Differences in genetic signaling, and not mechanical properties of the wall, are linked to ascending aortic aneurysms in fibulin-4 knockout mice

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 309, Issue 1, 2015, Pages H103-H113

  Kim, Jungsil ^a   Procknow, Jesse D ^a   Yanagisawa, Hiromi ^b,c   Wagenseil, Jessica E ^a  

^a WASHINGTON UNIVERSITY IN ST LOUIS   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^c UNIVERSITY OF TSUKUBA   (Japan)

Author keywords

Aneurysm; Elastin; Fibulin 4; Gene array; Mechanics

Indexed keywords

COLLAGEN TYPE 1; FIBULIN; FIBULIN 4; METALLOPROTEINASE; NEUTROPHIL COLLAGENASE; UNCLASSIFIED DRUG; ACUTE PHASE PROTEIN; ANKRD1 PROTEIN, MOUSE; CELL SURFACE RECEPTOR; COLLAGEN TYPE 8; CYCLOOXYGENASE 2; EMR1 PROTEIN, MOUSE; EPIREGULIN; EREG PROTEIN, MOUSE; FIBULIN-4; HBEGF PROTEIN, MOUSE; HEPARIN BINDING EPIDERMAL GROWTH FACTOR; MESSENGER RNA; MMP8 PROTEIN, MOUSE; MUSCLE PROTEIN; NUCLEAR PROTEIN; PTGS2 PROTEIN, MOUSE; REPRESSOR PROTEIN; SCLEROPROTEIN; SERINE PROTEINASE INHIBITOR; SERPINA3N PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; AORTA ANEURYSM; ARTICLE; ASCENDING AORTA; CELL PROLIFERATION; CONTROLLED STUDY; DESCENDING AORTA; DISEASE PREDISPOSITION; DOWN REGULATION; GENE EXPRESSION; GENOTYPE; INFLAMMATION; MOUSE; NEWBORN; NONHUMAN; NUCLEOTIDE SEQUENCE; PATHOGENESIS; PHENOTYPE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SMOOTH MUSCLE FIBER; UPREGULATION; ANIMAL; AORTA; CYTOLOGY; ELECTRON MICROSCOPY; GENE EXPRESSION PROFILING; GENETICS; KNOCKOUT MOUSE; METABOLISM; PATHOPHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SMOOTH MUSCLE CELL; THORACIC AORTA; THORACIC AORTA ANEURYSM; ULTRASTRUCTURE; VASCULAR SMOOTH MUSCLE; YOUNG MODULUS;

ACUTE-PHASE PROTEINS; ANIMALS; ANIMALS, NEWBORN; AORTA; AORTA, THORACIC; AORTIC ANEURYSM, THORACIC; COLLAGEN TYPE VIII; CYCLOOXYGENASE 2; ELASTIC MODULUS; EPIREGULIN; EXTRACELLULAR MATRIX PROTEINS; GENE EXPRESSION PROFILING; HEPARIN-BINDING EGF-LIKE GROWTH FACTOR; MATRIX METALLOPROTEINASE 8; MICE; MICE, KNOCKOUT; MICROSCOPY, ELECTRON; MUSCLE PROTEINS; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; NUCLEAR PROTEINS; RECEPTORS, CELL SURFACE; REPRESSOR PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SERPINS; UP-REGULATION;

EID: 84935444758     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00178.2015     Document Type: Article

References (89)

1. Absi TS, Sundt TM, Tung WS, Moon M, Lee JK, Damiano RR, Thompson RW. Altered patterns of gene expression distinguishing ascending aortic aneurysms from abdominal aortic aneurysms: complementary DNA expression profiling in the molecular characterization of aortic disease. J Thorac Cardiovasc Surg 126: 344–357; discission 357, 2003.
2. Adiguzel E, Hou G, Mulholland D, Hopfer U, Fukai N, Olsen B, Bendeck M. Migration and growth are attenuated in vascular smooth muscle cells with type VIII collagen-null alleles. Arterioscler Thromb Vasc Biol 26: 56–61, 2006.
