FGF signaling in craniofacial biological control and pathological craniofacial development

Critical Reviews in Eukaryotic Gene Expression

Volumn 20, Issue 4, 2010, Pages 295-311

  Hatch, Nan E ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

Author keywords

Craniofacial development; Craniosynostosis; Frs2; Heparin sulfate proteoglycan; MAPK; PLC

Indexed keywords

ALKALINE PHOSPHATASE; FIBROBLAST GROWTH FACTOR; FIBROBLAST GROWTH FACTOR RECEPTOR 1; FIBROBLAST GROWTH FACTOR RECEPTOR 2; FIBROBLAST GROWTH FACTOR RECEPTOR 3; HEPARIN; ISOPROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; PROTEOGLYCAN; FIBROBLAST GROWTH FACTOR RECEPTOR;

ACROCEPHALOSYNDACTYLY; ARTICLE; CRANIOFACIAL DEVELOPMENT; CRANIOFACIAL SYNOSTOSIS; CROUZON SYNDROME; GENE MUTATION; GENETIC COUNSELING; HUMAN; IN VITRO STUDY; IN VIVO STUDY; KNOCKOUT MOUSE; NONHUMAN; ORTHODONTICS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN STRUCTURE; SIGNAL TRANSDUCTION; SOCIAL SUPPORT; ANIMAL; BIOLOGICAL MODEL; FACIAL BONE; GENETICS; GROWTH, DEVELOPMENT AND AGING; MOUSE; MOUSE MUTANT; MUTATION; PHYSIOLOGY; REVIEW; SKULL;

ANIMALS; CRANIOSYNOSTOSES; FACIAL BONES; FIBROBLAST GROWTH FACTORS; HUMANS; MICE; MICE, KNOCKOUT; MODELS, BIOLOGICAL; MUTATION; RECEPTORS, FIBROBLAST GROWTH FACTOR; SIGNAL TRANSDUCTION; SKULL;

EID: 79955002353     PISSN: 10454403     EISSN: None     Source Type: Journal    
DOI: 10.1615/CritRevEukarGeneExpr.v20.i4.20     Document Type: Article

References (132)

1. Murakami M, Simons M. Fibroblast growth factor regulation of neovascularization. Curr Opin Hematol. 2008;15:215-20.
2. Turner N, Grose R. Fibroblast growth factor signalling: from development to cancer. Nat Rev Cancer. 2010;10:116-29.
3. Zhang Y, Gorry MC, Post JC, Ehrlich GD. Genomic organization of the human fbroblast growth factor receptor 2 (FGFR2) gene and comparative analysis of the human FGFR gene family. Gene. 1999;230:69-79.
4. Yayon A, Klagsbrun M, Esko JD, Leder P, Ornitz DM. Cell surface, heparin-like molecules are required for binding of basic fbroblast growth factor to its high afnity receptor. Cell. 1991;64:841-8.
5. Miki T, Bottaro DP, Fleming T P, Smith CL, Burgess WH, Chan AM, Aaronson SA. Determination of ligand-binding specifcity by alternative splicing: two distinct growth factor receptors encoded by a single gene. Proc Natl Acad Sci U S A. 1992;89:246-50.
6. Sakaguchi K, Lorenzi MB, Bottaro DP, Miki R. Te acidic domain and frst immunoglobulin-like loop of fbroblast growth factor receptor 2 modulate downstream signaling through glycosaminoglycan modifcation. Mol Cell Bio. 1999;19: 6754-64.
7. Bashkin P, Doctrow S, Klagsbrun M, Svahn CM, Folk-man J, Vlodavsky I. Basic fbroblast growth factor binds to subendothelial extracellular matrix and is released by heparitinase and heparin-like molecules. Biochemistry. 1989;28:1737-43.
8. Klagsbrun M, Baird A. A dual receptor system is required for basic fbroblast growth factor activity. Cell. 1991;67: 229-31.
9. Mohammadi M, Olsen SK, Ibrahimi OA. Structural basis for fbroblast growth factor receptor activation. Cytokine Growth Factor Rev. 2005;16:107-37.
10. Goetz R, Beenken A, Ibrahimi OA, Kalinina J, Olsen SK, Eliseenkova AV, Xu C, Neubert TA, Zhang F, Linhardt RJ, Yu X, White KE, Inagaki T, Kliewer SA, Yamamoto M, Kurosu H, Ogawa Y, Kuro-o M, Lanske B, Razzaque MS, Mohammadi M. Molecular insights into the klotho-depen-dent, endocrine mode of action of fbroblast growth factor 19 subfamily members. Mol Cell Biol. 2007;27:3417-28.
