Identification of a Tbx1/Tbx2/Tbx3 genetic pathway governing pharyngeal and arterial pole morphogenesis

Human Molecular Genetics

Volumn 21, Issue 6, 2012, Pages 1217-1229

  Mesbah, Karim ^a   Rana, M Sameer ^b   Francou, Alexandre ^a   van duijvenboden, Karel ^b   Papaioannou, Virginia E ^c   Moorman, Antoon F ^b   Kelly, Robert G ^a   Christoffels, Vincent M ^b  

^a AIX MARSEILLE UNIVERSITY   (France)

^b UNIVERSITY OF AMSTERDAM   (Netherlands)

^c Columbia University Medical Center ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN; FIBROBLAST GROWTH FACTOR; HH LIGAND; LIGAND; T BOX TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR TBX1; TRANSCRIPTION FACTOR TBX2; TRANSCRIPTION FACTOR TBX3; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CHROMOSOME 22Q; CONGENITAL HEART MALFORMATION; CONTROLLED STUDY; EMBRYO; GENE EXPRESSION; GENE IDENTIFICATION; GENE LOSS; GENETIC DISORDER; HAPLOINSUFFICIENCY; HYPOPLASIA; MESODERM; MORPHOGENESIS; MOUSE; NEURAL CREST; NONHUMAN; OUTFLOW TRACT DEVELOPMENT; PHARYNGX DEVELOPMENT; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; SIGNAL TRANSDUCTION;

ANIMALS; ARTERIES; CARDIOVASCULAR ABNORMALITIES; CHROMOSOMES, HUMAN, PAIR 22; EMBRYO, MAMMALIAN; FIBROBLAST GROWTH FACTORS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES, MODIFIER; HUMANS; IMMUNOENZYME TECHNIQUES; IN SITU HYBRIDIZATION; MICE; MICE, TRANSGENIC; MORPHOGENESIS; PHARYNX; PHENOTYPE; T-BOX DOMAIN PROTEINS; VENTRICULAR OUTFLOW OBSTRUCTION;

EID: 84857663919     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddr553     Document Type: Article

References (55)

