Summary
The subject of heart development has attracted the interest of many embryologists over the last two centuries. As a result, the main morphologic features of the developmental anatomy of the heart are already well established. Although there are still some controversial points, and there is probably much descriptive work yet to be done, emphasis is currently being placed on developmental mechanisms rather than simply on descriptive facts. The availability of new techniques and the overall advances in biological research are placing heart embryology in a new perspective. Today, we do not simply ask whether one or another embryonic structure arises further right or further left; instead, we are studying how cells, tissues, and their microenvironment interrelate at the several levels of biological organization (from the gene upwards) so as to give rise to a mature organ with a distinct shape and well-established functions.
This paper attempts to review some of the basic aspects of the developmental anatomy of the heart. Descriptive embryology is used here as a tool. Emphasis is placed on developmental mechanisms, and on the present knowledge of how these mechanisms are related to the structural development of the heart.
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Alpert, N. R., and Mulieri, L. A., Hypertrophic adaptation of the heart to stress: A myothermal analysis, in: Growth of the Heart in Health and Disease, pp. 363–379. Ed. R. Zak. Raven Press, New York 1984.
Anversa, P., Ricci, R., and Olivetti, G., Quantitative structural analysis of the myocardium during physiologic growth and induced cardiac hypertrophy: A review. J. Am. Coll. Cardiol.7 (1986) 1140–1149.
Bacon, R. L., Self-differentiation and induction in the heart of amblyostoma. J. exp. Zool.98 (1945) 87–125.
Becker, A. E., and Anderson, R. H., Cardiac embryology: A help or a hindrance in understanding congenital heart disease, in: Congenital Heart Disease. Causes and Processes, pp. 339–358. Eds J. J. Nora and A. Takao. Futura Publishing Co., New York 1984.
Bernfield, M. R., Mechanisms of embryonic organ formation, in: Abnormal Fetal Growth: Biological Bases and Consequences, pp. 101–120. Ed. F. Naftolin. Dahlem Konferenzen, Berlin 1978.
Caveney, S., The role of gap junctions in development. A. Rev. Physiol.47 (1985) 319–335.
Chacko, S., and Joseph, X., The effect of 5-bromodeoxyuridine (BrdU) on cardiac muscle differentiation. Devl Biol.40 (1974) 340–354.
Chizzonite, R. A., Everett, A. W., Clark, W. A., Jakovic, S., Rabinowitz, M., and Zak, R., Isolation and characterization of two molecular variants of myosin heavy chains from rabbit ventricle. Change in their content during normal growth and after a treatment with thyroid hormone. J. biol. Chem.257 (1982) 2056–2065.
Clark, E. B., Ventricular function and cardiac growth in the chick embryo, in: Cardiac Morphogenesis, pp 238–244, Eds Y. J. Ferrans, G. Rosenquist and C. Weinstein. Elsevier, New York 1985.
Clark, E. B., Hu, N., and Dooley, J. B., The effect of isoproterenol on cardiovascular function in the stage 24 chick embryo. Teratology31 (1985) 41–47.
Copenhaver, W. M., Heart, blood vessels, blood, and endodermal derivatives, in: Analysis of Development, pp. 440–461. Eds B. H. Willier, P. A. Weiss and V. Hamburger. Hafner Publishing Co., New York 1971.
Cummins, P., and Lambert, S. J., Myosin transitions in the bovine and human heart. A developmental and anatomical study of heavy and light chain subunits in the atrium and ventricle. Circ. Res.58 (1986) 846–858.
David, I. B., Haynes, S. R., Jamrich, M., Jonas, E., Miyatani, S., Sargent, T. D., and Winkles, J. A., Gene expression inXenopus embryogenesis. J. Embryol. exp. Morph.89 Suppl. (1984) 113–124.
DeHaan, R. L., Morphogenesis of the vertebrate heart, in: Organogenesis, pp. 377–419. Eds R. L. DeHaan and H. Ursprung. Holt, Rinehart and Winston, New York 1965.