11. Feige JJ, Baird A. Glycosylation of the basic fbroblast growth factor receptor. Te contribution of carbohydrate to receptor function. J Biol Chem. 1988;263:14023-9.
12. Petrescu AJ, Milac AL, Petrescu SM, Dwek RA, Wormald MR. Statistical analysis of the protein environment of N-glycosylation sites: implications for occupancy, structure, and folding. Glycobiology. 2004;14:103-14.
13. Parodi AJ. Role of N-oligosaccharide endoplasmic reticulum processing reactions in glycoprotein folding and degradation. Biochem J. 2000;348(Pt 1):1-13.
14. Lau KS, Partridge EA, Grigorian A, Silvescu CI, Reinhold VN, Demetriou M, Dennis JW. Complex N-glycan number and degree of branching cooperate to regulate cell proliferation and differentiation. Cell. 2007;129: 123-34.
15. Stanley P. A method to the madness of N-glycan complexity? Cell. 2007;129:27-9.
16. Duchesne L, Tissot B, Rudd TR, Dell A, Fernig DG. N-glycosylation of fbroblast growth factor receptor 1 regulates ligand and heparan sulfate co-receptor binding. J Biol Chem. 2006;281:27178-89.
17. Hatch NE, Hudson M, Seto ML, Cunningham ML, Bothwell M. Intracellular retention, degradation, and signaling of glycosylation-defcient FGFR2 and cran-iosynostosis syndrome-associated FGFR2C278F. J Biol Chem. 2006;281:27292-305.
18. Ornitz DM, Xu J, Colvin JS, McEwen DG, MacArthur CA, Coulier F, Gao G, Goldfarb M. Receptor specifc-ity of the fbroblast growth factor family. J Biol Chem. 1996;271:15292-7.
19. Zhang X, Ibrahimi OA, Olsen SK, Umemori H, Moham-madi M, Ornitz DM. Receptor specifcity of the fbroblast growth factor family. Te complete mammalian FGF family. J Biol Chem. 2006;281:15694-700.
20. Yayon A, Zimmer Y, Shen GH, Avivi A, Yarden Y, Givol D. A confned variable region confers ligand specifcity on fbroblast growth factor receptors: implications for the origin of the immunoglobulin fold. EMBO J. 1992;11:1885-90.
21. Shimizu A, Tada K, Shukunami C, Hiraki Y, Kurokawa T, Magane N, Kurokawa-Seo M. A novel alternatively spliced fbroblast growth factor receptor 3 isoform lacking the acid box domain is expressed during chondrogenic diferentiation of ATDC5 cells. J Biol Chem. 2001;276:11031-40.
22. Burgar HR, Burns HD, Elsden JL, Lalioti MD, Heath JK. Association of the signaling adaptor FRS2 with fbroblast growth factor receptor 1 (Fgfr1) is mediated by alternative splicing of the juxtamembrane domain. J Biol Chem. 2002;277:4018-23.
23. Orr-Urtreger A, Bedford MT, Burakova T, Arman E, Zimmer Y, Yayon A, Givol D, Lonai P. Developmental localization of the splicing alternatives of fbroblast growth factor receptor-2 (FGFR2). Dev Biol. 1993;158:475-86.
24. Mohammadi M, Dikic I, Sorokin A, Burgess WH, Jaye M, Schlessinger J. Identifcation of six novel autophospho-rylation sites on fbroblast growth factor receptor 1 and elucidation of their importance in receptor activation and signal transduction. Mol Cell Biol. 1996;16:977-89.
25. Ceridono M, Belleudi F, Ceccarelli S, Torrisi MR. Tyrosine 769 of the keratinocyte growth factor receptor is required for receptor signaling but not endocytosis. Biochem Biophys Res Commun. 2005;327:523-32.
26. Kong M, Wang CS, Donoghue DJ. Interaction of fbroblast growth factor receptor 3 and the adapter protein SH2-B. A role in STAT5 activation. J Biol Chem. 2002;77: 15962-70.
27. Berridge MJ. Inositol trisphosphate and calcium signalling. Nature. 1993;361:315-25.
28. Ridyard MS, Robbins SM. Fibroblast growth factor-2-induced signaling through lipid raft-associated fbroblast growth factor receptor substrate 2 (FRS2). J Biol Chem. 2003;278:13803-9.