1. Wilson, D.I., Burn, J., Scambler, P. and Goodship, J. (1993) DiGeorge syndrome: part of CATCH 22. JMG, 30, 852-856.
2. Hoffman, J.I. and Kaplan, S. (2002) The incidence of congenital heart disease. J. Am. Coll. Cardiol., 39, 1890-1900.
3. Pierpont, M.E., Basson, C.T., Benson, D.W. Jr., Gelb, B.D., Giglia, T.M., Goldmuntz, E., McGee, G., Sable, C.A., Srivastava, D. and Webb, C.L. (2007) Genetic basis for congenital heart defects: current knowledge. A scientific statement from the American Heart Association Congenital Cardiac Defects Committee, Council on Cardiovascular Disease in the Young: endorsed by the American Academy of Pediatrics. Circulation, 115, 3015-3038.
4. Buckingham, M., Meilhac, S. and Zaffran, S. (2005) Building the mammalian heart from two sources of myocardial cells. Nat. Rev. Genet., 6, 826-837.
5. Dyer, L.A. and Kirby, M.L. (2009) Sonic hedgehog maintains proliferation in secondary heart field progenitors and is required for normal arterial pole formation. Dev. Biol., 330, 305-317.
6. Rochais, F., Mesbah, K. and Kelly, R.G. (2009) Signaling pathways controlling second heart field development. Circ. Res., 104, 933-942.
7. Tirosh-Finkel, L., Zeisel, A., Brodt-Ivenshitz, M., Shamai, A., Yao, Z., Seger, R., Domany, E. and Tzahor, E. (2010) BMP-mediated inhibition of FGF signaling promotes cardiomyocyte differentiation of anterior heart field progenitors. Development, 137, 2989-3000.
8. Stankunas, K., Shang, C., Twu, K.Y., Kao, S.C., Jenkins, N.A., Copeland, N.G., Sanyal, M., Selleri, L., Cleary, M.L. and Chang, C.P. (2008) Pbx/ Meis deficiencies demonstrate multigenetic origins of congenital heart disease. Circ. Res., 103, 702-709.
9. Hoogaars, W.M.H., Barnett, P., Moorman, A.F.M. and Christoffels, V.M. (2007) T-box factors determine cardiac design. Cell. Mol. Life Sci., 64, 646-660.
10. Scambler, P.J. (2000) The 22q11 deletion syndromes. Hum. Mol. Genet., 9, 2421-2426.
11. Jerome, L.A. and Papaioannou, V.E. (2001) DiGeorge syndrome phenotype in mice mutant for the T-box gene, Tbx1. Nat. Genet., 27, 286-291.
12. Lindsay, E.A., Vitelli, F., Su, H., Morishima, M., Huynh, T., Pramparo, T., Jurecic, V., Ogunrinu, G., Sutherland, H.F., Scambler, P.J. et al. (2001) Tbx1 haploinsufficieny in the DiGeorge syndrome region causes aortic arch defects in mice. Nature, 410, 97-101.
13. Merscher, S., Funke, B., Epstein, J.A., Heyer, J., Puech, A., Lu, M.M., Xavier, R.J., Demay, M.B., Russell, R.G., Factor, S. et al. (2001) TBX1 is responsible for cardiovascular defects in velo-cardio-facial/DiGeorge syndrome. Cell, 104, 619-629.
14. Xu, H., Morishima, M., Wylie, J.N., Schwartz, R.J., Bruneau, B.G., Lindsay, E.A. and Baldini, A. (2004) Tbx1 has a dual role in the morphogenesis of the cardiac outflow tract. Development, 131, 3217-3227.
15. Kelly, R.G., Brown, N.A. and Buckingham, M.E. (2001) The arterial pole of the mouse heart forms from Fgf10-expressing cells in pharyngeal mesoderm. Dev. Cell, 1, 435-440.
16. Liao, J., Aggarwal, V.S., Nowotschin, S., Bondarev, A., Lipner, S. and Morrow, B.E. (2008) Identification of downstream genetic pathways of Tbx1 in the second heart field. Dev. Biol., 316, 524-537.
17. Chen, L., Fulcoli, F.G., Tang, S. and Baldini, A. (2009) Tbx1 regulates proliferation and differentiation of multipotent heart progenitors. Circ. Res., 105, 842-851.
18. Vitelli, F., Taddei, I., Morishima, M., Meyers, E.N., Lindsay, E.A. and Baldini, A. (2002) A genetic link between Tbx1 and fibroblast growth factor signaling. Development, 129, 4605-4611.
19. Vitelli, F., Lania, G., Huynh, T. and 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.
20. Bamshad, M., Lin, R.C., Law, D.J., Watkins, W.S., Krakowiak, P.A., Moore, M.E., Franceschini, P., Lala, R., Holmes, L.B., Gebuhr, T.C. et al. (1997) Mutations in human TBX3 alter limb, apocrine and genital development in Ulnar-mammary syndrome. Nat. Genet., 16, 311-315.
21. Christoffels, V.M., Smits, G.J., Kispert, A. and Moorman, A.F. (2010) Development of the pacemaker tissues of the heart. Circ. Res., 106, 240-254.
