Possible mechanical roles of glycosaminoglycans in thoracic aortic dissection and associations with dysregulated transforming growth factor-β

Journal of Vascular Research

Volumn 50, Issue 1, 2012, Pages 1-10

  Humphrey, J D ^a,b  

^a YALE UNIVERSITY   (United States)

^b Yale University   (United States)

Author keywords

Glycosaminoglycan; Proteoglycan; Stress concentration; Thoracic aneurysm; Transforming growth factor ; Wall strength

Indexed keywords

COLLAGEN; GLYCOSAMINOGLYCAN; PROTEOGLYCAN; TRANSFORMING GROWTH FACTOR BETA;

AORTA DISSECTION; AORTA WALL; GENETICS; HUMAN; PRIORITY JOURNAL; REVIEW; TENSILE STRENGTH; THORACIC AORTA ANEURYSM; THORACIC AORTIC ANEURYSM AND DISSECTION;

ANEURYSM, DISSECTING; ANIMALS; AORTA, THORACIC; AORTIC ANEURYSM, THORACIC; AORTIC RUPTURE; BIOMECHANICS; GLYCOSAMINOGLYCANS; HUMANS; SIGNAL TRANSDUCTION; TENSILE STRENGTH; TRANSFORMING GROWTH FACTOR BETA;

EID: 84866700286     PISSN: 10181172     EISSN: 14230135     Source Type: Journal    
DOI: 10.1159/000342436     Document Type: Review

References (110)

