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Planar Cell Polarity Signaling in Mammalian Cardiac Morphogenesis

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Abstract

The mammalian heart is the first organ to form and is critical for embryonic survival and development. With an occurrence of 1%, congenital heart defects (CHDs) are also the most common birth defects in humans, and major cause of childhood morbidity and mortality (Hoffman and Kaplan in J Am Coll Cardiol 39(12):1890–1900, 2002; Samanek in Cardiol Young 10(3):179–185, 2000). Understanding how the heart forms will not only help to determine the etiology and to design diagnostic and therapeutic approaches for CHDs, but may also provide insight into regenerative medicine to repair injured adult hearts. Mammalian heart development requires precise orchestration of growth, differentiation, and morphogenesis to remodel a simple linear heart tube into an intricate, four-chambered heart with properly connected pulmonary artery and aorta, a structural basis for establishing the pulmonary and systemic circulation. Here we will review the recent advance in our understanding of how the planar cell polarity pathway, a highly conserved morphogenetic engine in vertebrates, regulates polarized morphogenetic processes to contribute to both the arterial and venous poles development of the heart.

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References

  1. Harvey RP (2002) Patterning the vertebrate heart. Nat Rev Genet 3(7):544–556. https://doi.org/10.1038/nrg843.

    Article  PubMed  CAS  Google Scholar 

  2. Cai CL, Liang X, Shi Y, Chu PH, Pfaff SL, Chen J 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(6):877–889

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  3. Dyer LA, Kirby ML (2009) The role of secondary heart field in cardiac development. Dev Biol 336(2):137–144

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  4. Evans SM, Yelon D, Conlon FL, Kirby ML (2010) Myocardial lineage development. Circ Res 107(12):1428–1444. https://doi.org/10.1161/CIRCRESAHA.110.227405

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  5. 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(3):435–440

    Article  PubMed  CAS  Google Scholar 

  6. Verzi MP, McCulley DJ, De Val S, Dodou E, Black BL (2005) The right ventricle, outflow tract, and ventricular septum comprise a restricted expression domain within the secondary/anterior heart field. Dev Biol 287(1):134–145

    Article  PubMed  CAS  Google Scholar 

  7. Vincent SD, Buckingham ME (2010) How to make a heart: the origin and regulation of cardiac progenitor cells. Curr Top Dev Biol 90:1–41. https://doi.org/10.1016/S0070-2153(10)90001-X.

    Article  PubMed  Google Scholar 

  8. Snarr BS, O’Neal JL, Chintalapudi MR, Wirrig EE, Phelps AL, Kubalak SW et al (2007) Isl1 expression at the venous pole identifies a novel role for the second heart field in cardiac development. Circ Res 101(10):971–974. https://doi.org/10.1161/CIRCRESAHA.107.162206.

    Article  PubMed  CAS  Google Scholar 

  9. Briggs LE, Phelps AL, Brown E, Kakarla J, Anderson RH, van den Hoff MJ 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(11):1420–1432. https://doi.org/10.1161/CIRCRESAHA.112.300821.

    Article  PubMed  CAS  Google Scholar 

  10. Lawrence PA, Casal J, Struhl G (2004) Cell interactions and planar polarity in the abdominal epidermis of Drosophila. Development 131(19):4651–4664

    Article  PubMed  CAS  Google Scholar 

  11. Seifert JR, Mlodzik M (2007) Frizzled/PCP signalling: a conserved mechanism regulating cell polarity and directed motility. Nat Rev Genet 8(2):126–138. https://doi.org/10.1038/nrg2042.

    Article  PubMed  CAS  Google Scholar 

  12. Bayly R, Axelrod JD (2011) Pointing in the right direction: new developments in the field of planar cell polarity. Nat Rev Genet 12(6):385–391

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  13. Strutt H, Strutt D (2009) Asymmetric localisation of planar polarity proteins: mechanisms and consequences. Semin Cell Dev Biol 20(8):957–963

    Article  PubMed  CAS  Google Scholar 

  14. Zallen JA (2007) Planar polarity and tissue morphogenesis. Cell 129(6):1051–1063. https://doi.org/10.1016/j.cell.2007.05.050.

