Tbx1 is required for second heart field proliferation in zebrafish

Developmental Dynamics

Volumn 242, Issue 5, 2013, Pages 550-559

  Nevis, Kathleen ^a,b   Obregon, Pablo ^a,b   Walsh, Conor ^a,b   Guner Ataman, Burcu ^a,b   Burns, C Geoffrey ^a,b,c   Burns, Caroline E ^a,b,c  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c HARVARD STEM CELL INSTITUTE   (United States)

Author keywords

Cardiac; Heart; Second heart field; Tbx1; Zebrafish

Indexed keywords

ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; EMBRYO; GENE; GENE MUTATION; HEART; HEART DEVELOPMENT; HEART MUSCLE CELL; HEART VENTRICLE; NONHUMAN; PRIORITY JOURNAL; SECOND HEART FIELD; TBX1 GENE; ZEBRA FISH;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; CELL DIFFERENTIATION; CELL PROLIFERATION; EMBRYO, NONMAMMALIAN; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEART; HEART VENTRICLES; MYOCYTES, CARDIAC; STEM CELLS; T-BOX DOMAIN PROTEINS; ZEBRAFISH; ZEBRAFISH PROTEINS;

ANIMALIA; DANIO RERIO; MAMMALIA;

EID: 84876463659     PISSN: 10588388     EISSN: 10970177     Source Type: Journal    
DOI: 10.1002/dvdy.23928     Document Type: Article

References (49)