DeHaan, R. L., McDonald, T. F., and Sachs, H. G., Development of tetrodotoxin sensitivity of embryonic chick heart cells in vitro, in: Developmental and Physiological Correlates of Cardiac Muscle, pp. 155–168. Eds M. Lieberman and T. Sano. Raven Press, New York 1975.
Ebert, J. D., An analysis of the synthesis and distribution of the contractile protein, myosin, in the development of the heart. Proc. natl Acad. Sci. USA39 (1953) 333–344.
Ferrans, V. J., Cardiac hypertrophy: Morphological aspects, in: Growth of the Heart in Health and Disease, pp. 187–239. Ed. R. Zak. Raven Press, New York 1984.
Forbes, M. S. and Sperelakis, N., Intercalated discs of mammalian heart: A review of structure and function. Tiss. Cell17 (1985) 605–648.
Forbes, M. S., Hawkey, L. A., and Sperelakis, N., The transverseaxial tubular system (TATS) of mouse myocardium: Its morphology in the developing and adult animal. Am. J. Anat.170 (1983) 143–162.
Garrels, J. I., and Gibson, W., Identification and characterization of multiple forms of actin. Cell9 (1976) 793–805.
Gilula, N. B., Gap junctions and cell communication, in: International. Cell Biology, pp. 61–69. Eds B. R. Brinkley and K. R. Porter. Rockefeller University Press, New York 1977.
Gonzalez-Sanchez, A., and Bader, D., Immunochemical analysis of myosin heavy chains in the developing chick heart. Devl Biol.103 (1983) 151–158.
Gorza, L., Mercadier, J. J., Schwartz, K., Thornell, L. E., Sartore, S., and Schiaffino, S., Myosin types in the human heart. An immunofluorescence study of normal and hypertrophied atrial and ventricular myocardium. Circ. Res.54 (1984) 694–702.
Goss, C. M., Double hearts produced experimentally in rat embryos. J. exp. Zool.72 (1935) 33–45.
Goss, C. M., Development of the median coordinated ventricle from the lateral hearts in rat embryos with three to six somites. Anat. Rec.112 (1952) 761–796.
Gros, D., Mocquard, J. P., Schrevel, J., and Challice, C. E., Assembly of gap junctions in developing mouse cardiac muscle, in: Mechanisms of Cardiac Morphogenesis and Teratogenesis, pp. 285–298. Ed. T. Pexieder. Raven Press, New York 1981.
Gurdon, J. B., Introductory comments. Cold Spring Harbor Symp. Quant. Biol.50 (1985) 1–10.
Gurdon, J. B., Mohun, T. J., and Cascio, S., Actin genes inXenopus and their developmental control. J. Embryol. exp. Morphol.89 Suppl. (1984) 125–136.
Hammond, G. L., Lai, Y.-K., and Markert, C. L., Diverse forms of stress lead to new patterns of gene expression through a common and essential metabolic pathway. Proc. natl Acad. Sci. U.S.A.79 (1982) 3485–3488.
Icardo, J. M., Ultrastructure and function of the cardiac jelly. A review. Morfol. Norm. Patol., A-Histol.7 (1983) 43–58.
Icardo, J. M., The growing heart: An anatomical perspective, in: Growth of the Heart in Health and Disease, pp. 41–80. Ed. R. Zak. Raven Press, New York 1984.
Icardo, J. M., Distribution of fibronectin during the morphogenesis of the truncus. Anat. Embryol.171 (1985) 193–200.
Icardo, J. M., and Ojeda, J. L., Effects of colchicine on the formation and looping of the tubular heart of the embryonic chick. Acta anat.119 (1984) 1–9.
Icardo, J. M., Fernandez-Teran, M. A., and Ojeda, J. L., Early cardiac structure and developmental biology, in: Handbook of Human Growth and Developmental Biology. Eds E. Meisami and P. Timiras CRC Press, Florida (1988) in the press.
