Col10a1 gene expression and chondrocyte hypertrophy during skeletal development and disease

Frontiers in Biology

Volumn 9, Issue 3, 2014, Pages 195-204

  Lu, Yaojuan ^a,b   Qiao, Longwei ^b   Lei, Guanghua ^c   Mira, Ranim R ^a   Gu, Junxia ^b   Zheng, Qiping ^a,b  

^a RUSH UNIVERSITY MEDICAL CENTER   (United States)

^b JIANGSU UNIVERSITY   (China)

^c CENTRAL SOUTH UNIVERSITY   (China)

Author keywords

AP1 and Runx2; chondrocyte hypertrophy; cis enhancer; Col10a1 gene expression; skeletal development and diseases; transcription factors

Indexed keywords

MURINAE; MUS MUSCULUS; VERTEBRATA;

EID: 84912087369     PISSN: 16747984     EISSN: 16747992     Source Type: Journal    
DOI: 10.1007/s11515-014-1310-6     Document Type: Review

References (104)

1. Adams S L, Pallante K M, Niu Z, Cohen A J, Lu J, LeBoy P S (2003). Stimulation of type-X collagen gene transcription by retinoids occurs in part through the BMP signaling pathway. J Bone Joint Surg Am, 85-A(Suppl 3): 29–33
2. Arnold M A, Kim Y, Czubryt MP, Phan D, McAnally J, Qi X, Shelton J M, Richardson J A, Bassel-Duby R, Olson E N (2007). MEF2C transcription factor controls chondrocyte hypertrophy and bone development. Dev Cell, 12(3): 377–389
3. Bateman J F, Freddi S, McNeil R, Thompson E, Hermanns P, Savarirayan R, Lamandé S R (2004). Identification of four novel COL10A1 missense mutations in schmid metaphyseal chondrodysplasia: further evidence that collagen X NC1 mutations impair trimer assembly. Hum Mutat, 23(4): 396
4. Bateman J F, Freddi S, Nattrass G, Savarirayan R (2003). Tissue-specific RNA surveillance? Nonsense-mediated mRNA decay causes collagen X haploinsufficiency in Schmid metaphyseal chondrodysplasia cartilage. Hum Mol Genet, 12(3): 217–225
5. Bateman J F, Wilson R, Freddi S, Lamandé S R, Savarirayan R (2005). Mutations of COL10A1 in Schmid metaphyseal chondrodysplasia. Hum Mutat, 25(6): 525–534
6. Beier F, Vornehm S, Pöschl E, von der Mark K, Lammi M J (1997). Localization of silencer and enhancer elements in the human type X collagen gene. J Cell Biochem, 66(2): 210–218
7. Chambers D, Young D A, Howard C, Thomas J T, Boam D S, Grant M E, Wallis G A, Boot-Handford R P (2002). An enhancer complex confers both high-level and cell-specific expression of the human type X collagen gene. FEBS Lett, 531(3): 505–508
8. Chan D, Cole W G, Rogers J G, Bateman J F (1995). Type X collagen multimer assembly in vitro is prevented by a Gly618 to Val mutation in the alpha 1(X) NC1 domain resulting in Schmid metaphyseal chondrodysplasia. J Biol Chem, 270(9): 4558–4562
9. Chang H J, Yang M J, Yang Y H, Hou M F, Hsueh E J, Lin S R (2009). MMP13 is potentially a new tumor marker for breast cancer diagnosis. Oncol Rep, 22(5): 1119–1127
10. Chapman K B, Prendes M J, Sternberg H, Kidd J L, Funk W D, Wagner J, West MD (2012). COL10A1 expression is elevated in diverse solid tumor types and is associated with tumor vasculature. Future Oncol, 8(8): 1031–1040
11. D’Alonzo R C, Selvamurugan N, Karsenty G, Partridge N C (2002). Physical interaction of the activator protein-1 factors c-Fos and c-Jun with Cbfa1 for collagenase-3 promoter activation. J Biol Chem, 277(1): 816–822
12. Desmedt C, Majjaj S, Kheddoumi N, Singhal S K, Haibe-Kains B, El Ouriaghli F, Chaboteaux C, Michiels S, Lallemand F, Journe F, Duvillier H, Loi S, Quackenbush J, Dekoninck S, Blanpain C, Lagneaux L, Houhou N, Delorenzi M, Larsimont D, Piccart M, Sotiriou C (2012). Characterization and clinical evaluation of CD10+ stroma cells in the breast cancer microenvironment. Clin Cancer Res, 18(4): 1004–1014
