Metallothionein-dependent up-regulation of TGF-β2 participates in the remodelling of the myxomatous mitral valve

Cardiovascular Research

Volumn 93, Issue 3, 2012, Pages 480-489

  Hulin, Alexia ^a   Deroanne, Christophe F ^a   Lambert, Charles A ^a   Dumont, Bruno ^a   Castronovo, Vincent ^a   Defraigne, Jean Olivier ^b   Nusgens, Betty V ^a   Radermecker, Marc A ^b   Colige, Alain C ^a  

^a UNIVERSITY OF LIÈGE   (Belgium)

^b UNIVERSITY OF LIÈGE   (Belgium)

Author keywords

ADAMTS; Metallothionein; Myxomatous mitral valve; TGF ; Valvular interstitial cells

Indexed keywords

ADAMTS1 PROTEIN; METALLOTHIONEIN; METALLOTHIONEIN I; METALLOTHIONEIN II; TRANSFORMING GROWTH FACTOR BETA2;

ADULT; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; DISEASE COURSE; FEMALE; GENE CONTROL; GENE EXPRESSION; GENE SILENCING; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MALE; MITRAL VALVE; MITRAL VALVE DISEASE; MYXOMATOUS MITRAL VALVE; PRIORITY JOURNAL; TRANSCRIPTOMICS; UPREGULATION; WESTERN BLOTTING;

ADAM PROTEINS; ADULT; AGED; CELLS, CULTURED; FEMALE; HUMANS; MALE; METALLOTHIONEIN; MICROARRAY ANALYSIS; MIDDLE AGED; MITRAL VALVE; MITRAL VALVE INSUFFICIENCY; TRANSFORMING GROWTH FACTOR BETA1; TRANSFORMING GROWTH FACTOR BETA2; UP-REGULATION; VENTRICULAR REMODELING; VERSICANS;

EID: 84857603607     PISSN: 00086363     EISSN: 17553245     Source Type: Journal    
DOI: 10.1093/cvr/cvr337     Document Type: Article

References (42)

