The tight junction protein CAR regulates cardiac conduction and cell-cell communication

Journal of Experimental Medicine

Volumn 205, Issue 10, 2008, Pages 2369-2379

  Lisewski, Ulrike ^a   Shi, Yu ^a   Wrackmeyer, Uta ^a   Fischer, Robert ^b   Chen, Chen ^a   Schirdewan, Alexander ^b,c   Jüttner, Rene ^a   Rathjen, Fritz ^a   Poller, Wolfgang ^c   Radke, Michael H ^a   Gotthardt, Michael ^a,d  

^a MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^b HUMBOLDT UNIVERSITY   (Germany)

^c Campus Benjamin Franklin ^*  (Germany)

^d WASHINGTON STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COXSACKIE VIRUS AND ADENOVIRUS RECEPTOR; GAP JUNCTION PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL COMMUNICATION; CONTROLLED STUDY; COXSACKIE VIRUS INFECTION; GAP JUNCTION; HEART ARRHYTHMIA; HEART ATRIOVENTRICULAR NODE; HEART ATRIUM; HEART CONDUCTION; HEART DEVELOPMENT; HEART MUSCLE CELL; HEART VENTRICLE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SINUS NODE; TIGHT JUNCTION;

ANIMALS; ATRIOVENTRICULAR NODE; CADHERINS; CELL COMMUNICATION; CELLS, CULTURED; CONNEXIN 43; COXSACKIEVIRUS INFECTIONS; ELECTROCARDIOGRAPHY; ELECTROPHYSIOLOGY; GAP JUNCTIONS; HEART; HEART CONDUCTION SYSTEM; HUMANS; MICE; MICE, KNOCKOUT; MYOCYTES, CARDIAC; PHENOTYPE; RECEPTORS, VIRUS; TIGHT JUNCTIONS;

EID: 53349097084     PISSN: 00221007     EISSN: 00221007     Source Type: Journal    
DOI: 10.1084/jem.20080897     Document Type: Article

References (59)