1. Abu-Issa R, Smyth G, Smoak I, Yamamura K, Meyers EN. 2002. Fgf8 is required for pharyngeal arch and cardiovascular development in the mouse. Development 129:4613-4625.
2. Aggarwal VS, Morrow BE. 2008. Genetic modifiers of the physical malformations in velo-cardio-facial syndrome/DiGeorge syndrome. Dev Disabil Res Rev 14:19-25.
3. Arnold JS, Werling U, Braunstein EM, Liao J, Nowotschin S, Edelmann W, Hebert JM, Morrow BE. 2006. Inactivation of Tbx1 in the pharyngeal endoderm results in 22q11DS malformations. Development 133:977-987.
4. Brown CB, Wenning JM, Lu MM, Epstein DJ, Meyers EN, Epstein JA. 2004. 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.
5. Burns CG, Milan DJ, Grande EJ, Rottbauer W, MacRae CA, Fishman MC. 2005. High-throughput assay for small molecules that modulate zebrafish embryonic heart rate. Nat Chem Biol 1:263-264.
6. Chapman DL, Garvey N, Hancock S, Alexiou M, Agulnik SI, Gibson-Brown JJ, Cebra-Thomas J, Bollag RJ, Silver LM, Papaioannou VE. 1996. Expression of the T-box family genes, Tbx1-Tbx5, during early mouse development. Dev Dyn 206:379-390.
7. Chen L, Fulcoli FG, Tang S, Baldini A. 2009. Tbx1 regulates proliferation and differentiation of multipotent heart progenitors. Circ Res 105:842-851.
8. de Pater E, Clijsters L, Marques SR, Lin YF, Garavito-Aguilar ZV, Yelon D, Bakkers J. 2009. Distinct phases of cardiomyocyte differentiation regulate growth of the zebrafish heart. Development 136:1633-1641.
9. Garg V, Yamagishi C, Hu T, Kathiriya IS, Yamagishi H, Srivastava D. 2001. Tbx1, a DiGeorge syndrome candidate gene, is regulated by sonic hedgehog during pharyngeal arch development. Dev Biol 235:62-73.
10. Grimes AC, Stadt HA, Shepherd IT, Kirby ML. 2006. Solving an enigma: arterial pole development in the zebrafish heart. Dev Biol 290:265-276.
11. Hami D, Grimes AC, Tsai HJ, Kirby ML. 2011. Zebrafish cardiac development requires a conserved secondary heart field. Development 138:2389-2398.
12. Hinits Y, Pan L, Walker C, Dowd J, Moens CB, Hughes SM. 2012. Zebrafish Mef2ca and Mef2cb are essential for both first and second heart field cardiomyocyte differentiation. Dev Biol 369:199-210.
13. Hu T, Yamagishi H, Maeda J, McAnally J, Yamagishi C, Srivastava D. 2004. Tbx1 regulates fibroblast growth factors in the anterior heart field through a reinforcing autoregulatory loop involving forkhead transcription factors. Development 131:5491-5502.
14. Huynh T, Chen L, Terrell P, Baldini A. 2007. A fate map of Tbx1 expressing cells reveals heterogeneity in the second cardiac field. Genesis 45:470-475.
15. Jerome LA, Papaioannou VE. 2001. DiGeorge syndrome phenotype in mice mutant for the T-box gene, Tbx1. Nat Genet 27:286-291.
16. Kochilas LK, Potluri V, Gitler A, Balasubramanian K, Chin AJ. 2003. Cloning and characterization of zebrafish tbx1. Gene Expr Patterns 3:645-651.
17. Lazic S, Scott IC. 2011. Mef2cb regulates late myocardial cell addition from a second heart field-like population of progenitors in zebrafish. Dev Biol 354:123-133.
18. Liao J, Aggarwal VS, Nowotschin S, Bondarev A, Lipner S, Morrow BE. 2008. Identification of downstream genetic pathways of Tbx1 in the second heart field. Dev Biol 316:524-537.
19. Lindsay EA, Vitelli F, Su H, Morishima M, Huynh T, Pramparo T, Jurecic V, Ogunrinu G, Sutherland HF, Scambler PJ, Bradley A, Baldini A. 2001. Tbx1 haploinsufficieny in the DiGeorge syndrome region causes aortic arch defects in mice. Nature 410:97-101.
20. Mably JD, Mohideen MA, Burns CG, Chen JN, Fishman MC. 2003. heart of glass regulates the concentric growth of the heart in zebrafish. Curr Biol 13:2138-2147.
21. Mahler J, Filippi A, Driever W. 2010. DeltaA/DeltaD regulate multiple and temporally distinct phases of notch signaling during dopaminergic neurogenesis in zebrafish. J Neurosci 30:16621-16635.
22. Marques SR, Lee Y, Poss KD, Yelon D. 2008. Reiterative roles for FGF signaling in the establishment of size and proportion of the zebrafish heart. Dev Biol 321:397-406.
23. Merscher S, Funke B, Epstein JA, Heyer J, Puech A, Lu MM, Xavier RJ, Demay MB, Russell RG, Factor S, Tokooya K, Jore BS, Lopez M, Pandita RK, Lia M, Carrion D, Xu H, Schorle H, Kobler JB, Scambler P, Wynshaw-Boris A, Skoultchi AI, Morrow BE, Kucherlapati R. 2001. TBX1 is responsible for cardiovascular defects in velo-cardio-facial/DiGeorge syndrome. Cell 104:619-629.
24. Miao M, Bruce AE, Bhanji T, Davis EC, Keeley FW. 2007. Differential expression of two tropoelastin genes in zebrafish. Matrix Biol 26:115-124.
25. Parisot P, Mesbah K, Theveniau-Ruissy M, Kelly RG. 2011. Tbx1, subpulmonary myocardium and conotruncal congenital heart defects. Birth Defects Res A Clin Mol Teratol 91:477-484.
26. 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.