    Article  PubMed  CAS  Google Scholar 

  15. Hashimoto M, Shinohara K, Wang J, Ikeuchi S, Yoshiba S, Meno C et al (2010) Planar polarization of node cells determines the rotational axis of node cilia. Nat Cell Biol 12(2):170–176. https://doi.org/10.1038/ncb2020.

    Article  PubMed  CAS  Google Scholar 

  16. Wang J, Mark S, Zhang X, Qian D, Yoo SJ, Radde-Gallwitz K et al (2005) Regulation of polarized extension and planar cell polarity in the cochlea by the vertebrate PCP pathway. Nat Genet 37(9):980–985

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  17. Devenport D (2014) The cell biology of planar cell polarity. J Cell Biol 207(2):171–179. https://doi.org/10.1083/jcb.201408039.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  18. Devenport D, Fuchs E (2008) Planar polarization in embryonic epidermis orchestrates global asymmetric morphogenesis of hair follicles. Nat Cell Biol 10(11):1257–1268. https://doi.org/10.1038/ncb1784.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  19. Chang H, Smallwood PM, Williams J, Nathans J (2016) The spatio-temporal domains of Frizzled6 action in planar polarity control of hair follicle orientation. Dev Biol 409(1):181–193. https://doi.org/10.1016/j.ydbio.2015.10.027.

    Article  PubMed  CAS  Google Scholar 

  20. He X, Semenov M, Tamai K, Zeng X (2004) LDL receptor-related proteins 5 and 6 in Wnt/beta-catenin signaling: arrows point the way. Development 131(8):1663–1677

    Article  PubMed  CAS  Google Scholar 

  21. Logan CY, Nusse R (2004) The Wnt signaling pathway in development and disease. Annu Rev Cell Dev Biol 20:781–810

    Article  PubMed  CAS  Google Scholar 

  22. Wallingford JB, Habas R (2005) The developmental biology of Dishevelled: an enigmatic protein governing cell fate and cell polarity. Development 132(20):4421–4436

    Article  PubMed  CAS  Google Scholar 

  23. Zerlin M, Julius MA, Kitajewski J (2008) Wnt/Frizzled signaling in angiogenesis. Angiogenesis 11(1):63–69

    Article  PubMed  CAS  Google Scholar 

  24. Heisenberg CP, Tada M, Rauch GJ, Saude L, Concha ML, Geisler R et al (2000) Silberblick/Wnt11 mediates convergent extension movements during zebrafish gastrulation. Nature 405(6782):76–81

    Article  PubMed  CAS  Google Scholar 

  25. Jessen JR, Topczewski J, Bingham S, Sepich DS, Marlow F, Chandrasekhar A et al (2002) Zebrafish trilobite identifies new roles for Strabismus in gastrulation and neuronal movements. Nat Cell Biol 4(8):610–615

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  26. Keller R (2002) Shaping the vertebrate body plan by polarized embryonic cell movements. Science 298(5600):1950–1954

    Article  PubMed  CAS  Google Scholar 

  27. Yin C, Kiskowski M, Pouille PA, Farge E, Solnica-Krezel L (2008) Cooperation of polarized cell intercalations drives convergence and extension of presomitic mesoderm during zebrafish gastrulation. J Cell Biol 180(1):221–232

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  28. Gong Y, Mo C, Fraser SE (2004) Planar cell polarity signalling controls cell division orientation during zebrafish gastrulation. Nature 430(7000):689–693. https://doi.org/10.1038/nature02796.

    Article  PubMed  CAS  Google Scholar 

  29. Wallingford JB, Rowning BA, Vogeli KM, Rothbacher U, Fraser SE, Harland RM (2000) Dishevelled controls cell polarity during Xenopus gastrulation. Nature 405(6782):81–85. https://doi.org/10.1038/35011077.