3. Ahimastos AA, Aggarwal A, Savarirayan R, Dart AM, Kingwell BA. A role for plasma transforming growth factor-beta and matrix metallopro-teinases in aortic aneurysm surveillance in Marfan syndrome? Atherosclerosis 209: 211–214, 2010.
4. Amin M, Kunkel AG, Le VP, Wagenseil JE. Effect of storage duration on the mechanical behavior of mouse carotid artery. J Biomech Eng 133: 071007, 2011.
5. Amin M, Le VP, Wagenseil JE. Mechanical testing of mouse carotid arteries: from newborn to adult. J Vis Exp 60: 3733, 2012.
6. Anwar MA, Shalhoub J, Lim CS, Gohel MS, Davies AH. The effect of pressure-induced mechanical stretch on vascular wall differential gene expression. J Vasc Res 49: 463–478, 2012.
7. Besner G, Higashiyama S, Klagsbrun M. Isolation and characterization of a macrophage-derived heparin-binding growth factor. Cell Regul 1: 811–819, 1990.
8. Cheng J, Du J. Mechanical stretch simulates proliferation of venous smooth muscle cells through activation of the insulin-like growth factor-1 receptor. Arterioscler Thromb Vasc Biol 27: 1744–1751, 2007.
9. Cheuk BL, Cheng SW. Differential expression of elastin assembly genes in patients with Stanford Type A aortic dissection using microarray analysis. J Vasc Surg 53: 1071–1078 e1072, 2011.
10. Chiu JJ, Chien S. Effects of disturbed flow on vascular endothelium: pathophysiological basis and clinical perspectives. Physiol Rev 91: 327–387, 2011.
11. Chu W, Burns DK, Swerlick RA, Presky DH. Identification and characterization of a novel cytokine-inducible nuclear protein from human endothelial cells. J Biol Chem 270: 10236–10245, 1995.
12. Chung AW, Au Yeung K, Sandor GG, Judge DP, Dietz HC, van Breemen C. Loss of elastic fiber integrity and reduction of vascular smooth muscle contraction resulting from the upregulated activities of matrix metalloproteinase-2 and -9 in the thoracic aortic aneurysm in Marfan syndrome. Circ Res 101: 512–522, 2007.
13. Chung AW, Yang HH, Radomski MW, van Breemen C. Long-term doxycycline is more effective than atenolol to prevent thoracic aortic aneurysm in marfan syndrome through the inhibition of matrix metallo-proteinase-2 and -9. Circ Res 102: e73–85, 2008.
14. Chuong CJ, Fung YC. On residual stresses in arteries. J Biomech Eng 108: 189–192, 1986.
15. Dasouki M, Markova D, Garola R, Sasaki T, Charbonneau NL, Sakai LY, Chu ML. Compound heterozygous mutations in fibulin-4 causing neonatal lethal pulmonary artery occlusion, aortic aneurysm, arachnodac-tyly, and mild cutis laxa. Am J Med Genet A 143: 2635–2641, 2007.
16. Daugherty A, Cassis LA. Mouse models of abdominal aortic aneurysms. Arterioscler Thromb Vasc Biol 24: 429–434, 2004.
17. Davis EC. Elastic lamina growth in the developing mouse aorta. J Histochem Cytochem 43: 1115–1123, 1995.
18. de Waard V, van Achterberg TA, Beauchamp NJ, Pannekoek H, de Vries CJ. Cardiac ankyrin repeat protein (CARP) expression in human and murine atherosclerotic lesions: activin induces CARP in smooth muscle cells. Arterioscler Thromb Vasc Biol 23: 64–68, 2003.
19. Dietz HC, Cutting GR, Pyeritz RE, Maslen CL, Sakai LY, Corson GM, Puffenberger EG, Hamosh A, Nanthakumar EJ, Curristin SM, Stetten G, Meyers DA, Francomano CA. Marfan syndrome caused by a recurrent de novo missense mutation in the fibrillin gene. Nature 352: 337–339, 1991.