1. Sakalihasan N, Limet R, Defawe OD: Abdominal aortic aneurysm. Lancet 2005; 365: 1577-1589. (Pubitemid 40615407)
2. Socci L, Pennati G, Gastaldi D, Vena P: Modeling and mechanobiology of cerebral aneu-rysms. J Appl Biomat Biomech 2008; 6:63-71.
3. El-Hamamsy I, Yacoub MH: Cellular and molecular mechanisms of thoracic aortic an-eurysms. Nat Rev Cardiol 2009; 6: 771-786.
4. Schlatmann TJ, Becker AE: Pathogenesis of dissecting aneurysm of aorta: comparative histopathologic study of significance of medial changes. Am J Cardiol 1977; 39:21-26. (Pubitemid 8022420)
5. Cattell MA, Hasleton PS, Anderson JC: Gly-cosaminoglycan content is increased in dissecting aneurysms of human thoracic aorta. Clin Chim Acta 1994; 226: 29-46. (Pubitemid 24167301)
6. Borges LF, Touat Z, Leclercq A, Al Haj Zen A, Jou ndeau G, Franc B, Philippe M, Meilhac O, Gutierrez PS, Michel JB: Tissue diffusion and retention of metalloproteinases in ascending aortic aneurysms and dissections. Hum Path 2009; 40: 306-313.
7. Nataatmadja M, West J, West M: Overex-pression of transforming growth factor-beta is associated with increased hyaluronan content and impairment of repair in Marfan syndrome aortic aneurysm. Circulation 2006; 114:I-371-377.
8. Collins MJ, Dev V, Strauss BH, Fedak PWM, Butany J: Variation in the histopathological features of patients with ascending aortic an-eurysms: a study of 111 surgically excised cases. J Clin Pathol 2008; 61: 519-523. (Pubitemid 351518238)
9. Milewicz DM, Gou DC, Fadulu VT, Lafont AL, Papke CL, Inamoto S, Kwartler CS, Pan-nu H: Genetic basis of thoracic aortic aneu-rysms and dissections: focus on smooth muscle cell contractile dysfunction. Annu Rev Genomics Hum Genet 2008; 9: 283-302.
10. Maleszewski JJ, Miller DV, Lu J, Dietz HC, Halushka MK: Histopathologic findings in ascending aortas from individuals with Loeys-Dietz syndrome (LDS). Am J Surg Pathol 2009; 33: 194-201.
11. Jain D, Dietz HC, Oswald GL, Maleszewski JJ, Halushka MK: Causes and histopathology of ascending aortic disease in children and young adults. Cardiovasc Pathol 2011; 20: 15-25.
12. Grond-Ginsbach C, Pjonteck R, Aksay SS, Hyhlik-Durr A, Bockler D, Gross-Weiss-mann ML: Spontaneous arterial dissection: phenotype and molecular pathogenesis. Cell Mol Life Sci 2010; 67:1799-1815.
13. Bode-Janisch S, Schmidt A, Gunther D, Stuhrmann M, Fieguth A: Aortic dissecting aneurysms-histopathological findings. Forensic Sci Int 2011; 214: 13-17.
14. Guo DC, Regalado ES, Minn C, Tran-Fadulu V, Coney J, Cao J, Wang M, Yu RK, Estrera AL, Safi HJ, Shete SS, Milewicz DM: Familial thoracic aneurysms and dissections: identification of a novel locus for stable aneurysms with a low risk for progression to aortic dissection. Circ Cardiovasc Genet 2011; 4: 36-42.
15. Halushka MK: Single gene disorders of the aortic wall. Cardiovasc Pathol 2012; 21: 240-244.
16. Lindsay ME, Dietz HC: Lessons on the pathogenesis of aneurysm from heritable conditions. Nature 2011; 473:308-316.
17. Ilopoulos DC, Kritharis EP, Giagini AT, Pa-padodima SA, Sokolis DP: Ascending thoracic aortic aneurysms associated with compositional remodeling and vessel stiffening but not weakening in age matched subjects. J Thorac Cardiovasc Surg 2009; 137:101-109.
18. Dingemans RP, Teeling P, Lagendijk JH, Becker AE: Extracellular matrix of the human aortic media: an ultrastructural histochemical and immunohistochemical study of the adult aortic media. Anat Record 2000; 258: 1-14. (Pubitemid 30030450)
19. Rhodin JA: Architecture of the vessel wall; in Berne RM (ed): Handbook of Physiology, Section 2. Bethesda, American Physiological Society, 1979, vol 2.
