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Optical Mapping of Electrical Activation in the Developing Heart

Published online by Cambridge University Press:  12 May 2005

David Sedmera ,
Maria Reckova ,
Carlin Rosengarten ,
Maria I. Torres ,
Robert G. Gourdie  and
Robert P. Thompson
David Sedmera
Affiliation:
Department of Cell Biology and Anatomy, Medical University of South Carolina, Charleston, SC 29425, USA
Maria Reckova
Affiliation:
Department of Cell Biology and Anatomy, Medical University of South Carolina, Charleston, SC 29425, USA
Carlin Rosengarten
Affiliation:
Department of Cell Biology and Anatomy, Medical University of South Carolina, Charleston, SC 29425, USA
Maria I. Torres
Affiliation:
Department of Cell Biology and Anatomy, Medical University of South Carolina, Charleston, SC 29425, USA
Robert G. Gourdie
Affiliation:
Department of Cell Biology and Anatomy, Medical University of South Carolina, Charleston, SC 29425, USA
Robert P. Thompson
Affiliation:
Department of Cell Biology and Anatomy, Medical University of South Carolina, Charleston, SC 29425, USA
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Abstract

Specialized conduction tissues mediate coordinated propagation of electrical activity through the adult vertebrate heart. Following activation of the atria, the activation wave is slowed down in the atrioventricular canal or node, after which it spreads rapidly into the left and right ventricles via the His-Purkinje system (HPS). This results in the ventricles being activated from the apex toward the base, which is a hallmark of HPS function. The development of mature HPS function follows significant phases of cardiac morphogenesis. Initially, the cardiac impulse propagates in a slow, linear, and isotropic fashion from the sinus venosus at the most caudal portion of the tubular heart. Although the speed of impulse propagation gradually increases as it travels toward the anterior regions of the heart tube, the actual sequence of ventricular activation in the looped heart proceeds in the same direction as blood flow. Eventually, the immature base-to-apex sequence of ventricular activation undergoes an apparent reversal, changing to the mature apex-to-base pattern. Using an optical mapping approach, we demonstrate that the timing of this last transition shows striking dependence on hemodynamic loading of the ventricle, being accelerated by pressure overload and delayed in left ventricular hypoplasia. Comparison of chick and mammalian hearts revealed some striking similarities as well as key differences in the timing of such events during cardiac organogenesis.

Keywords

chick embryorat embryoHis bundlebundle branchesdi-4-ANEPPShigh-speed imagingaction potentialanterior septal branch
Type
Research Article
Information
Microscopy and Microanalysis , Volume 11 , Issue 3 , June 2005 , pp. 209 - 215
Copyright
© 2005 Microscopy Society of America