1. Tomaselli, G.F., D.J. Beuckelmann, H.G. Calkins, R.D. Berger, P.D. Kessler, J.H. Lawrence, D. Kass, A.M. Feldman, and E. Marban. 1994. Sudden cardiac death in heart failure. The role of abnormal repolarization. Circulation. 90:2534-2539.
2. Saffitz, J.E., J.G. Laing, and K.A. Yamada. 2000. Connexin expression and turnover: implications for cardiac excitability. Circ. Res. 86:723-728.
3. Peters, N.S. 2006. Gap junctions: clarifying the complexities of connexins and conduction. Circ. Res. 99:1156-1158.
4. Kreuzberg, M.M., K. Willecke, and F.F. Bukauskas. 2006. Connexin-mediated cardiac impulse propagation: connexin 30.2 slows atrioventricular conduction in mouse heart. Trends Cardiovasc. Med. 16:266-272.
5. Simon, A.M., D.A. Goodenough, and D.L. Paul. 1998. Mice lacking connexin40 have cardiac conduction abnormalities characteristic of atrioventricular block and bundle branch block. Curr. Biol. 8:295-298.
6. Li, J., V.V. Patel, I. Kostetskii, Y. Xiong, A.F. Chu, J.T. Jacobson, C. Yu, G.E. Morley, J.D. Molkentin, and G.L. Radice. 2005. Cardiac-specific loss of N-cadherin leads to alteration in connexins with conduction slowing and arrhythmogenesis. Circ. Res. 97:474-481.
7. Oxford, E.M., H. Musa, K. Maass, W. Coombs, S.M. Taffet, and M. Delmar. 2007. Connexin43 remodeling caused by inhibition of plakophilin-2 expression in cardiac cells. Circ. Res. 101:703-711.
8. Cohen, C.J., J.T. Shieh, R.J. Pickles, T. Okegawa, J.T. Hsieh, and J.M. Bergelson. 2001. The coxsackievirus and adenovirus receptor is a transmembrane component of the tight junction. Proc. Natl. Acad. Sci. USA. 98:15191-15196.
9. Bergelson, J.M., J.A. Cunningham, G. Droguett, E.A. Kurt-Jones, A. Krithivas, J.S. Hong, M.S. Horwitz, R.L. Crowell, and R.W. Finberg. 1997. Isolation of a common receptor for Coxsackie B viruses and adenoviruses 2 and 5. Science. 275:1320-1323.
10. Tomko, R.P., R. Xu, and L. Philipson. 1997. HCAR and MCAR: the human and mouse cellular receptors for subgroup C adenoviruses and group B coxsackieviruses. Proc. Natl. Acad. Sci. USA. 94:3352-3356.
11. Sollerbrant, K., E. Raschperger, M. Mirza, U. Engstrom, L. Philipson, P.O. Ljungdahl, and R.F. Pettersson. 2003. The Coxsackievirus and adenovirus receptor (CAR) forms a complex with the PDZ domain-containing protein ligand-of-numb protein-X (LNX). J. Biol. Chem. 278:7439-7444.
12. Coyne, C.B., T. Voelker, S.L. Pichla, and J.M. Bergelson. 2004. The coxsackievirus and adenovirus receptor interacts with the multi-PDZ domain protein-1 (MUPP-1) within the tight junction. J. Biol. Chem. 279:48079-48084.
13. Chung, S.K., J.Y. Kim, I.B. Kim, S.I. Park, K.H. Paek, and J.H. Nam. 2005. Internalization and trafficking mechanisms of coxsackievirus B3 in HeLa cells. Virology. 333:31-40.
14. Asher, D.R., A.M. Cerny, S.R. Weiler, J.W. Horner, M.L. Keeler, M.A. Neptune, S.N. Jones, R.T. Bronson, R.A. Depinho, and R.W. Finberg. 2005. Coxsackievirus and adenovirus receptor is essential for cardiomyocyte development. Genesis. 42:77-85.
15. Dorner, A.A., F. Wegmann, S. Butz, K. Wolburg-Buchholz, H. Wolburg, A. Mack, I. Nasdala, B. August, J. Westermann, F.G. Rathjen, and D. Vestweber. 2005. Coxsackievirus-adenovirus receptor (CAR) is essential for early embryonic cardiac development. J. Cell Sci. 118:3509-3521.
16. Chen, J.W., B. Zhou, Q.C. Yu, S.J. Shin, K. Jiao, M.D. Schneider, H.S. Baldwin, and J.M. Bergelson. 2006. Cardiomyocyte-specific deletion of the coxsackievirus and adenovirus receptor results in hyperplasia of the embryonic left ventricle and abnormalities of sinuatrial valves. Circ. Res. 98:923-930.