1. Freed LA, Levy D, Levine RA, Larson MG, Evans JC, Fuller DL et al. Prevalence and clinical outcome of mitral-valve prolapse. N Engl J Med 1999;341:1-7.
2. Grau JB, Pirelli L, Yu PJ, Galloway AC, Ostrer H. The genetics of mitral valve prolapse. Clin Genet 2007;72:288-295.
3. Nasuti JF, Zhang PJ, Feldman MD, Pasha T, Khurana JS, Gorman JH III et al. Fibrillin and other matrix proteins in mitral valve prolapse syndrome. Ann Thorac Surg 2004;77:532-536.
4. Gupta V, Barzilla JE, Mendez JS, Stephens EH, Lee EL, Collard CD et al. Abundance and location of proteoglycans and hyaluronan within normal and myxomatous mitral valves. Cardiovasc Pathol 2009;18:191-197.
5. Hayek E, Gring CN, Griffin BP. Mitral valve prolapse. Lancet 2005;365:507-518.
6. Liu AC, Joag VR, Gotlieb AI. The emerging role of valve interstitial cell phenotypes in regulating heart valve pathobiology. Am J Pathol 2007;171:1407-1418.
7. Rabkin E, Aikawa M, Stone JR, Fukumoto Y, Libby P, Schoen FJ. Activated interstitial myofibroblasts express catabolic enzymes and mediate matrix remodeling in myxomatous heart valves. Circulation 2001;104:2525-2532.
8. Weyman AE, Scherrer-Crosbie M. Marfan syndrome and mitral valve prolapse. J Clin Invest 2004;114:1543-1546.
9. Dietz HC, Cutting GR, Pyeritz RE, Maslen CL, Sakai LY, Corson GM et al. Marfan syndrome caused by a recurrent de novo missense mutation in the fibrillin gene. Nature 1991;352:337-339.
10. 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. Nat Genet 2005;37:275-281.
11. Ng CM, Cheng A, Myers LA, Martinez-Murillo F, Jie C, Bedja D et al. TGF-beta-dependent pathogenesis of mitral valve prolapse in a mouse model of Marfan syndrome. J Clin Invest 2004;114:1586-1592.
12. Loardi C, Alamanni F, Trezzi M, Kassem S, Cavallotti L, Tremoli E et al. Biology of mitral valve prolapse: the harvest is big, but the workers are few. Int J Cardiol 2011;151:129-135.
13. Phillippi JA, Klyachko EA, Kenny JPt, Eskay MA, Gorman RC, Gleason TG. Basal and oxidative stress-induced expression of metallothionein is decreased in ascending aortic aneurysms of bicuspid aortic valve patients. Circulation 2009;119:2498-2506.
14. Lambert CA, Colige AC, Lapiere CM, Nusgens BV. Coordinated regulation of procollagens I and III and their post-translational enzymes by dissipation of mechanical tension in human dermal fibroblasts. Eur J Cell Biol 2001;80:479-485.
15. Meloni G, Knipp M, Vasak M. Detection of neuronal growth inhibitory factor (metallothionein-3) in polyacrylamide gels and by Western blot analysis. J Biochem Biophys Methods 2005;64:76-81.
16. Mizzen CA, Cartel NJ, Yu WH, Fraser PE, McLachlan DR. Sensitive detection of metallothioneins-1,-2 and -3 in tissue homogenates by immunoblotting: a method for enhanced membrane transfer and retention. J Biochem Biophys Methods 1996;32:77-83.
17. Ho TT, Merajver SD, Lapiere CM, Nusgens BV, Deroanne CF. RhoA-GDP regulates RhoB protein stability. Potential involvement of RhoGDI alpha. J Biol Chem 2008;283:21588-21598.
18. Kischel P, Waltregny D, Dumont B, Turtoi A, Greffe Y, Kirsch S et al. Versican overexpression in human breast cancer lesions: known and new isoforms for stromal tumor targeting. Int J Cancer 2010;126:640-650.
19. Murphy BJ, Andrews GK, Bittel D, Discher DJ, McCue J, Green CJ et al. Activation of metallothionein gene expression by hypoxia involves metal response elements and metal transcription factor-1. Cancer Res 1999;59:1315-1322.
20. Andrews GK. Regulation of metallothionein gene expression by oxidative stress and metal ions. Biochem Pharmacol 2000;59:95-104.
21. Zhang B, Georgiev O, Hagmann M, Gunes C, Cramer M, Faller P et al. Activity of metal-responsive transcription factor 1 by toxic heavy metals and H2O2 in vitro is modulated by metallothionein. Mol Cell Biol 2003;23:8471-8485.
22. Zbinden S, Wang J, Adenika R, Schmidt M, Tilan JU, Najafi AH et al. Metallothionein enhances angiogenesis and arteriogenesis by modulating smooth muscle cell and macrophage function. Arterioscler Thromb Vasc Biol 2010;30:477-482.
