Sox9/Sox6 and Sp1 are involved in the insulin-like growth factor-I-mediated upregulation of human type II collagen gene expression in articular chondrocytes

Journal of Molecular Medicine

Volumn 90, Issue 6, 2012, Pages 649-666

  Renard, Emmanuelle ^a   Porée, Benoît ^a   Chadjichristos, Christos ^a   Kypriotou, Magdalini ^a   Maneix, Laure ^a   Bigot, Nicolas ^a   Legendre, Florence ^a   Ollitrault, David ^a   De Crombrugghe, Benoît ^b   Malléin Gérin, Frédéric ^c   Moslemi, Safa ^a   Demoor, Magali ^a   Boumediene, Karim ^a   Galéra, Philippe ^a  

^a UNIVERSITÉ DE CAEN   (France)

^b UNIVERSITY OF TEXAS   (United States)

^c UNIVERSITÉ LYON 1   (France)

Author keywords

Cartilage; Chondrocytes; COL2A1; IGF I; Osteoarthritis; p300; Sox6; Sox9; Sp1; Sp3; Type II collagen

Indexed keywords

COLLAGEN TYPE 2; HISTONE ACETYLTRANSFERASE PCAF; SMALL INTERFERING RNA; SOMATOMEDIN C; TRANSCRIPTION FACTOR SOX5; TRANSCRIPTION FACTOR SOX6; TRANSCRIPTION FACTOR SOX9; TRANSCRIPTION FACTOR SP1; TRANSCRIPTION FACTOR SP3;

ANIMAL CELL; ARTICLE; ARTICULAR CARTILAGE; CARTILAGE CELL; CHROMATIN IMMUNOPRECIPITATION; CIS ISOMER; COLLAGEN SYNTHESIS; CONTROLLED STUDY; ENHANCER REGION; EUCHROMATIN; GENE EXPRESSION; GENE SILENCING; GENE TARGETING; INTRON; NONHUMAN; PROMOTER REGION; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; TRANSACTIVATION; TRANSCRIPTION REGULATION; UPREGULATION;

ANIMALS; BLOTTING, WESTERN; CARTILAGE, ARTICULAR; CELLS, CULTURED; CHONDROCYTES; COLLAGEN TYPE II; GENE EXPRESSION REGULATION; HUMANS; IMMUNOGLOBULINS; INSULIN-LIKE GROWTH FACTOR I; POLYMERASE CHAIN REACTION; RABBITS; SOX9 TRANSCRIPTION FACTOR; SOXD TRANSCRIPTION FACTORS; UP-REGULATION;

EID: 84862670015     PISSN: 09462716     EISSN: 14321440     Source Type: Journal    
DOI: 10.1007/s00109-011-0842-3     Document Type: Article

References (48)