20. Lindeman JH, Ashcroft BA, Beenakker JW, van Es M, Koekkoek NB, Prins FA, Tiele-mans JF, Abdul-Hussien H, Bank RA, Oosterkamp TH: Distinct defects in collagen microarchitecture underlie vessel-wall failure in advanced abdominal aneurysms and aneurysms in Marfan syndrome. Proc Natl Acad Sci USA 2010; 107:862-865.
21. Humphrey JD: Cardiovascular Solid Mechanics: Cells, Tissues, and Organs. New York, Springer, 2002.
22. Humphrey JD: Vascular adaptation and mechanical homeostasis at tissue, cellular, and sub-cellular levels. Cell Biochem Biophys 2008; 50: 53-78.
23. Wagenseil JE, Mecham RP: Vascular extracellular matrix and arterial mechanics. Physiol Rev 2009; 89: 957-989.
24. Rodriguez-Feo JA, Sluijter JPG, Pasterkamp G: Modulation of collagen turnover in cardiovascular disease. Curr Pharmacol Design 2005; 11:2501-2514. (Pubitemid 40872694)
25. Arribas SM, Hinek A, González MC: Elastic fibres and vascular structure in hypertension. Pharmacol Ther 2006; 111:771-791. (Pubitemid 44118433)
26. Van Baardwijk C, Roach MR: Factors in the propagation of aortic dissections in canine thoracic aortas. J Biomech 1987; 20:67-73. (Pubitemid 17000568)
27. Sommer G, Gasser TC, Regitnig P, Auer M, Holzapfel GA: Dissection properties of the human aortic media: an experimental study. J Biomech Eng 2006; 130: 021007.
28. Khoynezhad A, Walot I, Kruse MJ, Rapae T, Donayre CE, White FA: Distribution of inti-momedial tears in patients with type B aortic dissection. J Vasc Surg 2010; 52: 562-568.
29. Wilson SK, Hutchins GM: Aortic dissecting aneurysms: causative factors in 204 subjects. Arch Pathol Lab Med 1982; 106:175-180. (Pubitemid 12135695)
30. Tse KM, Chiu P, Lee HP, Ho P: Investigation of hemodynamics in the development of dissecting aneurysm within patient-specific dissecting aneurismal aortas using computational fluid dynamics (CFD) simulations. J Biomech Eng 2011; 44: 827-836.
31. Matt P, Huso DL, Habashi J, Holm T, Doyle J, Schoenhoff F, Liu G, Black J, van Eyk JE, Deitz HC: Murine model of surgically induced acute aortic dissection type A. J Tho-rac Cardiovasc Surg 2010; 139: 1041-1047.
32. Chung AWY, Yeung KA, Sandor GGS, Judge DP, Dietz HC, van Breeman C: Loss of elastic fiber integrity and reduction of vascular smooth muscle contraction resulting from the upregulated activities of matrix metallo-proteinase-2 and-9 in the thoracic aortic an-eurysm in Marfan syndrome. Circ Res 2007; 101: 512-522. (Pubitemid 47351231)
33. Ferruzzi J, Collins MJ, Yeh AT, Humphrey JD: Mechanical assessment of elastin integrity in fibrillin-1 deficient carotid arteries: implications for Marfan syndrome. Cardio-vasc Res 2011; 92:287-295.
34. Wilson JF, Baek S, Humphrey JD: Importance of initial aortic properties on the evolving regional anisotropy, stiffness and wall thickness of human abdominal aortic aneurysms. J R Soc Interface 2012; 9: 2047-2058.
35. Dietz HC, Loeys B, Carta L, Ramirez F: Recent progress towards a molecular understanding of Marfan syndrome. Am J Med Genet C Semin Med Genet 2005; 139: 4-9. (Pubitemid 41739241)
36. Chaudhry SS, Cain SA, Morgan A, Dallas SL, Shuttleworth A, Kielty CM: Fibrillin-1 regulates the bioavailability of TGF-ß1. J Cell Biol 2007; 176: 355-367.
37. ten Dijke P, Arthur HM: Extracellular control of TGFbeta signaling in vascular development and disease. Nat Rev Molc Cell Biol 2007; 8: 857-869. (Pubitemid 47622560)
38. Inamoto S, Kwartler CS, Lafont AL, Liang YY, Fadulu VT, Duriaswamy 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 2010; 88:520-529.
39. Renard M, Callewaert B, Baetens M, Campens L, MacDermot K, Fryns JP, Bon-duelle M, Dietz HC, Gaspar IM, Cavaco D, Stattin EL, Schrander-Stumpel C, Coucke P, Loeys B, de Paepe A, de Backer J: Novel MYH11 and ACTA2 mutations reveal a role of enhanced TGF-beta signaling in FTAAD. Int J Cardiol 2011, E-pub ahead of print.
