N-cadherin/catenin complex as a master regulator of intercalated disc function

Cell Communication and Adhesion

Volumn 21, Issue 3, 2014, Pages 169-179

  Vite, Alexia ^a   Radice, Glenn L ^a  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

Author keywords

Adherens junction; Arrhythmogenic cardiomyopathy; Catenin; Desmosome; N cadherin

Indexed keywords

BETA CATENIN; CATENIN; NERVE CELL ADHESION MOLECULE; PLAKOGLOBIN; CADHERIN;

CELL COMMUNICATION; CELL JUNCTION; DESMOSOME; GAP JUNCTION; GENETIC MANIPULATION; HEART ARRHYTHMIA; HEART MUSCLE; HEART MUSCLE CELL; HUMAN; INTERCALATED DISK; NONHUMAN; PRIORITY JOURNAL; REVIEW; ANIMAL; CYTOLOGY; METABOLISM;

ADHERENS JUNCTIONS; ANIMALS; CADHERINS; CATENINS; HUMANS; MYOCYTES, CARDIAC;

EID: 84901474977     PISSN: 15419061     EISSN: 15435180     Source Type: Journal    
DOI: 10.3109/15419061.2014.908853     Document Type: Review

References (75)

1. Angst BD, Khan LU, Severs NJ, Whitely K, Rothery S, Thompson RP, Magee AI, Gourdie RG. (1997). Dissociated spatial patterning of gap junctions and cell adhesion junctions during postnatal differentiation of ventricular myocardium. Circ Res. 80 : 88-94.
2. Asimaki A, Tandri H, Huang H, Halushka MK, Gautam S, Basso C, Thiene G, Tsatsopoulou A, Protonotarios N, Mckenna WJ, Calkins H, Saffitz JE. (2009). A new diagnostic test for arrhythmogenic right ventricular cardiomyopathy. N Engl J Med. 360 : 1075-1084.
3. Basso C, Czarnowska E, Della Barbera M, Bauce B, Beffagna G, Wlodarska EK, Pilichou K, Ramondo A, Lorenzon A, Wozniek O, Corrado D, Daliento L, Danieli GA, Valente M, Nava A, Thiene G, Rampazzo A. (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.
4. Basso C, Bauce B, Corrado D, Thiene G. (2012). Pathophysiology of arrhythmogenic cardiomyopathy. Nat Rev Cardiol. 9 : 223-233.
5. Bauce B, Nava A, Beffagna G, Basso C, Lorenzon A, Smaniotto G, De Bortoli M., Rigato I, Mazzotti E, Steriotis A, Marra MP, Towbin JA, Thiene G, Danieli GA, Rampazzo A. (2010). Multiple mutations in desmosomal proteins encoding genes in arrhythmogenic right ventricular cardiomyopathy/dysplasia. Heart Rhythm. 7 : 22-29.
6. Baurand A, Zelarayan L, Betney R, Gehrke C, Dunger S, Noack C, Busjahn A, Huelsken J, Taketo MM, Birchmeier W, Dietz R, Bergmann MW. (2007). Beta-catenin downregulation is required for adaptive cardiac remodeling. Circ Res. 100 : 1353-1362.
7. Bergmann MW. (2010). WNT signaling in adult cardiac hypertrophy and remodeling: lessons learned from cardiac development. Circ Res. 107 : 1198-1208.
8. Borrmann CM, Grund C, Kuhn C, Hofmann I, Pieperhoff S, Franke WW. (2006). The area composita of adhering junctions connecting heart muscle cells of vertebrates. II. Colocalizations of desmosomal and fascia adhaerens molecules in the intercalated disk. Eur J Cell Biol. 85: 469-485.
9. Cerrone M, Noorman M, Lin X, Chkourko H, Liang FX, Van Der Nagel R, Hund T, Birchmeier W, Mohler P, Van Veen TA, Van Rijen HV, Delmar M. (2012). Sodium current deficit and arrhythmogenesis in a murine model of plakophilin-2 haploinsufficiency. Cardiovasc Res. 95: 460-468.
10. Chen X, Shevtsov SP, Hsich E, Cui L, Haq S, Aronovitz M, Kerkela R, Molkentin JD, Liao R, Salomon RN, Patten R, Force T. (2006). The beta-catenin/T-cell factor/lymphocyte enhancer factor signaling pathway is required for normal and stressinduced cardiac hypertrophy. Mol Cell Biol. 26 : 4462-4473.
11. Cheng L, Yung A, Covarrubias M, Radice GL. (2011). Cortactin is required for N-cadherin regulation of Kv1.5 channel function. J Biol Chem. 286 : 20478-20489.
12. Clevers H, Nusse R. (2012). Wnt/beta-catenin signaling and disease. Cell. 149 : 1192-1205.
