Skeletal morphogenesis during embryonic development

Critical Reviews in Eukaryotic Gene Expression

Volumn 19, Issue 3, 2009, Pages 197-218

  Yang, Yingzi ^a  

^a NATIONAL HUMAN GENOME RESEARCH INSTITUTE   (United States)

Author keywords

Bone; Cartilage; Cell signaling; Chondrocyte; Growth plate; Osteoblast; Osteochondral progenitors; Patterning; Transcription factor

Indexed keywords

PAIRED BOX TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR MSX1; TRANSCRIPTION FACTOR MSX2; TRANSCRIPTION FACTOR RUNX2; TRANSCRIPTION FACTOR SOX9;

CARTILAGE; CARTILAGE CELL; CELL DIFFERENTIATION; CELL INTERACTION; CELL PROLIFERATION; CELL SURVIVAL; CRANIOFACIAL MORPHOLOGY; EMBRYO PATTERN FORMATION; ENCHONDRAL OSSIFICATION; LIMB DEVELOPMENT; MESENCHYME CELL; MESODERM; MORPHOGENESIS; MUSCULOSKELETAL DEVELOPMENT; OSSIFICATION; OSTEOBLAST; OSTEOCYTE; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; SKELETON; STEM CELL; TRANSCRIPTION REGULATION; VERTEBRATE;

ANIMALIA; VERTEBRATA;

ANIMALS; BONE AND BONES; CALCIFICATION, PHYSIOLOGIC; CARTILAGE; CELL DIFFERENTIATION; CHONDROCYTES; EMBRYONIC DEVELOPMENT; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; MESENCHYMAL STEM CELLS; OSTEOBLASTS; OSTEOGENESIS; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

EID: 67650281205     PISSN: 10454403     EISSN: None     Source Type: Journal    
DOI: 10.1615/CritRevEukarGeneExpr.v19.i3.30     Document Type: Review

References (187)

1. Basch ML, Garcia-Castro MI, Bronner-Fraser M. Molecular mechanisms of neural crest induction. Birth Defects Res C Embryo Today. 2004;72(2):109-23.
2. Santagati F, Rijli FM. Cranial neural crest and the building of the vertebrate head. Nat Rev Neurosci. 2003;4(10):806-18.
3. Helms JA, Cordero D, Tapadia MD. New insights into craniofacial morphogenesis. Development. 2005;132(5):851-61.
4. Crump JG, Maves L, Lawson ND, Weinstein BM, Kimmel CB. An essential role for Fgfs in endodermal pouch formation influences later craniofacial skeletal patterning. Development. 2004;131(22):5703-16.
5. Walshe J, Mason I. Fgf signalling is required for formation of cartilage in the head. Dev Biol. 2003;264(2):522-36.
6. Richman JM, Herbert M, Matovinovic E, Walin J. Effect of fibroblast growth factors on outgrowth of facial mesenchyme. Dev Biol. 1997;189(1):135-47.
7. Goodnough LH, Brugmann SA, Hu D, Helms JA. Stage-dependent craniofacial defects resulting from Sprouty2 overexpression. Dev Dyn. 2007;236(7):1918-28.
8. Abzhanov A, Protas M, Grant BR, Grant PR, Tabin CJ. Bmp4 and morphological variation of beaks in Darwin's finches. Science. 2004;305 (5689):1462-5.
9. Christ B, Huang R, Scaal M. Formation and differentiation of the avian sclerotome. Anat Embryol (Berl). 2004;208(5):333-50.
10. Gossler A, Hrabe de Angelis M. Somitogenesis. Curr Top Dev Biol. 1998;38:225-87.
11. Hirsinger E, Jouve C, Dubrulle J, Pourquie O. Somite formation and patterning. Int Rev Cytol. 2000;198:1-65.
12. Scaal M, Christ B. Formation and differentiation of the avian dermomyotome. Anat Embryol (Berl). 2004;208(6):411-24.
13. Aulehla A, Pourquie O. On periodicity and directionality of somitogenesis. Anat Embryol (Berl). 2006;211(Suppl 1):3-8.
14. Dequeant ML, Glynn E, Gaudenz K, Wahl M, Chen J, Mushegian A, Pourquié O. A complex oscillating network of signaling genes underlies the mouse segmentation clock. Science. 2006;314 (5805):1595-8.
15. Ilagan MX, Kopan R. SnapShot: notch signaling pathway. Cell. 2007;128(6):1246.
16. Rida PC, Le Minh N, Jiang YJ. A Notch feeling of somite segmentation and beyond. Dev Biol. 2004;265(1):2-22.
17. Bessho Y, Hirata H, Masamizu Y, Kageyama R. Periodic repression by the bHLH factor Hes7 is an essential mechanism for the somite segmentation clock. Genes Dev. 2003;17(12):1451-6.
18. Dale JK, Maroto M, Dequeant ML, Malapert P, McGrew M, Pourquie O. Periodic notch inhibition by lunatic fringe underlies the chick segmentation clock. Nature. 2003;421 (6920):275-8.
19. Serth K, Schuster-Gossler K, Cordes R, Gossler A. Transcriptional oscillation of lunatic fringe is essential for somitogenesis. Genes Dev. 2003;17(7):912-25.
20. Aulehla A, Wehrle C, Brand-Saberi B, Kemler R, Gossler A, Kanzler B, Herrmann B. Wnt3a plays a major role in the segmentation clock controlling somitogenesis. Dev Cell. 2003;4(3):395-406.
21. Ishikawa A, Kitajima S, Takahashi Y, Kokubo H, Kanno J, Inoue T, Saga Y. Mouse Nkd1, a Wnt antagonist, exhibits oscillatory gene expression in the PSM under the control of Notch signaling. Mech Dev. 2004;121(12):1443-53.