29. Berra E, Díaz-Meco MT, Lozano J, Frutos S, Municio MM, Sánchez P, Sanz L, Moscat J. Evidence for a role of MEK and MAPK during signal transduction by protein kinase C zeta. EMBO J. 1995;14:6157-63.
30. Lim YP, Low BC, Lim J, Wong ES, Guy GR. Association of atypical protein kinase C isotypes with the docker protein FRS2 in fbroblast growth factor signaling. J Biol Chem. 1999;274:19025-34.
31. Tisse B, Tisse C. Functions and regulations of fbroblast growth factor signaling during embryonic development. Dev Biol. 2005;287:390-402.
32. Ong SH, Hadari YR, Gotoh N, Guy GR, Schlessinger J, Lax I. Stimulation of phosphatidylinositol 3-kinase by fbroblast growth factor receptors is mediated by coordinated recruitment of multiple docking proteins. Proc Natl Acad Sci USA. 2001;98:6074-9.
33. Maher P. p38 mitogen-activated protein kinase activation is required for fbroblast growth factor-2-stimulated cell proliferation but not diferentiation. J Biol Chem. 1999;274:17491-8.
34. Suzuki A, Palmer G, Bonjour JP, Caverzasio J. Stimulation of sodium-dependent phosphate transport and signaling mechanisms induced by basic fbroblast growth factor in MC3T3-E1 osteoblast-like cells. J Bone Miner Res. 2000;15:95-102.
35. Lemonnier J, Haÿ E, Delannoy P, Lomri A, Modrowski D, Caverzasio J, Marie PJ. Role of N-cadherin and protein kinase C in osteoblast gene activation induced by the S252W fbroblast growth factor receptor 2 mutation in Apert craniosynostosis. J Bone Miner Res. 2001;16:832-45.
36. Kim HJ, Kim JH, Bae SC, Choi JY, Kim HJ, Ryoo HM. Te protein kinase C pathway plays a central role in the fbroblast growth factor-stimulated expression and transacti-vation activity of Runx2. J Biol Chem. 2003;278:319-26.
37. Chin YE, Kitagawa M, Su WC, You ZH, Iwamoto Y, Fu XY. Cell growth arrest and induction of cyclin-dependent kinase inhibitor p21 WAF1/CIP1 mediated by STAT1. Science. 1996;272:719-22.
38. Su WC, Kitagawa M, Xue N, Xie B, Garofalo S, Cho J, Deng C, Horton WA, Fu XY. Activation of Stat1 by mutant fbroblast growth-factor receptor in thanatophoric dysplasia type II dwarfsm. Nature. 1997;386:288-92.
39. Sahni M, Ambrosetti DC, Mansukhani A, Gertner R, Levy D, Basilico C. FGF signaling inhibits chondrocyte proliferation and regulates bone development through the STAT-1 pathway. Genes Dev. 1999;13:1361-6.
40. Hart KC, Robertson SC, Donoghue DJ. Identifcation of tyrosine residues in constitutively activated fbroblast growth factor receptor 3 involved in mitogenesis, Stat activation, and phosphatidylinositol 3-kinase activation. Mol Biol Cell. 2001;12:931-42.
41. Lax I, Wong A, Lamothe B, Lee A, Frost A, Hawes J, Schlessinger J. Te docking protein FRS2alpha controls a MAP kinase-mediated negative feedback mechanism for signaling by FGF receptors. Mol Cell. 2002;10:709-19.
42. Wong A, Lamothe B, Lee A, Schlessinger J, Lax I. FRS2 alpha attenuates FGF receptor signaling by Grb2-mediated recruitment of the ubiquitin ligase Cbl. Proc Natl Acad Sci USA. 2002;14;99:6684-9.
43. Hacohen N, Kramer S, Sutherland D, Hiromi Y, Krasnow MA. Sprouty encodes a novel antagonist of FGF signaling that patterns apical branching of the Drosophila airways. Cell. 1998;92:253-63.
44. Minowada G, Jarvis LA, Chi CL, Neubüser A, Sun X, Hacohen N, Krasnow MA, Martin GR. Vertebrate Sprouty genes are induced by FGF signaling and can cause chondrodysplasia when overexpressed. Development. 1999;126:4465-75.
45. Hanafusa H, Torii S, Yasunaga T, Nishida E. Sprouty1 and Sprouty2 provide a control mechanism for the Ras/MAPK signalling pathway. Nat Cell Biol. 2002;4:850-8.
46. Fong CW, Leong HF, Wong ES, Lim J, Yusof P, Guy GR. Tyrosine phosphorylation of Sprouty2 enhances its interaction with c-Cbl and is crucial for its function. J Biol Chem. 2003;278:33456-64.
