Restrictive loss of plakoglobin in cardiomyocytes leads to arrhythmogenic cardiomyopathy

Human Molecular Genetics

Volumn 20, Issue 23, 2011, Pages 4582-4596

  Li, Deqiang ^a   Liu, Ying ^a   Maruyama, Mitsunori ^b   Zhu, Wuqiang ^a   Chen, Hanying ^a   Zhang, Wenjun ^a   Reuter, Sean ^a   Lin, Shien Fong ^b   Haneline, Laura S ^a   Field, Loren J ^a,b   Chen, Peng Sheng ^b   Shou, Weinian ^a  

^a INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; PLAKOGLOBIN; TRANSFORMING GROWTH FACTOR BETA; WNT PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DEATH; CELL JUNCTION; CONTROLLED STUDY; DESMOSOME; FEMALE; HEART MUSCLE CELL; HEART MUSCLE FIBROSIS; HEART RIGHT VENTRICLE DYSPLASIA; HEART VENTRICLE ANEURYSM; HEART VENTRICLE ARRHYTHMIA; LOSS OF FUNCTION MUTATION; MALE; MOLECULAR PATHOLOGY; MOUSE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; ULTRASTRUCTURE ANALYSIS AND ELECTRON MICROSCOPY;

ANIMALS; ARRHYTHMIAS, CARDIAC; ARRHYTHMOGENIC RIGHT VENTRICULAR DYSPLASIA; CELL DEATH; DESMOSOMES; FIBROSIS; GAMMA CATENIN; GENE DELETION; HEART CONDUCTION SYSTEM; HUMANS; MICE; MICE, MUTANT STRAINS; MYOCARDIUM; MYOCYTES, CARDIAC; ORGAN SPECIFICITY; SARCOMERES; WNT SIGNALING PATHWAY;

MUS;

EID: 81255209231     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddr392     Document Type: Article

References (53)

