Fuz Mutant Mice Reveal Shared Mechanisms between Ciliopathies and FGF-Related Syndromes

Developmental Cell

Volumn 25, Issue 6, 2013, Pages 623-635

  Tabler, JacquelineM ^a,c   Barrell, WilliamB ^a   Szabo Rogers, HeatherL ^a,d   Healy, Christopher ^a   Yeung, Yvonne ^a   Perdiguero, ElisaGomez ^a   Schulz, Christian ^a   Yannakoudakis, BasilZ ^a   Mesbahi, Aida ^a   Wlodarczyk, Bogdan ^b   Geissmann, Frederic ^a   Finnell, RichardH ^b   Wallingford, JohnB ^c   Liu, Karen J ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^c UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^d UNIVERSITY OF PITTSBURGH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FIBROBLAST GROWTH FACTOR 8;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CILIOPATHY; CONTROLLED STUDY; CRANIOFACIAL MALFORMATION; GENE EXPRESSION; GENETIC TRANSCRIPTION; HIGH ARCHED PALATE; MIDFACE HYPOPLASIA; MOUSE; MOUSE MUTANT; NEURAL CREST; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL;

ANIMALS; BARDET-BIEDL SYNDROME; CELL MOVEMENT; CILIARY MOTILITY DISORDERS; CRANIOFACIAL ABNORMALITIES; DISEASE MODELS, ANIMAL; FIBROBLAST GROWTH FACTOR 8; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; KRUPPEL-LIKE TRANSCRIPTION FACTORS; MAXILLA; MICE; MICE, MUTANT STRAINS; NEURAL CREST; OROFACIODIGITAL SYNDROMES; PALATE; PHENOTYPE;

MUS;

EID: 84879547625     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2013.05.021     Document Type: Article

References (88)

1. Agochukwu N.B., Solomon B.D., Doherty E.S., Muenke M. Palatal and oral manifestations of Muenke syndrome (FGFR3-related craniosynostosis). J.Craniofac. Surg. 2012, 23:664-668.
2. Anderson P.J., Hall C., Evans R.D., Harkness W.J., Hayward R.D., Jones B.M. The cervical spine in Crouzon syndrome. Spine (Phila Pa 1976) 1997, 22:402-405.
3. Aoto K., Nishimura T., Eto K., Motoyama J. Mouse GLI3 regulates Fgf8 expression and apoptosis in the developing neural tube, face, and limb bud. Dev. Biol. 2002, 251:320-332.
4. Arts H.H., Bongers E.M., Mans D.A., van Beersum S.E., Oud M.M., Bolat E., Spruijt L., Cornelissen E.A., Schuurs-Hoeijmakers J.H., de Leeuw N., et al. C14ORF179 encoding IFT43 is mutated in Sensenbrenner syndrome. J.Med. Genet. 2011, 48:390-395.
5. Beales P.L., Elcioglu N., Woolf A.S., Parker D., Flinter F.A. New criteria for improved diagnosis of Bardet-Biedl syndrome: results of a population survey. J.Med. Genet. 1999, 36:437-446.
6. Benadiba C., Magnani D., Niquille M., Morlé L., Valloton D., Nawabi H., Ait-Lounis A., Otsmane B., Reith W., Theil T., et al. The ciliogenic transcription factor RFX3 regulates early midline distribution of guidepost neurons required for corpus callosum development. PLoS Genet. 2012, 8:e1002606.
7. Berkowitz S. Stereophotogrammetric analysis of casts of normal and abnormal palates. Am. J. Orthod. 1971, 60:1-18.
8. Blaess S., Corrales J.D., Joyner A.L. Sonic hedgehog regulates Gli activator and repressor functions with spatial and temporal precision in the mid/hindbrain region. Development 2006, 133:1799-1809.
9. Brooks E.R., Wallingford J.B. Control of vertebrate intraflagellar transport by the planar cell polarity effector Fuz. J. Cell Biol. 2012, 198:37-45.
10. Brugmann S.A., Cordero D.R., Helms J.A. Craniofacial ciliopathies: A new classification for craniofacial disorders. Am. J. Med. Genet. A. 2010, 152A:2995-3006.
11. Chai Y., Maxson R.E. Recent advances in craniofacial morphogenesis. Dev. Dyn. 2006, 235:2353-2375.
12. Cobourne M.T., Xavier G.M., Depew M., Hagan L., Sealby J., Webster Z., Sharpe P.T. Sonic hedgehog signalling inhibits palatogenesis and arrests tooth development in a mouse model of the nevoid basal cell carcinoma syndrome. Dev. Biol. 2009, 331:38-49.
