;4:605-613. doi: 10.1161/CIRCGENETICS.111.960419.
24. Theruvath TP, Jones JA, Ikonomidis JS. Matrix metalloproteinases and descending aortic aneurysms: parity, disparity, and switch. J Card Surg. 2012;27:81-90. doi: 10.1111/j.1540-8191.2011.01315.x.
25. Longo GM, Xiong W, Greiner TC, Zhao Y, Fiotti N, Baxter BT. Matrix metalloproteinases 2 and 9 work in concert to produce aortic aneurysms. J Clin Invest. 2002;110:625-632. doi: 10.1172/JCI15334.
26. Sokolis DP, Boudoulas H, Karayannacos PE. Segmental differences of aortic function and composition: clinical implications. Hellenic J Cardiol. 2008;49:145-154.
27. Boudoulas KD, Vlachopoulos C, Raman SV, Sparks EA, Triposciadis F, Stefanadis C, Boudoulas H. Aortic function: from the research laboratory to the clinic. Cardiology. 2012;121:31-42. doi: 10.1159/000336147.
28. Tomaschitz A, Pilz S, Ritz E, Morganti A, Grammer T, Amrein K, Boehm BO, März W. Associations of plasma renin with 10-year cardiovascular mortality, sudden cardiac death, and death due to heart failure. Eur Heart J. 2011;32:2642-2649. doi: 10.1093/eurheartj/ehr150.
29. Javed U, Deedwania PC. Angiotensin receptor blockers: novel role in highrisk patients. Cardiol Clin. 2008;26:507-526. doi: 10.1016/j.ccl.2008.07.001.
30. Bohm M. Angiotensin receptor blockers versus angiotensin-converting enzyme inhibitors: where do we stand now? Am J Cardiol. 2007:100:38J-44J.
31. Rateri DL, Davis FM, Balakrishnan A, Howatt DA, Moorleghen JJ, O'Connor WN, Charnigo R, Cassis LA, Daugherty A. Angiotensin II induces regionspecific medial disruption during evolution of ascending aortic aneurysms. Am J Pathol. 2014;184:2586-2595. doi: 10.1016/j.ajpath.2014.05.014.
32. Ikonomidis JS, Barbour JR, Amani Z, Stroud RE, Herron AR, McClister DM Jr, Camens SE, Lindsey ML, Mukherjee R, Spinale FG. Effects of deletion of the matrix metalloproteinase 9 gene on development of murine thoracic aortic aneurysms. Circulation. 2005:112:I242-I248.
33. Xiong W, Knispel R, MacTaggart J, Greiner TC, Weiss SJ, Baxter BT. Membrane-type 1 matrix metalloproteinase regulates macrophage-dependent elastolytic activity and aneurysm formation in vivo. J Biol Chem. 2009;284:1765-1771. doi: 10.1074/jbc.M806239200.
34. Eckhouse SR, Logdon CB, Oelsen JM, Patel RK, Rice AD, Stroud RE, Wince WB, Mukherjee R, Spinale FG, Ikonomidis JS, Jones JA. Reproducible porcine model of thoracic aortic aneurysm. Circulation. 2013:128:S186-S193.
35. Itoh T, Tanioka M, Yoshida H, Yoshioka T, Nishimoto H, Itohara S. Reduced angiogenesis and tumor progression in gelatinase A-deficient mice. Cancer Res. 1998;58:1048-1051.
36. Manning MW, Cassis LA, Daugherty A. Differential effects of doxycycline, a broad-spectrum matrix metalloproteinase inhibitor, on angiotensin II-induced atherosclerosis and abdominal aortic aneurysms. Arterioscler Thromb Vasc Biol. 2003;23:483-488. doi: 10.1161/01. ATV.0000058404.92759.32.
37. Satoh K, Nigro P, Matoba T, O'Dell MR, Cui Z, Shi X, Mohan A, Yan C, Abe J, Illig KA, Berk BC. Cyclophilin A enhances vascular oxidative stress and the development of angiotensin II-induced aortic aneurysms. Nat Med. 2009;15:649-656. doi: 10.1038/nm.1958.
38. Wang Y, Ait-Oufella H, Herbin O, Bonnin P, Ramkhelawon B, Taleb S, Huang J, Offenstadt G, Combadière C, Rénia L, Johnson JL, Tharaux PL, Tedgui A, Mallat Z. TGF-beta activity protects against inflammatory aortic aneurysm progression and complications in angiotensin II-infused mice. J Clin Invest. 2010;120:422-432. doi: 10.1172/JCI38136.
