Patterning of the heart field in the chick.

In human development, it is postulated based on histological sections, that the cardiogenic mesoderm rotates 180 degrees with the pericardial cavity. This is also thought to be the case in mouse development where gene expression data suggests that the progenitors of the right ventricle and outflow tract invert their position with respect to the progenitors of the atria and left ventricle. However, the inversion in both cases is inferred and has never been shown directly. We have used 3D reconstructions and cell tracing in chick embryos to show that the cardiogenic mesoderm is organized such that the lateralmost cells are incorporated into the cardiac inflow (atria and left ventricle) while medially placed cells are incorporated into the cardiac outflow (right ventricle and outflow tract). This happens because the cardiogenic mesoderm is inverted. The inversion is concomitant with movement of the anterior intestinal portal which rolls caudally to form the foregut pocket. The bilateral cranial cardiogenic fields fold medially and ventrally and fuse. After heart looping the seam made by ventral fusion will become the greater curvature of the heart loop. The caudal border of the cardiogenic mesoderm which ends up dorsally coincides with the inner curvature. Physical ablation of selected areas of the cardiogenic mesoderm based on this new fate map confirmed these results and, in addition, showed that the right and left atria arise from the right and left heart fields. The inversion and the new fate map account for several unexplained observations and provide a unified concept of heart fields and heart tube formation for avians and mammals.

[1]  M. Barron,et al.  Requirement for BMP and FGF signaling during cardiogenic induction in non‐precardiac mesoderm is specific, transient, and cooperative , 2000, Developmental dynamics : an official publication of the American Association of Anatomists.

[2]  M. Buckingham,et al.  Atrial myocardium derives from the posterior region of the second heart field, which acquires left-right identity as Pitx2c is expressed , 2008, Development.

[3]  V. García-Martínez,et al.  Primitive-streak origin of the cardiovascular system in avian embryos. , 1993, Developmental biology.

[4]  J. Litvin,et al.  Fate map of early avian cardiac progenitor cells. , 2001, Development.

[5]  R. Markwald,et al.  Living Morphogenesis of the Heart , 1998, Cardiovascular Molecular Morphogenesis.

[6]  P. Tam,et al.  The allocation of epiblast cells to the embryonic heart and other mesodermal lineages: the role of ingression and tissue movement during gastrulation. , 1997, Development.

[7]  M. Kirby,et al.  Hensen's node gives rise to the ventral midline of the foregut: implications for organizing head and heart development. , 2003, Developmental biology.

[8]  E. Tzahor,et al.  Mesoderm progenitor cells of common origin contribute to the head musculature and the cardiac outflow tract , 2006, Development.

[9]  C. Sánchez-Gómez,et al.  Straight Tube Heart. Primitive Cardiac Cavities vs. Primitive Cardiac Segments , 1998 .

[10]  K. Linask,et al.  Cardiac morphogenesis: Matrix metalloproteinase coordination of cellular mechanisms underlying heart tube formation and directionality of looping , 2005, Developmental dynamics : an official publication of the American Association of Anatomists.

[11]  Rocky S. Tuan,et al.  Developmental Biology Protocols , 2000 .

[12]  R. Markwald,et al.  Bidirectional fusion of the heart‐forming fields in the developing chick embryo , 2006, Developmental dynamics : an official publication of the American Association of Anatomists.

[13]  K. Storey,et al.  A spatial and temporal map of FGF/Erk1/2 activity and response repertoires in the early chick embryo. , 2007, Developmental biology.

[14]  Roger M. Ilagan,et al.  Fgf8 is required for anterior heart field development , 2006, Development.

[15]  S. Chapman,et al.  Analysis of spatial and temporal gene expression patterns in blastula and gastrula stage chick embryos. , 2002, Developmental biology.

[16]  M. Buckingham,et al.  The arterial pole of the mouse heart forms from Fgf10-expressing cells in pharyngeal mesoderm. , 2001, Developmental cell.

[17]  F. T. Lewis.  Contributions to Embryology , 1919 .

[18]  A. Moorman,et al.  Formation of the Venous Pole of the Heart From an Nkx2–5–Negative Precursor Population Requires Tbx18 , 2006, Circulation research.

[19]  G. Schoenwolf,et al.  Evidence that translation of smooth muscle alpha‐actin mRNA is delayed in the chick promyocardium until fusion of the bilateral heart‐forming regions , 2000, Developmental dynamics : an official publication of the American Association of Anatomists.

[20]  A. Moorman,et al.  Morphogenesis of the Vertebrate Heart , 2007 .

[21]  K. Linask.  N-cadherin localization in early heart development and polar expression of Na+,K(+)-ATPase, and integrin during pericardial coelom formation and epithelialization of the differentiating myocardium. , 1992, Developmental biology.

[22]  A. Moorman,et al.  Trabeculated Right Ventricular Free Wall in the Chicken Heart Forms by Ventricularization of the Myocardium Initially Forming the Outflow Tract , 2007, Circulation research.

[23]  T. Yatskievych,et al.  Myocardin expression during avian embryonic heart development requires the endoderm but is independent of BMP signaling , 2008, Developmental dynamics : an official publication of the American Association of Anatomists.

