The cartilage-specific transcription factor Sox9 regulates AP-2ε expression in chondrocytes

FEBS Journal

Volumn 276, Issue 9, 2009, Pages 2494-2504

  Wenke, Ann Kathrin ^a   Grässel, Susanne ^a   Moser, Markus ^b   Bosserhoff, Anja K ^a  

^a UNIVERSITY OF REGENSBURG   (Germany)

^b MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

Author keywords

AP 2 ; Cartilage; Differentiation; Osteoarthritis; Transcriptional regulation

Indexed keywords

SMALL INTERFERING RNA; TRANSCRIPTION FACTOR AP 2; TRANSCRIPTION FACTOR AP 2ALPHA; TRANSCRIPTION FACTOR AP 2EPSILON; TRANSCRIPTION FACTOR SOX9; UNCLASSIFIED DRUG;

ANIMAL TISSUE; AP 2EPSILON GENE; ARTICLE; BINDING SITE; CARTILAGE CELL; CELL DIFFERENTIATION; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; EMBRYO; GEL MOBILITY SHIFT ASSAY; GENE; HUMAN; HUMAN CELL; HYPERTROPHY; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; MESENCHYMAL STEM CELL; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM;

ANIMALS; CARTILAGE; CELL LINE, TUMOR; CHONDROCYTES; EMBRYO, MAMMALIAN; GENE EXPRESSION REGULATION; HUMANS; MICE; MICE, KNOCKOUT; SOX9 TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR AP-2; TRANSFECTION;

EID: 64149100357     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2009.06973.x     Document Type: Article

References (46)

