Research progress on the role and mechanism of extracellular matrix in aortic aneurysm and dissection_Chinese Journal of Clinical Thoracic and Cardiovascular Surgery

Authors：

TIAN Ting ¹ , LUO Fan ¹ , ZHAO Liping ¹ , LUO Junyi ¹ , LIU Fen ^1,2 ,  YANG Yining ^2,3,4

1. Heart Center, The First Affiliated Hospital of Xinjiang University, Urumqi, 830054, P. R. China;
2. State Key Laboratory of Pathogenesis, Prevention and Treatment of High Incidence Diseases in Central Asia, Xinjiang Medical University, Urumqi, 830054, P. R. China;
3. Department of Cardiology, People’s Hospital of Xinjiang Uygur Autonomous Region, Urumqi, 830001, P. R. China;
4. Xinjiang Key Laboratory of Cardiovascular Homeostasis and Regeneration Research, Urumqi, 830001, P. R. China;

Corresponding author：

YANG Yining, Email: yangyn5126@163.com

Keywords：

Aortic dissection; aortic aneurysm; extracellular matrix; vascular remodeling; review

DOI：

10.7507/1007-4848.202211092

Video：

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Abstract Full text Figures/Tables Video References Cited by

Aortic aneurysm and dissection are critical cardiovascular diseases that threaten human life and health seriously. No pharmacological treatment can effectively prevent disease progression. The imbalance of aortic wall cells and non-cellular components leads to structural or functional degeneration of the aorta, which is a prerequisite for disease occurrence. As the important non-cellular component, extracellular matrix (ECM) is crucial to maintain the aortic structure, function, and homeostasis. Abnormal production of elastin and collagen, destruction of cross-linking between elastic fibers and collagen fibers, and the imbalance of metalloproteinase and inhibitors leads to excessive degradation of ECM proteins, all of which have destroyed the structure and function of aorta. It will provide more ideas for disease prevention and treatment by learning ECM proteins and their metabolic mechanism. Here, we focus on the ECM proteins that have been reported to be involved in aortic aneurysm and dissection, and discuss the regulatory mechanism of metalloproteinase and inhibitors.

Citation： TIAN Ting, LUO Fan, ZHAO Liping, LUO Junyi, LIU Fen, YANG Yining. Research progress on the role and mechanism of extracellular matrix in aortic aneurysm and dissection. Chinese Journal of Clinical Thoracic and Cardiovascular Surgery, 2024, 31(9): 1376-1384. doi: 10.7507/1007-4848.202211092 Copy

