A primary cilia-dependent etiology for midline facial disorders

Human Molecular Genetics

Volumn 19, Issue 8, 2010, Pages 1577-1592

  Brugmann, Samantha A ^a   Allen, Nancy C ^a   James, Aaron W ^a   Mekonnen, Zesemayat ^a   Madan, Elena ^a   Helms, Jill A ^a  

^a STANFORD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN PATCHED; SONIC HEDGEHOG PROTEIN; TRANSCRIPTION FACTOR GLI1; TRANSCRIPTION FACTOR GLI3; WNT PROTEIN;

ANIMAL EXPERIMENT; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; EMBRYO; EUKARYOTIC FLAGELLUM; FACE; HEDGEHOG; HUNTINGTON DISEASE LIKE SYNDROME; HYPERTELORISM; IMMUNOHISTOCHEMISTRY; MESENCHYME; NEURAL CREST; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION;

ANIMALS; CELL PROLIFERATION; CELLS, CULTURED; CHICK EMBRYO; CILIA; CRANIOFACIAL ABNORMALITIES; FACE; HEDGEHOG PROTEINS; HUMANS; KINESIN; MICE; MICE, KNOCKOUT; NEURAL CREST; SIGNAL TRANSDUCTION;

AVES; ERINACEIDAE; TALPIDAE;

EID: 77952311364     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddq030     Document Type: Article

References (75)