47. Kovalenko D, Yang X, Nadeau RJ, Harkins LK, Friesel R. Sef inhibits fbroblast growth factor signaling by inhibiting FGFR1 tyrosine phosphorylation and subsequent ERK activation. J Biol Chem. 2003;278:14087-91.
48. Deng CX, Wynshaw-Boris A, Shen MM, Daugherty C, Ornitz DM, Leder P. Murine FGFR-1 is required for early postimplantation growth and axial organization. Genes Dev. 1994;8:3045-57.
49. Yamaguchi TP, Harpal K, Henkemeyer M, Rossant J. Fgfr-1 is required for embryonic growth and mesodermal patterning during mouse gastrulation. Genes Dev. 1994;8:3032-44.
50. Ciruna BG, Schwartz L, Harpal K, Yamaguchi TP, Rossant J. Chimeric analysis of fbroblast growth factor receptor-1 (Fgfr1) function: a role for FGFR1 in morphogenetic movement through the primitive streak. Development. 1997;124:2829-41.
51. Xu X, Weinstein M, Li C, Naski M, Cohen RI, Ornitz DM, Leder P, Deng C. Fibroblast growth factor receptor 2 (FGFR2)-mediated reciprocal regulation loop between FGF8 and FGF10 is essential for limb induction. Development. 1998;125:753-65.
52. Arman E, Hafner-Krausz R, Gorivodsky M, Lonai P. Fgfr2 is required for limb outgrowth and lung-branching morphogenesis. Proc Natl Acad Sci USA. 1999;96: 11895-9.
53. Partanen J, Schwartz L, Rossant J. Opposite phenotypes of hypomorphic and Y766 phosphorylation site mutations reveal a function for Fgfr1 in anteroposterior patterning of mouse embryos. Genes Dev. 1998;12:2332-44.
54. Li C, Xu X, Nelson DK, Williams T, Kuehn MR, Deng CX. FGFR1 function at the earliest stages of mouse limb development plays an indispensable role in subsequent au-topod morphogenesis. Development. 2005;132:4755-64.
55. De Moerlooze L, Spencer-Dene B, Revest JM, Hajihosseini M, Rosewell I, Dickson C. An important role for the IIIb isoform of fbroblast growth factor receptor 2 (FGFR2) in mesenchymal-epithelial signalling during mouse organo-genesis. Development. 2000;127:483-92.
56. Eswarakumar VP, Monsonego-Ornan E, Pines M, Anto-nopoulou I, Morriss-Kay GM, Lonai P. Te IIIc alternative of Fgfr2 is a positive regulator of bone formation. Development. 2002;129:3783-93.
57. Yu K, Xu J, Liu Z, Sosic D, Shao J, Olson EN, Towler DA, Ornitz DM. Conditional inactivation of FGF receptor 2 reveals an essential role for FGF signaling in the regulation of osteoblast function and bone growth. Development. 2003;130:3063-74.
58. Deng C, Wynshaw-Boris A, Zhou F, Kuo A, Leder P. Fibroblast growth factor receptor 3 is a negative regulator of bone growth. Cell. 1996;84:911-21.
59. Colvin JS, Bohne BA, Harding GW, McEwen DG, Ornitz DM. Skeletal overgrowth and deafness in mice lacking fbroblast growth factor receptor 3. Nat Genet. 1996;12:390-7.
60. Eswarakumar V P, Schlessinger J. Skeletal overgrowth is mediated by defciency in a specifc isoform of fbro-blast growth factor receptor 3. Proc Natl Acad Sci USA. 2007;104:3937-42.
61. Weinstein M, Xu X, Ohyama K, Deng CX. FGFR-3 and FGFR-4 function cooperatively to direct alveogenesis in the murine lung. Development. 1998;125:3615-23.
62. Yu C, Wang F, Kan M, Jin C, Jones RB, Weinstein M, Deng CX, McKeehan WL. Elevated cholesterol metabolism and bile acid synthesis in mice lacking membrane tyrosine kinase receptor FGFR4. J Biol Chem. 2000;275:15482-9.
63. Huang X, Yang C, Luo Y, Jin C, Wang F, McKeehan WL. FGFR4 prevents hyperlipidemia and insulin resistance but underlies high-fat diet induced fatty liver. Diabetes. 2007;56:2501-10.
