Vertebrate skeletogenesis

Current Topics in Developmental Biology

Volumn 90, Issue C, 2010, Pages 291-317

  Lefebvre, Véronique ^a   Bhattaram, Pallavi ^a  

^a LERNER RESEARCH INSTITUTE   (United States)

Author keywords

Chondrogenesis; Development; Differentiation; Growth plate; Osteogenesis; Patterning; Skeletogenesis; Synovial joint; Vertebrate

Indexed keywords

ANATOMY AND HISTOLOGY; ANIMAL; ANIMAL EMBRYO; BONE; BONE DEVELOPMENT; CARTILAGE; CHONDROGENESIS; CYTOLOGY; EMBRYOLOGY; GROWTH, DEVELOPMENT AND AGING; HUMAN; JOINT; MORPHOGENESIS; PHYSIOLOGY; SIGNAL TRANSDUCTION; VERTEBRATE;

ANIMALS; BONE AND BONES; BONE DEVELOPMENT; CARTILAGE; CHONDROGENESIS; EMBRYO, MAMMALIAN; HUMANS; JOINTS; MORPHOGENESIS; OSTEOGENESIS; SIGNAL TRANSDUCTION; VERTEBRATES;

EID: 77955322520     PISSN: 00702153     EISSN: None     Source Type: Book Series    
DOI: 10.1016/S0070-2153(10)90008-2     Document Type: Chapter

References (106)

