Phenotype profile of a genetic mouse model for Muenke syndrome

Child's Nervous System

Volumn 28, Issue 9, 2012, Pages 1483-1493

  Nah, Hyun Duck ^a,e   Koyama, Eiki ^b   Agochukwu, Nneamaka B ^c,d   Bartlett, Scott P ^a   Muenke, Maximilian ^c  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c NATIONAL HUMAN GENOME RESEARCH INSTITUTE   (United States)

^d NATIONAL INSTITUTES OF HEALTH   (United States)

^e CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

Author keywords

FGFR3; Genetic mouse model; Muenke syndrome

Indexed keywords

FIBROBLAST GROWTH FACTOR RECEPTOR 3;

ACHONDROPLASIA; ACROCEPHALOSYNDACTYLY; ARTICLE; BONE DYSPLASIA; BRACHYDACTYLY; CARTILAGE CELL; CELL MATURATION; COCHLEA; CRANIOFACIAL SYNOSTOSIS; DISEASE MODEL; DWARFISM; ENCHONDRAL OSSIFICATION; EPIPHYSIS PLATE; GENE MUTATION; GENOTYPE; HUMAN; HYPOCHONDROPLASIA; INCIDENCE; LIMB MALFORMATION; MIDFACE HYPOPLASIA; MOUSE MUTANT; MUENKE SYNDROME; NONHUMAN; PERCEPTION DEAFNESS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SURFACE PLASMON RESONANCE; TEMPOROMANDIBULAR JOINT; THANATOPHORIC DWARFISM; X RAY CRYSTALLOGRAPHY;

ANIMALS; BONE DISEASES, DEVELOPMENTAL; CRANIAL SUTURES; CRANIOSYNOSTOSES; DISEASE MODELS, ANIMAL; FEMALE; HEARING LOSS, SENSORINEURAL; HUMANS; IMAGING, THREE-DIMENSIONAL; INFANT; MALE; MICE; MODELS, BIOLOGICAL; MUTATION; PHENOTYPE; RECEPTOR, FIBROBLAST GROWTH FACTOR, TYPE 3; TEMPOROMANDIBULAR JOINT; TOMOGRAPHY, X-RAY COMPUTED;

EID: 84866105445     PISSN: 02567040     EISSN: 14330350     Source Type: Journal    
DOI: 10.1007/s00381-012-1778-9     Document Type: Article

References (56)