64. Cohen MM Jr. Sutural biology and the correlates of cran-iosynostosis. Am J Med Genet. 1993;47:581-616.
65. Zeiger JS, Beaty TH, Hetmanski JB, Wang H, Scott AF, Kasch L, Raymond G, Jabs EW, VanderKolk C. Genetic and environmental risk factors for sagittal craniosynostosis. J Craniofac Surg. 2002;13:602-6.
66. Warren SM, Brunet LJ, Harland RM, Economides AN, Longaker MT. Te BMP antagonist noggin regulates cranial suture fusion. Nature. 2003;422:625-9.
67. Anderson J, Burns HD, Enriquez-Harris P, Wilkie AO, Heath JK. Apert syndrome mutations in fbroblast growth factor receptor 2 exhibit increased afnity for FGF ligand. Hum Mol Genet. 1998;7:1475-83.
68. Yu K, Herr AB, Waksman G, Ornitz DM. Loss of fbro-blast growth factor receptor 2 ligand-binding specifcity in Apert syndrome. Proc Natl Acad Sci USA. 2000;97: 14536-41.
69. Neilson KM, Friesel RE. Constitutive activation of fbroblast growth factor receptor-2 by a point mutation associated with Crouzon syndrome. J Biol Chem. 1995;270:26037-40.
70. Galvin BD, Hart KC, Meyer AN, Webster MK, Donoghue DJ. Constitutive receptor activation by Crouzon syndrome mutations in fbroblast growth factor receptor (FGFR)2 and FGFR2/Neu chimeras. Proc Natl Acad Sci USA. 1996;93:7894-9.
71. Robertson SC, Meyer AN, Hart KC, Galvin BD, Webster MK, Donoghue DJ. Activating mutations in the extracellular domain of the fbroblast growth factor receptor 2 function by disruption of the disulfde bond in the third immunoglobulin-like domain. Proc Natl Acad Sci USA. 1998;95:4567-72.
72. Ibrahimi OA, Zhang F, Eliseenkova AV, Linhardt RJ, Mo-hammadi M. Proline to arginine mutations in FGF receptors 1 and 3 result in Pfeifer and Muenke craniosynostosis syndromes through enhancement of FGF binding afnity. Hum Mol Genet. 2004;13:69-78.
73. Li E, You M, Hristova K. FGFR3 dimer stabilization due to a single amino acid pathogenic mutation. J Mol Biol. 2006;356:600-12.
74. Perlyn CA, Morriss-Kay G, Darvann T, Tenenbaum M, Ornitz DM. A model for the pharmacological treatment of Crouzon syndrome. Neurosurgery. 2006;59:210-5; discussion 210-5.
75. Shukla V, Coumoul X, Wang RH, Kim HS, Deng CX. RNA interference and inhibition of MEK-ERK signaling prevent abnormal skeletal phenotypes in a mouse model of craniosynostosis. Nat Genet. 2007 Sep;39(9):1145-50.
76. Yin L, Du X, Li C, Xu X, Chen Z, Su N, Zhao L, Qi H, Li F, Xue J, Yang J, Jin M, Deng C, Chen L. A Pro253Arg mutation in fbroblast growth factor receptor 2(Fgfr2) causes skeleton malformation mimicking human Apert syndrome by afecting both chondrogenesis and osteogenesis. Bone. 2008;42:631-43.
77. Eswarakumar VP, Ozcan F, Lew ED, Bae JH, Tomé F, Booth CJ, Adams DJ, Lax I, Schlessinger J. Attenuation of signaling pathways stimulated by pathologically activated FGF-receptor 2 mutants prevents craniosynostosis. Proc Natl Acad Sci USA. 2006;103:18603-8.
78. Snyder-Warwick AK, Perlyn CA, Pan J, Yu K, Zhang L, Ornitz DM. 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;107:2515-20.
79. Rutland P, Pulleyn LJ, Reardon W, Baraitser M, Hayward R, Jones B, Malcolm S, Winter RM, Oldridge M, Slaney SF, et al. Identical mutations in the FGFR2 gene cause both Pfeifer and Crouzon syndrome phenotypes. Nat Genet. 1995;9:173-6.
80. Webster MK, Donoghue DJ. FGFR activation in skeletal disorders: too much of a good thing. Trends Genet. 1997;13:178-82.
81. De Moerlooze L, Dickson C. Skeletal disorders associated with fbroblast growth factor receptor mutations. Curr Opin Genet Dev. 1997;7:378-85.
82. Muenke M, Schell U, Hehr A, Robin NH, Losken HW, Schinzel A, Pulleyn LJ, Rutland P, Reardon W, Malcolm S, et al. A common mutation in the fbroblast growth factor receptor 1 gene in Pfeifer syndrome. Nat Genet. 1994;8:269-74.