1. Akiyama H. Control of chondrogenesis by the transcription factor Sox9. Mod. Rheumatol. 2008, 18:213-219.
2. Akiyama H., Chaboissier M.C., Martin J.F., 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, 16:2813-2828.
3. Akiyama H., Lyons J.P., Mori-Akiyama Y., Yang X., Zhang R., Zhang Z., Deng J.M., Taketo M.M., Nakamura T., Behringer R.R., McCrea P.D., de Crombrugghe B. Interactions between Sox9 and beta-catenin control chondrocyte differentiation. Genes Dev. 2004, 18:1072-1087.
4. Arnold M.A., Kim Y., Czubryt M.P., Phan D., McAnally J., Qi X., Shelton J.M., Richardson J.A., Bassel-Duby R., Olson E.N. MEF2C transcription factor controls chondrocyte hypertrophy and bone development. Dev. Cell 2007, 12:377-389.
5. Bhattaram P., Penzo-Méndez A., Sock E., Colmenares C., Kaneko K.J., Vassilev A., DePamphilis M.L., Wegner M., Lefebvre V. Organogenesis relies on Soxc transcription factors for the survival of neural and mesenchymal progenitors. Nat. Commun. 2010, 1:9 doi: 10.1038/ncomms 1008.
6. Bi W., Deng J.M., Zhang Z., Behringer R.R., de Crombrugghe B. Sox9 is required for cartilage formation. Nat. Genet. 1999, 22:85-89.
7. Bialek P., Kern B., Yang X., Schrock M., Sosic D., Hong N., Wu H., Yu K., Ornitz D.M., Olson E.N., Justice M.J., Karsenty G. A twist code determines the onset of osteoblast differentiation. Dev. Cell 2004, 6:423-435.
8. Butterfield N.C., McGlinn E., Wicking C. The molecular regulation of vertebrate limb patterning. Curr. Top. Dev. Biol. 2010, (submitted).
9. Chen X., Macica C.M., Nasiri A., Broadus A.E. Regulation of articular chondrocyte proliferation and differentiation by Indian hedgehog and parathyroid hormone-related protein in mice. Arthritis Rheum. 2008, 58:3788-3797.
10. Clement-Jones M., Schiller S., Rao E., Blaschke R.J., Zuniga A., Zeller R., Robson S.C., Binder G., Glass I., Strachan T., Lindsay S., Rappold G.A. The short stature homeobox gene SHOX is involved in skeletal abnormalities in turner syndrome. Hum. Mol. Genet. 2000, 9:695-702.
11. Cobb J., Dierich A., Huss-Garcia Y., Duboule D. A mouse model for human short-stature syndromes identifies shox2 as an upstream regulator of runx2 during long-bone development. Proc. Natl. Acad. Sci. USA 2006, 103:4511-4515.
12. Cretekos C.J., Wang Y., Green E.D., Martin J.F., Rasweiler J.J., Behringer R.R. Regulatory divergence modifies limb length between mammals. Genes Dev. 2008, 22:141-151. NISC Comparative Sequencing Program.
13. Day T.F., Guo X., Garrett-Beal L., Yang Y. Wnt/beta-catenin signaling in mesenchymal progenitors controls osteoblast and chondrocyte differentiation during vertebrate skeletogenesis. Dev. Cell 2005, 8:739-750.
14. Day T.F., Yang Y. Wnt and hedgehog signaling pathways in bone development. J. Bone Joint Surg. Am. 2008, 90(Suppl. 1):19-24.
15. Ducy P., Zhang R., Geoffroy V., Ridall A.L., Karsenty G. Osf2/cbfa1: a transcriptional activator of osteoblast differentiation. Cell. 1997, 89:747-754.
16. Dy P., Penzo-Méndez A., Wang H., Pedraza C.E., Macklin W.B., Lefebvre V. The three SoxC proteins-Sox4, Sox11 and Sox12-exhibit overlapping expression patterns and molecular properties. Nucl. Acids Res. 2008, 36:3101-3117.
17. Dy P., Smits P., Silvester A., Penzo-Méndez A., Dumitriu B., Han Y., de la Motte C.A., Kingsley D.M., Lefebvre V. Synovial joint morphogenesis requires the chondrogenic action of Sox5 and Sox6 in growth plate and articular cartilage. Dev. Biol. 2010, 341:346-359.
18. Eames B.F., Sharpe P.T., Helms J.A. Hierarchy revealed in the specification of three skeletal fates by Sox9 and Runx2. Dev. Biol. 2004, 274:188-200.
19. Ellison J.W., Wardak Z., Young M.F., Robey P.G., Webster M., Chiong W. PHOG, a candidate gene for involvement in the short stature of turner syndrome. Hum. Mol. Genet. 1997, 6:1341-1347.
20. Foster J.W., Dominguez-Steglich M.A., Guioli S., Kwok C., Weller P.A., Stevanovi M., Weissenbach J., Mansour S., Young I.D., Goodfellow P.N., Brook J.D., Schafer A.J. Campomelic dysplasia and autosomal sex reversal caused by mutations in an SRY-related gene. Nature 1994, 372:525-530.
