Syndromic and non-syndromic aneurysms of the human ascending aorta share activation of the Smad2 pathway

Journal of Pathology

Volumn 218, Issue 1, 2009, Pages 131-142

  Gomez, Delphine ^a,b   Zen, Ayman Al Haj ^a,b   Borges, Luciano F ^c   Philippe, Monique ^a   Gutierrez, Paulo Sampaio ^c   Jondeau, Guillaume ^a,d   Michel, Jean Baptiste ^a   Vranckx, Roger ^a,d  

^a INSERM   (France)

^b UNIVERSITÉ PARIS DESCARTES   (France)

^c UNIVERSITY OF SÃO PAULO   (Brazil)

^d BICHAT HOSPITAL   (France)

Author keywords

Bicuspid aortic valves; Decorin; LTBP 1; Marfan syndrome; PAI 1; Proteoglycans; TGF J

Indexed keywords

LATENT TRANSFORMING GROWTH FACTOR BETA BINDING PROTEIN; LATENT TRANSFORMING GROWTH FACTOR BETA BINDING PROTEIN 1; MESSENGER RNA; SMAD2 PROTEIN; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 2; TRANSFORMING GROWTH FACTOR BETA1; UNCLASSIFIED DRUG;

ADULT; AGED; AORTA ANEURYSM; ARTICLE; ASCENDING AORTA; CLINICAL ARTICLE; CONTROLLED STUDY; HUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION;

EID: 66849131058     PISSN: 00223417     EISSN: 10969896     Source Type: Journal    
DOI: 10.1002/path.2516     Document Type: Article

References (55)