22. Bakker, M.L., Boukens, B.J., Mommersteeg, M.T.M., Brons, J.F., Wakker, V., Moorman, A.F.M. and Christoffels, V.M. (2008) Transcription factor Tbx3 is required for the specification of the atrioventricular conduction system. Circ. Res., 102, 1340-1349.
23. Mesbah, K., Harrelson, Z., Theveniau-Ruissy, M., Papaioannou, V.E. and Kelly, R.G. (2008) Tbx3 is required for outflow tract development. Circ. Res., 103, 743-750.
24. Harrelson, Z., Kelly, R.G., Goldin, S.N., Gibson-Brown, J.J., Bollag, R.J., Silver, L.M. and Papaioannou, V.E. (2004) Tbx2 is essential for patterning the atrioventricular canal and for morphogenesis of the outflow tract during heart development. Development, 131, 5041-5052.
25. Aanhaanen, W.T., Brons, J.F., Dominguez, J.N., Rana, M.S., Norden, J., Airik, R., Wakker, V., de Gier-de Vries, C., Brown, N.A., Kispert, A. et al. (2009) The Tbx2+ primary myocardium of the atrioventricular canal forms the atrioventricular node and the base of the left ventricle. Circ. Res., 104, 1267-1274.
26. Theveniau-Ruissy, M., Dandonneau, M., Mesbah, K., Ghez, O., Mattei, M.G., Miquerol, L. and Kelly, R.G. (2008) The del22q11.2 candidate gene Tbx1 controls regional outflow tract identity and coronary artery patterning. Circ. Res., 103, 142-148.
27. Kelly, R.G., Jerome-Majewska, L.A. and Papaioannou, V.E. (2004) The del22q11.2 candidate gene Tbx1 regulates branchiomeric myogenesis. Hum. Mol. Genet., 13, 2829-2840.
28. Vitelli, F., Morishima, M., Taddei, I., Lindsay, E.A. and Baldini, A. (2002) Tbx1 mutation causes multiple cardiovascular defects and disrupts neural crest and cranial nerve migratory pathways. Hum. Mol. Genet., 11, 915-922.
29. Calmont, A., Ivins, S., Van Bueren, K.L., Papangeli, I., Kyriakopoulou, V., Andrews, W.D., Martin, J.F., Moon, A.M., Illingworth, E.A., Basson, M.A. et al. (2009) Tbx1 controls cardiac neural crest cell migration during arch artery development by regulating Gbx2 expression in the pharyngeal ectoderm. Development, 136, 3173-3183.
30. Zirzow, S., Ludtke, T.H., Brons, J.F., Petry, M., Christoffels, V.M. and Kispert, A. (2009) Expression and requirement of T-box transcription factors Tbx2 and Tbx3 during secondary palate development in the mouse. Dev. Biol., 336, 145-155.
31. Goddeeris, M.M., Schwartz, R., Klingensmith, J. and Meyers, E.N. (2007) Independent requirements for Hedgehog signaling by both the anterior heart field and neural crest cells for outflow tract development. Development, 134, 1593-1604.
32. Garg, V., Yamagishi, C., Hu, T., Kathiriya, I.S., Yamagishi, H. and Srivastava, D. (2001) Tbx1, a DiGeorge syndrome candidate gene, is regulated by sonic hedgehog during pharyngeal arch development. Dev. Biol., 235, 62-73.
33. Yamagishi, H., Maeda, J., Hu, T., McAnally, J., Conway, S.J., Kume, T., Meyers, E.N., Yamagishi, C. and Srivastava, D. (2003) Tbx1 is regulated by tissue-specific forkhead proteins through a common Sonic hedgehog-responsive enhancer. Genes Dev., 17, 269-281.
34. Vitelli, F., Zhang, Z., Huynh, T., Sobotka, A., Mupo, A. and Baldini, A. (2006) Fgf8 expression in the Tbx1 domain causes skeletal abnormalities and modifies the aortic arch but not the outflow tract phenotype of Tbx1 mutants. Dev. Biol., 295, 559-570.
35. Aggarwal, V.S. and Morrow, B.E. (2008) Genetic modifiers of the physical malformations in velo-cardio-facial syndrome/DiGeorge syndrome. Dev. Disabil. Res. Rev., 14, 19-25.
36. Crossley, P.H. and Martin, G.R. (1995) The mouse Fgf8 gene encodes a family of polypeptides and is expressed in regions that direct outgrowth and patterning in the developing embryo. Development, 121, 439-451.
37. Ilagan, R., bu-Issa, R., Brown, D., Yang, Y.P., Jiao, K., Schwartz, R.J., Klingensmith, J. and Meyers, E.N. (2006) Fgf8 is required for anterior heart field development. Development, 133, 2435-2445.