    Article  PubMed  CAS  Google Scholar 

  30. Vladar EK, Antic D, Axelrod JD (2009) Planar cell polarity signaling: the developing cell’s compass. Cold Spring Harb Perspect Biol 1(3):a002964. https://doi.org/10.1101/cshperspect.a002964.

    Article  PubMed  PubMed Central  Google Scholar 

  31. Goodrich LV, Strutt D (2011) Principles of planar polarity in animal development. Development 138(10):1877–1892. https://doi.org/10.1242/dev.054080.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  32. Wang J, Sinha T, Wynshaw-Boris A. Wnt signaling in mammalian development: lessons from mouse genetics. Cold Spring Harb Perspect Biol. 2012;4(5). https://doi.org/10.1101/cshperspect.a007963.

  33. Matsuyama M, Aizawa S, Shimono A (2009) Sfrp controls apicobasal polarity and oriented cell division in developing gut epithelium. PLoS Genet 5(3):e1000427

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  34. Curtin JA, Quint E, Tsipouri V, Arkell RM, Cattanach B, Copp AJ et al (2003) Mutation of Celsr1 disrupts planar polarity of inner ear hair cells and causes severe neural tube defects in the mouse. Curr Biol 13(13):1129–1133

    Article  PubMed  CAS  Google Scholar 

  35. Etheridge SL, Ray S, Li S, Hamblet NS, Lijam N, Tsang M et al (2008) Murine dishevelled 3 functions in redundant pathways with dishevelled 1 and 2 in normal cardiac outflow tract, cochlea, and neural tube development. PLoS Genet 4(11):e1000259. https://doi.org/10.1371/journal.pgen.1000259.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  36. Kibar Z, Vogan KJ, Groulx N, Justice MJ, Underhill DA, Gros P (2001) Ltap, a mammalian homolog of Drosophila Strabismus/Van Gogh, is altered in the mouse neural tube mutant Loop-tail. Nat Genet 28(3):251–255

    Article  PubMed  CAS  Google Scholar 

  37. Murdoch JN, Doudney K, Paternotte C, Copp AJ, Stanier P (2001) Severe neural tube defects in the loop-tail mouse result from mutation of Lpp1, a novel gene involved in floor plate specification. Hum Mol Genet 10(22):2593–2601

    Article  PubMed  CAS  Google Scholar 

  38. Wang J, Hamblet NS, Mark S, Dickinson ME, Brinkman BC, Segil N et al (2006) Dishevelled genes mediate a conserved mammalian PCP pathway to regulate convergent extension during neurulation. Development 133(9):1767–1778

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  39. Wang Y, Guo N, Nathans J (2006) The role of Frizzled3 and Frizzled6 in neural tube closure and in the planar polarity of inner-ear sensory hair cells. J Neurosci 26(8):2147–2156

    Article  PubMed  CAS  Google Scholar 

  40. Torban E, Patenaude AM, Leclerc S, Rakowiecki S, Gauthier S, Andelfinger G et al (2008) Genetic interaction between members of the Vangl family causes neural tube defects in mice. Proc Natl Acad Sci USA 105(9):3449–3454. https://doi.org/10.1073/pnas.0712126105

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  41. Lu X, Borchers AG, Jolicoeur C, Rayburn H, Baker JC, Tessier-Lavigne M (2004) PTK7/CCK-4 is a novel regulator of planar cell polarity in vertebrates. Nature 430(6995):93–98

    Article  PubMed  CAS  Google Scholar 

  42. Gao B, Song H, Bishop K, Elliot G, Garrett L, English MA et al (2011) Wnt signaling gradients establish planar cell polarity by inducing Vangl2 phosphorylation through Ror2. Developmental cell 20(2):163–176. https://doi.org/10.1016/j.devcel.2011.01.001.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  43. Qian D, Jones C, Rzadzinska A, Mark S, Zhang X, Steel KP et al. (2007) Wnt5a functions in planar cell polarity regulation in mice. Dev Biol 306(1):121–133. https://doi.org/10.1016/j.ydbio.2007.03.011.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  44. Savory JG, Mansfield M, Rijli FM, Lohnes D (2011) Cdx mediates neural tube closure through transcriptional regulation of the planar cell polarity gene Ptk7. Development 138(7):1361–1370

    Article  PubMed  CAS  Google Scholar 

  45. Wang B, Sinha T, Jiao K, Serra R, Wang J (2011) Disruption of PCP signaling causes limb morphogenesis and skeletal defects and may underlie Robinow syndrome and brachydactyly type B. Hum Mol Genet 20(2):271–285. https://doi.org/10.1093/hmg/ddq462.