13. Collier S., Gubb D. Drosophila tissue polarity requires the cell-autonomous activity of the fuzzy gene, which encodes a novel transmembrane protein. Development 1997, 124:4029-4037.
14. Cordero D., Marcucio R., Hu D., Gaffield W., Tapadia M., Helms J.A. Temporal perturbations in sonic hedgehog signaling elicit the spectrum of holoprosencephaly phenotypes. J.Clin. Invest. 2004, 114:485-494.
15. Creuzet S., Schuler B., Couly G., Le Douarin N.M. Reciprocal relationships between Fgf8 and neural crest cells in facial and forebrain development. Proc. Natl. Acad. Sci. USA 2004, 101:4843-4847.
16. Danielian P.S., Muccino D., Rowitch D.H., Michael S.K., McMahon A.P. Modification of gene activity in mouse embryos in utero by a tamoxifen-inducible form of Cre recombinase. Curr. Biol. 1998, 8:1323-1326.
17. Endoh-Yamagami S., Evangelista M., Wilson D., Wen X., Theunissen J.W., Phamluong K., Davis M., Scales S.J., Solloway M.J., de Sauvage F.J., Peterson A.S. The mammalian Cos2 homolog Kif7 plays an essential role in modulating Hh signal transduction during development. Curr. Biol. 2009, 19:1320-1326.
18. Fedtsova N., Turner E.E. Signals from the ventral midline and isthmus regulate the development of Brn3.0-expressing neurons in the midbrain. Mech. Dev. 2001, 105:129-144.
19. Ferkol T.W., Leigh M.W. Ciliopathies: the central role of cilia in a spectrum of pediatric disorders. J.Pediatr. 2012, 160:366-371.
20. Ferrante M.I., Zullo A., Barra A., Bimonte S., Messaddeq N., Studer M., Dollé P., Franco B. Oral-facial-digital type I protein is required for primary cilia formation and left-right axis specification. Nat. Genet. 2006, 38:112-117.
21. Firnberg N., Neubüser A. FGF signaling regulates expression of Tbx2, Erm, Pea3, and Pax3 in the early nasal region. Dev. Biol. 2002, 247:237-250.
22. Goetz S.C., Anderson K.V. The primary cilium: a signalling centre during vertebrate development. Nat. Rev. Genet. 2010, 11:331-344.
23. Goodwin A., Oberoi S., Landan M., Charles C., Groth J., Martinez A., Fairley C., Weiss L., Tidyman W., Klein O., et al. Craniofacial and dental development in cardio-facio-cutaneous syndrome: the importance of Ras signaling homeostasis. Clin. Genet. 2012.
24. Gray R.S., Abitua P.B., Wlodarczyk B.J., Szabo-Rogers H.L., Blanchard O., Lee I., Weiss G.S., Liu K.J., Marcotte E.M., Wallingford J.B., Finnell R.H. The planar cell polarity effector Fuz is essential for targeted membrane trafficking, ciliogenesis and mouse embryonic development. Nat. Cell Biol. 2009, 11:1225-1232.
25. Gritli-Linde A., Hallberg K., Harfe B.D., Reyahi A., Kannius-Janson M., Nilsson J., Cobourne M.T., Sharpe P.T., McMahon A.P., Linde A. Abnormal hair development and apparent follicular transformation to mammary gland in the absence of hedgehog signaling. Dev. Cell 2007, 12:99-112.
26. Hajihosseini M.K., Wilson S., De Moerlooze L., Dickson C. A splicing switch and gain-of-function mutation in FgfR2-IIIc hemizygotes causes Apert/Pfeiffer-syndrome-like phenotypes. Proc. Natl. Acad. Sci. USA 2001, 98:3855-3860.
27. Hayward R., Jones B., Dunaway D. The Clinical Management of Craniosynostosis 2004, MacKeith Press, London.
28. Hennekam R., Allanson J., Krantz I. Gorlin's Syndromes of the Head and Neck 2010, Oxford University Press, New York.
29. Heydeck W., Zeng H., Liu A. Planar cell polarity effector gene Fuzzy regulates cilia formation and Hedgehog signal transduction in mouse. Dev. Dyn. 2009, 238:3035-3042.
30. Hippenmeyer S., Shneider N.A., Birchmeier C., Burden S.J., Jessell T.M., Arber S. A role for neuregulin1 signaling in muscle spindle differentiation. Neuron 2002, 36:1035-1049.
