Aortopathy in Marfan syndrome: An update

Cardiovascular Pathology

Volumn 23, Issue 5, 2014, Pages 261-266

  Romaniello, Federico ^a   Mazzaglia, Donatella ^a   Pellegrino, Antonio ^a   Grego, Susanna ^a   Fiorito, Roberto ^a   Ferlosio, Amedeo ^a   Chiariello, Luigi ^a   Orlandi, Augusto ^a  

^a UNIVERSITY OF ROME TOR VERGATA   (Italy)

Author keywords

Erk; Fibrillin 1; Marfan syndrome; Matrix metalloproteinases; Oxidative stress; Smooth muscle cells; TGF ; Thoracic aortic aneurysm

Indexed keywords

FIBRILLIN 1; GLYCOSAMINOGLYCAN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; REACTIVE OXYGEN METABOLITE; TRANSFORMING GROWTH FACTOR BETA;

AORTA ANEURYSM; AORTA DISEASE; BASOPHIL; CARDIOVASCULAR MALFORMATION; CLINICAL FEATURE; ENZYME SYNTHESIS; HISTOLOGY; HUMAN; MARFAN SYNDROME; MARFAN SYNDROME AORTOPATHY; MICROSCOPY; OXIDATIVE STRESS; PHENOTYPE; PROTEIN EXPRESSION; REVIEW; SIGNAL TRANSDUCTION; SMOOTH MUSCLE FIBER; TRANSMISSION ELECTRON MICROSCOPY; AORTIC DISEASES; COMPLICATION; PATHOLOGY; PATHOPHYSIOLOGY;

AORTIC DISEASES; HUMANS; MARFAN SYNDROME;

EID: 84908485587     PISSN: 10548807     EISSN: 18791336     Source Type: Journal    
DOI: 10.1016/j.carpath.2014.04.007     Document Type: Review

References (86)