    Article  PubMed  CAS  Google Scholar 

  46. Gros J, Hu JK, Vinegoni C, Feruglio PF, Weissleder R, Tabin CJ (2010) WNT5A/JNK and FGF/MAPK pathways regulate the cellular events shaping the vertebrate limb bud. Curr Biol: CB 20(22):1993–2002. https://doi.org/10.1016/j.cub.2010.09.063.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  47. Habas R, Kato Y, He X (2001) Wnt/Frizzled activation of Rho regulates vertebrate gastrulation and requires a novel Formin homology protein Daam1. Cell 107(7):843–854

    Article  PubMed  CAS  Google Scholar 

  48. Liu W, Sato A, Khadka D, Bharti R, Diaz H, Runnels LW et al (2008) Mechanism of activation of the Formin protein Daam1. Proc Natl Acad Sci USA 105(1):210–215. https://doi.org/10.1073/pnas.0707277105.

    Article  PubMed  Google Scholar 

  49. Habas R, Dawid IB, He X (2003) Coactivation of Rac and Rho by Wnt/Frizzled signaling is required for vertebrate gastrulation. Genes Dev 17(2):295–309

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  50. Tanegashima K, Zhao H, Dawid IB (2008) WGEF activates Rho in the Wnt-PCP pathway and controls convergent extension in Xenopus gastrulation. Embo J 27(4):606–617

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  51. Matusek T, Djiane A, Jankovics F, Brunner D, Mlodzik M, Mihaly J (2006) The Drosophila formin DAAM regulates the tracheal cuticle pattern through organizing the actin cytoskeleton. Development 133(5):957–966. https://doi.org/10.1242/dev.02266

    Article  PubMed  CAS  Google Scholar 

  52. Kilian B, Mansukoski H, Barbosa FC, Ulrich F, Tada M, Heisenberg CP (2003) The role of Ppt/Wnt5 in regulating cell shape and movement during zebrafish gastrulation. Mech Dev 120(4):467–476

    Article  PubMed  CAS  Google Scholar 

  53. Wallingford JB, Vogeli KM, Harland RM (2001) Regulation of convergent extension in Xenopus by Wnt5a and Frizzled-8 is independent of the canonical Wnt pathway. Int J Dev Biol 45(1):225–227

    PubMed  CAS  Google Scholar 

  54. Chen WS, Antic D, Matis M, Logan CY, Povelones M, Anderson GA et al (2008) Asymmetric homotypic interactions of the atypical cadherin flamingo mediate intercellular polarity signaling. Cell 133(6):1093–1105. https://doi.org/10.1016/j.cell.2008.04.048

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  55. Wu J, Roman AC, Carvajal-Gonzalez JM, Mlodzik M. Wg (2013) and Wnt4 provide long-range directional input to planar cell polarity orientation in Drosophila. Nat Cell Biol 15(9):1045–1055. https://doi.org/10.1038/ncb2806

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  56. Amonlirdviman K, Khare NA, Tree DR, Chen WS, Axelrod JD, Tomlin CJ (2005) Mathematical modeling of planar cell polarity to understand domineering nonautonomy. Science 307(5708):423–426. https://doi.org/10.1126/science.1105471.

