Advertisement

Abstract

The heart forms from the first and second heart fields which contribute to distinct regions of the myocardium. This is supported by clonal analyses which identify corresponding first and second cardiac cell lineages in the heart. Progenitor cells of the second heart field and its subdomains are controlled by a gene regulatory network and by signalling pathways which determine their behaviour. Multipotent cells in this field also can contribute cardiac endothelial and smooth muscle cells. Furthermore skeletal muscles of the head and neck are related clonally to myocardial cells that form the arterial and venous poles of the heart. These lineage relationships, together with the genes that regulate the heart fields, have major implications for congenital heart disease.

Keywords

First heart field FHF Second heart field SHF Progenitor cells Cardiogenesis Neural crest Pharyngeal mesoderm Fibroblast growth factor 10 Fgf10 Islet 1 Clonal analysis Mesp1 GATA-binding protein 4 GATA4 T-box 5 TBX5 Arterial pole Canonical WNT signalling Hedgehog signalling BMP signalling Venous pole of the heart Smarcd3 Baf60C Nkx2-5 MyoD Myogenesis Mef2c Sema3c Hox genes Nodal signalling Pitx2 Shh Actin Skeletal muscle 

Notes

Acknowledgements

MB acknowledges support from the Pasteur Institute and the CNRS (URA 2578). She thanks Robert G. Kelly for comments on the text.

