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Cell Patterning: Interaction of Cardiac Myocytes and Fibroblasts in Three-Dimensional Culture

Published online by Cambridge University Press:  03 March 2008

Troy A. Baudino ,
Alex McFadden ,
Charity Fix ,
Joshua Hastings ,
Robert Price  and
Thomas K. Borg
Troy A. Baudino
Affiliation:
Department of Cell and Developmental Biology and Anatomy, University of South Carolina, School of Medicine, Columbia, SC 29209, USA
Alex McFadden
Affiliation:
Department of Cell and Developmental Biology and Anatomy, University of South Carolina, School of Medicine, Columbia, SC 29209, USA
Charity Fix
Affiliation:
Department of Cell and Developmental Biology and Anatomy, University of South Carolina, School of Medicine, Columbia, SC 29209, USA
Joshua Hastings
Affiliation:
Department of Cell and Developmental Biology and Anatomy, University of South Carolina, School of Medicine, Columbia, SC 29209, USA
Robert Price
Affiliation:
Department of Cell and Developmental Biology and Anatomy, University of South Carolina, School of Medicine, Columbia, SC 29209, USA
Thomas K. Borg
Affiliation:
Department of Cell and Developmental Biology and Anatomy, University of South Carolina, School of Medicine, Columbia, SC 29209, USA
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Abstract

Patterning of cells is critical to the formation and function of the normal organ, and it appears to be dependent upon internal and external signals. Additionally, the formation of most tissues requires the interaction of several cell types. Indeed, both extracellular matrix (ECM) components and cellular components are necessary for three-dimensional (3-D) tissue formation in vitro. Using 3-D cultures we demonstrate that ECM arranged in an aligned fashion is necessary for the rod-shaped phenotype of the myocyte, and once this pattern is established, the myocytes were responsible for the alignment of any subsequent cell layers. This is analogous to the in vivo pattern that is observed, where there appears to be minimal ECM signaling, rather formation of multicellular patterns is dependent upon cell–cell interactions. Our 3-D culture of myocytes and fibroblasts is significant in that it models in vivo organization of cardiac tissue and can be used to investigate interactions between fibroblasts and myocytes. Furthermore, we used rotational cultures to examine cellular interactions. Using these systems, we demonstrate that specific connexins and cadherins are critical for cell–cell interactions. The data presented here document the feasibility of using these systems to investigate cellular interactions during normal growth and injury.

Keywords

myocytescardiac fibroblastscell–cell interactionsextracellular matrix (ECM)
Type
Research Article
Information
Microscopy and Microanalysis , Volume 14 , Issue 2 , April 2008 , pp. 117 - 125
Copyright
© 2008 Microscopy Society of America