22. Greco TL, Takada S, Newhouse MM, McMahon JA, McMahon AP, Camper SA. Analysis of the vestigial tail mutation demonstrates that Wnt-3a gene dosage regulates mouse axial development. Genes Dev. 1996;10(3):313-24.
23. Biris KK, Dunty WC Jr, Yamaguchi TP. Mouse Ripply2 is downstream of Wnt3a and is dynamically expressed during somitogenesis. Dev Dyn. 2007;236(11):3167-72.
24. Sakai Y, Meno C, Fujii H, Nishino J, Shiratori H, Saijoh Y, Rossant J, Hamada H. The retinoic acid-inactivating enzyme CYP26 is essential for establishing an uneven distribution of retinoic acid along the anterio-posterior axis within the mouse embryo. Genes Dev. 2001;15(2):213-25.
25. Blentic A, Gale E, Maden M. Retinoic acid signalling centres in the avian embryo identified by sites of expression of synthesising and catabolising enzymes. Dev Dyn. 2003;227(1):114-27.
26. Moreno TA, Kintner C. Regulation of segmental patterning by retinoic acid signaling during Xenopus somitogenesis. Dev Cell. 2004;6(2):205-18.
27. Dubrulle J, McGrew MJ, Pourquie O. FGF signaling controls somite boundary position and regulates segmentation clock control of spatiotemporal Hox gene activation. Cell. 2001;106(2):219-32.
28. Dubrulle J, Pourquie O. Coupling segmentation to axis formation. Development. 2004;131(23):5783-93.
29. Diez del Corral R, Olivera-Martinez I, Goriely A, Gale E, Maden M, Storey K. Opposing FGF and retinoid pathways control ventral neural pattern, neuronal differentiation, and segmentation during body axis extension. Neuron. 2003;40(1):65-79.
30. Maden M, Graham A, Zile M, Gale E. Abnormalities of somite development in the absence of retinoic acid. Int J Dev Biol. 2000;44(1):151-9.
31. Vermot J, Gallego Llamas J, Fraulob V, Niederreither K, Chambon P, Dolle P. Retinoic acid controls the bilateral symmetry of somite formation in the mouse embryo. Science. 2005;308 (5721):563-6.
32. Vermot J, Pourquie O. Retinoic acid coordinates somitogenesis and left-right patterning in vertebrate embryos. Nature. 2005;435 (7039):215-20.
33. Sirbu IO, Duester G. Retinoic-acid signalling in node ectoderm and posterior neural plate directs left-right patterning of somitic mesoderm. Nat Cell Biol. 2006;8(3):271-7.
34. Kawamura A, Koshida S, Hijikata H, Sakaguchi T, Kondoh H, Takada S. Zebrafish hairy/enhancer of split protein links FGF signaling to cyclic gene expression in the periodic segmentation of somites. Genes Dev. 2005;19(10):1156-61.
35. Shifley ET, Cole SE. The vertebrate segmentation clock and its role in skeletal birth defects. Birth Defects Res C Embryo Today. 2007;81(2):121-33.
36. Turnpenny PD, Alman B, Cornier AS, Giampietro PF, Offiah A, Tassy O, Pourquié O, Kusumi K, Dunwoodie S. Abnormal vertebral segmentation and the notch signaling pathway in man. Dev Dyn. 2007;236(6):1456-74.
37. Krantz ID, Colliton RP, Genin A, Rand EB, Li L, Piccoli DA, Spinner NB. Spectrum and frequency of jagged1 (JAG1) mutations in Alagille syndrome patients and their families. Am J Hum Genet. 1998;62(6):1361-9.
38. Li L, Krantz ID, Deng Y, Genin A, Banta AB, Collins CC, Qi M, Trask BJ, Kuo WL, Cochran J, Costa T, Pierpont ME, Rand EB, Piccoli DA, Hood L, Spinner NB. Alagille syndrome is caused by mutations in human Jagged1, which encodes a ligand for Notch1. Nat Genet. 1997;16(3):243-51.
39. Oda T, Elkahloun AG, Pike BL, Okajima K, Krantz ID, Genin A, Piccoli DA, Meltzer PS, Spinner NB, Collins FS, Chandrasekharappa SC. Mutations in the human Jagged1 gene are responsible for Alagille syndrome. Nat Genet. 1997;16(3):235-42.
40. McCright B, Lozier J, Gridley T. A mouse model of Alagille syndrome: Notch2 as a genetic modifier of Jag1 haploinsufficiency. Development. 2002;129(4):1075-82.
41. McDaniell R, Warthen DM, Sanchez-Lara PA, Pai A, Krantz ID, Piccoli DA, Spinner NB. NOTCH2 mutations cause Alagille syndrome, a heterogeneous disorder of the notch signaling pathway. Am J Hum Genet. 2006;79(1):169-73.
42. McCright B, Gao X, Shen L, Lozier J, Lan Y, Maguire M, Herzlinger D, Weinmaster G, Jiang R, Gridley T. Defects in development of the kidney, heart and eye vasculature in mice homozygous for a hypomorphic Notch2 mutation. Development. 2001;128(4):491-502.
43. Barrow JR, Thomas KR, Boussadia-Zahui O, Moore R, Kemler R, Capecchi MR, McMahon AP. Ectodermal Wnt3/beta-catenin signaling is required for the establishment and maintenance of the apical ectodermal ridge. Genes Dev. 2003;17(3):394-409.
44. Kamath BM, Stolle C, Bason L, Colliton RP, Piccoli DA, Spinner NB, Krantz ID. Craniosynostosis in Alagille syndrome. Am J Med Genet. 2002;112(2):176-80.
45. Kamath BM, Loomes KM, Oakey RJ, Krantz ID. Supernumerary digital flexion creases: an additional clinical manifestation of Alagille syndrome. Am J Med Genet. 2002;112(2):171-5.