1.	Harky A, Sokal PA, Hasan K, et al. The aortic pathologies: How far we understand it and its implications on thoracic aortic surgery. Braz J Cardiovasc Surg, 2021, 36(4): 535-549.
2.	Shen YH, LeMaire SA, Webb NR, et al. Aortic aneurysms and dissections series. Arterioscler Thromb Vasc Biol, 2020, 40(3): e37-e46.
3.	Koracevic GP. Aortic dissection and aneurysm are hypertensive target organ damages and should be listed in the guidelines. Am J Emerg Med, 2019, 37(2): 365-366.
4.	Akin I, Nienaber CA. Prediction of aortic dissection. Heart, 2020, 106(12): 870-871.
5.	Golledge J. Abdominal aortic aneurysm: Update on pathogenesis and medical treatments. Nat Rev Cardiol, 2019, 16(4): 225-242.
6.	Mammoto A, Matus K, Mammoto T. Extracellular matrix in aging aorta. Front Cell Dev Biol, 2022, 10: 822561.
7.	Xu J, Shi GP. Vascular wall extracellular matrix proteins and vascular diseases. Biochim Biophys Acta, 2014, 1842(11): 2106-2119.
8.	Yanagisawa H, Wagenseil J. Elastic fibers and biomechanics of the aorta: Insights from mouse studies. Matrix Biol, 2020, 85-86: 160-172.
9.	Stepien KL, Bajdak-Rusinek K, Fus-Kujawa A, et al. Role of extracellular matrix and inflammation in abdominal aortic aneurysm. Int J Mol Sci, 2022, 23(19): 1-10.
10.	Jana S, Hu M, Shen M, et al. Extracellular matrix, regional heterogeneity of the aorta, and aortic aneurysm. Exp Mol Med, 2019, 51(12): 1-15.
11.	Sato F, Seino-Sudo R, Okada M, et al. Lysyl oxidase enhances the deposition of tropoelastin through the catalysis of tropoelastin molecules on the cell surface. Biol Pharm Bull, 2017, 40(10): 1646-1653.
12.	Rai P, Robinson L, Davies HA, et al. Is there enough evidence to support the role of glycosaminoglycans and proteoglycans in thoracic aortic aneurysm and dissection? A systematic review. Int J Mol Sci, 2022, 23(16): 1-10.
13.	Ghadie NM, St-Pierre JP, Labrosse MR. The contribution of glycosaminoglycans/proteoglycans to aortic mechanics in health and disease: A critical review. IEEE Trans Biomed Eng, 2021, 68(12): 3491-3500.
14.	Wight TN. A role for proteoglycans in vascular disease. Matrix Biol, 2018, 71-72: 396-420.
15.	Guemann AS, Andrieux J, Petit F, et al. ELN gene triplication responsible for familial supravalvular aortic aneurysm. Cardiol Young, 2015, 25(4): 712-717.
16.	Hadj-Rabia S, Callewaert BL, Bourrat E, et al. Twenty patients including 7 probands with autosomal dominant cutis laxa confirm clinical and molecular homogeneity. Orphanet J Rare Dis, 2013, 8: 36.
17.	Rodrigues Bento J, Meester J, Luyckx I, et al. The genetics and typical traits of thoracic aortic aneurysm and dissection. Annu Rev Genomics Hum Genet, 2022, 23: 223-253.
18.	Gupta PA, Wallis DD, Chin TO, et al. FBN2 mutation associated with manifestations of Marfan syndrome and congenital contractural arachnodactyly. J Med Genet, 2004, 41(5): e56.
