Building the mammalian heart from two sources of myocardial cells (original) (raw)
Garcia-Martinez, V. & Schoenwolf, G. C. Primitive-streak origin of the cardiovascular system in avian embryos. Dev. Biol.159, 706–719 (1993). ArticleCASPubMed Google Scholar
Tam, P. P., Parameswaran, M., Kinder, S. J. & Weinberger, R. P. The allocation of epiblast cells to the embryonic heart and other mesodermal lineages: the role of ingression and tissue movement during gastrulation. Development124, 1631–1642 (1997). CASPubMed Google Scholar
Rawles, M. E. The heart-forming areas of the early chick blastoderm. Physiol. Zool. 22–42 (1943).
Rosenquist, G. C. Location and movements of cardiogenic cells in the chick embryo: the heart-forming portion of the primitive streak. Dev. Biol.22, 461–475 (1970). ArticleCASPubMed Google Scholar
de la Cruz, M. & Markwald, R. (eds) Living Morphogenesis of the Heart (Birkhauser, Boston, 1999). Google Scholar
de la Cruz, M. V., Sanchez Gomez, C., Arteaga, M. M. & Arguello, C. Experimental study of the development of the truncus and the conus in the chick embryo. J. Anat.123, 661–686 (1977). CASPubMedPubMed Central Google Scholar
Rosenquist, G. C. & DeHaan, R. L. Migration of precardiac cells in the chick embryo: a radioautographic study. Contrib. Embryol.38, 111–121 (1966). Google Scholar
Stalsberg, H. & DeHaan, R. L. The precardiac areas and formation of the tubular heart in the chick embryo. Dev. Biol.19, 128–159 (1969). ArticleCASPubMed Google Scholar
Inagaki, T., Garcia-Martinez, V. & Schoenwolf, G. C. Regulative ability of the prospective cardiogenic and vasculogenic areas of the primitive streak during avian gastrulation. Dev. Dyn.197, 57–68 (1993). ArticleCASPubMed Google Scholar
Patwardhan, V., Fernandez, S., Montgomery, M. & Litvin, J. The rostro-caudal position of cardiac myocytes affect their fate. Dev. Dyn.218, 123–135 (2000). ArticleCASPubMed Google Scholar
Redkar, A., Montgomery, M. & Litvin, J. Fate map of early avian cardiac progenitor cells. Development128, 2269–2279 (2001). CASPubMed Google Scholar
Satin, J., Fujii, S. & DeHaan, R. L. Development of cardiac beat rate in early chick embryos is regulated by regional cues. Dev. Biol.129, 103–113 (1988). ArticleCASPubMed Google Scholar
Meilhac, S. M. et al. A retrospective clonal analysis of the myocardium reveals two phases of clonal growth in the developing mouse heart. Development130, 3877–3889 (2003). ArticleCASPubMed Google Scholar
Christoffels, V. M. et al. Chamber formation and morphogenesis in the developing mammalian heart. Dev. Biol.223, 266–278 (2000). ArticleCASPubMed Google Scholar
Christoffels, V. M. et al. T-box transcription factor Tbx2 represses differentiation and formation of the cardiac chambers. Dev. Dyn.229, 763–770 (2004). ArticleCASPubMed Google Scholar
Meilhac, S. M., Esner, M., Kerszberg, M., Moss, J. E. & Buckingham, M. E. Oriented clonal cell growth in the developing mouse myocardium underlies cardiac morphogenesis. J. Cell Biol.164, 97–109 (2004). ArticleCASPubMedPubMed Central Google Scholar
Viragh, S. & Challice, C. E. Origin and differentiation of cardiac muscle cells in the mouse. J. Ultrastructure Res.42, 1–24 (1973). ArticleCAS Google Scholar
De Vries, P. A. Evolution of Precardiac and Splanchnic Mesoderm in Relationship to the Infundibulum and Truncus 31–48 (Raven, New York, 1981). Google Scholar
Mjaatvedt, C. H. et al. The outflow tract of the heart is recruited from a novel heart-forming field. Dev. Biol.238, 97–109 (2001). This paper demonstrates the existence of a second source of myocardial cells in pharyngeal mesoderm in the avian embryo; these cells constitute a novel heart field that contributes to the outflow-tract region of the heart. ArticleCASPubMed Google Scholar