1. Van de Velde S, Fillman R, Yandow S. Protrusio acetabuli in Marfan syndrome. History, diagnosis, and treatment. J Bone Joint Surg Am 2006;88:639-46.
2. Judge DP, Dietz HC. Marfan's syndrome. Lancet 2005;366:1965-76.
3. Faivre L, Collod-Beroud G, Loeys BL, Child A, Binquet C, Gautier E, et al. Effect of mutation type and location on clinical outcome in 1,013 probands with Marfan syndrome or related phenotypes and FBN1 mutations: an international study. Am J Hum Genet 2007;81:454-66.
4. De Paepe A, Devereux RB, Dietz HC, Hennekam RC, Pyeritz RE. Revised diagnostic criteria for the Marfan syndrome. Am J Med Genet 1996;62:417-26.
5. Loeys B, Nuytinck L, Delvaux I, De Bie S, De Paepe A. Genotype and phenotype analysis of 171 patients referred for molecular study of the fibrillin-1 gene FBN1 because of suspected Marfan syndrome. Arch Intern Med 2001;161:2447-54.
6. Loeys BL, Dietz HC, Braverman AC, Callewaert BL, De Backer J, Devereux RB, et al. The revised Ghent nosology for the Marfan syndrome. J Med Genet 2010;47:476-85.
7. Groenink M, den Hartog AW, Franken R, Radonic T, de Waard V, Timmermans J, et al. Losartan reduces aortic dilatation rate in adults with Marfan syndrome: a randomized controlled trial. Eur Heart J 2013;34:3491-500.
8. Finkbohner R, Johnston D, Crawford ES, Coselli J, Milewicz DM. Marfan syndrome. Long-term survival and complications after aortic aneurysm repair. Circulation 1995;91:728-33.
9. Silverman DI, Burton KJ, Gray J, Bosner MS, Kouchoukos NT, Roman MJ, et al. Life expectancy in the Marfan syndrome. Am J Cardiol 1995;75:157-60.
10. Lemaire SA, McDonald ML, Guo DC, Russell L, Miller CC, Johnson RJ, et al. Genome-wide association study identifies a susceptibility locus for thoracic aortic aneurysms and aortic dissections spanning FBN1 at 15q21.1. Nat Genet 2011;43:996-1000.
11. Gersony DR, McClaughlin MA, Jin Z, Gersony WM. The effect of beta-blocker therapy on clinical outcome in patients with Marfan's syndrome: a meta-analysis. Int J Cardiol 2007;114:303-8.
12. 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. J Med Genet 2006;43:769-87.
13. Canadas V, Vilacosta I, Bruna I, Fuster V. Marfan syndrome. Part 1: pathophysiology and diagnosis. Nat Rev Cardiol 2010;7:256-65.
14. D'Arrigo C, Burl S, Withers AP, Dobson H, Black C, Boxer M. TGF-beta1 binding protein-like modules of fibrillin-1 and -2 mediate integrin-dependent cell adhesion. Connect Tissue Res 1998;37:29-51.
15. Reinhardt DP, Keene DR, Corson GM, Poschl E, Bachinger HP, Gambee JE, et al. Fibrillin-1: organization in microfibrils and structural properties. J Mol Biol 1996;258:104-16.
16. Lonnqvist L, Reinhardt D, Sakai L, Peltonen L. Evidence for furin-type activity-mediated C-terminal processing of profibrillin-1 and interference in the processing by certain mutations. Hum Mol Genet 1998;7:2039-44.
17. Corson GM, Chalberg SC, Dietz HC, Charbonneau NL, Sakai LY. Fibrillin binds calcium and is coded by cDNAs that reveal a multidomain structure and alternatively spliced exons at the 5′ end. Genomics 1993;17:476-84.
18. Pereira L, D'Alessio M, Ramirez F, Lynch JR, Sykes B, Pangilinan T, et al. Genomic organization of the sequence coding for fibrillin, the defective gene product in Marfan syndrome. Hum Mol Genet 1993;2:961-8.
19. Piha-Gossack A, Sossin W, Reinhardt DP. The evolution of extracellular fibrillins and their functional domains. PLoS One 2012;7:1-13.
20. Dong J, Bu J, Du W, Li Y, Jia Y, Li J, et al. A new novel mutation in FBN1 causes autosomal dominant Marfan syndrome in a Chinese family. Mol Vis 2012;18:81-6.
21. Collod-Beroud G, Beroud C, Ades L, Black C, Boxer M, Brock DJ, et al. Marfan database (third edition): new mutations and new routines for the software. Nucleic Acids Res 1998;26:229-33.
