Expression of Id2 in the second heart field and cardiac defects in Id2 knock-out mice

Developmental Dynamics

Volumn 240, Issue 11, 2011, Pages 2561-2577

  Jongbloed, M R M ^a   Vicente Steijn, R ^a   Douglas, Y L ^b   Wisse, L J ^a   Mori, K ^c   Yokota, Y ^c   Bartelings, M M ^a   Schalij, M J ^a   Mahtab, E A ^a   Poelmann, R E ^a   Gittenberger de Groot, A C ^a  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^b UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^c UNIVERSITY OF FUKUI   (Japan)

Author keywords

Cardiac conduction system; Id2; Outflow tract; Posterior heart field; Second heart field; Sinoatrial node

Indexed keywords

GENE PRODUCT; INHIBITOR OF DIFFERENTIATION 2; PROTEIN HCN4; PROTEIN MLC 2A; TRANSCRIPTION FACTOR NKX2.5; UNCLASSIFIED DRUG; WT1 PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL LINEAGE; CONGENITAL HEART MALFORMATION; EMBRYO; ENDOCARDIUM; EPICARDIUM; HEART DEVELOPMENT; HEART MUSCLE; HEART RIGHT VENTRICLE DOUBLE OUTLET; HEART VENTRICLE SEPTUM DEFECT; KNOCKOUT MOUSE; MESENCHYME CELL; MESODERM; MOUSE; NEURAL CREST CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PULMONARY VEIN; STEM CELL; WILD TYPE;

ANIMALS; ANIMALS, NEWBORN; BODY PATTERNING; COMPUTER SIMULATION; EMBRYO, MAMMALIAN; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GESTATIONAL AGE; HEART; HEART DEFECTS, CONGENITAL; IMAGING, THREE-DIMENSIONAL; INHIBITOR OF DIFFERENTIATION PROTEIN 2; MICE; MICE, KNOCKOUT; MODELS, BIOLOGICAL; ORGANOGENESIS;

MUS;

EID: 80054841795     PISSN: 10588388     EISSN: 10970177     Source Type: Journal    
DOI: 10.1002/dvdy.22762     Document Type: Article

References (58)