27. Piotrowski T, Nusslein-Volhard C. 2000. The endoderm plays an important role in patterning the segmented pharyngeal region in zebrafish (Danio rerio). Dev Biol 225:339-356.
28. Piotrowski T, Schilling TF, Brand M, Jiang YJ, Heisenberg CP, Beuchle D, Grandel H, van Eeden FJ, Furutani-Seiki M, Granato M, Haffter P, Odenthal J, Warga RM, Trowe T, Nusslein-Volhard C. 1996. Jaw and branchial arch mutants in zebrafish II: anterior arches and cartilage differentiation. Development 123:345-356.
29. Piotrowski T, Ahn DG, Schilling TF, Nair S, Ruvinsky I, Geisler R, Rauch GJ, Haffter P, Zon LI, Zhou Y, Foott H, David IB, Ho RK. 2003. The zebrafish van gogh mutation disrupts tbx1, which is involved in the DiGeorge deletion syndrome in humans. Development 130:5043-5052.
30. Reifers F, Walsh EC, Leger S, Stainier DY, Brand M. 2000. Induction and differentiation of the zebrafish heart requires fibroblast growth factor 8 (fgf8/acerebellar). Development 127:225-235.
31. Ryan AK, Goodship JA, Wilson DI, Philip N, Levy A, Seidel H, Schuffenhauer S, Oechsler H, Belohradsky B, Prieur M, Aurias A, Raymond FL, Clayton-Smith J, Hatchwell E, McKeown C, Beemer FA, Dallapiccola B, Novelli G, Hurst JA, Ignatius J, Green AJ, Winter RM, Brueton L, Brondum-Nielsen K, Scambler PJ. 1997. Spectrum of clinical features associated with interstitial chromosome 22q11 deletions: a European collaborative study. J Med Genet 34:798-804.
32. Scambler PJ. 2010. 22q11 Deletion syndrome: a Role for TBX1 in pharyngeal and cardiovascular development. Pediatr Cardiol 31:378-390.
33. Schilling TF, Piotrowski T, Grandel H, Brand M, Heisenberg CP, Jiang YJ, Beuchle D, Hammerschmidt M, Kane DA, Mullins MC, van Eeden FJ, Kelsh RN, Furutani-Seiki M, Granato M, Haffter P, Odenthal J, Warga RM, Trowe T, Nusslein Volhard C. 1996. Jaw and branchial arch mutants in zebrafish I: branchial arches. Development 123:329-344.
34. Schoenebeck JJ, Keegan BR, Yelon D. 2007. Vessel and blood specification override cardiac potential in anterior mesoderm. Dev Cell 13:254-267.
35. Srivastava D, Olson EN. 2000. A genetic blueprint for cardiac development. Nature 407:221-226.
36. Thisse C, Thisse B, Schilling TF, Postlethwait JH. 1993. Structure of the zebrafish snail1 gene and its expression in wild-type, spadetail and no tail mutant embryos. Development 119:1203-1215.
37. 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.
38. Vitelli F, Morishima M, Taddei I, Lindsay EA, Baldini A. 2002a. Tbx1 mutation causes multiple cardiovascular defects and disrupts neural crest and cranial nerve migratory pathways. Hum Mol Genet 11:915-922.
39. Vitelli F, Taddei I, Morishima M, Meyers EN, Lindsay EA, Baldini A. 2002b. A genetic link between Tbx1 and fibroblast growth factor signaling. Development 129:4605-4611.
40. Vitelli F, Lania G, Huynh T, Baldini A. 2010. Partial rescue of the Tbx1 mutant heart phenotype by Fgf8: genetic evidence of impaired tissue response to Fgf8. J Mol Cell Cardiol 49:836-840.
41. Witzel HR, Jungblut B, Choe CP, Crump JG, Braun T, Dobreva G. 2012. The LIM protein ajuba restricts the second heart field progenitor pool by regulating Isl1 activity. Dev Cell 23:58-70.
42. Xu H, Morishima M, Wylie JN, Schwartz RJ, Bruneau BG, Lindsay EA, Baldini A. 2004. Tbx1 has a dual role in the morphogenesis of the cardiac outflow tract. Development 131:3217-3227.
43. Xu H, Cerrato F, Baldini A. 2005. Timed mutation and cell-fate mapping reveal reiterated roles of Tbx1 during embryogenesis, and a crucial function during segmentation of the pharyngeal system via regulation of endoderm expansion. Development 132:4387-4395.
44. Yagi H, Furutani Y, Hamada H, Sasaki T, Asakawa S, Minoshima S, Ichida F, Joo K, Kimura M, Imamura S, Kamatani N, Momma K, Takao A, Nakazawa M, Shimizu N, Matsuoka R. 2003. Role of TBX1 in human del22q11.2 syndrome. Lancet 362:1366-1373.
45. Yelon D, Horne SA, Stainier DY. 1999. Restricted expression of cardiac myosin genes reveals regulated aspects of heart tube assembly in zebrafish. Dev Biol 214:23-37.
46. Zhang Z, Cerrato F, Xu H, Vitelli F, Morishima M, Vincentz J, Furuta Y, Ma L, Martin JF, Baldini A, et al. 2005. Tbx1 expression in pharyngeal epithelia is necessary for pharyngeal arch artery development. Development 132:5307-5315.
47. Zhang L, Zhong T, Wang Y, Jiang Q, Song H, Gui Y. 2006a. TBX1, a DiGeorge syndrome candidate gene, is inhibited by retinoic acid. Int J Dev Biol 50:55-61.
48. Zhang Z, Huynh T, Baldini A. 2006b. Mesodermal expression of Tbx1 is necessary and sufficient for pharyngeal arch and cardiac outflow tract development. Development 133:3587-3595.
49. Zhou Y, Cashman TJ, Nevis KR, Obregon P, Carney SA, Liu Y, Gu A, Mosimann C, Sondalle S, Peterson RE, Heideman W, Burns CE, Burns CG. 2011. Latent TGF-β binding protein 3 identifies a second heart field in zebrafish. Nature 474:645-648.