Acute slowing of cardiac conduction in response to myofibroblast coupling to cardiomyocytes through N-cadherin

Journal of Molecular and Cellular Cardiology

Volumn 68, Issue , 2014, Pages 29-37

  Thompson, Susan A ^a   Blazeski, Adriana ^a   Copeland, Craig R ^b   Cohen, Daniel M ^c   Chen, Christopher S ^c   Reich, Daniel M ^b   Tung, Leslie ^a  

^a Johns Hopkins University   (United States)

^b JOHNS HOPKINS UNIVERSITY   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Cadherin; Cardiomyocyte; Electrophysiology; Mechanobiology; Myofibroblast; Optical mapping

Indexed keywords

CADHERIN; CARDIOMYOCYTE; ELECTROPHYSIOLOGY; MECHANOBIOLOGY; MYOFIBROBLAST; OPTICAL MAPPING;

ADHERENS JUNCTIONS; ANIMALS; CADHERINS; CELL MOVEMENT; CELLS, CULTURED; COCULTURE TECHNIQUES; EXCITATION CONTRACTION COUPLING; HEART CONDUCTION SYSTEM; MUTATION, MISSENSE; MYOCARDIAL CONTRACTION; MYOCYTES, CARDIAC; MYOFIBROBLASTS; NERVE TISSUE PROTEINS; RATS; RHOA GTP-BINDING PROTEIN;

EID: 84894238647     PISSN: 00222828     EISSN: 10958584     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2013.12.025     Document Type: Article

References (39)