1. Aanhaanen WT, Mommersteeg MT, Norden J, Wakker V, de Gier-de VC, Anderson RH, Kispert A, Moorman AF, Christoffels VM. 2010. Developmental origin, growth, and three-dimensional architecture of the atrioventricular conduction axis of the mouse heart. Circ Res 107: 728-736.
2. Bai G, Sheng N, Xie Z, Bian W, Yokota Y, Benezra R, Kageyama R, Guillemot F, Jing N. 2007. Id sustains Hes1 expression to inhibit precocious neurogenesis by releasing negative autoregulation of Hes1. Dev Cell 13: 283-297.
3. Bajolle F, Zaffran S, Losay J, Ou P, Buckingham M, Bonnet D. 2009. Conotruncal defects associated with anomalous pulmonary venous connections. Arch Cardiovasc Dis 102: 105-110.
4. Bax NA, Lie-Venema H, Vicente-Steijn R, Bleyl SB, Van Den Akker NM, Maas S, Poelmann RE, Gittenberger-de Groot AC. 2009. Platelet-derived growth factor is involved in the differentiation of second heart field-derived cardiac structures in chicken embryos. Dev Dyn 238: 2658-2669.
5. Bax NA, Bleyl SB, Gallini R, Wisse LJ, Hunter J, Van Oorschot AA, Mahtab EA, Lie-Venema H, Goumans MJ, Betsholtz C, Gittenberger-de Groot AC. 2010. Cardiac malformations in Pdgfralpha mutant embryos are associated with increased expression of WT1 and Nkx2.5 in the second heart field. Dev Dyn 239: 2307-2317.
6. Blaschke RJ, Hahurij ND, Kuijper S, Just S, Wisse LJ, Deissler K, Maxelon T, Anastassiadis K, Spitzer J, Hardt SE, Schöler H, Feitsma H, Rottbauer W, Blum M, Meijlink F, Rappold GA, Gittenberger-de Groot AC. 2007. Targeted mutation reveals essential functions of the homeodomain transcription factor Shox2 in sinoatrial and pacemaking development. Circulation 115: 1830-1838.
7. Bleyl SB, Saijoh Y, Bax NA, Gittenberger-de Groot AC, Wisse LJ, Chapman SC, Hunter J, Shiratori H, Hamada H, Yamada S, Shiota K, Klewer SE, Leppert MF, Schoenwolf GC. 2010. Dysregulation of the PDGFRA gene causes inflow tract anomalies including TAPVR: integrating evidence from human genetics and model organisms. Hum Mol Genet 19: 1286-1301.
8. Cai CL, Liang X, Shi Y, Chu PH, Pfaff SL, Chen J, Evans S. 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.
9. Chen Q, Chen H, Zheng D, Kuang C, Fang H, Zou B, Zhu W, Bu G, Jin T, Wang Z, Zhang X, Chen J, Field LJ, Rubart M, Shou W, Chen Y. 2009. Smad7 is required for the development and function of the heart. J Biol Chem 284: 292-300.
10. Christoffels VM, Mommersteeg MT, Trowe MO, Prall OW, Gier-de Vries C, Soufan AT, Bussen M, Schuster-Gossler K, Harvey RP, Moorman AF, Kispert A. 2006. Formation of the venous pole of the heart from an Nkx2-5-negative precursor population requires Tbx18. Circ Res 98: 1555-1563.
11. DeRuiter MC, Poelmann RE, VanderPlas-de Vries I, Mentink MMT, Gittenberger-de Groot AC. 1992. The development of the myocardium and endocardium in mouse embryos. Fusion of two heart tubes? Anat Embryol 185: 461-473.
12. Douglas YL, Mahtab EA, Jongbloed MR, Uhrin P, Zaujec J, Binder BR, Schalij MJ, Poelmann RE, DeRuiter MC, Gittenberger-de Groot AC. 2009. Pulmonary vein, dorsal atrial wall and atrial septum abnormalities in podoplanin knockout mice with disturbed posterior heart field contribution. Pediatr Res 65: 27-32.
13. Fraidenraich D, Stillwell E, Romero E, Wilkes D, Manova K, Basson CT, Benezra R. 2004. Rescue of cardiac defects in id knockout embryos by injection of embryonic stem cells. Science 306: 247-252.
14. Garcia-Frigola C, Shi Y, Evans SM. 2003. Expression of the hyperpolarization-activated cyclic nucleotide-gated cation channel HCN4 during mouse heart development. Gene Expr Patterns 3: 777-783.
15. Gittenberger-de Groot AC, Vrancken Peeters M-PFM, Mentink MMT, Gourdie RG, Poelmann RE. 1998. Epicardium-derived cells contribute a novel population to the myocardial wall and the atrioventricular cushions. Circ Res 82: 1043-1052.
16. Gittenberger-de Groot AC, Mahtab EAF, Hahurij ND, Wisse LJ, DeRuiter MC, Wijffels MCEF, Poelmann RE. 2007. Nkx2.5 negative myocardium of the posterior heart field and its correlation with podoplanin expression in cells from the developing cardiac pacemaking and conduction system. Anat Rec 290: 115-122.
17. Gundersen HJ, Jensen EB. 1987. The efficiency of systematic sampling in stereology and its prediction. J Microscopy 147: 229-263.