21. Gahunia H.K., Babyn P.S., Kirsch S., Mendoza-Londono R. Imaging of SHOX-associated anomalies. Semin. Musculoskelet. Radiol. 2009, 13:236-254.
22. Guo X., Day T.F., Jiang X., Garrett-Beal L., Topol L., Yang Y. Wnt/beta-catenin signaling is sufficient and necessary for synovial joint formation. Genes Dev. 2004, 18:2404-2417.
23. Guo X., Mak K.K., Taketo M.M., Yang Y. The wnt/beta-catenin pathway interacts differentially with PTHrP signaling to control chondrocyte hypertrophy and final maturation. PLoS One 2009, 4:e6067.
24. Hall B.K., Miyake T. All for one and one for all: condensations and the initiation of skeletal development. BioEssays 2000, 22:138-147.
25. Han Y., Lefebvre V. L-Sox5/Sox6 drive expression of the aggrecan gene in cartilage by securing binding of Sox9 to a far-upstream enhancer. Mol. Cell. Biol. 2008, 28:4999-5013.
26. Hartmann C. Transcriptional networks controlling skeletal development. Curr. Opin. Genet. Dev. 2009, 19:437-443.
27. Hartmann C., Tabin C.J. Wnt-14 plays a pivotal role in inducing synovial joint formation in the developing appendicular skeleton. Cell 2001, 104:341-351.
28. Hermanns P., Lee B. Transcriptional dysregulation in skeletal malformation syndromes. Am. J. Med. Genet. 2001, 106:258-271.
29. Hill T.P., Später D., Taketo M.M., Birchmeier W., Hartmann C. Canonical wnt/beta-catenin signaling prevents osteoblasts from differentiating into chondrocytes. Dev. Cell 2005, 8:727-738.
30. Huang W., Chung U.I., Kronenberg H.M., 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, 98:160-165.
31. Ikeda T., Kamekura S., Mabuchi A., Kou I., Seki S., Takato T., Nakamura K., Kawaguchi H., Ikegawa S., Chung U.I. The combination of SOX5, SOX6, and SOX9 (the SOX trio) provides signal sufficient for induction of permanent cartilage. Arthritis Rheum. 2004, 50:3561-3573.
32. Inada M., Yasui T., Nomura S., Miyake S., Deguchi K., Himeno M., Sato M., Yamagiwa H., Kimura T., Yasui N., Ochi T., Endo N., et al. Maturational disturbance of chondrocytes in cbfa1-deficient mice. Dev. Dyn. 1999, 214:279-290.
33. Ito M.M., Kida M.Y. Morphological and biochemical re-evaluation of the process of cavitation in the rat knee joint: cellular and cell strata alterations in the interzone. J. Anat. 2000, 4:659-679.
34. Iwamoto M., Tamamura Y., Koyama E., Komori T., Takeshita N., Williams J.A., Nakamura T., Enomoto-Iwamoto M., Pacifici M. Transcription factor ERG and joint and articular cartilage formation during mouse limb and spine skeletogenesis. Dev. Biol. 2007, 305:40-51.
35. Jensen E.D., Gopalakrishnan R., Westendorf J.J. Regulation of gene expression in osteoblasts. Biofactors 2010, 36:25-32.
36. Kahn J., Shwartz Y., Blitz E., Krief S., Sharir A., Breitel D.A., Rattenbach R., Relaix F., Maire P., Rountree R.B., Kingsley D.M., Zelzer E. Muscle contraction is necessary to maintain joint progenitor cell fate. Dev. Cell 2009, 16:734-743.
37. Karlsson C., Lindahl A. Notch signaling in chondrogenesis. Int. Rev. Cell. Mol. Biol. 2009, 275:65-88.
38. Karsenty G., Kronenberg H.M., Settembre C. Genetic control of bone formation. Annu. Rev. Cell. Dev. Biol. 2009, 25:629-648.
39. Khan I.M., Redman S.N., Williams R., Dowthwaite G.P., Oldfield S.F., Archer C.W. The development of synovial joints. Curr. Top. Dev. Biol. 2007, 79:1-36.
40. Kim I.S., Otto F., Zabel B., Mundlos S. Regulation of chondrocyte differentiation by cbfa1. Mech. Dev. 1999, 80:159-170.
41. Komori T., Yagi H., Nomura S., Yamaguchi A., Sasaki K., Deguchi K., Shimizu Y., Bronson R.T., Gao Y.H., Inada M., Sato M., Okamoto R., et al. Targeted disruption of cbfa1 results in a complete lack of bone formation owing to maturational arrest of osteoblasts. Cell 1997, 89:755-764.
42. Koyama E., Shibukawa Y., Nagayama M., Sugito H., Young B., Yuasa T., Okabe T., Ochiai T., Kamiya N., Rountree R.B., Kingsley D.M., Iwamoto M., et al. A distinct cohort of progenitor cells participates in synovial joint and articular cartilage formation during mouse limb skeletogenesis. Dev. Biol. 2008, 316:62-73.
43. Kozhemyakina E., Cohen T., Yao T.P., Lassar A.B. Parathyroid hormone-related peptide represses chondrocyte hypertrophy through a protein phosphatase 2a/histone deacetylase 4/MEF2 pathway. Mol. Cell. Biol. 2009, 29:5751-5762.