1. Hilger-Eversheim K, Moser M, Schorle H Buettner R (2000) Regulatory roles of AP-2 transcription factors in vertebrate development, apoptosis and cell-cycle control. Gene 260, 1 12.
2. Eckert D, Buhl S, Weber S, Jager R Schorle H (2005) The AP-2 family of transcription factors. Genome Biol 6, 246, doi :.
3. Bosher JM, Williams T Hurst HC (1995) The developmentally regulated transcription factor AP-2 is involved in c-errbB-2 overexpression in human mammary carcinoma. Proc Natl Acad Sci USA 92, 744 747.
4. Feng W Williams T (2003) Cloning and characterization of the mouse AP-2 epsilon gene: a novel family member expressed in the developing olfactory bulb. Mol Cell Neurosci 24, 460 475.
5. Moser M, Imhof A, Pscherer A, Bauer R, Amselgruber W, Sinowatz F, Hofstadter F, Schule R Buettner R (1995) Cloning and characterization of a second AP-2 transcription factor: AP-2 beta. Development 121, 2779 2788.
6. Oulad-Abdelghani M, Bouillet P, Chazaud C, Dolle P Chambon P (1996) AP-2.2: a novel AP-2-related transcription factor induced by retinoic acid during differentiation of P19 embryonal carcinoma cells. Exp Cell Res 225, 338 347.
7. Williams T, Admon A, Luscher B Tjian R (1988) Cloning and expression of AP-2, a cell-type-specific transcription factor that activates inducible enhancer elements. Genes Dev 2, 1557 1569.
8. Zhao F, Satoda M, Licht JD, Hayashizaki Y Gelb BD (2001) Cloning and characterization of a novel mouse AP-2 transcription factor, AP-2delta, with unique DNA binding and transactivation properties. J Biol Chem 276, 40755 40760.
9. Garcia MA, Campillos M, Ogueta S, Valdivieso F Vazquez J (2000) Identification of amino acid residues of transcription factor AP-2 involved in DNA binding. J Mol Biol 301, 807 816.
10. Wankhade S, Yu Y, Weinberg J, Tainsky MA Kannan P (2000) Characterization of the activation domains of AP-2 family transcription factors. J Biol Chem 275, 29701 29708.
11. Williams T Tjian R (1991) Analysis of the DNA-binding and activation properties of the human transcription factor AP-2. Genes Dev 5, 670 682.
12. Tummala R, Romano RA, Fuchs E Sinha S (2003) Molecular cloning and characterization of AP-2 epsilon, a fifth member of the AP-2 family. Gene 321, 93 102.
13. Wenke AK, Rothhammer T, Moser M Bosserhoff AK (2006) Regulation of integrin alpha10 expression in chondrocytes by the transcription factors AP-2epsilon and Ets-1. Biochem Biophys Res Commun 345, 495 501.
14. Thorogood PV Hinchliffe JR (1975) An analysis of the condensation process during chondrogenesis in the embryonic chick hind limb. J Embryol Exp Morphol 33, 581 606.
15. Janners MY Searls RL (1970) Changes in rate of cellular proliferation during the differentiation of cartilage and muscle in the mesenchyme of the embryonic chick wing. Dev Biol 23, 136 165.
16. Dessau W, von der MH, von der MK Fischer S (1980) Changes in the patterns of collagens and fibronectin during limb-bud chondrogenesis. J Embryol Exp Morphol 57, 51 60.
17. Mackie EJ Murphy LI (1998) The role of tenascin-C and related glycoproteins in early chondrogenesis. Microsc Res Tech 43, 102 110.
18. Kulyk WM, Upholt WB Kosher RA (1989) Fibronectin gene expression during limb cartilage differentiation. Development 106, 449 455.
19. Kosher RA, Kulyk WM Gay SW (1986) Collagen gene expression during limb cartilage differentiation. J Cell Biol 102, 1151 1156.
20. Kulyk WM, Coelho CN Kosher RA (1991) Type IX collagen gene expression during limb cartilage differentiation. Matrix 11, 282 288.
21. Tsonis PA Walker E (1991) Cell populations synthesizing cartilage proteoglycan core protein in the early chick limb bud. Biochem Biophys Res Commun 174, 688 695.
22. Bell DM, Leung KK, Wheatley SC, Ng LJ, Zhou S, Ling KW, Sham MH, Koopman P, Tam PP Cheah KS (1997) SOX9 directly regulates the type-II collagen gene. Nat Genet 16, 174 178.
23. Xie WF, Zhang X, Sakano S, Lefebvre V Sandell LJ (1999) Trans-activation of the mouse cartilage-derived retinoic acid-sensitive protein gene by Sox9. J Bone Miner Res 14, 757 763.
24. van de Wetering M Clevers H (1992) Sequence-specific interaction of the HMG box proteins TCF-1 and SRY occurs within the minor groove of a Watson-Crick double helix. EMBO J 11, 3039 3044.
25. Ng LJ, Wheatley S, Muscat GE, Conway-Campbell J, Bowles J, Wright E, Bell DM, Tam PP, Cheah KS Koopman P (1997) SOX9 binds DNA, activates transcription, and coexpresses with type II collagen during chondrogenesis in the mouse. Dev Biol 183, 108 121.
26. Zhao Q, Eberspaecher H, Lefebvre V De Crombrugghe B (1997) Parallel expression of Sox9 and Col2a1 in cells undergoing chondrogenesis. Dev Dyn 209, 377 386.
27. Roach HI, Aigner T, Soder S, Haag J Welkerling H (2007) Pathobiology of osteoarthritis: pathomechanisms and potential therapeutic targets. Curr Drug Targets 8, 271 282.
28. Bengtsson T, Aszodi A, Nicolae C, Hunziker EB, Lundgren-Akerlund E Fassler R (2005) Loss of alpha10beta1 integrin expression leads to moderate dysfunction of growth plate chondrocytes. J Cell Sci 118, 929 936.
29. Tscheudschilsuren G, Bosserhoff AK, Schlegel J, Vollmer D, Anton A, Alt V, Schnettler R, Brandt J Proetzel G (2006) Regulation of mesenchymal stem cell and chondrocyte differentiation by MIA. Exp Cell Res 312, 63 72.
30. Zhang J, Hagopian-Donaldson S, Serbedzija G, Elsemore J, Plehn-Dujowich D, McMahon AP, Flavell RA Williams T (1996) Neural tube, skeletal and body wall defects in mice lacking transcription factor AP-2. Nature 381, 238 241.
31. Wang HV, Vaupel K, Buettner R, Bosserhoff AK Moser M (2004) Identification and embryonic expression of a new AP-2 transcription factor, AP-2 epsilon. Dev Dyn 231, 128 135.
32. Boos N, Nerlich AG, Wiest I, von der MK, Ganz R Aebi M (1999) Immunohistochemical analysis of type-X-collagen expression in osteoarthritis of the hip joint. J Orthop Res 17, 495 502.
33. von der MK, Kirsch T, Nerlich A, Kuss A, Weseloh G, Gluckert K Stoss H (1992) Type X collagen synthesis in human osteoarthritic cartilage. Indication of chondrocyte hypertrophy. Arthritis Rheum 35, 806 811.
34. Adams SL, Cohen AJ Lassova L (2007) Integration of signaling pathways regulating chondrocyte differentiation during endochondral bone formation. J Cell Physiol 213, 635 641.
35. Goldring MB, Tsuchimochi K Ijiri K (2006) The control of chondrogenesis. J Cell Biochem 97, 33 44.
36. Chazaud C, Oulad-Abdelghani M, Bouillet P, Decimo D, Chambon P Dolle P (1996) AP-2.2, a novel gene related to AP-2, is expressed in the forebrain, limbs and face during mouse embryogenesis. Mech Dev 54, 83 94.
37. Schorle H, Meier P, Buchert M, Jaenisch R Mitchell PJ (1996) Transcription factor AP-2 essential for cranial closure and craniofacial development. Nature 381, 235 238.
38. Bi W, Deng JM, Zhang Z, Behringer RR De Crombrugghe B (1999) Sox9 is required for cartilage formation. Nat Genet 22, 85 89.
39. Akiyama H, Chaboissier MC, Martin JF, Schedl A De Crombrugghe B (2002) 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 16, 2813 2828.
40. Tchetina E, Mwale F Poole AR (2003) Distinct phases of coordinated early and late gene expression in growth plate chondrocytes in relationship to cell proliferation, matrix assembly, remodeling, and cell differentiation. J Bone Miner Res 18, 844 851.
41. Hamm A, Krott N, Breibach I, Blindt R Bosserhoff AK (2002) Efficient transfection method for primary cells. Tissue Eng 8, 235 245.
42. Kuphal S, Palm HG, Poser I Bosserhoff AK (2005) Snail-regulated genes in malignant melanoma. Melanoma Res 15, 305 313.
43. Rothhammer T, Poser I, Soncin F, Bataille F, Moser M Bosserhoff AK (2005) Bone morphogenic proteins are overexpressed in malignant melanoma and promote cell invasion and migration. Cancer Res 65, 448 456.
44. Lefebvre V, Huang W, Harley VR, Goodfellow PN De Crombrugghe B (1997) SOX9 is a potent activator of the chondrocyte-specific enhancer of the pro alpha1(II) collagen gene. Mol Cell Biol 17, 2336 2346.
45. Imhof A, Schuierer M, Werner O, Moser M, Roth C, Bauer R Buettner R (1999) Transcriptional regulation of the AP-2alpha promoter by BTEB-1 and AP-2rep, a novel wt-1-egr-related zinc finger repressor. Mol Cell Biol 19, 194 204.
46. Ho SN, Hunt HD, Horton RM, Pullen JK Pease LR (1989) Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 77, 51 59.