20. Dinardo CL, Venturini G, Zhou EH, Watanabe IS, Campos LC, Dariolli R, da Motta-Leal-Filho JM, Carvalho VM, Cardozo KH, Krieger JE, Alencar AM, Pereira AC. Variation of mechanical properties and quantitative proteomics of VSMC along the arterial tree. Am J Physiol Heart Circ Physiol 306: H505–H516, 2014.
21. Dobrin PB, Mrkvicka R. Failure of elastin or collagen as possible critical connective tissue alterations underlying aneurysmal dilatation. Cardiovasc Surg 2: 484–488, 1994.
22. Faury G, Pezet M, Knutsen RH, Boyle WA, Heximer SP, McLean SE, Minkes RK, Blumer KJ, Kovacs A, Kelly DP, Li DY, Starcher B, Mecham RP. Developmental adaptation of the mouse cardiovascular system to elastin haploinsufficiency. J Clin Invest 112: 1419–1428, 2003.
23. Fonck E, Prod’hom G, Roy S, Augsburger L, Rufenacht DA, Stergio-pulos N. Effect of elastin degradation on carotid wall mechanics as assessed by a constituent-based biomechanical model. Am J Physiol Heart Circ Physiol 292: H2754–H2763, 2007.
24. Freije JM, Diez-Itza I, Balbin M, Sanchez LM, Blasco R, Tolivia J, Lopez-Otin C. Molecular cloning and expression of collagenase-3, a novel human matrix metalloproteinase produced by breast carcinomas. J Biol Chem 269: 16766–16773, 1994.
25. Greenwald SE, Moore JE Jr, Rachev A, Kane TP, Meister JJ. Experimental investigation of the distribution of residual strains in the artery wall. J Biomech Eng 119: 438–444, 1997.
26. Guo DC, Pannu H, Tran-Fadulu V, Papke CL, Yu RK, Avidan N, Bourgeois S, Estrera AL, Safi HJ, Sparks E, Amor D, Ades L, McConnell V, Willoughby CE, Abuelo D, Willing M, Lewis RA, Kim DH, Scherer S, Tung PP, Ahn C, Buja LM, Raman CS, Shete SS, Milewicz DM. Mutations in smooth muscle alpha-actin (ACTA2) lead to thoracic aortic aneurysms and dissections. Nat Genet 39: 1488–1493, 2007.
27. Guo X, Kassab GS. Variation of mechanical properties along the length of the aorta in C57bl/6 mice. Am J Physiol Heart Circ Physiol 285: H2614–H2622, 2003.
28. Guo X, Kono Y, Mattrey R, Kassab GS. Morphometry and strain distribution of the C57BL/6 mouse aorta. Am J Physiol Heart Circ Physiol 283: H1829–H1837, 2002.
29. Habashi JP, Judge DP, Holm TM, Cohn RD, Loeys BL, Cooper TK, Myers L, Klein EC, Liu G, Calvi C, Podowski M, Neptune ER, Halushka MK, Bedja D, Gabrielson K, Rifkin DB, Carta L, Ramirez F, Huso DL, Dietz HC. Losartan, an AT1 antagonist, prevents aortic aneurysm in a mouse model of Marfan syndrome. Science 312: 117–121, 2006.
30. Han HC, Fung YC. Longitudinal strain of canine and porcine aortas. J Biomech 28: 637–641, 1995.
31. Hanada K, Vermeij M, Garinis GA, de Waard MC, Kunen MG, Myers L, Maas A, Duncker DJ, Meijers C, Dietz HC, Kanaar R, Essers J. Perturbations of vascular homeostasis and aortic valve abnormalities in fibulin-4 deficient mice. Circ Res 100: 738–746, 2007.