83. Rossi M, Jones RL, Norbury G, Bloch-Zupan A, Winter RM. Te appearance of the feet in Pfeifer syndrome caused by FGFR1 P252R mutation. Clin Dysmorphol. 2003;12:269-74.
84. Schell U, Hehr A, Feldman GJ, Robin NH, Zackai EH, de Die-Smulders C, Viskochil DH, Stewart JM, Wolf G, Ohashi H, et al. Mutations in FGFR1 and FGFR2 cause familial and sporadic Pfeifer syndrome. Hum Mol Genet. 1995;4:323-8.
85. Lajeunie E, Ma HW, Bonaventure J, Munnich A, Le Mer-rer M, Renier D. FGFR2 mutations in Pfeifer syndrome. Nat Genet. 1995;9:108.
86. Kan SH, Elanko N, Johnson D, Cornejo-Roldan L, Cook J, Reich EW, Tomkins S, Verloes A, Twigg SR, Rannan-Eliya S, McDonald-McGinn DM, Zackai EH, Wall SA, Muenke M, Wilkie AO. Genomic screening of fbroblast growth-factor receptor 2 reveals a wide spectrum of mutations in patients with syndromic craniosynostosis. Am J Hum Genet. 2002;70:472-86.
87. Jabs EW, Li X, Scott AF, Meyers G, Chen W, Eccles M, Mao JI, Charnas LR, Jackson CE, Jaye M. Jackson-Weiss and Crouzon syndromes are allelic with mutations in fbro-blast growth factor receptor 2. Nat Genet. 1994;8:275-9.
88. Jackson CE, Weiss L, Reynolds WA, Forman TF, Peterson JA. Craniosynostosis, midfacial hypoplasia and foot abnormalities: an autosomal dominant phenotype in a large Amish kindred. J Pediatr. 1976;88:963-8.
89. Muenke M, Gripp KW, McDonald-McGinn DM, Gau-denz 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, Adès LC, Haan EA, Mulley JC, Cohen MM Jr, Bellus GA, Francomano CA, Moloney DM, Wall SA, Wilkie AO, et al. A unique point mutation in the fbroblast growth factor receptor 3 gene (FGFR3) defnes a new craniosynostosis syndrome. Am J Hum Genet. 1997;60:555-64.
90. Kimonis V, Gold JA, Hofman TL, Panchal J, Boyadjiev SA. Genetics of craniosynostosis. Semin Pediatr Neurol. 2007;14:150-61.
91. Reardon W, Winter RM, Rutland P, Pulleyn LJ, Jones BM, Malcolm S. Mutations in the fbroblast growth factor receptor 2 gene cause Crouzon syndrome. Nat Genet. 1994;8:98-103.
92. Kreiborg S. Crouzon syndrome. A clinical and roentgen-cephalometric study. Scand J Plast Reconstr Surg. 1981;18 (Suppl):1-198.
93. Meyers GA, Orlow SJ, Munro IR, Przylepa KA, Jabs EW. Fibroblast growth factor receptor 3 (FGFR3) transmembrane mutation in Crouzon syndrome with acanthosis nigricans. Nat Genet. 1995;11:462-4.
94. Wilkes D, Rutland P, Pulleyn LJ, Reardon W, Moss C, Ellis JP, Winter RM, Malcolm S. A recurrent mutation, ala391glu, in the transmembrane region of FGFR3 causes Crouzon syndrome and acanthosis nigricans. J Med Genet. 1996;33:744-8.
95. Schweitzer DN, Graham JM Jr, Lachman RS, et al. Subtle radiographic findings of achondroplasia in patients with Crouzon syndrome with acanthosis nigricans due to an Ala391Glu substitution in FGFR3. Am J Med Genet. 2001;98:75-91.
96. Wilkie AO, Slaney SF, Oldridge M, Poole MD, Ashworth GJ, Hockley AD, Hayward RD, David DJ, Pulleyn LJ, Rutland P, et al. Apert syndrome results from localized mutations of FGFR2 and is allelic with Crouzon syndrome. Nat Genet. 1995;9:165-72.
97. Kreiborg S, Barr M Jr, Cohen MM Jr. Cervical spine in the Apert syndrome. Am J Med Genet. 1992;43:704-8.
98. Cohen MM Jr, Kreiborg S. Skeletal abnormalities in the Apert syndrome. Am J Med Genet. 1993;47:624-32.
99. Glaser RL, Jiang W, Boyadjiev SA, Tran AK, Zachary AA, Van Maldergem L, Johnson D, Walsh S, Oldridge M, Wall SA, Wilkie AO, Jabs EW. Paternal origin of FGFR2 mutations in sporadic cases of Crouzon syndrome and Pfeifer syndrome. Am J Hum Genet. 2000;66:768-77.