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References

REFERENCES

Arbel, E.R., Liberthson, R., Langendorf, R., Pick, A., Lev, M., & Fishman, A.P. (1977). Electrophysiological and anatomical observations on the heart of the African lungfish. Am J Physiol 232, H24–34.Google Scholar
Biermann, M., Rubart, M., Moreno, A., Wu, J., Josiah-Durant, A., & Zipes, D.P. (1998). Differential effects of cytochalasin D and 2,3 butanedione monoxime on isometric twitch force and transmembrane action potential in isolated ventricular muscle: Implications for optical measurements of cardiac repolarization. J Cardiovasc Electrophysiol 9, 1348–1357.Google Scholar
Cheng, G., Litchenberg, W.H., Cole, G.J., Mikawa, T., Thompson, R.P., & Gourdie, R.G. (1999). Development of the cardiac conduction system involves recruitment within a multipotent cardiomyogenic lineage. Development 126, 5041–5049.Google Scholar
Chuck, E.T., Freeman, D.M., Watanabe, M., & Rosenbaum, D.S. (1997). Changing activation sequence in the embryonic chick heart. Implications for the development of the His-Purkinje system. Circ Res 81, 470–476.Google Scholar
Chuck, E.T., Meyers, K., France, D., Creazzo, T.L., & Morley, G.E. (2004). Transitions in ventricular activation revealed by two-dimensional optical mapping. Anat Rec 280A, 990–1000.Google Scholar
Chuck, E.T. & Watanabe, M. (1997). Differential expression of PSA-NCAM and HNK-1 epitopes in the developing cardiac conduction system of the chick. Dev Dyn 209, 182–195.Google Scholar
Clark, E.B., Hu, N., Dummett, J.L., Vandekieft, G.K., Olson, C., & Tomanek, R. (1986). Ventricular function and morphology in chick embryo from stages 18 to 29. Am J Physiol 250, H407–413.Google Scholar
Clark, E.B., Hu, N., Frommelt, P., Vandekieft, G.K., Dummett, J.L., & Tomanek, R.J. (1989). Effect of increased pressure on ventricular growth in stage 21 chick embryos. Am J Physiol 257, H55–61.Google Scholar
Clark, E.B., Hu, N., & Rosenquist, G.C. (1984). Effect of conotruncal constriction on aortic-mitral valve continuity in the stage 18, 21 and 24 chick embryo. Am J Cardiol 53, 324–327.Google Scholar
de la Cruz, M.V., Castillo, M.M., Villavicencio, L., Valencia, A., & Moreno-Rodriguez, R.A. (1997). Primitive interventricular septum, its primordium, and its contribution in the definitive interventricular septum: In vivo labelling study in the chick embryo heart. Anat Rec 247, 512–520.Google Scholar
Dillon, S. & Morad, M. (1981). A new laser scanning system for measuring action potential propagation in the heart. Science 214, 453–456.Google Scholar
Durrer, D., Buller, J., Graaff, P., Lo, G.I., & Meyler, F.L. (1961). Epicardial excitation pattern as observed in the isolated revived and perfused fetal human heart. Circ Res 9, 29–38.Google Scholar
Germroth, P.G., Gourdie, R.G., & Thompson, R.P. (1995). Confocal microscopy of thick sections from acrylamide gel embedded embryos. Microsc Res Tech 30, 513–520.Google Scholar
Gourdie, R.G., Harris, B.S., Bond, J., Justus, C., Hewett, K.W., O'Brien, T.X., Thompson, R.P., & Sedmera, D. (2003). Development of the cardiac pacemaking and conduction system. Birth Defects Res 69C, 46–57.Google Scholar
Gourdie, R.G., Wei, Y., Kim, D., Klatt, S.C., & Mikawa, T. (1998). Endothelin-induced conversion of embryonic heart muscle cells into impulse-conducting Purkinje fibers. Proc Natl Acad Sci USA 95, 6815–6818.Google Scholar
Hall, C.E., Hurtado, R., Hewett, K.W., Shulimovich, M., Poma, C.P., Reckova, M., Justus, C., Pennisi, D.J., Tobita, K., Sedmera, D., Gourdie, R.G., & Mikawa, T. (2004). Hemodynamic-dependent patterning of endothelin converting enzyme 1 expression and differentiation of impulse-conducting Purkinje fibers in the embryonic heart. Development 131, 581–592.Google Scholar
Hamburger, V. & Hamilton, H.L. (1951). A series of normal stages in the development of the chick embryo. J Morphol 88, 49–92.Google Scholar
Jalife, J., Morley, G.E., Tallini, N.Y., & Vaidya, D. (1998). A fungal metabolite that eliminates motion artifacts. J Cardiovasc Electrophysiol 9, 1358–1362.Google Scholar
James, J.F., Hewett, T.E., & Robbins, J. (1998). Cardiac physiology in transgenic mice. Circ Res 82, 407–415.Google Scholar