18. Jen Y, Manova K, Benezra R. 1996. Expression patterns of Id1, Id2, and Id3 are highly related but distinct from that of Id4 during mouse embryogenesis. Dev Dyn 207: 235-252.
19. Jogi A, Persson P, Grynfeld A, Pahlman S, Axelson H. 2002. Modulation of basic helix-loop-helix transcription complex formation by Id proteins during neuronal differentiation. J Biol Chem 277: 9118-9126.
20. Jongbloed MR, Wijffels MC, Schalij MJ, Blom NA, Poelmann RE, van Der LA, Mentink MM, Wang Z, Fishman GI, Gittenberger-de Groot AC. 2005. Development of the right ventricular inflow tract and moderator band: a possible morphological and functional explanation for Mahaim tachycardia. Circ Res 96: 776-783.
21. Kelly RG. 2005. Molecular inroads into the anterior heart field. Trends Cardiovasc Med 15: 51-56.
22. Kelly RG, Buckingham ME. 2002. The anterior heart-forming field: voyage to the arterial pole of the heart. Trends Genet 18: 210-216.
23. 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.
24. Kelly RG, Jerome-Majewska LA, Papaioannou VE. 2004. The del22q11.2 candidate gene Tbx1 regulates branchiomeric myogenesis. Hum Mol Genet 13: 2829-2840.
25. Kubalak SW, Miller-Hance WC, O'Brien TX, Dyson E, Chien KR. 1994. Chamber specification of atrial myosin light chain-2 expression precedes septation during murine cardiogenesis. J Biol Chem 269: 16961-16970.
26. Lasorella A, Rothschild G, Yokota Y, Russell RG, Iavarone A. 2005. Id2 mediates tumor initiation, proliferation, and angiogenesis in Rb mutant mice. Mol Cell Biol 25: 3563-3574.
27. Lie-Venema H, van den Akker NMS, Bax NAM, Winter EM, Maas S, Kekarainen T, Hoeben RC, DeRuiter MC, Poelmann RE, Gittenberger-de Groot AC. 2007. Origin, fate, and function of epicardium-derived cells (EPCDs) in normal and abnormal cardiac development. Sci World J 7: 1777-1798.
28. Lim JY, Kim WH, Kim J, Park SI. 2008. Induction of Id2 expression by cardiac transcription factors GATA4 and Nkx2.5. J Cell Biochem 103: 182-194.
29. Mahtab EAF, Wijffels MCEF, van den Akker NMS, Hahurij ND, Lie-Venema H, Wisse LJ, DeRuiter MC, Uhrin P, Zaujec J, Binder BR, Schalij M.J., Poelmann RE, Gittenberger-de Groot AC. 2008. Cardiac malformations and myocardial abnormalities in podoplanin knockout mouse embryos: correlation with abnormal epicardial development. Dev Dyn 237: 847-857.
30. Mahtab EA, Vicente-Steijn R, Hahurij ND, Jongbloed MR, Wisse LJ, DeRuiter MC, Uhrin P, Zaujec J, Binder BR, Schalij MJ, Poelmann RE, Gittenberger-de Groot AC. 2009. Podoplanin deficient mice show a Rhoa-related hypoplasia of the sinus venosus myocardium including the sinoatrial node. Dev Dyn 238: 183-193.
31. Martinez-Estrada OM, Lettice LA, Essafi A, Guadix JA, Slight J, Velecela V, Hall E, Reichmann J, Devenney PS, Hohenstein P, Hosen N, Hill RE, Munoz-Chapuli R, Hastie ND. 2010. Wt1 is required for cardiovascular progenitor cell formation through transcriptional control of Snail and E-cadherin. Nat Genet 42: 89-93.
32. Martinsen BJ, Frasier AJ, Baker CV, Lohr JL. 2004. Cardiac neural crest ablation alters Id2 gene expression in the developing heart. Dev Biol 272: 176-190.
33. Mesbah K, Harrelson Z, Theveniau-Ruissy M, Papaioannou VE, Kelly RG. 2008a. Tbx3 is required for outflow tract development. Circ Res 103: 743-750.
34. Mesbah K, Harrelson Z, Theveniau-Ruissy M, Papaioannou VE, Kelly RG. 2008b. Tbx3 is required for outflow tract development. Circ Res 103: 743-750.
35. Mjaatvedt CH, Nakaoka T, Moreno-Rodriguez R, Norris RA, Kern MJ, Eisenberg CA, Turner D, Markwald RR. 2001. The outflow tract of the heart is recruited from a novel heart-forming field. Dev Biol 238: 97-109.
36. Moreno-Rodriguez RA, Krug EL, Reyes L, Villavicencio L, Mjaatvedt CH, Markwald RR. 2006. Bidirectional fusion of the heart-forming fields in the developing chick embryo. Dev Dyn 235: 191-202.
37. Moskowitz IP, Pizard A, Patel VV, Bruneau BG, Kim JB, Kupershmidt S, Roden D, Berul CI, Seidman CE, Seidman JG. 2004. The T-Box transcription factor Tbx5 is required for the patterning and maturation of the murine cardiac conduction system. Development 131: 4107-4116.
38. Moskowitz IP, Kim JB, Moore ML, Wolf CM, Peterson MA, Shendure J, Nobrega MA, Yokota Y, Berul C, Izumo S, Seidman JG, Seidman CE. 2007. A molecular pathway including Id2, Tbx5, and Nkx2-5 required for cardiac conduction system development. Cell 129: 1365-1376.
