Tbx1 regulates progenitor cell proliferation in the dental epithelium by modulating Pitx2 activation of p21

Developmental Biology

Volumn 347, Issue 2, 2010, Pages 289-300

  Cao, Huojun ^a   Florez, Sergio ^a   Amen, Melanie ^a   Huynh, Tuong ^a   Skobe, Ziedonis ^b   Baldini, Antonio ^a,c   Amendt, Brad A ^a  

^a UNIVERSITY OF TEXAS   (United States)

^b FORSYTH INSTITUTE   (United States)

^c INSTITUTE OF GENETICS AND BIOPHYSICS ADRIANO BUZZATI TRAVERSO   (Italy)

Author keywords

DiGeorge syndrome; P21; PITX2; Tbx1; Tooth development

Indexed keywords

BETA GALACTOSIDASE; LYMPHOID ENHANCER FACTOR 1; PROTEIN P21; PROTEIN TBX1; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR PITX2; UNCLASSIFIED DRUG; CDKN1A PROTEIN, MOUSE; CYCLIN DEPENDENT KINASE INHIBITOR 1A; HOMEODOMAIN PROTEIN; PRIMER DNA; T BOX TRANSCRIPTION FACTOR; TBX1 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL PROLIFERATION; CONTROLLED STUDY; EMBRYO; EPITHELIUM; FIBROBLAST; GENE INTERACTION; HETEROZYGOSITY; MOLECULAR MECHANICS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN INTERACTION; REGULATORY MECHANISM; STEM CELL; TOOTH DEVELOPMENT; ANIMAL; C57BL MOUSE; CYTOLOGY; DEFICIENCY; DIGEORGE SYNDROME; DISEASE MODEL; EMBRYOLOGY; EMBRYONIC STEM CELL; FEMALE; GENE EXPRESSION REGULATION; GENETICS; HUMAN; KNOCKOUT MOUSE; MALE; METABOLISM; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; PREGNANCY; SIGNAL TRANSDUCTION; TOOTH; TOOTH MALFORMATION; TRANSCRIPTION INITIATION; TRANSGENIC MOUSE;

MUS; MUS MUSCULUS;

ANIMALS; BASE SEQUENCE; CELL PROLIFERATION; CYCLIN-DEPENDENT KINASE INHIBITOR P21; DIGEORGE SYNDROME; DISEASE MODELS, ANIMAL; DNA PRIMERS; EMBRYONIC STEM CELLS; EPITHELIUM; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HOMEODOMAIN PROTEINS; HUMANS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; ODONTOGENESIS; PREGNANCY; SIGNAL TRANSDUCTION; T-BOX DOMAIN PROTEINS; TOOTH; TOOTH ABNORMALITIES; TRANSCRIPTION FACTORS; TRANSCRIPTIONAL ACTIVATION;

EID: 77957929950     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2010.08.031     Document Type: Article

References (54)