1. Basso, C., Corrado, D., Marcus, F.I., Nava, A. and Thiene, G. (2009) Arrhythmogenic right ventricular cardiomyopathy. Lancet, 373, 1289-1300.
2. Lahtinen, A.M., Lehtonen, E., Marjamaa, A., Kaartinen, M., Helio, T., Porthan, K., Oikarinen, L., Toivonen, L., Swan, H., Jula, A. et al. (2011) Population-prevalent desmosomal mutations predisposing to arrhythmogenic right ventricular cardiomyopathy. Heart Rhythm, 8, 1214-1221.
3. Maron, B.J., Shirani, J., Poliac, L.C., Mathenge, R., Roberts, W.C. and Mueller, F.O. (1996) Sudden death in young competitive athletes. Clinical, demographic, and pathological profiles. J. Am. Med. Assoc., 276, 199-204.
4. Protonotarios, N.I., Tsatsopoulou, A.A. and Gatzoulis, K.A. (2002) Arrhythmogenic right ventricular cardiomyopathy caused by a deletion in plakoglobin (Naxos disease). Card. Electrophysiol. Rev., 6, 72-80.
5. Lai-Cheong, J.E., Arita, K. and McGrath, J.A. (2007) Genetic diseases of junctions. J. Invest. Dermatol., 127, 2713-2725.
6. Beffagna, G., Occhi, G., Nava, A., Vitiello, L., Ditadi, A., Basso, C., Bauce, B., Carraro, G., Thiene, G., Towbin, J.A. et al. (2005) Regulatory mutations in transforming growth factor-beta3 gene cause arrhythmogenic right ventricular cardiomyopathy type 1. Cardiovasc. Res., 65, 366-373.
7. den Haan, A.D., Tan, B.Y., Zikusoka, M.N., Llado, L.I., Jain, R., Daly, A., Tichnell, C., James, C., Amat-Alarcon, N., Abraham, T. et al. (2009) Comprehensive desmosome mutation analysis in north americans with arrhythmogenic right ventricular dysplasia/cardiomyopathy. Circ. Cardiovasc. Genet., 2, 428-435.
8. Green, K.J. and Gaudry, C.A. (2000) Are desmosomes more than tethers for intermediate filaments? Nat. Rev. Mol. Cell Biol., 1, 208-216.
9. Garcia-Gras, E., Lombardi, R., Giocondo, M.J., Willerson, J.T., Schneider, M.D., Khoury, D.S. and Marian, A.J. (2006) Suppression of canonical Wnt/beta-catenin signaling by nuclear plakoglobin recapitulates phenotype of arrhythmogenic right ventricular cardiomyopathy. J. Clin. Invest., 116, 2012-2021.
10. Pilichou, K., Remme, C.A., Basso, C., Campian, M.E., Rizzo, S., Barnett, P., Scicluna, B.P., Bauce, B., van den Hoff, M.J., de Bakker, J.M. et al. (2009) Myocyte necrosis underlies progressive myocardial dystrophy in mouse dsg2-related arrhythmogenic right ventricular cardiomyopathy. J. Exp. Med., 206, 1787-1802.
11. Yang, Z., Bowles, N.E., Scherer, S.E., Taylor, M.D., Kearney, D.L., Ge, S., Nadvoretskiy, V.V., DeFreitas, G., Carabello, B., Brandon, L.I. et al. (2006) Desmosomal dysfunction due to mutations in desmoplakin causes arrhythmogenic right ventricular dysplasia/cardiomyopathy. Circ. Res., 99, 646-655.
12. McKoy, G., Protonotarios, N., Crosby, A., Tsatsopoulou, A., Anastasakis, A., Coonar, A., Norman, M., Baboonian, C., Jeffery, S. and McKenna, W.J. (2000) Identification of a deletion in plakoglobin in arrhythmogenic right ventricular cardiomyopathy with palmoplantar keratoderma and woolly hair (Naxos disease). Lancet, 355, 2119-2124.
13. Kirchhof, P., Fabritz, L., Zwiener, M., Witt, H., Schafers, M., Zellerhoff, S., Paul, M., Athai, T., Hiller, K.H., Baba, H.A. et al. (2006) Age- and training-dependent development of arrhythmogenic right ventricular cardiomyopathy in heterozygous plakoglobin-deficient mice. Circulation, 114, 1799-1806.
14. Agah, R., Frenkel, P.A., French, B.A., Michael, L.H., Overbeek, P.A. and Schneider, M.D. (1997) Gene recombination in postmitotic cells. Targeted expression of Cre recombinase provokes cardiac-restricted, site-specific rearrangement in adult ventricular muscle in vivo. J. Clin. Invest., 100, 169-179.
15. MacLellan, W.R., Garcia, A., Oh, H., Frenkel, P., Jordan, M.C., Roos, K.P. and Schneider, M.D. (2005) Overlapping roles of pocket proteins in the myocardium are unmasked by germ line deletion of p130 plus heart-specific deletion of Rb. Mol. Cell Biol., 25, 2486-2497.
16. Basso, C., Thiene, G., Corrado, D., Angelini, A., Nava, A. and Valente, M. (1996) Arrhythmogenic right ventricular cardiomyopathy. Dysplasia, dystrophy, or myocarditis? Circulation, 94, 983-991.
