Vangl2-Regulated Polarisation of Second Heart Field-Derived Cells Is Required for Outflow Tract Lengthening during Cardiac Development

PLoS Genetics

Volumn 10, Issue 12, 2014, Pages

  Ramsbottom, Simon A ^a   Sharma, Vipul ^a   Rhee, Hong Jun ^a   Eley, Lorraine ^a   Phillips, Helen M ^a   Rigby, Hannah F ^a   Dean, Charlotte ^b,c   Chaudhry, Bill ^a   Henderson, Deborah J ^a  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

^b NATIONAL HEART AND LUNG INSTITUTE   (United Kingdom)

^c MRC MAMMALIAN GENETICS UNIT   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANIMAL TISSUE; AORTA; ARTICLE; CELL DIFFERENTIATION; CELL MOTILITY; CELLULAR PARAMETERS; CONTROLLED STUDY; DOWN REGULATION; EMBRYO; GENE; GENE FUNCTION; GENETIC REGULATION; HEART; HEART DEVELOPMENT; HEART MUSCLE CELL; HEART OUTFLOW TRACT; HEART VENTRICLE; MOUSE; NONHUMAN; PERICARDIUM; PHENOTYPE; PLANAR CELL POLARITY; PULMONARY ARTERY; SECOND HEART FIELD; SIGNAL TRANSDUCTION; STEM CELL; VANGL2 GENE; ANIMAL; C57BL MOUSE; CELL POLARITY; CYTOLOGY; EMBRYOLOGY; EMBRYONIC STEM CELL; EPITHELIUM; MORPHOGENESIS; PHYSIOLOGY; TRANSGENIC MOUSE;

LTAP PROTEIN, MOUSE; NERVE PROTEIN;

ANIMALS; CELL DIFFERENTIATION; CELL POLARITY; EMBRYONIC STEM CELLS; EPITHELIUM; HEART VENTRICLES; MICE, INBRED C57BL; MICE, TRANSGENIC; MORPHOGENESIS; NERVE TISSUE PROTEINS; PERICARDIUM; PHENOTYPE;

EID: 84919625941     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1004871     Document Type: Article

References (60)

