A model for the molecular underpinnings of tooth defects in axenfeld-rieger syndrome

Human Molecular Genetics

Volumn 23, Issue 1, 2014, Pages 194-208

  Li, Xiao ^a   Venugopalan, Shankar R ^a   Cao, Huojun ^a   Pinho, Flavia O ^a   Paine, Michael L ^b   Snead, Malcolm L ^b   Semina, Elena V ^c   Amendt, Brad A ^a  

^a UNIVERSITY OF IOWA   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^c MEDICAL COLLEGE OF WISCONSIN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMELOGENIN; HIGH MOBILITY GROUP N2 PROTEIN; TRANSCRIPTION FACTOR PITX2;

ARTICLE; AUTOSOMAL DOMINANT DISORDER; AXENFELD RIEGER SYNDROME; ENAMEL HYPOPLASIA; GENE EXPRESSION; GENE EXPRESSION REGULATION; MISSENSE MUTATION; PRIORITY JOURNAL; PROMOTER REGION; SEQUENCE ANALYSIS; TOOTH DEVELOPMENT; TOOTH MALFORMATION; TRANSGENIC MOUSE;

AMELOGENIN; ANIMALS; ANTERIOR EYE SEGMENT; CELL LINE; DENTAL ENAMEL; DISEASE MODELS, ANIMAL; EMBRYO, MAMMALIAN; EYE ABNORMALITIES; GENE EXPRESSION REGULATION; HMGN2 PROTEIN; HOMEODOMAIN PROTEINS; HUMANS; INCISOR; MICE; MICE, KNOCKOUT; MUTATION, MISSENSE; PROMOTER REGIONS, GENETIC; TRANSCRIPTION FACTORS;

EID: 84890369688     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddt411     Document Type: Article

References (75)