13. Dong Y, Drissi H, Chen M, Chen D, Zuscik MJ, Schwarz EM, O’Keefe R J (2005). Wnt-mediated regulation of chondrocyte maturation: modulation by TGF-beta. J Cell Biochem, 95(5): 1057–1068
14. Dong Y F, Soung Y, Schwarz E M, O’Keefe R J, Drissi H (2006). Wnt induction of chondrocyte hypertrophy through the Runx2 transcription factor. J Cell Physiol, 208(1): 77–86
15. Dourado G, LuValle P (1998). Proximal DNA elements mediate repressor activity conferred by the distal portion of the chicken collagen X promoter. J Cell Biochem, 70(4): 507–516
16. Drissi M H, Li X, Sheu T J, Zuscik M J, Schwarz E M, Puzas J E, Rosier R N, O’Keefe R J (2003). Runx2/Cbfa1 stimulation by retinoic acid is potentiated by BMP2 signaling through interaction with Smad1 on the collagen X promoter in chondrocytes. J Cell Biochem, 90(6): 1287–1298
17. Drissi H, Zuscik M, Rosier R, O’Keefe R (2005). Transcriptional regulation of chondrocyte maturation: potential involvement of transcription factors in OA pathogenesis. Mol Aspects Med, 26(3): 169–179
18. Dy P, Wang W, Bhattaram P, Wang Q, Wang L, Ballock R T, Lefebvre V (2012). Sox9 directs hypertrophic maturation and blocks osteoblast differentiation of growth plate chondrocytes. Dev Cell, 22(3): 597–609
19. Eerola I, Salminen H, Lammi P, Lammi M, von der Mark K, Vuorio E, Säämänen A M (1998). Type X collagen, a natural component of mouse articular cartilage: association with growth, aging, and osteoarthritis. Arthritis Rheum, 41(7): 1287–1295
20. Eferl R, Hoebertz A, Schilling A F, Rath M, Karreth F, Kenner L, Amling M, Wagner E F (2004). The Fos-related antigen Fra-1 is an activator of bone matrix formation. EMBO J, 23(14): 2789–2799
21. Eferl R, Wagner E F (2003). AP-1: a double-edged sword in tumorigenesis. Nat Rev Cancer, 3(11): 859–868
22. Fang J, Hall B K (1997). Chondrogenic cell differentiation from membrane bone periostea. Anat Embryol (Berl), 196(5): 349–362 (Review)
23. Gebhard S, Pöschl E, Riemer S, Bauer E, Hattori T, Eberspaecher H, Zhang Z, Lefebvre V, de Crombrugghe B, von der Mark K (2004). A highly conserved enhancer in mammalian type X collagen genes drives high levels of tissue-specific expression in hypertrophic cartilage in vitro and in vivo. Matrix Biol, 23(5): 309–322
24. Goldring M B, Tsuchimochi K, Ijiri K (2006). The control of chondrogenesis. J Cell Biochem, 97(1): 33–44
25. Gomez S, Lopez-Cepero J M, Silvestrini G, Bonucci E (1996). Matrix vesicles and focal proteoglycan aggregates are the nucleation sites revealed by the lanthanum incubation method: a correlated study on the hypertrophic zone of the rat epiphyseal cartilage. Calcif Tissue Int, 58(4): 273–282
26. Gregory C A, Zabel B, Grant M E, Boot-Handford R P, Wallis G A (2000). Equal expression of typ X collagen mRNA fom mutant and wild type COL10A1 alleles in growth plate cartilage from a patient with metaphyseal chondrodysplasia type Schmid. J Med Genet, 37(8): 627–629
27. Grskovic I, Kutsch A, Frie C, Groma G, Stermann J, Schlötzer-Schrehardt U, Niehoff A, Moss S E, Rosenbaum S, Pöschl E, Chmielewski M, Rappl G, Abken H, Bateman J F, Cheah K S, Paulsson M, Brachvogel B (2012). Depletion of annexin A5, annexin A6, and collagen X causes no gross changes in matrix vesiclemediated mineralization, but lack of collagen X affects hematopoiesis and the Th1/Th2 response. J Bone Miner Res, 27(11): 2399–2412
28. Hattori T, Müller C, Gebhard S, Bauer E, Pausch F, Schlund B, Bösl M R, Hess A, Surmann-Schmitt C, von der Mark H, de Crombrugghe B, von der Mark K (2010). SOX9 is a major negative regulator of cartilage vascularization, bone marrow formation and endochondral ossification. Development, 137(6): 901–911