1. Dobaczewski M., Bujak M., Zymek P., Ren G., Entman M., Frangogiannis N. Extracellular matrix remodeling in canine and mouse myocardial infarcts. Cell Tissue Res 2006, 324:475-488.
2. Souders C.A., Bowers S.L.K., Baudino T.A. Cardiac fibroblast: the renaissance cell. Circ Res 2009, 105:1164-1176.
3. Rohr S. Arrhythmogenic implications of fibroblast-myocyte interactions. Circ Arrhythm Electrophysiol 2012, 5:442-452.
4. Brown R.D., Ambler S.K., Mitchell M.D., Long C.S. The cardiac fibroblast: therapeutic target in myocardial remodeling and failure. Annu Rev Pharmacol Toxicol 2005, 45:657-687.
5. Tomasek J.J., Gabbiani G., Hinz B., Chaponnier C., Brown R.A. Myofibroblasts and mechano-regulation of connective tissue remodelling. Nat Rev Mol Cell Biol 2002, 3:349-363.
6. Castella L.F., Buscemi L., Godbout C., Meister J.-J., Hinz B. A new lock-step mechanism of matrix remodelling based on subcellular contractile events. J Cell Sci 2010, 123:1751-1760.
7. Thompson S.A., Copeland C.R., Reich D.H., Tung L. Mechanical coupling between myofibroblasts and cardiomyocytes slows electric conduction in fibrotic cell monolayers. Circulation 2011, 123:2083-2093.
8. SdF Askar, Bingen B.O., Swildens J., Ypey D.L., van der Laarse A., Atsma D.E., et al. Connexin43 silencing in myofibroblasts prevents arrhythmias in myocardial cultures: role of maximal diastolic potential. Cardiovasc Res 2012, 93:434-444.
9. Rosker C., Salvarani N., Schmutz S., Grand T., Rohr S. Abolishing myofibroblast arrhythmogeneicity by pharmacological ablation of α-smooth muscle actin containing stress fibers. Circ Res 2012, 109:1120-1131.
10. Kamkin A., Kiseleva I., Wagner K.-D., Leiterer K.P., Theres H., Scholz H., et al. Mechano-electric feedback in right atrium after left ventricular infarction in rats. J Mol Cell Cardiol 2000, 32:465-477.
11. Kamkin A., Kiseleva I., Lozinsky I. The role of mechanosensitive fibroblasts in the heart: evidence from acutely isolated single cells, cultured cells and from intracellular microelectrode recordings on multicellular preparations from healthy and diseased cardiac tissue. Mechanosensitivity of the Heart 2010, 239-266. Springer Netherlands.
12. Ganz A., Lambert M., Saez A., Silberzan P., Buguin A., Mège R.M., et al. Traction forces exerted through N-cadherin contacts. Biol Cell 2006, 98:721-730.
13. Liu Z., Tan J.L., Cohen D.M., Yang M.T., Sniadecki N.J., Ruiz S.A., et al. Mechanical tugging force regulates the size of cell-cell junctions. Proc Natl Acad Sci U S A 2010, 107:9944-9949.
14. Hinz B., Pittet P., Smith-Clerc J., Chaponnier C., Meister J.J. Myofibroblast development is characterized by specific cell-cell adherens junctions. Mol Biol Cell 2004, 15:4310-4320.
15. Pittet P., Lee K., Kulik A.J., Meister J.-J., Hinz B. Fibrogenic fibroblasts increase intercellular adhesion strength by reinforcing individual OB-cadherin bonds. J Cell Sci 2008, 121:877-886.
16. Baudino T.A., McFadden A., Fix C., Hastings J., Price R., Borg T.K. Cell patterning: interaction of cardiac myocytes and fibroblasts in three-dimensional culture. Microsc Microanal 2008, 14:117-125.
17. Zuppinger C., Schaub M.C., Eppenberger H.M. Dynamics of early contact formation in cultured adult rat cardiomyocytes studied by N-cadherin fused to green fluorescent protein. J Mol Cell Cardiol 2000, 32:539-555.
18. De Wever O., Westbroek W., Verloes A., Bloemen N., Bracke M., Gespach C., et al. Critical role of N-cadherin in myofibroblast invasion and migration in vitro stimulated by colon-cancer-cell-derived TGF-beta or wounding. J Cell Sci 2004, 117:4691-4703.
19. Angst B.D., Khan L.U., Severs N.J., Whitely K., Rothery S., Thompson R.P., et al. Dissociated spatial patterning of gap junctions and cell adhesion junctions during postnatal differentiation of ventricular myocardium. Circ Res 1997, 80:88-94.
20. Kostin S., Hein S., Bauer E.P., Schaper J. Spatiotemporal development and distribution of intercellular junctions in adult rat cardiomyocytes in culture. Circ Res 1999, 85:154-167.
21. Kostetskii I., Li J., Xiong Y., Zhou R., Ferrari V.A., Patel V.V., et al. Induced deletion of the N-cadherin gene in the heart leads to dissolution of the intercalated disc structure. Circ Res 2005, 96:346-354.
22. Matsuda T., Fujio Y., Nariai T., Ito T., Yamane M., Takatani T., et al. N-cadherin signals through Rac1 determine the localization of connexin 43 in cardiac myocytes. J Mol Cell Cardiol 2006, 40:495-502.
23. Ko K.S., Arora P.D., McCulloch C.A.G. Cadherins mediate intercellular mechanical signaling in fibroblasts by activation of stretch-sensitive calcium-permeable channels. J Biol Chem 2001, 276:35967-35977.
24. Follonier L., Schaub S., Meister J.-J., Hinz B. Myofibroblast communication is controlled by intercellular mechanical coupling. J Cell Sci 2008, 121:3305-3316.
25. Marrs G.S., Theisen C.S., Brusés J.L. N-cadherin modulates voltage activated calcium influx via RhoA, p120-catenin, and myosin-actin interaction. Mol Cell Neurosci 2009, 40:390-400.
26. Koutsouki E., Lam R.S., Seebohm G., Ureche O.N., Ureche L., Baltaev R., et al. Modulation of human Kv1.5 channel kinetics by N-cadherin. Biochem Biophys Res Commun 2007, 363:18-23.
27. van den Borne S.W.M., Diez J., Blankesteijn W.M., Verjans J., Hofstra L., Narula J. Myocardial remodeling after infarction: the role of myofibroblasts. Nat Rev Cardiol 2009, 7:30-37.
28. Samarel A.M. Costameres, focal adhesions, and cardiomyocyte mechanotransduction. Am J Physiol Heart Circ Physiol 2005, 289:H2291-H2301.
29. Weber G.F., Bjerke M.A., DeSimone D.W. Integrins and cadherins join forces to form adhesive networks. J Cell Sci 2011, 124:1183-1193.
30. Chopra A., Tabdanov E., Patel H., Janmey P.A., Kresh J.Y. Cardiac myocyte remodeling mediated by N-cadherin-dependent mechanosensing. Am J Physiol Heart Circ Physiol 2011, 300:H1252-H1266.
31. Lloyd C.W., Rees D.A., Smith C.G., Judge F.J. Mechanisms of cell adhesion: early-forming junctions between aggregating fibroblasts. J Cell Sci 1976, 22:671-684.
32. Haraguchi Y., Shimizu T., Yamato M., Okano T. Electrical interaction between cardiomyocyte sheets separated by non-cardiomyocyte sheets in heterogeneous tissues. J Tissue Eng Regen Med 2010, 4:291-299.
33. Driesen R.B., Dispersyn G.D., Verheyen F.K., van den Eijnde S.M., Hofstra L., Thoné F., et al. Partial cell fusion: a newly recognized type of communication between dedifferentiating cardiomyocytes and fibroblasts. Cardiovasc Res 2005, 68:37-46.
34. Noorman M., van der Heyden M.A., van Veen T.A., Cox M.G., Hauer R.N., de Bakker J.M., et al. Cardiac cell-cell junctions in health and disease: electrical versus mechanical coupling. J Mol Cell Cardiol 2009, 47:23-31.
35. Zuppinger C., Eppenberger-Eberhardt M., Eppenberger H.M. N-cadherin: structure, function and importance in the formation of new intercalated disc-Like cell contacts in cardiomyocytes. Heart Fail Rev 2000, 5:251-257.
36. Katsamba P., Carroll K., Ahlsen G., Bahna F., Vendome J., Posy S., et al. Linking molecular affinity and cellular specificity in cadherin-mediated adhesion. Proc Natl Acad Sci U S A 2009, 106:11594-11599.
37. Omelchenko T., Fetisova E., Ivanova O., Bonder E.M., Feder H., Vasiliev J.M., et al. Contact interactions between epitheliocytes and fibroblasts: formation of heterotypic cadherin-containing adhesion sites is accompanied by local cytoskeletal reorganization. Proc Natl Acad Sci U S A 2001, 98:8632-8637.
38. Ferreira-Cornwell M.C., Luo Y., Narula N., Lenox J.M., Lieberman M., Radice G.L. Remodeling the intercalated disc leads to cardiomyopathy in mice misexpressing cadherins in the heart. J Cell Sci 2002, 115:1623-1634.
39. Duffy H.S. Fibroblasts, myofibroblasts, and fibrosis: fact, fiction, and the future. J Cardiovasc Pharmacol 2011, 57:373-375.