    Article  PubMed  CAS  Google Scholar 

  57. Wu J, Mlodzik M (2008) The frizzled extracellular domain is a ligand for Van Gogh/Stbm during nonautonomous planar cell polarity signaling. Dev Cell 15(3):462–469. https://doi.org/10.1016/j.devcel.2008.08.004.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  58. Tree DR, Shulman JM, Rousset R, Scott MP, Gubb D, Axelrod JD (2002) Prickle mediates feedback amplification to generate asymmetric planar cell polarity signaling. Cell 109(3):371–381

    Article  PubMed  CAS  Google Scholar 

  59. Yu H, Smallwood PM, Wang Y, Vidaltamayo R, Reed R, Nathans J (2010) Frizzled 1 and frizzled 2 genes function in palate, ventricular septum and neural tube closure: general implications for tissue fusion processes. Development 137(21):3707–3717. https://doi.org/10.1242/dev.052001.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  60. Seo HS, Habas R, Chang C, Wang J (2017) Bimodal regulation of Dishevelled function by Vangl2 during morphogenesis. Hum Mol Genet 26(11):2053–2061. https://doi.org/10.1093/hmg/ddx095.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  61. Schleiffarth JR, Person AD, Martinsen BJ, Sukovich DJ, Neumann A, Baker CV et al (2007) Wnt5a is required for cardiac outflow tract septation in mice. Pediatr Res 61(4):386–391. https://doi.org/10.1203/pdr.0b013e3180323810.

    Article  PubMed  Google Scholar 

  62. Zhou W, Lin L, Majumdar A, Li X, Zhang X, Liu W et al (2007) Modulation of morphogenesis by noncanonical Wnt signaling requires ATF/CREB family-mediated transcriptional activation of TGFbeta2. Nat Genet 39(10):1225–1234. https://doi.org/10.1038/ng2112

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  63. van Vliet PP, Lin L, Boogerd CJ, Martin JF, Andelfinger G, Grossfeld PD et al (2017) Tissue specific requirements for WNT11 in developing outflow tract and dorsal mesenchymal protrusion. Dev Biol 429(1):249–259. https://doi.org/10.1016/j.ydbio.2017.06.021.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  64. Hamblet NS, Lijam N, Ruiz-Lozano P, Wang J, Yang Y, Luo Z et al (2002) Dishevelled 2 is essential for cardiac outflow tract development, somite segmentation and neural tube closure. Development 129(24):5827–5838

    Article  PubMed  CAS  Google Scholar 

  65. Sinha T, Wang B, Evans S, Wynshaw-Boris A, Wang J (2012) Disheveled mediated planar cell polarity signaling is required in the second heart field lineage for outflow tract morphogenesis. Dev Biol 370(1):135–144. https://doi.org/10.1016/j.ydbio.2012.07.023

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  66. Yu H, Ye X, Guo N, Nathans J (2012) Frizzled 2 and frizzled 7 function redundantly in convergent extension and closure of the ventricular septum and palate: evidence for a network of interacting genes. Development 139(23):4383–4394. https://doi.org/10.1242/dev.083352

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  67. Henderson DJ, Conway SJ, Greene ND, Gerrelli D, Murdoch JN, Anderson RH et al (2001) Cardiovascular defects associated with abnormalities in midline development in the Loop-tail mouse mutant. Circ Res 89(1):6–12

    Article  PubMed  CAS  Google Scholar 

  68. Capelluto DG, Kutateladze TG, Habas R, Finkielstein CV, He X, Overduin M (2002) The DIX domain targets dishevelled to actin stress fibres and vesicular membranes. Nature 419(6908):726–729

    Article  PubMed  CAS  Google Scholar 

  69. Rothbacher U, Laurent MN, Deardorff MA, Klein PS, Cho KW, Fraser SE (2000) Dishevelled phosphorylation, subcellular localization and multimerization regulate its role in early embryogenesis. Embo J 19(5):1010–1022

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  70. Axelrod JD, Miller JR, Shulman JM, Moon RT, Perrimon N (1998) Differential recruitment of Dishevelled provides signaling specificity in the planar cell polarity and Wingless signaling pathways. Genes Dev 12(16):2610–2622

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  71. Boutros M, Paricio N, Strutt DI, Mlodzik M (1998) Dishevelled activates JNK and discriminates between JNK pathways in planar polarity and wingless signaling. Cell 94(1):109–118

    Article  PubMed  CAS  Google Scholar 

  72. Ramsbottom SA, Sharma V, Rhee HJ, Eley L, Phillips HM, Rigby HF et al (2014) Vangl2-regulated polarisation of second heart field-derived cells is required for outflow tract lengthening during cardiac development. PLoS Genet 10(12):e1004871. https://doi.org/10.1371/journal.pgen.1004871.