46. Fan CM, Tessier-Lavigne M. Patterning of mammalian somites by surface ectoderm and notochord: evidence for sclerotome induction by a hedgehog homolog. Cell. 1994;79(7):1175-86.
47. Johnson RL, Laufer E, Riddle RD, Tabin C. Ectopic expression of Sonic hedgehog alters dorsal-ventral patterning of somites. Cell. 1994;79(7):1165-73.
48. Fan CM, Lee CS, Tessier-Lavigne M. A role for WNT proteins in induction of dermomyotome. Dev Biol. 1997;191(1):160-5.
49. Capdevila J, Tabin C, Johnson RL. Control of dorsoventral somite patterning by Wnt-1 and beta-catenin. Dev Biol. 1998;193(2):182-94.
50. Brand-Saberi B, Ebensperger C, Wilting J, Balling R, Christ B. The ventralizing Effect of the notochord on somite differentiation in chick embryos. Anat Embryol (Berl). 1993;188(3):239-45.
51. Koseki H, Wallin J, Wilting J, Mizutani Y, Kispert A, Ebensperger C, Herrmann BG, Christ B, Balling R. A role for Pax-1 as a mediator of notochordal signals during the dorsoventral specification of vertebrae. Development. 1993;119(3):649-60.
52. Chiang C, Litingtung Y, Lee E, Young KE, Corden JL, Westphal H, Beachy PA. Cyclopia and defective axial patterning in mice lacking Sonic hedgehog gene function. Nature. 1996;383 (6599):407-13.
53. Wallin J, Wilting J, Koseki H, Fritsch R, Christ B, Balling R. The role of Pax-1 in axial skeleton development. Development. 1994;120(5):1109-21.
54. Niswander L, Tickle C, Vogel A, Booth I, Martin GR. FGF-4 replaces the apical ectodermal ridge and directs outgrowth and patterning of the limb. Cell. 1993;75(3):579-87.
55. Crossley PH, Minowada G, MacArthur CA, Martin GR. Roles for FGF8 in the induction, initiation, and maintenance of chick limb development. Cell. 1996;84(1):127-36.
56. Sun X, Mariani FV, Martin GR. Functions of FGF signalling from the apical ectodermal ridge in limb development. Nature. 2002;418 (6897):501-8.
57. Ohuchi H, Nakagawa T, Yamamoto A, Araga A, Ohata T, Ishimaru Y, Yoshioka H, Kuwana T, Nohno T, Yamasaki M, Itoh N, Noji S. The mesenchymal factor, FGF10, initiates and maintains the outgrowth of the chick limb bud through interaction with FGF8, an apical ectodermal factor. Development. 1997;124(11):2235-44.
58. Sekine K, Ohuchi H, Fujiwara M, Yamasaki M, Yoshizawa T, Sato T, Yagishita N, Matsui D, Koga Y, Itoh N, Kato S. Fgf10 is essential for limb and lung formation. Nat Genet. 1999;21(1):138-41.
59. Min H, Danilenko DM, Scully SA, Bolon B, Ring BD, Tarpley JE, DeRose M, Simnonet WS. Fgf-10 is required for both limb and lung development and exhibits striking functional similarity to Drosophila branchless. Genes Dev. 1998;12(20):3156-61.
60. Globus M, Vethamany-Globus S. An in vitro analogue of early chick limb bud outgrowth. Differentiation. 1976;6(2):91-6.
61. Summerbell D, Lewis JH. Time, place and positional value in the chick limb-bud. J Embryol Exp Morphol. 1975;33(3):621-43.
62. Dudley AT, Ros MA, Tabin CJ. A re-examination of proximodistal patterning during vertebrate limb development. Nature. 2002;418 (6897):539-44.
63. Capdevila J, Tsukui T, Rodriquez Esteban C, Zappavigna V, Izpisua Belmonte JC. Control of vertebrate limb outgrowth by the proximal factor Meis2 and distal antagonism of BMPs by Gremlin. Mol Cell. 1999;4(5):839-49.
64. Mercader N, Leonardo E, Piedra ME, Martinez AC, Ros MA, Torres M. Opposing RA and FGF signals control proximodistal vertebrate limb development through regulation of Meis genes. Development. 2000;127(18):3961-70.
65. Saunders JWJ, Gasseling MT. Ectoderm-mesenchymal interaction in the origin of wing symmetry. In: Fleischmajer R, Billingham RE, editors. Epithelia-Mesenchymal Interactions. Baltimore: Williams and Wilkins; 1968: 78-97.
66. Riddle RD, Johnson RL, Laufer E, Tabin C. Sonic hedgehog mediates the polarizing activity of the ZPA. Cell. 1993;75(7):1401-16.
67. Chan DC, Laufer E, Tabin C, Leder P. Polydactylous limbs in Strong's Luxoid mice result from ectopic polarizing activity. Development. 1995;121(7):1971-8.
68. Ericson J, Morton S, Kawakami A, Roelink H, Jessell TM. Two critical periods of Sonic Hedgehog signaling required for the specification of motor neuron identity. Cell. 1996;87(4):661-73.
69. Chiang C, Litingtung Y, Harris MP, Simandl BK, Li Y, Beachy PA, Fallon JF. Manifestation of the limb prepattern: limb development in the absence of sonic hedgehog function. Dev Biol. 2001;236(2):421-35.
70. Yang Y, Drossopoulou G, Chuang PT, Duprez D, Marti E, Bumcrot D, Vargesson N, Clarke J, Niswander L, McMahon A, Tickle C. Relationship between dose, distance and time in Sonic Hedgehog-mediated regulation of anteroposterior polarity in the chick limb. Development. 1997;124(21):4393-404.