Ingber, D. E., and Jamieson, J. D., in: Gene Expression During Normal and Malignant Differentiation, pp. 13–32. Eds L. C. Anderson, C. G. Gahmberg and P. Ekblom. Academio Press, London 1985.
Jacob, R., Gulch, R. W., and Kissling, G. (eds), in: Cardiac Adaptation to Hemodynamic Load, Training and Stress. Stemkopff Verlag, Darmstadt 1983.
Kirby, M. L., Gale, T. F., and Stewart, D., Neural crest cells contribute to aorticpulmonary septation. Science220 (1983) 1059–1061.
Kojima, M., and Sperelakis, N., Development of slow Ca2+−Na+ channels during organ culture of young embryonic chick hearts. J. devl Physiol.7 (1985) 355–363.
Kurnitt, D. M., Aldridge, J. F., Matsuoka, R., and Matthysse, S., Increased adhesiveness of trisomy 21 cells and atrioventricular canal malformations in Down's syndrome: A stochastic model. Am. J. Med. Genet.20 (1985) 385–399.
Laane, M. H., The septation of the arterial pole of the heart in the chick embryo. IV. Discussion. Acta morphol. neerl.-scand.17 (1979) 21–32.
Lacktis, J. W., An Experimental and Descriptive Study of Heart Morphogenesis in the Chick. Ph. D. Thesis, University of Chicago 1981.
Lai, Y.-K., Havre, P. A., and Hammond, G. L., Heat shock stress initiates simultaneous transcriptional and translational changes in the dog heart. Biochem. biophys. Res. Commun.134 (1986) 166–171.
Layton, W. M. Jr, Heart malformations in mice homozygous for a gene causing situs inversus, in: Morphogenesis and Malformations of the Cardiovascular System, pp. 277–293. Eds G. C. Rosenquist and D. Bergsma. Alan R. Liss, New York 1978.
Layton, W. M. Jr., and Manasek, F. J. Cardiac looping in early iv/iv mouse embryos, in: Etiology and Morphogenesis of Congenital Heart Disease, pp. 109–126. Eds R. van Praagh and A. Takao. Futura Publishing Co., New York 1980.
Le Douarin, G. H., Analyse expérimentale des premiers stades du dévelopement cardiaque chez les vertébrates supérieurs. Annls Biol.13 (1974) 43–50.
Le Douarin, G. H., and Renaud, D., Differentiation of cellular electrical properties in the developing embryonic chick heart, in: Mechanisms of Cardiac Morphogenesis and Teratogenesis, pp. 317–330. Ed. T. Pexieder. Raven Press, New York 1981.
Legato, M. J., Ultrastructural changes during normal growth in the dog and rat ventricular myofiber, in: Developmental and Physiological Correlates of Cardiac Muscle, pp. 249–274. Eds. M. Lieberman and T. Sano. Raven Press, New York 1975.
Lim, S.-S., Woodroofe, M. N., and Lemanski, L. F., An analysis of contractile proteins in developing chick heart by SDS polyacrylamide gel electrophoresis and electron microscopy. J. Embryol. exp. Morphol.77 (1983) 1–14.
Litten, R. Z., Martin, B. J., Buchthal, R. H., Nagai, R., Low, R. B., and Alpert, N. R., Heterogeneity of myosin isozyme content of rabbit heart. Circ. Res.57 (1985) 406–414.
Manasek, F. J., Embryonic development of the heart. I. A. light and electron microscopic study of myocardial development in the early chick embryo. J. Morph.125 (1968) 329–366.
Manasek, F. J., Histogenesis of the embryonic myocardium. Am. J. Cardiol.25 (1970) 149–168.
Manasek, F. J., The extracellular matrix: A dynamic component of the developing embryo. Curr. Top. devl Biol.10 (1975) 35–102.