1. V Lefebvre G Zhou K Mukhopadhyay CN Smith Z Zhang H Eberspaecher X Zhou S Sinha SN Maity B De Crombrugghe 1996 A 18-base pair sequence in the mouse proα(II) collagen gene is sufficient for expression in cartilage and binds nuclear proteins that are selectively expressed in chondrocytes Mol Cell Biol 16 4512 4523 8754852 1:CAS:528:DyaK28XksVaktr0%3D
2. PH Krebsbach K Nakata SM Bernier O Hatano T Miyashita CS Rhodes Y Yamada 1996 Identification of a minimum enhancer sequence for the type II collagen gene reveals several core sequence motifs in common with the link protein gene J Biol Chem 271 4298 4303 8626777 10.1074/jbc.271.8.4298 1:CAS:528: DyaK28XhtlSmt7s%3D
3. DM Bell KK Leung SC Wheatley LJ Ng S Zhou KW Ling MH Sham P Koopman PPL Tam KSE Cheah 1997 SOX9 directly regulates the type-II collagen gene Nat Genet 16 174 178 9171829 10.1038/ng0697-174 1:CAS:528:DyaK2sXjs1agsr4%3D
4. KK Leung LJ Ng KK Ho PPL Tam KSE Cheah 1998 Different cis-regulatory DNA elements mediate developmental stage- and tissue-specific expression of the human COL2A1 gene in transgenic mice J Cell Biol 141 1291 1300 9628886 10.1083/jcb.141.6.1291 1:CAS:528:DyaK1cXjvFKksLc%3D
5. C Ghayor JF Herrouin C Chadjichristos L Ala-Kokko M Takigawa JP Pujol P Galéra 2000 Regulation of human COL2A1 gene expression in chondrocytes: identification of C-Krox responsive elements and modulation by phenotype alteration J Biol Chem 275 27421 27438 10856292 1:CAS:528:DC%2BD3cXmsVWqt7k%3D
6. G Zhou V Lefebvre ZP Zhang H Eberspaecher B de Crombrugghe 1998 Three high mobility group-like sequences within a 48-base pair enhancer of the Col2a1 gene are required for cartilage-specific expression in vivo J Biol Chem 273 14989 14997 9614106 10.1074/jbc.273.24.14989 1:CAS:528:DyaK1cXktVehsbg%3D
7. V Lefebvre P Li B de Crombrugghe 1998 A new long form of Sox5 (L-Sox5), Sox6 and Sox9 are coexpressed in chondrogenesis and cooperatively activate the type II collagen gene EMBO J 17 5718 5733 9755172 10.1093/emboj/17.19.5718 1:CAS:528:DyaK1cXmvVyjsLs%3D
8. C Ghayor C Chadjichristos JF Herrouin L Ala-Kokko G Suske JP Pujol P Galéra 2001 Sp3 represses the Sp1-mediated transactivation of the human COL2A1 gene in primary and de-differentiated chondrocytes J Biol Chem 276 36881 36895 11447232 10.1074/jbc.M105083200 1:CAS:528:DC%2BD3MXns1eltr0%3D
9. I Sakiya K Tsuji P Koopman H Watanabe Y Yamada K Shinomiya A Nifuji M Noda 2000 SOX9 enhances aggrecan gene promoter/enhancer activity and is up-regulated by retinoic acid in a cartilage-derived cell line, TC6 J Biol Chem 275 10738 10744 10.1074/jbc.275.15.10738
10. W Bi JM Deng Z Zhang RR Beringher B de Crombrugghe 1999 Sox9 is required for cartilage formation Nat Genet 22 85 89 10319868 10.1038/8792 1:CAS:528:DyaK1MXjtVagsLw%3D
11. V Lefebvre W Huang VR Harley PN Goodfellow B de Crombrugghe 1997 SOX9 is a potent activator of the chondrocyte-specific enhancer of the pro alpha1(II) collagen gene Mol Cell Biol 17 2336 2346 9121483 1:CAS:528:DyaK2sXhvFOhsLg%3D
12. V Lefebvre B de Crombrugghe 1998 Toward understanding Sox9 function in chondrocyte differentiation Matrix Biol 16 529 540 9569122 10.1016/S0945- 053X(98)90065-8 1:CAS:528:DyaK1cXivFKltrY%3D