19.	Carta L, Pereira L, Arteaga-Solis E, et al. Fibrillins 1 and 2 perform partially overlapping functions during aortic development. J Biol Chem, 2006, 281(12): 8016-8023.
20.	Dasouki M, Markova D, Garola R, et al. Compound heterozygous mutations in fibulin-4 causing neonatal lethal pulmonary artery occlusion, aortic aneurysm, arachnodactyly, and mild cutis laxa. Am J Med Genet A, 2007, 143A(22): 2635-2641.
21.	Wang X, LeMaire SA, Chen L, et al. Decreased expression of fibulin-5 correlates with reduced elastin in thoracic aortic dissection. Surgery, 2005, 138(2): 352-359.
22.	Nakamura T, Lozano PR, Ikeda Y, et al. Fibulin-5/DANCE is essential for elastogenesis in vivo. Nature, 2002, 415(6868): 171-175.
23.	Huang J, Davis EC, Chapman SL, et al. Fibulin-4 deficiency results in ascending aortic aneurysms: A potential link between abnormal smooth muscle cell phenotype and aneurysm progression. Circ Res, 2010, 106(3): 583-592.
24.	Carmo M, Colombo L, Bruno A, et al. Alteration of elastin, collagen and their cross-links in abdominal aortic aneurysms. Eur J Vasc Endovasc Surg, 2002, 23(6): 543-549.
25.	Xiong J, Wang SM, Chen LH, et al. Elastic fibers reconstructed using adenovirus-mediated expression of tropoelastin and tested in the elastase model of abdominal aortic aneurysm in rats. J Vasc Surg, 2008, 48(4): 965-973.
26.	Isenburg JC, Simionescu DT, Starcher BC, et al. Elastin stabilization for treatment of abdominal aortic aneurysms. Circulation, 2007, 115(13): 1729-1737.
27.	Kuivaniemi H, Tromp G, Prockop DJ. Mutations in fibrillar collagens (typesⅠ,Ⅱ,Ⅲ, and Ⅺ), fibril-associated collagen (type Ⅸ), and network-forming collagen (typeⅩ) cause a spectrum of diseases of bone, cartilage, and blood vessels. Hum Mutat, 1997, 9(4): 300-315.
28.	Pepin M, Schwarze U, Superti-Furga A, et al. Clinical and genetic features of Ehlers-Danlos syndrome typeⅣ, the vascular type. N Engl J Med, 2000, 342(10): 673-680.
29.	Kashtan CE, Segal Y, Flinter F, et al. Aortic abnormalities in males with Alport syndrome. Nephrol Dial Transplant, 2010, 25(11): 3554-3560.
30.	Plaisier E, Gribouval O, Alamowitch S, et al. COL4A1 mutations and hereditary angiopathy, nephropathy, aneurysms, and muscle cramps. N Engl J Med, 2007, 357(26): 2687-2695.
31.	Landis BJ, Schubert JA, Lai D, et al. Exome sequencing identifies candidate genetic modifiers of syndromic and familial thoracic aortic aneurysm severity. J Cardiovasc Transl Res, 2017, 10(4): 423-432.
32.	Rahkonen O, Su M, Hakovirta H, et al. Mice with a deletion in the first intron of the Col1a1 gene develop age-dependent aortic dissection and rupture. Circ Res, 2004, 94(1): 83-90.
33.	Smith LB, Hadoke PW, Dyer E, et al. Haploinsufficiency of the murine Col3a1 locus causes aortic dissection: A novel model of the vascular type of Ehlers-Danlos syndrome. Cardiovasc Res, 2011, 90(1): 182-190.