31. Hong S.K., Dawid I.B. FGF-dependent left-right asymmetry patterning in zebrafish is mediated by Ier2 and Fibp1. Proc. Natl. Acad. Sci. USA 2009, 106:2230-2235.
32. Hopwood N.D., Pluck A., Gurdon J.B. A Xenopus mRNA related to Drosophila twist is expressed in response to induction in the mesoderm and the neural crest. Cell 1989, 59:893-903.
33. Hosokawa R., Deng X., Takamori K., Xu X., Urata M., Bringas P., Chai Y. Epithelial-specific requirement of FGFR2 signaling during tooth and palate development. J.Exp. Zoolog. B Mol. Dev. Evol. 2009, 312B:343-350.
34. Hu D., Helms J.A. The role of sonic hedgehog in normal and abnormal craniofacial morphogenesis. Development 1999, 126:4873-4884.
35. Huang X., Goudy S.L., Ketova T., Litingtung Y., Chiang C. Gli3-deficient mice exhibit cleft palate associated with abnormal tongue development. Dev. Dyn. 2008, 237:3079-3087.
36. Huber C., Cormier-Daire V. Ciliary disorder of the skeleton. Am. J. Med. Genet. C. Semin. Med. Genet. 2012, 160C:165-174.
37. Ilagan R., Abu-Issa R., Brown D., Yang Y.P., Jiao K., Schwartz R.J., Klingensmith J., Meyers E.N. Fgf8 is required for anterior heart field development. Development 2006, 133:2435-2445.
38. Itoh N., Ornitz D.M. Fibroblast growth factors: from molecular evolution to roles in development, metabolism and disease. J.Biochem. 2011, 149:121-130.
39. Kreiborg S., Cohen M.M. The oral manifestations of Apert syndrome. J.Craniofac. Genet. Dev. Biol. 1992, 12:41-48.
40. Kreiborg S., Barr M., Cohen M.M. Cervical spine in the Apert syndrome. Am. J. Med. Genet. 1992, 43:704-708.
41. Kuschel S., Rüther U., Theil T. A disrupted balance between Bmp/Wnt and Fgf signaling underlies the ventralization of the Gli3 mutant telencephalon. Dev. Biol. 2003, 260:484-495.
42. Lai C.K., Gupta N., Wen X., Rangell L., Chih B., Peterson A.S., Bazan J.F., Li L., Scales S.J. Functional characterization of putative cilia genes by high-content analysis. Mol. Biol. Cell 2011, 22:1104-1119.
43. Lan Y., Jiang R. Sonic hedgehog signaling regulates reciprocalepithelial-mesenchymal interactions controlling palatal outgrowth. Development 2009, 136:1387-1396.
44. Letra A., de Almeida A.L., Kaizer R., Esper L.A., Sgarbosa S., Granjeiro J.M. Intraoral features of Apert's syndrome. Oral Surg. Oral Med. Oral Pathol. Oral Radiol. Endod. 2007, 103:e38-e41.
45. Levin L.S., Perrin J.C., Ose L., Dorst J.P., Miller J.D., McKusick V.A. A heritable syndrome of craniosynostosis, short thin hair, dental abnormalities, and short limbs: cranioectodermal dysplasia. J.Pediatr. 1977, 90:55-61.
46. Liu A., Wang B., Niswander L.A. Mouse intraflagellar transport proteins regulate both the activator and repressor functions of Gli transcription factors. Development 2005, 132:3103-3111.
47. Livet J., Sigrist M., Stroebel S., De Paola V., Price S.R., Henderson C.E., Jessell T.M., Arber S. ETS gene Pea3 controls the central position and terminal arborization of specific motor neuron pools. Neuron 2002, 35:877-892.
48. Lorente C.A., Tassinari M.S., Keith D.A. The effects of phenytoin on rat development: an animal model system for fetal hydantoin syndrome. Teratology 1981, 24:169-180.
49. Mahmood R., Bresnick J., Hornbruch A., Mahony C., Morton N., Colquhoun K., Martin P., Lumsden A., Dickson C., Mason I. A role for FGF-8 in the initiation and maintenance of vertebrate limb bud outgrowth. Curr. Biol. 1995, 5:797-806.
50. Martínez-Abadías N., Percival C., Aldridge K., Hill C.A., Ryan T., Sirivunnabood S., Wang Y., Jabs E.W., Richtsmeier J.T. Beyond the closed suture in apert syndrome mouse models: evidence of primary effects of FGFR2 signaling on facial shape at birth. Dev. Dyn. 2010, 239:3058-3071.