44. Kumar D., Lassar A.B. The transcriptional activity of Sox9 in chondrocytes is regulated by RhoA signaling and actin polymerization. Mol. Cell. Biol 2009, 29:4262-4273.
45. Lefebvre V., Huang W., Harley V.R., Goodfellow P.N., de Crombrugghe B. SOX9 is a potent activator of the chondrocyte-specific enhancer of the pro alpha1(II) collagen gene. Mol. Cell. Biol. 1997, 17:2336-2346.
46. Lefebvre V., Li P., de Crombrugghe B. A new long form of Sox5 (L-Sox5), Sox6 and Sox9 are co-expressed in chondrogenesis and cooperatively activate the type II collagen gene. EMBO J. 1998, 17:5718-5733.
47. Lefebvre V., Smits P. Transcriptional control of chondrocyte fate and differentiation. Birth Defects Res. C Embryo Today 2005, 75:200-212.
48. Lettre G. Genetic regulation of adult stature. Curr. Opin. Pediatr. 2009, 21:515-522.
49. Li Y., Toole B.P., Dealy C.N., Kosher R.A. Hyaluronan in limb morphogenesis. Dev. Biol. 2007, 305:411-420.
50. Ligon A.H., Moore S.D.P., Parisi M.A., Mealiffe M.E., Harris D.J., Ferguson H.L., Quade B.J., Morton C.C. Constitutional rearrangement of the architectural factor HMGA2: a novel human phenotype including overgrowth and lipomas. Am. J. Hum. Genet. 2005, 76:340-348.
51. Limura T., Denans N., Pourqui O. Establishment of hox vertebral identities in the embryonic spine precursors. Curr. Top. Dev. Biol. 2009, 88:201-234.
52. Macgregor S., Cornes B.K., Martin N.G., Visscher P.M. Bias, precision and heritability of self-reported and clinically measured height in Australian twins. Hum. Genet. 2006, 120:571-580.
53. Mackie E.J., Ahmed Y.A., Tatarczuch L., Chen K.S., Mirams M. Endochondral ossification: how cartilage is converted into bone in the developing skeleton. Int. J. Biochem. Cell Biol. 2008, 40:46-62.
54. Matsumoto K., Li Y., Jakuba C., Sugiyama Y., Sayo T., Okuno M., Dealy C.N., Toole B.P., Takeda J., Yamaguchi Y., Kosher R.A. Conditional inactivation of has2 reveals a crucial role for hyaluronan in skeletal growth, patterning, chondrocyte maturation and joint formation in the developing limb. Development 2009, 136:2825-2835.
55. McIntyre D.C., Rakshit S., Yallowitz A.R., Loken L., Jeannotte L., Capecchi M.R., Wellik D.M. Hox patterning of the vertebrate rib cage. Development 2007, 134:2981-2989.
56. Mundlos S., Otto F., Mundlos C., Mulliken J.B., Aylsworth A.S., Albright S., Lindhout D., Cole W.G., Henn W., Knoll J.H., Owen M.J., Mertelsmann R., et al. Mutations involving the transcription factor CBFA1 cause cleidocranial dysplasia. Cell 1997, 89:773-779.
57. 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, 18:290-305.
58. Murakami S., Kan M., McKeehan W.L., de Crombrugghe B. Up-regulation of the chondrogenic Sox9 gene by fibroblast growth factors is mediated by the mitogen-activated protein kinase pathway. Proc. Natl. Acad. Sci. USA 2000, 97:1113-1118.
59. Nakashima K., Zhou X., Kunkel G., Zhang Z., Deng J.M., Behringer R.R., de Crombrugghe B. The novel zinc finger-containing transcription factor osterix is required for osteoblast differentiation and bone formation. Cell 2002, 108:17-29.
60. Ng L.J., Wheatley S., Muscat G.E., Conway-Campbell J., Bowles J., Wright E., Bell D.M., Tam P.P., Cheah K.S., Koopman P. SOX9 binds DNA, activates transcription, and coexpresses with type II collagen during chondrogenesis in the mouse. Dev. Biol. 1997, 183:108-121.
61. Olney R.C. Mechanisms of impaired growth: effect of steroids on bone and cartilage. Horm. Res. 2009, 72(Suppl 1):30-35.
62. Opperman L.A. Cranial sutures as intramembranous bone growth sites. Dev. Dyn. 2000, 219:472-485.
63. Ornitz D.M. FGF signaling in the developing endochondral skeleton. Cytokine Growth Factor Rev. 2005, 16:205-213.
64. Ota K.G., Kuratani S. Evolutionary origin of bone and cartilage in vertebrates. In. The Skeletal System 2009, 1-18. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York. O. Pourquié (Ed.).
65. Otto F., Thornell A.P., Crompton T., Denzel A., Gilmour K.C., Rosewell I.R., Stamp G.W., Beddington R.S., Mundlos S., Olsen B.R., Selby P.B., Owen M.J. Cbfa1, a candidate gene for cleidocranial dysplasia syndrome, is essential for osteoblast differentiation and bone development. Cell 1997, 89:765-771.