1. Agochukwu NB, Solomon BD, Doherty ES, Muenke M (2012) The palatal and oral manifestations of Muenke syndrome (FGFR3-related craniosynostosis). J Craniofac Surg (in press)
2. Bellus GA, Hefferon TW, Ortiz de Luna RI, Hecht JT, Horton WA, Machado M, Kaitila I, McIntosh I, Francomano CA (1995) Achondroplasia is defined by recurrent G380R mutations of FGFR3. Am J Hum Genet 56:368-373
3. Bellus GA, McIntosh I, Smith EA, Aylsworth AS, Kaitila I, Horton WA, Greenhaw GA, Hecht JT, Francomano CA (1995) A recurrent mutation in the tyrosine kinase domain of fibroblast growth factor receptor 3 causes hypochondroplasia. Nat Genet 10:357-359
4. Bellus GA, Gaudenz K, Zackai EH, Clarke LA, Szabo J, Francomano CA, Muenke M (1996) Identical mutations in three different fibroblast growth factor receptor genes in autosomal dominant craniosynostosis syndromes. Nat Genet 14:174-176
5. Boulet SL, Rasmussen SA, Honein MA (2008) A population-based study of craniosynostosis in metropolitan Atlanta, 1989-2003. Am J Med Genet A 146A:984-991
6. Chellaiah AT, McEwen DG, Werner S, Xu J, Ornitz DM (1994) Fibroblast growth factor receptor (FGFR) 3. Alternative splicing in immunoglobulin-like domain III creates a receptor highly specific for acidic FGF/FGF-1. J Biol Chem 269:11620-11627
7. Chen L, Li C, Qiao W, Xu X, Deng C (2001) A Ser(365)->Cys mutation of fibroblast growth factor receptor 3 in mouse downregulates Ihh/PTHrP signals and causes severe achondroplasia. Hum Mol Genet 10:457-465
8. Collman H, Schweitzer T, Bohm H (2011) Imaging studies and neurosurgical treatment. In: Muenke M KW, Collman H, Solomon BD (ed) Monographs in Human Genetics Craniosynostoses: Molecular Genetics, Principles of Diagnosis and Treatment. Karger Publishing, Basel, pp 216-231
9. Colvin JS, Bohne BA, Harding GW, McEwen DG, Ornitz DM (1996) Skeletal overgrowth and deafness in mice lacking fibroblast growth factor receptor 3. Nat Genet 12:390-397
10. de Jong T, Mathijssen IM, Hoogeboom AJ (2011) Additional phenotypic features of Muenke syndrome in 2 Dutch families. J Craniofac Surg 22:571-575
11. 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
12. Deng C, Wynshaw-Boris A, Zhou F, Kuo A, Leder P (1996) Fibroblast growth factor receptor 3 is a negative regulator of bone growth. Cell 84:911-921
13. Doherty ES, Lacbawan F, Hadley DW, Brewer C, Zalewski C, Kim HJ, Solomon B, Rosenbaum K, Domingo DL, Hart TC, Brooks BP, Immken L, Lowry RB, Kimonis V, Shanske AL, Jehee FS, Bueno MR, Knightly C, McDonald-McGinn D, Zackai EH, Muenke M (2007) Muenke syndrome (FGFR3-related craniosynostosis): expansion of the phenotype and review of the literature. Am J Med Genet A 143A:3204-3215
14. Escobar LF, Hiett AK, Marnocha A (2009) Significant phenotypic variability of Muenke syndrome in identical twins. Am J Med Genet A 149A:1273-1276
15. Fakhry A, Ratisoontorn C, Vedhachalam C, Salhab I, Koyama E, Leboy P, Pacifici M, Kirschner RE, Nah HD (2005) Effects of FGF-2/-9 in calvarial bone cell cultures: differentiation stage-dependent mitogenic effect, inverse regulation of BMP-2 and noggin, and enhancement of osteogenic potential. Bone 36:254-266
16. Glass IA, Chapman S, Hockley AD (1994) A distinct autosomal dominant craniosynostosis-brachydactyly syndrome. Clin Dysmorphol 3:215-223
17. Graham JM Jr, Braddock SR, Mortier GR, Lachman R, Van Dop C, Jabs EW (1998) Syndrome of coronal craniosynostosis with brachydactyly and carpal/tarsal coalition due to Pro250Arg mutation in FGFR3 gene. Am J Med Genet 77:322-329
18. Harada M, Murakami H, Okawa A, Okimoto N, Hiraoka S, Nakahara T, Akasaka R, Shiraishi Y, Futatsugi N, Mizutani-Koseki Y, Kuroiwa A, Shirouzu M, Yokoyama S, Taiji M, Iseki S, Ornitz DM, Koseki H (2009) FGF9 monomer-dimer equilibrium regulates extracellular matrix affinity and tissue diffusion. Nat Genet 41:289-298