References

  1. 1.
    Bruneau BG (2008) The developmental genetics of congenital heart disease. Nature 451:943–948PubMedCrossRefGoogle Scholar
  2. 2.
    Buckingham M, Meilhac S, Zaffran S (2005) Building the mammalian heart from two sources of myocardial cells. Nat Rev Genet 6:826–835PubMedCrossRefGoogle Scholar
  3. 3.
    Christoffels VM, Habets PE, Franco D et al (2000) Chamber formation and morphogenesis in the developing mammalian heart. Dev Biol 223:266–278, Erratum in: Dev Biol 225:266PubMedCrossRefGoogle Scholar
  4. 4.
    Brand T (2003) Heart development: molecular insights into cardiac specification and early morphogenesis. Dev Biol 258:1–19PubMedCrossRefGoogle Scholar
  5. 5.
    Mjaatvedt CH, Nakaoka T, Moreno-Rodriguez R et al (2001) The outflow tract of the heart is recruited from a novel heart-forming field. Dev Biol 238:97–109PubMedCrossRefGoogle Scholar
  6. 6.
    Waldo KL, Kumiski DH, Wallis KT et al (2001) Conotruncal myocardium arises from a secondary heart field. Development 128:3179–3188PubMedGoogle Scholar
  7. 7.
    Kelly RG, Brown NA, Buckingham ME (2001) The arterial pole of the mouse heart forms from Fgf10-expressing cells in pharyngeal mesoderm. Dev Cell 1:435–440PubMedCrossRefGoogle Scholar
  8. 8.
    Cai CL, Liang X, Shi Y et al (2003) Isl1 identifies a cardiac progenitor population that proliferates prior to differentiation and contributes a majority of cells to the heart. Dev Cell 5:877–889PubMedCrossRefGoogle Scholar
  9. 9.
    Galli D, Domínguez JN, Zaffran S et al (2008) Atrial myocardium derives from the posterior region of the second heart field, which acquires left-right identity as Pitx2c is expressed. Development 135:1157–1167PubMedCrossRefGoogle Scholar
  10. 10.
    Zaffran S, Kelly RG, Meilhac SM et al (2004) Right ventricular myocardium derives from the anterior heart field. Circ Res 95:261–268PubMedCrossRefGoogle Scholar
  11. 11.
    Meilhac SM, Esner M, Kelly RG et al (2004) The clonal origin of myocardial cells in different regions of the embryonic mouse heart. Dev Cell 6:685–698PubMedCrossRefGoogle Scholar
  12. 12.
    Lescroart F, Chabab S, Lin X et al (2014) Early lineage restriction in temporally distinct populations of Mesp1 progenitors during mammalian heart development. Nat Cell Biol 16:829–840PubMedCrossRefGoogle Scholar
  13. 13.
    Saga Y, Miyagawa-Tomita S, Takagi A et al (1999) MesP1 is expressed in the heart precursor cells and required for the formation of a single heart tube. Development 126:3437–3447PubMedGoogle Scholar
  14. 14.
    Devine WP, Wythe JD, George M et al (2014) Early patterning and specification of cardiac progenitors in gastrulating mesoderm. Elife. doi: 10.7554/eLife.03848
  15. 15.
    Bruneau BG, Nemer G, Schmitt JP et al (2001) A murine model of Holt-Oram syndrome defines roles of the T-box transcription factor Tbx5 in cardiogenesis and disease. Cell 106:709–721PubMedCrossRefGoogle Scholar
  16. 16.
    Rana MS, Théveniau-Ruissy M, De Bono C et al (2014) Tbx1 coordinates addition of posterior second heart field progenitor cells to the arterial and venous poles of the heart. Circ Res 115:790–799PubMedCrossRefGoogle Scholar
  17. 17.
    Liang X, Wang G, Lin L et al (2013) HCN4 dynamically marks the first heart field and conduction system precursors. Circ Res 113:399–407PubMedCentralPubMedCrossRefGoogle Scholar
  18. 18.
    Vincent SD, Buckingham ME (2010) How to make a heart: the origin and regulation of cardiac progenitor cells. Curr Top Dev Biol 90:1–41PubMedCrossRefGoogle Scholar
  19. 19.
    Bajolle F, Zaffran S, Losay J et al (2009) Conotruncal defects associated with anomalous pulmonary venous connections. Arch Cardiovasc Dis 102:105–110PubMedCrossRefGoogle Scholar
  20. 20.
    Hutson MR, Zeng XL, Kim AJ et al (2010) Arterial pole progenitors interpret opposing FGF/BMP signals to proliferate or differentiate. Development 137:3001–3011PubMedCentralPubMedCrossRefGoogle Scholar
  21. 21.
    Tirosh-Finkel L, Zeisel A, Brodt-Ivenshitz M et al (2010) BMP-mediated inhibition of FGF signaling promotes cardiomyocyte differentiation of anterior heart field progenitors. Development 137:2989–3000PubMedCrossRefGoogle Scholar
  22. 22.
    Xie L, Hoffmann AD, Burnicka-Turek O et al (2012) Tbx5-hedgehog molecular networks are essential in the second heart field for atrial septation. Dev Cell 23:280–291PubMedCentralPubMedCrossRefGoogle Scholar
  23. 23.
    Briggs LE, Kakarla J, Wessels A (2012) The pathogenesis of atrial and atrioventricular septal defects with special emphasis on the role of the dorsal mesenchymal protrusion. Differentiation 84:117–130PubMedCentralPubMedCrossRefGoogle Scholar
  24. 24.
    Kelly RG (2012) The second heart field. Curr Top Dev Biol 100:33–65PubMedCrossRefGoogle Scholar
  25. 25.
    Chen L, Fulcoli FG, Tang S et al (2009) Tbx1 regulates proliferation and differentiation of multipotent heart progenitors. Circ Res 105:842–851PubMedCentralPubMedCrossRefGoogle Scholar
  26. 26.
    Watanabe Y, Zaffran S, Kuroiwa A et al (2012) Fibroblast growth factor 10 gene regulation in the second heart field by Tbx1, Nkx2-5, and Islet1 reveals a genetic switch for down-regulation in the myocardium. Proc Natl Acad Sci U S A 109:18273–18280PubMedCentralPubMedCrossRefGoogle Scholar
  27. 27.
    Takeuchi JK, Bruneau BG (2009) Directed transdifferentiation of mouse mesoderm to heart tissue by defined factors. Nature 459:708–711PubMedCentralPubMedCrossRefGoogle Scholar
  28. 28.
    Prall OWJ, Menon MK, Solloway MJ et al (2007) An Nkx2-5/Bmp2/Smad1 negative feedback loop controls heart progenitor specification and proliferation. Cell 128:947–959PubMedCentralPubMedCrossRefGoogle Scholar
  29. 29.
