Ultrastructure and cell-cell coupling of cardiac myocytes differentiating in embryonic stem cell cultures

Cell Motility and the Cytoskeleton

Volumn 36, Issue 1, 1997, Pages 43-54

  Westfall, Margaret V ^a   Pasyk, Krystyna A ^a   Yule, David I ^a   Samuelson, Linda C ^a   Metzger, Joseph M ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

Author keywords

cardiogenesis; connexin 43; embryonic stem cells; gap junctions; morphometry; sarcomere

Indexed keywords

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL JUNCTION; CELL ULTRASTRUCTURE; EMBRYO; EMBRYO DEVELOPMENT; HEART DEVELOPMENT; HEART MUSCLE CELL; MICROTUBULE ASSEMBLY; MOUSE; NONHUMAN; PRIORITY JOURNAL; STEM CELL;

ANIMALS; CELL DIFFERENTIATION; CELL SIZE; CELLS, CULTURED; DESMOSOMES; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; FLUORESCENT DYES; GAP JUNCTIONS; INTERCELLULAR JUNCTIONS; MICE; MICROSCOPY, CONFOCAL; MYOCARDIAL CONTRACTION; MYOCARDIUM; SARCOMERES; STEM CELLS;

ANIMALIA;

EID: 0031030219     PISSN: 08861544     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-0169(1997)36:1<43::AID-CM4>3.0.CO;2-I     Document Type: Article

References (35)