34.	Guo DC, Regalado ES, Gong L, et al. LOX mutations predispose to thoracic aortic aneurysms and dissections. Circ Res, 2016, 118(6): 928-934.
35.	Lee VS, Halabi CM, Hoffman EP, et al. Loss of function mutation in LOX causes thoracic aortic aneurysm and dissection in humans. Proc Natl Acad Sci U S A, 2016, 113(31): 8759-8764.
36.	Cikach FS, Koch CD, Mead TJ, et al. Massive aggrecan and versican accumulation in thoracic aortic aneurysm and dissection. JCI Insight, 2018, 3(5): 1-10.
37.	Shen YH, Lu HS, LeMaire SA, et al. Unfolding the story of proteoglycan accumulation in thoracic aortic aneurysm and dissection. Arterioscler Thromb Vasc Biol, 2019, 39(10): 1899-1901.
38.	Konig KC, Lahm H, Dressen M, et al. Aggrecan: A new biomarker for acute type A aortic dissection. Sci Rep, 2021, 11(1): 10371.
39.	Mattson JM, Turcotte R, Zhang Y. Glycosaminoglycans contribute to extracellular matrix fiber recruitment and arterial wall mechanics. Biomech Model Mechanobiol, 2017, 16(1): 213-225.
40.	Schriefl AJ, Collins MJ, Pierce DM, et al. Remodeling of intramural thrombus and collagen in an Ang-Ⅱinfusion ApoE-/- model of dissecting aortic aneurysms. Thromb Res, 2012, 130(3): e139-e146.
41.	Longo GM, Xiong W, Greiner TC, et al. Matrix metalloproteinases 2 and 9 work in concert to produce aortic aneurysms. J Clin Invest, 2002, 110(5): 625-632.
42.	Li Y, Wang W, Li L, et al. MMPs and ADAMs/ADAMTS inhibition therapy of abdominal aortic aneurysm. Life Sci, 2020, 253: 117659.
43.	Hovsepian DM, Ziporin SJ, Sakurai MK, et al. Elevated plasma levels of matrix metalloproteinase-9 in patients with abdominal aortic aneurysms: A circulating marker of degenerative aneurysm disease. J Vasc Interv Radiol, 2000, 11(10): 1345-1352.
44.	Shen M, Lee J, Basu R, et al. Divergent roles of matrix metalloproteinase 2 in pathogenesis of thoracic aortic aneurysm. Arterioscler Thromb Vasc Biol, 2015, 35(4): 888-898.
45.	Wang X, Khalil RA. Matrix metalloproteinases, vascular remodeling, and vascular disease. Adv Pharmacol, 2018, 81: 241-330.
46.	Maguire EM, Pearce SWA, Xiao R, et al. Matrix metalloproteinase in abdominal aortic aneurysm and aortic dissection. Pharmaceuticals (Basel), 2019, 12(3).
47.	Wilson WR, Schwalbe EC, Jones JL, et al. Matrix metalloproteinase 8 (neutrophil collagenase) in the pathogenesis of abdominal aortic aneurysm. Br J Surg, 2005, 92(7): 828-833.
48.	Silence J, Lupu F, Collen D, et al. Persistence of atherosclerotic plaque but reduced aneurysm formation in mice with stromelysin-1 (MMP-3) gene inactivation. Arterioscler Thromb Vasc Biol, 2001, 21(9): 1440-1445.
49.	Longo GM, Buda SJ, Fiotta N, et al. MMP-12 has a role in abdominal aortic aneurysms in mice. Surgery, 2005, 137(4): 457-462.
50.	Kilic T, Okuno K, Eguchi S, et al. Disintegrin and metalloproteinases [ADAMs (a disintegrin and metalloproteinase)] and ADAMTSs (ADAMs with a thrombospondin motif)] in aortic aneurysm. Hypertension, 2022, 79(7): 1327-1338.