1. Ming, J.E. and Muenke, M. (1998) Holoprosencephaly: from homer to hedgehog. Clin. Genet., 53, 155-163.
2. Muenke, M. and Beachy, P.A. (2000) Genetics of ventral forebrain development and holoprosencephaly. Curr. Opin. Genet. Dev, 10, 262-269.
3. Cohen, M.M.J. and Sulik, K.K. (1992) Perspectives on holoprosencephaly: Part II. Central nervous system, craniofacial anatomy, syndrome commentary, diagnostic approach, and experimental studies. J. Craniofac. Genet. Dev. Biol., 12, 196-244.
4. Ming, J.E. and Muenke, M. (2002) Multiple hits during early embryonic development: digenic diseases and holoprosencephaly. Am. J. Hum. Genet., 71, 1017-1032.
5. McKusick, V.A. (2000) Online Mendelian Inheritance in Man, OMIM (TM). McKusick-Nathans Institute for Genetic Medicine, Johns Hopkins University, Baltimore, MD and National Center for Biotechnology Information, National Library of Medicine, Bethesda, MD, Vol. 2002
6. Schachter, K.A. and Krauss, R.S. (2008) Murine models of holoprosencephaly. Curr. Top. Dev. Biol., 84, 139-170.
7. Wu, J., Staffenberg, D.A., Mulliken, J.B. and Shanske, A.L. (2002) Diprosopus: a unique case and review of the literature. Teratology, 66, 282-287.
8. Guion-Almeida, M.L., Richieri-Costa, A., Saavedra, D. and Cohen, M.M. Jr (1996) Frontonasal dysplasia: analysis of 21 cases and literature review. Int. J. Oral Maxillofac. Surg., 25, 91-97.
9. Nanni, L., Ming, J.E., Bocian, M., Steinhaus, K., Bianchi, D.W., Die-Smulders, C., Giannotti, A., Imaizumi, K., Jones, K.L., Campo, M.D. et al. (1999) The mutational spectrum of the sonic hedgehog gene in holoprosencephaly: SHH mutations cause a significant proportion of autosomal dominant holoprosencephaly. Hum. Mol. Genet., 8, 2479-2488.
10. Cordero, D., Marcucio, R., Hu, D., Gaffield, W., Tapadia, M. and Helms, J.A. (2004) Temporal perturbations in sonic hedgehog signaling elicit the spectrum of holoprosencephaly phenotypes. J. Clin. Invest., 114, 485-494.
11. Marcucio, R., Cordero, D.R., Hu, D. and Helms, J.A. (2005) Molecular interactions coordinating development of the forebrain and face. Dev. Biol., 284, 48-61.
12. Zhang, W., Kang, J.S., Cole, F., Yi, M.J. and Krauss, R.S. (2006) Cdo functions at multiple points in the Sonic Hedgehog pathway, and Cdo-deficient mice accurately model human holoprosencephaly. Dev. Cell., 10, 657-665.
13. Allen, B.L., Tenzen, T. and McMahon, A.P. (2007) The Hedgehog-binding proteins Gas1 and Cdo cooperate to positively regulate Shh signaling during mouse development. Genes Dev., 21, 1244-1257
14. Twigg, S.R., Versnel, S.L., Nurnberg, G., Lees, M.M., Bhat, M., Hammond, P., Hennekam, R.C., Hoogeboom, A.J., Hurst, J.A., Johnson, D. et al. (2009) Frontorhiny, a distinctive presentation of frontonasal dysplasia caused by recessive mutations in the ALX3 homeobox gene. Am. J. Hum. Genet., 84, 698-705.
15. 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.
16. Fogelgren, B., Kuroyama, M.C., McBratney-Owen, B., Spence, A.A., Malahn, L.E., Anawati, M.K., Cabatbat, C., Alarcon, V.B., Marikawa, Y. and Lozanoff, S. (2008) Misexpression of Six2 is associated with heritable frontonasal dysplasia and renal hypoplasia in 3H1 Br mice. Dev. Dyn., 237, 1767-1779.
17. Vortkamp, A., Gessler, M. and Grzeschik, K.H. (1991) GLI3 zinc-finger gene interrupted by translocations in Greig syndrome families. Nature, 352, 539-540.
18. Hu, D. and Helms, J.A. (1999) The role of sonic hedgehog in normal and abnormal craniofacial morphogenesis. Development, 126, 4873-4884.
19. Brugmann, S.A., Goodnough, L.H., Gregorieff, A., Leucht, P., Ten Berge, D., Fuerer, C., Clevers, H., Nusse, R. and Helms, J.A. (2007) Wnt signaling mediates regional specification in the vertebrate face. Development, 134, 3283-3295.
