Summary
Grafts of mesoderm taken from the precardiac region of quail embryos of stages 5–7 were inserted into the precardiac mesoderm of chick embryos of stages 5–7. The experiments were of four types and were codenamed to indicate the origin and the destination of the graft. QACP: tissue from the anterior end of the quail precardiac area was inserted into the posterior end of the chick precardiac mesoderm; QPCA: tissue from the posterior end of the quail precardiac area was inserted into the anterior end of the chick precardiac mesoderm; QACA: tissue from the anterior end of the quail precardiac area was inserted into the anterior end of the chick precardiac mesoderm; QPCP: tissue from the posterior end of the quail precardiac area was inserted into the posterior end of the chick precardiac mesoderm. In no case was precardiac tissue removed from the host. Three main types of anomaly were obtained: inverted hearts, in which looping took place to the left rather than to the right; compact hearts, in which no looping occurred, and hearts in which extra tissues or regions were apparent. The incidence of compact hearts was significantly greater with QPCA than with any other category of experiment. When older donors were used (stages 8–9), the incidence of compact hearts fell. No variations in the origin of the graft, nor in its ultimate destination in the host, were found to affect the frequency of any of the anomalies. Sections showed that quail hearts tended to have thicker walls than chick hearts; although quail tissues were often incorporated into the host chick hearts, they retained the histological characteristics of the donors. The fact that no compact hearts resulted from the experiment QACA, or from the mock operations, leads us to conclude that failure to loop in the compact hearts was not due to mechanical trauma caused by the operation, but to some specific difference between grafts taken from the anterior and posterior precardiac mesoderm. The fact that compact hearts were obtained when chick donors were used instead of quails, shows that the effect is not species-specific. We propose that a morphogen is secreted by the posterior end of the precardiac mesoderm and this plays a role in controlling the cessation of looping.
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References
Baldwin HS, Solursh M (1989) Degradation of hyaluronic acid does not prevent looping of the mammalian heart in situ. Dev Biol 136:555–559
Boucaut JC, Darribere T, Poole TJ, Aoyama H, Thiery JP (1984) Biologically active synthetic peptides as probes of embryonic development: a competitive inhibitor of fibronectin function inhibits gastrulation in amphibian embryos and neural crest migration in avian embryos. J Cell Biol 99:1822–1830
Brown NA, Wolpert L (1990) The development of handedness in left/right asymmetry. Development 109:1–9
Butler JK (1952) An experimental analysis of cardiac loop formation of the heart tube in the chick. MA thesis University of Texas. Not seen (quoted by Manasek 1981)
Castro-Quezada A, Nadal-Ginard B, De La Cruz M (1972) Experimental study of the formation of the bulbo-ventricular loop in the chick. J Embryol Exp Morphol 27:623–637
Chambers EG (1952) Statistical Calculation. Cambridge University Press, Cambridge
Easton HS (1991) Migration and differentiation of precardiac mesoderm in the chick embryo. PhD thesis, University of London
Hamburger V, Hamilton HL (1951) A series of normal stages in the development of the chick embryo. J Morphol 88:49–92
Hay DA, Markwald RR, Fitzharris TP (1984) Selected views of early heart development by scanning electron microscopy. Scanning Electron Microsc IV: 1983–1993
Hiruma T, Hirakow R (1985) An ultrastructural topographic study on myofibrillogenesis in the heart of the chick embryo during pulsation onset period. Anat Embryol 172:325–329
Hutson JM, Donahoe PK (1984) Improved histology for chickquail chimaeras. Stain Technol 59:105–111
Itasaki N, Nakamura H, Yasuda M (1989) Changes in the arrangement of actin bundles during heart looping in the chick embryo. Anat Embryol 180:413–420
Itasaki N, Nakamura H, Sumida H, Yasuda M (1991) Actin bundles on the right side in the caudal part of the heart tube play a role in dextro-looping in the embryonic chick heart. Anat Embryol 183:29–39