39. Moskowitz IP, Wang J, Peterson MA, Pu WT, Mackinnon AC, Oxburgh L, Chu GC, Sarkar M, Berul C, Smoot L, Robertson EJ, Schwartz R, Seidman JG, Seidman CE. 2011. Transcription factor genes Smad4 and Gata4 cooperatively regulate cardiac valve development. Proc Natl Acad Sci USA 108: 4006-4011.
40. Nakahiro T, Kurooka H, Mori K, Sano K, Yokota Y. 2010. Identification of BMP-responsive elements in the mouse Id2 gene. Biochem Biophys Res Commun 399: 416-421.
41. Park EJ, Ogden LA, Talbot A, Evans S, Cai CL, Black BL, Frank DU, Moon AM. 2006. Required, tissue-specific roles for Fgf8 in outflow tract formation and remodeling. Development 133: 2419-2433.
42. Prall OW, Menon MK, Solloway MJ, Watanabe Y, Zaffran S, Bajolle F, Biben C, McBride JJ, Robertson BR, Chaulet H, Stennard FA, Wise N, Schaft D, Wolstein O, Furtado MB, Shiratori H, Chien KR, Hamada H, Black BL, Saga Y, Robertson EJ, Buckingham ME, Harvey RP. 2007. An Nkx2-5/Bmp2/Smad1 negative feedback loop controls heart progenitor specification and proliferation. Cell 128: 947-959.
43. Puskaric S, Schmitteckert S, Mori AD, Glaser A, Schneider KU, Bruneau BG, Blaschke RJ, Steinbeisser H, Rappold G. 2010. Shox2 mediates Tbx5 activity by regulating Bmp4 in the pacemaker region of the developing heart. Hum Mol Genet 19: 4625-4633.
44. 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: e6267.
45. Snarr BS, O'Neal JL, Chintalapudi MR, Wirrig EE, Phelps AL, Kubalak SW, Wessels A. 2007a. Isl1 expression at the venous pole identifies a novel role for the second heart field in cardiac development. Circ Res 101: 971-974.
46. Snarr BS, Wirrig EE, Phelps AL, Trusk TC, Wessels A. 2007b. A spatiotemporal evaluation of the contribution of the dorsal mesenchymal protrusion to cardiac development. Dev Dyn 236: 1287-1294.
47. Song L, Yan W, Chen X, Deng CX, Wang Q, Jiao K. 2007. Myocardial smad4 is essential for cardiogenesis in mouse embryos. Circ Res 101: 277-285.
48. Sun Y, Liang X, Najafi N, Cass M, Lin L, Cai CL, Chen J, Evans SM. 2007. Islet 1 is expressed in distinct cardiovascular lineages, including pacemaker and coronary vascular cells. Dev Biol 304: 286-296.
49. Thomas PS, Kasahara H, Edmonson AM, Izumo S, Yacoub MH, Barton PJ, Gourdie RG. 2001. Elevated expression of Nkx-2.5 in developing myocardial conduction cells. Anat Rec 263: 307-313.
50. Valcourt U, Kowanetz M, Niimi H, Heldin CH, Moustakas A. 2005. TGF-beta and the Smad signaling pathway support transcriptomic reprogramming during epithelial-mesenchymal cell transition. Mol Biol Cell 16: 1987-2002.
51. van den Akker NMS, Lie-Venema H, Maas S, Eralp I, DeRuiter MC, Poelmann RE, Gittenberger-de-Groot AC. 2005. Platelet-derived growth factors in the developing avian heart and maturating coronary vasculature. Dev Dyn 233: 1579-1588.
52. Vicente-Steijn R, Kolditz DP, Mahtab EA, Askar SF, Bax NA, van der Graaf LM, Wisse LJ, Passier R, Pijnappels DA, Schalij MJ, Poelmann RE, Gittenberger-de Groot AC, Jongbloed MR. 2010. Electrical activation of sinus venosus myocardium and expression patterns of RhoA and Isl-1 in the chick embryo. J Cardiovasc Electrophysiol 21: 1284-1292.
53. Vicente-Steijn R, Passier R, Wisse LJ, Schalij MJ, Poelmann RE, Gittenberger-de Groot AC, Jongbloed MR. 2011. Funny current channel HCN4 delineates the developing cardiac conduction system in chicken heart. Heart Rhythm 8:1254-1263.
54. Waldo K, Kumiski DH, Wallis KT, Stadt HA, Hutson MR, Platt DH, Kirby ML. 2001. Conotruncal myocardium arises from a secondary heart field. Development 128: 3179-3188.
55. Yanni J, Boyett MR, Anderson RH, Dobrzynski H. 2009. The extent of the specialized atrioventricular ring tissues. Heart Rhythm 6: 672-680.
56. Yokota Y, Mansouri A, Mori S, Sugawara S, Adachi S, Nishikawa S, Gruss P. 1999. Development of peripheral lymphoid organs and natural killer cells depends on the helix-loop-helix inhibitor Id2. Nature 397: 702-706.
57. Yokota Y, Mori S, Narumi O, Kitajima K. 2001. In vivo function of a differentiation inhibitor, Id2. IUBMB Life 51: 207-214.
58. Zhao Q, Beck AJ, Vitale JM, Schneider JS, Gao S, Chang C, Elson G, Leibovich SJ, Park JY, Tian B, Nam HS, Fraidenraich D. 2011. Developmental ablation of Id1 and Id3 genes in the vasculature leads to postnatal cardiac phenotypes. Dev Biol 349: 53-64.