1. Isselbacher EM. Thoracic and abdominal aortic aneurysms. Circulation 2005;111:816-828.
2. Touat Z, Lepage L, Ollivier V, Nataf P, Hvass U, Labreuche J, et al. Dilation-dependent activation of platelets and prothrombin in human thoracic ascending aortic aneurysm. Arterioscler Thromb Vasc Biol 2008;28:940-946.
3. Mizuguchi T, Collod-Beroud G, Akiyama T, Abifadel M, Harada N, Morisaki T, et al. Heterozygous TGFBR2 mutations in Marfan syndrome. Nature Genet 2004;36:855-860.
4. Loeys BL, Chen J, Neptune ER, Judge DP, Podowski M, Holm T, et al. A syndrome of altered cardiovascular, craniofacial, neurocognitive and skeletal development caused by mutations in TGFBR1 or TGFBR2. Nature Genet 2005;37:275-281.
5. Loeys BL, Schwarze U, Holm T, Callewaert BL, Thomas GH, Pannu H, et al. Aneurysm syndromes caused by mutations in the TGF-beta receptor. N Engl J Med 2006;355:788-798.
6. Robinson PN, Arteaga-Solis E, Baldock C, Collod-Beroud G, Booms P, De Paepe A, et al. The molecular genetics of Marfan syndrome and related disorders. JMed Genet 2006;43:769-787.
7. Zhu L, Vranckx R, Khau Van Kien P, Lalande A, Boisset N, Mathieu F, et al. Mutations in myosin heavy chain 11 cause a syndrome associating thoracic aortic aneurysm/aortic dissection and patent ductus arteriosus. Nature Genet 2006;38:343-349.
8. Guo DC, Pannu H, Tran-Fadulu V, Papke CL, Yu RK, Avidan N, et al. Mutations in smooth muscle alpha-actin (ACTA2) lead to thoracic aortic aneurysms and dissections. Nature Genet 2007;39:1488-1493.
9. Coucke PJ, Willaert A, Wessels MW, Callewaert B, Zoppi N, De Backer J, et al. Mutations in the facilitative glucose transporter GLUT10 alter angiogenesis and cause arterial tortuosity syndrome. Nature Genet 2006;38:452-457.
10. Roos-Hesselink JW, Scholzel BE, Heijdra RJ, Spitaels SE, Meij- boom FJ, Boersma E, et al. Aortic valve and aortic arch pathology after coarctation repair. Heart 2003;89:1074-1077.
11. Klein DG. Thoracic aortic aneurysms. J Cardiovasc Nurs 2005;20:245 - 250.
12. Borges LF, Touat Z, Leclercq A, Al Haj Zen A, Jondeau G, Franc B, et al. Tissue diffusion and retention ofmetalloproteinases in ascending aortic aneurysms and dissections. Hum Pathol 2008; Oct 28 [Epub ahead of print].
13. 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.
14. de Figueiredo Borges L, Jaldin RG, Dias RR, Stolf NA, Michel JB, Gutierrez PS. Collagen is reduced and disrupted in human aneurysms and dissections of ascending aorta. Hum Pathol 2008;39:437-443.
15. Klima T, Spjut HJ, Coelho A, Gray AG, Wukasch DC, Reul GJ Jr, et al. The morphology of ascending aortic aneurysms. Hum Pathol 1983;14:810-817.
16. Bonderman D, Gharehbaghi-Schnell E, Wollenek G, Maurer G, Baumgartner H, Lang IM. Mechanisms underlying aortic dilatation in congenital aortic valve malformation. Circulation 1999;99:2138-2143.
17. Bonyadi M, Rusholme SA, Cousins FM, Su HC, Biron CA, Farrall M, et al. Mapping of a major genetic modifier of embryonic lethality in TGF beta 1 knockout mice. Nature Genet 1997;15:207-211.
18. Owens GK, Wise G. Regulation of differentiation/maturation in vascular smooth muscle cells by hormones and growth factors. Agents Actions Suppl 1997;48:3-24.
19. Cordenonsi M, Dupont S, Maretto S, Insinga A, Imbriano C, Piccolo S. Links between tumor suppressors: p53 is required for TGF-beta gene responses by cooperating with Smads. Cell 2003;113:301-314.
20. Derynck R, Zhang YE. Smad-dependent and Smad-independent pathways in TGF-beta family signalling. Nature 2003;425:577-584.
21. Shi Y, Massague J. Mechanisms of TGF-beta signaling from cell membrane to the nucleus. Cell 2003;113:685-700.
22. Ignotz RA, Massague J. Transforming growth factor-beta stimulates the expression of fibronectin and collagen and their incorporation into the extracellular matrix. JBiolChem 1986;261:4337-4345.
23. Ma C, Tarnuzzer RW, Chegini N. Expression of matrix metallo- proteinases and tissue inhibitor of matrix metalloproteinases in mesothelial cells and their regulation by transforming growth factor-beta1. Wound Repair Regen 1999;7:477-485.
24. Dong C, Zhu S, Wang T, Yoon W, Goldschmidt-Clermont PJ. Upregulation of PAI-1 is mediated through TGF-beta/Smad pathway in transplant arteriopathy. J Heart Lung Transplant 2002;21:999-1008.
25. Oklu R, Hesketh R. The latent transforming growth factor beta binding protein (LTBP) family. Biochem J 2000;352:601-610.
26. Isogai Z, Ono RN, Ushiro S, Keene DR, Chen Y, Mazzieri R, et al. Latent transforming growth factor beta-binding protein 1 interacts with fibrillin and is a microfibril-associated protein. J Biol Chem 2003;278:2750-2757.
27. ten Dijke P, Arthur HM. Extracellular control of TGFbeta signalling in vascular development and disease. Nature Rev Mol Cell Biol 2007;8:857-869.
28. Neptune ER, Frischmeyer PA, Arking DE, Myers L, Bunton TE, Gayraud B, et al. Dysregulation of TGF-beta activation contributes to pathogenesis in Marfan syndrome. Nature Genet 2003;33:407-411.
29. Habashi JP, Judge DP, Holm TM, Cohn RD, Loeys BL, Cooper TK, et al. Losartan, an AT1 antagonist, prevents aortic aneurysm in a mouse model of Marfan syndrome. Science 2006;312:117-121.