17. Kaplan, S.R., Gard, J.J., Protonotarios, N., Tsatsopoulou, A., Spiliopoulou, C., Anastasakis, A., Squarcioni, C.P., McKenna, W.J., Thiene, G., Basso, C. et al. (2004) Remodeling of myocyte gap junctions in arrhythmogenic right ventricular cardiomyopathy due to a deletion in plakoglobin (Naxos disease). Heart Rhythm, 1, 3-11.
18. Hamilton, R.M. (2009) Arrhythmogenic right ventricular cardiomyopathy. Pacing Clin. Electrophysiol., 32(Suppl. 2), S44-51.
19. Zhurinsky, J., Shtutman, M. and Ben-Ze'ev, A. (2000) Plakoglobin and beta-catenin: protein interactions, regulation and biological roles. J. Cell Sci., 113(Pt 18), 3127-3139.
20. Bierkamp, C., Schwarz, H., Huber, O. and Kemler, R. (1999) Desmosomal localization of beta-catenin in the skin of plakoglobin null-mutant mice. Development, 126, 371-381.
21. Soonpaa, M.H., Koh, G.Y., Pajak, L., Jing, S., Wang, H., Franklin, M.T., Kim, K.K. and Field, L.J. (1997) Cyclin D1 overexpression promotes cardiomyocyte DNA synthesis and multinucleation in transgenic mice. J. Clin. Invest., 99, 2644-2654.
22. DasGupta, R. and Fuchs, E. (1999) Multiple roles for activated LEF/TCF transcription complexes during hair follicle development and differentiation. Development, 126, 4557-4568.
23. Grasl-Kraupp, B., Ruttkay-Nedecky, B., Koudelka, H., Bukowska, K., Bursch, W. and Schulte-Hermann, R. (1995) In situ detection of fragmented DNA (TUNEL assay) fails to discriminate among apoptosis, necrosis, and autolytic cell death: a cautionary note. Hepatology, 21, 1465-1468.
24. Thomsen, H. and Held, H. (1994) Susceptibility of C5b-9(m) to postmortem changes. Int. J. Legal Med., 106, 291-293.
25. Han, R., Bansal, D., Miyake, K., Muniz, V.P., Weiss, R.M., McNeil, P.L. and Campbell, K.P. (2007) Dysferlin-mediated membrane repair protects the heart from stress-induced left ventricular injury. J. Clin. Invest., 117, 1805-1813.
26. Chen, G. and Goeddel, D.V. (2002) TNF-R1 signaling: a beautiful pathway. Science, 296, 1634-1635.
27. Kitsis, R.N. and Molkentin, J.D. (2010) Apoptotic cell death 'Nixed' by an ER-mitochondrial necrotic pathway. Proc. Natl Acad. Sci. USA, 107, 9031-9032.
28. Dhanasekaran, D.N. and Reddy, E.P. (2008) JNK signaling in apoptosis. Oncogene, 27, 6245-6251.
29. Heldin, C.H., Landstrom, M. and Moustakas, A. (2009) Mechanism of TGF-beta signaling to growth arrest, apoptosis, and epithelial-mesenchymal transition. Curr. Opin. Cell Biol., 21, 166-176.
30. Kania, G., Blyszczuk, P. and Eriksson, U. (2009) Mechanisms of cardiac fibrosis in inflammatory heart disease. Trends Cardiovasc. Med., 19, 247-252.
31. Chen, H., Yong, W., Ren, S., Shen, W., He, Y., Cox, K.A., Zhu, W., Li, W., Soonpaa, M., Payne, R.M. et al. (2006) Overexpression of bone morphogenetic protein 10 in myocardium disrupts cardiac postnatal hypertrophic growth. J. Biol. Chem., 281, 27481-27491.
32. Ranganathan, P., Agrawal, A., Bhushan, R., Chavalmane, A.K., Kalathur, R.K., Takahashi, T. and Kondaiah, P. (2007) Expression profiling of genes regulated by TGF-beta: differential regulation in normal and tumour cells. BMC Genomics, 8, 98.
33. Khalil, N. (1999) TGF-beta: from latent to active. Microbes Infect., 1, 1255-1263.
34. Kassiri, Z., Defamie, V., Hariri, M., Oudit, G.Y., Anthwal, S., Dawood, F., Liu, P. and Khokha, R. (2009) Simultaneous transforming growth factor beta-tumor necrosis factor activation and cross-talk cause aberrant remodeling response and myocardial fibrosis in Timp3-deficient heart. J. Biol. Chem., 284, 29893-29904.
35. Christensen, A.H., Benn, M., Bundgaard, H., Tybjaerg-Hansen, A., Haunso, S. and Svendsen, J.H. (2010) Wide spectrum of desmosomal mutations in Danish patients with arrhythmogenic right ventricular cardiomyopathy. J. Med. Genet., 47, 736-744.
36. Sen-Chowdhry, S., Morgan, R.D., Chambers, J.C. and McKenna, W.J. (2010) Arrhythmogenic cardiomyopathy: etiology, diagnosis, and treatment. Annu. Rev. Med., 61, 233-253.