38. Prall, O.W.J., Menon, M.K., Solloway, M.J., Watanabe, Y., Zaffran, S., Bajolle, F., Biben, C., McBride, J.J., Robertson, B.R., Chaulet, H. et al. (2007) An Nkx2-5/Bmp2/Smad1 negative feedback loop controls heart progenitor specification and proliferation. Cell, 128, 947-959.
39. Peterkin, T., Gibson, A. and Patient, R. (2003) GATA-6 maintains BMP-4 and Nkx2 expression during cardiomyocyte precursor maturation. EMBO J., 22, 4260-4273.
40. Naiche, L.A., Harrelson, Z., Kelly, R.G. and Papaioannou, V.E. (2005) T-box genes in vertebrate development. Annu. Rev. Genet., 39, 219-239.
41. Dupays, L., Kotecha, S. and Mohun, T.J. (2009) Tbx2 misexpression impairs deployment of second heart field derived progenitor cells to the arterial pole of the embryonic heart. Dev. Biol., 333, 121-131.
42. Kirby, M.L. and Hutson, M.R. (2010) Factors controlling cardiac neural crest cell migration. Cell Adhes. Migr., 4, 609-621.
43. Wang, J., Greene, S.B., Bonilla-Claudio, M., Tao, Y., Zhang, J., Bai, Y., Huang, Z., Black, B.L., Wang, F. and Martin, J.F. (2010) Bmp signaling regulates myocardial differentiation from cardiac progenitors through a microRNA-mediated mechanism. Dev. Cell, 19, 903-912.
44. Guo, T., McGinn, D.M., Blonska, A., Shanske, A., Bassett, A., Chow, E., Bowser, M., Sheridan, M., Beemer, F., Devriendt, K. et al. (2011) Genotype and cardiovascular phenotype correlations with TBX1 in 1,022 velo-cardio-facial/DiGeorge/22q11.2 deletion syndrome patients. Hum. Mutat., 32, 1278-1289.
45. Nowotschin, S., Liao, J., Gage, P.J., Epstein, J.A., Campione, M. and Morrow, B.E. (2006) Tbx1 affects asymmetric cardiac morphogenesis by regulating Pitx2 in the secondary heart field. Development, 133, 1565-1573.
46. Guris, D.L., Duester, G., Papaioannou, V.E. and Imamoto, A. (2006) Dose-dependent interaction of Tbx1 and Crkl and locally aberrant RA signaling in a model of del22q11 syndrome. Dev. Cell, 10, 81-92.
47. Randall, V., McCue, K., Roberts, C., Kyriakopoulou, V., Beddow, S., Barrett, A.N., Vitelli, F., Prescott, K., Shaw-Smith, C., Devriendt, K. et al. (2009) Great vessel development requires biallelic expression of Chd7 and Tbx1 in pharyngeal ectoderm in mice. J. Clin. Invest., 119, 3301-3310.
48. Guo, C., Sun, Y., Zhou, B., Adam, R.M., Li, X., Pu, W.T., Morrow, B.E., Moon, A. and Li, X. (2011) A Tbx1-Six1/Eya1-Fgf8 genetic pathway controls mammalian cardiovascular and craniofacial morphogenesis. J. Clin. Invest, 121, 1585-1595.
49. Wakker, V., Brons, J.F., Aanhaanen, W.T., van Roon, M.A., Moorman, A.F. and Christoffels, V.M. (2010) Generation of mice with a conditional null allele for Tbx2. Genesis, 48, 195-199.
50. Davenport, T.G., Jerome-Majewska, L.A. and Papaioannou, V.E. (2003) Mammary gland, limb and yolk sac defects in mice lacking Tbx3, the gene mutated in human Ulnar-mammary syndrome. Development, 130, 2263-2273.
51. Hoogaars, W.M.H., Tessari, A., Moorman, A.F.M., de Boer, P.A.J., Hagoort, J., Soufan, A.T., Campione, M. and Christoffels, V.M. (2004) The transcriptional repressor Tbx3 delineates the developing central conduction system of the heart. Cardiovasc. Res., 62, 489-499.
52. Moorman, A.F.M., Houweling, A.C., de Boer, P.A.J. and Christoffels, V.M. (2001) Sensitive nonradioactive detection of mRNA in tissue sections: novel application of the whole-mount in situ hybridization protocol. J. Histochem. Cytochem., 49, 1-8.
53. Chapman, D.L., Garvey, N., Hancock, S., Alexiou, M., Agulnik, S.I., Gibson-Brown, J.J., Cebra-Thomas, J., Bollag, R.J., Silver, L.M. and Papaioannou, V.E. (1996) Expression of the T-box family genes, Tbx1-Tbx5, during early mouse development. Dev. Dyn., 206, 379-390.
54. Kelly, R.G. and Papaioannou, V.E. (2007) Visualization of outflow tract development in the absence of Tbx1 using an FgF10 enhancer trap transgene. Dev. Dyn., 236, 821-828.
55. Soufan, A.T., van den Berg, G., Moerland, P.D., Massink, M.M.G., van den Hoff, M.J.B., Moorman, A.F.M. and Ruijter, J.M. (2007) Three-dimensional measurement and visualization of morphogenesis applied to cardiac embryology. J. Microsc., 225, 269-274.