29. Hess J, Angel P, Schorpp-Kistner M (2004). AP-1 subunits: quarrel and harmony among siblings. J Cell Sci, 117(Pt 25): 5965–5973
30. Hess J, Hartenstein B, Teurich S, Schmidt D, Schorpp-Kistner M, Angel P (2003). Defective endochondral ossification in mice with strongly compromised expression of JunB. J Cell Sci, 116(Pt 22): 4587–4596
31. Hess J, Porte D, Munz C, Angel P (2001). AP-1 and Cbfa/runt physically interact and regulate parathyroid hormone-dependent MMP13 expression in osteoblasts through a new osteoblast-specific element 2/AP-1 composite element. J Biol Chem, 276(23): 20029–20038
32. Higashikawa A, Saito T, Ikeda T, Kamekura S, Kawamura N, Kan A, Oshima Y, Ohba S, Ogata N, Takeshita K, Nakamura K, Chung U I, Kawaguchi H (2009). Identification of the core element responsive to runt-related transcription factor 2 in the promoter of human type X collagen gene. Arthritis Rheum, 60(1): 166–178
33. Hinoi E, Bialek P, Chen Y T, Rached M T, Groner Y, Behringer R R, Ornitz D M, Karsenty G (2006). Runx2 inhibits chondrocyte proliferation and hypertrophy through its expression in the perichondrium. Genes Dev, 20(21): 2937–2942
34. Ho M S, Tsang K Y, Lo R L, Susic M, Mäkitie O, Chan T W, Ng V C, Sillence D O, Boot-Handford R P, Gibson G, Cheung K M, Cole W G, Cheah K S, Chan D (2007). COL10A1 nonsense and frame-shift mutations have a gain-of-function effect on the growth plate in human and mouse metaphyseal chondrodysplasia type Schmid. Hum Mol Genet, 16(10): 1201–1215
35. Hovhannisyan H, Zhang Y, Hassan M Q, Wu H, Glackin C, Lian J B, Stein J L, Montecino M, Stein G S, van Wijnen A J (2013). Genomic occupancy of HLH, AP1 and Runx2 motifs within a nuclease sensitive site of the Runx2 gene. J Cell Physiol, 228(2): 313–321
36. Ijiri K, Zerbini L F, Peng H, Correa R G, Lu B, Walsh N, Zhao Y, Taniguchi N, Huang X L, Otu H, Wang H, Wang J F, Komiya S, Ducy P, Rahman M U, Flavell R A, Gravallese E M, Oettgen P, Libermann T A, Goldring MB (2005). A novel role for GADD45beta as a mediator of MMP-13 gene expression during chondrocyte terminal differentiation. J Biol Chem, 280(46): 38544–38555
37. Ikegawa S, Nakamura K, Nagano A, Haga N, Nakamura Y (1997). Mutations in the N-terminal globular domain of the type X collagen gene (COL10A1) in patients with Schmid metaphyseal chondrodysplasia. Hum Mutat, 9(2): 131–135
38. Ikegawa S, Nishimura G, Nagai T, Hasegawa T, Ohashi H, Nakamura Y (1998). Mutation of the type X collagen gene (COL10A1) causes spondylometaphyseal dysplasia. Am J Hum Genet, 63(6): 1659–1662
39. Imabuchi R, Ohmiya Y, Kwon H J, Onodera S, Kitamura N, Kurokawa T, Gong J P, Yasuda K (2011). Gene expression profile of the cartilage tissue spontaneously regenerated in vivo by using a novel double-network gel: comparisons with the normal articular cartilage. BMC Musculoskelet Disord, 12(1): 213
40. Inada M, Yasui T, Nomura S, Miyake S, Deguchi K, Himeno M, Sato M, Yamagiwa H, Kimura T, Yasui N, Ochi T, Endo N, Kitamura Y, Kishimoto T, Komori T (1999). Maturational disturbance of chondrocytes in Cbfa1-deficient mice. Dev Dyn, 214(4): 279–290
41. Jacenko O, LuValle P A, Olsen B R (1993). Spondylometaphyseal dysplasia in mice carrying a dominant negative mutation in a matrix protein specific for cartilage-to-bone transition. Nature, 365(6441): 56–61
42. Jochum W, David J P, Elliott C, Wutz A, Plenk H Jr, Matsuo K, Wagner E F (2000). Increased bone formation and osteosclerosis in mice overexpressing the transcription factor Fra-1. Nat Med, 6(9): 980–984