13. LJ Ng S Wheatley GE Muscat J Conway-Campbell J Bowles E Wright DM Bell PP Tam KS Cheah P Koopman 1997 SOX9 binds DNA, activates transcription, and coexpresses with type II collagen during chondrogenesis in the mouse Dev Biol 183 108 121 9119111 10.1006/dbio.1996.8487 1:CAS:528:DyaK2sXhvVyqtL4%3D
14. Q Zhao H Eberspaecher V Lefebvre B de Crombrugghe 1997 Parallel expression of Sox9 and Col2α1 in cells undergoing chondrogenesis Dev Dyn 209 377 386 9264261 10.1002/(SICI)1097-0177(199708)209:4<377::AID-AJA5>3. 0.CO;2-F 1:CAS:528:DyaK2sXls1WktLk%3D
15. A Matsuno T Sasaki T Nagashima R Matsuura H Tanaka M Hirakawa M Murakami T Kirino 1997 Immunohistochemical examination of proliferative potentials and the expression of cell cycle-related proteins of intracranial chordomas Hum Pathol 28 714 719 9191006 10.1016/S0046-8177(97)90181-7 1:STN:280: DyaK2szjsVejuw%3D%3D
16. M Kypriotou M Fossard-Demoor C Chadjichristos C Ghayor B de Crombrugghe JP Pujol P Galéra 2003 Sox9 exerts a bifunctional effect on type II collagen gene (COL2A1) expression in chondrocytes depending on the differentiation state DNA Cell Biol 22 119 129 12713737 10.1089/ 104454903321515922 1:CAS:528:DC%2BD3sXis1Cgtb8%3D
17. E Kolettas HI Muir JC Barrett TE Hardingham 2001 Chondrocyte phenotype and cell survival are regulated by culture conditions and by specific cytokines through the expression of Sox-9 transcription factor Rheumatology 40 1146 1156 11600745 10.1093/rheumatology/40.10.1146 1:CAS:528:DC%2BD3MXot1GlurY%3D
18. J Martel-Pelletier JA Di Battista D Lajeunesse JP Pelletier 1998 IGF/IGFBP axis in cartilage and bone in osteoarthritis pathogenesis Inflamm Res 47 90 100 9562333 10.1007/s000110050288 1:CAS:528:DyaK1cXhvFyit74%3D
19. Y Wang S Nishida T Sakata HZ Elalieh W Chang BP Halloran SB Doty DD Bikle 2006 Insulin-like growth factor is essential for embryonic bone development Endocrinology 147 4753 4761 16857753 10.1210/en.2006-0196 1:CAS:528: DC%2BD28XhtVSksbrE
20. JP Liu J Baker AS Perkins E Robertson A Efstratiadis 1993 Mice carrying null mutations of the genes encoding insulin-like growth factor I (Igf-1) and type 1 IGF receptor (Igf1r) Cell 75 59 72 8402901 1:CAS:528:DyaK2cXps12nsg%3D%3D
21. J Baker JP Liu AS Perkins E Robertson A Efstratiadis 1993 Role of insulin-like growth factors in embryonic and postnatal growth Cell 75 73 82 8402902 1:CAS:528:DyaK3sXms1entLs%3D
22. JL Liu S Yakar D LeRoith 2000 Conditional knockout of mouse insulin-like growth factor-1 gene using the Cre/lox P system Proc Soc Exp Biol Med 223 344 351 10721003 10.1046/j.1525-1373.2000.22349.x 1:CAS:528:DC%2BD3cXitlCqt74%3D
23. J Middleton A Manthey J Tyler 1996 Insulin-like growth factor (IGF) receptor, IGF-I, interleukin-1 beta (IL-1 beta), and IL-6 mRNA expression in osteoarthritic and normal human cartilage J Histochem Cytochem 44 133 141 8609369 10.1177/44.2.8609369 1:CAS:528:DyaK28XhtF2ktL4%3D
24. Morales TI (1992) Articular cartilage and osteoarthritis, 1st edn. Raven, New York
25. P Van der Kraan P Buma T van Kuppevelt WB van der Berg 2002 Interaction of chondrocytes, extracellular matrix and growth factors: relevance for articular cartilage tissue engineering Osteoarthritis Cartilage 10 631 637 12479385 10.1053/joca.2002.0806