13. Cowin P, Burke B. (1996). Cytoskeleton-membrane interactions. Curr Opin Cell Biol. 8 : 56-65.
14. Forbes MS, Sperelakis N. (1985). Intercalated discs of mammalian heart: a review of structure and function. Tissue Cell. 17 : 605-648.
15. Franceschini A, Szklarczyk D, Frankild S, Kuhn M, Simonovic M, Roth A, Lin J, Minguez P, Bork P, Von Mering C, Jensen LJ. (2013). STRING v9.1: protein-protein interaction networks, with increased coverage and integration. Nucleic Acids Res. 41 : D808-D815.
16. Franke WW, Borrmann CM, Grund C, Pieperhoff S. (2006). The area composita of adhering junctions connecting heart muscle cells of vertebrates. I. Molecular definition in intercalated disks of cardiomyocytes by immunoelectron microscopy of desmosomal proteins. Eur J Cell Biol. 85 : 69-82.
17. Fressart V, Duthoit G, Donal E, Probst V, Deharo JC, Chevalier P, Klug D, Dubourg O, Delacretaz E, Cosnay P, Scanu P, Extramiana F, Keller D, Hidden-Lucet F, Simon F, Bessirard V, Roux-Buisson N, Hebert JL, Azarine A, Casset-Senon D, Rouzet F, Lecarpentier Y, Fontaine G, Coirault C, Frank R, Hainque B, Charron P. (2010). Desmosomal gene analysis in arrhythmogenic right ventricular dysplasia/cardiomyopathy: spectrum of mutations and clinical impact in practice. Europace. 12 : 861-868.
18. Garcia-Gras E, Lombardi R, Giocondo MJ, Willerson JT, Schneider MD, Khoury DS, Marian AJ. (2006). Suppression of canonical Wnt/beta-catenin signaling by nuclear plakoglobin recapitulates phenotype of arrhythmogenic right ventricular cardiomyopathy. J Clin Invest. 116 : 2012-2021.
19. Giepmans BN, Moolenaar WH. (1998). The gap junction protein connexin43 interacts with the second PDZ domain of the zona occludens-1 protein. Curr Biol. 8 : 931-934.
20. Glukhov AV, Fedorov VV, Kalish PW, Ravikumar VK, Lou Q, Janks D, Schuessler RB, Moazami N, Efimov IR. (2012). Conduction remodeling in human end-stage nonischemic left ventricular cardiomyopathy. Circulation. 125 : 1835-1847.
21. Goossens S, Janssens B, Bonne S, DE Rycke R, Braet F, van Hengel J, Van Roy F. (2007). A unique and specific interaction between alphaT-catenin and plakophilin-2 in the area composita, the mixed-type junctional structure of cardiac intercalated discs. J Cell Sci. 120 : 2126-2136.
22. Green KJ, Getsios S, Troyanovsky S, Godsel LM. (2010). Intercellular junction assembly, dynamics, and homeostasis. Cold Spring Harb Perspect Biol. 2 : a000125.
23. Gutstein DE, Morley GE, Tamaddon H, Vaidya D, Schneider MD, Chen J, Chien KR, Stuhlmann H, Fishman GI. (2001). Conduction slowing and sudden arrhythmic death in mice with cardiac-restricted inactivation of connexin43. Circ Res. 88 : 333-339.
24. Hertig CM, Butz S, Koch S, Eppenberger-Eberhardt M, Kemler R, Eppenberger HM. (1996). N-cadherin in adult rat cardiomyocytes in culture. II. Spatio-temporal appearance of proteins involved in cell-cell contact and communication. Formation of two distinct N-cadheri. n/catenin complexes. J Cell Sci. 109 : 11-20.
25. Hirschy A, Croquelois A, Perriard E, Schoenauer R, Agarkova I, Hoerstrup SP, Taketo MM, Pedrazzini T, Perriard JC, Ehler E. (2010). Stabilised beta-catenin in postnatal ventricular myocardium leads to dilated cardiomyopathy and premature death. Basic Res Cardiol. 105 : 597-608.
26. Hirschy A, Schatzmann F, Ehler E, Perriard JC. (2006). Establishment of cardiac cytoarchitecture in the developing mouse heart. Dev Biol. 289 : 430-441.
27. Hunter AW, Barker RJ, Zhu C, Gourdie RG. (2005). Zonula occludens-1 alters connexin43 gap junction size and organization by influencing channel accretion. Mol Biol Cell. 16 : 5686-5698.