32. He R, Guo DC, Sun W, Papke CL, Duraisamy S, Estrera AL, Safi HJ, Ahn C, Buja LM, Arnett FC, Zhang J, Geng YJ, Milewicz DM. Characterization of the inflammatory cells in ascending thoracic aortic aneurysms in patients with Marfan syndrome, familial thoracic aortic aneurysms, and sporadic aneurysms. J Thorac Cardiovasc Surg 136: 922–929, 929 e921, 2008.
33. Hou G, Mulholland D, Gronska MA, Bendeck MP. Type VIII collagen stimulates smooth muscle cell migration and matrix metalloproteinase synthesis after arterial injury. Am J Pathol 156: 467–476, 2000.
34. Huang J, Davis EC, Chapman SL, Budatha M, Marmorstein LY, Word RA, Yanagisawa H. Fibulin-4 deficiency results in ascending aortic aneurysms: a potential link between abnormal smooth muscle cell phenotype and aneurysm progression. Circ Res 106: 583–592, 2010.
35. Huang J, Yamashiro Y, Papke CL, Ikeda Y, Lin Y, Patel M, Inagami T, Le VP, Wagenseil JE, Yanagisawa H. Angiotensin-converting enzyme-induced activation of local angiotensin signaling is required for ascending aortic aneurysms in fibulin-4-deficient mice. Sci Transl Med 5: 183ra158, 181–111, 2013.
36. Hucthagowder V, Sausgruber N, Kim KH, Angle B, Marmorstein LY, Urban Z. Fibulin-4: a novel gene for an autosomal recessive cutis laxa syndrome. Am J Hum Genet 78: 1075–1080, 2006.
37. Humphrey JD, Milewicz DM, Tellides G, Schwartz MA. Cell biology. Dysfunctional mechanosensing in aneurysms. Science 344: 477–479, 2014.
38. Inamoto S, Kwartler CS, Lafont AL, Liang YY, Fadulu VT, Du-raisamy S, Willing M, Estrera A, Safi H, Hannibal MC, Carey J, Wiktorowicz J, Tan FK, Feng XH, Pannu H, Milewicz DM. TGFBR2 mutations alter smooth muscle cell phenotype and predispose to thoracic aortic aneurysms and dissections. Cardiovasc Res 88: 520–529, 2010.
39. Isselbacher EM. Thoracic and abdominal aortic aneurysms. Circulation 111: 816–828, 2005.
40. Judge DP, Biery NJ, Keene DR, Geubtner J, Myers L, Huso DL, Sakai LY, Dietz HC. Evidence for a critical contribution of haploinsufficiency in the complex pathogenesis of Marfan syndrome. J Clin Invest 114: 172–181, 2004.
41. Kanai H, Tanaka T, Aihara Y, Takeda S, Kawabata M, Miyazono K, Nagai R, Kurabayashi M. Transforming growth factor-beta/Smads signaling induces transcription of the cell type-restricted ankyrin repeat protein CARP gene through CAGA motif in vascular smooth muscle cells. Circ Res 88: 30–36, 2001.
42. Katora ME, Hollis TM. Regional variation in rat aortic endothelial surface morphology: relationship to regional aortic permeability. Exp Mol Pathol 24: 23–34, 1976.
43. Kim JH, Na CY, Choi SY, Kim HW, Du Kim Y, Kwon JB, Chung MY, Hong JM, Park CB. Integration of gene-expression profiles and pathway analysis in ascending thoracic aortic aneurysms. Ann Vasc Surg 24: 538–549, 2010.
44. Komurasaki T, Toyoda H, Uchida D, Morimoto S. Epiregulin binds to epidermal growth factor receptor and ErbB-4 and induces tyrosine phos-phorylation of epidermal growth factor receptor, ErbB-2, ErbB-3 and ErbB-4. Oncogene 15: 2841–2848, 1997.
45. Koo BH, Kim DS. Factor Xa induces mitogenesis of vascular smooth muscle cells via autocrine production of epiregulin. J Biol Chem 278: 52578–52586, 2003.