19. Honnebier MB, Cabiling DS, Hetlinger M, McDonald-McGinn DM, Zackai EH, Bartlett SP (2008) The natural history of patients treated for FGFR3-associated (Muenke-type) craniosynostosis. Plast Reconstr Surg 121:919-931
20. Ibrahimi OA, Zhang F, Eliseenkova AV, Linhardt RJ, Mohammadi M (2004) Proline to arginine mutations in FGF receptors 1 and 3 result in Pfeiffer and Muenke craniosynostosis syndromes through enhancement of FGF binding affinity. Hum Mol Genet 13:69-78
21. Jacques BE, Montcouquiol ME, Layman EM, Lewandoski M, Kelley MW (2007) Fgf8 induces pillar cell fate and regulates cellular patterning in the mammalian cochlea. Development 134:3021-3029
22. Keller MK, Hermann NV, Darvann TA, Larsen P, Hove HD, Christensen L, Schwartz M, Marsh JL, Kreiborg S (2007) Craniofacial morphology in Muenke syndrome. J Craniofac Surg 18:374-386
23. Krejci P, Prochazkova J, Bryja V, Jelinkova P, Pejchalova K, Kozubik A, Thompson LM, Wilcox WR (2009) Fibroblast growth factor inhibits interferon gamma-STAT1 and interleukin 6-STAT3 signaling in chondrocytes. Cell Signal 21:151-160
24. Lajeunie E, El Ghouzzi V, Le Merrer M, Munnich A, Bonaventure J, Renier D (1999) Sex related expressivity of the phenotype in coronal craniosynostosis caused by the recurrent P250R FGFR3 mutation. J Med Genet 36:9-13
25. Laurita J, Koyama E, Chin B, Taylor JA, Lakin GE, Hankenson KD, Bartlett SP, Nah HD (2011) The Muenke syndrome mutation (FgfR3P244R) causes cranial base shortening associated with growth plate dysfunction and premature perichondrial ossification in murine basicranial synchondroses. Dev Dyn 240:2584-2596
26. Madeline LA, Elster AD (1995) Suture closure in the human chondrocranium: CT assessment. Radiology 196:747-756
27. Mansour SL, Twigg SR, Freeland RM, Wall SA, Li C, Wilkie AO (2009) Hearing loss in a mouse model of Muenke syndrome. Hum Mol Genet 18:43-50
28. Matsunobu T, Torigoe K, Ishikawa M, de Vega S, Kulkarni AB, Iwamoto Y, Yamada Y (2009) Critical roles of the TGF-beta type I receptor ALK5 in perichondrial formation and function, cartilage integrity, and osteoblast differentiation during growth plate development. Dev Biol 332:325-338
29. Matsushita T, Wilcox WR, Chan YY, Kawanami A, Bukulmez H, Balmes G, Krejci P, Mekikian PB, Otani K, Yamaura I, Warman ML, Givol D, Murakami S (2009) FGFR3 promotes synchondrosis closure and fusion of ossification centers through the MAPK pathway. Hum Mol Genet 18:227-240
30. 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
31. Minina E, Kreschel C, Naski MC, Ornitz DM, Vortkamp A (2002) Interaction of FGF, Ihh/Pthlh, and BMP signaling integrates chondrocyte proliferation and hypertrophic differentiation. Dev Cell 3:439-449
32. Moloney DM, Wall SA, Ashworth GJ, Oldridge M, Glass IA, Francomano CA, Muenke M, Wilkie AO (1997) Prevalence of Pro250Arg mutation of fibroblast growth factor receptor 3 in coronal craniosynostosis. Lancet 349:1059-1062
33. Morriss-Kay GM, Wilkie AO (2005) Growth of the normal skull vault and its alteration in craniosynostosis: insights from human genetics and experimental studies. J Anat 207:637-653
34. Mueller KL, Jacques BE, Kelley MW (2002) Fibroblast growth factor signaling regulates pillar cell development in the organ of corti. J Neurosci 22:9368-9377
35. Muenke M, Schell U (1995) Fibroblast-growth-factor receptor mutations in human skeletal disorders. Trends Genet 11:308-313
36. Muenke M, Gripp KW, McDonald-McGinn DM, Gaudenz K, Whitaker LA, Bartlett SP, Markowitz RI, Robin NH, Nwokoro N, Mulvihill JJ, Losken HW, Mulliken JB, Guttmacher AE, Wilroy RS, Clarke LA, Hollway G, Ades LC, Haan EA, Mulley JC, Cohen MM Jr, Bellus GA, Francomano CA, Moloney DM, Wall SA, Wilkie AO et al (1997) A unique point mutation in the fibroblast growth factor receptor 3 gene (FGFR3) defines a new craniosynostosis syndrome. Am J Hum Genet 60:555-564
37. Murakami S, Kan M, McKeehan WL, de Crombrugghe B (2000) Up-regulation of the chondrogenic Sox9 gene by fibroblast growth factors is mediated by the mitogen-activated protein kinase pathway. Proc Natl Acad Sci U S A 97:1113-1118