100. Goriely A, McVean GA, Röjmyr M, Ingemarsson B, Wilkie AO. Evidence for selective advantage of pathogenic FGFR2 mutations in the male germ line. Science. 2003;301(5633):643-6.
101. Goriely A, McVean GA, van Pelt AM, O'Rourke AW, Wall SA, de Rooij DG, Wilkie AO. Gain-of-function amino acid substitutions drive positive selection of FGFR2 mutations in human spermatogonia. Proc Natl Acad Sci USA. 2005;102:6051-6.
102. Iseki S, Wilkie AO, Heath JK, Ishimaru T, Eto K, Morriss-Kay GM. Fgfr2 and osteopontin domains in the developing skull vault are mutually exclusive and can be altered by locally applied FGF2. Development. 1997;124: 3375-84.
103. Iseki S, Wilkie AO, Morriss-Kay GM. Fgfr1 and Fgfr2 have distinct diferentiation- and proliferation-related roles in the developing mouse skull vault. Development. 1999;126:5611-20.
104. Rice DP, Kim HJ, Teslef I. Apoptosis in murine cal-varial bone and suture development. Eur J Oral Sci. 1999;107:265-75.
105. Lana-Elola E, Rice R, Grigoriadis AE, Rice DP. Cell fate specifcation during calvarial bone and suture development. Dev Biol. 2007;311:335-46.
106. De Pollack C, Renier D, Hott M, Marie PJ. Increased bone formation and osteoblastic cell phenotype in premature cranial suture ossifcation (craniosynostosis). J Bone Miner Res. 1996;11:401-7.
107. Lomri A, Lemonnier J, Hott M, de Parseval N, Lajeunie E, Munnich A, Renier D, Marie PJ. Increased calvaria cell diferentiation and bone matrix formation induced by fbroblast growth factor receptor 2 mutations in Apert syndrome. J Clin Invest. 1998;101:1310-7.
108. Fragale A, Tartaglia M, Bernardini S, Di Stasi AM, Di Rocco C, Velardi F, Teti A, Battaglia PA, Migliaccio S. Decreased proliferation and altered diferentiation in osteoblasts from genetically and clinically distinct craniosynostotic disorders. Am J Pathol. 1999;154:1465-77.
109. Dry GM, Yasinskaya YI, Williams JK, Ehrlich GD, Preston RA, Hu FZ, Gruss JS, Ellenbogen RG, Cunningham ML. Inhibition of apoptosis: a potential mechanism for syndromic craniosynostosis. Plast Reconstr Surg. 2001;107:425-32.
110. Mansukhani A, Bellosta P, Sahni M, Basilico C. Signaling by fbroblast growth factors (FGF) and fbroblast growth factor receptor 2 (FGFR2)-activating mutations blocks mineralization and induces apoptosis in osteoblasts. J Bone Min Res. 2000;149:1297-308.
111. Lemonnier J, Haÿ E, Delannoy P, Fromigué O, Lomri A, Modrowski D, Marie PJ. Increased osteoblast apoptosis in Apert craniosynostosis: role of protein kinase C and interleukin-1. Am J Pathol. 2001;158:1833-42.
112. Petiot A, Ferretti P, Copp AJ, Chan CT. Induction of chondrogenesis in neural crest cells by mutant fbroblast growth factor receptors. Dev Dyn. 2002;224:210-21.
113. Ratisoontorn C, Fan GF, McEntee K, Nah HD. Activating (P253R, C278F) and dominant negative mutations of FGFR2: diferential efects on calvarial bone cell proliferation, diferentiation, and mineralization. Connect Tissue Res. 2003;44(Suppl 1):292-7.
114. Yang F, Wang Y, Zhang Z, Hsu B, Jabs EW, Elisseef JH. Te study of abnormal bone development in the Apert syndrome Fgfr2+/S252W mouse using a 3D hydrogel culture model. Bone. 2008;43:55-63.
115. Miraoui H, Oudina K, Petite H, Tanimoto Y, Moriyama K, Marie PJ. Fibroblast growth factor receptor 2 promotes osteogenic diferentiation in mesenchymal cells via ERK1/2 and protein kinase C signaling. J Biol Chem. 2009;284:4897-904.
