Tissue-specific responses to aberrant FGF signaling in complex head phenotypes

Developmental Dynamics

Volumn 242, Issue 1, 2013, Pages 80-94

  Martínez Abadías, Neus ^a,d   Motch, Susan M ^a   Pankratz, Talia L ^a   Wang, Yingli ^b   Aldridge, Kristina ^c   Jabs, Ethylin Wang ^b   Richtsmeier, Joan T ^a  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

^b Mount Sinai SOM ^*  (United States)

^c University of Missouri   (United States)

^d CENTRE FOR GENOMIC REGULATION CRG   (Spain)

Author keywords

Brain; Craniosynostosis; Crouzon syndrome; Eye; FGFR2; Inner ear; Nasopharynx; Pfeiffer syndrome; Skull

Indexed keywords

FIBROBLAST GROWTH FACTOR; FIBROBLAST GROWTH FACTOR RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; BRAIN SIZE; CRANIOFACIAL DEVELOPMENT; CROUZON SYNDROME; EYE DEVELOPMENT; GENE MUTATION; HIGH RESOLUTION COMPUTER TOMOGRAPHY; INNER EAR; MAGNETIC RESONANCE MICROSCOPY; MORPHOLOGY; MOUSE; NASOPHARYNX; NEWBORN; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PHENOTYPE; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; SIGNAL TRANSDUCTION; TISSUE SPECIFICITY; VERTEBRATE;

ANIMALS; BRAIN; CRANIAL SUTURES; CRANIOFACIAL DYSOSTOSIS; MAGNETIC RESONANCE IMAGING; MICE; MUTATION, MISSENSE; PHENOTYPE; RECEPTOR, FIBROBLAST GROWTH FACTOR, TYPE 2; SIGNAL TRANSDUCTION; SKULL; X-RAY MICROTOMOGRAPHY;

MUS; VERTEBRATA;

EID: 84870911694     PISSN: 10588388     EISSN: 10970177     Source Type: Journal    
DOI: 10.1002/dvdy.23903     Document Type: Article

References (62)