38. Naski MC, Wang Q, Xu J, Ornitz DM (1996) Graded activation of fibroblast growth factor receptor 3 by mutations causing achondroplasia and thanatophoric dysplasia. Nat Genet 13:233-237
39. Naski MC, Colvin JS, Coffin JD, Ornitz DM (1998) Repression of hedgehog signaling and BMP4 expression in growth plate cartilage by fibroblast growth factor receptor 3. Development 125:4977-4988
40. Okamoto K, Ito J, Tokiguchi S, Furusawa T (1996) High-resolution CT findings in the development of the sphenooccipital synchondrosis. AJNR Am J Neuroradiol 17:117-120
41. Ornitz DM, Xu J, Colvin JS, McEwen DG, MacArthur CA, Coulier F, Gao G, Goldfarb M (1996) Receptor specificity of the fibroblast growth factor family. J Biol Chem 271:15292-15297
42. Pickles JO (2001) The expression of fibroblast growth factors and their receptors in the embryonic and neonatal mouse inner ear. Hear Res 155:54-62
43. Reardon W, Wilkes D, Rutland P, Pulleyn LJ, Malcolm S, Dean JC, Evans RD, Jones BM, Hayward R, Hall CM, Nevin NC, Baraister M, Winter RM (1997) Craniosynostosis associated with FGFR3 pro250arg mutation results in a range of clinical presentations including unisutural sporadic craniosynostosis. J Med Genet 34:632-636
44. Rice DP, Rice R, Thesleff I (2003) Fgfr mRNA isoforms in craniofacial bone development. Bone 33:14-27
45. Ridgway EB, Wu JK, Sullivan SR, Vasudavan S, Padwa BL, Rogers GF, Mulliken JB (2011) Craniofacial growth in patients with FGFR3Pro250Arg mutation after fronto-orbital advancement in infancy. J Craniofac Surg 22:455-461
46. Rousseau F, Bonaventure J, Legeai-Mallet L, Pelet A, Rozet JM, Maroteaux P, Le Merrer M, Munnich A (1994) Mutations in the gene encoding fibroblast growth factor receptor-3 in achondroplasia. Nature 371:252-254
47. Sabatino G, Di Rocco F, Zampino G, Tamburrini G, Caldarelli M, Di Rocco C (2004) Muenke syndrome. Childs Nerv Syst 20:297-301
48. Shim K, Minowada G, Coling DE, Martin GR (2005) Sprouty2, a mouse deafness gene, regulates cell fate decisions in the auditory sensory epithelium by antagonizing FGF signaling. Dev Cell 8:553-564
49. Thomas GP, Wilkie AO, Richards PG, Wall SA (2005) FGFR3 P250R mutation increases the risk of reoperation in apparent 'nonsyndromic' coronal craniosynostosis. J Craniofac Surg 16:347-352, discussion 353-344
50. Twigg SR, Healy C, Babbs C, Sharpe JA, Wood WG, Sharpe PT, Morriss-Kay GM, Wilkie AO (2009) Skeletal analysis of the Fgfr3(P244R) mouse, a genetic model for the Muenke craniosynostosis syndrome. Dev Dyn 238:331-342
51. Wilkie AO, Oldridge M, Tang Z, Maxson RE Jr (2001) Craniosynostosis and related limb anomalies. Novartis Found Symp 232:122-133, discussion 133-143
52. Wilkie AO, Byren JC, Hurst JA, Jayamohan J, Johnson D, Knight SJ, Lester T, Richards PG, Twigg SR, Wall SA (2010) Prevalence and complications of single-gene and chromosomal disorders in craniosynostosis. Pediatrics 126:e391-e400
53. Wu XL, Gu MM, Huang L, Liu XS, Zhang HX, Ding XY, Xu JQ, Cui B, Wang L, Lu SY, Chen XY, Zhang HG, Huang W, Yuan WT, Yang JM, Gu Q, Fei J, Chen Z, Yuan ZM, Wang ZG (2009) Multiple synostoses syndrome is due to a missense mutation in exon 2 of FGF9 gene. Am J Hum Genet 85:53-63
54. Yasuda T, Nah HD, Laurita J, Kinumatsu T, Shibukawa Y, Shibutani T, Minugh-Purvis N, Pacific M, Koyama E (2012) Muenke syndrome mutation, FgfR3(P244R), causes TMJ defects in postnatal mice. J Dent Res (in press)
55. Zhang R, Murakami S, Coustry F, Wang Y, de Crombrugghe B (2006) Constitutive activation of MKK6 in chondrocytes of transgenic mice inhibits proliferation and delays endochondral bone formation. Proc Natl Acad Sci U S A 103:365-370
56. Zhou G, Schwartz LT, Gopen Q (2009) Inner ear anomalies and conductive hearing loss in children with Apert syndrome: an overlooked otologic aspect. Otol Neurotol 30:184-189