116. Eswarakumar VP, Horowitz MC, Locklin R, Morriss-Kay GM, Lonai P. A gain-of-function mutation of Fgfr2c demonstrates the roles of this receptor variant in osteogenesis. Proc Natl Acad Sci USA. 2004;101:12555-60.
117. Chen L, Li D, Li C, Engel A, Deng CX. A Ser252Trp [corrected] substitution in mouse fbroblast growth factor receptor 2 (Fgfr2) results in craniosynostosis. Bone. 2003;33:169-78.
118. Yin L, Du X, Li C, Xu X, Chen Z, Su N, Zhao L, Qi H, Li F, Xue J, Yang J, Jin M, Deng C, Chen L. A Pro253Arg mutation in fbroblast growth factor receptor 2 (Fgfr2) causes skeleton malformation mimicking human Apert syndrome by afecting both chondrogenesis and osteogenesis. Bone. 2008;42:631-43.
119. Wang Y, Sun M, Uhlhorn VL, Zhou X, Peter I, Martinez-Abadias N, Hill CA, Percival CJ, Richtsmeier J T, Huso DL, Jabs EW. Activation of p38 MAPK pathway in the skull abnormalities of Apert syndrome Fgfr2(+P253R) mice. BMC Dev Biol. 2010;10:22.
120. Twigg SR, Healy C, Babbs C, Sharpe JA, Wood WG, Sharpe PT, Morriss-Kay GM, Wilkie AO. Skeletal analysis of the Fgfr3(P244R) mouse, a genetic model for the Muenke craniosynostosis syndrome. Dev Dyn. 2009;238: 331-42.
121. Zhou YX, Xu X, Chen L, Li C, Brodie SG, Deng CX. A Pro250Arg substitution in mouse Fgfr1 causes increased expression of Cbfa1 and premature fusion of calvarial sutures. Hum Mol Genet. 2000;9:2001-8.
122. White KE, Cabral JM, Davis SI, Fishburn T, Evans WE, Ichikawa S, Fields J, Yu X, Shaw NJ, McLellan NJ, McKeown C, Fitzpatrick D, Yu K, Ornitz DM, Econs MJ. Mutations that cause osteoglophonic dysplasia defne novel roles for FGFR1 in bone elongation. Am J Hum Genet. 2005;76:361-7.
123. Roy WA, Iorio RJ, Meyer GA. Craniosynostosis in vitamin D-resistant rickets. A mouse model. J Neurosurg. 1981;55:265-71.
124. Sabbagh Y, Jones AO, Tenenhouse HS. PHEXdb, a locus-specifc database for mutations causing X-linked hypophosphatemia. Hum Mutat. 2000;16:1-6.
125. Liang G, Katz LD, Insogna KL, Carpenter TO, Macica CM. Survey of the enthesopathy of X-linked hypophosphatemia and its characterization in Hyp mice. Calcif Tissue Int. 2009;85:235-46.
126. Wenkert D, Benigno M, Mack K, McAlister W, Mumm S and Whyte M. 2009. Hypophosphatasia: Prevalence of clinical problems in 175 pediatric patients. American Society for Bone and Mineral Research 31st Annual Meeting, Denver, CO. Abstract A09001674.
127. Mornet E. Hypophosphatasia. Orphanet J Rare Dis. 2007;2:40.
128. Murshed M, Harmey D, Millán JL, McKee MD, Karsenty G. Unique coexpression in osteoblasts of broadly expressed genes accounts for the spatial restriction of ECM mineralization to bone. Genes Dev. 2005; 19:1093-104.
129. Narisawa S, Fröhlander N, Millán JL. Inactivation of two mouse alkaline phosphatase genes and establishment of a model of infantile hypophosphatasia. Dev Dyn. 1997; 208:432-46.
130. Spector JA, Greenwald JA, Warren SM, Bouletreau PJ, Detch RC, Fagenholz PJ, Crisera FE, Longaker MT. Dura mater biology: autocrine and paracrine efects of fbroblast growth factor 2. Plast Reconstr Surg. 2002;109:645-54.
131. Rodan SB, Wesolowski G, Tomas KA, Yoon K, Rodan GA. Efects of acidic and basic fbroblast growth factors on osteoblastic cells. Connect Tissue Res. 1989;20:283-8.
132. Hatch NE, Nociti F, Swanson E, Bothwell M, Somerman M. FGF2 alters expression of the pyrophosphate/phosphate regulating proteins, PC-1, ANK and TNAP, in the calva-rial osteoblastic cell line, MC3T3E1(C4). Connect Tissue Res. 2005;46:184-92.