1. Anversa, P., Olivetti, G., and Loud, A.V. (1980): Morphometric study of early postnatal development in the left and right ventricular myocardium of the rat. Circ. Res. 46:495-502.
2. Barr, L., Dewey, M.M., and Berger, W. (1965): Propagation of action potentials and the nexus in cardiac muscle. J. Gen. Physiol. 48:797-823.
3. Bishop, S.P., Anderson, P.G., and Tucker, D.C. (1990): Morphological development of the rat heart growing in oculo in the absence of hemodynamic work load. Circ. Res. 66:84-102.
4. Chacko, K.J. (1976): Observations on the ultrastructure of developing myocardium of rat embryos. J. Morphol. 150:681-710.
5. Darrow, B.J., Laing, J.G., Lampe, P.D., Saffitz, J.E., and Beyer, E.C. (1995): Expression of multiple connexins in cultured neonatal rat ventricular myocytes. Circ. Res. 76:381-387.
6. Delcarpio, J.B., Lanson, N.A., Jr., Field, L.J., and Claycomb, W.C. (1991): Morphological characterization of cardiomyocytes isolated from a transplantable cardiac tumor derived from transgenic mouse atria (AT-1 cells). Circ. Res. 69:1591-1600.
7. DeMello, W.C., Castillo, M.G., and vanLoon, P. (1983): Intercellular diffusion of lucifer yellow CH in mammalian cardiac fibers. J. Mol. Cell. Cardiol. 15:637-643.
8. 2+ oscillations in pancreatic acini by multiple mechanisms. Am. J. Physiol. 269:G779-G788.
9. Doetschman, T.C., Eistetter, H., Katz, M., Schmidt, W., and Kemler, R. (1985): The in vitro development of blastocyst-derived embryonic stem cell lines: Formation of visceral yolk sac, blood islands and myocardium. J. Embryol. Exp. Morphol. 87:27-45.
10. Forbes, M.S., and Sperelakis, N. (1985): Intercalated discs of mammalian heart: A review of structure and function. Tissue Cell 17:605-648.
11. Fromaget, C., El Aoumari, A., Dupont, E., Briand, J.P., and Gros, D. (1990): Changes in the expression of connexin 43, a cardiac gap junctional protein, during mouse heart development. J. Mol. Cell. Cardiol. 22:1245-1258.
12. Klug, M.G., Soonpaa, M.H., Koh, G.Y., and Field, L.J. (1996): Genetically selected cardiomyocytes from differentiating embryonic stem cells form stable intracardiac grafts. J. Clin. Invest. 98:216-224.
13. Koh, G.Y., Klug, M.G., Soonpaa, M.H., and Field, L.J. (1993a): Differentiation and long-term survival of C2C12 myoblast grafts in heart. J. Clin. Invest. 92:1548-1554.
14. Koh, G.Y., Soonpaa, M.H., Klug, M.G., and Field, L.J. (1993b): Long-term survival of AT-1 cardiomyocyte grafts in syngeneic myocardium. Am. J. Physiol. 264:H1727-1733.
15. Korecky, B., and Rakusan, K. (1978): Normal and hypertrophic growth of the rat heart: Changes in cell dimensions and number. Am. J. Physiol. 234:H123-H128.
16. Li, R.K., Mickle, D.A.G., Weisel, R.D., Zhang, J., and Mohabeer, M.K. (1996): In vivo survival and function of transplanted rat cardiomyocytes. Circ. Res. 78:283-288.
17. Mahdavi, V., Izumo, S., and Nadal-Ginard, B. (1987): Developmental and hormonal regulation of sarcomeric myosin heavy chain gene family. Circ. Res. 60:804-814.
18. Manasek, F.J. (1970): Histogenesis of the embryonic myocardium. Am. J. Cardiol. 25:149-168.
19. Marino, T.A., Kuseryk, L., and Lauva, I.K. (1987): Role of contraction in the structure and growth of neonatal rat cardiomyocytes. Am. J. Physiol. 253:H1391-H1399.
20. McNutt, S. (1970): Ultrastructure of intercellular junctions in adult and developing cardiac muscle. Am. J. Cardiol. 25:169-183.
21. Metzger, J.M., Lin, W., and Samuleson, L.C. (1994): Transition in cardiac contractile sensitivity to calcium during the in vitro differentiation of mouse embryonic stem cells. J. Cell Biol. 126:701-711.
22. Metzger, J.M., Lin, W., Johns ton, R.A., Westfall, M.V., and Samuelson, L.C. (1995): Myosin heavy chain expression in contracting myocytes isolated during embryonic stem cell cardiogenesis. Circ. Res. 76:710-719.
23. Miller-Hance, W.C., LaCorbiere, M., Fuller, S., Evans, S., Lyons, G., Schmidt, C., Robbins, J., and Chien, K. (1993): In vitro chamber specification during embryonic stem cell cardiogenesis. J. Biol. Chem. 268:25244-25252.
24. Muthuchamy, M., Pajak, L., Howles, P., Doetschman, T., and Wieczorek, D. (1993): Developmental analysis of tropomyosin gene expression in embryonic stem cells and mouse embryos. Mol. Cell. Biol. 13:3311-3323.
25. Robbins, J., Gulick, J., Sanchez, A., Howles, P., and Doetschman, T. (1990): Mouse embryonic stem cells express the cardiac myosin heavy chain genes during development in vitro. J. Biol. Chem. 265:11905-11909.
26. Robbins, J., Doetschman, T., Jones, W.K., and Sanchez, A. (1992): Embryonic stem cells as a model for cardiogenesis. Trends Cardiovasc. Med. 2:44-50.
27. Rohr, S., Scholly, D.M., Kleber, A.G. (1991): Patterned growth of neonatal rat heart cells in culture. Circ. Res. 68:114-130.
28. Saggin, L., Gorza, L., Ausoni, S., and Schiaffino, S. (1989): Troponin I switching in the developing heart. J. Biol. Chem. 264: 16299-16302.
29. Severs, N.J. (1989): Constituent cells of the heart and isolated cell models in cardiovascular research. In Piper, H.M., and Isenberg, G. (eds): "Isolated Adult Cardiomyocytes." Boca Raton, FL: CRC Press, Inc. pp. 3-41.
30. Shibata, Y., Nakata, K., and Page, E. (1980): Ultrastructural changes during development of gap junctions in rabbit left ventricular myocardial cells. J. Ultrastruct. Res. 71:258-271.
31. Soonpaa, M.H., Koh, G.Y., Klug, M.G., and Field, L.J. (1994): Formation of nascent intercalated disks between grafted fetal cardiomyocytes and host myocardium. Science 264:98-101.
32. Spray, D.C., and Burt, J.M. (1990): Structure-activity relations of the cardiac gap junction channel. Am. J. Physiol. 258:C195-C205.
33. Stewart, W.W. (1981): Lucifer dyes: Highly fluorescent dyes for biological tracing. Nature 292:17-21.
34. VanKempen, M.J.A., TenVelde, I., Wessels, A., Oosthoek, P.W., Gros, D., Jongsma, H.J., Moorman, A.F.M., and Lamers, W.H. (1995): Differential connexin distribution accommodates cardiac function in different species. Microsc. Res. Tech. 31: 420-436.
35. Westfall, M.V., Samuelson, L.C., and Metzger, J.M. (1996): Troponin I isoform expression is developmentally regulated in differentiating embryonic stem cell-derived cardiac myocytes. Dev. Dyn. 206:24-38.