Tbx1 regulates oral epithelial adhesion and palatal development

Human Molecular Genetics

Volumn 21, Issue 11, 2012, Pages 2524-2537

  Funato, Noriko ^a,b   Nakamura, Masataka ^a   Richardson, James A ^b,c   Srivastava, Deepak ^d   Yanagisawa, Hiromi ^b  

^a TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^c UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

T BOX TRANSCRIPTION FACTOR; T BOX TRANSCRIPTION FACTOR 1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL ADHESION; CELL CYCLE ARREST; CELL DIFFERENTIATION; CELL GROWTH; CLEFT PALATE; CONTROLLED STUDY; DIGEORGE SYNDROME; EMBRYO; GENE DELETION; GENE DISRUPTION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; KERATINOCYTE; MANDIBLE; MOUSE; MOUTH MUCOSA; NONHUMAN; PALATE; PRIORITY JOURNAL;

ANIMALS; CELL ADHESION; CELL DIFFERENTIATION; CELL PROLIFERATION; CLEFT PALATE; EMBRYO, MAMMALIAN; EPITHELIUM; KERATINOCYTES; MICE; MICE, TRANSGENIC; MOUTH; T-BOX DOMAIN PROTEINS; TRANSFECTION;

MAMMALIA; MUS;

EID: 84861125165     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/dds071     Document Type: Article

References (70)