    Article  PubMed  PubMed Central  Google Scholar 

  73. Ai D, Fu X, Wang J, Lu MF, Chen L, Baldini A et al (2007) Canonical Wnt signaling functions in second heart field to promote right ventricular growth. Proc Natl Acad Sci USA 104(22):9319–9324

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  74. Cohen ED, Wang Z, Lepore JJ, Lu MM, Taketo MM, Epstein DJ et al (2007) Wnt/beta-catenin signaling promotes expansion of Isl-1-positive cardiac progenitor cells through regulation of FGF signaling. J Clin Investig 117(7):1794–1804

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  75. Lin L, Cui L, Zhou W, Dufort D, Zhang X, Cai CL et al (2007) Beta-catenin directly regulates Islet1 expression in cardiovascular progenitors and is required for multiple aspects of cardiogenesis. Proc Natl Acad Sci USA 104(22):9313–9318

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  76. Kwon C, Arnold J, Hsiao EC, Taketo MM, Conklin BR, Srivastava D (2007) Canonical Wnt signaling is a positive regulator of mammalian cardiac progenitors. Proc Natl Acad Sci USA 104(26):10894–10899. https://doi.org/10.1073/pnas.0704044104.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  77. Sinha T, Li D, Theveniau-Ruissy M, Hutson MR, Kelly RG, Wang J (2015) Loss of Wnt5a disrupts second heart field cell deployment and may contribute to OFT malformations in DiGeorge syndrome. Hum Mol Genet 24(6):1704–1716. https://doi.org/10.1093/hmg/ddu584.

    Article  PubMed  CAS  Google Scholar 

  78. van den Berg G, Abu-Issa R, de Boer BA, Hutson MR, de Boer PA, Soufan AT et al (2009) A caudal proliferating growth center contributes to both poles of the forming heart tube. Circ Res 104(2):179–188. https://doi.org/10.1161/CIRCRESAHA.108.185843.

    Article  PubMed  CAS  Google Scholar 

  79. Li D, Sinha T, Ajima R, Seo HS, Yamaguchi TP, Wang J (2016) Spatial regulation of cell cohesion by Wnt5a during second heart field progenitor deployment. Dev Biol 412(1):18–31. https://doi.org/10.1016/j.ydbio.2016.02.017.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  80. Waldo KL, Hutson MR, Ward CC, Zdanowicz M, Stadt HA, Kumiski D et al (2005) Secondary heart field contributes myocardium and smooth muscle to the arterial pole of the developing heart. Dev Biol 281(1):78–90. https://doi.org/10.1016/j.ydbio.2005.02.012

    Article  PubMed  CAS  Google Scholar 

  81. Francou A, Saint-Michel E, Mesbah K, Kelly RG (2014) TBX1 regulates epithelial polarity and dynamic basal filopodia in the second heart field. Development 141(22):4320–4331. https://doi.org/10.1242/dev.115022

    Article  PubMed  CAS  Google Scholar 

  82. Theveniau-Ruissy M, Dandonneau M, Mesbah K, Ghez O, Mattei MG, Miquerol L et al (2008) The del22q11.2 candidate gene Tbx1 controls regional outflow tract identity and coronary artery patterning. Circ Res 103(2):142–148. https://doi.org/10.1161/CIRCRESAHA.108.172189

    Article  PubMed  CAS  Google Scholar 

  83. Kelly RG, Papaioannou VE (2007) Visualization of outflow tract development in the absence of Tbx1 using an FgF10 enhancer trap transgene. Dev Dyn 236(3):821–828. https://doi.org/10.1002/dvdy.21063.