46. Le VP, Yamashiro Y, Yanagisawa H, Wagenseil JE. Measuring, reversing, and modeling the mechanical changes due to the absence of Fibulin-4 in mouse arteries. Biomech Model Mechanobiol 13: 1081–1095, 2014.
47. 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 26: 3957–3967, 2007.
48. Li DY, Brooke B, Davis EC, Mecham RP, Sorensen LK, Boak BB, Eichwald E, Keating MT. Elastin is an essential determinant of arterial morphogenesis. Nature 393: 276–280, 1998.
49. Lindsay ME, Dietz HC. The genetic basis of aortic aneurysm. Cold Spring Harb Perspect Med 4: a015909, 2014.
50. Lindsay ME, Schepers D, Bolar NA, Doyle JJ, Gallo E, Fert-Bober J, Kempers MJ, Fishman EK, Chen Y, Myers L, Bjeda D, Oswald G, Elias AF, Levy HP, Anderlid BM, Yang MH, Bongers EM, Timmer-mans J, Braverman AC, Canham N, Mortier GR, Brunner HG, Byers PH, Van Eyk J, Van Laer L, Dietz HC, Loeys BL. Loss-of-function mutations in TGFB2 cause a syndromic presentation of thoracic aortic aneurysm. Nat Genet 44: 922–927, 2012.
51. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2[-delta delta C(T)] method. Methods 25: 402–408, 2001.
52. Lopes J, Adiguzel E, Gu S, Liu SL, Hou G, Heximer S, Assoian RK, Bendeck MP. Type VIII collagen mediates vessel wall remodeling after arterial injury and fibrous cap formation in atherosclerosis. Am J Pathol 182: 2241–2253, 2013.
53. Majesky MW. Developmental basis of vascular smooth muscle diversity. Arterioscler Thromb Vasc Biol 27: 1248–1258, 2007.
54. Matsuki H, Fujimoto N, Iwata K, Knauper V, Okada Y, Hayakawa T. A one-step sandwich enzyme immunoassay for human matrix metallopro-teinase 8 (neutrophil collagenase) using monoclonal antibodies. Clin Chim Acta 244: 129–143, 1996.
55. McLaughlin PJ, Chen Q, Horiguchi M, Starcher BC, Stanton JB, Broekelmann TJ, Marmorstein AD, McKay B, Mecham R, Nakamura T, Marmorstein LY. Targeted disruption of fibulin-4 abolishes elasto-genesis and causes perinatal lethality in mice. Mol Cell Biol 26: 1700–1709, 2006.
56. Miyagawa J, Higashiyama S, Kawata S, Inui Y, Tamura S, Yamamoto K, Nishida M, Nakamura T, Yamashita S, Matsuzawa Y. Localization of heparin-binding EGF-like growth factor in the smooth muscle cells and macrophages of human atherosclerotic plaques. J Clin Invest 95: 404–411, 1995.
57. Moltzer E, te Riet L, Swagemakers SM, van Heijningen PM, Vermeij M, van Veghel R, Bouhuizen AM, van Esch JH, Lankhorst S, Ram-nath NW, de Waard MC, Duncker DJ, van der Spek PJ, Rouwet EV, Danser AH, Essers J. Impaired vascular contractility and aortic wall degeneration in fibulin-4 deficient mice: effect of angiotensin II type 1 (AT1) receptor blockade. PLoS One 6: e23411, 2011.
58. Muller BT, Modlich O, Prisack HB, Bojar H, Schipke JD, Goecke T, Feindt P, Petzold T, Gams E, Muller W, Hort W, Sandmann W. Gene expression profiles in the acutely dissected human aorta. Eur J Vasc Endovasc Surg 24: 356–364, 2002.
59. Nakamura T, Lozano PR, Ikeda Y, Iwanaga Y, Hinek A, Minamisawa S, Cheng CF, Kobuke K, Dalton N, Takada Y, Tashiro K, Ross J Jr, Honjo T, Chien KR. Fibulin-5/DANCE is essential for elastogenesis in vivo. Nature 415: 171–175, 2002.