Waldo, K. L. et al. Conotruncal myocardium arises from a secondary heart field. Development128, 3179–3188 (2001). Similar to reference 20, this study describes manipulations in the chick embryo that showed the presence of a novel heart field that contributes to outflow-tract myocardium. These cells are reported to be located anteriorly to the heart tube and immediately adjacent to it. CASPubMed Google Scholar
Kelly, R. G., Brown, N. A. & Buckingham, M. E. The arterial pole of the mouse heart forms from _Fgf10_-expressing cells in pharyngeal mesoderm. Dev. Cell1, 435–440 (2001). This study in mice demonstrates the existence of a second source of myocardial cells in pharyngeal mesoderm that contribute to the outflow-tract myocardium at the arterial pole of the heart. These cells initially lie medially to the cardiac crescent before assuming a position that is dorsal and anterior to the heart tube. ArticleCASPubMed Google Scholar
Zaffran, S., Kelly, R. G., Meilhac, S. M., Buckingham, M. E. & Brown, N. A. Right ventricular myocardium derives from the anterior heart field. Circ. Res.95, 261–268 (2004). This paper extends the observations reported in reference 22 to show that pharyngeal mesoderm also contributes to right-ventricular, as well as outflow-tract, myocardium. In addition, the authors show that the primitive heart tube in the mouse has an essentially left-ventricular identity. ArticleCASPubMed Google Scholar
Kelly, R. G. & Buckingham, M. E. The anterior heart-forming field: voyage to the arterial pole of the heart. Trends Genet.18, 210–216 (2002). ArticleCASPubMed Google Scholar
Cai, C. L. et al. Isl1 identifies a cardiac progenitor population that proliferates prior to differentiation and contributes a majority of cells to the heart. Dev. Cell5, 877–889 (2003). This paper provides evidence for a more extensive second heart field. The authors show thatIsl1is expressed and required in myocardial progenitor cells that contribute to the venous as well as the arterial pole of the mouse heart. ArticleCASPubMedPubMed Central Google Scholar
Meilhac, S. M., Esner, M., Kelly, R. G., Nicolas, J. F. & Buckingham, M. E. The clonal origin of myocardial cells in different regions of the embryonic mouse heart. Dev. Cell6, 685–698 (2004). This paper presents a retrospective clonal analysis of myocardial cells in the early mouse heart and demonstrates the existence of two lineages that segregate early. The second lineage contribution can be compared to that of the second heart field, marked byIsl1, whereas the first lineage colonizes all myocardium except that of the outflow tract. ArticleCASPubMed Google Scholar
Yutzey, K. E., Rhee, J. T. & Bader, D. Expression of the atrial-specific myosin heavy chain AMHC1 and the establishment of anteroposterior polarity in the developing chicken heart. Development120, 871–883 (1994). CASPubMed Google Scholar
Kitajima, S., Takagi, A., Inoue, T. & Saga, Y. MesP1 and MesP2 are essential for the development of cardiac mesoderm. Development127, 3215–3226 (2003). Google Scholar
Brand, T. Heart development: molecular insights into cardiac specification and early morphogenesis. Dev. Biol.258, 1–19 (2003). ArticleCASPubMed Google Scholar
Brown, C. O. 3rd et al. The cardiac determination factor, Nkx2-5, is activated by mutual cofactors GATA-4 and Smad1/4 via a novel upstream enhancer. J. Biol. Chem.279, 10659–10669 (2004). ArticleCASPubMed Google Scholar
Hochgreb, T. et al. A caudorostral wave of RALDH2 conveys anteroposterior information to the cardiac field. Development130, 5363–5374 (2003). ArticleCASPubMed Google Scholar
Franco, D. & Campione, M. The role of Pitx2 during cardiac development. Linking left-right signaling and congenital heart diseases. Trends Cardiovasc. Med.13, 157–163 (2003). ArticleCASPubMed Google Scholar
Liu, C. et al. Pitx2c patterns anterior myocardium and aortic arch vessels and is required for local cell movement into atrioventricular cushions. Development129, 5081–5091 (2002). ArticleCASPubMed Google Scholar