Krug EL, Runyan RB, Markwald RR (1985) Protein extracts from early embryonic hearts initiate cardiac endothelial cytodifferentiation. Dev Biol 112:414–426
Krug EL, Mjaatvedt CH, Markwald RR (1987) Extracellular matrix from embryonic myocardium elicits an early morphogenetic event in cardiac endothelial differentiation. Dev Biol 120:348–355
Lash JW, Seitz AW, Cheney CM, Ostrovsky D (1984) On the role of fibronectin during the compaction stage of somitogenesis in the chick embryo. J Exp Zool 232:197–206
Lash JW, Linask KK, Yamada KM (1987) Synthetic peptides that mimic the adhesive recognition signal of fibronectin: differential effects on cell-cell and cell-substratum adhesion in embryonic chick cells. Dev Biol 123:411–420
Lepori NG (1967) Research on heart development in the chick embryo under normal and experimental conditions. Monit Zool Ital (NS) 1:159–183
Linask KK, Lash JW (1986) Precardiac cell migration: fibronectin localization at mesoderm: endoderm interface during directional migration. Dev Biol 114:87–101
Linask KK, Lash JW (1988) A role for fibronectin in the migration of avian precardiac cells. II Rotation of the heart-forming region during different stages and its effects. Dev Biol 129:324–329
Manasek FJ (1970) Histogenesis of the embryonic myocardium. Am J Cardiol 25:149–168
Manasek FJ, Nakamura A (1985) Forces and deformations: their origins and regulation in early development. In: Ferrans VF, Rosenquist G, Weinstein C (eds) Cardiac morphogenesis. Elsevier
Manasek FJ, Burnside MB, Waterman RE (1972) Myocardial cell shape change as a mechanism of embryonic heart looping. Dev Biol 29:349–371
Manasek FM (1981) Determinants of heart shape in early embryos. Fed Proc 40:2011–2016
Nakamura A, Kulikowski RR, Lacktis JW, Manasek DMD (1980) Heart looping: a regulated response to deforming forces. In: Van Pragh R (ed) Etiology and morphogenesis of congenital heart disease. Futura, New York, pp 81–98
New DAT (1955) A new technique for the cultivation of the chick embryo in vitro. J Embryol Exp Morphol 3:320–331
Norgren G, Ebendal T, Wikstrom H (1984) Production of nerve growth-stimulating factor(s) from chick embryo heart cells. Exp Cell Res 152:427–435
Osmond MK (1989) The effects of vitamin A on the development of mesodermal tissues in the chick embryo. PhD thesis, University of London
Pannett CA, Compton A (1924) The cultivation of tissues in saline embryonic juice. Lancet 1:289–317
Pollock RC, Palmer MY, Bellairs R (1991) The effect of fibronectin on cultures of precardiac mesoderm cells from the chick embryo. J Anat 176:246
Potts JD, Runyan RB (1989) Epithelial-mesenchymal cell transformation in the embryonic heart can be mediated, in part, by transforming growth factor β. Dev Biol 134:392–401
Rosenquist GC, DeHaan RL (1966) Migration of precardiac cells in the chick embryo: a radioautographic study. Carnegie Inst, Washington Contrib Embryol 263:71–110
Sanders EJ (1989) The cell surface in embryogenesis and carcinogenesis. Telford Press, New Jersey
Satin J, Fujii S, DeHaan RL (1988) Development of cardiac beat rate in early chick embryos is regulated by regional cues. Dev Biol 129:103–113
Smith SC, Armstrong JB (1991) Heart development in normal and cardiac-lethal mutant axolotls: a model for the control of vertebrate cardiogenesis. Differentiaton (in press)
Stalsberg H (1969) The origin of heart asymmetry: right and left contributions to the early chick embryo heart. Dev Biol 19:109–127
Stalsberg H (1970) Mechanism of dextral looping of the heart. Am J Cardiol 25:265–271
Stalsberg H, DeHaan RL (1968) Endodermal movements during foregut formation in the chick embryo. Dev Biol 18:198–215
Stalsberg H, DeHaan RL (1969) The precardiac areas and formation of the tubular heart in the chick embryo. Dev Biol 19:128–159
Tickle C, Lee J, Eichele G (1985) A quantitative analysis of the effect of all-trans-retinoic acid on the pattern of chick wing development. Dev Biol 109:82–95
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Easton, H., Veini, M. & Bellairs, R. Cardiac looping in the chick embryo: the role of the posterior precardiac mesoderm. Anat Embryol 185, 249–258 (1992). https://doi.org/10.1007/BF00211823
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DOI: https://doi.org/10.1007/BF00211823