51.	Ren P, Hughes M, Krishnamoorthy S, et al. Critical role of ADAMTS-4 in the development of sporadic aortic aneurysm and dissection in mice. Sci Rep, 2017, 7(1): 12351.
52.	Dupuis LE, Nelson EL, Hozik B, et al. Adamts5(-/-) mice exhibit altered aggrecan proteolytic profiles that correlate with ascending aortic anomalies. Arterioscler Thromb Vasc Biol, 2019, 39(10): 2067-2081.
53.	Adam DJ, Lee AJ, Ruckley CV, et al. Elevated levels of soluble tumor necrosis factor receptors are associated with increased mortality rates in patients who undergo operation for ruptured abdominal aortic aneurysm. J Vasc Surg, 2000, 31(3): 514-519.
54.	Shen M, Hu M, Fedak PWM, et al. Cell-specific functions of ADAM17 regulate the progression of thoracic aortic aneurysm. Circ Res, 2018, 123(3): 372-388.
55.	Kawai T, Takayanagi T, Forrester SJ, et al. Vascular ADAM17 (a disintegrin and metalloproteinase domain 17) is required for angiotensinⅡ/beta-aminopropionitrile-induced abdominal aortic aneurysm. Hypertension, 2017, 70(5): 959-963.
56.	Jana S, Chute M, Hu M, et al. ADAM (a disintegrin and metalloproteinase) 15 deficiency exacerbates AngⅡ (AngiotensinⅡ)-induced aortic remodeling leading to abdominal aortic aneurysm. Arterioscler Thromb Vasc Biol, 2020, 40(8): 1918-1934.
57.	Jiao T, Yao Y, Zhang B, et al. Role of microRNA-103a targeting ADAM10 in abdominal aortic aneurysm. Biomed Res Int, 2017, 2017: 9645874.
58.	Eskandari MK, Vijungco JD, Flores A, et al. Enhanced abdominal aortic aneurysm in TIMP-1-deficient mice. J Surg Res, 2005, 123(2): 289-293.
59.	Allaire E, Forough R, Clowes M, et al. Local overexpression of TIMP-1 prevents aortic aneurysm degeneration and rupture in a rat model. J Clin Invest, 1998, 102(7): 1413-1420.
60.	Xiong W, Knispel R, Mactaggart J, et al. Effects of tissue inhibitor of metalloproteinase 2 deficiency on aneurysm formation. J Vasc Surg, 2006, 44(5): 1061-1066.
61.	Basu R, Fan D, Kandalam V, et al. Loss of Timp3 gene leads to abdominal aortic aneurysm formation in response to angiotensinⅡ. J Biol Chem, 2012, 287(53): 44083-44096.
62.	Lee MH, Rapti M, Murphy G. Total conversion of tissue inhibitor of metalloproteinase (TIMP) for specific metalloproteinase targeting: Fine-tuning TIMP-4 for optimal inhibition of tumor necrosis factor-alpha-converting enzyme. J Biol Chem, 2005, 280(16): 15967-15975.
63.	Narayanan N, Tyagi N, Shah A, et al. Hyperhomocysteinemia during aortic aneurysm, a plausible role of epigenetics. Int J Physiol Pathophysiol Pharmacol, 2013, 5(1): 32-42.
64.	Barbour JR, Stroud RE, Lowry AS, et al. Temporal disparity in the induction of matrix metalloproteinases and tissue inhibitors of metalloproteinases after thoracic aortic aneurysm formation. J Thorac Cardiovasc Surg, 2006, 132(4): 788-795.