43. Jochum W, Passegué E, Wagner E F (2001). AP-1 in mouse development and tumorigenesis. Oncogene, 20(19): 2401–2412
44. Kamekura S, Kawasaki Y, Hoshi K, Shimoaka T, Chikuda H, Maruyama Z, Komori T, Sato S, Takeda S, Karsenty G, Nakamura K, Chung U I, Kawaguchi H (2006). Contribution of runt-related transcription factor 2 to the pathogenesis of osteoarthritis in mice after induction of knee joint instability. Arthritis Rheum, 54(8): 2462–2470
45. Karreth F, Hoebertz A, Scheuch H, Eferl R, Wagner E F (2004). The AP1 transcription factor Fra2 is required for efficient cartilage development. Development, 131(22): 5717–5725
46. Kawaguchi H (2008). Endochondral ossification signals in cartilage degradation during osteoarthritis progression in experimental mouse models. Mol Cells, 25(1): 1–6
47. Kenner L, Hoebertz A, Beil F T, Keon N, Karreth F, Eferl R, Scheuch H, Szremska A, Amling M, Schorpp-Kistner M, Angel P, Wagner E F (2004). Mice lacking JunB are osteopenic due to cell-autonomous osteoblast and osteoclast defects. J Cell Biol, 164(4): 613–623
48. Kim I S, Otto F, Zabel B, Mundlos S (1999). Regulation of chondrocyte differentiation by Cbfa1. Mech Dev, 80(2): 159–170
49. 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, Kitamura Y, Yoshiki S, Kishimoto T (1997). Targeted disruption of Cbfa1 results in a complete lack of bone formation owing to maturational arrest of osteoblasts. Cell, 89(5): 755–764
50. Kronenberg H M (2003). Developmental regulation of the growth plate. Nature, 423(6937): 332–336
51. Kung L H, Rajpar M H, Briggs M D, Boot-Handford R P (2012). Hypertrophic chondrocytes have a limited capacity to cope with increases in endoplasmic reticulum stresswithout triggering the unfolded protein response. J Histochem Cytochem, 60(10): 734–48
52. Kwan KM, Pang MK, Zhou S, Cowan S K, Kong R Y, Pfordte T, Olsen B R, Sillence D O, Tam P P, Cheah K S (1997). Abnormal compartmentalization of cartilage matrix components in mice lacking collagen X: implications for function. J Cell Biol, 136(2): 459–471
53. Lee B, Thirunavukkarasu K, Zhou L, Pastore L, Baldini A, Hecht J, Geoffroy V, Ducy P, Karsenty G (1997). Missense mutations abolishing DNA binding of the osteoblast-specific transcription factor OSF2/CBFA1 in cleidocranial dysplasia. Nat Genet, 16(3): 307–310
54. Leung V Y, Gao B, Leung K K, Melhado I G, Wynn S L, Au T Y, Dung N W, Lau J Y, Mak A C, Chan D, Cheah K S (2011). SOX9 governs differentiation stage-specific gene expression in growth plate chondrocytes via direct concomitant transactivation and repression. PLoS Genet, 7(11): e1002356
55. Li F, Lu Y, Ding M, Napierala D, Abbassi S, Chen Y, Duan X, Wang S, Lee B, Zheng Q (2011). Runx2 contributes to murine Col10a1 gene regulation through direct interaction with its cis-enhancer. J Bone Miner Res, 26(12): 2899–2910
56. Linsenmayer T F, Chen Q A, Gibney E, Gordon M K, Marchant J K, Mayne R, Schmid T M (1991). Collagen types IX and X in the developing chick tibiotarsus: analyses of mRNAs and proteins. Development, 111(1): 191–196
57. Linsenmayer T F, Fitch J M, Gross J, Mayne R (1985). Are collagen fibrils in the developing avian cornea composed of two different collagen types? Evidence from monoclonal antibody studies. Ann N Y Acad Sci, 460(1 Biology, Chem): 232–245
58. Long F, Linsenmayer T F (1995). Tissue-specific regulation of the type X collagen gene. Analyses by in vivo footprinting and transfection with a proximal promoter region. J Biol Chem, 270(52): 31310–31314