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References

REFERENCES

Baudino, T.A., Carver, W., Giles, W. & Borg, T.K. (2006). Cardiac fibroblasts: Friend or foe. Am J Physiol 291, H1015–H1026.Google Scholar
Borg, K.T., Burgess, W., Terracio, L. & Borg, T.K. (1997). Expression of metalloproteases by cardiac myocytes and fibroblasts in vitro. Cardiac Pathol 6, 261–269.Google Scholar
Borg, T.K. & Caulfield, J.B. (1981). The collagen matrix of the heart. Fed Proc 40, 2037–2041.Google Scholar
Bullard, T.A., Borg, T.K. & Price, R.L. (2005). The expression and role of protein kinase C in neonatal cardiac myocyte attachment, cell volume, and myofibril formation is dependent on the composition of the extracellular matrix. Microsc Microanal 11, 224–234.Google Scholar
Camelliti, P., Borg, T.K. & Kohl, P. (2004). Structural and functional characterisation of cardiac fibroblasts. Cardiovasc Res 65, 40–51.Google Scholar
Camelliti, P., Gallagher, J.O., Kohl, P. & McCulloch, A.D. (2006b). Micropatterned cell cultures on elastic membranes as an in vitro model of myocardium. Nature Protocols 1, 1379–1391.Google Scholar
Camelliti, P., Green, C.R. & Kohl, P. (2006a). Structural and functional coupling of cardiac myocytes and fibroblasts. Adv Cardiol 42, 132–149.Google Scholar
Camelliti, P., McCulloch, A. & Kohl, P. (2005). Microstructured cocultures of cardiacmyocytes and fibroblasts: A two-dimensional in vitro model of cardiac tissue. Microsc Microanal 11, 249–259.Google Scholar
Ciulla, M.M., Paliotti, R., Ferrero, S., Braidotti, P., Espositio, A., Gianelli, U., Cioffi, U. & Bulfamante, G. (2004). Left ventricular remodeling after experimental myocardial cryoinjury in rats. J Surg Res 116, 91–97.Google Scholar
Gaudesius, G., Miragoli, M., Thomas, S.P. & Rohr, S. (2003). Coupling of cardiac electrical activity over extended distances by fibroblasts of cardiac origin. Circ Res 93, 421–428.Google Scholar
Goldsmith, E.C., Hoffman, A., Morales, M.O., Potts, J.D., Price, R.L., McFadden, A., Rice, M. & Borg, T.K. (2004). Organization of fibroblasts in the heart. Dev Dyn 230, 787–794.Google Scholar
Grinnell, F. (2003). Fibroblast biology in three-dimensional collagen matrices. Trends Cell Biol 13, 264–269.Google Scholar
Legrice, I.J., Hunter, P.J. & Smaill, B.H. (1997). Laminar structure of the heart: A mathematical model. Am J Physiol 272, H2466–H2476.Google Scholar
Linask, K.K., Manisastry, S. & Han, M. (2005). Cross talk between cell–cell and cell–matrix adhesion signaling pathways during heart organogenesis: Implications for cardiac birth defects. Microsc Microanal 11, 200–208.Google Scholar
Lorenzen-Schmidt, I., Schmid-Schonbein, G.W., Giles, W.R., McCulloch, A.D., Chien, S. & Omens, J.H. (2006). Chronotropic response of cultured neonatal rat ventricular myocytes to short-term fluid shear. Cell Biochem Biophys 46, 113–122.Google Scholar
Miragoli, M., Gaudesius, G. & Rohr, S. (2006). Electronic modulation of cardiac impulse conduction by myofibroblasts. Circ Res 98, 801–810.Google Scholar
Pederson, J.A. & Swartz, M.A. (2005). Mechanobiology in the 3rd dimension. Ann Biomed Eng 33, 1469–1490.Google Scholar
Sharp, W.W., Simpson, D.G., Borg, T.K., Samarel, A.M. & Terracio, L. (1997). Mechanical forces regulate focal adhesion and costamere assembly in cardiac myocytes. Am J Physiol 273, H546–H556.Google Scholar
Simpson, D.G., Terracio, L., Terracio, M., Price, R.L., Turner, D.C. & Borg, T.K. (1994). Modulation of cardiac myocyte phenotype in vitro by the composition and orientation of the extracellular matrix. J Cell Physiol 161, 89–105.Google Scholar
Streeter, D.D. (1979). Gross morphology and fiber geometry of the heart. In Handbook of Physiology, Hamilton, W.F. & Dow, P. (Eds.), Vol. 1, pp. 61–112. Baltimore, MD: Williams and Wilkins.
Sussman, M.A., McCulloch, A. & Borg, T.K. (2002). Dance band on the Titanic: Biomechanical signaling in cardiac hypertrophy. Circ Res 91, 888–898.Google Scholar
Terracio, L., Rubin, K., Gullberg, D., Balog, E., Carver, W., Jyring, R. & Borg, T.K. (1991). Expression of collagen binding integrins during cardiac development and hypertrophy. Circ Res 68, 734–744.Google Scholar
Yamada, K., Green, K.G., Sammarel, A.M. & Saffitz, J.E. (2005). Distinct pathways regulate expression of cardiac electrical and mechanical junction proteins in response to stretch. Circ Res 97, 346–353.Google Scholar
Young, A.A., Legrice, I.J., Young, M.A. & Smaill, B.H. (1998). Extended confocal microscopy of myocardial laminae and collagen network. J Microsc 192, 139–150.Google Scholar
Zak, R. (1974). Development and proliferative capacity of cardiac muscle cells. Circ Res 32, 17–26.Google Scholar
Zimmermann, W.H., Schneiderbanger, K., Schubert, P., Didie, M., Munzel, F., Heubach, J.F., Kostin, S., Neuhuber, W.L. & Eschenhagen, T. (2002). Tissue engineering of a differentiated cardiac muscle construct. Circ Res 90, 223–230.Google Scholar