17. Agah, R., P.A. Frenkel, B.A. French, L.H. Michael, P.A. Overbeek, and M.D. Schneider. 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.
18. Peng, J., K. Raddatz, J.D. Molkentin, Y. Wu, S. Labeit, H. Granzier, and M. Gotthardt. 2007. Cardiac hypertrophy and reduced contractility in hearts deficient in the titin kinase region. Circulation. 115:743-751.
19. Nikolski, V.P., S.A. Jones, M.K. Lancaster, M.R. Boyett, and I.R. Efimov. 2003. Cx43 and dual-pathway electrophysiology of the atrioventricular node and atrioventricular nodal reentry. Circ. Res. 92:469-475.
20. Ciray, H.N., B.E. Persson, G.M. Roomans, and U. Ulmsten. 1995. Dye-coupling between term pregnant human myometrial cells before labor: carboxyfluorescein versus lucifer yellow. Cell Biol. Int. 19:609-617.
21. Toyofuku, T., M. Yabuki, K. Otsu, T. Kuzuya, M. Hori, and M. Tada. 1998. Direct association of the gap junction protein connexin-43 with ZO-1 in cardiac myocytes. J. Biol. Chem. 273:12725-12731.
22. Thoelen, I., C. Magnusson, S. Tagerud, C. Polacek, M. Lindberg, and M. Van Ranst. 2001. Identification of alternative splice products encoded by the human coxsackie-adenovirus receptor gene. Biochem. Biophys. Res. Commun. 287:216-222.
23. Dorner, A., D. Xiong, K. Couch, T. Yajima, and K.U. Knowlton. 2004. Alternatively spliced soluble coxsackie-adenovirus receptors inhibit coxsackievirus infection. J. Biol. Chem. 279:18497-18503.
24. Nguyen, H.H., J.T. Wolfe III, D.R. Holmes Jr., and W.D. Edwards. 1988. Pathology of the cardiac conduction system in myotonic dystrophy: a study of 12 cases. J. Am. Coll. Cardiol. 11:662-671.
25. Nagasawa, K., H. Chiba, H. Fujita, T. Kojima, T. Saito, T. Endo, and N. Sawada. 2006. Possible involvement of gap junctions in the barrier function of tight junctions of brain and lung endothelial cells. J. Cell. Physiol. 208:123-132.
26. Nishii, K., M. Kumai, K. Egashira, T. Miwa, K. Hashizume, Y. Miyano, and Y. Shibata. 2003. Mice lacking connexin45 conditionally in cardiac myocytes display embryonic lethality similar to that of germline knockout mice without endocardial cushion defect. Cell Commun. Adhes. 10:365-369.
27. Bagwe, S., O. Berenfeld, D. Vaidya, G.E. Morley, and J. Jalife. 2005. Altered right atrial excitation and propagation in connexin40 knockout mice. Circulation. 112:2245-2253.
28. Danik, S.B., G. Rosner, J. Lader, D.E. Gutstein, G.I. Fishman, and G.E. Morley. 2007. Electrical remodeling contributes to complex tachyarrhythmias in connexin43-deficient mouse hearts. FASEB J. 22:1204-1212.
29. Cereijido, M., R.G. Contreras, D. Flores-Benitez, C. Flores-Maldonado, I. Larre, A. Ruiz, and L. Shoshani. 2007. New diseases derived or associated with the tight junction. Arch. Med. Res. 38:465-478.
30. Sato, Y., A. Osaku, S. Koyama, S. Mizukawa, S. Onikura, H. Yagi, T. Suzuki, T. Sawada, T. Uchiyama, and K. Kanmatsuse. 1989. Complete atrioventricular block associated with regional myocardial scarring in a patient with Coxsackie B2 myocarditis. Jpn. Heart J. 30:935-941.
31. Walters, R.W., P. Freimuth, T.O. Moninger, I. Ganske, J. Zabner, and M.J. Welsh. 2002. Adenovirus fiber disrupts CAR-mediated intercellular adhesion allowing virus escape. Cell. 110:789-799.
32. Kishimoto, C., A. Matsumori, M. Ohmae, N. Tomioka, and C. Kawai. 1984. Electrocardiographic findings in experimental myocarditis in DBA/2 mice: complete atrioventricular block in the acute stage, low voltage of the QRS complex in the subacute stage and arrhythmias in the chronic stage. J. Am. Coll. Cardiol. 3:1461-1468.