1. Shields, M.B., Buckley, E., Klintworth, G.K. and Thresher, R. (1985) Axenfeld-Rieger syndrome. A spectrum of developmental disorders. Survey Ophthal., 29, 387-409.
2. Amendt, B.A. (2005) The Molecular Mechanisms of Axenfeld-Rieger Syndrome. Springer, New York, NY, USA.
3. Amendt, B., Semina, E. and Alward, W. (2000) Rieger syndrome: a clinical, molecular, and biochemical analysis. Cell Mol. Life Sci., 57, 1652-1666.
4. Lines, M.A., Kozlowski, K. and Walter, M.A. (2002) Molecular genetics of Axenfeld-Rieger malformations. Hum. Mol. Genet., 11, 1177-1187.
5. Fitch, N. and Kaback, M. (1978) The Axenfeld syndrome and the Rieger syndrome. J. Med. Genet., 15, 30-34.
6. Semina, E.V., Reiter, R., Leysens, N.J., Alward, W.L.M., Small, K.W., Datson, N.A., Siegel-Bartelt, J., Bierke-Nelson, D., Bitoun, P. and Zabel, B.U. (1996) Cloning and characterization of a novel bicoid-related homeobox transcription factor gene, RIEG, involved in Rieger syndrome. Nat. Genet., 14, 392-399.
7. O'Dwyer, E. and Jones, D. (2005) Dental anomalies in Axenfeld-Rieger syndrome. Int. J. Paediat. Dent., 15, 459-463.
8. Gadhia, K., McDonald, S., Arkutu, N. and Malik, K. (2012) Amelogenesis imperfecta: an introduction. Br. Dent. J., 212, 377-379.
9. Fincham, A., Moradian-Oldak, J. and Simmer, J. (1999) The structural biology of the developing dental enamel matrix. J. Struct. Biol., 126, 270- 299.
10. Snead, M.L., Lau, E.C., Zeichner-David, M., Fincham, A.G., Woo, S.L. and Slavkin, H.C. (1985) DNA Sequence for cloned cDNA for murine amelogenin reveal the amino acid sequence for enamel-specific protein. Biochem. Biophys. Res. Comm., 129, 812-818.
11. Nakahori, Y., Takenaka, O. and Nakagome, Y. (1991) A human XY homologous region encodes 'amelogenin'. Genomics, 9, 264-269.
12. Snead, M.L. (2003) Amelogenin protein exhibits a modular design: implications for form and function. Connect. Tissue Res., 44, 47-51.
13. Dressler, S., Meyer-Marcotty, P., Weisschuh, N., Jablonski-Momeni, A., Pieper, K., Gramer, G. and Gramer, E. (2010) Dental and craniofacial anomalies associated with Axenfeld-Rieger syndrome with PITX2 mutation. Case Rep. Med., 2010, http://dx.doi.org/10.1155/2010/621984.
14. Mears, A.J., Mirzayans, F., Gould, D.B., Pearce, W.G. and Walter, M.A. (1996) Autosomal dominant iridogoniodysgenesis anomaly maps to 6p25. Am. J. Hum. Genet., 59, 1321.
15. Nishimura, D.Y., Swiderski, R.E., Alward, W.L., Searby, C.C., Patil, S.R., Bennet, S.R., Kanis, A.B., Gastier, J.M., Stone, E.M. and Sheffield, V.C. (1998) The forkhead transcription factor gene FKHL7 is responsible for glaucoma phenotypes which map to 6p25. Nat. Genet., 19, 140-147.
16. Murray, J.C., Bennett, S.R., Kwitek, A.E., Small, K.W., Schinzel, A., Alward, W.L., Weber, J.L., Bell, G.I. and Buetow, K.H. (1992) Linkage of Rieger syndrome to the region of the epidermal growth factor gene on chromosome 4. Nat. Genet., 2, 46-49.
17. Datson, N.A., Semina, E.,VanStaalduinen, A., Dauwerse, H.G., Meershoek, E.J., Heus, J.J., Frants, R.R., Den Dunnen, J., Murray, J.C. and Van Ommen, G. (1996) Closing in on the Rieger syndrome gene on 4q25: mapping translocation breakpoints within a 50-kb region. Am. J. Hum. Genet., 59, 1297.
18. Mirzayans, F., Gould, D.B., Heon, E., Billingsley, G.D., Cheung, J.C., Mears, A.J. and Walter, M.A. (2000) Axenfeld-Rieger syndrome resulting from mutation of the FKHL7 gene on chromosome 6p25. EJHG, 8, 71.
19. Hjalt, T.A., Semina, E.V., Amendt, B.A. and Murray, J.C. (2000) The Pitx2 protein in mouse development. Dev. Dyn., 218, 195-200.
20. Mucchielli, M.-L., Mitsiadis, T.A., Raffo, S., Brunet, J.-F., Proust, J.-P. and Goridis, C. (1997) Mouse Otlx2/RIEG expression in the odontogenic epithelium precedes tooth initiation and requires mesenchyme-derived signals for its maintenance. Dev. Biol., 189, 275-284.
