ELF3 modulates type II collagen gene (COL2A1) transcription in chondrocytes by inhibiting SOX9-CBP/p300-driven histone acetyltransferase activity

References

• Oettgen P, Alani RM, Barcinski MA, Brown L, Akbarali Y, Boltax J, Kunsch C, Munger K, Libermann TA. Isolation and characterization of a novel epithelium-specific transcription factor, ESE-1, a member of the ets family. Mol Cell Biol 1997;17(8):4419–33.
   PubMed Web of Science ®Google Scholar
• Oettgen P, Barcinski M, Boltax J, Stolt P, Akbarali Y, Libermann TA. Genomic organization of the human ELF3 (ESE-1/ESX) gene, a member of the Ets transcription factor family, and identification of a functional promoter. Genomics 1999;55(3):358–62.
   PubMed Web of Science ®Google Scholar
• Grall F, Gu X, Tan L, Cho JY, Inan MS, Pettit AR, Thamrongsak U, Choy BK, Manning C, Akbarali Y, Zerbini L, Rudders S, Goldring SR, Gravallese EM, Oettgen P, Goldring MB, Libermann TA. Responses to the proinflammatory cytokines interleukin-1 and tumor necrosis factor alpha in cells derived from rheumatoid synovium and other joint tissues involve nuclear factor kappaB-mediated induction of the Ets transcription factor ESE-1. Arthritis Rheum 2003;48(5):1249–60.
   PubMed Web of Science ®Google Scholar
• Rudders S, Gaspar J, Madore R, Voland C, Grall F, Patel A, Pellacani A, Perrella MA, Libermann TA, Oettgen P. ESE-1 is a novel transcriptional mediator of inflammation that interacts with NF-kappa B to regulate the inducible nitric-oxide synthase gene. J Biol Chem 2001;276(5):3302–9.
   PubMed Web of Science ®Google Scholar
• Grall FT, Prall WC, Wei W, Gu X, Cho JY, Choy BK, Zerbini LF, Inan MS, Goldring SR, Gravallese EM, Goldring MB, Oettgen P, Libermann TA. The Ets transcription factor ESE-1 mediates induction of the COX-2 gene by LPS in monocytes. FEBS J 2005;272(7):1676–87.
   PubMed Web of Science ®Google Scholar
• Otero M, Plumb DA, Tsuchimochi K, Dragomir CL, Hashimoto K, Peng H, Olivotto E, Bevilacqua M, Tan L, Yang Z, Zhan Y, Oettgen P, Li Y, Marcu KB, Goldring MB. E74-like factor 3 (ELF3) impacts on matrix metalloproteinase 13 (MMP13) transcriptional control in articular chondrocytes under proinflammatory stress. J Biol Chem 2012;287(5):3559–72.
   PubMed Web of Science ®Google Scholar
• Peng H, Tan L, Osaki M, Zhan Y, Ijiri K, Tsuchimochi K, Otero M, Wang H, Choy BK, Grall FT, Gu X, Libermann TA, Oettgen P, Goldring MB. ESE-1 is a potent repressor of type II collagen gene (COL2A1) transcription in human chondrocytes. J Cell Physiol 2008;215(2):562–73.
   PubMed Web of Science ®Google Scholar
• Davies SR, Sakano S, Zhu Y, Sandell LJ. Distribution of the transcription factors Sox9, AP-2, and [delta]EF1 in adult murine articular and meniscal cartilage and growth plate. J Histochem Cytochem 2002;50(8):1059–65.
   PubMed Web of Science ®Google Scholar
• Lefebvre V, Smits P. Transcriptional control of chondrocyte fate and differentiation. Birth Defects Res C Embryo Today 2005;75(3):200–12.
   PubMedGoogle Scholar
• Leung KK, Ng LJ, Ho KK, Tam PP, Cheah KS. Different cis-regulatory DNA elements mediate developmental stage- and tissue-specific expression of the human COL2A1 gene in transgenic mice. J Cell Biol 1998;141(6):1291–300.