1. Loscalzo ML, (2010) Left outflow tract anomalies in children. Curr Opin Pediatr 22: 593–597.
2. Sun Y, Liang X, Najafi N, Cass M, Lin L, et al. (2007) Islet 1 is expressed in distinct cardiovascular lineages, including pacemaker and coronary vascular cells. Dev Biol 304: 286–296.
3. Snarr BS, O'Neal JL, Chintalapudi MR, Wirrig EE, Phelps AL, et al. (2007) Isl1 expression at the venous pole identifies a novel role for the second heart field in cardiac development. Circ Res 101: 971–974.
4. 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: 435–440.
5. Cai CL, Liang X, Shi Y, Chu PH, Pfaff SL, 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: 877–889.
6. van den Berg G, Abu-Issa R, de Boer BA, Hutson MR, de Boer PA, et al. (2009) A caudal proliferating growth center contributes to both poles of the forming heart tube. Circ Res 104: 179–188.
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.
8. Stevens KN, Hakonarson H, Kim CE, Doevendans PA, Koeleman BP, et al. (2010) Common variation in ISL1 confers genetic susceptibility for human congenital heart disease. PLoS One 5: e10855.
9. Yagi H, Furutani Y, Hamada H, Sasaki T, Asakawa S, et al. (2003) Role of TBX1 in human del22q11.2 syndrome. Lancet 362: 1366–1373.
10. Chen L, Fulcoli FG, Tang S, Baldini A, (2009) Tbx1 regulates proliferation and differentiation of multipotent heart progenitors. Circ Res 105: 842–851.
11. Theveniau-Ruissy M, Dandonneau M, Mesbah K, Ghez O, Mattei MG, et al. (2008) The del22q11.2 candidate gene Tbx1 controls regional outflow tract identity and coronary artery patterning. Circ Res 103: 142–148.
12. Anderson RH, Brown NA, Mohun TJ, Moorman AF, (2013) Insights from cardiac development relevant to congenital defects and adult clinical anatomy. J Cardiovasc Transl Res 6: 107–117.
13. Phillips HM, Mahendra P, Singh E, Anderson RH, Chaudhry B, et al. (2013) Neural crest cells are required for correct positioning of the developing outflow cushions and pattern the arterial valve leaflets. Cardiovasc Res 99: 452–460.
14. Anderson RH, Chaudhry B, Mohun TJ, Bamforth SD, Hoyland D, et al. (2012) Normal and abnormal development of the intrapericardial arterial trunks in humans and mice. Cardiovasc Res 95: 108–115.
15. Kirby ML, Gale TF, Stewart DE, (1983) Neural crest cells contribute to normal aorticopulmonary septation. Science 220: 1059–1061.
16. Mayor R, Theveneau E, (2014) The role of the non-canonical Wnt-planar cell polarity pathway in neural crest migration. Biochem J 457: 19–26.
17. Carmona-Fontaine C, Matthews HK, Kuriyama S, Moreno M, Dunn GA, et al. (2008) Contact inhibition of locomotion in vivo controls neural crest directional migration. Nature 456: 957–961.
18. Bayly R, Axelrod JD, (2011) Pointing in the right direction: new developments in the field of planar cell polarity. Nat Rev Genet 12: 385–391.
19. Tao H, Suzuki M, Kiyonari H, Abe T, Sasaoka T, et al. (2009) Mouse prickle1, the homolog of a PCP gene, is essential for epiblast apical-basal polarity. Proc Natl Acad Sci U S A 106: 14426–14431.
20. Tao H, Inoue K, Kiyonari H, Bassuk AG, Axelrod JD, et al. (2012) Nuclear localization of Prickle2 is required to establish cell polarity during early mouse embryogenesis. Dev Biol 364: 138–148.
21. Goodrich LV, Strutt D, (2011) Principles of planar polarity in animal development. Development 138: 1877–1892.
22. Henderson DJ, Chaudhry B, (2011) Getting to the heart of planar cell polarity signaling. Birth Defects Res A Clin Mol Teratol 91: 460–467.
23. Wang J, Mark S, Zhang X, Qian D, Yoo SJ, et al. (2005) Regulation of polarized extension and planar cell polarity in the cochlea by the vertebrate PCP pathway. Nat Genet 37: 980–985.
24. Yin H, Copley CO, Goodrich LV, Deans MR, (2012) Comparison of phenotypes between different vangl2 mutants demonstrates dominant effects of the Looptail mutation during hair cell development. PLoS One 7: e31988.
25. Strong LC, Hollander WF, (1949) Hereditary loop-tail in the house mouse. J Hered 40: 329–334.
26. Henderson DJ, Conway SJ, Greene ND, Gerrelli D, Murdoch JN, et al. (2001) Cardiovascular defects associated with abnormalities in midline development in the Loop-tail mouse mutant. Circ Res 89: 6–12.
27. Phillips HM, Hildreth V, Peat JD, Murdoch JN, Kobayashi K, et al. (2008) Non-cell-autonomous roles for the planar cell polarity gene Vangl2 in development of the coronary circulation. Circ Res 102: 615–623.
28. Montcouquiol M, Sans N, Huss D, Kach J, Dickman JD, et al. (2006) Asymmetric localization of Vangl2 and Fz3 indicate novel mechanisms for planar cell polarity in mammals. J Neurosci 26: 5265–5275.
29. Torban E, Wang HJ, Groulx N, Gros P, (2004) Independent mutations in mouse Vangl2 that cause neural tube defects in looptail mice impair interaction with members of the Dishevelled family. J Biol Chem 279: 52703–52713.
30. Phillips HM, Murdoch JN, Chaudhry B, Copp AJ, Henderson DJ, (2005) Vangl2 acts via RhoA signaling to regulate polarized cell movements during development of the proximal outflow tract. Circ Res 96: 292–299.
31. Moses KA, DeMayo F, Braun RM, Reecy JL, Schwartz RJ, (2001) Embryonic expression of an Nkx2-5/Cre gene using ROSA26 reporter mice. Genesis 31: 176–180.