1. Alappat S., Zhang Z., Suzuki K., Zhang X., Liu H., Jiang R., Yamada G., Chen Y. The cellular and molecular etiology of the cleft secondary palate in Fgf10 mutant mice. Dev. Biol. 2005, 277:102-113.
2. Amen M., Liu X., Vadlamudi U., Elizondo G., Diamond E., Engelhardt J.F., Amendt B.A. PITX2 and β-catenin interactions regulate Lef-1 isoform expression. Mol. Cell. Biol. 2007, 27:7560-7573.
3. Amen M., Espinoza H.M., Cox C., Liang X., Wang J., Link T.M., Brennan R.G., Martin J.F., Amendt B.A. Chromatin-associated HMG-17 is a major regulator of homeodomain transcription factor activity modulated by Wnt/beta-catenin signaling. Nuc. Acids Res. 2008, 36:462-476.
4. Amendt B.A., Sutherland L.B., Russo A.F. Multifunctional role of the Pitx2 homeodomain protein C-terminal tail. Mol. Cel. Biol. 1999, 19:7001-7010.
5. Bei M., Kratochwil K., Maas R.L. BMP4 rescues a non-cell-autonomous function of Msx1 in tooth development. Development 2000, 127:4711-4718.
6. Berry F.B., Lines M.A., Oas J.M., Footz T., Underhill D.A., Gage P.J., Walter M.A. Functional interactions between FOXC1 and PITX2 underlie the sensitivity to FOXC1 gene dose in Axenfeld-Rieger syndrome and anterior segment dysgenesis. Hum. Mol. Genet. 2006, 15:905-919.
7. Bloch-Zupan A., Leveilard T., Gorry P., Fausser J.L., Ruch J.V. Expression of p21 (WAF1/CIP1) during mouse odontogenesis. Eur. J. Oral Sci. 1998, 106:104-111.
8. Bollag R.J., Siegfried Z., Cebra-Thomas J.A., Garvey N., Davison E.M., Silver L.M. An ancient family of embryonically expressed mouse genes sharing a conserved protein motif with the T locus. Nat. Genet. 1994, 7:383-389.
9. Cai J., Cho S.-W., Kim J.-Y., Lee M.-J., Cha Y.-G., Jung H.-S. Patterning the size and number of tooth and its cusps. Dev. Biol. 2007, 304:499-507.
10. Caton J., Luder H.-U., Zoupa M., Bradman M., Bluteau G., Tucker A.S., Klein O., Mitsiadis T.A. Enamel-free teeth: Tbx1 deletion affects amelogenesis in rodent incisors. Dev. Biol. 2009, 328:493-505.
11. Chen L.S., Couwenhoven R.I., Hsu D., Luo W., Snead M.L. Maintenance of amelogenin gene expression by transformed epithelial cells of mouse enamel organ. Archs oral Biol. 1992, 37:771-778.
12. Cox C.J., Espinoza H.M., McWilliams B., Chappell K., Morton L., Hjalt T.A., Semina E.V., Amendt B.A. Differential regulation of gene expression by PITX2 isoforms. J. Biol. Chem. 2002, 277:25001-25010.
13. Datto M.B., Li Y., Panus J.F., Howe D.J., Xiong Y., Wang X.-F. Transforming growth factor beta induces the cyclin-dependent kinase inhibitor p21 through a p53 independent mechanism. Proc. Natl Acad. Sci. USA 1995, 92:5545-5549.
14. Diamond E., Amen M., Hu Q., Espinoza H.M., Amendt B.A. Functional interactions between Dlx2 and lymphoid enhancer factor regulate Msx2. Nuc. Acids Res. 2006, 34:5951-5965.
15. Dodson W.E., Alexander D., Al-Aish M., De La Cruz F. The DiGeorge syndrome. Lancet 1969, 15:574-575.
16. Espinoza H.M., Ganga M., Vadlamudi U., Martin D.M., Brooks B.P., Semina E.V., Murray J.C., Amendt B.A. Protein kinase C phosphorylation modulates N- and C-terminal regulatory activities of the PITX2 homeodomain protein. Biochemistry 2005, 44:3942-3954.
17. Fukui N., Amano A., Akiyama S., Daikoku H., Wakisaka S., Morisaki I. Oral findings in DiGeorge syndrome. Oral Surg. Oral Med. Oral Pathol. Oral adiol. Endod. 2000, 89:208-215.
18. Goldberg R., Motzkin B., Marion R., Scambler P.J., Shprintzen R.J. Velo-cardio-facial syndrome: a review of 120 patients. Am. J. Med. Genet. 1993, 45:313-319.