33. Salomonsson, S., S.E. Sonesson, L. Ottosson, S. Muhallab, T. Olsson, M. Sunnerhagen, V.K. Kuchroo, P. Thoren, E. Herlenius, and M. Wahren-Herlenius. 2005. Ro/SSA autoantibodies directly bind cardiomyocytes, disturb calcium homeostasis, and mediate congenital heart block. J. Exp. Med. 201:11-17.
34. Gotthardt, M., R.E. Hammer, N. Hubner, J. Monti, C.C. Witt, M. McNabb, J.A. Richardson, H. Granzier, S. Labeit, and J. Herz. 2003. Conditional expression of mutant M-line titins results in cardiomyopathy with altered sarcomere structure. J. Biol. Chem. 278:6059-6065.
35. Weinert, S., N. Bergmann, X. Luo, B. Erdmann, and M. Gotthardt. 2006. M line-deficient titin causes cardiac lethality through impaired maturation of the sarcomere. J. Cell Biol. 173:559-570.
36. Royer, A., T.A. van Veen, B.S. Le, C. Marionneau, V. Griol-Charhbili, A.L. Leoni, M. Steenman, H.V. van Rijen, S. Demolombe, C.A. Goddard, et al. 2005. Mouse model of SCN5A-linked hereditary Lenegre ' s disease: age-related conduction slowing and myocardial fibrosis. Circulation. 111:1738-1746.
37. Berul, C.I., M.E. Christe, M.J. Aronovitz, C.E. Seidman, J.G. Seidman, and M.E. Mendelsohn. 1997. Electrophysiological abnormalities and arrhythmias in alpha MHC mutant familial hypertrophic cardiomyopathy mice. J. Clin. Invest. 99:570-576.
38. VanderBrink, B.A., M.S. Link, M.J. Aronovitz, S. Saba, S.B. Sloan, M.K. Homoud, N.A. Estes III, and P.J. Wang. 1999. Assessment of atrioventricular nodal physiology in the mouse. J. Interv. Card. Electrophysiol. 3:207-212.
39. El-Badawi, A., and E.A. Schenk. 1967. Histochemical methods for separate, consecutive and simultaneous demonstration of acetylcholinesterase and norepinephrine in cryostat sections. J. Histochem. Cytochem. 15:580-588.
40. Radke, M.H., J. Peng, Y. Wu, M. McNabb, O.L. Nelson, H. Granzier, and M. Gotthardt. 2007. Targeted deletion of titin N2B region leads to diastolic dysfunction and cardiac atrophy. Proc. Natl. Acad. Sci. USA. 104:3444-3449.
41. Platzer, J., J. Engel, A. Schrott-Fischer, K. Stephan, S. Bova, H. Chen, H. Zheng, and J. Striessnig. 2000. Congenital deafness and sinoatrial node dysfunction in mice lacking class D L-type Ca2+ channels. Cell. 102:89-97.
42. Chen, B., R.T. Bronson, L.D. Klaman, T.G. Hampton, J.F. Wang, P.J. Green, T. Magnuson, P.S. Douglas, J.P. Morgan, and B.G. Neel. 2000. Mice mutant for Egfr and Shp2 have defective cardiac semilunar valvulogenesis. Nat. Genet. 24:296-299.
43. Stephen, L.J., A.L. Fawkes, A. Verhoeve, G. Lemke, and A. Brown. 2007. A critical role for the EphA3 receptor tyrosine kinase in heart development. Dev. Biol. 302:66-79.
44. Kirchhoff, S., E. Nelles, A. Hagendorff, O. Kruger, O. Traub, and K. Willecke. 1998. Reduced cardiac conduction velocity and predisposition to arrhythmias in connexin40-deficient mice. Curr. Biol. 8:299-302.
45. Reaume, A.G., P. A.de Sousa, S. Kulkarni, B.L. Langille, D. Zhu, T.C. Davies, S.C. Juneja, G.M. Kidder, and J. Rossant. 1995. Cardiac malformation in neonatal mice lacking connexin43. Science. 267:1831-1834.
46. Flenniken, A.M., L.R. Osborne, N. Anderson, N. Ciliberti, C. Fleming, J.E. Gittens, X.Q. Gong, L.B. Kelsey, C. Lounsbury, L. Moreno, et al. 2005. A Gja1 missense mutation in a mouse model of oculodentodigital dysplasia. Development. 132:4375-4386.
47. Kumai, M., K. Nishii, K. Nakamura, N. Takeda, M. Suzuki, and Y. Shibata. 2000. Loss of connexin45 causes a cushion defect in early cardiogenesis. Development. 127:3501-3512.