22. Halliday D, Hutchinson S, Kettle S, Firth H, Wordsworth P, Handford PA. Molecular analysis of eight mutations in FBN1. Hum Genet 1999;105:587-97.
23. Liu W, Qian C, Comeau K, Brenn T, Furthmayr H, Francke U. Mutant fibrillin-1 monomers lacking EGF-like domains disrupt microfibril assembly and cause severe Marfan syndrome. Hum Mol Genet 1996;5:1581-7.
24. Tiecke F, Katzke S, Booms P, Robinson PN, Neumann L, Godfrey M, et al. Classic, atypically severe and neonatal Marfan syndrome: twelve mutations and genotype-phenotype correlations in FBN1 exons 24-40. Eur J Hum Genet 2001;9:13-21.
25. Hartog AW, Franken R, Zwinderman AH, Groenink M, Mulder BJ. Current and future pharmacological treatment strategies with regard to aortic disease in Marfan syndrome. Expert Opin Pharmacother 2012;13:647-62.
26. Milewicz DM, Michael K, Fisher N, Coselli JS, Markello T, Biddinger A. Fibrillin-1 (FBN1) mutations in patients with thoracic aortic aneurysms. Circulation 1996;94:2708-11.
27. Fedak PW, de Sa MP, Verma S, Nili N, Kazemian P, Butany J, et al. Vascular matrix remodeling in patients with bicuspid aortic valve malformations: implications for aortic dilatation. J Thorac Cardiovasc Surg 2003;126:797-806.
28. Rybczynski M, Mir TS, Sheikhzadeh S, Bernhardt AM, Schad C, Treede H, et al. Frequency and age-related course of mitral valve dysfunction in the Marfan syndrome. Am J Cardiol 2010;106:1048-53.
29. Brautbar A, LeMaire SA, Franco LM, Coselli JS, Milewicz DM, Belmont JW. FBN1 mutations in patients with descending thoracic aortic dissections. Am J Med Genet A 2010;152A:413-6.
30. Detaint D, Aegerter P, Tubach F, Hoffman I, Plauchu H, Dulac Y, et al. Rationale and design of a randomized clinical trial (Marfan Sartan) of angiotensin II receptor blocker therapy versus placebo in individuals with Marfan syndrome. Arch Cardiovasc Dis 2010;103:317-25.
31. Hayward C, Porteous ME, Brock DJ. A novel mutation in the fibrillin gene (FBN1) in familial arachnodactyly. Mol Cell Probes 1994;8:325-7.
32. Faivre L, Dollfus H, Lyonnet S, Alembik Y, Megarbane A, Samples J, et al. Clinical homogeneity and genetic heterogeneity in Weill-Marchesani syndrome. Am J Med Genet A 2003;123A:204-7.
33. Ha HI, Seo JB, Lee SH, Kang JW, Goo HW, Lim TH, et al. Imaging of Marfan syndrome: multisystemic manifestations. Radiographics 2007;27:989-1004.
34. Chandra A, Ekwalla V, Child A, Charteris D. Prevalence of ectopia lentis and retinal detachment in Marfan syndrome. Acta Ophthalmol 2014;92:e82-3.
35. Fattori R, Nienaber CA, Descovich B, Ambrosetto P, Reggiani LB, Pepe G, et al. Importance of dural ectasia in phenotypic assessment of Marfan's syndrome. Lancet 1999;354:910-3.
36. Murdoch JL, Walker BA, Halpern BL, Kuzma JW, McKusick VA. Life expectancy and causes of death in the Marfan syndrome. N Engl J Med 1972;286:804-8.
37. Basso C, Frescura C, Corrado D, Muriago M, Angelini A, Daliento L, et al. Congenital heart disease and sudden death in the young. Hum Pathol 1995;26:1065-72.
38. Vaidyanathan B. Role of beta-blockers in Marfan's syndrome and bicuspid aortic valve: a time for re-appraisal. Ann Pediatr Cardiol 2008;1:149-52.
39. Davies RR, Goldstein LJ, Coady MA, Tittle SL, Rizzo JA, Kopf GS, et al. Yearly rupture or dissection rates for thoracic aortic aneurysms: simple prediction based on size. Ann Thorac Surg 2002;73:17-27.
40. Gott VL, Greene PS, Alejo DE, Cameron DE, Naftel DC, Miller DC, et al. Replacement of the aortic root in patients with Marfan's syndrome. N Engl J Med 1999;340:1307-13.
41. Stanley P, Roebuck D, Barboza A. Takayusu's arteritis in children. Tech Vasc Interv Radiol 2003;6:158-68.
42. Pyeritz RE. Marfan syndrome and related disorders. Ann Thorac Surg 2008;86:335-6.
43. Sheppard MN. Aetiology of sudden cardiac death in sport: a histopathologist's perspective. Br J Sports Med 2012;46(Suppl 1):i15-21.