    Buckingham M, Rigby PW (2014) Gene regulatory networks and transcriptional mechanisms that control myogenesis. Dev Cell 28:225–238PubMedCrossRefGoogle Scholar
  30. 30.
    Dodou E, Verzi MP, Anderson JP et al (2004) Mef2c is a direct transcriptional target of ISL1 and GATA factors in the anterior heart field during mouse embryonic development. Development 131:3931–3942PubMedCrossRefGoogle Scholar
  31. 31.
    Papangeli I, Scambler P (2013) The 22q11 deletion: DiGeorge and velocardiofacial syndromes and the role of TBX1. Wiley Interdiscip Rev Dev Biol 2:393–403PubMedCrossRefGoogle Scholar
  32. 32.
    Bertrand N, Roux M, Ryckebüsch L et al (2011) Hox genes define distinct progenitor sub-domains within the second heart field. Dev Biol 353:266–274PubMedCentralPubMedCrossRefGoogle Scholar
  33. 33.
    Briggs LE, Phelps AL, Brown E et al (2013) Expression of the BMP receptor Alk3 in the second heart field is essential for development of the dorsal mesenchymal protrusion and atrioventricular septation. Circ Res 112:1420–1432PubMedCrossRefGoogle Scholar
  34. 34.
    Christoffels VM, Mommersteeg MT, Trowe MO et al (2006) Formation of the venous pole of the heart from an Nkx2-5-negative precursor population requires Tbx18. Circ Res 98:1555–1563PubMedCrossRefGoogle Scholar
  35. 35.
    Lescroart F, Mohun T, Meilhac SM et al (2012) A lineage tree for the venous pole of the heart: clonal analysis clarifies controversial genealogy based on genetic tracing. Circ Res 111:1313–1322PubMedCrossRefGoogle Scholar
  36. 36.
    Domínguez JN, Meilhac SM, Bland YS et al (2012) Asymmetric fate of the posterior part of the second heart field results in unexpected left/right contributions to both poles of the heart. Circ Res 111:1323–1335PubMedCrossRefGoogle Scholar
  37. 37.
    Huynh T, Chen L, Terrell P et al (2007) A fate map of Tbx1 expressing cells reveals heterogeneity in the second cardiac field. Genesis 45:470–475PubMedCrossRefGoogle Scholar
  38. 38.
    Mommersteeg MT, Brown NA, Prall OW et al (2007) Pitx2c and Nkx2-5 are required for the formation and identity of the pulmonary myocardium. Circ Res 101:902–909PubMedCrossRefGoogle Scholar
  39. 39.
    von Both I, Silvestri C, Erdemir T et al (2004) Foxh1 is essential for development of the anterior heart field. Dev Cell 7:331–345CrossRefGoogle Scholar
  40. 40.
    Roessler E, Ouspenskaia MV, Karkera JD et al (2008) Reduced NODAL signaling strength via mutation of several pathway members including FOXH1 is linked to human heart defects and holoprosencephaly. Am J Hum Genet 83:18–29PubMedCentralPubMedCrossRefGoogle Scholar
  41. 41.
    Washington Smoak I, Byrd NA, Abu-Issa R et al (2005) Sonic hedgehog is required for cardiac outflow tract and neural crest cell development. Dev Biol 283:357–372PubMedCrossRefGoogle Scholar
  42. 42.
    Hildreth V, Webb S, Chaudhry B et al (2009) Left cardiac isomerism in the Sonic hedgehog null mouse. J Anat 214:894–904PubMedCentralPubMedCrossRefGoogle Scholar
  43. 43.
    Milgrom-Hoffman M, Harrelson Z, Ferrara N et al (2011) The heart endocardium is derived from vascular endothelial progenitors. Development 138:4777–4787PubMedCentralPubMedCrossRefGoogle Scholar
  44. 44.
    Watanabe Y, Miyagawa-Tomita S, Vincent SD et al (2010) Role of mesodermal FGF8 and FGF10 overlaps in the development of the arterial pole of the heart and pharyngeal arch arteries. Circ Res 106:495–503PubMedCentralPubMedCrossRefGoogle Scholar
  45. 45.
    Vincent SD, Mayeuf-Louchart A, Watanabe Y et al (2014) Prdm1 functions in the mesoderm of the second heart field, where it interacts genetically with Tbx1, during outflow tract morphogenesis in the mouse embryo. Hum Mol Genet 23:5087–5101PubMedCrossRefGoogle Scholar
  46. 46.
    Moretti A, Caron L, Nakano A et al (2006) Multipotent embryonic isl1+ progenitor cells lead to cardiac, smooth muscle, and endothelial cell diversification. Cell 127:1151–1165PubMedCrossRefGoogle Scholar
  47. 47.
    Grifone R, Jarry T, Dandonneau M et al (2008) Properties of branchiomeric and somite-derived muscle development in Tbx1 mutant embryos. Dev Dyn 237:3071–3078PubMedCrossRefGoogle Scholar
  48. 48.
    Nathan E, Monovich A, Tirosh-Finkel L et al (2008) The contribution of Islet1-expressing splanchnic mesoderm cells to distinct branchiomeric muscles reveals significant heterogeneity in head muscle development. Development 135:647–657PubMedCrossRefGoogle Scholar
  49. 49.
    Lescroart F, Kelly RG, Le Garrec JF et al (2010) Clonal analysis reveals common lineage relationships between head muscles and second heart field derivatives in the mouse embryo. Development 137:3269–3279PubMedCrossRefGoogle Scholar
  50. 50.
    Theis S, Patel K, Valasek P et al (2010) The occipital lateral plate mesoderm is a novel source for vertebrate neck musculature. Development 137:2961–2971PubMedCrossRefGoogle Scholar
  51. 51.
    Lescroart F, Hamou W, Francou A et al (2015) Clonal analysis reveals a common origin between non-somitic derived neck muscles and heart myocardium. Proc Natl Acad Sci U S A 112:1446–1451PubMedCentralPubMedCrossRefGoogle Scholar
  52. 52.
    Wang W, Razy-Krajka F, Siu E et al (2013) NK4 antagonizes Tbx1/10 to promote cardiac versus pharyngeal muscle fate in the ascidian second heart field. PLoS Biol 11, e1001725PubMedCentralPubMedCrossRefGoogle Scholar
  53. 53.
    Diogo R, Kelly RG, Christiaen L et al (2015) The cardiopharyngeal field and vertebrate evolution: a new heart for a new head. Nature 520:466–473PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Wien 2016

Authors and Affiliations

  1. 1.Department of Developmental and Stem Cell BiologyInstitut PasteurParisFrance

Personalised recommendations