Kuo, C. T. et al. GATA4 transcription factor is required for ventral morphogenesis and heart tube formation. Genes Dev.11, 1048–1060 (1997). ArticleCASPubMed Google Scholar
Molkentin, J. D., Lin, Q., Duncan, S. A. & Olson, E. N. Requirement for the transcription factor GATA4 for heart tube formation and ventral morphogenesis. Genes Dev.11, 1061–1072 (1997). ArticleCASPubMed Google Scholar
Li, S., Zhou, D., Lu, M. M. & Morrisey, E. E. Advanced cardiac morphogenesis does not require heart tube fusion. Science305, 1619–1622 (2004). ArticleCASPubMed Google Scholar
Lin, Q., Schwarz, J., Bucana, C. & Olson, E. N. Control of mouse cardiac morphogenesis and myogenesis by transcription factor MEF2C. Science276, 1404–1407 (1997). ArticleCASPubMedPubMed Central Google Scholar
Tanaka, M., Schinke, M., Liao, H. S., Yamasaki, N. & Izumo, S. Nkx2.5 and Nkx2.6, homologs of Drosophila tinman, are required for development of the pharynx. Mol. Cell. Biol.21, 4391–4398 (2001). ArticleCASPubMedPubMed Central Google Scholar
Small, E. M. & Krieg, P. A. Molecular regulation of cardiac chamber-specific gene expression. Trends Cardiovasc. Med.14, 13–18 (2004). ArticleCASPubMed Google Scholar
Habets, P. E., Moorman, A. F. & Christoffels, V. M. Regulatory modules in the developing heart. Cardiovasc. Res.58, 246–263 (2003). ArticleCASPubMed Google Scholar
Lyons, I. et al. Myogenic and morphogenetic defects in the heart tubes of murine embryos lacking the homeo box gene Nkx2-5. Genes Dev.9, 1654–1666 (1995). ArticleCASPubMed Google Scholar
Tanaka, M. et al. Complex modular _cis_-acting elements regulate expression of the cardiac specifying homeobox gene Csx/Nkx2.5. Development126, 1439–1450 (1999). CASPubMed Google Scholar
Yamagishi, H. et al. The combinatorial activities of Nkx2.5 and dHAND are essential for cardiac ventricle formation. Dev. Biol.239, 190–203 (2001). ArticleCASPubMed Google Scholar
Srivastava, D. HAND proteins: molecular mediators of cardiac development and congenital heart disease. Trends Cardiovasc. Med.9, 11–18 (1999). ArticleCASPubMed Google Scholar
Biben, C. & Harvey, R. P. Homeodomain factor Nkx2–5 controls left/right asymmetric expression of bHLH gene eHand during murine heart development. Genes Dev.11, 1357–1369 (1997). ArticleCASPubMed Google Scholar
Riley, P., Anson-Cartwright, L. & Cross, J. C. The Hand1 bHLH transcription factor is essential for placentation and cardiac morphogenesis. Nature Genet.18, 271–275 (1998). ArticleCASPubMed Google Scholar
Firulli, A. B., McFadden, D. G., Lin, Q., Srivastava, D. & Olson, E. N. Heart and extra-embryonic mesodermal defects in mouse embryos lacking the bHLH transcription factor Hand1. Nature Genet.18, 266–270 (1998). ArticleCASPubMed Google Scholar
McFadden, D. G. et al. A GATA-dependent right ventricular enhancer controls dHAND transcription in the developing heart. Development127, 5331–5341 (2000). CASPubMed Google Scholar
McFadden, D. G. et al. The Hand1 and Hand2 transcription factors regulate expansion of the embryonic cardiac ventricles in a gene dosage-dependent manner. Development132, 189–201 (2005). ArticleCASPubMed Google Scholar
Bruneau, B. G. et al. A murine model of Holt–Oram syndrome defines roles of the T-box transcription factor Tbx5 in cardiogenesis and disease. Cell106, 709–721 (2001). ArticleCASPubMed Google Scholar
Takeuchi, J. K. et al. Tbx5 specifies the left/right ventricles and ventricular septum position during cardiogenesis. Development130, 5953–5964 (2003). ArticleCASPubMed Google Scholar
Min, H. et al. Fgf-10 is required for both limb and lung development and exhibits striking functional similarity to Drosophila branchless. Genes Dev.12, 3156–3161 (1998). ArticleCASPubMedPubMed Central Google Scholar
Sekine, K. et al. Fgf10 is essential for limb and lung formation. Nature Genet.21, 138–141 (1999). ArticleCASPubMed Google Scholar