71. Harfe BD, Scherz PJ, Nissim S, Tian H, McMahon AP, Tabin CJ. Evidence for an expansion-based temporal Shh gradient in specifying vertebrate digit identities. Cell. 2004;118(4):517-28.
72. Ahn S, Joyner AL. Dynamic changes in the response of cells to positive hedgehog signaling during mouse limb patterning. Cell. 2004;118(4):505-16.
73. te Welscher P, Fernandez-Teran M, Ros MA, Zeller R. Mutual genetic antagonism involving GLI3 and dHAND prepatterns the vertebrate limb bud mesenchyme prior to SHH signaling. Genes Dev. 2002;16(4):421-6.
74. Charite J, McFadden DG, Olson EN. The bHLH transcription factor dHAND controls Sonic hedgehog expression and establishment of the zone of polarizing activity during limb development. Development. 2000;127(11):2461-70.
75. Fernandez-Teran M, Piedra ME, Kathiriya IS, Srivastava D, Rodriguez-Rey JC, Ros MA. Role of dHAND in the anterior-posterior polarization of the limb bud: implications for the Sonic hedgehog pathway. Development. 2000;127(10):2133-42.
76. Firulli BA, Krawchuk D, Centonze VE, Vargesson N, Virshup DM, Conway SJ, Cserjesi P, Laufer E, Firulli AB. Altered Twist1 and Hand2 dimerization is associated with Saethre-Chotzen syndrome and limb abnormalities. Nat Genet. 2005 Apr; 37(4):373-81.
77. Tickle C. Patterning systems--from one end of the limb to the other. Dev Cell. 2003;4(4):449-58.
78. Niswander L. Interplay between the molecular signals that control vertebrate limb development. Int J Dev Biol. 2002;46(7):877-81.
79. Riddle RD, Ensini M, Nelson C, Tsuchida T, Jessell TM, Tabin C. Induction of the LIM homeobox gene Lmx1 by WNT7a establishes dorsoventral pattern in the vertebrate limb. Cell. 1995;83(4):631-40.
80. Parr BA, Shea MJ, Vassileva G, McMahon AP. Mouse Wnt genes exhibit discrete domains of expression in the early embryonic CNS and limb buds. Development. 1993;119(1):247-61.
81. Parr BA, McMahon AP. Dorsalizing signal Wnt-7a required for normal polarity of D-V and A-P axes of mouse limb. Nature. 1995;374 (6520):350-3.
82. Cygan JA, Johnson RL, McMahon AP. Novel regulatory interactions revealed by studies of murine limb pattern in Wnt-7a and En-1 mutants. Development. 1997;124(24):5021-32.
83. Loomis CA, Harris E, Michaud J, Wurst W, Hanks M, Joyner AL. The mouse Engrailed-1 gene and ventral limb patterning. Nature. 1996;382 (6589):360-3.
84. Loomis CA, Kimmel RA, Tong CX, Michaud J, Joyner AL. Analysis of the genetic pathway leading to formation of ectopic apical ectodermal ridges in mouse Engrailed-1 mutant limbs. Development. 1998;125(6):1137-48.
85. Francis-West PH, Robertson KE, Ede DA, Rodriguez C, Izpisua-Belmonte JC, Houston B, Burt DW, Gribbin C, Brickell PM, Tickle C. Expression of genes encoding bone morphogenetic proteins and sonic hedgehog
86. Francis PH, Richardson MK, Brickell PM, Tickle C. Bone morphogenetic proteins and a signalling pathway that controls patterning in the developing chick limb. Development. 1994;120(1):209-18.
87. Lyons KM, Pelton RW, Hogan BL. Organogenesis and pattern formation in the mouse: RNA distribution patterns suggest a role for bone morphogenetic protein-2A (BMP-2A). Development. 1990;109(4):833-44.
88. Ahn K, Mishina Y, Hanks MC, Behringer RR, Crenshaw EB, 3rd. BMPR-IA signaling is required for the formation of the apical ectodermal ridge and dorsal-ventral patterning of the limb. Development. 2001;128(22):4449-61.
89. Pizette S, Abate-Shen C, Niswander L. BMP controls proximodistal outgrowth, via induction of the apical ectodermal ridge, and dorsoventral patterning in the vertebrate limb. Development. 2001;128(22):4463-74.
90. Lallemand Y, Nicola MA, Ramos C, Bach A, Cloment CS, Robert B. Analysis of Msx1; Msx2 double mutants reveals multiple roles for Msx genes in limb development. Development. 2005;132(13):3003-14.
91. Ovchinnikov DA, Selever J, Wang Y, Chen YT, Mishina Y, Martin JF, Behringer RR. BMP receptor type IA in limb bud mesenchyme regulates distal outgrowth and patterning. Dev Biol. 2006;295(1):103-15.
92. Khokha MK, Hsu D, Brunet LJ, Dionne MS, Harland RM. Gremlin is the BMP antagonist required for maintenance of Shh and Fgf signals during limb patterning. Nat Genet. 2003;34(3):303-7.
93. Niswander L, Jeffrey S, Martin GR, Tickle C. A positive feedback loop coordinates growth and patterning in the vertebrate limb. Nature. 1994;371 (6498):609-12.
94. Laufer E, Nelson CE, Johnson RL, Morgan BA, Tabin C. Sonic hedgehog and Fgf-4 act through a signaling cascade and feedback loop to integrate growth and patterning of the developing limb bud. Cell. 1994;79(6):993-1003.
95. Yang Y, Niswander L. Interaction between the signaling molecules WNT7a and SHH during vertebrate limb development: dorsal signals regulate anteroposterior patterning. Cell. 1995;80(6):939-47.
96. Komori T, Yagi H, Nomura S, Yamaguchi A, Sasaki K, Deguchi K, Shimizu Y, Bronson RT, Gao YH, Inada M, Sato M, Okamoto R, Kitamura Y, Yoshiki S, Kishimoto T. Targeted disruption of Cbfa1 results in a complete lack of bone formation owing to maturational arrest of osteoblasts. Cell. 1997;89(5):755-64.