1. Harky A, Sokal PA, Hasan K, et al. The aortic pathologies: How far we understand it and its implications on thoracic aortic surgery. Braz J Cardiovasc Surg, 2021, 36(4): 535-549.
2. Shen YH, LeMaire SA, Webb NR, et al. Aortic aneurysms and dissections series. Arterioscler Thromb Vasc Biol, 2020, 40(3): e37-e46.
3. Koracevic GP. Aortic dissection and aneurysm are hypertensive target organ damages and should be listed in the guidelines. Am J Emerg Med, 2019, 37(2): 365-366.
4. Akin I, Nienaber CA. Prediction of aortic dissection. Heart, 2020, 106(12): 870-871.
5. Golledge J. Abdominal aortic aneurysm: Update on pathogenesis and medical treatments. Nat Rev Cardiol, 2019, 16(4): 225-242.
6. Mammoto A, Matus K, Mammoto T. Extracellular matrix in aging aorta. Front Cell Dev Biol, 2022, 10: 822561.
7. Xu J, Shi GP. Vascular wall extracellular matrix proteins and vascular diseases. Biochim Biophys Acta, 2014, 1842(11): 2106-2119.
8. Yanagisawa H, Wagenseil J. Elastic fibers and biomechanics of the aorta: Insights from mouse studies. Matrix Biol, 2020, 85-86: 160-172.
9. Stepien KL, Bajdak-Rusinek K, Fus-Kujawa A, et al. Role of extracellular matrix and inflammation in abdominal aortic aneurysm. Int J Mol Sci, 2022, 23(19): 1-10.
10. Jana S, Hu M, Shen M, et al. Extracellular matrix, regional heterogeneity of the aorta, and aortic aneurysm. Exp Mol Med, 2019, 51(12): 1-15.
11. Sato F, Seino-Sudo R, Okada M, et al. Lysyl oxidase enhances the deposition of tropoelastin through the catalysis of tropoelastin molecules on the cell surface. Biol Pharm Bull, 2017, 40(10): 1646-1653.
12. Rai P, Robinson L, Davies HA, et al. Is there enough evidence to support the role of glycosaminoglycans and proteoglycans in thoracic aortic aneurysm and dissection? A systematic review. Int J Mol Sci, 2022, 23(16): 1-10.
13. Ghadie NM, St-Pierre JP, Labrosse MR. The contribution of glycosaminoglycans/proteoglycans to aortic mechanics in health and disease: A critical review. IEEE Trans Biomed Eng, 2021, 68(12): 3491-3500.
14. Wight TN. A role for proteoglycans in vascular disease. Matrix Biol, 2018, 71-72: 396-420.
15. Guemann AS, Andrieux J, Petit F, et al. ELN gene triplication responsible for familial supravalvular aortic aneurysm. Cardiol Young, 2015, 25(4): 712-717.
16. Hadj-Rabia S, Callewaert BL, Bourrat E, et al. Twenty patients including 7 probands with autosomal dominant cutis laxa confirm clinical and molecular homogeneity. Orphanet J Rare Dis, 2013, 8: 36.
17. Rodrigues Bento J, Meester J, Luyckx I, et al. The genetics and typical traits of thoracic aortic aneurysm and dissection. Annu Rev Genomics Hum Genet, 2022, 23: 223-253.
18. Gupta PA, Wallis DD, Chin TO, et al. FBN2 mutation associated with manifestations of Marfan syndrome and congenital contractural arachnodactyly. J Med Genet, 2004, 41(5): e56.
19. Carta L, Pereira L, Arteaga-Solis E, et al. Fibrillins 1 and 2 perform partially overlapping functions during aortic development. J Biol Chem, 2006, 281(12): 8016-8023.
20. Dasouki M, Markova D, Garola R, et al. Compound heterozygous mutations in fibulin-4 causing neonatal lethal pulmonary artery occlusion, aortic aneurysm, arachnodactyly, and mild cutis laxa. Am J Med Genet A, 2007, 143A(22): 2635-2641.
21. Wang X, LeMaire SA, Chen L, et al. Decreased expression of fibulin-5 correlates with reduced elastin in thoracic aortic dissection. Surgery, 2005, 138(2): 352-359.
22. Nakamura T, Lozano PR, Ikeda Y, et al. Fibulin-5/DANCE is essential for elastogenesis in vivo. Nature, 2002, 415(6868): 171-175.
23. Huang J, Davis EC, Chapman SL, et al. Fibulin-4 deficiency results in ascending aortic aneurysms: A potential link between abnormal smooth muscle cell phenotype and aneurysm progression. Circ Res, 2010, 106(3): 583-592.