19. Green P.D., Hjalt T.A., Kirk D.E., Sutherland L.B., Thomas B.L., Sharpe P.T., Snead M.L., Murray J.C., Russo A.F., Amendt B.A. Antagonistic regulation of Dlx2 expression by PITX2 and Msx2: implications for tooth development. Gene Expr. 2001, 9:265-281.
20. Harada H., Ohshima H. New perspectives on tooth development and the dental stem cell niche. Arch. Histol. Cytol. 2004, 67:1-11.
21. Harada H., Kettumen P., Jung H.-S., Mustonen T., Wang Y.A., Thesleff I. Localization of putative stem cells in dental epithelium and their association with notch and FGF signaling. J. Cell Biol. 1999, 147:105-120.
22. Harada H., Toyono T., Toyoshima K., Yamasaki M., Itoh N., Kato S., Sekine K., Ohuchi H. FGF10 maintains stem cell compartment in developing mouse incisors. Development 2002, 129:1533-1541.
23. Hjalt T.A., Semina E.V. Current molecular understanding of Axenfeld-Rieger syndrome. Expert Rev. Mol. Med. 2005, 7:1-17.
24. Hjalt T.A., Semina E.V., Amendt B.A., Murray J.C. The Pitx2 protein in mouse development. Dev. Dyn. 2000, 218:195-200.
25. Jernvall J., Kettunen P., Karavanova I., Martin L.B., Thesleff I. Evidence for the role of the enamel knot as a control center in mammalian tooth cusp formation: non-dividing cells express growth stimulating Fgf-4 gene. Int. J. Dev. Biol. 1994, 38:463-469.
26. Jernvall J., Aberg T., Kettunen P., Keranen S., Thesleff I. The life history of an embryonic signaling center: BMP-4 induces p21 and is associated with apoptosis in the mouse tooth enamel knot. Development 1998, 125:161-169.
27. Jerome L.A., Papaioannou V.E. DiGeorge syndrome phenotype in mice mutant for the T-box gene, Tbx1. Nat. Genet. 2001, 27:286-291.
28. Kispert A. The Brachyury protein: a T-domain transcription factor. Semin. Dev. Biol. 1995, 6:395-403.
29. Lesot H., Lisi S., Peterkova R., Peterka M., Mitolo V., Ruch J.V. Epigenetic signals during odontoblast differentiation. Adv. Dent. Res. 2001, 15:8-13.
30. Lindsay E.A., Botta A., Jurecic V., Carattini-Rivera S., Cheah Y.C., Rosenblatt H.M., Bradley A., Baldini A. Congenital heart disease in mice deficient for the DiGeorge syndrome region. Nature 1999, 401:379-383.
31. Lindsay E.A., Vitelli F., Su H., Morishima M., Huynh T., Pramparo T., Jurecic V., Ogunrinu G., Sutherland H.F., Scambler P.J., Bradley A., Baldini A. Tbx1 haploinsufficiency identified by functional scanning of the DiGeorge syndrome region is the cause of aortic arch defects in mice. Nature 2001, 401:97-101.
32. Lu M., Pressman C., Dyer R., Johnson R.L., Martin J.F. Function of Rieger syndrome gene in left-right asymmetry and craniofacial development. Nature 1999, 401:276-278.
33. 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., Tokooya K., Jore B.S., Lopez M., Pandita R.K., Lia M., Carrion D., Xu H., Schorle H., Kobler J.B., Scambler P., Wynshaw-Boris A., Skoultchi A.I., Morrow B.E., Kucherlapati R. TBX1 is responsible for cardiovascular defects in velo-cardio-facial/DiGeorge syndrome. Cell 2001, 104:619-629.
34. Mitsiadis T.A., Tucker A.S., De Bari C., Cobourne M.T., Rice D.P.C. A regulatory relationship between Tbx1 and FGF signaling during tooth morphogenesis and ameloblast lineage determination. Dev. Biol. 2008, 320:39-48.
35. Naiche L.A., Harrelson Z., Kelly R.G., Papaioannou V.E. T-Box genes in vertebrate development. Annu. Rev. Genet. 2005, 39:219-239.
36. Nakano K., Mizuno T., Sowa Y., Orita T., Yoshino T., Okuyama Y., Fujita T., Ohtani-Fujita N., Matsukawa Y., Tokino T., Yamagrishi H., Oka T., Nomura H., Sakai T. Butyrate activates the WAF1/Cip1 gene promoter through Sp1 sites in a p53-negative human colon cancer cell line. J. Biol. Chem. 1997, 272:22199-22206.
