Ephrin-B1 is a novel specific component of the lateral membrane of the cardiomyocyte and is essential for the stability of cardiac tissue architecture cohesion

Circulation Research

Volumn 110, Issue 5, 2012, Pages 688-700

  Genet, Gaël ^a   Guilbeau Frugier, Céline ^b   Honton, Benjamin ^a   Dague, Etienne ^b   Schneider, Michael D ^c   Coatrieux, Christelle ^a   Calise, Denis ^a   Cardin, Christelle ^a   Nieto, Cécile ^c   Payré, Bruno ^c   Dubroca, Caroline ^a   Marck, Pauline ^a   Heymes, Christophe ^a   Dubrac, Alexandre ^a   Arvanitis, Dina ^d   Despas, Fabien ^a,b   Altié, Marie Françoise ^a   Seguelas, Marie Hélène ^a   Delisle, Marie Bernadette ^b   Davy, Alice ^d   Sénard, Jean Michel ^a,b   Pathak, Atul ^a,b   Galés, Céline ^a   more..

^a Institut National de la Santé   (United Kingdom)

^b CNRS   (France)

^c UNIVERSITÉ PAUL SABATIER   (France)

^d CNRS   (United Kingdom)

Author keywords

architecture; cardiac tissue; cardiomyocyte; extracellular matrix; heart failure; lateral membrane

Indexed keywords

CLAUDIN 5; DYSTROGLYCAN; EPHRIN B1; FIBRILLAR COLLAGEN; UBIQUINONE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; ATOMIC FORCE MICROSCOPY; ATRIOVENTRICULAR CONDUCTION; CARDIAC TISSUE ARCHITECTURE COHESION; CELL ADHESION; DOWN REGULATION; ELECTRON MICROSCOPY; ENDOTHELIUM CELL; GENE EXPRESSION; HEART; HEART MUSCLE CELL; HEART MUSCLE COMPLIANCE; HEART STRESS; HEART VENTRICLE SIZE; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; WILD TYPE;

ANIMALS; CELL COMMUNICATION; CELL MEMBRANE; CELLS, CULTURED; COLLAGEN; ENDOTHELIUM, VASCULAR; EPHRIN-B1; MALE; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MODELS, ANIMAL; MYOCYTES, CARDIAC; SARCOMERES;

EID: 84857911170     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.111.262451     Document Type: Article

References (42)