20. Corbit, K.C., Aanstad, P., Singla, V., Norman, A.R., Stainier, D.Y. and Reiter, J.F. (2005) Vertebrate smoothened functions at the primary cilium. Nature, 437, 1018-1021.
21. Rohatgi, R., Milenkovic, L. and Scott, M.P. (2007) Patched1 regulates hedgehog signaling at the primary cilium. Science, 317, 372-376.
22. Haycraft, C.J., Zhang, Q., Song, B., Jackson, W.S., Detloff, P.J., Serra, R. and Yoder, B.K. (2007) Intraflagellar transport is essential for endochondral bone formation. Development, 134, 307-316.
23. Corbit, K.C., Shyer, A.E., Dowdle, W.E., Gaulden, J., Singla, V., Chen, M.H., Chuang, P.T. and Reiter, J.F. (2008) Kif3a constrains beta-catenin-dependent Wnt signalling through dual ciliary and non-ciliary mechanisms. Nat. Cell Biol., 10, 70-76.
24. Kondo, S., Sato-Yoshitake, R., Noda, Y., Aizawa, H., Nakata, T., Matsuura, Y. and Hirokawa, N. (1994) KIF3A is a new microtubule-based anterograde motor in the nerve axon. J. Cell Biol., 125, 1095-1107.
25. Alieva, I.B., Gorgidze, L.A., Komarova, Y.A., Chernobelskaya, O.A. and Vorobjev, I.A. (1999) Experimental model for studying the primary cilia in tissue culture cells. Membr. Cell Biol., 12, 895-905.
26. Caspary, T., Larkins, C.E. and Anderson, K.V. (2007) The graded response to Sonic Hedgehog depends on cilia architecture. Dev. Cell, 12, 767-778.
27. Takeda, S., Yonekawa, Y., Tanaka, Y., Okada, Y., Nonaka, S. and Hirokawa, N. (1999) Left-right asymmetry and kinesin superfamily protein KIF3A: new insights in determination of laterality and mesoderm induction by kif3A -/- mice analysis. J. Cell Biol., 145, 825-836.
28. Marszalek, J.R., Liu, X., Roberts, E.A., Chui, D., Marth, J.D., Williams, D.S. and Goldstein, L.S. (2000) Genetic evidence for selective transport of opsin and arrestin by kinesin-II in mammalian photoreceptors. Cell, 102, 175-187.
29. Chai, Y., Jiang, X., Ito, Y., Bringas, P. Jr, Han, J., Rowitch, D.H., Soriano, P., McMahon, A.P. and Sucov, H.M. (2000) Fate of the mammalian cranial neural crest during tooth and mandibular morphogenesis. Development, 127, 1671-1679.
30. Osumi-Yamashita, N., Ninomiya, Y., Doi, H. and Eto, K. (1994) The contribution of both forebrain and midbrain crest cells to the mesenchyme in the frontonasal mass of mouse embryos. Dev. Biol., 164, 409-419.
31. Gorlin, R.J., Cohen, M.M. and Levin, L.S. (1990) Syndromes of the Head and Neck., 3rd edn. Oxford University Press, New York.
32. Guion-Almeida, M.L. and Richieri-Costa, A. (2001) Frontonasal dysplasia, macroblepharon, eyelid colobomas, ear anomalies, macrostomia, mental retardation and CNS structural anomalies: defining the phenotype. Clin. Dysmorphol., 10, 81-86.
33. Koyama, E., Young, B., Nagayama, M., Shibukawa, Y., Enomoto-Iwamoto, M., Iwamoto, M., Maeda, Y., Lanske, B., Song, B., Serra, R. et al. (2007) Conditional Kif3a ablation causes abnormal hedgehog signaling topography, growth plate dysfunction, and excessive bone and cartilage formation during mouse skeletogenesis. Development, 134, 2159-2169.
34. Eggenschwiler, J.T. and Anderson, K.V. (2007) Cilia and developmental signaling. Annu. Rev. Cell Dev. Biol., 23, 345-373.
35. Ocbina, P.J., Tuson, M. and Anderson, K.V. (2009) Primary cilia are not required for normal canonical Wnt signaling in the mouse embryo. PLoS One, 4, e6839.
36. DasGupta, R. and Fuchs, E. (1999) Multiple roles for activated LEF/TCF transcription complexes during hair follicle development and differentiation. Development, 126, 4557-4568.
37. Sarkar, L., Cobourne, M., Naylor, S., Smalley, M., Dale, T. and Sharpe, P.T. (2000) Wnt/Shh interactions regulate ectodermal boundary formation during mammalian tooth development. Proc. Natl Acad. Sci. USA, 97, 4520-4524.