37. Sen-Chowdhry, S., Lowe, M.D., Sporton, S.C. and McKenna, W.J. (2004) Arrhythmogenic right ventricular cardiomyopathy: clinical presentation, diagnosis, and management. Am. J. Med., 117, 685-695.
38. Basso, C., Czarnowska, E., Della Barbera, M., Bauce, B., Beffagna, G., Wlodarska, E.K., Pilichou, K., Ramondo, A., Lorenzon, A., Wozniek, O. et al. (2006) Ultrastructural evidence of intercalated disc remodelling in arrhythmogenic right ventricular cardiomyopathy: an electron microscopy investigation on endomyocardial biopsies. Eur. Heart J., 27, 1847-1854.
39. Li, J., Swope, D., Raess, N., Cheng, L., Muller, E.J. and Radice, G.L. (2011) Cardiac tissue-restricted deletion of plakoglobin results in progressive cardiomyopathy and activation of {beta}-catenin signaling. Mol. Cell Biol., 31, 1134-1144.
40. Matsuo, S., Sato, Y., Nakae, I., Masuda, D., Yomota, M., Ashihara, T. and Horie, M. (2007) Left ventricular involvement in arrhythmogenic right ventricular cardiomyopathy demonstrated by multidetector-row computed tomography. Int. J. Cardiol., 115, e129-131.
41. Mackey-Bojack, S.M., Roe, S.J. and Titus, J.L. (2009) Sudden death with circumferential subepicardial fibrofatty replacement: left-sided arrhythmogenic ventricular cardiomyopathy. Am. J. Forensic. Med. Pathol., 30, 209-214.
42. Sen-Chowdhry, S., Syrris, P., Prasad, S.K., Hughes, S.E., Merrifield, R., Ward, D., Pennell, D.J. and McKenna, W.J. (2008) Left-dominant arrhythmogenic cardiomyopathy: an under-recognized clinical entity. J. Am. Coll. Cardiol., 52, 2175-2187.
43. McCauley, M.D. and Wehrens, X.H. (2009) Animal models of arrhythmogenic cardiomyopathy. Dis. Model. Mech., 2, 563-570.
44. Chen, X., Shevtsov, S.P., Hsich, E., Cui, L., Haq, S., Aronovitz, M., Kerkela, R., Molkentin, J.D., Liao, R., Salomon, R.N. et al. (2006) The beta-catenin/T-cell factor/lymphocyte enhancer factor signaling pathway is required for normal and stress-induced cardiac hypertrophy. Mol. Cell Biol., 26, 4462-4473.
45. Baurand, A., Zelarayan, L., Betney, R., Gehrke, C., Dunger, S., Noack, C., Busjahn, A., Huelsken, J., Taketo, M.M., Birchmeier, W. et al. (2007) Beta-catenin downregulation is required for adaptive cardiac remodeling. Circ. Res., 100, 1353-1362.
46. Mallat, Z., Tedgui, A., Fontaliran, F., Frank, R., Durigon, M. and Fontaine, G. (1996) Evidence of apoptosis in arrhythmogenic right ventricular dysplasia. N. Engl. J. Med., 335, 1190-1196.
47. McLennan, I.S. and Koishi, K. (2002) The transforming growth factor-betas: multifaceted regulators of the development and maintenance of skeletal muscles, motoneurons and Schwann cells. Int. J. Dev. Biol., 46, 559-567.
48. Taniguti, A.P., Pertille, A., Matsumura, C.Y., Santo Neto, H. and Marques, M.J. (2011) Prevention of muscle fibrosis and myonecrosis in mdx mice by suramin, a TGF-beta1 blocker. Muscle Nerve, 43, 82-87.
49. Buja, L.M. and Vela, D. (2008) Cardiomyocyte death and renewal in the normal and diseased heart. Cardiovasc. Pathol., 17, 349-374.
50. Lakso, M., Pichel, J.G., Gorman, J.R., Sauer, B., Okamoto, Y., Lee, E., Alt, F.W. and Westphal, H. (1996) Efficient in vivo manipulation of mouse genomic sequences at the zygote stage. Proc. Natl Acad. Sci. USA, 93, 5860-5865.
51. Pasumarthi, K.B., Nakajima, H., Nakajima, H.O., Soonpaa, M.H. and Field, L.J. (2005) Targeted expression of cyclin D2 results in cardiomyocyte DNA synthesis and infarct regression in transgenic mice. Circ. Res., 96, 110-118.
52. Li, D., Hallett, M.A., Zhu, W., Rubart, M., Liu, Y., Yang, Z., Chen, H., Haneline, L.S., Chan, R.J., Schwartz, R.J. et al. (2011) Dishevelled-associated activator of morphogenesis 1 (Daam1) is required for heart morphogenesis. Development, 138, 303-315.
53. Maruyama, M., Li, B.Y., Chen, H., Xu, X., Song, L.S., Guatimosim, S., Zhu, W., Yong, W., Zhang, W., Bu, G. et al. (2011) FKBP12 is a critical regulator of the heart rhythm and the cardiac voltage-gated sodium current in mice. Circ. Res., 108, 1042-1052.