97. Otto F, Thornell AP, Crompton T, Denzel A, Gilmour KC, Rosewell IR, Stamp GW, Beddington RS, Mundlos S, Olsen BR, Selby PB, Owen MJ. Cbfa1, a candidate gene for cleidocranial dysplasia syndrome, is essential for osteoblast differentiation and bone development. Cell. 1997;89(5):765-71.
98. Ducy P, Zhang R, Geoffroy V, Ridall AL, Karsenty G. Osf2/Cbfa1: a transcriptional activator of osteoblast differentiation. Cell. 1997;89(5):747-54.
99. Bi W, Deng JM, Zhang Z, Behringer RR, de Crombrugghe B. Sox9 is required for cartilage formation. Nat Genet. 1999;22(1):85-9.
100. Akiyama H, Chaboissier MC, Martin JF, Schedl A, de Crombrugghe B. The transcription factor Sox9 has essential roles in successive steps of the chondrocyte differentiation pathway and is required for expression of Sox5 and Sox6. Genes Dev. 2002;16(21):2813-28.
101. Akiyama H, Kim JE, Nakashima K, Balmes G, Iwai N, Deng JM, Zhang Z, Martin JF, Behringer RR, Nakamura T, de Crombrugghe B. Osteo-chondroprogenitor cells are derived from Sox9 expressing precursors. Proc Natl Acad Sci USA. 2005;102(41):14665-70.
102. Topol L, Jiang X, Choi H, Garrett-Beal L, Carolan PJ, Yang Y. Wnt-5a inhibits the canonical Wnt pathway by promoting GSK-3-independent {beta}-catenin degradation. J Cell Biol. 2003;162(5):899-908.
103. DasGupta R, Fuchs E. Multiple roles for activated LEF/TCF transcription complexes during hair follicle development and differentiation. Development. 1999;126(20):4557-68.
104. Hartmann C, Tabin CJ. Dual roles of Wnt signaling during chondrogenesis in the chicken limb. Development. 2000;127(14):3141-59.
105. Guo X, Day TF, Jiang X, Garrett-Beal L, Topol L, Yang Y. Wnt/beta-catenin signaling is suffcient and necessary for synovial joint formation. Genes Dev. 2004;18(19):2404-17.
106. Day TF, Guo X, Garrett-Beal L, Yang Y. Wnt/betacatenin signaling in mesenchymal progenitors controls osteoblast and chondrocyte differentiation during vertebrate skeletogenesis. Dev Cell. 2005;8(5):739-50.
107. Hill TP, Spater D, Taketo MM, Birchmeier W, Hartmann C. Canonical Wnt/beta-catenin signaling prevents osteoblasts from differentiating into chondrocytes. Dev Cell. 2005;8(5):727-38.
108. Hu H, Hilton MJ, Tu X, Yu K, Ornitz DM, Long F. Sequential roles of Hedgehog and Wnt signaling in osteoblast development. Development. 2005;132(1):49-60.
109. St-Jacques B, Hammerschmidt M, McMahon AP. Indian hedgehog signaling regulates proliferation and differentiation of chondrocytes and is essential for bone formation. Genes Dev. 1999;13(16):2072-86.
110. Long F, Chung UI, Ohba S, McMahon J, Kronenberg HM, McMahon AP. Ihh signaling is directly required for the osteoblast lineage in the endochondral skeleton. Development. 2004;131(6):1309-18.
111. Nakashima K, Zhou X, Kunkel G, Zhang Z, Deng JM, Behringer RR, de Crombrugghe B. The novel zinc finger-containing transcription factor osterix is required for osteoblast differentiation and bone formation. Cell. 2002;108(1):17-29.
112. Mak KK, Chen MH, Day TF, Chuang PT, Yang Y. Wnt/beta-catenin signaling interacts differentially with Ihh signaling in controlling endochondral bone and synovial joint formation. Development. 2006 Sep; 133(18):3695-707.
113. Rodda SJ, McMahon AP. Distinct roles for Hedgehog and canonical Wnt signaling in specification, differentiation and maintenance of osteoblast progenitors. Development. 2006;133(16):3231-44.
114. Baksh D, Boland GM, Tuan RS. Cross-talk between Wnt signaling pathways in human mesenchymal stem cells leads to functional antagonism during osteogenic differentiation. J Cell Biochem. 2007;101(5):1109-24.
115. Wozney JM. Bone morphogenetic proteins. Prog Growth Factor Res. 1989;1(4):267-80.
116. Derynck R, Zhang YE. Smad-dependent and Smadindependent pathways in TGF-beta family signalling. Nature. 2003;425 (6958):577-84.
117. Zimmerman LB, De Jesus-Escobar JM, Harland RM. The Spemann organizer signal noggin binds and inactivates bone morphogenetic protein 4. Cell. 1996;86(4):599-606.
118. Sasai Y, Lu B, Steinbeisser H, De Robertis EM. Regulation of neural induction by the Chd and Bmp-4 antagonistic patterning signals in Xenopus. Nature. 1995;376 (6538):333-6.
119. Holley SA, Jackson PD, Sasai Y, Lu B, De Robertis EM, Hoffmann FM, Ferguson EL. A conserved system for dorsal-ventral patterning in insects and vertebrates involving sog and chordin. Nature. 1995;376 (6537):249-53.
120. Schmidt J, Francois V, Bier E, Kimelman D. Drosophila short gastrulation induces an ectopic axis in Xenopus: evidence for conserved mechanisms of dorsal-ventral patterning. Development. 1995;121(12):4319-28.