[24]  Yunqing Shi,et al.  Isl1 identifies a cardiac progenitor population that proliferates prior to differentiation and contributes a majority of cells to the heart. , 2003, Developmental cell.

[25]  J. Seidman,et al.  Chamber-specific cardiac expression of Tbx5 and heart defects in Holt-Oram syndrome. , 1999, Developmental biology.

[26]  Jan M Ruijter,et al.  Three-dimensional reconstruction of gene expression patterns during cardiac development. , 2003, Physiological genomics.

[27]  Cornelis J Weijer,et al.  Cell movement patterns during gastrulation in the chick are controlled by positive and negative chemotaxis mediated by FGF4 and FGF8. , 2002, Developmental cell.

[28]  V. García-Martínez,et al.  Localization of Cells of the Prospective Neural Plate, Heart and Somites within the Primitive Streak and Epiblast of Avian Embryos at Intermediate Primitive-Streak Stages , 2001, Cells Tissues Organs.

[29]  G. Rosenquist.  Location and movements of cardiogenic cells in the chick embryo: the heart-forming portion of the primitive streak. , 1970, Developmental Biology.

[30]  H. Stalsberg,et al.  The precardiac areas and formation of the tubular heart in the chick embryo. , 1969, Developmental biology.

[31]  András Czirók,et al.  Mesodermal cell displacements during avian gastrulation are due to both individual cell-autonomous and convective tissue movements , 2006, Proceedings of the National Academy of Sciences.

[32]  M. E. Rawles.  The Heart-Forming Areas of the Early Chick Blastoderm , 1943, Physiological Zoology.

[33]  M. Kirby,et al.  Secondary heart field contributes myocardium and smooth muscle to the arterial pole of the developing heart. , 2005, Developmental biology.

[34]  M. E. Rawles.  A study in the localization of organ-forming areas in the chick blastoderm of the head-process stage , 1936 .

[35]  J. Bernanke,et al.  Left-right lineage analysis of the embryonic Xenopus heart reveals a novel framework linking congenital cardiac defects and laterality disease , 2006, Development.

[36]  G. Schoenwolf,et al.  Islet‐1 marks the early heart rudiments and is asymmetrically expressed during early rotation of the foregut in the chick embryo , 2000, The Anatomical record.

[37]  A. Lassar,et al.  Induction of avian cardiac myogenesis by anterior endoderm. , 1995, Development.

[38]  M. Mercola,et al.  Heart induction by Wnt antagonists depends on the homeodomain transcription factor Hex. , 2005, Genes & development.

[39]  A. G. Gittenberger-de Groot,et al.  Early formation of the vascular system in quail embryos , 1993, The Anatomical record.

[40]  S. Chapman,et al.  Improved method for chick whole‐embryo culture using a filter paper carrier , 2001, Developmental dynamics : an official publication of the American Association of Anatomists.

[41]  Yunfu Sun,et al.  Islet 1 is expressed in distinct cardiovascular lineages, including pacemaker and coronary vascular cells. , 2007, Developmental biology.

[42]  D. Noden.  Origins and patterning of avian outflow tract endocardium. , 1991, Development.

[43]  M. Buckingham,et al.  Building the mammalian heart from two sources of myocardial cells , 2005, Nature Reviews Genetics.

[44]  G. Eichele,et al.  Expression of chick Tbx-2, Tbx-3, and Tbx-5 genes during early heart development: evidence for BMP2 induction of Tbx2. , 2000, Developmental biology.

[45]  D. Wilkinson.  In situ hybridization: a practical approach , 1998 .

[46]  M. Kirby,et al.  Conotruncal myocardium arises from a secondary heart field. , 2001, Development.

[47]  M. Mercola,et al.  Multiple functions of Cerberus cooperate to induce heart downstream of Nodal. , 2007, Developmental biology.

[48]  Y. Jiang,et al.  Common role for each of the cGATA-4/5/6 genes in the regulation of cardiac morphogenesis. , 1998, Developmental genetics.

[49]  D. Rudnick.  PROSPECTIVE AREAS AND DIFFERENTIATION POTENCIES IN THE CHICK BLASTODERM , 1948, Annals of the New York Academy of Sciences.

[50]  Jane A. Langdale,et al.  In situ Hybridization , 1994 .

[51]  M. Buckingham,et al.  A retrospective clonal analysis of the myocardium reveals two phases of clonal growth in the developing mouse heart , 2003, Development.

[52]  K. Yutzey,et al.  Lack of regulation in the heart forming region of avian embryos. , 1999, Developmental biology.

[53]  D. New.  A New Technique for the Cultivation of the Chick Embryo in vitro , 1955 .

[54]  T. Schultheiss,et al.  Regulation of avian cardiogenesis by Fgf8 signaling. , 2002, Development.

[55]  M. DeRuiter,et al.  The development of the myocardium and endocardium in mouse embryos , 1992, Anatomy and Embryology.

[56]  K. L. Moore,et al.  The Developing Human: Clinically Oriented Embryology , 1973 .

[57]  D. Darnell,et al.  Dynamic labeling techniques for fate mapping, testing cell commitment, and following living cells in avian embryos. , 2000, Methods in molecular biology.