26. AM Garcia N Szasz SB Trippel TI Morales AJ Grodzinsky EH Frank 2003 Transport and binding of insulin-like growth factor I through articular cartilage Arch Biochem Biophys 415 69 79 12801514 10.1016/S0003-9861(03)00215-7 1:CAS:528:DC%2BD3sXksVakurw%3D
27. CM Mierisch PC Anderson G Balian DR Diduch 2002 Treatment with insulin-like growth factor-1 increases chondrogenesis by periosteum in vitro Connect Tissue Res 43 559 568 12685862 1:CAS:528:DC%2BD38XovVGgsrk%3D
28. FP Luyten VC Hascall SP Nissley TI Morales AH Reddi 1988 Insulin-like growth factors maintain steady-state metabolism of proteoglycans in bovine articular cartilage explants Arch Biochem Biophys 267 416 425 3214163 10.1016/0003-9861(88)90047-1 1:CAS:528:DyaL1MXjsVeksw%3D%3D
29. P Smith FD Schuler HI Georgescu SC Ghivizzani B Johnstone C Niyibizi PD Robbins CH Evans 2000 Genetic enhancement of matrix synthesis by articular chondrocytes: comparison of different growth factor genes in the presence and absence of interleukin-1 Arthritis Rheum 43 1156 1164 10817570 10.1002/1529-0131(200005)43:5<1156::AID-ANR26>3.0.CO;2-M 1:CAS:528:DC%2BD3cXjvVeiu74%3D
30. H Madry R Pareda J Seidel R Langer LE Freed SB Trippel G Vunjak-Novakovic 2002 Gene transfer of a human insulin-like growth factor I cDNA enhances tissue engineering of cartilage Human Genet Ther 8 1443 1449
31. P Mathieu 2002 A new mechanism of action of chondroitin sulfates ACS4-ACS6 in osteoarthritic cartilage Presse Med 31 1383 1385 12375394
32. B Porée M Kypriotou C Chadjichristos G Beauchef E Renard F Legendre M Melin S Gueret DJ Hartmann F Mallein-Guerin JP Pujol K Boumediene P Galéra 2008 Interleukin-6 (IL-6) and/or soluble IL-6 receptor down-regulation of human type II collagen gene expression in articular chondrocytes requires a decrease of Sp1.Sp3 ratio and of the binding activity of both factors to the COL2A1 promoter J Biol Chem 283 4850 4865 18065760 10.1074/jbc.M706387200
33. C Chadjichristos C Ghayor JF Herrouin L Ala-Kokko G Suske JP Pujol P Galéra 2002 Down-regulation of human type II collagen gene expression by transforming growth factor-β1 (TGF-β1) in articular chondrocytes involves Sp1/Sp3 ratio J Biol Chem 277 43903 43917 12186868 10.1074/jbc. M206111200 1:CAS:528:DC%2BD38Xos1aksrc%3D
34. C Chadjichristos C Ghayor M Kypriotou G Martin E Renard L Ala-Kokko G Suske B de Crombrugghe JP Pujol P Galéra 2003 Sp1 and Sp3 transcription factors mediate interleukin-1β down-regulation of human type II collagen gene expression in articular chondrocytes J Biol Chem 278 39762 39772 12888570 10.1074/jbc.M303541200 1:CAS:528:DC%2BD3sXnvFanu78%3D
35. M Shakibaei C Seifarth T John M Rahmanzadeh A Mobasheri 2006 IGF-I extends the chondrogenic potential of human articular chondrocytes in vitro: molecular association between Sox9 and Erk1/2 Biochem Pharmacol 72 1382 1395 17010943 10.1016/j.bcp.2006.08.022 1:CAS:528:DC%2BD28XhtFOjtrbI
36. C Magee M Nurminskaya L Faverman P Galera T Linsenmayer 2005 Sp3/Sp1 transcription activity regulates specific expression of collagen type X in hypertrophic chondrocytes J Biol Chem 280 25331 25338 15849196 10.1074/jbc.M412549200 1:CAS:528:DC%2BD2MXlslyltLw%3D