1. Brancaccio M, Hirsch E, Notte A, Selvetella G, Lembo G, Tarone G. Integrin signalling: the tug-of-war in heart hypertrophy. Cardiovasc Res. 2006;70:422-433.
2. Li J, Patel VV, Radice GL. Dysregulation of cell adhesion proteins and cardiac arrhythmogenesis. Clin Med Res. 2006;4:42-52.
3. Noorman M, van der Heyden MA, van Veen TA, Cox MG, Hauer RN, de Bakker JM, van Rijen HV. Cardiac cell-cell junctions in health and disease: electrical versus mechanical coupling. J Mol Cell Cardiol. 2009; 47:23-31.
4. Lapidos KA, Kakkar R, McNally EM. The dystrophin glycoprotein complex: signaling strength and integrity for the sarcolemma. Circ Res. 2004;94:1023-1031. (Pubitemid 38579696)
5. Samarel AM. Costameres, focal adhesions, and cardiomyocyte mechanotransduction. Am J Physiol Heart Circ Physiol. 2005;289:H2291-H2301. (Pubitemid 41698534)
6. Kullander K, Klein R. Mechanisms and functions of Eph and ephrin signalling. Nat Rev Mol Cell Biol. 2002;3:475-486. (Pubitemid 34733429)
7. Kuijper S, Turner CJ, Adams RH. Regulation of angiogenesis by Eph-ephrin interactions. Trends Cardiovasc Med. 2007;17:145-151. (Pubitemid 46898841)
8. Pasquale EB. Eph-ephrin bidirectional signaling in physiology and disease. Cell. 2008;133:38-52. (Pubitemid 351442996)
9. Merlos-Suarez A, Batlle E. Eph-ephrin signalling in adult tissues and cancer. Curr Opin Cell Biol. 2008;20:194-200.
10. Zhao C, Irie N, Takada Y, Shimoda K, Miyamoto T, Nishiwaki T, Suda T, Matsuo K. Bidirectional ephrinB2-EphB4 signaling controls bone homeostasis. Cell Metab. 2006;4:111-121. (Pubitemid 44138718)
11. Konstantinova I, Nikolova G, Ohara-Imaizumi M, Meda P, Kucera T, Zarbalis K, Wurst W, Nagamatsu S, Lammert E. EphA-Ephrin-A-mediated beta cell communication regulates insulin secretion from pancreatic islets. Cell. 2007;129:359-370. (Pubitemid 46574973)
12. Ogawa K, Wada H, Okada N, Harada I, Nakajima T, Pasquale EB, Tsuyama S. EphB2 and ephrin-B1 expressed in the adult kidney regulate the cytoarchitecture of medullary tubule cells through Rho family GTPases. J Cell Sci. 2006;119:559-570.
13. Cooper MA, Son AI, Komlos D, Sun Y, Kleiman NJ, Zhou R. Loss of ephrin-A5 function disrupts lens fiber cell packing and leads to cataract. Proc Natl Acad Sci U S A. 2008;105:16620-16625.
14. Stephen LJ, Fawkes AL, Verhoeve A, Lemke G, Brown A. A critical role for the EphA3 receptor tyrosine kinase in heart development. Dev Biol. 2007;302:66-79. (Pubitemid 46096924)
15. Ishii M, Mueller I, Nakajima T, Pasquale EB, Ogawa K. EphB signaling inhibits gap junctional intercellular communication and synchronized contraction in cultured cardiomyocytes. Basic Res Cardiol:1057-1068.
16. Twigg SR, Matsumoto K, Kidd AM, Goriely A, Taylor IB, Fisher RB, Hoogeboom AJ, Mathijssen IM, Lourenco MT, Morton JE, Sweeney E, Wilson LC, Brunner HG, Mulliken JB, Wall SA, Wilkie AO. The origin of EFNB1 mutations in craniofrontonasal syndrome: frequent somatic mosaicism and explanation of the paucity of carrier males. Am J Hum Genet. 2006;78:999-1010. (Pubitemid 43787691)
17. Davy A, Bush JO, Soriano P. Inhibition of gap junction communication at ectopic Eph/ephrin boundaries underlies craniofrontonasal syndrome. PLoS Biol. 2006;4:e315.
18. Lee HS, Nishanian TG, Mood K, Bong YS, Daar IO. EphrinB1 controls cell-cell junctions through the Par polarity complex. Nat Cell Biol. 2008;10:979-986.
19. Huynh-Do U, Stein E, Lane AA, Liu H, Cerretti DP, Daniel TO. Surface densities of ephrin-B1 determine EphB1-coupled activation of cell attachment through alphavbeta3 and alpha5beta1 integrins. Embo J. 1999; 18:2165-2173. (Pubitemid 29179173)
20. Huynh-Do U, Vindis C, Liu H, Cerretti DP, McGrew JT, Enriquez M, Chen J, Daniel TO. Ephrin-B1 transduces signals to activate integrin-mediated migration, attachment and angiogenesis. J Cell Sci. 2002;115:3073-3081.
21. Davy A, Aubin J, Soriano P. EphrinB1 forward and reverse signaling are required during mouse development. Genes Dev. 2004;18:572-583. (Pubitemid 38372813)
22. Sanford JL, Edwards JD, Mays TA, Gong B, Merriam AP, Rafael-Fortney JA. Claudin-5 localizes to the lateral membranes of cardiomyocytes and is altered in utrophin/dystrophin-deficient cardiomyopathic mice. J Mol Cell Cardiol. 2005;38:323-332. (Pubitemid 40215202)