21. Lin, C.R., Kioussi, C., O'Connell, S., Briata, P., Szeto, D., Liu, F., Izpisúa-Belmonte, J.C. and Rosenfeld, M.G. (1999) Pitx2 regulates lung asymmetry, cardiac positioning and pituitary and tooth morphogenesis. Nature, 401, 279-281.
22. 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.
23. Pispa, J. and Thesleff, I. (2003) Mechanisms of ectodermal organogenesis. Dev. Biol., 262, 195-205.
24. Tucker, A. and Sharpe, P. (2004) The cutting-edge of mammalian development; how the embryo makes teeth. Nat. Rev. Genet., 5, 499-508.
25. Weisschuh, N., Dressler, P., Schuettauf, F., Wolf, C., Wissinger, B. and Gramer, E. (2006) Novel mutations of FOXC1 and PITX2 in patients with Axenfeld-Rieger malformations. Invest. Ophthal. Vis. Sci., 47, 3846-3852.
26. Perveen, R., Lloyd, I.C., Clayton-Smith, J., Churchill, A., van Heyningen, V., Hanson, I., Taylor, D., McKeown, C., Super, M. and Kerr, B. (2000) Phenotypic variability and asymmetry of Rieger syndrome associated with PITX2 mutations. Invest. Ophthal. Vis. Sci., 41, 2456-2460.
27. Phillips, J.C. (2002) Four novel mutations in the PITX2 gene in patients with Axenfeld-Rieger syndrome. Ophthal. Res., 34, 324-326.
28. Gibson, C.W. (2011) The amelogenin proteins and enamel development in humans and mice. J. Oral Biosci., 53, 248-256.
29. Wright, J.T., Hart, T.C., Hart, P.S., Simmons, D., Suggs, C., Daley, B., Simmer, J., Hu, J., Bartlett, J.D., Li, Y. et al. (2009) Human and mouse enamel phenotypes resulting from mutation or altered expression of AMEL, ENAM, MMP20 and KLK4. Cells Tissues Organs, 189, 224-229.
30. Gibson, C.W. (1999) Regulation of amelogenin gene expression. Crit. Rev. Eukaryot. Gene Expr., 9, 45-57.
31. Thomas, B.L., Liu, J.K., Rubenstein, J. and Sharpe, P.T. (2000) Independent regulation of Dlx2 expression in the epithelium and mesenchyme of the first branchial arch. Development, 127, 217-224.
32. Lézot, F., Thomas, B., Greene, S.R., Hotton, D., Yuan, Z.A., Castaneda, B., Bolanos, A., Depew, M., Sharpe, P. and Gibson, C.W. (2008) Physiological implications of DLX homeoproteins in enamel formation. J. Cell. Physiol., 216, 688-697.
33. Blatt, E.N., Yan, X.H., Wuerffel, M.K., Hamilos, D.L. and Brody, S.L. (1999) Forkhead transcription factorHFH-4expression is temporally related to ciliogenesis. Am. J. Respir. Cell Mol. Biol., 21, 168.
34. Venugopalan, S.R., Li, X., Amen, M.A., Florez, S., Gutierrez, D., Cao, H., Wang, J. and Amendt, B.A. (2011) Hierarchical interactions of homeodomain and forkhead transcription factors in regulating odontogenic gene expression. J. Biol. Chem., 286, 21372-21383.
35. 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. and Amendt, B.A. (2008) Novel expression and transcriptional regulation of FoxJ1 during oro-facial morphogenesis. Hum. Mol. Genet., 17, 3643-3654.
36. Liu, F., Chu, E.Y., Watt, B., Zhang, Y., Gallant, N.M., Andl, T., Yang, S.H., Lu, M.-M., Piccolo, S. and Schmidt-Ullrich, R. (2008) Wnt/b-catenin signaling directs multiple stages of tooth morphogenesis. Dev. Biol., 313, 210-224.
37. Chen, J., Lan, Y., Baek, J.-A., Gao, Y. and Jiang, R. (2009) Wnt/beta-catenin signaling plays an essential role in activation of odontogenic mesenchyme during early tooth development. Dev. Biol., 334, 174-185.
38. Amen, M., Liu, X., Vadlamudi, U., Elizondo, G., Diamond, E., Engelhardt, J.F. and Amendt, B.A. (2007) PITX2 And b-catenin interactions regulate Lef-1 isoform expression. Mol. Cell. Biol., 27, 7560-7573.
39. Vadlamudi, U., Espinoza, H.M., Ganga, M., Martin, D.M., Liu, X., Engelhardt, J.F. and Amendt, B.A. (2005) PITX2, b-catenin, and LEF-1 interact to synergistically regulate the LEF-1 promoter. J. Cell Sci., 118, 1129-1137.