Manasek, F. J., Heart development: Interactions involved in cardiac morphogenesis, in: The Cell Surface in Animal Embryogenesis and Development, pp. 545–598. Eds G. Poste and G. L. Nicolson. North Holland, Amsterdam 1976.
Manasek, F. J., and Monroe, R. G., Early cardiac morphogenesis is independent of function. Devl Biol.27 (1972) 584–588.
Manasek, F. J., and Nakamura, A., Forces and deformations: Their origins and regulation in early development, in: Cardiac Morphogenesis, pp. 126–133. Eds V. J. Ferrans, G. Rosenquist and C. Weinstein. Elsevier, New York 1985.
Manasek, F. J., Icardo, J. M., Nakamura, A., and Sweeney, L. J., Cardiogenesis: Developmental mechanisms and embryology, in: The Heart and Cardiovascular System, pp. 965–985. Eds H. A. Fozzard, E. Haber, R. B. Jennings, A. M. Katz and H. E. Morgan. Raven Press, New York 1986.
Manasek, F. J., Isobe, Y., Shimada, Y., and Hopkins, W., The embryonic myocardial cytoskeleton, interstitial pressure, and the control of morphogenesis, in: Congenital Heart Disease. Causes and Processes, pp. 359–376. Eds J. Nora and A. Takao. Futura Publishing Co., New York 1984.
Manasek, F. J., Kulikowski, R. R., Nakamura, A., Nguyenphuc, Q., and Lacktis, J. W., Early heart development: a new model of cardiac morphogenesis, in: Growth of the Heart in Health and Disease, pp. 105–130. Ed. R. Zak. Raven Press, New York 1984.
Marino, T. A., Houser, S. R., and Cooper, G. IV., Early morphological alterations of pressure-overload cat right ventricular myocardium. Anat. Rec.207 (1983) 417–426.
Markwald, R. R., Fitzharris, T. P., and Adams Smith, W. N., Morphologic recognition of complex carbohydrates in embryonic cardiac extracellular matrix. J. Histochem. Cytochem.27 (1979) 1171–1173.
Markwald, R. R., Funderberg, F. M., and Bernanke, D. H., Glycosaminoglycans: Potential determinants in cardiac morphogenesis. Tex. Rep. Biol. Med.39 (1979) 253–270.
McDermott, P., Daood, M., and Klein, I. Contraction regulates myosin synthesis and myosin content of cultured heart cells. Am. J. Physiol.249 (1985) H763-H769.
Mercadier, J. J., Lompre, A. M., Wisneswky, C., Samuel, J. L., Bercovici, B., Swynghedauw, B., and Schwartz, K., Myosin isoenzymic changes in several models of rat cardiac hypertrophy. Circ. Res.49 (1981) 525–532.
Nadal-Ginard, B., Nguyen, H. T., Medford, R. M., and Mahdavi, V., Regulation of gene expression during development: The myosin heavy chain genes, in: Congenital Heart Disease. Causes and Processes, pp. 79–96. Eds J. J. Nora and A. Takao. Futura Publishing Co., New York 1984.
Nakamura, A., and Manasek, F. J., Experimental studies of the shape and structure of isolated cardiac jelly. J. Embryol. exp. Morph.43 (1978) 167–183.
Nakamura, A., and Manasek, F. J., An experimental study of the relation of cardiac jelly to the shape of the early chick embryonic heart. J. Embryol. exp. Morph.65 (1981) 235–256.
Nakamura, A., Kulikowski, R. R., Lacktis, J. W., and Manasek, F. J., Heart looping: A regulated response to deforming forces, in: Etiology and Morphogenesis of Congenital Heart Disease, pp. 81–98. Eds R. van Praagh and A. Takao. Futura, Publishing Co., New York 1980.
Nakamura, S., Asai, J., and Hama, K., The transverse tubular system of rat myocardium: Its morphology and morphometry in the developing and adult animal. Anat. Embryol.173 (1986) 307–315.