Abu-Issa, R., Smyth, G., Smoak, I., Yamamura, K. & Meyers, E. N. Fgf8 is required for pharyngeal arch and cardiovascular development in the mouse. Development129, 4613–4625 (2002). CASPubMed Google Scholar
Frank, D. U. et al. An Fgf8 mouse mutant phenocopies human 22q11 deletion syndrome. Development129, 4591–4603 (2002). CASPubMed Google Scholar
Yelbuz, T. M. et al. Myocardial volume and organization are changed by failure of addition of secondary heart field myocardium to the cardiac outflow tract. Dev. Dyn.228, 152–160 (2003). ArticlePubMed Google Scholar
Garg, V. et al. Tbx1, a DiGeorge syndrome candidate gene, is regulated by sonic hedgehog during pharyngeal arch development. Dev. Biol.235, 62–73 (2001). ArticleCASPubMed Google Scholar
Jerome, L. A. & Papaioannou, V. E. DiGeorge syndrome phenotype in mice mutant for the T-box gene, Tbx1. Nature Genet.27, 286–291 (2001). ArticleCASPubMed Google Scholar
Lindsay, E. A. et al. Tbx1 haploinsufficieny in the DiGeorge syndrome region causes aortic arch defects in mice. Nature410, 97–101 (2001). ArticleCASPubMed Google Scholar
Merscher, S. et al. Tbx1 is responsible for cardiovascular defects in velo-cardio-facial/DiGeorge syndrome. Cell104, 619–629 (2001). ArticleCASPubMed Google Scholar
Hu, T. et al. Tbx1 regulates fibroblast growth factors in the anterior heart field through a reinforcing autoregulatory loop involving forkhead transcription factors. Development131, 5491–5502 (2004). This paper uses a genetic approach to show a role of TBX1 in the second heart field, distinguishing effects on outflow-tract myocardium from those on pharyngeal-arch development. The authors also identify a TBX1-dependent enhancer that functions on theFgf8gene, so providing evidence for a direct link between these markers of the second heart field. ArticleCASPubMed Google Scholar
Brown, C. B. et al. Cre-mediated excision of Fgf8 in the Tbx1 expression domain reveals a critical role for Fgf8 in cardiovascular development in the mouse. Dev. Biol.267, 190–202 (2004). With the caveat thatTbx1is not re-expressed in the myocardium, these Cre–loxPexperiments indicate that the second heart field makes an extensive contribution to the adult heart. ArticleCASPubMed Google Scholar
Xu, H. et al. Tbx1 has a dual role in the morphogenesis of the cardiac outflow tract. Development131, 3217–3227 (2004). This paper, as with reference 64, points to a role forTbx1in the anterior part of the second heart field and shows thatTbx1-expressing progenitor cells contribute to the arterial pole of the heart.Tbx1affects the proliferation of these cells, possibly through an effect onFgf10. ArticleCASPubMed Google Scholar
Vitelli, F. et al. A genetic link between Tbx1 and fibroblast growth factor signaling. Development129, 4605–4611 (2002). CASPubMed Google Scholar
Kochilas, L. et al. The role of neural crest during cardiac development in a mouse model of DiGeorge syndrome. Dev. Biol.251, 157–166 (2002). ArticleCASPubMed Google Scholar
Kume, T., Jiang, H., Topczewska, J. M. & Hogan, B. L. The murine winged helix transcription factors, Foxc1 and Foxc2, are both required for cardiovascular development and somitogenesis. Genes Dev.15, 2470–2482 (2001). ArticleCASPubMedPubMed Central Google Scholar
Yamagishi, H. et al. Tbx1 is regulated by tissue-specific forkhead proteins through a common Sonic hedgehog-responsive enhancer. Genes Dev.17, 269–281 (2003). ArticleCASPubMedPubMed Central Google Scholar
Takeuchi, J. K. et al. Tbx20 dose-dependently regulates transcription factor networks required for mouse heart and motoneuron development. Development132, 2463–2474 (2005). ArticleCASPubMed Google Scholar