37. Paylor R., Glaser B., Mupo A., Atallotis P., Spencer C., Sobotka A., Sparks C., Choi C.H., Oghalai J., Curran S., Murphy K.C., Monks S., Williams N., O'Donovan M.C., Owen M.J., Scambler P.J., Lindsay E. Tbx1 haploinsufficiency is linked to behavioral disorders in mice and humans: implications for 22q11 deletion syndrome. Proc. Natl Acad. Sci. USA 2006, 103:7729-7734.
38. Peters H., Balling R. Teeth, where and how to make them. TIG 1999, 15:59-64.
39. Scambler P.J. The 22q11 deletion syndromes. Hum. Mol. Genet. 2000, 16:2421-2426.
40. Shprintzen R.J., Goldberg R.B., Lewin M.L., Sidoti E.J., Berkman M.D., Argamaso R.V., Young D. A new syndrome involving cleft palate, cardiac anomalies, typical facies, and learning disabilities: velo-cardio-facial syndrome. Cleft Palate J. 1978, 15:56-62.
41. Stennard F.A., Costa M.W., Elliott D.A., Rankin S., Haast S.J., Lai D., McDonald L.P.A., Niederreither K., Dolle P., Bruneau B.G., Zorn A.M., Harvey R.P. Cardiac T-box factor Tbx20 directly interacts with Nkx2-5, GATA4, and GATA5 in regulation of gene expression in the developing heart. Dev. Biol. 2003, 262:206-224.
42. Thesleff I. Epithelial-mesenchymal signalling regulating tooth morphogenesis. J. Cell Sci. 2003, 116:1647-1648.
43. Thesleff I., Sharpe P. Signalling networks regulating dental development. Mech. Dev. 1997, 67:111-123.
44. Thesleff I., Keranen S., Jernvall J. Enamel knots as signaling centers linking tooth morphogenesis and odontoblast differentiation. Adv. Dent. Res. 2001, 15:14-18.
45. Tucker A., Sharpe P. The cutting-edge of mammalian development; how the embryo makes teeth. Nat. Rev. Genet. 2004, 5:499-508.
46. Vadlamudi U., Espinoza H.M., Ganga M., Martin D.M., Liu X., Engelhardt J.F., Amendt B.A. PITX2, β-catenin, and LEF-1 interact to synergistically regulate the LEF-1 promoter. J. Cell Sci. 2005, 118:1129-1137.
47. Venugopalan S.R., Amen M.A., Wang J., Wong L., Cavender A.C., D'Souza R.N., Akerlund M., Brody S.L., Hjalt T.A., Amendt B.A. Novel expression and transcriptional regulation of FoxJ1 during oro-facial morphogenesis. Hum. Mol. Genet. 2008, 17:3643-3654.
48. Vitelli F., Taddei I., Morishima M., Meyers E.N., Lindsey E.A., Baldini A. A genetic link between Tbx1 and fibroblast growth factor signaling. Development 2002, 129:4605-4611.
49. Wang X.-P., O'Connell D.J., Lund J.J., Saadi I., Kuraguchi M., Turbe-Doan A., Cavallesco R., Kim H., Park P.J., Harada H., Kucherlapati R., Maas R.L. Apc inhibition of Wnt signaling regulates supernumerary tooth formation during embryogenesis and throughout adulthood. Development 2009, 136:1939-1949.
50. Weber A., Marquardt J., Elzi D., Forster N., Starke S., Glaum A., Yamada D., Defossez P.-A., Delrow J., Eisenman R.N., Christiansen H., Eilers M. Zbtb4 represses transcription of P21CIP1 and controls the cellular response to p53 activation. EMBO J. 2008, 27:1563-1574.
51. Xu H., Morishima M., Wylie J.N., Schwartz R.J., Bruneau B.G., Lindsay E.A., Baldini A. Tbx1 has a dual role in the morphogenesis of the cardiac outflow tract. Development 2004, 131:3217-3227.
52. 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. Role of TBX1 in human del22q11.2 syndrome. Lancet 2003, 362:1366-1373.
53. Zhang Z., Huynh T., Baldini A. Mesodermal expression of Tbx1 is necessary and sufficient for pharyngeal arch and cardiac outflow tract development. Development 2006, 133:3587-3595.
54. Zoupa M., Seppala M., Mitsiadis T., Cobourne M.T. Tbx1 is expressed at multiple sites of epithelial-mesenchymal interaction during early development of the facial complex. Int. J. Dev. Biol. 2006, 50:505-510.