24. Carmo M, Colombo L, Bruno A, et al. Alteration of elastin, collagen and their cross-links in abdominal aortic aneurysms. Eur J Vasc Endovasc Surg, 2002, 23(6): 543-549.
25. Xiong J, Wang SM, Chen LH, et al. Elastic fibers reconstructed using adenovirus-mediated expression of tropoelastin and tested in the elastase model of abdominal aortic aneurysm in rats. J Vasc Surg, 2008, 48(4): 965-973.
26. Isenburg JC, Simionescu DT, Starcher BC, et al. Elastin stabilization for treatment of abdominal aortic aneurysms. Circulation, 2007, 115(13): 1729-1737.
27. Kuivaniemi H, Tromp G, Prockop DJ. Mutations in fibrillar collagens (typesⅠ,Ⅱ,Ⅲ, and Ⅺ), fibril-associated collagen (type Ⅸ), and network-forming collagen (typeⅩ) cause a spectrum of diseases of bone, cartilage, and blood vessels. Hum Mutat, 1997, 9(4): 300-315.
28. Pepin M, Schwarze U, Superti-Furga A, et al. Clinical and genetic features of Ehlers-Danlos syndrome typeⅣ, the vascular type. N Engl J Med, 2000, 342(10): 673-680.
29. Kashtan CE, Segal Y, Flinter F, et al. Aortic abnormalities in males with Alport syndrome. Nephrol Dial Transplant, 2010, 25(11): 3554-3560.
30. Plaisier E, Gribouval O, Alamowitch S, et al. COL4A1 mutations and hereditary angiopathy, nephropathy, aneurysms, and muscle cramps. N Engl J Med, 2007, 357(26): 2687-2695.
31. Landis BJ, Schubert JA, Lai D, et al. Exome sequencing identifies candidate genetic modifiers of syndromic and familial thoracic aortic aneurysm severity. J Cardiovasc Transl Res, 2017, 10(4): 423-432.
32. Rahkonen O, Su M, Hakovirta H, et al. Mice with a deletion in the first intron of the Col1a1 gene develop age-dependent aortic dissection and rupture. Circ Res, 2004, 94(1): 83-90.
33. Smith LB, Hadoke PW, Dyer E, et al. Haploinsufficiency of the murine Col3a1 locus causes aortic dissection: A novel model of the vascular type of Ehlers-Danlos syndrome. Cardiovasc Res, 2011, 90(1): 182-190.
34. Guo DC, Regalado ES, Gong L, et al. LOX mutations predispose to thoracic aortic aneurysms and dissections. Circ Res, 2016, 118(6): 928-934.
35. Lee VS, Halabi CM, Hoffman EP, et al. Loss of function mutation in LOX causes thoracic aortic aneurysm and dissection in humans. Proc Natl Acad Sci U S A, 2016, 113(31): 8759-8764.
36. Cikach FS, Koch CD, Mead TJ, et al. Massive aggrecan and versican accumulation in thoracic aortic aneurysm and dissection. JCI Insight, 2018, 3(5): 1-10.
37. Shen YH, Lu HS, LeMaire SA, et al. Unfolding the story of proteoglycan accumulation in thoracic aortic aneurysm and dissection. Arterioscler Thromb Vasc Biol, 2019, 39(10): 1899-1901.
38. Konig KC, Lahm H, Dressen M, et al. Aggrecan: A new biomarker for acute type A aortic dissection. Sci Rep, 2021, 11(1): 10371.
39. Mattson JM, Turcotte R, Zhang Y. Glycosaminoglycans contribute to extracellular matrix fiber recruitment and arterial wall mechanics. Biomech Model Mechanobiol, 2017, 16(1): 213-225.
40. Schriefl AJ, Collins MJ, Pierce DM, et al. Remodeling of intramural thrombus and collagen in an Ang-Ⅱinfusion ApoE-/- model of dissecting aortic aneurysms. Thromb Res, 2012, 130(3): e139-e146.
41. Longo GM, Xiong W, Greiner TC, et al. Matrix metalloproteinases 2 and 9 work in concert to produce aortic aneurysms. J Clin Invest, 2002, 110(5): 625-632.
42. Li Y, Wang W, Li L, et al. MMPs and ADAMs/ADAMTS inhibition therapy of abdominal aortic aneurysm. Life Sci, 2020, 253: 117659.
43. Hovsepian DM, Ziporin SJ, Sakurai MK, et al. Elevated plasma levels of matrix metalloproteinase-9 in patients with abdominal aortic aneurysms: A circulating marker of degenerative aneurysm disease. J Vasc Interv Radiol, 2000, 11(10): 1345-1352.
44. Shen M, Lee J, Basu R, et al. Divergent roles of matrix metalloproteinase 2 in pathogenesis of thoracic aortic aneurysm. Arterioscler Thromb Vasc Biol, 2015, 35(4): 888-898.