66. Pacifici M., Koyama E., Iwamoto M. Mechanisms of synovial joint and articular cartilage formation: recent advances, but many lingering mysteries. Birth Defects Res. C Embryo Today 2005, 75:237-248.
67. Pitsillides A.A., Ashhurst D.E. A critical evaluation of specific aspects of joint development. Dev. Dyn. 2008, 237:2284-2294.
68. Pogue R., Lyons K. BMP signaling in the cartilage growth plate. Curr. Top. Dev. Biol. 2006, 76:1-48.
69. Rached M.T., Kode A., Xu L., Yoshikawa Y., Paik J.H., Depinho R.A., Kousteni S. FoxO1 is a positive regulator of bone formation by favoring protein synthesis and resistance to oxidative stress in osteoblasts. Cell Metab. 2010, 11:147-160.
70. Rentsendorj O., Nagy A., Sink I., Daraba A., Barta E., Kiss I. Highly conserved proximal promoter element harbouring paired Sox9-binding sites contributes to the tissue- and developmental stage-specific activity of the matrilin-1 gene. Biochem. J. 2005, 389:705-716.
71. Rimoin D.L., Cohn D., Krakow D., Wilcox W., Lachman R.S., Alanay Y. The skeletal dysplasias: clinical-molecular correlations. Ann. NY Acad. Sci. 2007, 1117:302-309.
72. Rodda S.J., McMahon A.P. Distinct roles for hedgehog and canonical wnt signaling in specification, differentiation and maintenance of osteoblast progenitors. Development 2006, 133:3231-3244.
73. Rosen V. BMP and BMP inhibitors in bone. Ann. NY Acad. Sci. 2006, 1068:19-25.
74. Rountree R.B., Schoor M., Chen H., Marks M.E., Harley V., Mishina Y., Kingsley D.M. BMP receptor signaling is required for postnatal maintenance of articular cartilage. PLoS Biol. 2004, 2:e355.
75. Sauka-Spengler T., Bronner-Fraser M. A gene regulatory network orchestrates neural crest formation. Nat. Rev. Mol. Cell. Biol 2008, 9:557-568.
76. Selvamurugan N., Kwok S., Alliston T., Reiss M., Partridge N.C. Transforming growth factor-beta 1 regulation of collagenase-3 expression in osteoblastic cells by cross-talk between the smad and MAPK signaling pathways and their components, Smad2 and Runx2. J. Biol. Chem. 2004, 279:19327-19334.
77. Seo H.S., Serra R. Deletion of Tgfbr2 in Prx1-cre expressing mesenchyme results in defects in development of the long bones and joints. Dev. Biol. 2007, 310:304-316.
78. Serra R., Johnson M., Filvaroff E.H., LaBorde J., Sheehan D.M., Derynck R., Moses H.L. Expression of a truncated, kinase-defective TGF-beta type II receptor in mouse skeletal tissue promotes terminal chondrocyte differentiation and osteoarthritis. J. Cell Biol. 1997, 139:541-552.
79. Shum L., Coleman C.M., Hatakeyama Y., Tuan R.S. Morphogenesis and dysmorphogenesis of the appendicular skeleton. Birth Defects Res. C Embryo Today 2003, 69:102-122.
80. Sinha K.M., Yasuda H., Coombes M.M., Dent S.Y., de Crombrugghe B. Regulation of the osteoblast-specific transcription factor osterix by NO66, a jumonji family histone demethylase. EMBO J. 2010, 29:68-79.
81. Smits P., Dy P., Mitra S., Lefebvre V. Sox5 and Sox6 are needed to develop and maintain source, columnar and hypertrophic chondrocytes in the cartilage growth plate. J. Cell Biol. 2004, 164:747-758.
82. Smits P., Li P., Mandel J., Zhang Z., Deng J.M., Behringer R.R., de Crombrugghe B., Lefebvre V. The transcription factors L-Sox5 and Sox6 are essential for cartilage formation. Dev. Cell 2001, 1:277-290.
83. Spagnoli A., O'Rear L., Chandler R.L., Granero-Molto F., Mortlock D.P., Gorska A.E., Weis J.A., Longobardi L., Chytil A., Shimer K., Moses H.L. TGF-beta signaling is essential for joint morphogenesis. J. Cell Biol. 2007, 177:1105-1117.
84. Spranger J. Skeletal dysplasias. In. Human Malformations and Related Anomalies, second edition 2006, Oxford University Press, Oxford, New York, Chapter 22. R.E. Stevenson, J.G. Hall (Eds.).
85. St-Jacques B., Hammerschmidt M., McMahon A.P. Indian hedgehog signaling regulates proliferation and differentiation of chondrocytes and is essential for bone formation. Genes Dev. 1999, 13:2072-2086.