39. Basu R, Lee J, Morton JS, Takawale A, Fan D, Kandalam V, Wang X, Davidge ST, Kassiri Z. TIMP3 is the primary TIMP to regulate agonist-induced vascular remodelling and hypertension. Cardiovasc Res. 2013;98:360-371. doi: 10.1093/cvr/cvt067.
40. Ikonomidis JS, Gibson WC, Gardner J, Sweterlitsch S, Thompson RP, Mukherjee R, Spinale FG. A murine model of thoracic aortic aneurysms. J Surg Res. 2003;115:157-163.
41. Ikonomidis JS, Ivey CR, Wheeler JB, Akerman AW, Rice A, Patel RK, Stroud RE, Shah AA, Hughes CG, Ferrari G, Mukherjee R, Jones JA. Plasma biomarkers for distinguishing etiologic subtypes of thoracic aortic aneurysm disease. J Thorac Cardiovasc Surg. 2013;145:1326-1333. doi: 10.1016/j.jtcvs.2012.12.027.
42. Touyz RM. Intracellular mechanisms involved in vascular remodelling of resistance arteries in hypertension: role of angiotensin II. Exp Physiol. 2005;90:449-455. doi: 10.1113/expphysiol.2005.030080.
43. Odenbach J, Wang X, Cooper S, Chow FL, Oka T, Lopaschuk G, Kassiri Z, Fernandez-Patron C. MMP-2 mediates angiotensin II-induced hypertension under the transcriptional control of MMP-7 and TACE. Hypertension. 2011;57:123-130. doi: 10.1161/HYPERTENSIONAHA.110.159525.
44. Xiong W, Knispel R, Mactaggart J, Baxter BT. Effects of tissue inhibitor of metalloproteinase 2 deficiency on aneurysm formation. J Vasc Surg. 2006;44:1061-1066. doi: 10.1016/j.jvs.2006.06.036.
45. Jones JA, Ruddy JM, Bouges S, Zavadzkas JA, Brinsa TA, Stroud RE, Mukherjee R, Spinale FG, Ikonomidis JS. Alterations in membrane type-1 matrix metalloproteinase abundance after the induction of thoracic aortic aneurysm in a murine model. Am J Physiol Heart Circ Physiol. 2010;299:H114-H124. doi: 10.1152/ajpheart.00028.2010.
46. Halloran BG, Davis VA, McManus BM, Lynch TG, Baxter BT. Localization of aortic disease is associated with intrinsic differences in aortic structure. J Surg Res. 1995;59:17-22. doi: 10.1006/jsre.1995.1126.
47. Daugherty A, Powell JT. Recent highlights of ATVB: aneurysms. Arterioscler Thromb Vasc Biol. 2014;34:691-694. doi: 10.1161/ ATVBAHA.114.303353.
48. Basu R, Fan D, Kandalam V, Lee J, Das SK, Wang X, Baldwin TA, Oudit GY, Kassiri Z. Loss of Timp3 gene leads to abdominal aortic aneurysm formation in response to angiotensin II. J Biol Chem. 2012;287:44083-44096. doi: 10.1074/jbc.M112.425652.
49. Silence J, Collen D, Lijnen HR. Reduced atherosclerotic plaque but enhanced aneurysm formation in mice with inactivation of the tissue inhibitor of metalloproteinase-1 (TIMP-1) gene. Circ Res. 2002;90:897-903.
50. Lindeman JH, Abdul-Hussien H, van Bockel JH, Wolterbeek R, Kleemann R. Clinical trial of doxycycline for matrix metalloproteinase-9 inhibition in patients with an abdominal aneurysm: doxycycline selectively depletes aortic wall neutrophils and cytotoxic T cells. Circulation. 2009;119:2209-2216. doi: 10.1161/CIRCULATIONAHA.108.806505.
51. Meijer CA, Stijnen T, Wasser MN, Hamming JF, van Bockel JH, Lindeman JH; Pharmaceutical Aneurysm Stabilisation Trial Study Group. Doxycycline for stabilization of abdominal aortic aneurysms: A randomized trial. Ann Intern Med. 2013;159:815-823.
52. Wheeler JB, Ikonomidis JS, Jones JA. Connective tissue disorders and cardiovascular complications: The indomitable role of transforming growth factor-beta signaling. Adv Exp Med Biol. 2014;802:107-127. doi: 10.1007/978-94-007-7893-1-8.
53. Kucich U, Rosenbloom JC, Abrams WR, Rosenbloom J. Transforming growth factor-beta stabilizes elastin mRNA by a pathway requiring active Smads, protein kinase C-delta, and p38. Am J Respir Cell Mol Biol. 2002;26:183-188. doi: 10.1165/ajrcmb.26.2.4666.