44. Grego S, Nardi P, Gislao V, Nicolo F, D'Annolfo A, Marcucci R, et al. The new 2010 Ghent criteria for the indication to surgical treatment of patients affected by Marfan syndrome. Experience of a single cardiac surgery center. G Ital Cardiol (Rome) 2013;14:548-54.
45. Baumgartner H, Bonhoeffer P, De Groot NM, de Haan F, Dean field JE, Galie N, et al. ESC Guidelines for the management of grown-up congenital heart disease (new version 2010). Eur Heart J 2010;31:2915-57.
46. Dormand H, Mohiaddin RH. Cardiovascular magnetic resonance in Marfan syndrome. J Cardiovasc Magn Reson 2013;15:33.
47. Humphrey JD. Possible mechanical roles of glycosaminoglycans in thoracic aortic dissection and associations with dysregulated transforming growth factor-beta. J Vasc Res 2013;50:1-10.
48. Orlandi A, Mauriello A, Marino B, Spagnoli LG. Age-related modifications of aorta and coronaries in the rabbit: a morphological and morphometrical assessment. Arch Gerontol Geriatr 1993;17:37-53.
49. Spagnoli LG, Orlandi A, Mauriello A, Santeusanio G, de Angelis C, Lucreziotti R, et al. Aging and atherosclerosis in the rabbit. 1. Distribution, prevalence and morphology of atherosclerotic lesions. Atherosclerosis 1991;89:11-24.
50. Moritz AR. Medionecrosis Aortae Idiopathica Cystica. Am J Pathol 1932;8:717-34.
51. Nollen GJ, Westerhof BE, Groenink M, Osnabrugge A, van der Wall EE, Mulder BJ. Aortic pressure-area relation in Marfan patients with and without beta blocking agents: a new non-invasive approach. Heart 2004;90:314-8.
52. Orlandi A, Marcellini M, Spagnoli LG. Aging in fluences development and progression of early aortic atherosclerotic lesions in cholesterol-fed rabbits. Arterioscler Thromb Vasc Biol 2000;20:1123-36.
53. McGettrick AJ, Knott V, Willis A, Handford PA. Molecular effects of calcium binding mutations in Marfan syndrome depend on domain context. Hum Mol Genet 2000;9:1987-94.
54. Whiteman P, Smallridge RS, Knott V, Cordle JJ, Downing AK, Handford PA. A G1127S change in calcium-binding epidermal growth factor-like domain 13 of human fibrillin-1 causes short range conformational effects. J Biol Chem 2001;276:17156-62.
55. Vollbrandt T, Tiedemann K, El-Hallous E, Lin G, Brinckmann J, John H, et al. Consequences of cysteine mutations in calcium-binding epidermal growth factor modules of fibrillin-1. J Biol Chem 2004;279:32924-31.
56. 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;139C:4-9.
57. Kanfi Y, Shalman R, Peshti V, Pilosof SN, Gozlan YM, Pearson KJ, et al. Regulation of SIRT6 protein levels by nutrient availability. FEBS Lett 2008;582:543-8.
58. Schacke W, Beck KF, Pfeilschifter J, Koch F, Hattenbach LO. Modulation of tissue plasminogen activator and plasminogen activator inhibitor-1 by transforming growth factor-beta in human retinal glial cells. Invest Ophthalmol Vis Sci 2002;43:2799-805.
59. Dingemans KP, Teeling P, van der Wal AC, Becker AE. Ultrastructural pathology of aortic dissections in patients with Marfan syndrome: comparison with dissections in patients without Marfan syndrome. Cardiovasc Pathol 2006;15:203-12.
60. Bunton TE, Biery NJ, 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.
61. Orlandi A, Ehrlich HP, Ropraz P, Spagnoli LG, Gabbiani G. Rat aortic smooth muscle cells isolated from different layers and at different times after endothelial denudation show distinct biological features in vitro. Arterioscler Thromb 1994;14:982-9.
62. Orlandi A, Ropraz P, Gabbiani G. Proliferative activity and alpha-smooth muscle actin expression in cultured rat aortic smooth muscle cells are differently modulated by transforming growth factor-beta 1 and heparin. Exp Cell Res 1994;214:528-36.