1. 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.
2. 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 haploinsufficiency in the DiGeorge syndrome region causes aortic arch defects in mice. Nature, 410, 97-101.
3. 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.
4. Scambler, P.J. (2000) The 22q11 deletion syndromes. Hum. Mol. Genet., 9, 2421-2426.
5. Gorlin, R.J., Cohen, M.M.J. and Hennekam, R.C.M. (2001) Syndromes of the Head and the Neck. Oxford University Press, New York, NY, pp. 850-853.
6. Oberoi, S. and Vargervik, K. (2005) Velocardiofacial syndrome with single central incisor. Am. J. Med. Genet. A, 132A, 194-197.
7. Yagi, H., Furutani, Y., Hamada, H., Sasaki, T., Asakawa, S., Minoshima, S., Ichida, F., Joo, K., Kimura, M., Imamura, S. et al. (2003) Role of TBX1 in human del22q11.2 syndrome. Lancet, 362, 1366-1373.
8. Osoegawa, K., Vessere, G.M., Utami, K.H., Mansilla, M.A., Johnson, M.K., Riley, B.M., L'Heureux, J., Pfundt, R., Staaf, J., van der Vliet, W.A. et al. (2008) Identification of novel candidate genes associated with cleft lip and palate using array comparative genomic hybridisation. J. Med. Genet., 45, 81-86.
9. Hu, T., Yamagishi, H., Maeda, J., McAnally, J., Yamagishi, C. and 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.
10. Tolarova, M.M. and Cervenka, J. (1998) Classification and birth prevalence of orofacial clefts. Am. J. Med. Genet., 75, 126-137.
11. Murray, J.C. (2002) Gene/environment causes of cleft lip and/or palate. Clin. Genet., 61, 248-256.
12. Jones, M.C. (1988) Etiology of facial clefts: prospective evaluation of 428 patients. Cleft Palate J., 25, 16-20.
13. van den Boogaard, M.J., Dorland, M., Beemer, F.A. and van Amstel, H.K. (2000) MSX1 mutation is associated with orofacial clefting and tooth agenesis in humans. Nat. Genet., 24, 342-343.
14. van Bokhoven, H., Hamel, B.C., Bamshad, M., Sangiorgi, E., Gurrieri, F., Duijf, P.H., Vanmolkot, K.R., van Beusekom, E., van Beersum, S.E., Celli, J. et al. (2001) p63 gene mutations in EEC syndrome, limb-mammary syndrome, and isolated split hand-split foot malformation suggest a genotype-phenotype correlation. Am. J. Hum. Genet., 69, 481-492.
15. Suzuki, K., Hu, D., Bustos, T., Zlotogora, J., Richieri-Costa, A., Helms, J.A. and Spritz, R.A. (2000) Mutations of PVRL1, encoding a cell-cell adhesion molecule/herpesvirus receptor, in cleft lip/palate-ectodermal dysplasia. Nat. Genet., 25, 427-430.
16. Braybrook, C., Doudney, K., Marcano, A.C., Arnason, A., Bjornsson, A., Patton, M.A., Goodfellow, P.J., Moore, G.E. and Stanier, P. (2001) The T-box transcription factor gene TBX22 is mutated in X-linked cleft palate and ankyloglossia. Nat. Genet., 29, 179-183.
17. Sozen, M.A., Suzuki, K., Tolarova, M.M., Bustos, T., Fernandez Iglesias, J.E. and Spritz, R.A. (2001) Mutation of PVRL1 is associated with sporadic, non-syndromic cleft lip/palate in northern Venezuela. Nat. Genet., 29, 141-142.
18. Kondo, S., Schutte, B.C., Richardson, R.J., Bjork, B.C., Knight, A.S., Watanabe, Y., Howard, E., de Lima, R.L., Daack-Hirsch, S., Sander, A. et al. (2002) Mutations in IRF6 cause Van der Woude and popliteal pterygium syndromes. Nat. Genet., 32, 285-289.
19. Jezewski, P.A., Vieira, A.R., Nishimura, C., Ludwig, B., Johnson, M., O'Brien, S.E., Daack-Hirsch, S., Schultz, R.E., Weber, A., Nepomucena, B. et al. (2003) Complete sequencing shows a role for MSX1 in non-syndromic cleft lip and palate. J. Med. Genet., 40, 399-407.
20. Schupbach, P.M., Chamberlain, J.G. and Schroeder, H.E. (1983) Development of the secondary palate in the rat: a scanning electron microscopic study. J. Craniofac. Genet. Dev. Biol., 3, 159-177.
21. Gritli-Linde, A. (2007) Molecular control of secondary palate development. Dev. Biol., 301, 309-326.
22. Thyagarajan, T., Totey, S., Danton, M.J. and Kulkarni, A.B. (2003) Genetically altered mouse models: the good, the bad, and the ugly. Crit. Rev. Oral Biol. Med., 14, 154-174.
23. Johnston, M.C. and Bronsky, P.T. (1995) Prenatal craniofacial development: new insights on normal and abnormal mechanisms. Crit. Rev. Oral Biol. Med., 6, 368-422.
24. Ferguson, M.W. (1988) Palate development. Development, 103 (suppl.), 41-60.
25. Greene, R.M. and Pratt, R.M. (1976) Developmental aspects of secondary palate formation. J. Embryol. Exp. Morphol., 36, 225-245.