38. Han, Y.G., Spassky, N., Romaguera-Ros, M., Garcia-Verdugo, J.M., Aguilar, A., Schneider-Maunoury, S. and Alvarez-Buylla, A. (2008) Hedgehog signaling and primary cilia are required for the formation of adult neural stem cells. Nat. Neurosci., 11, 277-284.
39. Spassky, N., Han, Y.G., Aguilar, A., Strehl, L., Besse, L., Laclef, C., Ros, M.R., Garcia-Verdugo, J.M. and Alvarez-Buylla, A. (2008) Primary cilia are required for cerebellar development and Shh-dependent expansion of progenitor pool. Dev. Biol., 317, 246-259.
40. Huangfu, D., Liu, A., Rakeman, A.S., Murcia, N.S., Niswander, L. and Anderson, K.V. (2003) Hedgehog signalling in the mouse requires intraflagellar transport proteins. Nature, 426, 83-87.
41. Chiang, C., Litingtung, Y., Lee, E., Young, K.E., Corden, J.L., Westphal, H. and Beachy, P.A. (1996) Cyclopia and defective axial patterning in mice lacking Sonic hedgehog gene function. Nature, 383, 407-413.
42. Jeong, J., Mao, J., Tenzen, T., Kottmann, A.H. and McMahon, A.P. (2004) Hedgehog signaling in the neural crest cells regulates the patterning and growth of facial primordia. Genes Dev., 18, 937-951.
43. Huangfu, D. and Anderson, K.V. (2005) Cilia and Hedgehog responsiveness in the mouse. Proc. Natl Acad. Sci. USA, 102, 11325-11330.
44. 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.
45. Benouaiche, L., Gitton, Y., Vincent, C., Couly, G. and Levi, G. (2008) Sonic hedgehog signalling from foregut endoderm patterns the avian nasal capsule. Development, 135, 2221-2225.
46. Etchevers, H.C., Couly, G., Vincent, C. and Le Douarin, N.M. (1999) Anterior cephalic neural crest is required for forebrain viability. Development, 126, 3533-3543.
47. Lee, J., Platt, K.A., Censullo, P., Ruiz, I. and Altaba, A. (1997) Gli1 is a target of Sonic hedgehog that induces ventral neural tube development. Development, 124, 2537-2552.
48. Hynes, M., Stone, D.M., Dowd, M., Pitts-Meek, S., Goddard, A., Gurney, A. and Rosenthal, A. (1997) Control of cell pattern in the neural tube by the zinc finger transcription factor and oncogene Gli-1. Neuron, 19, 15-26.
49. Tobin, J.L., Di Franco, M., Eichers, E., May-Simera, H., Garcia, M., Yan, J., Quinlan, R., Justice, M.J., Hennekam, R.C., Briscoe, J. et al. (2008) Inhibition of neural crest migration underlies craniofacial dysmorphology and Hirschsprung's disease in Bardet-Biedl syndrome. Proc. Natl Acad. Sci. USA, 105, 6714-6719.
50. Cole, R.K. (1942) The 'talpid' lethal in the domestic fowl. J. Hered., 33, 82-86.
51. Schneider, R.A., Hu, D. and Helms, J.A. (1999) From head to toe: conservation of molecular signals regulating limb and craniofacial morphogenesis. Cell Tissue Res., 296, 103-109.
52. Yin, Y., Bangs, F., Paton, I.R., Prescott, A., James, J., Davey, M.G., Whitley, P., Genikhovich, G., Technau, U., Burt, D.W. et al. (2009) The Talpid3 gene (KIAA0586) encodes a centrosomal protein that is essential for primary cilia formation. Development, 136, 655-664.
53. Caruccio, N.C., Martinez-Lopez, A., Harris, M., Dvorak, L., Bitgood, J., Simandl, B.K. and Fallon, J.F. (1999) Constitutive activation of sonic hedgehog signaling in the chicken mutant talpid(2): Shh-independent outgrowth and polarizing activity. Dev. Biol., 212, 137-149.
54. Wilder, H. (1908) The morphology of Cosmobia; speculations concerning the significance of certain types of monsters. Am. J. Anat., 8, 355-440
55. Belloni, E., Muenke, M., Roessler, E., Traverso, G., Siegel-Bartelt, J., Frumkin, A., Mitchell, H.F., Donis-Keller, H., Helms, C., Hing, A.V. et al. (1996) Identification of Sonic hedgehog as a candidate gene responsible for holoprosencephaly. Nat. Genet., 14, 353-356.
56. Kolpakova-Hart, E., Jinnin, M., Hou, B., Fukai, N. and Olsen, B.R. (2007) Kinesin-2 controls development and patterning of the vertebrate skeleton by Hedgehogand Gli3-dependent mechanisms. Dev. Biol., 309, 273-284.