    Article  PubMed  CAS  Google Scholar 

  84. Kirby ML (2008) Pulmonary atresia or persistent truncus arteriosus: is it important to make the distinction and how do we do it? Circ Res 103(4):337–339

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  85. Chen L, Fulcoli FG, Ferrentino R, Martucciello S, Illingworth EA, Baldini A (2012) Transcriptional control in cardiac progenitors: Tbx1 interacts with the BAF chromatin remodeling complex and regulates Wnt5a. PLoS Genet 8(3):e1002571. https://doi.org/10.1371/journal.pgen.1002571

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  86. Madisen L, Zwingman TA, Sunkin SM, Oh SW, Zariwala HA, Gu H et al (2010) A robust and high-throughput Cre reporting and characterization system for the whole mouse brain. Nat Neurosci 13(1):133–140. https://doi.org/10.1038/nn.2467

    Article  PubMed  CAS  Google Scholar 

  87. Xie L, Hoffmann AD, Burnicka-Turek O, Friedland-Little JM, Zhang K, Moskowitz IP (2012) Tbx5-hedgehog molecular networks are essential in the second heart field for atrial septation. Dev Cell 23(2):280–291. https://doi.org/10.1016/j.devcel.2012.06.006.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  88. Goddeeris MM, Rho S, Petiet A, Davenport CL, Johnson GA, Meyers EN et al (2008) Intracardiac septation requires hedgehog-dependent cellular contributions from outside the heart. Development 135(10):1887–1895. https://doi.org/10.1242/dev.016147.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  89. Bertrand N, Roux M, Ryckebusch L, Niederreither K, Dolle P, Moon A et al (2011) Hox genes define distinct progenitor sub-domains within the second heart field. Dev Biol 353(2):266–274. https://doi.org/10.1016/j.ydbio.2011.02.029.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  90. Rochais F, Dandonneau M, Mesbah K, Jarry T, Mattei MG, Kelly RG (2009) Hes1 is expressed in the second heart field and is required for outflow tract development. PloS ONE 4(7):e6267. https://doi.org/10.1371/journal.pone.0006267.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  91. Zhou Z, Wang J, Guo C, Chang W, Zhuang J, Zhu P et al (2017) Temporally distinct Six2-positive second heart field progenitors regulate mammalian heart development and disease. Cell Rep 18(4):1019–1032. https://doi.org/10.1016/j.celrep.2017.01.002.

    Article  PubMed  CAS  Google Scholar 

  92. Yamaguchi TP, Bradley A, McMahon AP, Jones S (1999) A Wnt5a pathway underlies outgrowth of multiple structures in the vertebrate embryo. Development 126(6):1211–1223

    PubMed  CAS  Google Scholar 

  93. Ho HY, Susman MW, Bikoff JB, Ryu YK, Jonas AM, Hu L et al (2012) Wnt5a-Ror-Dishevelled signaling constitutes a core developmental pathway that controls tissue morphogenesis. Proc Natl Acad Sci USA 109(11):4044–4051. https://doi.org/10.1073/pnas.1200421109.

    Article  PubMed  PubMed Central  Google Scholar 

  94. Cohen ED, Miller MF, Wang Z, Moon RT, Morrisey EE (2012) Wnt5a and Wnt11 are essential for second heart field progenitor development. Development 139(11):1931–1940. https://doi.org/10.1242/dev.069377.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  95. Mikels AJ, Nusse R (2006) Purified Wnt5a protein activates or inhibits beta-catenin-TCF signaling depending on receptor context. PLoS Biol 4(4):e115. https://doi.org/10.1371/journal.pbio.0040115.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  96. Nemeth MJ, Topol L, Anderson SM, Yang Y, Bodine DM (2007) Wnt5a inhibits canonical Wnt signaling in hematopoietic stem cells and enhances repopulation. Proc Natl Acad Sci USA 104(39):15436–15441. https://doi.org/10.1073/pnas.0704747104.

