Epithelial-to-mesenchymal transformation alters electrical conductivity of human epicardial cells

Journal of Cellular and Molecular Medicine

Volumn 15, Issue 12, 2011, Pages 2675-2683

  Bax, Noortje A M ^a   Pijnappels, Daniël A ^a   van Oorschot, Angelique A M ^a   Winter, Elizabeth M ^a   de Vries, Antoine A F ^a   van Tuyn, John ^a   Braun, Jerry ^a   Maas, Saskia ^a   Schalij, Martin J ^a   Atsma, Douwe E ^a   Goumans, Marie José ^a   Gittenberger de Groot, Adriana C ^a  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Electrical conduction; EPDCs; Epicardium; Epithelial to mesenchymal transformation

Indexed keywords

MESSENGER RNA;

ANIMAL; ARTICLE; CELL CULTURE; CELL DIFFERENTIATION; CYTOLOGY; ELECTRIC CONDUCTIVITY; EPITHELIAL MESENCHYMAL TRANSITION; FLUORESCENCE MICROSCOPY; GENETICS; HEART MUSCLE; HEART MUSCLE CELL; HUMAN; MALE; METABOLISM; PERICARDIUM; PHYSIOLOGY; RAT; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING; WISTAR RAT;

ANIMALS; BLOTTING, WESTERN; CELL DIFFERENTIATION; CELLS, CULTURED; ELECTRIC CONDUCTIVITY; EPITHELIAL-MESENCHYMAL TRANSITION; HUMANS; MALE; MICROSCOPY, FLUORESCENCE; MYOCARDIUM; MYOCYTES, CARDIAC; PERICARDIUM; RATS; RATS, WISTAR; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER;

EID: 82555193327     PISSN: 15821838     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1582-4934.2011.01266.x     Document Type: Article

References (44)