59. Mackie E J, Ahmed Y A, Tatarczuch L, Chen K S, Mirams M (2008). Endochondral ossification: how cartilage is converted into bone in the developing skeleton. Int J Biochem Cell Biol, 40(1): 46–62
60. MacLean H E, Kim J I, Glimcher M J, Wang J, Kronenberg H M, Glimcher L H (2003). Absence of transcription factor c-maf causes abnormal terminal differentiation of hypertrophic chondrocytes during endochondral bone development. Dev Biol, 262(1): 51–63
61. Magee C, Nurminskaya M, Faverman L, Galera P, Linsenmayer T F (2005). SP3/SP1 transcription activity regulates specific expression of collagen type X in hypertrophic chondrocytes. J Biol Chem, 280(27): 25331–25338
62. Mäkitie O, Susic M, Cole W G (2010). Early-onset metaphyseal chondrodysplasia type Schmid associated with a COL10A1 frameshift mutation and impaired trimerization of wild-type α1(X) protein chains. J Orthop Res, 28(11): 1497–1501
63. Mäkitie O, Susic M, Ward L, Barclay C, Glorieux F H, Cole WG (2005). Schmid type of metaphyseal chondrodysplasia and COL10A1 mutations—findings in 10 patients. Am J Med Genet A, 137A(3): 241–248
64. Marks D S, Gregory C A, Wallis G A, Brass A, Kadler K E, Boot-Handford R P (1999). Metaphyseal chondrodysplasia type Schmid mutations are predicted to occur in two distinct three-dimensional clusters within type X collagen NC1 domains that retain the ability to trimerize. J Biol Chem, 274(6): 3632–3641
65. Maruyama T, Miyamoto Y, Yamamoto G, Yamada A, Yoshimura K, Suzawa T, Takami M, Akiyama T, Hoshino M, Iwasa F, Ikumi N, Tachikawa T, Mishima K, Baba K, Kamijo R (2013). Downregulation of carbonic anhydrase IX promotes Col10a1 expression in chondrocytes. PLoS ONE, 8(2): e56984
66. Matsui Y, Yasui N, Kawabata H, Ozono K, Nakata K, Mizushima T, Tsumaki N, Kataoka E, Fujita Y, Ochi T (2000). A novel type X collagen gene mutation (G595R) associated with Schmid-type metaphyseal chondrodysplasia. J Hum Genet, 45(2): 105–108
67. McIntosh I, Abbott M H, Francomano C A (1995). Concentration of mutations causing Schmid metaphyseal chondrodysplasia in the Cterminal noncollagenous domain of type X collagen. Hum Mutat, 5(2): 121–125
68. Myšičková A, Vingron M (2012). Detection of interacting transcription factors in human tissues using predicted DNA binding affinity. BMC Genomics, 13(13 Suppl 1): S2
69. Naef F, Huelsken J (2005). Cell-type-specific transcriptomics in chimeric models using transcriptome-based masks. Nucleic Acids Res, 33(13): e111
70. 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 (1997). Cbfa1, a candidate gene for cleidocranial dysplasia syndrome, is essential for osteoblast differentiation and bone development. Cell, 89(5): 765–771
71. Papachristou D, Pirttiniemi P, Kantomaa T, Agnantis N, Basdra E K (2006). Fos- and Jun-related transcription factors are involved in the signal transduction pathway of mechanical loading in condylar chondrocytes. Eur J Orthod, 28(1): 20–26
72. Penolazzi L, Lisignoli G, Lambertini E, Torreggiani E, Manferdini C, Lolli A, Vecchiatini R, Ciardo F, Gabusi E, Facchini A, Gambari R, Piva R (2011). Transcription factor decoy against NFATc1 in human primary osteoblasts. Int J Mol Med, 28(2): 199–206
73. Pullig O, Weseloh G, Ronneberger D, Käkönen S, Swoboda B (2000). Chondrocyte differentiation in human osteoarthritis: expression of osteocalcin in normal and osteoarthritic cartilage and bone. Calcif Tissue Int, 67(3): 230–240
74. Rajpar M H, McDermott B, Kung L, Eardley R, Knowles L, Heeran M, Thornton D J, Wilson R, Bateman J F, Poulsom R, Arvan P, Kadler K E, Briggs M D, Boot-Handford R P (2009). Targeted induction of endoplasmic reticulum stress induces cartilage pathology. PLoS Genet, 5(10): e1000691