32. Goddeeris MM, Schwartz R, Klingensmith J, Meyers EN, (2007) Independent requirements for Hedgehog signaling by both the anterior heart field and neural crest cells for outflow tract development. Development 134: 1593–1604.
33. Torban E, Wang HJ, Patenaude AM, Riccomagno M, Daniels E, et al. (2007) Tissue, cellular and sub-cellular localization of the Vangl2 protein during embryonic development: effect of the Lp mutation. Gene Expr Patterns 7: 346–354.
34. Lake BB, Sokol SY, (2009) Strabismus regulates asymmetric cell divisions and cell fate determination in the mouse brain. J Cell Biol 185: 59–66.
35. Kallay LM, McNickle A, Brennwald PJ, Hubbard AL, Braiterman LT, (2006) Scribble associates with two polarity proteins, Lgl2 and Vangl2, via distinct molecular domains. J Cell Biochem 99: 647–664.
36. Boczonadi V, Gillespie R, Keenan I, Ramsbottom SA, Donald-Wilson C, et al. (2014) Scrib: Rac1 interactions are required for the morphogenesis of the ventricular myocardium. Cardiovasc Res.
37. Torban E, Patenaude AM, Leclerc S, Rakowiecki S, Gauthier S, et al. (2008) Genetic interaction between members of the Vangl family causes neural tube defects in mice. Proc Natl Acad Sci U S A 105: 3449–3454.
38. Pryor SE, Massa V, Savery D, Andre P, Yang Y, et al. (2014) Vangl-dependent planar cell polarity signalling is not required for neural crest migration in mammals. Development 141: 3153–3158.
39. Munoz-Soriano V, Belacortu Y, Paricio N, (2012) Planar cell polarity signaling in collective cell movements during morphogenesis and disease. Curr Genomics 13: 609–622.
40. Guillot C, Lecuit T, (2013) Mechanics of epithelial tissue homeostasis and morphogenesis. Science 340: 1185–1189.
41. Yates LL, Schnatwinkel C, Hazelwood L, Chessum L, Paudyal A, et al. (2013) Scribble is required for normal epithelial cell-cell contacts and lumen morphogenesis in the mammalian lung. Dev Biol 373: 267–280.
42. Wu X, Li S, Chrostek-Grashoff A, Czuchra A, Meyer H, et al. (2007) Cdc42 is crucial for the establishment of epithelial polarity during early mammalian development. Dev Dyn 236: 2767–2778.
43. Chung S, Vining MS, Bradley PL, Chan CC, Wharton KA, Jret al. (2009) Serrano (sano) functions with the planar cell polarity genes to control tracheal tube length. PLoS Genet 5: e1000746.
44. Hoffmann M, Segbert C, Helbig G, Bossinger O, (2010) Intestinal tube formation in Caenorhabditis elegans requires vang-1 and egl-15 signaling. Dev Biol 339: 268–279.
45. Chen L, Fulcoli FG, Ferrentino R, Martucciello S, Illingworth EA, et al. (2012) Transcriptional control in cardiac progenitors: Tbx1 interacts with the BAF chromatin remodeling complex and regulates Wnt5a. PLoS Genet 8: e1002571.
46. Yelbuz TM, Waldo KL, Kumiski DH, Stadt HA, Wolfe RR, et al. (2002) Shortened outflow tract leads to altered cardiac looping after neural crest ablation. Circulation 106: 504–510.
47. Ward C, Stadt H, Hutson M, Kirby ML, (2005) Ablation of the secondary heart field leads to tetralogy of Fallot and pulmonary atresia. Dev Biol 284: 72–83.
48. Hamblet NS, Lijam N, Ruiz-Lozano P, Wang J, Yang Y, et al. (2002) Dishevelled 2 is essential for cardiac outflow tract development, somite segmentation and neural tube closure. Development 129: 5827–5838.
49. Etheridge SL, Ray S, Li S, Hamblet NS, Lijam N, 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: e1000259.
50. Schleiffarth JR, Person AD, Martinsen BJ, Sukovich DJ, Neumann A, et al. (2007) Wnt5a is required for cardiac outflow tract septation in mice. Pediatr Res 61: 386–391.
51. Zhou W, Lin L, Majumdar A, Li X, Zhang X, et al. (2007) Modulation of morphogenesis by noncanonical Wnt signaling requires ATF/CREB family-mediated transcriptional activation of TGFbeta2. Nat Genet 39: 1225–1234.
52. Yu H, Smallwood PM, Wang Y, Vidaltamayo R, Reed R, et al. (2010) Frizzled 1 and frizzled 2 genes function in palate, ventricular septum and neural tube closure: general implications for tissue fusion processes. Development 137: 3707–3717.
53. 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: 135–144.
54. Farley FW, Soriano P, Steffen LS, Dymecki SM, (2000) Widespread recombinase expression using FLPeR (flipper) mice. Genesis 28: 106–110.
55. Srinivas S, Watanabe T, Lin CS, William CM, Tanabe Y, et al. (2001) Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus. BMC Dev Biol 1: 4.
56. Hayashi S, Lewis P, Pevny L, McMahon AP, (2002) Efficient gene modulation in mouse epiblast using a Sox2Cre transgenic mouse strain. Gene Expr Patterns 2: 93–97.
57. Lallemand Y, Luria V, Haffner-Krausz R, Lonai P, (1998) Maternally expressed PGK-Cre transgene as a tool for early and uniform activation of the Cre site-specific recombinase. Transgenic Res 7: 105–112.
58. Yang L, Cai CL, Lin L, Qyang Y, Chung C, et al. (2006) Isl1Cre reveals a common Bmp pathway in heart and limb development. Development 133: 1575–1585.
59. Danielian PS, Muccino D, Rowitch DH, Michael SK, McMahon AP, (1998) Modification of gene activity in mouse embryos in utero by a tamoxifen-inducible form of Cre recombinase. Curr Biol 8: 1323–1326.
60. Chen J, Kubalak SW, Minamisawa S, Price RL, Becker KD, et al. (1998) Selective requirement of myosin light chain 2v in embryonic heart function. J Biol Chem 273: 1252–1256.