40. Ghosh J, Murphy MO, Turner N, Khwaja N, Halka A, Kielty CM, Walker MG: The role of transforming growth factor-beta 1 in the vascular system. Cardiovasc Pathol 2005; 14: 28-36. (Pubitemid 40248430)
41. Ruiz-Ortega M, Rodriguez-Vita J, Sanchez-Lopez E, Carvajal G, Egido J: TGF-beta signaling in vascular fibrosis. Cardiovasc Res 2007; 74:196-206.
42. Wang X, LeMaire SA, Chen L, Shen YH, Gan Y, Bartsch H, Carter SA, Utama B, Ou H, Co-selli JS, Wang XL: Increased collagen deposition and elevated expression of connective tissue growth factor in human thoracic aortic dissection. Circulation 2006; 114:200-205.
43. Theruvath TP, Jones JA, Ikonomidis JS: Matrix metalloproteinases and descending aortic aneurysms: parity, disparity, and switch. J Card Surg 2011; 27: 81-90.
44. Dai J, Losy F, Guinault AM, Pages C, Anegon I, Desgranges P, Becquemin JP, Allaire E: Overexpression of transforming growth factor-beta 1 stabilizes already formed aortic aneurysms: a first approach to induction of functional healing by endovascular gene therapy. Circulation 2005; 112:1008-1015. (Pubitemid 41170269)
45. Frutkin AD, Otsuka G, Otero-Stempien A, Sesti C, Du L, Jaffe M, Dichek HL, Pennington CJ, Edwards DR, Nieves-Cintron M, Minter D, Preusch M, Hu JH, Marie JC, Dichek DA: TGF-beta1 limits plaque growth, stabilizes plaque structure, and prevents aortic dilatation in apolipoprotein E-null mice. Arterio-scler Thromb Vasc Biol 2009; 29: 1251-1257.
46. Maegdefessel L, Azuma J, Toh R, Merk DR Deng A, Chin JT, Raaz U, Schoelmerich AM, Ralesdana A, Leeper NJ, McConnell MV, Dalman RP, Spin JM, Tsao PS: Inhibition of microRNA-29b reduces murine abdominal aortic aneurysm development. J Clin Invest 2012; 122:497-506.
47. Milewicz DM: MicroRNAs, fibrotic remodeling, and aortic aneurysms. J Clin Invest 2012; 122:490-493.
48. Schmierer B, Hill CS: TGFß-Smad signal transduction: molecular specificity and functional flexibility. Nat Rev Mol Cell Biol 2007; 8:970-980.
49. Holm TM, Habashi JP, Doyle JJ, Bedja D, Chen YC, van Erp C, Lindsay ME, Kim D, Schoenhoff F, Cohn RD, Loeys B, Thomas CJ, Patmaik S, Marugan JJ, Judge DP, Dietz HC: Noncanonical TGF-beta signaling contributes to aortic aneurysm progression in Marfan syndrome mice. Science 2011; 332: 358-361.
50. Jones JA, Spinale FG, Ikonomidis JS: Transforming growth factor signaling in thoracic aortic aneurysm development: a paradox in pathogenesis. J Vasc Res 2009; 46:119-137.
51. Ruddy JM, Jones JA, Spinale FG, Ilonomidis JS: Regional heterogeneity within the aorta: relevance to aneurysm disease. J Thorac Cardiovasc Surg 2008; 136: 1123-1130.
52. Majesky MW, Dong XR, Hoglund VJ: Parsing aortic aneurysms: more surprises. Circ Res 2011; 108: 528-530.
53. Thieszen SL, Dalton M, Gadson PF, Patterson E, Rosenquist TH: Embryonic lineage of vascular smooth muscle cells determines responses to collagen matrices and integrin receptor expression. Exp Cell Res 1996; 227: 135-145. (Pubitemid 26293424)
54. Gadson PF, Dalton ML, Patterson E, Svobo-da DD, Hutchinson L, Schram D, Rosenquist TH: Differential response of mesoderm-and neural crest-derived smooth muscle to TGF-beta 1: regulation of c-myb and alpha 1 (I) procollagen genes. Exp Cell Res 1997; 230: 169-180. (Pubitemid 27190637)
55. Merk DR, Chin JT, Dake BA, Maegdefessel L, Miller MO, Kimura N, Tsao RO, Iosef C, Berry GJ, Mohr FW, Spin JM, Alvira CM, Rob-bins RC, Fischbein MP: miR-29b participates in early aneurysm development in Marfan syndrome. Circ Res 2012; 110:312-324.
56. Alberts B, Johnson A, Lewis J, Raff M, Roberts K, Walter P: Molecular Biology of the Cell. New York, Garland Science, 2002.