von Both, I. et al. Foxh1 is essential for development of the anterior heart field. Dev. Cell7, 331–345 (2004). These authors show that FOXH1, expressed in the anterior part of the second heart field, has a role in the formation of outflow-tract and right-ventricular myocardium. They also propose thatMef2cmay be regulated by FOXH1, in conjunction with NKX2-5. ArticleCASPubMed Google Scholar
Chen, X. et al. Smad4 and FAST-1 in the assembly of activin-responsive factor. Nature389, 85–89 (1997). ArticleCASPubMed Google Scholar
Weisberg, E. et al. A mouse homologue of FAST-1 transduces TGF-β superfamily signals and is expressed during early embryogenesis. Mech. Dev.79, 17–27 (1998). ArticleCASPubMed Google Scholar
Edmondson, D. G., Lyons, G. E., Martin, J. F. & Olson, E. N. Mef2 gene expression marks the cardiac and skeletal muscle lineages during mouse embryogenesis. Development120, 1251–1263 (1994). CASPubMed Google Scholar
Pollock, R. & Treisman, R. Human SRF-related proteins: DNA-binding properties and potential regulatory targets. Genes Dev.5, 2327–2341 (1991). ArticleCASPubMed Google Scholar
Dodou, E., Verzi, M. P., Anderson, J. P., Xu, S. M. & Black, B. L. Mef2c is a direct transcriptional target of ISL1 and GATA factors in the anterior heart field during mouse embryonic development. Development131, 3931–3942 (2004). This paper describes an enhancer that controls expression of theMef2cgene. The enhancer is active in the second heart field and is activated by ISL1 and GATA4, so providing an example of a regulatory network in this field. ArticleCASPubMed Google Scholar
Phan, D. et al. BOP, a regulator of right ventricular heart development, is a direct transcriptional target of MEF2C in the developing heart. Development132, 2669–2678 (2005). ArticleCASPubMed Google Scholar
Gottlieb, P. D. et al. Bop encodes a muscle-restricted protein containing MYND and SET domains and is essential for cardiac differentiation and morphogenesis. Nature Genet.31, 25–32 (2002). ArticleCASPubMed Google Scholar
Srivastava, D., Cserjesi, P. & Olson, E. N. A subclass of bHLH proteins required for cardiac morphogenesis. Science270, 1995–1999 (1995). ArticleCASPubMed Google Scholar
Srivastava, D. et al. Regulation of cardiac mesodermal and neural crest development by the bHLH transcription factor, dHAND. Nature Genet.16, 154–160 (1997). ArticleCASPubMed Google Scholar
Thomas, T. et al. A signaling cascade involving endothelin-1, dHAND and msx1 regulates development of neural-crest-derived branchial arch mesenchyme. Development125, 3005–3014 (1998). CASPubMed Google Scholar
Singh, M. K. et al. Tbx20 is essential for cardiac chamber differentiation and repression of Tbx2. Development132, 2697–2707 (2005). ArticleCASPubMed Google Scholar
Stennard, F. A. et al. Murine T-box transcription factor Tbx20 acts as a repressor during heart development, and is essential for adult heart integrity, function and adaptation. Development132, 2451–2462 (2005). ArticleCASPubMed Google Scholar
Cai, C. L. et al. T-box genes coordinate regional rates of proliferation and regional specification during cardiogenesis. Development132, 2475–2487 (2005). ArticleCASPubMed Google Scholar
Harrelson, Z. et al. Tbx2 is essential for patterning the atrioventricular canal and for morphogenesis of the outflow tract during heart development. Development131, 5041–5052 (2004). ArticleCASPubMed Google Scholar
Christoffels, V. M., Burch, J. B. & Moorman, A. F. Architectural plan for the heart: early patterning and delineation of the chambers and the nodes. Trends Cardiovasc. Med.14, 301–307 (2004). ArticlePubMed Google Scholar
Clark, E. B. in The Genetics of Cardiovascular Diseases (eds Pierpont, M. E. & Moller, J. M.) 3–11 (Martinus-Nijoff, Boston, 1986). Google Scholar
Fishman, M. & Olson, E. Parsing the heart: genetic modules for organ assembly. Cell17, 153–156 (1997). Article Google Scholar
Abu-Issa, R., Waldo, K. & Kirby, M. L. Heart fields: one, two or more? Dev. Biol.272, 281–285 (2004). ArticleCASPubMed Google Scholar