Nathan, R. D., Houck, P. C., Fung, S. J., Stocco, D. M., and Markwald, R. R., Mechanisms of pacemaker activity in embryonic cardiac muscle, in: Mechanisms of Cardiac Morphogenesis and Teratogenesis, pp. 337–348. Ed. T. Pexieder. Raven Press, New York 1981.
Newkoop, P. D., Inductive interactions in early amphibian development and their general nature. J. Embryol. exp. Morph.89 Suppl. (1984) 333–347.
Nora, J. J., and Takao, A. (eds), Congenital Heart Disease. Causes and Processes. Futura Publishing Co., New York 1984.
Okamoto, N., Satow, Y., Hidaka, N., and Akimoto, N., Anomalous development of the conotruncus in neutron-irradiated rats, in: Etiology and Morphogenesis of Congenital Heart Disease, pp. 195–214. Eds R. Van Praagh and A. Takao. Futura Publishing Co., New York 1980.
Orts-Llorca, F., Influence of the endoderm on heart differentiation during the early stages of development of the chicken embryo. Wilhelm Roux' Arch.154 (1963) 533–551.
Patten, B. M., The development of the heart, in: Pathology of the Heart and Blood Vessels, pp. 20–90. Ed. S. E. Gould, Charles C. Thomas, Springfield 1968.
Pexieder, T., Cell death in the morphogenesis and teratogenesis of the heart. Adv. Anat. Embryol. Cell Biol.51 (1975) 1–100.
Pexieder, T., Cellular mechanisms underlying the normal and abnormal development of the heart, in: Etiology and Morphogenesis of Congenital Heart Disease, pp. 127–153. Eds R. Van Praagh and A. Takao. Futura Publishing Co., New York 1980.
Rajala, G. M., Kuhlmann, R. S., and Kolesari, G. L., The role of dysrhythmic heart function during cardiovascular teratogenesis in epinephrine-treated chick embryos. Teratology30 (1984) 385–392.
Satow, Y., and Manasek, F. J., Direct effects of trypan blue on cardiac extracellular macromolecule synthesis. Lab. Invest.36 (1977) 100–105.
Scheuer, J., and Bahn, A. K., Cardiac contractile proteins. Adenosine triphosphatase activity and physiological function. Circ. Res.45 (1979) 1–12.
Schwartz, K., Le Carpentier, Y., Martin, J. L., Lompre, A. M., Mercadier, J. J., and Swynghedaw, B., Myosin isoenzymic distribution correlates with speed of myocardial contraction. J. molec. cell. Cardiol.13 (1981) 1074–1075.
Shimada, Y., and Toyota, N., Troponin types in cardiac and skeletal muscles in vivo and in vitro: an immunofluorescence microscopic study, in: Congenital Heart Disease. Causes and Processes, pp. 133–144. Eds J. Nora and A. Takao. Futura Publishing Co., New York 1984.
Sissman, N. J., Cell multiplication rates during development of the primitive cardiac tube in the chick embryo. Nature210 (1966) 504–507.
Sperelakis, N., The possibility of propagation between myocardial cells not connected by low-resistance pathways, in: Myocardial Injury, pp. 1–23. Ed. J. J. Spitzer. Plenum Publishing Co., New York 1983.
Sperelakis, N., Shigenobu, K., and McLean, M. J., Membrane cation channels: Changes in developing hearts, in cell culture, and in organ culture, in: Developmental and Physiological Correlates of Cardiac Muscle, pp. 209–234. Eds M. Lieberman and T. Sano. Raven Press, New York 1975.
St. John Sutton, M. G., Plappert, T., Crosby, L., Douglas, P., Mullen, J., and Reichek, N., Effects of reduced left ventricular mass on chamber architecture, load, and function: a study of anorexis nervosa. Circulation5 (1985) 991–1000.
Stalsberg, H., The origin of heart asymmetry: Right and left contributions to the early chick embryo heart. Devl Biol.19 (1969) 109–127.
