Hostname: page-component-cd9895bd7-8ctnn Total loading time: 0 Render date: 2024-12-28T12:40:58.506Z Has data issue: false hasContentIssue false
  • English
  • Français

Epicardial Development in the Rat: A New Perspective

Published online by Cambridge University Press:  19 September 2006

Tresa Nesbitt ,
Aubrey Lemley ,
Jeff Davis ,
Michael J. Yost ,
Richard L. Goodwin  and
Jay D. Potts
Tresa Nesbitt
Affiliation:
Department of Cell & Developmental Biology and Anatomy, University of South Carolina, School of Medicine, Columbia, SC 29209, USA
Aubrey Lemley
Affiliation:
Department of Cell & Developmental Biology and Anatomy, University of South Carolina, School of Medicine, Columbia, SC 29209, USA
Jeff Davis
Affiliation:
Department of Cell & Developmental Biology and Anatomy, University of South Carolina, School of Medicine, Columbia, SC 29209, USA
Michael J. Yost
Affiliation:
Department of Cell & Developmental Biology and Anatomy, University of South Carolina, School of Medicine, Columbia, SC 29209, USA
Richard L. Goodwin
Affiliation:
Department of Cell & Developmental Biology and Anatomy, University of South Carolina, School of Medicine, Columbia, SC 29209, USA
Jay D. Potts
Affiliation:
Department of Cell & Developmental Biology and Anatomy, University of South Carolina, School of Medicine, Columbia, SC 29209, USA
Get access

Abstract

Development of the epicardium is critical to proper heart formation. It provides all of the precursor cells that form the coronary system and supplies signals that stimulate cardiac myocyte proliferation. The epicardium forms from mesothelial cells associated with the septum transversum and is referred to as the proepicardium (PE). Two different methods by which these PE cells colonize the developing heart have been described. In avians, PE cells form a bridge to the heart over which PE cells migrate onto the heart. In fish and mammals, PE cells form vesicles of cells that detach from the mesothelium, float through the pericardial cavity, and attach to the heart. A previous study of rat PE development investigated this process at the histological level. Protein markers have been developed since this study. Thus, we investigated this important developmental process coupled with these new markers using other visualization techniques such as scanning electron microscopy (SEM) and confocal microscopy. Finally, a novel, three-dimensional (3-D) culture system was used to confirm the identity of the PE cells. In this study, we found convincing evidence that the rat PE cells directly attach to the heart in a manner similar to that observed in avians.

Keywords

proepicardiumepicardiumheart developmentcoronary vasculogenesis
Type
BIOLOGICAL APPLICATIONS
Information
Microscopy and Microanalysis , Volume 12 , Issue 5 , October 2006 , pp. 390 - 398
Copyright
© 2006 Microscopy Society of America