121. Brunet LJ, McMahon JA, McMahon AP, Harland RM. Noggin, cartilage morphogenesis, and joint formation in the mammalian skeleton. Science. 1998;280 (5368):1455-7.
122. Warren SM, Brunet LJ, Harland RM, Economides AN, Longaker MT. The BMP antagonist noggin regulates cranial suture fusion. Nature. 2003;422 (6932):625-9.
123. Wan DC, Pomerantz JH, Brunet LJ, Kim JB, Chou YF, Wu BM, Harland R, Blau HM, Longaker MT. Noggin suppression enhances in vitro osteogenesis and accelerates in vivo bone formation. J Biol Chem. 2007;282(36):26450-9.
124. Pizette S, Niswander L. BMPs are required at two steps of limb chondrogenesis: formation of prechondrogenic condensations and their differentiation into chondrocytes. Dev Biol. 2000;219(2):237-49.
125. Yoon BS, Ovchinnikov DA, Yoshii I, Mishina Y, Behringer RR, Lyons KM. Bmpr1a and Bmpr1b have overlapping functions and are essential for chondrogenesis in vivo. Proc Natl Acad Sci USA. 2005;102(14):5062-7.
126. Mishina Y, Starbuck MW, Gentile MA, Fukuda T, Kasparcova V, Seedor JG, Hanks MC, Amling M, Pinero GJ, Harada S, Behringer RR. Bone morphogenetic protein type IA receptor signaling regulates postnatal osteoblast function and bone remodeling. J Biol Chem. 2004;279(26):27560-6.
127. Mansukhani A, Ambrosetti D, Holmes G, Cornivelli L, Basilico C. Sox2 induction by FGF and FGFR2 activating mutations inhibits Wnt signaling and osteoblast differentiation. J Cell Biol. 2005;168(7):1065-76.
128. Fakhry A, Ratisoontorn C, Vedhachalam C, Salhab I, Koyama E, Leboy P, Pacificib M, Kirschnerc RE, Naha H.-D. 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. 2005;36(2):254-66.
129. Vortkamp A, Lee K, Lanske B, Segre GV, Kronenberg HM, Tabin CJ. Regulation of rate of cartilage differentiation by Indian hedgehog and PTH-related protein. Science. 1996;273 (5275):613-22.
130. Long F, Zhang XM, Karp S, Yang Y, McMahon AP. Genetic manipulation of hedgehog signaling in the endochondral skeleton reveals a direct role in the regulation of chondrocyte proliferation. Development. 2001;128(24):5099-108.
131. Karaplis AC, Luz A, Glowacki J, Bronson RT, Tybulewicz VL, Kronenberg HM, Mulliqan RC. Lethal skeletal dysplasia from targeted disruption of the parathyroid hormone-related peptide gene. Genes Dev. 1994;8(3):277-89.
132. Lanske B, Karaplis AC, Lee K, Luz A, Vortkamp A, Pirro A, Karperien M, Defize LHK, Ho C, Mulligan RC, Abou-Samra A-B, Jüppner H, Segre GV, Kronenberg HM. PTH/PTHrP receptor in early development and Indian hedgehog-regulated bone growth. Science. 1996;273 (5275):663-6.
133. Lee K, Lanske B, Karaplis AC, Deeds JD, Kohno H, Nissenson RA, Kronenberg HM, Segre GV. Parathyroid hormone-related peptide delays terminal differentiation of chondrocytes during endochondral bone development. Endocrinology. 1996;137(11):5109-18.
134. Schipani E, Lanske B, Hunzelman J, Luz A, Kovacs CS, Lee K, Pirro A, Kronenberg HM, Jūpper H. Targeted expression of constitutively active receptors for parathyroid hormone and parathyroid hormone-related peptide delays endochondral bone formation and rescues mice that lack parathyroid hormone-related peptide. Proc Natl Acad Sci USA. 1997;94(25):13689-94.
135. Karp SJ, Schipani E, St-Jacques B, Hunzelman J, Kronenberg H, McMahon AP. Indian hedgehog coordinates endochondral bone growth and morphogenesis via parathyroid hormone related-protein-dependent and -independent pathways. Development. 2000;127(3):543-8.
136. Chung UI, Schipani E, McMahon AP, Kronenberg HM. Indian hedgehog couples chondrogenesis to osteogenesis in endochondral bone development. J Clin Invest. 2001;107(3):295-304.
137. Gao B, Guo J, She C, Shu A, Yang M, Tan Z, Yang X, Guo S, Feng G, He L. Mutations in IHH, encoding Indian hedgehog, cause brachydactyly type A-1. Nat Genet. 2001;28(4):386-8.
138. Yang Y, Topol L, Lee H, Wu J. Wnt5a and Wnt5b exhibit distinct activities in coordinating chondrocyte proliferation and differentiation. Development. 2003;130(5):1003-15.
139. Akiyama H, Lyons JP, Mori-Akiyama Y, Yang X, Zhang R, Zhang Z, Deng JM, Taketo MM, Nakamura T, Behringer RR, McCrea PD, de Crombrugghe B. Interactions between Sox9 and {beta}-catenin control chondrocyte differentiation. Genes Dev. 2004;18(9):1072-87.
140. Ornitz DM. FGF signaling in the developing endochondral skeleton. Cytokine Growth Factor Rev. 2005;16(2):205-13.
141. Montero A, Okada Y, Tomita M, Ito M, Tsurukami H, Nakamura T, Doetschman T, Coffn JD, Hurley MM. Disruption of the fibroblast growth factor-2 gene results in decreased bone mass and bone formation. J Clin Invest. 2000;105(8):1085-93.
142. Guo L, Degenstein L, Fuchs E. Keratinocyte growth factor is required for hair development but not for wound healing. Genes Dev. 1996;10(2):165-75.