45. Wang X, Khalil RA. Matrix metalloproteinases, vascular remodeling, and vascular disease. Adv Pharmacol, 2018, 81: 241-330.
46. Maguire EM, Pearce SWA, Xiao R, et al. Matrix metalloproteinase in abdominal aortic aneurysm and aortic dissection. Pharmaceuticals (Basel), 2019, 12(3).
47. Wilson WR, Schwalbe EC, Jones JL, et al. Matrix metalloproteinase 8 (neutrophil collagenase) in the pathogenesis of abdominal aortic aneurysm. Br J Surg, 2005, 92(7): 828-833.
48. Silence J, Lupu F, Collen D, et al. Persistence of atherosclerotic plaque but reduced aneurysm formation in mice with stromelysin-1 (MMP-3) gene inactivation. Arterioscler Thromb Vasc Biol, 2001, 21(9): 1440-1445.
49. Longo GM, Buda SJ, Fiotta N, et al. MMP-12 has a role in abdominal aortic aneurysms in mice. Surgery, 2005, 137(4): 457-462.
50. Kilic T, Okuno K, Eguchi S, et al. Disintegrin and metalloproteinases [ADAMs (a disintegrin and metalloproteinase)] and ADAMTSs (ADAMs with a thrombospondin motif)] in aortic aneurysm. Hypertension, 2022, 79(7): 1327-1338.
51. Ren P, Hughes M, Krishnamoorthy S, et al. Critical role of ADAMTS-4 in the development of sporadic aortic aneurysm and dissection in mice. Sci Rep, 2017, 7(1): 12351.
52. Dupuis LE, Nelson EL, Hozik B, et al. Adamts5(-/-) mice exhibit altered aggrecan proteolytic profiles that correlate with ascending aortic anomalies. Arterioscler Thromb Vasc Biol, 2019, 39(10): 2067-2081.
53. Adam DJ, Lee AJ, Ruckley CV, et al. Elevated levels of soluble tumor necrosis factor receptors are associated with increased mortality rates in patients who undergo operation for ruptured abdominal aortic aneurysm. J Vasc Surg, 2000, 31(3): 514-519.
54. Shen M, Hu M, Fedak PWM, et al. Cell-specific functions of ADAM17 regulate the progression of thoracic aortic aneurysm. Circ Res, 2018, 123(3): 372-388.
55. Kawai T, Takayanagi T, Forrester SJ, et al. Vascular ADAM17 (a disintegrin and metalloproteinase domain 17) is required for angiotensinⅡ/beta-aminopropionitrile-induced abdominal aortic aneurysm. Hypertension, 2017, 70(5): 959-963.
56. Jana S, Chute M, Hu M, et al. ADAM (a disintegrin and metalloproteinase) 15 deficiency exacerbates AngⅡ (AngiotensinⅡ)-induced aortic remodeling leading to abdominal aortic aneurysm. Arterioscler Thromb Vasc Biol, 2020, 40(8): 1918-1934.
57. Jiao T, Yao Y, Zhang B, et al. Role of microRNA-103a targeting ADAM10 in abdominal aortic aneurysm. Biomed Res Int, 2017, 2017: 9645874.
58. Eskandari MK, Vijungco JD, Flores A, et al. Enhanced abdominal aortic aneurysm in TIMP-1-deficient mice. J Surg Res, 2005, 123(2): 289-293.
59. Allaire E, Forough R, Clowes M, et al. Local overexpression of TIMP-1 prevents aortic aneurysm degeneration and rupture in a rat model. J Clin Invest, 1998, 102(7): 1413-1420.
60. Xiong W, Knispel R, Mactaggart J, et al. Effects of tissue inhibitor of metalloproteinase 2 deficiency on aneurysm formation. J Vasc Surg, 2006, 44(5): 1061-1066.
61. Basu R, Fan D, Kandalam V, et al. Loss of Timp3 gene leads to abdominal aortic aneurysm formation in response to angiotensinⅡ. J Biol Chem, 2012, 287(53): 44083-44096.
62. Lee MH, Rapti M, Murphy G. Total conversion of tissue inhibitor of metalloproteinase (TIMP) for specific metalloproteinase targeting: Fine-tuning TIMP-4 for optimal inhibition of tumor necrosis factor-alpha-converting enzyme. J Biol Chem, 2005, 280(16): 15967-15975.
63. Narayanan N, Tyagi N, Shah A, et al. Hyperhomocysteinemia during aortic aneurysm, a plausible role of epigenetics. Int J Physiol Pathophysiol Pharmacol, 2013, 5(1): 32-42.
64. Barbour JR, Stroud RE, Lowry AS, et al. Temporal disparity in the induction of matrix metalloproteinases and tissue inhibitors of metalloproteinases after thoracic aortic aneurysm formation. J Thorac Cardiovasc Surg, 2006, 132(4): 788-795.

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