48. Kao, H.J., C.F. Cheng, Y.H. Chen, S.I. Hung, C.C. Huang, D. Millington, T. Kikuchi, J.Y. Wu, and Y.T. Chen. 2006. ENU mutagenesis identifies mice with cardiac fibrosis and hepatic steatosis caused by a mutation in the mitochondrial trifunctional protein beta-subunit. Hum. Mol. Genet. 15:3569-3577.
49. Casimiro, M.C., B.C. Knollmann, S.N. Ebert, J.C. Vary Jr., A.E. Greene, M.R. Franz, A. Grinberg, S.P. Huang, and K. Pfeifer. 2001. Targeted disruption of the Kcnq1 gene produces a mouse model of Jervell and Lange-Nielsen Syndrome. Proc. Natl. Acad. Sci. USA. 98:2526-2531.
50. Arimura, T., A. Helbling-Leclerc, C. Massart, S. Varnous, F. Niel, E. Lacene, Y. Fromes, M. Toussaint, A.M. Mura, D.I. Keller, et al. 2005. Mouse model carrying H222P-Lmna mutation develops muscular dystrophy and dilated cardiomyopathy similar to human striated muscle laminopathies. Hum. Mol. Genet. 14:155-169.
51. Biben, C., R. Weber, S. Kesteven, E. Stanley, L. McDonald, D.A. Elliott, L. Barnett, F. Koentgen, L. Robb, M. Feneley, and R.P. Harvey. 2000. Cardiac septal and valvular dysmorphogenesis in mice heterozygous for mutations in the homeobox gene Nkx2-5. Circ. Res. 87:888-895.
52. Jay, P.Y., B.S. Harris, C.T. Maguire, A. Buerger, H. Wakimoto, M. Tanaka, S. Kupershmidt, D.M. Roden, T.M. Schultheiss, T.X. O ' Brien, et al. 2004. Nkx2-5 mutation causes anatomic hypoplasia of the cardiac conduction system. J. Clin. Invest. 113:1130-1137.
53. Papadatos, G.A., P.M. Wallerstein, C.E. Head, R. Ratcliff, P.A. Brady, K. Benndorf, R.C. Saumarez, A.E. Trezise, C.L. Huang, J.I. Vandenberg, et al. 2002. Slowed conduction and ventricular tachycardia after targeted disruption of the cardiac sodium channel gene Scn5a. Proc. Natl. Acad. Sci. USA. 99:6210-6215.
54. Remme, C.A., A.O. Verkerk, D. Nuyens, A.C. van Ginneken, S. van Brunschott, C.N. Belterman, R. Wilders, M.A. van Roon, H.L. Tan, A.A. Wilde, P. Carmeliet, J.M. de Bakker, M.W. Veldkamp, and C.R. Bezzina. 2006. Overlap syndrome of cardiac sodium channel disease in mice carrying the equivalent mutation of human SCN5A-1795insD. Circulation. 114:2584-2594.
55. Moskowitz, I.P., A. Pizard, V.V. Patel, B.G. Bruneau, J.B. Kim, S. Kupershmidt, D. Roden, C.I. Berul, C.E. Seidman, and J.G. Seidman. 2004. The T-Box transcription factor Tbx5 is required for the patterning and maturation of the murine cardiac conduction system. Development. 131:4107-4116.
56. Mori, A.D., Y. Zhu, I. Vahora, B. Nieman, K. Koshiba-Takeuchi, L. Davidson, A. Pizard, J.G. Seidman, C.E. Seidman, X.J. Chen, et al. 2006. Tbx5-dependent rheostatic control of cardiac gene expression and morphogenesis. Dev. Biol. 297:566-586.
57. Hein, L., M.E. Stevens, G.S. Barsh, R.E. Pratt, B.K. Kobilka, and V.J. Dzau. 1997. Overexpression of angiotensin AT1 receptor transgene in the mouse myocardium produces a lethal phenotype associated with myocyte hyperplasia and heart block. Proc. Natl. Acad. Sci. USA. 94:6391-6396.
58. Chen, H.H., C.J. Baty, T. Maeda, S. Brooks, L.C. Baker, T. Ueyama, E. Gursoy, S. Saba, G. Salama, B. London, and A.F. Stewart. 2004. Transcription enhancer factor-1-related factor-transgenic mice develop cardiac conduction defects associated with altered connexin phosphorylation. Circulation. 110:2980-2987.
59. Aase, K., G. von Euler, X. Li, A. Ponten, P. Thoren, R. Cao, Y. Cao, B. Olofsson, S. Gebre-Medhin, M. Pekny, K. Alitalo, C. Betsholtz, and U. Eriksson. 2001. Vascular endothelial growth factor-B-deficient mice display an atrial conduction defect. Circulation. 104:358-364.