1. Lie-Venema H, van den Akker NMS, Bax NAM, et al. Origin, fate, and function of epicardium-derived cells (EPDCs) in normal and abnormal cardiac development. Sci World J. 2007; 7: 1777-98.
2. Winter EM, Grauss RW, Hogers B, et al. Preservation of left ventricular function and attenuation of remodeling after transplantation of human epicardium-derived cells into the infarcted mouse heart. Circulation. 2007; 116: 917-27.
3. Gittenberger-de Groot AC, Vrancken Peeters M-PFM, Mentink MMT, et al. Epicardium-derived cells contribute a novel population to the myocardial wall and the atrioventricular cushions. Circ Res. 1998; 82: 1043-52.
4. Dettman RW, Denetclaw W, Ordahl CP, et al. Common epicardial origin of coronary vascular smooth muscle, perivascular fibroblasts, and intermyocardial fibroblasts in the avian heart. Dev Biol. 1998; 193: 169-81.
5. Vrancken Peeters M-PFM, Gittenberger-de Groot AC, Mentink MMT, et al. Smooth muscle cells and fibroblasts of the coronary arteries derive from epithelial-mesenchymal transformation of the epicardium. Anat Embryol. 1999; 199: 367-78.
6. Eralp I, Lie-Venema H, DeRuiter MC, et al. Coronary artery and orifice development is associated with proper timing of epicardial outgrowth and correlated Fas ligand associated apoptosis patterns. Circ Res. 2005; 96: 526-34.
7. Gittenberger-de Groot AC, Vrancken Peeters M-PFM, Bergwerff M, et al. Epicardial outgrowth inhibition leads to compensatory mesothelial outflow tract collar and abnormal cardiac septation and coronary formation. Circ Res. 2000; 87: 969-71.
8. Van Loo PF, Mahtab EAF, Wisse LJ, et al. Transcription Factor Sp3 knockout mice display serious cardiac malformations. Mol Cell Biol. 2007; 27: 8571-82.
9. Mahtab EAF, Wijffels MCEF, van den Akker NMS, et al. Cardiac malformations and myocardial abnormalities in podoplanin knockout mouse embryos: correlation with abnormal epicardial development. Dev Dyn. 2008; 237: 847-57.
10. Eralp I, Lie-Venema H, Bax NAM, et al. Epicardium-derived cells are important for correct development of the Purkinje fibers in the avian heart. Anat Rec. 2006; 288A: 1272-80.
11. Eid H, Larson DM, Springhorn JP, et al. Role of epicardial mesothelial cells in the modification of phenotype and function of adult rat ventricular myocytes in primary coculture. Circ Res. 1992; 71: 40-50.
12. van Tuyn J, Atsma DE, Winter EM, et al. Epicardial cells of human adults can undergo an epithelial-to-mesenchymal transition and obtain characteristics of smooth muscle cellsin vitro. Stem Cells. 2007; 25: 271-8.
13. Winter EM, Grauss RW, Hogers B, et al. Preservation of left ventricular function and attenuation of remodeling after transplantation of human epicardium-derived cells into the infarcted mouse heart. Circulation. 2007; 116: 917-27.
14. Wills AA, Holdway JE, Major RJ, et al. Regulated addition of new myocardial and epicardial cells fosters homeostatic cardiac growth and maintenance in adult zebrafish. Development. 2008; 135: 183-92.
15. Gittenberger-de Groot AC. Epicardium-derived cells (EPDCs) in development, cardiac disease and repair of ischemia. J Cell Mol Med. 2010; 14: 1056-60.
16. Smart N, Risebro CA, Melville AA, et al. Thymosin beta4 induces adult epicardial progenitor mobilization and neovascularization. Nature. 2007; 445: 177-82.
17. Winter EM, Van Oorschot AA, Hogers B, et al. A new direction for cardiac regeneration therapy: application of synergistically acting epicardium-derived cells and cardiomyocyte progenitor cells. Circ Heart Fail. 2009; 2: 643-53.
18. Leobon B, Garcin I, Menasche P, et al. Myoblasts transplanted into rat infarcted myocardium are functionally isolated from their host. Proc Natl Acad Sci USA. 2003; 100: 7808-11.
19. Gaudesius G, Miragoli M, Thomas SP, et al. Coupling of cardiac electrical activity over extended distances by fibroblasts of cardiac origin. Circ Res. 2003; 93: 421-8.
20. Pijnappels DA, Schalij MJ, van Tuyn J, et al. Progressive increase in conduction velocity across human mesenchymal stem cells is mediated by enhanced electrical coupling. Cardiovasc Res. 2006; 72: 282-91.
21. Pijnappels DA, van Tuyn J, de Vries AA, et al. Resynchronization of separated rat cardiomyocyte fields with genetically modified human ventricular scar fibroblasts. Circulation. 2007; 116: 2018-28.
22. Pijnappels DA, Schalij MJ, Ramkisoensing AA, et al. Forced alignment of mesenchymal stem cells undergoing cardiomyogenic differentiation affects functional integration with cardiomyocyte cultures. Circ Res. 2008; 103: 167-76.
23. Winter EM, Gittenberger-de Groot AC. Cardiovascular development: towards biomedical applicability: epicardium-derived cells in cardiogenesis and cardiac regeneration. Cell Mol Life Sci. 2007; 64: 692-703.
24. Manner J. Extracardiac tissues and the epigenetic control of myocardial development in vertebrate embryos. Ann Anat. 2006; 188: 199-212.
25. Abu-Issa R, Waldo K, Kirby ML. Heart fields: one, two or more? Dev Biol. 2004; 272: 281-5.
26. Jongbloed MR, Mahtab EAF, Blom NA, et al. Development of the cardiac conduction system and the possible relation to predilection sites of arrhythmogenesis. Sci World J. 2008; 8:239-69.
27. Gourdie RG, Wei Y, Kim D, et al. Endothelin-induced conversion of embryonic heart muscle cells into impulse-conducting Purkinje fibers. Proc Natl Acad Sci USA. 1998; 95: 6815-8.
28. Hyer J, Johansen M, Prasad A, et al. Induction of purkinje fiber differentiation by coronary arterialization. Proc Natl Acad Sci USA. 1999; 96: 13214-8.
29. Zhou B, Ma Q, Rajagopal S, et al. Epicardial progenitors contribute to the cardiomyocyte lineage in the developing heart. Nature. 2008; 454: 109-13.
30. Camelliti P, Borg TK, Kohl P. Structural and functional characterisation of cardiac fibroblasts. Cardiovasc Res. 2005; 65: 40-51.
31. Mercado-Pimentel ME, Runyan RB. Multiple transforming growth factor β isoforms and receptors function during epithelial-mesenchymal cell transformation in the embryonic heart. Cells Tissues Organs. 2007; 185: 146-56.
32. Nishii K, Kumai M, Shibata Y. Regulation of the epithelial-mesenchymal transformation through gap junction channels in heart development. Trends Cardiovasc Med. 2001; 11: 213-8.
33. Wu JC, Tsai RY, Chung TH. Role of catenins in the development of gap junctions in rat cardiomyocytes. J Cell Biochem. 2003; 88: 823-35.
34. Luo Y, High FA, Epstein JA, et al. N-cadherin is required for neural crest remodeling of the cardiac outflow tract. Dev Biol. 2006; 299: 517-28.
35. Ai Z, Fischer A, Spray DC, et al. Wnt-1 regulation of connexin43 in cardiac myocytes. J Clin Invest. 2000; 105: 161-71.
36. Li J, Patel VV, Kostetskii I, et al. Cardiac-specific loss of N-cadherin leads to alteration in connexins with conduction slowing and arrhythmogenesis. Circ Res. 2005; 97: 474-81.
37. de Boer TP, van Veen TA, Bierhuizen MF, et al. Connexin43 repression following epithelium-to-mesenchyme transition in embryonal carcinoma cells requires Snail1 transcription factor. Differentiation. 2007; 75: 208-18.
38. Brink PR. Gap junctions in vascular smooth muscle. Acta Physiol Scand. 1998; 164: 349-56.
39. Dhein S, Hagen A, Jozwiak J, et al. Improving cardiac gap junction communication as a new antiarrhythmic mechanism: the action of antiarrhythmic peptides. Naunyn Schmiedebergs Arch Pharmacol. 2010; 381: 221-34.
40. Coppen SR, Dupont E, Rothery S, et al. Connexin45 expression is preferentially associated with the ventricular conduction system in mouse and rat heart. Circ Res. 1998; 82: 232-43.
41. Huber SM, Braun GS, Segerer S, et al. Metanephrogenic mesenchyme-to-epithelium transition induces profound expression changes of ion channels. Am J Physiol Renal Physiol. 2000; 279: F65-76.
42. Compton LA, Potash DA, Mundell NA, et al. Transforming growth factor-beta induces loss of epithelial character and smooth muscle cell differentiation in epicardial cells. Dev Dyn. 2006; 235: 82-93.
43. Avila G, Medina IM, Jimenez E, et al. Transforming growth factor-beta1 decreases cardiac muscle L-type Ca2+ current and charge movement by acting on the Cav1.2 mRNA. Am J Physiol Heart Circ Physiol. 2007; 292: H622-31.
44. Chang CT, Hung CC, Chen YC, et al. Transforming growth factor-beta1 decreases epithelial sodium channel functionality in renal collecting duct cellsviaa Smad4-dependent pathway. Nephrol Dial Transplant. 2008; 23: 1126-34.