30. 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.
31. Delbosc S, Haloui M, Louedec L, Dupuis M, Cubizolles M, Podust VN, et al. Proteomic analysis permits the identification of new biomarkers of arterial wall remodeling in hypertension. Mol Med 2008;14:383-394.
32. Moustakas A, Souchelnytskyi S, Heldin CH. Smad regulation in TGF-beta signal transduction. J Cell Sci 2001;114:4359-4369.
33. Owens GK. Regulation of differentiation of vascular smooth muscle cells. Physiol Rev 1995;75:487-517.
34. Sinha S, Hoofnagle MH, Kingston PA, McCanna ME, Owens GK. Transforming growth factor-beta1 signaling contributes to development of smooth muscle cells from embryonic stem cells. Am J Physiol Cell Physiol 2004;287: C1560-C1568.
35. O'Rourke MF, Nichols WW. Aortic diameter, aortic stiffness, and wave reflection increase with age and isolated systolic hypertension. Hypertension 2005;45:652-658.
36. Taipale J, Saharinen J, Hedman K, Keski-Oja J. Latent transforming growth factor-beta 1 and its binding protein are components of extracellular matrix microfibrils. J Histochem Cytochem 1996;:875-88944
37. DellaCorte A, De Santo LS, Montagnani S, Quarto C, Romano G, Amarelli C, et al. Spatial patterns of matrix protein expression in dilated ascending aorta with aortic regurgitation: congenital bicuspid valve versus Marfan's syndrome. J Heart Valve Dis 2006;15:20-7; discussion 27.
38. Kinsella MG, Bressler SL, Wight TN. The regulated synthesis of versican, decorin, and biglycan: extracellular matrix proteoglycans that influence cellular phenotype. Crit Rev Eukaryot Gene Expr 2004;14:203-234.
39. Yamaguchi Y, Mann DM, Ruoslahti E. Negative regulation of transforming growth factor-beta by the proteoglycan decorin. Nature 1990;346:281-284.
40. Trask TM, Trask BC, Ritty TM, Abrams WR, Rosenbloom J, Mecham RP. Interaction of tropoelastin with the amino-terminal domains of fibrillin-1 and fibrillin-2 suggests a role for the fibrillins in elastic fiber assembly. JBiolChem 2000;275:24400-24406.
41. Kaartinen V, Warburton D. Fibrillin controls TGF-beta activation. Nature Genet 2003;33:331-332.
42. Dai J, Losy F, Guinault AM, Pages C, Anegon I, Desgranges P, et al. Overexpression of transforming growth factor-beta1 stabilizes already-formed aortic aneurysms: a first approach to induction of functional healing by endovascular gene therapy. Circulation 2005;112:1008- 1015.
43. Kamada Y, Tamura S, Kiso S, Fukui K, Doi Y, Ito N, et al. Angiotensin II stimulates the nuclear translocation of Smad2 and induces PAI-1 mRNA in rat hepatic stellate cells. Hepatol Res 2003;25:296-305.
44. Rodriguez-Vita J, Sanchez-Lopez E, Esteban V, Ruperez M, Egido J, Ruiz-Ortega M. Angiotensin II activates the Smad pathway in vascular smooth muscle cells by a transforming growth factor-beta-independent mechanism. Circulation 2005;111:2509-2517.
45. Milewicz DM, Guo DC, Tran-Fadulu V, Lafont AL, Papke CL, Inamoto S, et al. Genetic basis of thoracic aortic aneurysms and dissections: focus on smooth muscle cell contractile dysfunction. Annu Rev Genomics Hum Genet 2008;9:283-302.
46. Boyum J, Fellinger EK, Schmoker JD, Trombley L, McPart- land K, Ittleman FP, et al. Matrix metalloproteinase activity in thoracic aortic aneurysms associated with bicuspid and tricuspid aortic valves. J Thorac Cardiovasc Surg 2004;127:686-691.
47. Koullias GJ, Ravichandran P, Korkolis DP, Rimm DL, Elefteri- ades JA. Increased tissue microarray matrix metalloproteinase expression favors proteolysis in thoracic aortic aneurysms and dissections. Ann Thorac Surg 2004;78:2106-2110; discussion 2110-2111.
48. Kim ES, Kim MS, Moon A. TGF-beta-induced upregulation of MMP-2 and MMP-9 depends on p38 MAPK, but not ERK signaling in MCF10A human breast epithelial cells. Int J Oncol 2004;25:1375-1382.
49. Owens GK, Kumar MS, Wamhoff BR. Molecular regulation of vascular smooth muscle cell differentiation in development and disease. Physiol Rev 2004;84:767-801.
50. Aikawa M, Sivam PN, Kuro-o M, Kimura K, Nakahara K, Takewaki S, et al. Human smooth muscle myosin heavy chain isoforms as molecular markers for vascular development and atherosclerosis. Circ Res 1993;73:1000- 1012.
51. UedaM, Becker AE, Naruko T, Kojima A. Smooth muscle cell de-differentiation is a fundamental change preceding wound healing after percutaneous transluminal coronary angioplasty in humans. Coron Artery Dis 1995;6:71-81.
52. Bergwerff M, Verberne ME, DeRuiter MC, Poelmann RE, Gittenberger-de Groot AC. Neural crest cell contribution to the developing circulatory system: implications for vascular morphology? CircRes 1998;82:221-231.
53. 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 transcrip- tional responses to transforming growth factor-beta. Dev Biol 1996;178:430-445.
54. Karnik SK, Brooke BS, Bayes-Genis A, Sorensen L, Wythe JD, Schwartz RS, et al. A critical role for elastin signaling in vascular morphogenesis and disease. Development 2003;130:411-423.
55. 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.