    Article  PubMed  PubMed Central  Google Scholar 

  97. Topol L, Jiang X, Choi H, Garrett-Beal L, Carolan PJ, Yang Y (2003) Wnt-5a inhibits the canonical Wnt pathway by promoting GSK-3-independent beta-catenin degradation. J Cell Biol 162(5):899–908. https://doi.org/10.1083/jcb.200303158.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  98. Jaiswal R, Breitsprecher D, Collins A, Correa IR Jr, Xu MQ, Goode BL (2013) The formin Daam1 and fascin directly collaborate to promote filopodia formation. Curr Biol 23(14):1373–1379. https://doi.org/10.1016/j.cub.2013.06.013.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  99. Sato A, Khadka DK, Liu W, Bharti R, Runnels LW, Dawid IB et al (2006) Profilin is an effector for Daam1 in non-canonical Wnt signaling and is required for vertebrate gastrulation. Development 133(21):4219–4231

    Article  PubMed  CAS  Google Scholar 

  100. Radice GL, Rayburn H, Matsunami H, Knudsen KA, Takeichi M, Hynes RO (1997) Developmental defects in mouse embryos lacking N-cadherin. Dev Biol 181(1):64–78. https://doi.org/10.1006/dbio.1996.8443.

    Article  PubMed  CAS  Google Scholar 

  101. Linask KK (1992) 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. Dev Biol 151(1):213–224

    Article  PubMed  CAS  Google Scholar 

  102. Linask KK, Knudsen KA, Gui YH (1997) N-cadherin-catenin interaction: necessary component of cardiac cell compartmentalization during early vertebrate heart development. Dev Biol 185(2):148–164. https://doi.org/10.1006/dbio.1997.8570.

    Article  PubMed  CAS  Google Scholar 

  103. Soh BS, Buac K, Xu H, Li E, Ng SY, Wu H et al (2014) N-cadherin prevents the premature differentiation of anterior heart field progenitors in the pharyngeal mesodermal microenvironment. Cell Res 24(12):1420–1432. https://doi.org/10.1038/cr.2014.142

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  104. Li J, Gao E, Vite A, Yi R, Gomez L, Goossens S et al (2015) Alpha-catenins control cardiomyocyte proliferation by regulating Yap activity. Circ Res 116(1):70–79. https://doi.org/10.1161/CIRCRESAHA.116.304472

    Article  PubMed  CAS  Google Scholar 

  105. Li J, Miao L, Shieh D, Spiotto E, Li J, Zhou B et al (2016) Single-cell lineage tracing reveals that oriented cell division contributes to trabecular morphogenesis and regional specification. Cell Rep 15(1):158–170. https://doi.org/10.1016/j.celrep.2016.03.012.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  106. Merscher S, Funke B, Epstein JA, Heyer J, Puech A, Lu MM et al (2001) TBX1 is responsible for cardiovascular defects in velo-cardio-facial/DiGeorge syndrome. Cell 104(4):619–629

    Article  PubMed  CAS  Google Scholar 

  107. Jerome LA, Papaioannou VE (2001) DiGeorge syndrome phenotype in mice mutant for the T-box gene, Tbx1. Nature genetics 27(3):286–291. https://doi.org/10.1038/85845.

    Article  PubMed  CAS  Google Scholar 

  108. Hoffman JI, Kaplan S (2002) The incidence of congenital heart disease. J Am Coll Cardiol 39(12):1890–1900

    Article  PubMed  Google Scholar 

  109. Samanek M (2000) Congenital heart malformations: prevalence, severity, survival, and quality of life. Cardiol Young 10(3):179–185

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

We thank Dr. Deborah Henderson for helpful discussion and for the permission to adapt Fig. 8M in [72] the current publication.

Funding

This work was supported by Grants HL109130 and HL138470 from the National Institute of Health, and 14GRNT20380467 from the American Heart Association.

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  1. Department of Cell, Developmental and Integrative Biology, University of Alabama at Birmingham, Birmingham, AL, USA

    Ding Li & Jianbo Wang

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  1. Ding Li
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Correspondence to Jianbo Wang.

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Li, D., Wang, J. Planar Cell Polarity Signaling in Mammalian Cardiac Morphogenesis. Pediatr Cardiol 39, 1052–1062 (2018). https://doi.org/10.1007/s00246-018-1860-5

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