75. Riemer S, Gebhard S, Beier F, Pöschl E, von der Mark K (2002). Role of c-fos in the regulation of type X collagen gene expression by PTH and PTHrP: Localization of a PTH/PTHrPresponsive region in the human COL10A1 enhancer. J Cell Biochem, 86: 688–699
76. Sahar D E, Longaker M T, Quarto N (2005). Sox9 neural crest determinant gene controls patterning and closure of the posterior frontal cranial suture. Dev Biol, 280(2): 344–361
77. Saito T, Fukai A, Mabuchi A, Ikeda T, Yano F, Ohba S, Nishida N, Akune T, Yoshimura N, Nakagawa T, Nakamura K, Tokunaga K, Chung U I, Kawaguchi H (2010). Transcriptional regulation of endochondral ossification by HIF-2alpha during skeletal growth and osteoarthritis development. Nat Med, 16(6): 678–686
78. Sakimura R, Tanaka K, Yamamoto S, Matsunobu T, Li X, Hanada M, Okada T, Nakamura T, Li Y, Iwamoto Y (2007). The effects of histone deacetylase inhibitors on the induction of differentiation in chondrosarcoma cells. Clin Cancer Res, 13(1): 275–282
79. Sawai H, Ida A, Nakata Y, Koyama K (1998). Novel missense mutation resulting in the substitution of tyrosine by cysteine at codon 597 of the type X collagen gene associated with Schmid metaphyseal chondrodysplasia. J Hum Genet, 43(4): 259–261
80. Schipani E, Provot S (2003). PTHrP, PTH, and the PTH/PTHrP receptor in endochondral bone development. Birth Defects Res C Embryo Today, 69(4): 352–362
81. Shen G (2005). The role of type X collagen in facilitating and regulating endochondral ossification of articular cartilage. Orthod Craniofac Res, 8(1): 11–17
82. Simões B, Conceição N, Viegas C S, Pinto J P, Gavaia P J, Hurst L D, Kelsh R N, Cancela M L (2006). Identification of a promoter element within the zebrafish colXalpha1 gene responsive to runx2 isoforms Osf2/Cbfa1 and til-1 but not to pebp2alphaA2. Calcif Tissue Int, 79(4): 230–244
83. Stratakis C A, Orban Z, Burns A L, Vottero A, Mitsiades C S, Marx S J, Abbassi V, Chrousos G P (1996). Dideoxyfingerprinting (ddF) analysis of the type X collagen gene (COL10A1) and identification of a novel mutation (S671P) in a kindred with Schmid metaphyseal chondrodysplasia. Biochem Mol Med, 59(2): 112–117
84. Takeda S, Bonnamy J P, Owen M J, Ducy P, Karsenty G (2001). Continuous expression of Cbfa1 in nonhypertrophic chondrocytes uncovers its ability to induce hypertrophic chondrocyte differentiation and partially rescues Cbfa1-deficient mice. Genes Dev, 15(4): 467–481
85. Tan J T, Kremer F, Freddi S, Bell K M, Baker N L, Lamandé S R, Bateman J F (2008). Competency for nonsense-mediated reduction in collagen X mRNA is specified by the 3′ UTR and corresponds to the position of mutations in Schmid metaphyseal chondrodysplasia. Am J Hum Genet, 82(3): 786–793
86. Thomas D P, Sunters A, Gentry A, Grigoriadis A E (2000). Inhibition of chondrocyte differentiation in vitro by constitutive and inducible overexpression of the c-fos proto-oncogene. J Cell Sci, 113(Pt 3): 439–450
87. Thomas-Chollier M, Hufton A, Heinig M, O’Keeffe S, Masri N E, Roider H G, Manke T, Vingron M (2011). Transcription factor binding predictions using TRAP for the analysis of ChIP-seq data and regulatory SNPs. Nat Protoc, 6(12): 1860–1869
88. Tsuchimochi K, Otero M, Dragomir C L, Plumb D A, Zerbini L F, Libermann T A, Marcu K B, Komiya S, Ijiri K, Goldring MB (2010). GADD45beta enhances Col10a1 transcription via the MTK1/MKK3/6/p38 axis and activation of C/EBPbeta-TAD4 in terminally differentiating chondrocytes. J Biol Chem, 285(11): 8395–8407