40. Amen, M., Espinoza, H.M., Cox, C., Liang, X., Wang, J., Link, T.M.E., Brennan, R.G., Martin, J.F. and Amendt, B.A. (2008) Chromatin-associated HMG-17 is a major regulator of homeodomain transcription factor activity modulated by Wnt/beta-catenin signaling. Nucleic Acids Res., 36, 462-476.
41. Phair, R.D. and Misteli, T. (2000) High mobility of proteins in the mammalian cell nucleus. Nature, 404, 604-608.
42. Catez, F., Yang, H., Tracey, K.J., Reeves, R., Misteli, T. and Bustin, M. (2004) Network of dynamic interactions between histone H1 and high-mobility-group proteins in chromatin. Mol. Cell. Biol., 24, 4321-4328.
43. Hock, R., Furusawa, T., Ueda, T. and Bustin,M. (2007)HMGChromosomal proteins in development and disease. Trends Cell Biol., 17, 72-79.
44. Lin, C.R., Kioussi, C., O'Connell, S., Briata, P., Szeto, D., Liu, F., Izpisua-Belmonte, J.C. and Rosenfeld, M.G. (1999) Pitx2 regulates lung asymmetry, cardiac positioning and pituitary and tooth morphogenesis. Nature, 401, 279-282.
45. Chen, L., Couwenhoven, R., Hsu, D., Luo, W. and Snead, M. (1992) Maintenance of amelogenin gene expression by transformed epithelial cells of mouse enamel organ. Arch. Oral Biol., 37, 771-778.
46. Dhamija, S., Liu, Y., Yamada, Y., Snead, M.L. and Krebsbach, P.H. (1999) Cloning and characterization of the murine ameloblastin promoter. J. Biol. Chem., 274, 20738-20743.
47. 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. and Amendt, B.A. (2001) Antagonistic regulation of Dlx2 expression by PITX2 and Msx2: implications for tooth development. Gene Expr., 9, 265-281.
48. Jheon, A.H., Mostowfi, P., Snead, M.L., Ihrie, R.A., Sone, E., Pramparo, T., Attardi, L.D. and Klein, O.D. (2011) PERP Regulates enamel formation via effects on cell-cell adhesion and gene expression. J. Cell Sci., 124, 745- 754.
49. Cox, C.J., Espinoza, H.M., McWilliams, B., Chappell, K., Morton, L., Hjalt, T.A., Semina, E.V. and Amendt, B.A. (2002) Differential regulation of gene expression by PITX2 isoforms. J. Biol. Chem., 277, 25001-25010.
50. Thesleff, I. (1976) Differentiation of odontogenic tissues in organ culture. Eur. J. Oral Sci., 84, 353-356.
51. Footz, T., Idrees, F., Acharya, M., Kozlowski, K. and Walter, M.A. (2009) Analysis of mutations of the PITX2 transcription factor found in patients with Axenfeld-Rieger syndrome. Invest. Ophthal. Vis. Sci., 50, 2599-2606.
52. Plikus, M.V., Zeichner-David, M., Mayer, J.A., Reyna, J., Bringas, P., Thewissen, J., Snead, M.L., Chai, Y. and Chuong, C.M. (2005) Morphoregulation of teeth: modulating the number, size, shape and differentiation by tuning Bmp activity. Evol. Dev., 7, 440-457.
53. Andl, C.D., Mizushima, T., Nakagawa, H., Oyama, K., Harada, H., Chruma, K., Herlyn, M. and Rustgi, A.K. (2003) Epidermal growth factor receptor mediates increased cell proliferation, migration, and aggregation in esophageal keratinocytes in vitro and in vivo. J. Biol. Chem., 278, 1824- 1830.
54. Andl, T., Ahn, K., Kairo, A., Chu, E.Y., Wine-Lee, L., Reddy, S.T., Croft, N.J., Cebra-Thomas, J.A., Metzger, D. and Chambon, P. (2004) Epithelial Bmpr1a regulates differentiation and proliferation in postnatal hair follicles and is essential for tooth development. Development, 131, 2257-2268.
55. Drum, M., Kaiser-Kupfer, M., Guckes, A. and Roberts, M. (1985) Oral manifestations of the Rieger syndrome: report of case. J. Am. Dent. Assoc., 110, 343-346.
56. Idrees, F., Bloch-Zupan, A., Free, S.L., Vaideanu, D., Thompson, P.J., Ashley, P., Brice, G., Rutland, P., Bitner-Glindzicz, M. and Khaw, P.T. (2006) A novel homeobox mutation in the PITX2 gene in a family with Axenfeld-Rieger syndrome associated with brain, ocular, and dental phenotypes. Am. J. Med. Genet. Part B: Neuropsyc. Genet., 141, 184-191.
57. Brooks, J.K., Coccaro, P.J. and Zarbin, M.A. (1989) The Rieger anomaly concomitant with multiple dental, craniofacial, and somatic midline anomalies and short stature. Oral Surg. Oral Med. Oral Path., 68, 717-724.