60. Owens AP, Subramanian V, Moorleghen JJ, Guo Z, McNamara CA, Cassis LA, Daugherty A. Angiotensin II induces a region-specific hyperplasia of the ascending aorta through regulation of inhibitor of differentiation 3. Circ Res 106: 611–619, 2010.
61. Pannu H, Tran-Fadulu V, Papke CL, Scherer S, Liu Y, Presley C, Guo D, Estrera AL, Safi HJ, Brasier AR, Vick GW, Marian AJ, Raman CS, Buja LM, Milewicz DM. MYH11 mutations result in a distinct vascular pathology driven by insulin-like growth factor 1 and angiotensin II. Hum Mol Genet 16: 2453–2462, 2007.
62. 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 17: 218–222, 1997.
63. 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 USA 96: 3819–3823, 1999.
64. Pfaltzgraff ER, Shelton EL, Galindo CL, Nelms BL, Hooper CW, Poole SD, Labosky PA, Bader DM, Reese J. Embryonic domains of the aorta derived from diverse origins exhibit distinct properties that converge into a common phenotype in the adult. J Mol Cell Cardiol 69: 88–96, 2014.
65. Ramnath NW, van de Luijtgaarden KM, van der Pluijm I, van Nimwegen M, van Heijningen PM, Swagemakers SM, van Thiel BS, Ridwan RY, van Vliet N, Vermeij M, Hawinkels LJ, de Munck A, Dzyubachyk O, Meijering E, van der Spek P, Rottier R, Yanagisawa H, Hendriks RW, Kanaar R, Rouwet EV, Kleinjan A, Essers J. Extracellular matrix defects in aneurysmal Fibulin-4 mice predispose to lung emphysema. PLoS One 9: e106054, 2014.
66. Renard M, Holm T, Veith R, Callewaert BL, Ades LC, Baspinar O, Pickart A, Dasouki M, Hoyer J, Rauch A, Trapane P, Earing MG, Coucke PJ, Sakai LY, Dietz HC, De Paepe AM, Loeys BL. Altered TGFbeta signaling and cardiovascular manifestations in patients with autosomal recessive cutis laxa type I caused by fibulin-4 deficiency. Eur J Hum Genet 18: 895–901, 2010.
67. Reynolds CM, Eguchi S, Frank GD, Motley ED. Signaling mechanisms of heparin-binding epidermal growth factor-like growth factor in vascular smooth muscle cells. Hypertension 39: 525–529, 2002.
68. Riese DJ 2nd, Cullum RL. Epiregulin: roles in normal physiology and cancer. Semin Cell Dev Biol 28: 49–56, 2014.
69. Schwill S, Seppelt P, Grunhagen J, Ott CE, Jugold M, Ruhparwar A, Robinson PN, Karck M, Kallenbach K. The fibrillin-1 hypomorphic mgR/mgR murine model of Marfan syndrome shows severe elastolysis in all segments of the aorta. J Vasc Surg 57: 1628–1636, 1636.e1-3, 2013.
70. Serbina NV, Jia T, Hohl TM, Pamer EG. Monocyte-mediated defense against microbial pathogens. Annu Rev Immunol 26: 421–452, 2008.
71. Shi C, Pamer EG. Monocyte recruitment during infection and inflammation. Nat Rev Immunol 11: 762–774, 2011.
72. Shirakata Y, Komurasaki T, Toyoda H, Hanakawa Y, Yamasaki K, Tokumaru S, Sayama K, Hashimoto K. Epiregulin, a novel member of the epidermal growth factor family, is an autocrine growth factor in normal human keratinocytes. J Biol Chem 275: 5748–5753, 2000.
73. Shuttleworth CA. Type VIII collagen. Int J Biochem Cell Biol 29: 1145–1148, 1997.
74. Sibinga NE, Foster LC, Hsieh CM, Perrella MA, Lee WS, Endege WO, Sage EH, Lee ME, Haber E. Collagen VIII is expressed by vascular smooth muscle cells in response to vascular injury. Circ Res 80: 532–541, 1997.