1. Abzhanov A, Rodda SJ, McMahon AP, Tabin CJ. 2007. Regulation of skeletogenic differentiation in cranial dermal bone. Development 134: 3133-3144.
2. Aldridge K, Boyadjiew S, Capone G, DeLeon V, Richtsmeier JT. 2005. Precision and error of three-dimensional phenotypic measures acquired from 3dMD photogrammetric images. Am J Med Genet. 138: 247-253.
3. Aldridge K, Hill CA, Austin JR, Percival C, Martínez-Abadías N, Neuberger T, Wang Y, Jabs EW, Richtsmeier JT. 2010. Brain phenotypes in two FGFR2 mouse models for Apert syndrome. Dev Dyn 239: 987-997.
4. Bertrand S, Camasses A, Somorjai I, Belgacem MR, Chabrol O, Escande ML, Pontarotti P, Escriva H. 2011. Amphioxus FGF signaling predicts the acquisition of vertebrate morphological traits. Proc Natl Acad Sci USA 108: 9160-9165.
5. Cohen MM Jr, MacLean RE, editors. 2000. Craniosynostosis: diagnosis, evaluation, and management. New York: Oxford University Press. 361-365 pp.
6. Cole T III. 2002. WinEDMA. In: Windows-based software for euclidean distance matrix analysis.
7. Cremers CW. 1981. Hearing loss in Pfeiffer's syndrome. Int J Pediatr Otorhinolaryngol 3: 343-353.
8. Crump JG, Maves L, Lawson ND, Weinstein BM, Kimmel CB. 2004. An essential role for Fgfs in endodermal pouch formation influences later craniofacial skeletal patterning. Development 131: 5703-5716.
9. Darroch J, Mosimann J. 1985. Canonical and principal components of shape. Biometrika 72: 241-252.
10. de Jong T, Toll MS, de Gier HH, Mathijssen IM. 2011. Audiological profile of children and young adults with syndromic and complex craniosynostosis. Arch Otolaryngol Head Neck Surg 137: 775-778.
11. Degnin CR, Laederich MB, Horton WA. 2010. FGFs in endochondral skeletal development. J Cell Biochem 110: 1046-1057.
12. Drake AG, Klingenberg CP. 2008. The pace of morphological change: historical transformation of skull shape in St Bernard dogs. Proc Biol Sci 275: 71-76.
13. Dryden I, Mardia K. 1998. Statistical shape analysis. Chichester: John Wiley & Sons.
14. Eswarakumar VP, Horowitz MC, Locklin R, Morriss-Kay GM, Lonai P. 2004. A gain-of-function mutation of Fgfr2c demonstrates the roles of this receptor variant in osteogenesis. Proc Natl Acad Sci USA 101: 12555-12560.
15. Eswarakumar VP, Lax I, Schlessinger J. 2005. Cellular signaling by fibroblast growth factor receptors. Cytokine Growth Factor Rev 16: 139-149.
16. Hatch NE. 2010. FGF signaling in craniofacial biological control and pathological craniofacial development. Crit Rev Eukaryot Gene Expr 20: 295-311.
17. Hebert JM. 2011. FGFs: Neurodevelopment's jack-of-all-trades: how do they do it? Front Neurosci 5: 133.
18. Hill C, Martínez-Abadías N, Motch S, Austin J, Wang Y, Jabs E, Richtsmeier J, Aldridge K. 2012. Growth of the skull and brain differ postnatally in a mouse odel for Apert syndrome. Am J Med Genet (in press).
19. Huh SH, Jones J, Warchol ME, Ornitz DM. 2012. Differentiation of the lateral compartment of the cochlea requires a temporally restricted FGF20 signal. PLoS Biol 10: e1001231.
20. Itoh N, Ornitz DM. 2004. Evolution of the Fgf and Fgfr gene families. Trends Genet 20: 563-569.
21. Johnson D, Wilkie AO. 2011. Craniosynostosis. Eur J Hum Genet 19: 369-376.
22. Klingenberg C. 2008. MophoJ. In: Faculy of Life Sciences, University of Manchester, UK: http://www.flywings.org.uk/MorphoJ_page.htm.
23. Lele S, McCulloch C. 2002. Invariance, identifiability and morphometrics. JASA 971: 796-806.
24. Lele S, Richtsmeier JT. 2001. An invariant approach to the statistical analysis of shapes. London: Chapman and Hall/CRC Press. 308 p.
25. Martínez-Abadías N, Heuze Y, Wang Y, Jabs EW, Aldridge K, Richtsmeier JT. 2011. FGF/FGFR signaling coordinates skull development by modulating magnitude of morphological integration: evidence from Apert syndrome mouse models. PLoS One 6: e26425. doi:10.1371/journal.pone.0026425.
26. Martínez-Abadías N, Percival C, Aldridge K, Hill C, Ryan T, Sirivunnabood S, Wang Y, Jabs E, Richtsmeier J. 2010. Beyond the closed suture in Apert syndrome mouse models: evidence of primary effects of FGFR2 signaling on facial shape at birth. Dev Dyn 239: 3058-3071.
27. McBratney-Owen B, Iseki S, Bamforth SD, Olsen BR, Morriss-Kay GM. 2008. Development and tissue origins of the mammalian cranial base. Dev Biol 322: 121-132.
28. Mitsukawa N, Satoh K. 2010. Midfacial distraction using a transfacial pinning technique for syndromic craniosynostosis with obstructive respiratory disorders. J Plast Reconstr Aesthet Surg 63: 1990-1994.
29. Mitsukawa N, Satoh K, Hayashi T, Furukawa Y, Uemura T, Hosaka Y. 2004. A reflectable case of obstructive sleep apnea in an infant with Crouzon syndrome. J Craniofac Surg 15: 874-878; discussion 878-879.
30. Moore MH. 1993. Upper airway obstruction in the syndromal craniosynostoses. Br J Plast Surg 46: 355-362.
31. Moss M. 1959. The pathogenesis of premature cranial synostosis in man. Acta Anat 37: 351-370.
32. Moss M. 1962. The functional matrix. In: Kraus B, Riedel R, editors. Vistas in orthodontics. Chicago: Lea & Febiger. p 85-98.