37. P Savagner PH Krebsbach O Hatano T Miyashita J Liebman Y Yamada 1995 Collagen II promoter and enhancer interact synergistically through Sp1 and distinct nuclear factors DNA Cell Biol 14 501 510 7598805 10.1089/dna.1995.14. 501 1:CAS:528:DyaK2MXmsFKktL0%3D
38. T Hattori F Coustry S Stephens H Eberspaecher M Takigawa H Yasuda B de Crombrugghe 2008 Transcriptional regulation of chondrogenesis by coactivator Tip60 via chromatin association with Sox9 and Sox5 Nucleic Acids Res 36 3011 3024 18390577 10.1093/nar/gkn150 1:CAS:528:DC%2BD1cXmtleru7k%3D
39. T Furumatsu M Tsuda K Yoshida N Taniguchi T Ito M Hashimoto T Ito H Asahara 2005 Sox9 and p300 cooperatively regulate chromatin-mediated transcription J Biol Chem 280 35203 35208 16109717 10.1074/jbc.M502409200 1:CAS:528:DC%2BD2MXhtFWmtbjE
40. M Tsuda S Takahashi Y Takahashi H Asahara 2003 Transcriptional co-activators CREB-binding protein and p300 regulate chondrocyte-specific gene expression via association with Sox9 J Biol Chem 278 27224 27229 12732631 10.1074/jbc.M303471200 1:CAS:528:DC%2BD3sXltlOjsr4%3D
41. Y Kawakami M Tsuda S Takahashi N Taniguchi CR Esteban M Zemmyo T Furumatsu M Lotz JC Belmonte H Asahara 2005 Transcriptional coactivator PGC-1α regulates chondrogenesis via association with Sox9 Proc Natl Acad Sci USA 102 2414 2419 15699338 10.1073/pnas.0407510102 1:CAS:528: DC%2BD2MXhvFKitLw%3D
42. S Piera-Velazquez DF Hawkins MK Whitecavage DC Colter DG Stokes SA Jimenez 2007 Regulation of the human SOX9 promoter by Sp1 and CREB Exp Cell Res 313 1069 1079 17289023 10.1016/j.yexcr.2007.01.001 1:CAS:528: DC%2BD2sXjsVWgtbY%3D
43. D Breitner-Johnson H Werner CT Roberts Jr D LeRoith 1995 Regulation of insulin-like growth factor receptor gene expression by Sp1: physical and functional interactions of Sp1 at GC boxes and at a CT element Mol Endo 9 1147 1156 10.1210/me.9.9.1147
44. C Kramps V Strieder A Sapetschnig G Suske W Lutz 2004 E2F and Sp1/Sp3 synergize but are not sufficient to activate the MYCN gene in neuroblastomas J Biol Chem 279 5110 5117 14645238 10.1074/jbc.M304758200 1:CAS:528: DC%2BD2cXhtFeqsLs%3D
45. M Brittberg A Lindahl A Nilsson C Ohlsson O Isaksson L Peterson 1994 Treatment of deep cartilage defects in the knee with autologous chondrocyte transplantation N Engl J Med 331 889 895 8078550 10.1056/NEJM199410063311401 1:STN:280:DyaK2czlvFGlug%3D%3D
46. AF Steinert U Nöth RS Tuan 2008 Concepts in gene therapy for cartilage repair Injury 39S1 S97 S113 10.1016/j.injury.2008.01.034
47. G Zhai F Rivadeneira JJ Houwing-Duistermaat I Meulenbelt C Bijkerk A Hofman JBJ van Meurs AG Uitterlinden HAP Pols PE Slagboom CM van Duijn 2003 Insulin-like growth factor I gene promoter polymorphism, collagen type II α1 (COL2A1) gene, and the prevalence of radiographic osteoarthritis: the Rotterdam Study Ann Rheum Dis 63 544 548 10.1136/ard.2003.010751
48. SR Tew Y Li P Pothacharoen LM Tweats RE Hawkins TE Hardingham 2005 Retroviral transduction with SOX9 enhances re-expression of the chondrocyte phenotype in passaged osteoarthritic human articular chondrocytes Osteoarthritis Cartilage 13 80 89 15639641 10.1016/j.joca.2004.10.011