Stalsberg, H., Regional mitotic activity in the precardiac mesoderm and differentiating heart tube in the chick embryo. Devl Biol.20 (1969) 18–45.
Steding, G., and Seidl, E., Contribution to the development of the heart. I. Normal development. J. thorac. cardiovasc. Surg.28 (1980) 386–409.
Sweency, L. J., Contractile protein expression in embryonic heart development, in: Cardiac Morphogenesis, pp. 78–84. Eds V. J. Ferrans, G. C. Rosenquist and C. Weinstein. Elsevier, New York 1985.
Thompson, E. W., Marino, T. A., Uboh, C. E., Kent, R. L., and Cooper, G. IV, Atrophy reversal and cardiocyte redifferentiation in reloaded cat myocardium. Circ. Res.54 (1984) 367–377.
Thompson, R. P., Wong, Y.-M. H., and Fitzharris, T. P., A computer graphic study of cardiac truncal septation. Anat. Rec.206 (1983) 207–214.
Thornell, L. E., and Forsgren, S., Myocardial cell heterogeneity in the human heart with respect to myosin ATPase activity. Histochem. J.14 (1982) 479–490.
Tomanek, R. J., and Cooper, G. IV, Morphological changes in the mechanically unloaded myocardial cell. Anat. Rec.200 (1981) 271–280.
Van Mierop, L. H. S., Morphological and functional development of the chick cardiovascular system during the first week of incubation, in: Cardiac Development with Special Reference to Congenital Heart Disease. Ed. O. Jaffee. University of Dayton Press, Dayton 1970.
Van Mierop, L. H. S., Morphological development of the heart, in: Handbook of Physiology, Sect 2, Vol. 1, The Heart, pp. 1–27. American Physiological Society, Bethesda 1979.
Wainright, S. A., Biggs, W. D., Currey, J. D., and Gosline, J. M., Mechanical Designs in Organisms. John Wiley and Sons. New York 1976.
Whalen, R. G., Sell, S. M., Eriksson, A., and Thornell, L.-E., Myosin subunit types in skeletal and cardiac tissues and their developmental distribution. Devl Biol.91 (1982) 478–484.
Wiens, D., and Spooner, B. S., Actin isotype biosynthetic transitions in early cardiac organogenesis. Eur. J. Cell Biol.30 (1983) 60–66.
Wiens, D., Sullins, M., and Spooner, B. S., Precardiac mesoderm differentiation in vitro. Actin isotype synthetic transitions, myofibrillogenesis, initiation of heart beat, and the possible involvement of collagen. Differentiation28 (1984) 62–72.
Wilkinson, J. M., and Grand, R. J. A., Comparison of amino acid sequence of troponin I from different striated muscles. Nature271 (1978) 31–33.
Williams, R. S., Salmons, S., Newsholme, E. A., Kaufman, R. E., and Mellor, J., Regulation of nuclear and mitochondrial gene expression by contractile activity in skeletal muscle. J. biol. Chem.261 (1986) 376–380.
Woodroofe, M. N., and Lemanski, L. F., Two action variants in developing axolotl heart. Devl Biol.82 (1981) 172–179.
Wright, T. C., Destrempes, M., Orkin, R., and Kurnitt, D. M., Increased adhesiveness of Down syndrome fetal fibroblasts in vitro. Proc. natl Acad. Sci. USA81 (1984) 2426–2430.
Zak, R., Contractile function as a determinant of muscle growth, in: Cell and Muscle Motility, vol. 1, pp. 1–33. Eds R. M. Dowben and J. W. Shay. Plenum Publishing Corporation, New York 1981.
Zak, R., Factors controlling cardiac growth, in: Growth of the Heart in Health and Disease, pp. 165–185. Ed. R. Zak. Raven Press, New York 1984.
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Icardo, J.M. Heart anatomy and developmental biology. Experientia 44, 910–919 (1988). https://doi.org/10.1007/BF01939884
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DOI: https://doi.org/10.1007/BF01939884