28. Janssens B, Goossens S, Staes K, Gilbert B, van Hengel J, Colpaert C, Bruyneel E, Mareel M, Van Roy F. (2001). alphaT-catenin: a novel tissue-specific beta-catenin-binding protein mediating strong cell-cell adhesion. J Cell Sci. 114 : 3177-3188.
29. Kostetskii I, Li J, Xiong Y, Zhou R, Ferrari VA, Patel VV, Molkentin JD, Radice GL. (2005). Induced deletion of the N-cadherin gene in the heart leads to dissolution of the intercalated disc structure. Circ Res. 96 : 346-354.
30. Kostin S, Rieger M, Dammer S, Hein S, Richter M, Klovekorn WP, Bauer EP, Schaper J. (2003). Gap junction remodeling and altered connexin43 expression in the failing human heart. Mol Cell Biochem. 242 : 135-144.
31. Li D, Liu Y, Maruyama M, Zhu W, Chen H, Zhang W, Reuter S, Lin SF, Haneline LS, Field LJ, Chen PS, Shou W. (2011a). Restrictive loss of plakoglobin in cardiomyocytes leads to arrhythmogenic cardiomyopathy. Hum Mol Genet. 20: 4582-4596.
32. Li J, Goossens S, van Hengel J, Gao E, Cheng L, Tyberghein K, Shang X, De Rycke R, Van Roy F, Radice GL. (2012). Loss of alphaT-catenin alters the hybrid adhering junctions in the heart and leads to dilated cardiomyopathy and ventricular arrhythmia following acute ischemia. J Cell Sci. 125 : 1058-1067.
33. Li J, Levin MD, Xiong Y, Petrenko N, Patel VV, Radice GL. (2008). N-cadherin haploinsufficiency affects cardiac gap junctions and arrhythmic susceptibility. J Mol Cell Cardiol. 44: 597-606.
34. Li J, Patel VV, Kostetskii I, Xiong Y, Chu AF, Jacobson JT, Yu C, Morley GE, Molkentin JD, Radice GL. (2005). Cardiac-specific loss of N-cadherin leads to alteration in connexins with conduction slowing and arrhythmogenesis. Circ Res. 97: 474-481.
35. Li J, Swope D, Raess N, Cheng L, Muller EJ, Radice GL. (2011b). Cardiac tissue-restricted deletion of plakoglobin results in progressive cardiomyopathy and activation of {beta}-catenin signaling. Mol Cell Biol. 31 : 1134-1144.
36. Lombardi R, DA Graca Cabreira-Hansen M, Bell A, Fromm RR, Willerson JT, Marian AJ. (2011). Nuclear plakoglobin is essential for differentiation of cardiac progenitor cells to adipocytes in arrhythmogenic right ventricular cardiomyopathy. Circ Res. 109 : 1342-1353.
37. Lombardi R, Dong J, Rodriguez G, Bell A, Leung TK, Schwartz RJ, Willerson JT, Brugada R, Marian AJ. (2009). Genetic fate mapping identifies second heart field progenitor cells as a source of adipocytes in arrhythmogenic right ventricular cardiomyopathy. Circ Res. 104 : 1076-1084.
38. Luo Y, Ferreira-Cornwell M, Baldwin H, Kostetskii I, Lenox J, Lieberman M, Radice G. (2001). Rescuing the N-cadherin knockout by cardiac-specific expression of N- or E-cadherin. Development. 128 : 459-469.
39. Luo Y, Radice GL. (2005). N-cadherin acts upstream of VEcadherin in controlling vascular morphogenesis. J Cell Biol. 169 : 29-34.
40. Luo Y, High FA, Epstein JA, Radice GL. (2006). N-cadherin is required for neural crest remodeling of the cardiac outflow tract. Dev Biol. 299 : 517-528.
41. Luo Y, Radice GL. (2003). Cadherin-mediated adhesion is essential for myofibril continuity across the plasma membrane but not for assembly of the contractile apparatus. J Cell Sci. 116 : 1471-1479.
42. Matsushita T, Oyamada M, Fujimoto K, Yasuda Y, Masuda S, Wada Y, Oka T, Takamatsu T. (1999). Remodeling of cell-cell and cell-extracellular matrix interactions at the border zone of rat myocardial infarcts. Circ Res. 85 : 1046-1055.
43. McKoy G, Protonotarios N, Crosby A, Tsatsopoulou A, Anastasakis A, Coonar A, Norman M, Baboonian C, Jeffery S, Mckenna WJ. (2000). Identification of a deletion in plakoglobin in arrhythmogenic right ventricular cardiomyopathy with palmoplantar keratoderma and woolly hair (Naxos disease). Lancet. 355 : 2119-2124.