75. Simon LS. Role and regulation of cyclooxygenase-2 during inflammation. Am J Med 106: 37S–42S, 1999.
76. Stacey M, Lin HH, Hilyard KL, Gordon S, McKnight AJ. Human epidermal growth factor (EGF) module-containing mucin-like hormone receptor 3 is a new member of the EGF-TM7 family that recognizes a ligand on human macrophages and activated neutrophils. J Biol Chem 276: 18863–18870, 2001.
77. Takahashi M, Hayashi K, Yoshida K, Ohkawa Y, Komurasaki T, Kitabatake A, Ogawa A, Nishida W, Yano M, Monden M, Sobue K. Epiregulin as a major autocrine/paracrine factor released from ERK- and p38MAPK-activated vascular smooth muscle cells. Circulation 108: 2524–2529, 2003.
78. Takamiya A, Takeda M, Yoshida A, Kiyama H. Expression of serine protease inhibitor 3 in ocular tissues in endotoxin-induced uveitis in rat. Invest Ophthalmol Vis Sci 42: 2427–2433, 2001.
79. Taylor DS, Cheng X, Pawlowski JE, Wallace AR, Ferrer P, Molloy CJ. Epiregulin is a potent vascular smooth muscle cell-derived mitogen induced by angiotensin II, endothelin-1, and thrombin. Proc Natl Acad Sci USA 96: 1633–1638, 1999.
80. Topouzis S, Majesky MW. Smooth muscle lineage diversity in the chick embryo. Two types of aortic smooth muscle cell differ in growth and receptor-mediated transcriptional responses to transforming growth factor-beta. Dev Biol 178: 430–445, 1996.
81. Wagenseil JE, Ciliberto CH, Knutsen RH, Levy MA, Kovacs A, Mecham RP. Reduced vessel elasticity alters cardiovascular structure and function in newborn mice. Circ Res 104: 1217–1224, 2009.
82. Wagenseil JE, Mecham RP. Vascular extracellular matrix and arterial mechanics. Physiol Rev 89: 957–989, 2009.
83. Wagenseil JE, Nerurkar NL, Knutsen RH, Okamoto RJ, Li DY, Mecham RP. Effects of elastin haploinsufficiency on the mechanical behavior of mouse arteries. Am J Physiol Heart Circ Physiol 289: H1209–H1217, 2005.
84. Wan W, Gleason RL. Dysfunction in elastic fiber formation in fibulin-5 null mice abrogates the evolution in mechanical response of carotid arteries during maturation. Am J Physiol Heart Circ Physiol 304: H674– H686, 2013.
85. Wilson WR, Schwalbe EC, Jones JL, Bell PR, Thompson MM. Matrix metalloproteinase 8 (neutrophil collagenase) in the pathogenesis of abdominal aortic aneurysm. Br J Surg 92: 828–833, 2005.
86. Xiong W, Meisinger T, Knispel R, Worth JM, Baxter BT. MMP-2 regulates Erk1/2 phosphorylation and aortic dilatation in Marfan syndrome. Circ Res 110: e92–e101, 2012.
87. Yanagisawa H, Davis EC, Starcher BC, Ouchi T, Yanagisawa M, Richardson JA, Olson EN. Fibulin-5 is an elastin-binding protein essential for elastic fibre development in vivo. Nature 415: 168–171, 2002.
88. Yoshida T, Owens GK. Molecular determinants of vascular smooth muscle cell diversity. Circ Res 96: 280–291, 2005.
89. Zhu L, Vranckx R, Khau Van Kien P, Lalande A, Boisset N, Mathieu F, Wegman M, Glancy L, Gasc JM, Brunotte F, Bruneval P, Wolf JE, Michel JB, Jeunemaitre X. Mutations in myosin heavy chain 11 cause a syndrome associating thoracic aortic aneurysm/aortic dissection and patent ductus arteriosus. Nat Genet 38: 343–349, 2006.