26. Richardson, R.J., Dixon, J., Malhotra, S., Hardman, M.J., Knowles, L., Boot-Handford, R.P., Shore, P., Whitmarsh, A. and Dixon, M.J. (2006) Irf6 is a key determinant of the keratinocyte proliferation-differentiation switch. Nat. Genet., 38, 1329-1334.
27. Chai, Y. and Maxson, R.E. Jr (2006) Recent advances in craniofacial morphogenesis. Dev. Dyn., 235, 2353-2375.
28. 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.
29. Zoupa, M., Seppala, M., Mitsiadis, T. and Cobourne, M.T. (2006) Tbx1 is expressed at multiple sites of epithelial-mesenchymal interaction during early development of the facial complex. Int. J. Dev. Biol., 50, 504-510.
30. Dassule, H.R., Lewis, P., Bei, M., Maas, R. and McMahon, A.P. (2000) Sonic hedgehog regulates growth and morphogenesis of the tooth. Development, 127, 4775-4785.
31. Soriano, P. (1999) Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat. Genet., 21, 70-71.
32. Ittner, L.M., Wurdak, H., Schwerdtfeger, K., Kunz, T., Ille, F., Leveen, P., Hjalt, T.A., Suter, U., Karlsson, S., Hafezi, F. et al. (2005) Compound developmental eye disorders following inactivation of TGFbeta signaling in neural-crest stem cells. J. Biol., 4, 11.
33. Zhang, Z., Huynh, T. and Baldini, A. (2006) Mesodermal expression of Tbx1 is necessary and sufficient for pharyngeal arch and cardiac outflow tract development. Development, 133, 3587-3595.
34. Fuchs, E. and Raghavan, S. (2002) Getting under the skin of epidermal morphogenesis. Nat. Rev. Genet., 3, 199-209.
35. Watt, F.M. (2001) Stem cell fate and patterning in mammalian epidermis. Curr. Opin. Genet. Dev., 11, 410-417.
36. Goudy, S., Law, A., Sanchez, G., Baldwin, H.S. and Brown, C. (2010) Tbx1 is necessary for palatal elongation and elevation. Mech. Dev., 127, 292-300.
37. Jiang, R., Lan, Y., Chapman, H.D., Shawber, C., Norton, C.R., Serreze, D.V., Weinmaster, G. and Gridley, T. (1998) Defects in limb, craniofacial, and thymic development in Jagged2 mutant mice. Genes Dev., 12, 1046-1057.
38. Alappat, S.R., Zhang, Z., Suzuki, K., Zhang, X., Liu, H., Jiang, R., Yamada, G. and Chen, Y. (2005) The cellular and molecular etiology of the cleft secondary palate in Fgf10 mutant mice. Dev. Biol., 277, 102-113.
39. Poliakov, A., Cotrina, M. and Wilkinson, D.G. (2004) Diverse roles of Eph receptors and ephrins in the regulation of cell migration and tissue assembly. Dev. Cell, 7, 465-480.
40. Halford, M.M., Armes, J., Buchert, M., Meskenaite, V., Grail, D., Hibbs, M.L., Wilks, A.F., Farlie, P.G., Newgreen, D.F., Hovens, C.M. et al. (2000) Ryk-deficient mice exhibit craniofacial defects associated with perturbed Eph receptor crosstalk. Nat. Genet., 25, 414-418.
41. Twigg, S.R., Kan, R., Babbs, C., Bochukova, E.G., Robertson, S.P., Wall, S.A., Morriss-Kay, G.M. and Wilkie, A.O. (2004) Mutations of ephrin-B1 (EFNB1), a marker of tissue boundary formation, cause craniofrontonasal syndrome. Proc. Natl Acad. Sci. USA, 101, 8652-8657.
42. Orioli, D., Henkemeyer, M., Lemke, G., Klein, R. and Pawson, T. (1996) Sek4 and Nuk receptors cooperate in guidance of commissural axons and in palate formation. EMBO J., 15, 6035-6049.
43. Compagni, A., Logan, M., Klein, R. and Adams, R.H. (2003) Control of skeletal patterning by ephrinB1-EphB interactions. Dev. Cell, 5, 217-230.
44. Liu, W., Sun, X., Braut, A., Mishina, Y., Behringer, R.R., Mina, M. and Martin, J.F. (2005) Distinct functions for Bmp signaling in lip and palate fusion in mice. Development, 132, 1453-1461.
45. Fulcoli, F.G., Huynh, T., Scambler, P.J. and Baldini, A. (2009) Tbx1 regulates the BMP-Smad1 pathway in a transcription independent manner. PLoS One, 4, e6049.
46. Tucker, A.S., Matthews, K.L. and Sharpe, P.T. (1998) Transformation of tooth type induced by inhibition of BMP signaling. Science, 282, 1136-1138.
47. Peters, H., Neubuser, A., Kratochwil, K. and Balling, R. (1998) Pax9-deficient mice lack pharyngeal pouch derivatives and teeth and exhibit craniofacial and limb abnormalities. Genes Dev., 12, 2735-2747.
48. Tissier-Seta, J.P., Mucchielli, M.L., Mark, M., Mattei, M.G., Goridis, C. and Brunet, J.F. (1995) Barx1, a new mouse homeodomain transcription factor expressed in cranio-facial ectomesenchyme and the stomach. Mech. Dev., 51, 3-15.