89. van der Kraan PM, van den Berg WB (2012). Chondrocyte hypertrophy and osteoarthritis: role in initiation and progression of cartilage degeneration?. Osteoarthritis Cartilage, 20(3): 223–232
90. von der Mark K, Frischholz S, Aigner T, Beier F, Belke J, Erdmann S, Burkhardt H (1995). Upregulation of type X collagen expression in osteoarthritic cartilage. Acta Orthop Scand Suppl, 266: 125–129
91. von der Mark K, Kirsch T, Nerlich A, Kuss A, Weseloh G, Glückert K, Stöss H (1992). Type X collagen synthesis in human osteoarthritic cartilage. Indication of chondrocyte hypertrophy. Arthritis Rheum, 35(7): 806–811
92. Vonk L A, Kragten A H, Dhert W J, Saris D B, Creemers L B (2014). Overexpression of hsa-miR-148a promotes cartilage production and inhibits cartilage degradation by osteoarthritic chondrocytes. Osteoarthritis Cartilage, 22(1): 145–153
93. Wagner E F (2002). Functions of AP1 (Fos/Jun) in bone development. Ann Rheum Dis, 61(61 Suppl 2): ii40–ii42
94. Wallis G A, Rash B, Sykes B, Bonaventure J, Maroteaux P, Zabel B, Wynne-Davies R, Grant M E, Boot-Handford R P (1996). Mutations within the gene encoding the alpha 1 (X) chain of type X collagen (COL10A1) cause metaphyseal chondrodysplasia type Schmid but not several other forms of metaphyseal chondrodysplasia. J Med Genet, 33(6): 450–457
95. Warman M L, Abbott M, Apte S S, Hefferon T, McIntosh I, Cohn D H, Hecht J T, Olsen B R, Francomano C A (1993). A type X collagen mutation causes Schmid metaphyseal chondrodysplasia. Nat Genet, 5(1): 79–82
96. Wilson R, Freddi S, Chan D, Cheah K S, Bateman J F (2005). Misfolding of collagen X chains harboring Schmid metaphyseal chondrodysplasia mutations results in aberrant disulfide bond formation, intracellular retention, and activation of the unfolded protein response. J Biol Chem, 280(16): 15544–15552
97. Woelfle J V, Brenner R E, Zabel B, Reichel H, Nelitz M(2011). Schmidtype metaphyseal chondrodysplasia as the result of a collagen type X defect due to a novel COL10A1 nonsense mutation: A case report of a novel COL10A1 mutation. J Orthop Sci, 16(2): 245–249
98. Zanotti S, Canalis E (2013). Notch suppresses nuclear factor of activated T cells (NFAT) transactivation and Nfatc1 expression in chondrocytes. Endocrinology, 154(2): 762–772
99. Zheng Q, Keller B, Zhou G, Napierala D, Chen Y, Zabel B, Parker A E, Lee B (2009). Localization of the cis-enhancer element for mouse type X collagen expression in hypertrophic chondrocytes in vivo. J Bone Miner Res, 24(6): 1022–1032
100. Zheng Q, Sebald E, Zhou G, Chen Y, Wilcox W, Lee B, Krakow D (2005). Dysregulation of chondrogenesis in human cleidocranial dysplasia. Am J Hum Genet, 77(2): 305–312
101. Zheng Q, Zhou G, Morello R, Chen Y, Garcia-Rojas X, Lee B (2003). Type X collagen gene regulation by Runx2 contributes directly to its hypertrophic chondrocyte-specific expression in vivo. J Cell Biol, 162(5): 833–842
102. Zhou G, Zheng Q, Engin F, Munivez E, Chen Y, Sebald E, Krakow D, Lee B (2006). Dominance of SOX9 function over RUNX2 during skeletogenesis. Proc Natl Acad Sci USA, 103(50): 19004–19009
103. Zhu Y, Li L, Zhou L, Mei H, Jin K, Liu K, Xu W, Tang J, Yang Y, Zhao R, He X (2011). A novel mutation leading to elongation of the deduced α1(X) chain results in Metaphyseal Chondrodysplasia type Schmid. Clin Chim Acta, 412(13–14): 1266–1269
104. Zimmermann P, Boeuf S, Dickhut A, Boehmer S, Olek S, Richter W (2008). Correlation of COL10A1 induction during chondrogenesis of mesenchymal stem cells with demethylation of two CpG sites in the COL10A1 promoter. Arthritis Rheum, 58(9): 2743–2753