44. Meng W, Takeichi M. (2009). Adherens junction: molecular architecture and regulation. Cold Spring Harb Perspect Biol. 1 : a002899.
45. Oxford EM, Musa H, Maass K, Coombs W, Taffet SM, Delmar M. (2007). Connexin43 remodeling caused by inhibition of plakophilin-2 expression in cardiac cells. Circ Res. 101 : 703-711.
46. Pieperhoff S, Franke WW. (2007). The area composita of adhering junctions connecting heart muscle cells of vertebrates - IV: coalescence and amalgamation of desmosomal and adhaerens junction components - late processes in mammalian heart development. Eur J Cell Biol. 86 : 377-391.
47. Pieperhoff S, Franke WW. (2008). The area composita of adhering junctions connecting heart muscle cells of vertebrates. VI. Different precursor structures in non-mammalian species. Eur J Cell Biol. 87 : 413-430.
48. Protonotarios N, Tsatsopoulou A, Patsourakos P, Alexopoulos D, Gezerlis P, Simitsis S, Scampardonis G. (1986). Cardiac abnormalities in familial palmoplantar keratosis. Br Heart J. 56 : 321-326.
49. Qu J, Zhou J, Yi XP, Dong B, Zheng H, Miller LM, Wang X, Schneider MD, Li F. (2007). Cardiac-specific haploinsufficiency of beta-catenin attenuates cardiac hypertrophy but enhances fetal gene expression in response to aortic constriction. J Mol Cell Cardiol. 43 : 319-326.
50. Radice GL, Rayburn H, Matsunami H, Knudsen KA, Takeichi M, Hynes RO. (1997). Developmental defects in mouse embryos lacking N-cadherin. Dev Biol. 181 : 64-78.
51. Remo BF, Giovannone S, Fishman G. (2012). Connexin43 cardiac gap junction remodeling: lessons from genetically engineered murine models. J Membr Biol. 245 : 275-281.
52. Ross SE, Hemati N, Longo KA, Bennett CN, Lucas PC, Erickson RL, Macdougald OA. (2000). Inhibition of adipogenesis by Wnt signaling. Science. 289 : 950-953.
53. Saffitz JE. (2009). Arrhythmogenic cardiomyopathy and abnormalities of cell-to-cell coupling. Heart Rhythm. 6 : S62-S65.
54. Sato PY, Coombs W, Lin X, Nekrasova O, Green KJ, Isom LL, Taffet SM, Delmar M. (2011). Interactions between ankyrin-G, Plakophilin-2, and Connexin43 at the cardiac intercalated disc. Circ Res. 109 : 193-201.
55. Sato PY, Musa H, Coombs W, Guerrero-Serna G, Patino GA, Taffet SM, Isom LL, Delmar M. (2009). Loss of plakophilin-2 expression leads to decreased sodium current and slower conduction velocity in cultured cardiac myocytes. Circ Res. 105 : 523-526.
56. Schaper J, Froede R, Hein S, Buck A, Hashizume H, Speiser B, Friedl A, Bleese N. (1991). Impairment of the myocardial ultrastructure and changes of the cytoskeleton in dilated cardiomyopathy. Circulation. 83 : 504-514.
57. Severs NJ, Bruce AF, Dupont E, Rothery S. (2008). Remodelling of gap junctions and connexin expression in diseased myocardium. Cardiovasc Res. 80 : 9-19.
58. Shaw RM, Fay AJ, Puthenveedu MA, Von Zastrow M, Jan YN, Jan LY. (2007). Microtubule plus-end-tracking proteins target gap junctions directly from the cell interior to adherens junctions. Cell. 128 : 547-560.
59. Sheikh F, Chen Y, Liang X, Hirschy A, Stenbit AE, Gu Y, Dalton ND, Yajima T, Lu Y, Knowlton KU, Peterson KL, Perriard JC, Chen J. (2006). alpha-E-catenin inactivation disrupts the cardiomyocyte adherens junction, resulting in cardiomyopathy and susceptibility to wall rupture. Circulation. 114 : 1046-1055.
60. Smyth JW, Hong TT, Gao D, Vogan JM, Jensen BC, Fong TS, Simpson PC, Stainier DY, Chi NC, Shaw RM. (2010). Limited forward trafficking of connexin 43 reduces cell-cell coupling in stressed human and mouse myocardium. J Clin Invest. 120 : 266-279.