51. Mo R., Freer A.M., Zinyk D.L., Crackower M.A., Michaud J., Heng H.H., Chik K.W., Shi X.M., Tsui L.C., Cheng S.H., et al. Specific and redundant functions of Gli2 and Gli3 zinc finger genes in skeletal patterning and development. Development 1997, 124:113-123.
52. Monsoro-Burq A.H., Fletcher R.B., Harland R.M. Neural crest induction by paraxial mesoderm in Xenopus embryos requires FGF signals. Development 2003, 130:3111-3124.
53. Moore M.H., Lodge M.L., Clark B.E. Spinal anomalies in Pfeiffer syndrome. Cleft Palate Craniofac. J. 1995, 32:251-254.
54. Moore S.J., Green J.S., Fan Y., Bhogal A.K., Dicks E., Fernandez B.A., Stefanelli M., Murphy C., Cramer B.C., Dean J.C., et al. Clinical and genetic epidemiology of Bardet-Biedl syndrome in Newfoundland: a 22-year prospective, population-based, cohort study. Am. J. Med. Genet. A. 2005, 132:352-360.
55. Muzumdar M.D., Tasic B., Miyamichi K., Li L., Luo L. A global double-fluorescent Cre reporter mouse. Genesis 2007, 45:593-605.
56. Neugebauer J.M., Amack J.D., Peterson A.G., Bisgrove B.W., Yost H.J. FGF signalling during embryo development regulates cilia length in diverse epithelia. Nature 2009, 458:651-654.
57. Noden D.M. An analysis of migratory behavior of avian cephalic neural crest cells. Dev. Biol. 1975, 42:106-130.
58. Novarino G., Akizu N., Gleeson J.G. Modeling human disease in humans: the ciliopathies. Cell 2011, 147:70-79.
59. Okada T., Okumura Y., Motoyama J., Ogawa M. FGF8 signaling patterns the telencephalic midline by regulating putative key factors of midline development. Dev. Biol. 2008, 320:92-101.
60. Osumi-Yamashita N., Ninomiya Y., Doi H., Eto K. The contribution of both forebrain and midbrain crest cells to the mesenchyme in the frontonasal mass of mouse embryos. Dev. Biol. 1994, 164:409-419.
61. Park T.J., Haigo S.L., Wallingford J.B. Ciliogenesis defects in embryos lacking inturned or fuzzy function are associated with failure of planar cell polarity and Hedgehog signaling. Nat. Genet. 2006, 38:303-311.
62. Peterson S.J., Pruzansky S. Palatal anomalies in the syndromes of Apert and Crouzon. Cleft Palate J. 1974, 11:394-403.
63. Prattichizzo C., Macca M., Novelli V., Giorgio G., Barra A., Franco B. Mutational spectrum of the oral-facial-digital type I syndrome: a study on a large collection of patients. Hum. Mutat. 2008, 29:1237-1246. Oral-Facial-Digital Type I (OFDI) Collaborative Group.
64. Raible F., Brand M. Tight transcriptional control of the ETS domain factors Erm and Pea3 by Fgf signaling during early zebrafish development. Mech. Dev. 2001, 107:105-117.
65. Rash B.G., Grove E.A. Patterning the dorsal telencephalon: a role for sonic hedgehog?. J.Neurosci. 2007, 27:11595-11603.
66. Rice R., Spencer-Dene B., Connor E.C., Gritli-Linde A., McMahon A.P., Dickson C., Thesleff I., Rice D.P. Disruption of Fgf10/Fgfr2b-coordinated epithelial-mesenchymal interactions causes cleft palate. J.Clin. Invest. 2004, 113:1692-1700.
67. Roehl H., Nüsslein-Volhard C. Zebrafish pea3 and erm are general targets of FGF8 signaling. Curr. Biol. 2001, 11:503-507.
68. Rynearson R.D. Case report: orthodontic and dentofacial orthopedic considerations in Apert's syndrome. Angle Orthod. 2000, 70:247-252.
69. Schulz C., Gomez Perdiguero E., Chorro L., Szabo-Rogers H., Cagnard N., Kierdorf K., Prinz M., Wu B., Jacobsen S.E., Pollard J.W., et al. A lineage of myeloid cells independent of Myb and hematopoietic stem cells. Science 2012, 336:86-90.