58. Bei, M., Stowell, S. and Maas, R. (2004) Msx2 controls ameloblast terminal differentiation. Dev. Dyn., 231, 758-765.
59. St Amand, T.R., Zhang, Y., Semina, E.V., Zhao, X., Hu, Y., Nguyen, L., Murray, J.C. and Chen, Y. (2000) Antagonistic signals between BMP4 and FGF8 define the expression of Pitx1 and Pitx2 in mouse tooth-forming anlage. Dev. Biol., 217, 323-332.
60. Simeone, A., Acampora, D.,Mallamaci, A., Stornaiuolo, A., D'Apice,M.R., Nigro,V. and Boncinelli, E. (1993)Avertebrate gene related to orthodenticle contains a homeodomain of the bicoid class and demarcates anterior neuroectoderm in the gastrulating mouse embryo. EMBO J., 12, 2735.
61. Hanes, S.D. and Brent, R. (1989) DNA Specificity of the bicoid activator protein is determined by homeodomain recognition helix residue 9. Cell, 57, 1275-1283.
62. Gehring, W.J., Qian, Y.Q., Billeter, M., Furukubo-Tokunaga, K., Schier, A.F., Resendez-Perez, D., Affolter, M., Otting, G. and Wüthrich, K. (1994) Homeodomain-DNA recognition. Cell, 78, 211.
63. Zhang, Z., Gutierrez, D., Li, X., Bidlack, F., Cao, H., Wang, J., Andrade, K., Margolis, H.C. and Amendt, B.A. (2013) The LIM homeodomain transcription factor LHX6: a transcriptional repressor that interacts with pituitary homeobox 2 (pitx2) to regulate odontogenesis. J. Biol. Chem., 288, 2485-2500.
64. Li, X., Florez, S., Wang, J., Cao, H. and Amendt, B.A. (2013) Dact2 represses PITX2 transcriptional activation and cell proliferation through Wnt/beta-catenin signaling during odontogenesis. PloS One, 8, e54868.
65. Smidt, M.P., Cox, J.J., Schaick, H.S.v., Coolen, M., Schepers, J., Kleij, A.M. and Burbach, J.P.H. (2000) Analysis of three Ptx2 splice variants on transcriptional activity and differential expression pattern in the brain. J. Neurochem., 75, 1818-1825.
66. Toro, R., Saadi, I., Kuburas, A., Nemer, M. and Russo, A.F. (2004) Cell-specific activation of the atrial natriuretic factor promoterbyPITX2and MEF2A. J. Biol. Chem., 279, 52087-52094.
67. L'Honoré, A., Ouimette, J.-F., Lavertu-Jolin, M. and Drouin, J. (2010) Pitx2 defines alternate pathways acting through myoD during limb and somitic myogenesis. Development, 137, 3847-3856.
68. Amendt, B.A., Sutherland, L.B., Semina, E.V. and Russo, A.F. (1998) The molecular basis of Rieger syndrome: analysis of Pitx2 homeodomain protein activities. J. Biol. Chem., 273, 20066-20072.
69. Kozlowski, K. and Walter, M.A. (2000) Variation in residual PITX2 activity underlies the phenotypic spectrum of anterior segment developmental disorders. Hum. Mol. Genet., 9, 2131-2139.
70. Dingwall, C. and Laskey, R.A. (1991) Nuclear targeting sequences-a consensus? Trends Biochem. Sci., 16, 478.
71. Herrera, J.E., Sakaguchi, K., Bergel, M., Trieschmann, L., Nakatani, Y. and Bustin, M. (1999) Specific acetylation of chromosomal protein HMG-17 by PCAF alters its interaction with nucleosomes. Mol. Cell. Biol., 19, 3466- 3473.
72. Shirakawa, H., Herrera, J.E., Bustin, M. and Postnikov, Y. (2000) Targeting of high mobility group-14/-17 proteins in chromatin is independent of DNA sequence. J. Biol. Chem., 275, 37937-37944.
73. Lehtonen, S., Olkkonen, V.M., Stapleton, M., Zerial, M. and Lehtonen, E. (1998) HMG-17, a chromosomal non-histone protein, shows developmental regulation during organogenesis. Internat. J. Dev. Biol., 42, 775.
74. Mohamed, O.A., Bustin, M. and Clarke, H.J. (2001) High-mobility group proteins 14 and 17 maintain the timing of early embryonic development in the mouse. Dev. Biol., 229, 237-249.
75. Cao, H., Wang, J., Li, X., Florez, S., Huang, Z., Venugopalan, S.R., Elangovan, S., Skobe, Z., Margolis, H.C., Martin, J.F. et al. (2010) MicroRNAs play a critical role in tooth development. J. Dent. Res., 89, 779-784.