57. Wight TN: Arterial remodeling in vascular disease: a key role for hyaluronan and versi-can. Front Biosci 2008; 4933-4937. (Pubitemid 351599647)
58. Gupta V, Werdenberg JA, Lawrence BD, Mendez JS, Stephens EH, Grande-Allen KJ: Reversible secretion of glycosaminoglycans and proteoglycans by cyclically stretched valvular cells in 3D culture. Ann Biomed Eng 2008; 36:1092-1103.
59. Zhang G, Chen S, Goldoni S, Calder BW, Simpson HC, Owens RT, McQuillan DJ, Young MF, Iozzo RV, Birk DE: Genetic evidence for the coordinated regulation of collagen fibrillogenesis in the cornea by decorin and biglycan. J Biol Chem 2009; 284:8888-8897.
60. Baker AB: Role of proteoglycans in vascular mechanotransduction; in Kamkin A, Kisele-va I (eds): Mechanosensitivity and Mechano-transduction. Heidelberg, Springer, 2011.
61. Turley EA: Extracellular matrix remodeling: multiple paradigms in vascular diseases. Circ Res 2001; 88:2-4. (Pubitemid 32064073)
62. Heegaard AM, Corsi A, Danielsen CC, Nielsen KL, Jorgensen HL, Riminucci M, Young MF, Bianco P (2007) Biglycan deficiency causes spontaneous aortic dissection and rupture in mice. Circulation 2011; 115: 2731-2738. (Pubitemid 46842789)
63. Dobrin PB, Baker WH, Gley WC: Elastolytic and collagenolytic studies of arteries. Exper-imentia 1984; 41:1040-1042.
64. Powell JT, Lanne T: Through thick and thin collagen fibrils, stress, and aortic rupture: another piece of the jigsaw. Circulation 2007; 115:2687-2688. (Pubitemid 46842783)
65. Reynertson RH, Parmley RT, Roden L, Oparil S: Proteoglycans and hypertension. 1. A biochemical and ultrastructural study of aorta glycosaminoglycans in spontaneously hypertensive rats. Coll Relat Res 1986; 6:77-101.
66. Rasmussen LM, Wolf YG, Ruoslahti E: Vascular smooth muscle cells from injured rat aortas display elevated matrix production associated with transforming growth factor-beta activity. Am J Pathol 1995; 147:1041-1048.
67. Aytekin M, Comhair SAA, de la Motte C, Bandyopadhyay SK, Farver CF, Hascall VC, Erzurum SC, Dweik RA: High levels of hyal-uronan in idiopathic pulmonary arterial hypertension. Am J Physiol 2008; 295:L789-L799.
68. Yang SN, Burch ML, Tannock LR, Evanko S, Osman N, Little PJ: Transforming growth factor-beta regulation of proteoglycan synthesis in vascular smooth muscle: contribution to lipid binding and accelerated atherosclerosis in diabetes. J Diabetes 2010; 2: 233-242.
69. Engle J, Safi HJ, Abbassi O, Iliopoulos DC, Dorsay D, Cartw right J, Weilbaecher D: Mu-copolysaccharidosis presenting as pediatric multiple aortic aneurysm: first reported case. J Vasc Surg 1997; 26: 704-710. (Pubitemid 27459621)
70. Ma Z, Tittiger M, Knutsen RH, Kovacs A, Schaller L, Mecham RP, Ponder KP: Upregu-lation of elasta se proteins in aortic di latation in mucopolysaccharidosis I mice. Mol Genet Metab 2008; 94: 298-304.
71. Tang PCY, Coady MA, Lovoulos C, Dardik A, Aslan M, Elefteriades JA, Tellides G: Hy-perplastic cellular remodeling of the media in ascending thoracic aortic aneurysms. Circulation 2005; 112: 1098-1105. (Pubitemid 41216115)
72. Sluijter JPG, de Kleijn DPV, Pasterkamp G: Vasc u lar remodel i ng a nd protease i nh ibi-tion-bench to bedside. Cardiovasc Res 2006; 69: 595-603.
73. Newby AC: Matrix metalloproteinases regulate migration, proliferation, and death of vascular smooth muscle cells by degrading matrix and non-matrix substances. Cardio-vas Res 2006; 69:614-624. (Pubitemid 43140745)
74. Schonherr E, Jarvelainen HT, Sandell LJ, Wight TN: Effects of platelet-derived growth factor and transforming growth factor-beta I on the synthesis of a large versican-like chondroitin sulfate proteoglycan by arterial smooth muscle cells. J Biol Chem 1991; 266: 17640-17647. (Pubitemid 21907985)