57. Bisgrove, B.W. and Yost, H.J. (2006) The roles of cilia in developmental disorders and disease. Development, 133, 4131-4143.
58. Haycraft, C.J., Banizs, B., Aydin-Son, Y., Zhang, Q., Michaud, E.J. and Yoder, B.K. (2005) Gli2 and Gli3 localize to cilia and require the intraflagellar transport protein polaris for processing and function. PLoS Genet., 1, e53.
59. May, S.R., Ashique, A.M., Karlen, M., Wang, B., Shen, Y., Zarbalis, K., Reiter, J., Ericson, J. and Peterson, A.S. (2005) Loss of the retrograde motor for IFT disrupts localization of Smo to cilia and prevents the expression of both activator and repressor functions of Gli. Dev. Biol., 287, 378-389.
60. Bai, C.B., Auerbach, W., Lee, J.S., Stephen, D. and Joyner, A.L. (2002) Gli2, but not Gli1, is required for initial Shh signaling and ectopic activation of the Shh pathway. Development, 129, 4753-4761.
61. Johnson, D.R. (1967) Extra-toes: a new mutant gene causing multiple abnormalities in the mouse. J. Embryol. Exp. Morph., 17, 543-581.
62. Hui, C.C. and Joyner, A.L. (1993) A mouse model of greig cephalopolysyndactyly syndrome: the extra-toesJ mutation contains an intragenic deletion of the Gli3 gene. Nat. Genet., 3, 241-246.
63. Alvarez-Medina, R., Cayuso, J., Okubo, T., Takada, S. and Marti, E. (2008) Wnt canonical pathway restricts graded Shh/Gli patterning activity through the regulation of Gli3 expression. Development, 135, 237-247
64. Aszterbaum, M., Rothman, A., Johnson, R.L., Fisher, M., Xie, J., Bonifas, J.M., Zhang, X., Scott, M.P. and Epstein, E.H. Jr (1998) Identification of mutations in the human PATCHED gene in sporadic basal cell carcinomas and in patients with the basal cell nevus syndrome. J. Invest. Dermatol., 110, 885-888.
65. Villavicencio, E.H., Walterhouse, D.O. and Iannaccone, P.M. (2000) The sonic hedgehog-patched-gli pathway in human development and disease. Am. J. Hum. Genet., 67, 1047-1054.
66. Xie, J., Murone, M., Luoh, S.M., Ryan, A., Gu, Q., Zhang, C., Bonifas, J.M., Lam, C.W., Hynes, M., Goddard, A. et al. (1998) Activating Smoothened mutations in sporadic basal-cell carcinoma. Nature, 391, 90-92.
67. Gorlin, R.J. (2004) Nevoid basal cell carcinoma (Gorlin) syndrome. Genet. Med., 6, 530-539.
68. Stevens, C.A. and Qumsiyeh, M.B. (1995) Syndromal frontonasal dysostosis in a child with a complex translocation involving chromosomes 3, 7 and 11. Am. J. Med. Genet., 55, 494-497.
69. 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.
70. Sheehan, D.C. and Hrapchak, B.B. (1980) Theory and practice of Histotechnology, 2nd edn. Batelle Press, Columbus, Ohio.
71. Marszalek, J.R., Ruiz-Lozano, P., Roberts, E., Chien, K.R. and Goldstein, L.S. (1999) Situs inversus and embryonic ciliary morphogenesis defects in mouse mutants lacking the KIF3A subunit of kinesin-II. Proc. Natl Acad. Sci. USA, 96, 5043-5048.
72. Goodrich, L.V., Jung, D., Higgins, K.M. and Scott, M.P. (1999) Overexpression of ptc1 inhibits induction of Shh target genes and prevents normal patterning in the neural tube. Dev. Biol., 211, 323-334.
73. Maretto, S., Cordenonsi, M., Dupont, S., Braghetta, P., Broccoli, V., Hassan, A.B., Volpin, D., Bressan, G.M. and Piccolo, S. (2003) Mapping Wnt/beta-catenin signaling during mouse development and in colorectal tumors. Proc. Natl Acad. Sci. USA, 100, 3299-3304.
74. James, A.W., Xu, Y., Wang, R. and Longaker, M.T. (2008) Proliferation, osteogenic differentiation, and fgf-2 modulation of posterofrontal/sagittal suture-derived mesenchymal cells in vitro. Plast. Reconstr. Surg., 122, 53-63.
75. Hamburger, V. and Hamilton, H.L. (1951) A series of normal stages in the development of the chick embryo. J. Morphol., 88, 49-92.