70. Sensenbrenner J.A., Dorst J.P., Owens R.P. New syndrome of skeletal, dental and hair anomalies. Birth Defects Orig. Artic. Ser. 1975, 11:372-379.
71. Seo J.H., Zilber Y., Babayeva S., Liu J., Kyriakopoulos P., De Marco P., Merello E., Capra V., Gros P., Torban E. Mutations in the planar cell polarity gene, Fuzzy, are associated with neural tube defects in humans. Hum. Mol. Genet. 2011, 20:4324-4333.
72. Singla V., Reiter J.F. The primary cilium as the cell's antenna: signaling at a sensory organelle. Science 2006, 313:629-633.
73. Singla V., Romaguera-Ros M., Garcia-Verdugo J.M., Reiter J.F. Ofd1, a human disease gene, regulates the length and distal structure of centrioles. Dev. Cell 2010, 18:410-424.
74. Sive H.L., Grainger R.M., Harland R.M. Early Development of Xenopus laevis: A Laboratory Manual 2000, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
75. Slaney S.F., Oldridge M., Hurst J.A., Moriss-Kay G.M., Hall C.M., Poole M.D., Wilkie A.O. Differential effects of FGFR2 mutations on syndactyly and cleft palate in Apert syndrome. Am. J. Hum. Genet. 1996, 58:923-932.
76. Snyder-Warwick A.K., Perlyn C.A., Pan J., Yu K., Zhang L., Ornitz D.M. Analysis of a gain-of-function FGFR2 Crouzon mutation provides evidence of loss of function activity in the etiology of cleft palate. Proc. Natl. Acad. Sci. USA 2010, 107:2515-2520.
77. Somlo S., Rutecki G., Giuffra L.A., Reeders S.T., Cugino A., Whittier F.C. A kindred exhibiting cosegregation of an overlap connective tissue disorder and the chromosome 16 linked form of autosomal dominant polycystic kidney disease. J.Am. Soc. Nephrol. 1993, 4:1371-1378.
78. Soriano P. Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat. Genet. 1999, 21:70-71.
79. Tagliani M.M., Gomide M.R., Carrara C.F. Oral-facial-digital syndrome type 1: oral features in 12 patients submitted to clinical and radiographic examination. Cleft Palate Craniofac. J. 2010, 47:162-166.
80. Theil T., Alvarez-Bolado G., Walter A., Rüther U. Gli3 is required for Emx gene expression during dorsal telencephalon development. Development 1999, 126:3561-3571.
81. 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. Inhibition of neural crest migration underlies craniofacial dysmorphology and Hirschsprung's disease in Bardet-Biedl syndrome. Proc. Natl. Acad. Sci. USA 2008, 105:6714-6719.
82. Tukachinsky H., Lopez L.V., Salic A. A mechanism for vertebrate Hedgehog signaling: recruitment to cilia and dissociation of SuFu-Gli protein complexes. J. Cell Biol. 2010, 191:415-428.
83. Ueta E., Kurome M., Teshima Y., Kodama M., Otsuka Y., Naruse I. Altered signaling pathway in the dysmorphogenesis of telencephalon in the Gli3 depressed mouse embryo, Pdn/Pdn. Congenit. Anom. (Kyoto) 2008, 48:74-80.
84. Vadiati Saberi B., Shakoorpour A. Apert syndrome: report of a case with emphasis on oral manifestations. J.Dent. (Tehran) 2011, 8:90-95.
85. Wen X., Lai C.K., Evangelista M., Hongo J.A., de Sauvage F.J., Scales S.J. Kinetics of hedgehog-dependent full-length Gli3 accumulation in primary cilia and subsequent degradation. Mol. Cell. Biol. 2010, 30:1910-1922.
86. Wilkie A.O., Slaney S.F., Oldridge M., Poole M.D., Ashworth G.J., Hockley A.D., Hayward R.D., David D.J., Pulleyn L.J., Rutland P., et al. Apert syndrome results from localized mutations of FGFR2 and is allelic with Crouzon syndrome. Nat. Genet. 1995, 9:165-172.
87. Wilkinson D.G., Bhatt S., McMahon A.P. Expression pattern of the FGF-related proto-oncogene int-2 suggests multiple roles in fetal development. Development 1989, 105:131-136.
88. Zhang Z., Wlodarczyk B.J., Niederreither K., Venugopalan S., Florez S., Finnell R.H., Amendt B.A. Fuz regulates craniofacial development through tissue specific responses to signaling factors. PLoS ONE 2011, 6:e24608.