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Dettman, R.W., Denetclaw, W., Jr., Ordahl, C.P., & Bristow, J. (1998). Common epicardial origin of coronary vascular smooth muscle, perivascular fibroblasts, and intermyocardial fibroblasts in the avian heart. Dev Biol 193, 169–181.Google Scholar
Evans, H.J., Sweet, J.K., Price, R.L., Yost, M., & Goodwin, R.L. (2003). Novel 3D culture system for study of cardiac myocyte development. Am J Physiol Heart Circ Physiol 285, H570–H578.Google Scholar
Goodwin, R.L., Nesbitt, T., Price, R.L., Wells, J.C., Yost, M.J., & Potts, J.D. (2005). Three-dimensional model system of valvulogenesis. Dev Dyn 233, 122–129.Google Scholar
Hamburger, V. & Hamilton, H.L. (1992). A series of normal stages in the development of the chick embryo. Dev Dyn 195, 231–272.Google Scholar
Kirby, M.L. (2002). Molecular embryogenesis of the heart. Pediatr Dev Pathol 5, 516–543.Google Scholar
Majesky, M.W. (2004). Development of coronary vessels. Curr Top Dev Biol 62, 225–259.Google Scholar
Manner, J. (1992). The development of pericardial villi in the chick embryo. Anat Embryol (Berl) 186, 379–385.Google Scholar
Manner, J., Perez-Pomares, J.M., Macias, D., & Munoz-Chapuli, R. (2001). The origin, formation and developmental significance of the epicardium. Cells Tissues Organs 169, 89–103.Google Scholar
Mikawa, T. & Fischman, D.A. (1992). Retroviral analysis of cardiac morphogenesis: Discontinuous formation of coronary vessels. Proc Natl Acad Sci USA 89, 9504–9508.Google Scholar
Mikawa, T. & Gourdie, R.G. (1996). Pericardial mesoderm generates a population of coronary smooth muscle cells migrating into the heart along with ingrowth of the epicardial organ. Dev Biol 174, 221–232.Google Scholar
Nahirney, P.C., Mikawa, T., & Fischman, D.A. (2003). Evidence for an extracellular matrix bridge guiding proepicardial cell migration to the myocardium of chick embryos. Dev Dyn 227, 511–523.Google Scholar
Olivey, H.E., Compton, L.A., & Barnett, J.V. (2004). Coronary vessel development: The epicardium delivers. Trends Cardiovasc Med 14, 247–251.Google Scholar
Perez-Pomares, J.M., Carmona, R., Gonzalez-Iriarte, M., Macias, D., Guadix, J.A., & Munoz-Chapuli, R. (2004). Contribution of mesothelium-derived cells to liver sinusoids in avian embryos. Dev Dyn 229, 465–474.Google Scholar
Perez-Pomares, J.M., Macias, D., Garcia-Garrido, L., & Munoz-Chapuli, R. (1997). Contribution of the primitive epicardium to the subepicardial mesenchyme in hamster and chick embryos. Dev Dyn 210, 96–105.Google Scholar
Perez-Pomares, J.M., Phelps, A., Sedmerova, M., & Wessels, A. (2003). Epicardial-like cells on the distal arterial end of the cardiac outflow tract do not derive from the proepicardium but are derivatives of the cephalic pericardium. Dev Dyn 227, 56–68.Google Scholar
Potts, J.D., Yost, M., & Goodwin, R.L. (2006). Models of cardiovascular development: New approaches are making in vitro en vogue. Curr Card Rev 2, 55–64.Google Scholar
Reese, D.E., Mikawa, T., & Bader, D.M. (2002). Development of the coronary vessel system. Circ Res 91, 761–768.Google Scholar
Takahashi, G. (1979). Conductive staining method. The Cell 11, 114–123.Google Scholar
van den Eijnde, S.M., Wenink, A.C., & Vermeij-Keers, C. (1995). Origin of subepicardial cells in rat embryos. Anat Rec 242, 96–102.Google Scholar
Viragh, S. & Challice, C.E. (1981). The origin of the epicardium and embryonic myocardial circulation in the mouse. Anat Embryol 188, 381–393.Google Scholar
Vrancken Peeters, M.P., Mentink, M.M., Poelmann, R.E., & Gittenberger-de Groot, A.C. (1995). Cytokeratins as a marker for epicardial formation in the quail embryo. Anat Embryol (Berl) 191, 503–508.Google Scholar
Wada, A.M., Willet, S.G., & Bader, D. (2003). Coronary vessel development: A unique form of vasculogenesis. Arterioscler Thromb Vasc Biol 23, 2138–2145.Google Scholar
Wessels, A. & Perez-Pomares, J.M. (2004). The epicardium and epicardially derived cells (EPDCs) as cardiac stem cells. Anat Rec 276, 43–57.Google Scholar
Xavier-Neto, J., Shapiro, M.D., Houghton, L., & Rosenthal, N. (2000). Sequential programs of retinoic acid synthesis in the myocardial and epicardial layers of the developing avian heart. Dev Biol 219, 129–141.Google Scholar
Yost, M.J., Baicu, C.F., Stonerock, C.E., Goodwin, R.L., Price, R.L., Davis, J.M., Evans, H., Watson, P.D., Gore, C.M., Sweet, J., Creech, L., Zile, M.R., & Terracio, L. (2004). A novel tubular scaffold for cardiovascular tissue engineering. Tissue Eng 10, 273–284.Google Scholar