49. Ivins, S., Lammerts van Beuren, K., Roberts, C., James, C., Lindsay, E., Baldini, A., Ataliotis, P. and Scambler, P.J. (2005) Microarray analysis detects differentially expressed genes in the pharyngeal region of mice lacking Tbx1. Dev. Biol., 285, 554-569.
50. Aggarwal, V.S., Carpenter, C., Freyer, L., Liao, J., Petti, M. and Morrow, B.E. (2011) Mesodermal Tbx1 is required for patterning the proximal mandible in mice. Dev. Biol., 344, 669-681.
51. 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.
52. Lu, M.F., Pressman, C., Dyer, R., Johnson, R.L. and Martin, J.F. (1999) Function of Rieger syndrome gene in left-right asymmetry and craniofacial development. Nature, 401, 276-278.
53. Ming, J.E., Kaupas, M.E., Roessler, E., Brunner, H.G., Golabi, M., Tekin, M., Stratton, R.F., Sujansky, E., Bale, S.J. and Muenke, M. (2002) Mutations in PATCHED-1, the receptor for SONIC HEDGEHOG, are associated with holoprosencephaly. Hum. Genet., 110, 297-301.
54. Richardson, R.J., Dixon, J., Jiang, R. and Dixon, M.J. (2009) Integration of IRF6 and Jagged2 signalling is essential for controlling palatal adhesion and fusion competence. Hum. Mol. Genet., 18, 2632-2642.
55. Rice, R., Spencer-Dene, B., Connor, E.C., Gritli-Linde, A., McMahon, A.P., Dickson, C., Thesleff, I. and Rice, D.P. (2004) Disruption of Fgf10/Fgfr2b-coordinated epithelial-mesenchymal interactions causes cleft palate. J. Clin. Invest., 113, 1692-1700.
56. Casey, L.M., Lan, Y., Cho, E.S., Maltby, K.M., Gridley, T. and Jiang, R. (2006) Jag2-Notch1 signaling regulates oral epithelial differentiation and palate development. Dev. Dyn., 235, 1830-1844.
57. Arnold, J.S., Werling, U., Braunstein, E.M., Liao, J., Nowotschin, S., Edelmann, W., Hebert, J.M. and Morrow, B.E. (2006) Inactivation of Tbx1 in the pharyngeal endoderm results in 22q11DS malformations. Development, 133, 977-987.
58. 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.
59. Trempus, C.S., Wei, S.J., Humble, M.M., Dang, H., Bortner, C.D., Sifre, M.I., Kissling, G.E., Sunman, J.A., Akiyama, S.K., Roberts, J.D. et al. (2011) A novel role for the T-box transcription factor Tbx1 as a negative regulator of tumor cell growth in mice. Mol. Carcinog., 50, 981-991.
60. Jugessur, A. and Murray, J.C. (2005) Orofacial clefting: recent insights into a complex trait. Curr. Opin. Genet. Dev., 15, 270-278.
61. Marcano, A.C., Doudney, K., Braybrook, C., Squires, R., Patton, M.A., Lees, M.M., Richieri-Costa, A., Lidral, A.C., Murray, J.C., Moore, G.E. et al. (2004) TBX22 mutations are a frequent cause of cleft palate. J. Med. Genet., 41, 68-74.
62. Tallquist, M.D. and Soriano, P. (2000) Epiblast-restricted Cre expression in MORE mice: a tool to distinguish embryonic vs. extra-embryonic gene function. Genesis, 26, 113-115.
63. Danielian, P.S., Muccino, D., Rowitch, D.H., Michael, S.K. and McMahon, A.P. (1998) Modification of gene activity in mouse embryos in utero by a tamoxifen-inducible form of Cre recombinase. Curr. Biol., 8, 1323-1326.
64. McLeod, M.J. (1980) Differential staining of cartilage and bone in whole mouse fetuses by alcian blue and alizarin red S. Teratology, 22, 299-301.
65. Shelton, J.M., Lee, M.H., Richardson, J.A. and Patel, S.B. (2000) Microsomal triglyceride transfer protein expression during mouse development. J. Lipid Res., 41, 532-537.
66. Neubuser, A., Koseki, H. and Balling, R. (1995) Characterization and developmental expression of Pax9, a paired-box-containing gene related to Pax1. Dev. Biol., 170, 701-716.
67. Meyers, E.N. and Martin, G.R. (1999) Differences in left-right axis pathways in mouse and chick: functions of FGF8 and SHH. Science, 285, 403-406.
68. Goodrich, L.V., Johnson, R.L., Milenkovic, L., McMahon, J.A. and Scott, M.P. (1996) Conservation of the hedgehog/patched signaling pathway from flies to mice: induction of a mouse patched gene by Hedgehog. Genes Dev., 10, 301-312.
69. Thomas, T., Kurihara, H., Yamagishi, H., Kurihara, Y., Yazaki, Y., Olson, E.N. and Srivastava, D. (1998) A signaling cascade involving endothelin-1, dHAND and msx1 regulates development of neural-crest-derived branchial arch mesenchyme. Development, 125, 3005-3014.
70. Funato, N., Ohtani, K., Ohyama, K., Kuroda, T. and Nakamura, M. (2001) Common regulation of growth arrest and differentiation of osteoblasts by helix-loop-helix factors. Mol. Cell. Biol., 21, 7416-7428.