86. Stickens D., Behonick D.J., Ortega N., Heyer B., Hartenstein B., Yu Y., Fosang A.J., Schorpp-Kistner M., Angel P., Werb Z. Altered endochondral bone development in matrix metalloproteinase 13-deficient mice. Development 2004, 131:5883-5895.
87. Su N., Du X., Chen L. FGF signaling: its role in bone development and human skeleton diseases. Front. Biosci. 2008, 13:2842-2865.
88. Takeda S., Bonnamy J.P., Owen M.J., 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, 15:467-481.
89. Tuli R., Tuli S., Nandi S., Huang X., Manner P.A., Hozack W.J., Danielson K.G., Hall D.J., Tuan R.S. Transforming growth factor-beta-mediated chondrogenesis of human mesenchymal progenitor cells involves N-cadherin and mitogen-activated protein kinase and wnt signaling cross-talk. J. Biol. Chem. 2003, 278:41227-41236.
90. Vega R.B., Matsuda K., Oh J., Barbosa A.C., Yang X., Meadows E., McAnally J., Pomajzl C., Shelton J.M., Richardson J.A., Karsenty G., Olson E.N. Histone deacetylase 4 controls chondrocyte hypertrophy during skeletogenesis. Cell 2004, 119:555-566.
91. Wagner E.F. Functions of AP1 (fos/Jun) in bone development. Ann. Rheum. Dis. 2002, 61(Suppl 2:ii):40-42.
92. Wagner T., Wirth J., Meyer J., Zabel B., Held M., Zimmer J., Pasantes J., Bricarelli F.D., Keutel J., Hustert E., Wolf U., Tommerup N., et al. Autosomal sex reversal and campomelic dysplasia are caused by mutations in and around the SRY-related gene. Cell 1994, 79:1111-1120.
93. Wellik D.M. Hox genes and vertebrate axial pattern. Curr. Top. Dev. Biol. 2009, 88:257-278.
94. Yang X., Chen L., Xu X., Li C., Huang C., Deng C.X. TGF-beta/Smad3 signals repress chondrocyte hypertrophic differentiation and are required for maintaining articular cartilage. J. Cell Biol. 2001, 153:35-46.
95. Yang X., Matsuda K., Bialek P., Jacquot S., Masuoka H.C., Schinke T., Li L., Brancorsini S., Sassone-Corsi P., Townes T.M., Hanauer A., Karsenty G. ATF4 is a substrate of RSK2 and an essential regulator of osteoblast biology; implication for Coffin-Lowry Syndrome. Cell 2004, 117:387-398.
96. Yavropoulou M.P., Yovos J.G. Osteoclastogenesis-current knowledge and future perspectives. J. Musculoskelet. Neuronal Interact. 2008, 8:204-216.
97. Yoon B.S., Ovchinnikov D.A., Yoshii I., Mishina Y., Behringer R.R., Lyons K.M. Bmpr1a and bmpr1b have overlapping functions and are essential for chondrogenesis in vivo. Proc. Natl. Acad. Sci. USA 2005, 102:5062-5067.
98. Yoshida C.A., 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, 18:952-963.
99. Yuasa T., Kondo N., Yasuhara R., Shimono K., Mackem S., Pacifici M., Iwamoto M., Enomoto-Iwamoto M. Transient activation of wnt/{beta}-catenin signaling induces abnormal growth plate closure and articular cartilage thickening in postnatal mice. Am. J. Pathol. 2009, 175:1993-2003.
100. Zelzer E., Mamluk R., Ferrara N., Johnson R.S., Schipani E., Olsen B.R. VEGFA is necessary for chondrocyte survival during bone development. Development 2004, 131:2161-2171.
101. Zeng L., Kempf H., Murtaugh L.C., Sato M.E., Lassar A.B. Shh establishes an nkx3.2/Sox9 autoregulatory loop that is maintained by BMP signals to induce somitic chondrogenesis. Genes Dev. 2002, 16:1990-2005.
102. Zhao X., Sun M., Zhao J., Leyva J.A., Zhu H., Yang W., Zeng X., Ao Y., Liu Q., Liu G., Lo W.H.Y., Jabs E.W., et al. Mutations in HOXD13 underlie syndactyly type V and a novel brachydactyly-syndactyly syndrome. Am. J. Hum. Genet. 2007, 80:361-371.
103. Zheng Q., Zhou G., Morello R., Chen Y., Garcia-Rojas X., Lee B. Type X collagen gene regulation by Runx2 contributes directly to its hypertrophic chondrocyte-specific expression in vivo. J. Cell Biol. 2003, 162:833-842.
104. Zhou X., Benson K.F., Ashar H.R., Chada K. Mutation responsible for the mouse pygmy phenotype in the developmentally regulated factor HMGI-C. Nature 1995, 377:771-774.
105. Zhou G., Zheng Q., Engin F., Munivez E., Chen Y., Sebald E., Krakow D., Lee B. Dominance of SOX9 function over RUNX2 during skeletogenesis. Proc. Natl. Acad. Sci. USA 2006, 103:19004-19009.
106. Zhu M., Chen M., Zuscik M., Wu Q., Wang Y.J., Rosier R.N., O'Keefe R.J., Chen D. Inhibition of beta-catenin signaling in articular chondrocytes results in articular cartilage destruction. Arthritis Rheum. 2008, 58:2053-2064.