143. Xu J, Liu Z, Ornitz DM. Temporal and spatial gradients of Fgf8 and Fgf17 regulate proliferation and differentiation of midline cerebellar structures. Development. 2000;127(9):1833-43.
144. Sun X, Meyers EN, Lewandoski M, Martin GR. Targeted disruption of Fgf8 causes failure of cell migration in the gastrulating mouse embryo. Genes Dev. 1999;13(14):1834-46.
145. Liu Z, Xu J, Colvin JS, Ornitz DM. Coordination of chondrogenesis and osteogenesis by fibroblast growth factor 18. Genes Dev. 2002;16(7):859-69.
146. Ohbayashi N, Shibayama M, Kurotaki Y, Imanishi M, Fujimori T, Itoh N, Takada S. FGF18 is required for normal cell proliferation and differentiation during osteogenesis and chondrogenesis. Genes Dev. 2002;16(7):870-9.
147. 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(6):911-21.
148. Colvin JS, Bohne BA, Harding GW, McEwen DG, Ornitz DM. Skeletal overgrowth and deafness in mice lacking fibroblast growth factor receptor 3. Nat Genet. 1996;12(4):390-7.
149. Naski MC, Colvin JS, Coffn JD, Ornitz DM. Repression of hedgehog signaling and BMP4 expression in growth plate cartilage by fibroblast growth factor receptor 3. Development. 1998;125(24):4977-88.
150. Chen L, Adar R, Yang X, Monsonego EO, Li C, Hauschka PV, Yayon A, Deng C.-X. Gly369Cys mutation in mouse FGFR3 causes achondroplasia by affecting both chondrogenesis and osteogenesis. J Clin Invest. 1999;104(11):1517-25.
151. Chen L, Li C, Qiao W, Xu X, Deng C. A Ser(365)-->Cys mutation of fibroblast growth factor receptor 3 in mouse downregulates Ihh/PTHrP signals and causes severe achondroplasia. Hum Mol Genet. 2001;10(5):457-65.
152. Li C, Chen L, Iwata T, Kitagawa M, Fu XY, Deng CX. A Lys644Glu substitution in fibroblast growth factor receptor 3 (FGFR3) causes dwarfism in mice by activation of STATs and ink4 cell cycle inhibitors. Hum Mol Genet. 1999;8(1):35-44.
153. Iwata T, Chen L, Li C, Ovchinnikov DA, Behringer RR, Francomano CA, Deng C.-X. A neonatal lethal mutation in FGFR3 uncouples proliferation and differentiation of growth plate chondrocytes in embryos. Hum Mol Genet. 2000;9(11):1603-13.
154. Wang Y, Spatz MK, Kannan K, Hayk H, Avivi A, Gorivodsky M, Pines M, Yayon A, Lonai P, Givol D. A mouse model for achondroplasia produced by targeting fibroblast growth factor receptor 3. Proc Natl Acad Sci USA. 1999;96(8):4455-60.
155. Dailey L, Laplantine E, Priore R, Basilico C. A network of transcriptional and signaling events is activated by FGF to induce chondrocyte growth arrest and differentiation. J Cell Biol. 2003;161(6):1053-66.
156. Henderson JE, Naski MC, Aarts MM, Wang D, Cheng L, Goltzman D, Ornitz DM. Expression of FGFR3 with the G380R achondroplasia mutation inhibits proliferation and maturation of CFK2 chondrocytic cells. J Bone Miner Res. 2000 Jan; 15(1):155-65.
157. Kronenberg HM. Developmental regulation of the growth plate. Nature. 2003;423 (6937):332-6.
158. Minina E, Kreschel C, Naski MC, Ornitz DM, Vortkamp A. Interaction of FGF, Ihh/Pthlh, and BMP signaling integrates chondrocyte proliferation and hypertrophic differentiation. Dev Cell. 2002;3(3):439-49.
159. Wang Q, Green RP, Zhao G, Ornitz DM. Differential regulation of endochondral bone growth and joint development by FGFR1 and FGFR3 tyrosine kinase domains. Development. 2001;128(19):3867-76.
160. Hart KC, Robertson SC, Kanemitsu MY, Meyer AN, Tynan JA, Donoghue DJ. Transformation and Stat activation by derivatives of FGFR1, FGFR3, and FGFR4. Oncogene. 2000;19(29):3309-20.
161. Legeai-Mallet L, Benoist-Lasselin C, Munnich A, Bonaventure J. Overexpression of FGFR3, Stat1, Stat5 and p21Cip1 correlates with phenotypic severity and defective chondrocyte differentiation in FGFR3-related chondrodysplasias. Bone. 2004;34(1):26-36.
162. Su WC, Kitagawa M, Xue N, Xie B, Garofalo S, Cho J, Deng C, Horton WA, Fu XY. Activation of Stat1 by mutant fibroblast growth-factor receptor in thanatophoric dysplasia type II dwarfism. Nature. 1997;386 (6622):288-92.
163. 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(11):1361-6.
164. Legeai-Mallet L, Benoist-Lasselin C, Delezoide AL, Munnich A, Bonaventure J. Fibroblast growth factor receptor 3 mutations promote apoptosis but do not alter chondrocyte proliferation in thanatophoric dysplasia. J Biol Chem. 1998;273(21):13007-14.
165. Sahni M, Raz R, Coffn JD, Levy D, Basilico C. STAT1 mediates the increased apoptosis and reduced chondrocyte proliferation in mice overexpressing FGF2. Development. 2001 Jun; 128(11):2119-29.
166. Raucci A, Laplantine E, Mansukhani A, Basilico C. Activation of the ERK1/2 and p38 mitogen-activated protein kinase pathways mediates fibroblast growth factor-induced growth arrest of chondrocytes. J Biol Chem. 2004 Jan 16;279(3):1747-56.