61. Sosinsky GE, Solan JL, Gaietta GM, Ngan L, Lee GJ, Mackey MR, Lampe PD. (2007). The C-terminus of connexin43 adopts different conformations in the Golgi and gap junction as detected with structure-specific antibodies. Biochem J. 408 : 375-385.
62. Swope D, Cheng L, Gao E, Li J, Radice GL. (2012). Loss of cadherin-binding proteins beta-catenin and plakoglobin in the heart leads to gap junction remodeling and arrhythmogenesis. Mol Cell Biol. 32 : 1056-1067.
63. Swope D, Li J, Radice GL. (2013). Beyond cell adhesion: the role of armadillo proteins in the heart. Cell Signal. 25 : 93-100.
64. Tavora F, Zhang M, Cresswell N, Li L, Fowler D, Franco M, Burke A. (2013). Quantitative Immunohistochemistry of Desmosomal Proteins (Plakoglobin, Desmoplakin and Plakophilin), Connexin-43, and N-cadherin in Arrhythmogenic Cardiomyopathy: An Autopsy Study. Open Cardiovasc Med J. 7 : 28-35.
65. Twiss F, de Rooij J. (2013). Cadherin mechanotransduction in tissue remodeling. Cell Mol Life Sci. 70 : 4101-4116.
66. van den Borne SW, Narula J, Voncken JW, Lijnen PM, Vervoort-Peters HT, Dahlmans VE, Smits JF, Daemen MJ, Blankesteijn WM. (2008). Defective intercellular adhesion complex in myocardium predisposes to infarct rupture in humans. J Am Coll Cardiol. 51 : 2184-2192.
67. van Hengel J, Calore M, Bauce B, Dazzo E, Mazzotti E, DE Bortoli M, Lorenzon A, LI Mura IE, Beffagna G, Rigato I, Vleeschouwers M, Tyberghein K, Hulpiau P, Van Hamme E, Zaglia T, Corrado D, Basso C, Thiene G, Daliento L, Nava A, Van Roy F, Rampazzo A. (2012). Mutations in the area composita protein alphaT-catenin are associated with arrhythmogenic right ventricular cardiomyopathy. Eur Heart J. 34 : 201-210.
68. van Tintelen JP, Hofstra RM, Wiesfeld AC, Van Den Berg MP, Hauer RN, Jongbloed JD. (2007). Molecular genetics of arrhythmogenic right ventricular cardiomyopathy: emerging horizon? Curr Opin Cardiol. 22 : 185-192.
69. Wang X, Gerdes AM. (1999). Chronic pressure overload cardiac hypertrophy and failure in guinea pigs: III. Intercalated disc remodeling. J Mol Cell Cardiol. 31 : 333-343.
70. Xu T, Yang Z, Vatta M, Rampazzo A, Beffagna G, Pilichou K, Scherer SE, Saffitz J, Kravitz J, Zareba W, Danieli GA, Lorenzon A, Nava A, Bauce B, Thiene G, Basso C, Calkins H, Gear K, Marcus F, Towbin JA. (2010). Compound and digenic heterozygosity contributes to arrhythmogenic right ventricular cardiomyopathy. J Am Coll Cardiol. 55 : 587-597.
71. Zelarayan LC, Noack C, Sekkali B, Kmecova J, Gehrke C, Renger A, Zafiriou MP, Van Der Nagel R, Dietz R, De Windt LJ, Balligand JL, Bergmann MW. (2008). Beta-Catenin downregulation attenuates ischemic cardiac remodeling through enhanced resident precursor cell differentiation. Proc Natl Acad Sci U S A. 105 : 19762-19767.
72. Zemljic-Harpf AE, Godoy JC, Platoshyn O, Asfaw EK, Busija AR, Domenighetti AA, Ross RS. (2014). Vinculin directly binds zonula occludens-1 and is essential for stabilizing connexin- 43-containing gap junctions in cardiac myocytes. J Cell Sci. 127 : 1104-1116.
73. Zhou J, Qu J, Yi XP, Graber K, Huber L, Wang X, Gerdes AM, Li F. (2007). Upregulation of gamma-catenin compensates for the loss of beta-catenin in adult cardiomyocytes. Am J Physiol Heart Circ Physiol. 292 : H270-H276.
74. Zhuang J, Yamada KA, Saffitz JE, Kleber AG. (2000). Pulsatile stretch remodels cell-to-cell communication in cultured myocytes. Circ Res. 87 : 316-322.
75. Zhurinsky J, Shtutman M, Ben-Ze'ev A. (2000). Plakoglobin and beta-catenin: protein interactions, regulation and biological roles. J Cell Sci. 113 : 3127-3139.