23. Li J, Patel VV, Kostetskii I, Xiong Y, Chu AF, Jacobson JT, Yu C, Morley GE, Molkentin JD, Radice GL. Cardiac-specific loss of N-cadherin leads to alteration in connexins with conduction slowing and arrhythmogenesis. Circ Res. 2005;97:474-481. (Pubitemid 41298178)
24. Konieczny P, Fuchs P, Reipert S, Kunz WS, Zeold A, Fischer I, Paulin D, Schroder R, Wiche G. Myofiber integrity depends on desmin network targeting to Z-disks and costameres via distinct plectin isoforms. J Cell Biol. 2008;181:667-681. (Pubitemid 351717513)
25. Wang X, Osinska H, Dorn GW II, Nieman M, Lorenz JN, Gerdes AM, Witt S, Kimball T, Gulick J, Robbins J. Mouse model of desmin-related cardiomyopathy. Circulation. 2001;103:2402-2407. (Pubitemid 32448807)
26. Lairez O, Calise D, Bianchi P, Ordener C, Spreux-Varoquaux O, Guilbeau-Frugier C, Escourrou G, Seif I, Roncalli J, Pizzinat N, Galinier M, Parini A, Mialet-Perez J. Genetic deletion of MAO-A promotes serotonin-dependent ventricular hypertrophy by pressure overload. J Mol Cell Cardiol. 2009;46:587-595.
27. Silver MDGAISFJ. Chapter 10: cardiomyoapthies, 2001.
28. Danialou G, Comtois AS, Dudley R, Karpati G, Vincent G, Des Rosiers C, Petrof BJ. Dystrophin-deficient cardiomyocytes are abnormally vulnerable to mechanical stress-induced contractile failure and injury. Faseb J. 2001;15:1655-1657.
29. Paulin D, Li Z. Desmin: a major intermediate filament protein essential for the structural integrity and function of muscle. Exp Cell Res. 2004;301:1-7. (Pubitemid 39388889)
30. Ross RS, Borg TK. Integrins and the myocardium. Circ Res. 2001;88: 1112-1119. (Pubitemid 34132510)
31. Arvanitis D, Davy A. Eph/ephrin signaling: networks. Genes Dev. 2008; 22:416-429. (Pubitemid 351272750)
32. Gregory M, Dufresne J, Hermo L, Cyr D. Claudin-1 is not restricted to tight junctions in the rat epididymis. Endocrinology. 2001;142:854-863. (Pubitemid 32222436)
33. Harris HJ, Davis C, Mullins JG, Hu K, Goodall M, Farquhar MJ, Mee CJ, McCaffrey K, Young S, Drummer H, Balfe P, McKeating JA. Claudin association with CD81 defines hepatitis C virus entry. J Biol Chem. 285: 21092-21102.
34. Goodenough DA, Paul DL. Beyond the gap: functions of unpaired connexon channels. Nat Rev Mol Cell Biol. 2003;4:285-294. (Pubitemid 36383955)
35. Barresi R, Di Blasi C, Negri T, Brugnoni R, Vitali A, Felisari G, Salandi A, Daniel S, Cornelio F, Morandi L, Mora M. Disruption of heart sarcoglycan complex and severe cardiomyopathy caused by beta sarcoglycan mutations. J Med Genet. 2000;37:102-107. (Pubitemid 30245892)
36. Milner DJ, Taffet GE, Wang X, Pham T, Tamura T, Hartley C, Gerdes AM, Capetanaki Y. The absence of desmin leads to cardiomyocyte hypertrophy and cardiac dilation with compromised systolic function. J Mol Cell Cardiol. 1999;31:2063-2076. (Pubitemid 29537605)
37. Sakamoto A, Ono K, Abe M, Jasmin G, Eki T, Murakami Y, Masaki T, Toyo-oka T, Hanaoka F. Both hypertrophic and dilated cardiomyopathies are caused by mutation of the same gene, delta-sarcoglycan, in hamster: an animal model of disrupted dystrophin-associated glycoprotein complex. Proc Natl Acad Sci U S A. 1997;94:13873-13878. (Pubitemid 28009677)
38. Shai SY, Harpf AE, Babbitt CJ, Jordan MC, Fishbein MC, Chen J, Omura M, Leil TA, Becker KD, Jiang M, Smith DJ, Cherry SR, Loftus JC, Ross RS. Cardiac myocyte-specific excision of the beta1 integrin gene results in myocardial fibrosis and cardiac failure. Circ Res. 2002;90: 458-464. (Pubitemid 34633916)
39. Rasi K, Piuhola J, Czabanka M, Sormunen R, Ilves M, Leskinen H, Rysa J, Kerkela R, Janmey P, Heljasvaara R, Peuhkurinen K, Vuolteenaho O, Ruskoaho H, Vajkoczy P, Pihlajaniemi T, Eklund L. Collagen XV is necessary for modeling of the extracellular matrix and its deficiency predisposes to cardiomyopathy. Circ Res. 2010;107:1241-1252.
40. Aumailley M, Pesch M, Tunggal L, Gaill F, Fassler R. Altered synthesis of laminin 1 and absence of basement membrane component deposition in (beta)1 integrin-deficient embryoid bodies. J Cell Sci. 2000;113(Pt 2):259-268. (Pubitemid 30088971)
41. Boulaksil M, Winckels SK, Engelen MA, et al. Heterogeneous connexin43 distribution in heart failure is associated with dispersed conduction and enhanced susceptibility to ventricular arrhythmias. Eur J Heart Fail. 2010;12:913-921.
42. Mays TA, Binkley PF, Lesinski A, Doshi AA, Quaile MP, Margulies KB, Janssen PM, Rafael-Fortney JA. Claudin-5 levels are reduced in human end-stage cardiomyopathy. J Mol Cell Cardiol. 2008;45:81-87.