167. Murakami S, Balmes G, McKinney S, Zhang Z, Givol D, de Crombrugghe B. Constitutive activation of MEK1 in chondrocytes causes Stat1-independent achondroplasia-like dwarfism and rescues the Fgfr3-deficient mouse phenotype. Genes Dev. 2004;18(3):290-305.
168. Eswarakumar VP, Monsonego-Ornan E, Pines M, Antonopoulou I, Morriss-Kay GM, Lonai P. The IIIc alternative of Fgfr2 is a positive regulator of bone
169. 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(13):3063-74.
170. Valverde-Franco G, Liu H, Davidson D, Chai S, Valderrama-Carvajal H, Goltzman D, Ornitz DM, Henderson JE. Defective bone mineralization and osteopenia in young adult FGFR3-/-mice. Hum Mol Genet. 2004;13(3):271-84.
171. Xiao L, Naganawa T, Obugunde E, Gronowicz G, Ornitz DM, Coffn JD, Hurley MM. Stat1 controls postnatal bone formation by regulating fibroblast growth factor signaling in osteoblasts. J Biol Chem. 2004;279(26):27743-52.
172. Wolfman NM, Hattersley G, Cox K, Celeste AJ, Nelson R, Yamaji N, Dube JL, DiBlasio-Smith E, Nove J, Song JJ, Wozney JM, Rosen V. Ectopic induction of tendon and ligament in rats by growth and differentiation factors 5, 6, and 7, members of the TGF-beta gene family. J Clin Invest. 1997;100(2):321-30.
173. Storm EE, Huynh TV, Copeland NG, Jenkins NA, Kingsley DM, Lee SJ. Limb alterations in brachypodism mice due to mutations in a new member of the TGF beta-superfamily. Nature. 1994;368 (6472):639-43.
174. Yoon BS, Pogue R, Ovchinnikov DA, Yoshii I, Mishina Y, Behringer RR, Lyons KM. BMPs regulate multiple aspects of growth-plate chondrogenesis through opposing actions on FGF pathways. Development. 2006;133(23):4667-78.
175. Minina E, Wenzel HM, Kreschel C, Karp S, Gaffield W, McMahon AP, Vortkamp A. BMP and Ihh/PTHrP signaling interact to coordinate chondrocyte proliferation and differentiation. Development. 2001;128(22):4523-34.
176. Smits P, Li P, Mandel J, Zhang Z, Deng JM, Behringer RR, de Crombrugghe B, Lefebvre V. The transcription factors L-Sox5 and Sox6 are essential for cartilage formation. Dev Cell. 2001;1(2):277-90.
177. Bi W, Huang W, Whitworth DJ, Deng JM, Zhang Z, Behringer RR, de Crombrugge B. Haploinsuffciency of Sox9 results in defective cartilage primordia and premature skeletal mineralization. Proc Natl Acad Sci USA. 2001;98(12):6698-703.
178. Huang W, Chung UI, Kronenberg HM, de Crombrugghe B. The chondrogenic transcription factor Sox9 is a target of signaling by the parathyroid hormone-related peptide in the growth plate of endochondral bones. Proc Natl Acad Sci USA. 2001;98(1):160-5.
179. Kato M, Patel MS, Levasseur R, Lobov I, Chang BH, Glass DA, 2nd, Hartmann C, Li L, Hwang T-H, Brayton CF, Lang RA, Karsenty G, Chan L. Cbfa1-independent decrease in osteoblast proliferation, osteopenia, and persistent embryonic eye vascularization in mice deficient in Lrp5, a Wnt coreceptor. J Cell Biol. 2002;157(2):303-14.
180. Mundlos S, Otto F, Mundlos C, Mulliken JB, Aylsworth AS, Albright S, Lindhout D, Cole WG, Henn W, Knoll JH, Owen MJ, Mertelsmann R, Zaabel Bu, Olsen BR. Mutations involving the transcription factor CBFA1 cause cleidocranial dysplasia. Cell. 1997;89(5):773-9.
181. Kim IS, Otto F, Zabel B, Mundlos S. Regulation of chondrocyte differentiation by Cbfa1. Mech Dev. 1999;80(2):159-70.
182. Takeda S, Bonnamy JP, Owen MJ, Ducy P, Karsenty G. Continuous expression of Cbfa1 in nonhypertrophic chondrocytes uncovers its ability to induce hypertrophic chondrocyte differentiation and partially rescues Cbfa1-deficient mice. Genes Dev. 2001;15(4):467-81.
183. Yoshida CA, Yamamoto H, Fujita T, Furuichi T, Ito K, Inoue K, Yamana K, Zanma A, Takada K, Ito Y, Komori T. Runx2 and Runx3 are essential for chondrocyte maturation, and Runx2 regulates limb growth through induction of Indian hedgehog. Genes Dev. 2004;18(8):952-63.
184. Hinoi E, Bialek P, Chen YT, Rached MT, Groner Y, Behringer RR, Ornitz DM, Karsenty G. Runx2 inhibits chondrocyte proliferation and hypertrophy through its expression in the perichondrium. Genes Dev. 2006;20(21):2937-42.
185. Vega RB, Matsuda K, Oh J, Barbosa AC, Yang X, Meadows E, McAnally J, Pomajzi C, Shelton JM, Richardson JA, Karsenty G, Olson EN. Histone deacetylase 4 controls chondrocyte hypertrophy during skeletogenesis. Cell. 2004;119(4):555-66.
186. Schipani E, Ryan HE, Didrickson S, Kobayashi T, Knight M, Johnson RS. Hypoxia in cartilage: HIF-1alpha is essential for chondrocyte growth arrest and survival. Genes Dev. 2001;15(21):2865-76.
187. Zelzer E, Mamluk R, Ferrara N, Johnson RS, Schipani E, Olsen BR. VEGFA is necessary for chondrocyte survival during bone development. Development. 2004;131(9):2161-71.