33. Neilson KM, Friesel RE. 1995. Constitutive activation of fibroblast growth factor receptor-2 by a point mutation associated with Crouzon syndrome. J Biol Chem 270: 26037-26040.
34. Noden DM, Trainor PA. 2005. Relations and interactions between cranial mesoderm and neural crest populations. J Anat 207: 575-601.
35. Ornitz DM, Itoh N. 2001. Fibroblast growth factors. Genome Biol 2: REVIEWS3005.
36. Ornitz DM, Marie PJ. 2002. FGF signaling pathways in endochondral and intramembranous bone development and human genetic disease. Genes Dev 16: 1446-1465.
37. Orr-Urtreger A, Bedford MT, Burakova T, Arman E, Zimmer Y, Yayon A, Givol D, Lonai P. 1993. Developmental localization of the splicing alternatives of fibroblast growth factor receptor-2 (FGFR2). Dev Biol 158: 475-486.
38. Orvidas LJ, Fabry LB, Diacova S, McDonald TJ. 1999. Hearing and otopathology in Crouzon syndrome. Laryngoscope 109: 1372-1375.
39. Perkins JA, Sie KC, Milczuk H, Richardson MA. 1997. Airway management in children with craniofacial anomalies. Cleft Palate Craniofac J 34: 135-140.
40. Perlyn CA, DeLeon VB, Babbs C, Govier D, Burell L, Darvann T, Kreiborg S, Morriss-Kay G. 2006. The craniofacial phenotype of the Crouzon mouse: analysis of a model for syndromic craniosynostosis using three-dimensional MicroCT. Cleft Palate Craniofac J 43: 740-748.
41. Peterson SJ, Pruzansky S. 1974. Palatal anomalies in the syndromes of Apert and Crouzon. Cleft Palate J 11: 394-403.
42. Peterson-Falzone SJ, Pruzansky S, Parris PJ, Laffer JL. 1981. Nasopharyngeal dysmorphology in the syndromes of Apert and Crouzon. Cleft Palate J 18: 237-250.
43. Popovici C, Roubin R, Coulier F, Birnbaum D. 2005. An evolutionary history of the FGF superfamily. Bioessays 27: 849-857.
44. Proudman TW, Clark BE, Moore MH, Abbott AH, David DJ. 1995. Central nervous system imaging in Crouzon's syndrome. J Craniofac Surg 6: 401-405.
45. Randhawa PS, Ahmed J, Nouraei SR, Wyatt ME. 2011. Impact of long-term nasopharyngeal airway on health-related quality of life of children with obstructive sleep apnea caused by syndromic craniosynostosis. J Craniofac Surg 22: 125-128.
46. Richtsmeier J, Paik C, Elfert P, Cole TI, Dahlman H. 1995. Precision, repeatability, and validation of the localization of cranial landmarks using computed tomography scans. Cleft Palate Craniofac J 32: 217-227.
47. Richtsmeier JT, Deleon VB, Lele SR. 2002. The promise of geometric morphometrics. Yearbook Phys Anthropol 45: 63-91.
48. Riley BM, Mansilla MA, Ma J, Daack-Hirsch S, Maher BS, Raffensperger LM, Russo ET, Vieira AR, Dode C, Mohammadi M, Marazita ML, Murray JC. 2007. Impaired FGF signaling contributes to cleft lip and palate. Proc Natl Acad Sci USA 104: 4512-4517.
49. Rohlf FJ, Slice D. 1990a. Extensions of the Procrustes method for the optimal superimposition of landmarks. Syst Zool 39: 40-59.
50. Rohlf FJ, Slice D. 1990b. Extensions of the Procrustes method for the optimal superimposition of landmarks. Syst Zool 39: 40-59.
51. Rutland P, Pulleyn LJ, Reardon W, Baraitser M, Hayward R, Jones B, Malcolm S, Winter RM, Oldridge M, Slaney SF, Poole MD, Wilkie AOM. 1995. Identical mutations in the Fgfr2 gene cause both Pfeiffer and Crouzon Syndrome phenotypes. Nature Genet 9: 173-176.
52. Scheid SC, Spector AR, Luft JD. 2002. Tracheal cartilaginous sleeve in Crouzon syndrome. Int J Pediatr Otorhinolaryngol 65: 147-152.
53. Sirotnak J, Brodsky L, Pizzuto M. 1995. Airway obstruction in the Crouzon syndrome: case report and review of the literature. Int J Pediatr Otorhinolaryngol 31: 235-246.
54. Snyder-Warwick AK, Perlyn CA, Pan J, Yu K, Zhang L, Ornitz DM. 2010. 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 107: 2515-2520.
55. Szabo-Rogers HL, Geetha-Loganathan P, Nimmagadda S, Fu KK, Richman JM. 2008. FGF signals from the nasal pit are necessary for normal facial morphogenesis. Dev Biol 318: 289-302.
56. Thisse B, Thisse C. 2005. Functions and regulations of fibroblast growth factor signaling during embryonic development. Dev Biol 287: 390-402.
57. Turner N, Grose R. 2010. Fibroblast growth factor signalling: from development to cancer. Nature Rev Cancer 10: 116-129.
58. Vallino-Napoli LD. 1996. Audiologic and otologic characteristics of Pfeiffer syndrome. Cleft Palate Craniofac J 33: 524-529.
59. Wilkie AO. 1997. Craniosynostosis: genes and mechanisms. Hum Mol Genet 6: 1647-1656.
60. Wilkie AO. 2005. Bad bones, absent smell, selfish testes: the pleiotropic consequences of human FGF receptor mutations. Cytokine Growth Factor Rev 16: 187-203.
61. Yeh BK, Igarashi M, Eliseenkova AV, Plotnikov AN, Sher I, Ron D, Aaronson SA, Mohammadi M. 2003. Structural basis by which alternative splicing confers specificity in fibroblast growth factor receptors. Proc Natl Acad Sci USA 100: 2266-2271.
62. Yu JC, Lucas JH, Fryberg K, Borke JL. 2001. Extrinsic tension results in FGF-2 release, membrane permeability change, and intracellular Ca++ increase in immature cranial sutures. J Craniofac Surg 12: 391-398.