54. Saharinen J, Hyytiäinen M, Taipale J, Keski-Oja J. Latent transforming growth factor-beta binding proteins (LTBPs)-structural extracellular matrix proteins for targeting TGF-beta action. Cytokine Growth Factor Rev. 1999;10:99-117.
55. Liu JM, Davidson JM. The elastogenic effect of recombinant transforming growth factor-beta on porcine aortic smooth muscle cells. Biochem Biophys Res Commun. 1988;154:895-901.
56. Yu Q, Stamenkovic I. Cell surface-localized matrix metalloproteinase-9 proteolytically activates TGF-beta and promotes tumor invasion and angiogenesis. Genes Dev. 2000;14:163-176.
57. Tatti O, Vehviläinen P, Lehti K, Keski-Oja J. MT1-MMP releases latent TGF-beta1 from endothelial cell extracellular matrix via proteolytic processing of LTBP-1. Exp Cell Res. 2008;314:2501-2514. doi: 10.1016/j. yexcr.2008.05.018.
58. Spinale FG, Escobar GP, Mukherjee R, Zavadzkas JA, Saunders SM, Jeffords LB, Leone AM, Beck C, Bouges S, Stroud RE. Cardiacrestricted overexpression of membrane type-1 matrix metalloproteinase in mice: effects on myocardial remodeling with aging. Circ Heart Fail. 2009;2:351-360. doi: 10.1161/CIRCHEARTFAILURE.108.844845.
59. Wang M, Zhao D, Spinetti G, Zhang J, Jiang LQ, Pintus G, Monticone R, Lakatta EG. Matrix metalloproteinase 2 activation of transforming growth factor-beta1 (TGF-beta1) and TGF-beta1-type II receptor signaling within the aged arterial wall. Arterioscler Thromb Vasc Biol. 2006;26:1503-1509. doi: 10.1161/01.ATV.0000225777.58488.f2.
60. Lee MK, Pardoux C, Hall MC, Lee PS, Warburton D, Qing J, Smith SM, Derynck R. TGF-beta activates Erk MAP kinase signalling through direct phosphorylation of ShcA. EMBO J. 2007;26:3957-3967. doi: 10.1038/ sj.emboj.7601818.
61. Yamashita M, Fatyol K, Jin C, Wang X, Liu Z, Zhang YE. TRAF6 mediates Smad-independent activation of JNK and p38 by TGF-beta. Mol Cell. 2008;31:918-924. doi: 10.1016/j.molcel.2008.09.002.
62. Milewicz DM, Michael K, Fisher N, Coselli JS, Markello T, Biddinger A. Fibrillin-1 (FBN1) mutations in patients with thoracic aortic aneurysms. Circulation. 1996;94:2708-2711.
63. Pereira L, Andrikopoulos K, Tian J, Lee SY, Keene DR, Ono R, Reinhardt DP, Sakai LY, Biery NJ, Bunton T, Dietz HC, Ramirez F. Targetting of the gene encoding fibrillin-1 recapitulates the vascular aspect of Marfan syndrome. Nat Genet. 1997;17:218-222. doi: 10.1038/ng1097-218.
64. Pereira L, Lee SY, Gayraud B, Andrikopoulos K, Shapiro SD, Bunton T, Biery NJ, Dietz HC, Sakai LY, Ramirez F. Pathogenetic sequence for aneurysm revealed in mice underexpressing fibrillin-1. Proc Natl Acad Sci U S A. 1999;96:3819-3823.
65. Bolar N, Van Laer L, Loeys BL. Marfan syndrome: from gene to therapy. Curr Opin Pediatr. 2012;24:498-504. doi: 10.1097/ MOP.0b013e3283557d4c.
66. Cook JR, Carta L, Galatioto J, Ramirez F. Cardiovascular manifestations in Marfan syndrome and related diseases; multiple genes causing similar phenotypes. Clinical Genet. 2014;87:11-20.
67. Xiong W, Meisinger T, Knispel R, Worth JM, Baxter BT. MMP-2 regulates Erk1/2 phosphorylation and aortic dilatation in Marfan syndrome. Circ Res. 2012;110:e92-e101. doi: 10.1161/CIRCRESAHA.112.268268.
68. Lindsay ME, Schepers D, Bolar NA, et al. Loss-of-function mutations in TGFB2 cause a syndromic presentation of thoracic aortic aneurysm. Nat Genet. 2012;44:922-927. doi: 10.1038/ng.2349.
69. Gallo EM, Loch DC, Habashi JP, et al. Angiotensin II-dependent TGF-β signaling contributes to Loeys-Dietz syndrome vascular pathogenesis. J Clin Invest. 2014;124:448-460. doi: 10.1172/JCI69666.