63. Nataatmadja M, West M, West J, Summers K, Walker P, Nagata M, et al. Abnormal extracellular matrix protein transport associated with increased apoptosis of vascular smooth muscle cells in marfan syndrome and bicuspid aortic valve thoracic aortic aneurysm. Circulation 2003;108(Suppl 1):Ii329-34.
64. Massague J. TGF-beta signal transduction. Annu Rev Biochem 1998;67:753-91.
65. 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;278:2750-7.
66. Chaudhry SS, Cain SA, Morgan A, Dallas SL, Shuttleworth CA, Kielty CM. Fibrillin-1 regulates the bioavailability of TGFbeta1. J Cell Biol 2007;176:355-67.
67. Freimuth J, Clermont FF, Huang X, DeSapio A, Tokuyasu TA, Sheppard D, et al. Epistatic interactions between Tgfb1 and genetic loci, Tgfbm2 and Tgfbm3, determine susceptibility to an asthmatic stimulus. Proc Natl Acad Sci U S A 2012;109:18042-7.
68. Doyle JJ, Gerber EE, Dietz HC. Matrix-dependent perturbation of TGFbeta signaling and disease. FEBS Lett 2012;586:2003-15.
69. Pardali E, Ten Dijke P. TGFbeta signaling and cardiovascular diseases. Int J Biol Sci 2012;8:195-213.
70. Bettelli E, Carrier Y, Gao W, Korn T, Strom TB, Oukka M, et al. Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature 2006;441:235-8.
71. Gutcher I, Donkor MK, Ma Q, Rudensky AY, Flavell RA, Li MO. Autocrine transforming growth factor-beta1 promotes in vivo Th17 cell differentiation. Immunity 2011;34:396-408.
72. ten Dijke P, Arthur HM. Extracellular control of TGFbeta signalling in vascular development and disease. Nat Rev Mol Cell Biol 2007;8:857-69.
73. Annes JP, Munger JS, Rifkin DB. Making sense of latent TGFbeta activation. J Cell Sci 2003;116:217-24.
74. Nguyen AT, Gomez D, Bell RD, Campbell JH, Clowes AW, Gabbiani G, et al. Smooth muscle cell plasticity: fact or fiction? Circ Res 2013;112:17-22.
75. Wrana JL, Attisano L, Wieser R, Ventura F, Massague J. Mechanism of activation of the TGF-beta receptor. Nature 1994;370:341-7.
76. Inman GJ. Linking Smads and transcriptional activation. Biochem J 2005;386:e1-3.
77. Akhurst RJ, Hata A. Targeting the TGFbeta signalling pathway in disease. Nat Rev Drug Discov 2012;11:790-811.
78. Edgley AJ, Krum H, Kelly DJ. Targeting fibrosis for the treatment of heart failure: a role for transforming growth factor-beta. Cardiovasc Ther 2012;30:e30-40.
79. Nagasawa A, Yoshimura K, Suzuki R, Mikamo A, Yamashita O, Ikeda Y, et al. Important role of the angiotensin II pathway in producing matrix metalloproteinase-9 in human thoracic aortic aneurysms. J Surg Res 2013;183:472-7.
80. 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:e92-101.
81. Orlandi A, Ferlosio A, Gabbiani G, Spagnoli LG, Ehrlich PH. Phenotypic heterogeneity influences the behavior of rat aortic smooth muscle cells in collagen lattice. Exp Cell Res 2005;311:317-27.
82. Orlandi A, Bochaton-Piallat ML, Gabbiani G, Spagnoli LG. Aging, smooth muscle cells and vascular pathobiology: implications for atherosclerosis. Atherosclerosis 2006;188:221-30.
83. Orlandi A, Ciucci A, Ferlosio A, Pellegrino A, Chiariello L, Spagnoli LG. Increased expression and activity of matrix metalloproteinases characterize embolic cardiac myxomas. Am J Pathol 2005;166:1619-28.
84. Merk DR, Chin JT, Dake BA, Maegdefessel L, Miller MO, Kimura N, et al. miR-29b participates in early aneurysm development in Marfan syndrome. Circ Res 2012;110:312-24.
85. Yang HH, van Breemen C, Chung AW. Vasomotor dysfunction in the thoracic aorta of Marfan syndrome is associated with accumulation of oxidative stress. Vascul Pharmacol 2010;52:37-45.
86. Stasi MA, Scioli MG, Arcuri G, Mattera GG, Lombardo K, Marcellini M, et al. Propionyl-L-carnitine improves postischemic blood flow recovery and arteriogenetic revascularization and reduces endothelial NADPH-oxidase 4-mediated superoxide production. Arterioscler Thromb Vasc Biol 2010;30:426-35.