75. Schmidt A, Lorkowski S, Seidler D, Breit-hardt G, Buddecke E: TGF-beta 1 generates specific multicomponent extracellular matrix in human coronary SMC. Eur J Clin Invest 2006; 36:473-482. (Pubitemid 43876127)
76. Lee A, Dillmann WH, McCulloch AD, Vil-larreal FJ: Angiotensin II stimulates the au-tocrine production of transforming growth factor-beta 1 in adult rat cardiac fibroblasts. J Mol Cell Cardiol 1995; 27: 2347-2357.
77. Guo N, Li X, Mann MM, Funderburgh ML, Du Y, Funderburgh JL: Hyaluronan synthesis mediates the fibrotic response of kerato-cytes to transforming growth factor beta. J Biol Chem 2010; 285:32012-32019.
78. Susarla BTS, Laing ED, Yu P, Katagiri Y, Geller HM, Symes AJ: Smad proteins differentially regulate transforming growth factor-beta-mediated induction of chondroitin sulfate proteoglycans. J Neurochem 2011; 119:868-878.
79. Matalon R, Dorfman A: The accumulation of hyaluronic acid in cultured fibroblasts of the Marfan syndrome. Biochem Biophys Res Comm 1968; 32:150-154.
80. Dzau VJ: Tissue angiotensin and pathology of vascular disease: a unifying hypothesis. Hyper tension 2001; 37: 1047-1052. (Pubitemid 32304002)
81. Huang F, Thompson JC, Wilson PG, Aung HH, Rutledge JC, Tannock LR: Angiotensin II increases vascular proteoglycan content preceding and contributing to atherosclero sis development. J Lipid Res 2008; 49:521-530.
82. Nagy N, Melchior-Becker A, Fischer JW: Long-term treatment with the AT1-receptor antagonist telmisartan inhibits biglycan accumulation in murine atherosclerosis. Basic Res Cardiol 2010; 105:29-38.
83. Habashi JP, Judge DP, Holm TM, et al: Losar-tan, an AT1 antagonist, prevents aortic aneu-rysm in a mouse model of Marfan syndrome. Science 2006; 312:117-121.
84. Sobolewski K, Wolanska M, Bankowski E, Gacko M, Glowinski S: Collagen, elastin, and glycosaminoglycans in aortic aneurysms. Acta Biochim Pol 1995; 42: 301-308.
85. Tamarina NA, Grassi MA, Johnson DA, Pearce WH: Proteoglycan gene expression is decreased in abdominal aortic aneurysms. J Surg Res 1998; 74:76-80. (Pubitemid 28272003)
86. Theocharis AD, Karamanos NK: Decreased biglycan expression and differential decorin localization in human abdominal aortic an-eurysms. Atherosclerosis 2002; 165: 221-230. (Pubitemid 35333348)
87. Por terf ild SP, Ca lhoon TB, Weiss HS: Changes in connective tissue colloidal charge density with atherosclerosis and age. Am J Physi-ol 1968; 215:324-329.
88. Azeloglu EU, Albro MB, Thimmappa VA, Ateshian GA, Costa KD: Heterogeneous transmural proteoglycan distribution provides a mechanism for regulating residual stresses in the aorta. Am J Physiol 2008; 294:H1197-H1205. (Pubitemid 351468715)
89. Bian L, Angione SL, Ng KW, Lima EG, Williams DY, Mao DQ, Ateshian GA, Hung CT: Influence of decreasing nutrient path length on the development of engineered cartilage. Osteoarthritis Cartilage 2009; 17: 677-685.
90. Tinoco I, Sauer K, Wang JC, Puglisi JD: Physical Chemistry, Principles and Applications in Biological Sciences. New Jersey, Prentice-Hall, 2002.
91. Maroudas A: Balance between swelling pressure and collagen tension in normal and degenerate cartilage. Nature 1976; 260: 808-809.
92. Chahine NO, Chen FH, Hung CT, Ateshian GA: Direct measurement of osmotic pressure of glycosaminoglycans solutions by membrane osmometry at room temperature. Biophys J 2005; 89:1543-1550. (Pubitemid 41233512)
93. Evanko SP, Johnson PY, Braun KR, Under-hill CB, Dudhia J, Wight TN: Platelet-derived growth factor stimulates the formation of versican-hyaluronan aggregates and peri-cellular matrix expansion in arterial smooth muscle cells. Arch Biochem Biophys 2001; 394: 29-38. (Pubitemid 32948281)