Kamino, K. (1991). Optical approaches to ontogeny of electrical activity and related functional organization during early heart development. Physiol Rev 71, 53–91.Google Scholar
Kamino, K., Hirota, A., & Fujii, S. (1981). Localization of pacemaking activity in early embryonic heart monitored using voltage-sensitive dye. Nature 290, 595–597.Google Scholar
Kurosawa, H. & Becker, A.E. (1985). Dead-end tract of the conduction axis. Int J Cardiol 7, 13–20.Google Scholar
Morley, G.E. & Vaidya, D. (2001). Understanding conduction of electrical impulses in the mouse heart using high-resolution video imaging technology. Microsc Res Tech 52, 241–250.Google Scholar
Peinado, M.A., Torres, M.I., Thompson, R.P., & Esteban, F.J. (2000). Immunolocalization of the HNK-1 epitope in the autonomic innervation to the liver and upper digestive tract of the developing rat embryo. Histochem J 32, 439–446.Google Scholar
Reckova, M., Rosengarten, C., DeAlmeida, A., Stanley, C.P., Wessels, A., Gourdie, R.G., Thompson, R.P., & Sedmera, D. (2003). Hemodynamics is a key epigenetic factor in development of the cardiac conduction system. Circ Res 93, 77–85.Google Scholar
Rentschler, S., Vaidya, D.M., Tamaddon, H., Degenhardt, K., Sassoon, D., Morley, G.E., Jalife, J., & Fishman, G.I. (2001). Visualization and functional characterization of the developing murine cardiac conduction system. Development 128, 1785–1792.Google Scholar
Rentschler, S., Zander, J., Meyers, K., France, D., Levine, R., Porter, G., Rivkees, S.A., Morley, G.E., & Fishman, G.I. (2002). Neuregulin-1 promotes formation of the murine cardiac conduction system. Proc Natl Acad Sci USA 99, 10464–10469.Google Scholar
Sedmera, D., Kucera, P., & Raddatz, E. (2002). Developmental changes in cardiac recovery from anoxia-reoxygenation. Am J Physiol Regul Integr Comp Physiol 283, R379–388.Google Scholar
Sedmera, D., Pexieder, T., Rychterova, V., Hu, N., & Clark, E.B. (1999). Remodeling of chick embryonic ventricular myoarchitecture under experimentally changed loading conditions. Anat Rec 254, 238–252.Google Scholar
Sedmera, D., Pexieder, T., Vuillemin, M., Thompson, R.P., & Anderson, R.H. (2000). Developmental patterning of the myocardium. Anat Rec 258, 319–337.Google Scholar
Sedmera, D., Reckova, M., Bigelow, M.R., DeAlmeida, A., Stanley, C.P., Mikawa, T., Gourdie, R.G., & Thompson, R.P. (2004). Developmental transitions in electrical activation patterns in chick embryonic heart. Anat Rec 280A, 1001–1009.Google Scholar
Sedmera, D., Reckova, M., DeAlmeida, A., Coppen, S.R., Kubalak, S.W., Gourdie, R.G., & Thompson, R.P. (2003a). Spatiotemporal pattern of commitment to slowed proliferation in the embryonic mouse heart indicates progressive differentiation of the cardiac conduction system. Anat Rec 274A, 773–777.Google Scholar
Sedmera, D., Reckova, M., DeAlmeida, A., Sedmerova, M., Biermann, M., Volejnik, J., Sarre, A., Raddatz, E., McCarthy, R.A., Gourdie, R.G., & Thompson, R.P. (2003b). Functional and morphological evidence for a ventricular conduction system in the zebrafish and Xenopus heart. Am J Physiol Heart Circ Physiol 284, H1152–H1160.Google Scholar
Tamaddon, H.S., Vaidya, D., Simon, A.M., Paul, D.L., Jalife, J., & Morley, G.E. (2000). High-resolution optical mapping of the right bundle branch in connexin40 knockout mice reveals slow conduction in the specialized conduction system. Circ Res 87, 929–936.Google Scholar
Thompson, R.P., Reckova, M., DeAlmeida, A., Bigelow, M., Stanley, C.P., Spruill, J.B., Trusk, T., & Sedmera, D. (2003). The oldest, toughest cells in the heart. In Development of the Cardiac Conduction System, Chadwick, D.J. & Goode, J. (Eds.), pp. 157–176. Chichester, UK: Wiley.
Vaidya, D., Tamaddon, H.S., Lo, C.W., Taffet, S.M., Delmar, M., Morley, G.E., & Jalife, J. (2001). Null mutation of connexin43 causes slow propagation of ventricular activation in the late stages of mouse embryonic development. Circ Res 88, 1196–1202.Google Scholar
Wessels, A. & Sedmera, D. (2003). Developmental anatomy of the heart: A tale of mice and man. Physiol Genomics 15, 165–176.Google Scholar
Witkowski, F.X., Clark, R.B., Larsen, T.S., Melnikov, A., & Giles, W.R. (1997). Voltage-sensitive dye recordings of electrophysiological activation in a Langendorff-perfused mouse heart. Can J Cardiol 13, 1077–1082.Google Scholar