23. Joshi B, Ordonez-Ercan D, Dasgupta P, Chellappan S. Induction of human metallothionein 1G promoter by VEGF and heavy metals: differential involvement of E2F and metal transcription factors. Oncogene 2005;24:2204-2217.
24. White SJ, Hayes EM, Lehoux S, Jeremy JY, Horrevoets AJ, Newby AC. Characterization of the differential response of endothelial cells exposed to normal and elevated laminar shear stress. J Cell Physiol 2011;226:2841-2848.
25. Salhiyyah K, Yacoub MH, Chester AH. Cellular mechanisms in mitral valve disease. J Cardiovasc Transl Res 2011.
26. Butcher JT, Nerem RM. Valvular endothelial cells regulate the phenotype of interstitial cells in co-culture: effects of steady shear stress. Tissue Eng 2006;12:905-915.
27. Gomez D, Al Haj Zen A, Borges LF, Philippe M, Gutierrez PS, Jondeau G et al. Syndromic and non-syndromic aneurysms of the human ascending aorta share activation of the Smad2 pathway. J Pathol 2009;218:131-142.
28. Le Goff C, Morice-Picard F, Dagoneau N, Wang LW, Perrot C, Crow YJ et al. ADAMTSL2 mutations in geleophysic dysplasia demonstrate a role for ADAMTS-like proteins in TGF-beta bioavailability regulation. Nat Genet 2008;40:1119-1123.
29. Aupperle H, Marz I, Thielebein J, Schoon HA. Expression of transforming growth factor-beta1, -beta2 and -beta3 in normal and diseased canine mitral valves. J Comp Pathol 2008;139:97-107.
30. Haroon ZA, Amin K, Lichtlen P, Sato B, Huynh NT, Wang Z et al. Loss of metal transcription factor-1 suppresses tumor growth through enhanced matrix deposition. FASEB J 2004;18:1176-1184.
31. Moffatt P, Plaa GL, Denizeau F. Induction of metallothionein gene expression by epidermal growth factor and its inhibition by transforming growth factor-beta and dexamethasone in rat hepatocytes. Hepatology (Baltimore, MD) 1995;21:1038-1044.
32. Toh PP, Li JJ, Yip GW, Lo SL, Guo CH, Phan TT et al. Modulation of metallothionein isoforms is associated with collagen deposition in proliferating keloid fibroblasts in vitro. Exp Dermatol 2010;19:987-993.
33. Townsend TA, Robinson JY, Deig CR, Hill CR, Misfeldt A, Blobe GC et al. BMP-2 and TGFbeta2 shared pathways regulate endocardial cell transformation. Cells Tissues Organs 2011;194:1-12.
34. Paruchuri S, Yang JH, Aikawa E, Melero-Martin JM, Khan ZA, Loukogeorgakis S et al. Human pulmonary valve progenitor cells exhibit endothelial/mesenchymal plasticity in response to vascular endothelial growth factor-A and transforming growth factorbeta2. Circ Res 2006;99:861-869.
35. Azhar M, Brown K, Gard C, Chen H, Rajan S, Elliott DA et al. Transforming growth factor Beta2 is required for valve remodeling during heart development. Developmental dynamics: an official publication of the American Association of Anatomists 2011;240:2127-2141.
36. Walker GA, Masters KS, Shah DN, Anseth KS, Leinwand LA. Valvular myofibroblast activation by transforming growth factor-beta: implications for pathological extracellular matrix remodeling in heart valve disease. Circ Res 2004;95:253-260.
37. Wight TN. Arterial remodeling in vascular disease: a key role for hyaluronan and versican. Front Biosci 2008;13:4933-4937.
38. Arslan F, Bosserhoff AK, Nickl-Jockschat T, Doerfelt A, Bogdahn U, Hau P. The role of versican isoforms V0/V1 in glioma migration mediated by transforming growth factorbeta2. Br J Cancer 2007;96:1560-1568.
39. Salter RC, Ashlin TG, Kwan AP, Ramji DP. ADAMTS proteases: key roles in atherosclerosis? J Mol Med 2010;88:1203-1211.
40. Dupuis LE, McCulloch DR, McGarity JD, Bahan A, Wessels A, Weber D et al. Altered versican cleavage in ADAMTS5 deficient mice; a novel etiology of myxomatous valve disease. Dev Biol 2011;357:152-164.
41. Kern CB, Wessels A, McGarity J, Dixon LJ, Alston E, Argraves WS et al. Reduced versican cleavage due to Adamts9 haploinsufficiency is associated with cardiac and aortic anomalies. Matrix Biol 2010;29:304-316.
42. Hattori N, Carrino DA, Lauer ME, Vasanji A, Wylie JD, Nelson CM et al. Pericellular versican regulates the fibroblast-myofibroblast transition: a role for ADAMTS5 protease-mediated proteolysis. J Biol Chem 2011;286:34298-34310.