94. Hosoda Y, Iri H: Angiolathyrism. 1. A histo-logical and histochemical study on successive changes of the lathyritic rat aorta. Acta Pathol Jpn 1966; 16:239-252.
95. Lesauskaite V, Tanganelli P, Sassi C, Neri E, DiCiolla F, Ivanoviene L, Epistolato MC, Lalinga AV, Alessandrini C, Spina D: Smoot h muscle cells of the media in the dilatative pathology of ascending thoracic aorta: morphology, immunoreactivity for osteopontin, matrix metalloproteinases, and their inhibitors. Hum Pathol 2001; 32:1003-1011. (Pubitemid 32911325)
96. Nakashima Y, Sueishi K: Alteration of elastic architecture in the lathyritic rat aorta implies the pathogenesis of aortic dissecting aneur ysm. Am J Pathol 1992; 140: 959-969.
97. Bunton TE, Biery J, Myers L, Gayraud B, Ramirez F, Dietz HC: Phenotypic alteration of vascular smooth muscle cells precedes elastolysis in a mouse model of Marfan syndrome. Circ Res 2001; 88: 37-43. (Pubitemid 32064080)
98. Hornebeck W, Emonard H: The cell-elastin-elastase(s) interacting triade directs elastoly-sis. Front Biosci 2011; 16:707-722.
99. Jondeau G, Boutouy r ie P, Lacolley P, Laloux B, Dubourg O, Bourdarias JP, Laurent S: Central pulse pressure is a major determinant of ascending aorta dilatation in Mar-fan sy ndrome. Circu lation 1999; 99: 2677-2681. (Pubitemid 29237456)
100. O'Rourke MF, Nichols WW: Aortic diameter, aortic stiffness, and wave reflection increase with age and isolated systolic hypertension. Hypertension 2005; 45:652-658. (Pubitemid 40418361)
101. Pasta S, Phillippi JA, Gleason TG, Vorp DA: Effect of aneurysm on the mechanical dissection properties of the human ascending thoracic aorta. J Thorac Cardiovasc Surg 2012; 143:460-467.
102. Humphrey JD, Taylor CA: Intracranial and abdominal aortic aneurysms: similarities, differences, and need for a new class of computational models. Annu Rev Biomed Eng 2008; 10:221-246.
103. Beller CJ, Labrosse MR, Thubrikar MJ, Ro-bicsek F: Finite element modeling of the thoracic aorta: including aortic root motion to evaluate risk of aortic dissection. J Med Eng Technol 2008; 32: 167-170. (Pubitemid 351302365)
104. Nathan DP, Xu C, Gorman JH, Fairman RM, Bavaria JE, Gorman RC, Chandran KB, Jackson BM: Pathogenesis of acute aortic dissection: a finite element stress analysis. Ann Thorac Surg 2011; 91:458-464.
105. Khanafer K, Berguer R: Fluid-structure interaction analysis of turbulent pulsatile flow within a layered aortic wall as related to aortic dissection. J Biomech 2009; 42: 2642-2648.
106. Kroner BL, Tolunay HE, Basson CT, Pyeritz RE, Holmes KW, Maslen CL, Milewicz DM, LeMaire SA, Hendershot T, Desvigne-Nickens P, Devereux RB, Dietz HC, Song HK, Ringer D, Mitchell M, Weinsaft JW, Ravekes W, Menashe V, Eagle KA: The national registry of genetically triggered thoracic aortic aneurysms and cardiovascular conditions (GenTAC): results from phase I and scientific opportunities in phase II. Am Heart J 2011; 162: 627-632.
107. Barbour JR, Spinale FG, Ikonomidis JS: Proteinase systems and thoracic aortic an-eur ysm progression. J Surg Res 2007; 139: 292-307. (Pubitemid 46551165)
108. Elefteriades JA, Farkas EA: Thoracic aortic aneurysm: clinically pertinent controversies and uncertainties. J Am Coll Cardiol 2010; 55:841-857.
109. Mayerick C, Carre F, Elefteriades J: Aortic dissection and sport: physiologic and clinical understanding provide an opportunity to save young lives. J Cardiovasc Surg (Torino) 2010; 51: 669-681.
110. Koullias G, Modak R, Tranquilli M, Korkolis DP, Barash P, Elefteriades JA: Mechanical deterioration underlies malignant behavior of aneurysmal human ascending aorta. J Thorac Cardiovasc Surg 2005; 130: 677-683.