   PubMed Web of Science ®Google Scholar
• Lefebvre V, Huang W, Harley VR, Goodfellow PN, 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(4):2336–46.
   PubMed Web of Science ®Google Scholar
• Lefebvre V, Li P, de Crombrugghe B. 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 1998;17(19):5718–33.
   PubMed Web of Science ®Google Scholar
• Bi W, Deng JM, Zhang Z, Behringer RR, de Crombrugghe B. Sox9 is required for cartilage formation. Nat Genet 1999;22(1):85–9.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Fernandez-Lloris R, Vinals F, Lopez-Rovira T, Harley V, Bartrons R, Rosa JL, Ventura F. Induction of the Sry-related factor SOX6 contributes to bone morphogenetic protein-2-induced chondroblastic differentiation of C3H10T1/2 cells. Mol Endocrinol 2003;17(7):1332–43.
   PubMed Web of Science ®Google Scholar
• 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(5):747–58.
   PubMed Web of Science ®Google Scholar
• Murray D, Precht P, Balakir R, Horton WE, Jr. The transcription factor deltaEF1 is inversely expressed with type II collagen mRNA and can repress Col2a1 promoter activity in transfected chondrocytes. J Biol Chem 2000;275(5):3610–8.
   PubMed Web of Science ®Google Scholar
• Zhang P, Jimenez SA, Stokes DG. Regulation of human COL9A1 gene expression. Activation of the proximal promoter region by SOX9. J Biol Chem 2003;278(1):117–23.
   PubMed Web of Science ®Google Scholar
• Bridgewater LC, Walker MD, Miller GC, Ellison TA, Holsinger LD, Potter JL, Jackson TL, Chen RK, Winkel VL, Zhang Z, McKinney S, de Crombrugghe B. Adjacent DNA sequences modulate Sox9 transcriptional activation at paired Sox sites in three chondrocyte-specific enhancer elements. Nucleic Acids Res 2003;31(5):1541–53.
   PubMed Web of Science ®Google Scholar
• Bridgewater LC, Lefebvre V, de Crombrugghe B. Chondrocyte-specific enhancer elements in the Col11a2 gene resemble the Col2a1 tissue-specific enhancer. J Biol Chem 1998;273(24):14998–5006.
   PubMed Web of Science ®Google Scholar
• Sekiya I, Tsuji K, Koopman P, Watanabe H, Yamada Y, Shinomiya K, Nifuji A, Noda M. SOX9 enhances aggrecan gene promoter/enhancer activity and is up-regulated by retinoic acid in a cartilage-derived cell line, TC6. J Biol Chem 2000;275(15):10738–44.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Genzer MA, Bridgewater LC. A Col9a1 enhancer element activated by two interdependent SOX9 dimers. Nucleic Acids Res 2007;35(4):1178–86.
   PubMed Web of Science ®Google Scholar
• Aigner T, Gebhard PM, Schmid E, Bau B, Harley V, Poschl E. SOX9 expression does not correlate with type II collagen expression in adult articular chondrocytes. Matrix Biol 2003;22(4):363–72.
   PubMed Web of Science ®Google Scholar
• Tchetina EV, Squires G, Poole AR. Increased type II collagen degradation and very early focal cartilage degeneration is associated with upregulation of chondrocyte differentiation related genes in early human articular cartilage lesions. J Rheumatol 2005;32(5):876–86.
   PubMed Web of Science ®Google Scholar
• Tsuda M, Takahashi S, Takahashi Y, Asahara H. Transcriptional co-activators CREB-binding protein and p300 regulate chondrocyte-specific gene expression via association with Sox9. J Biol Chem 2003;278(29):27224–9.
   PubMed Web of Science ®Google Scholar
• Furumatsu T, Tsuda M, Yoshida K, Taniguchi N, Ito T, Hashimoto M, Ito T, Asahara H. Sox9 and p300 cooperatively regulate chromatin-mediated transcription. J Biol Chem 2005;280(42):35203–8.
   PubMed Web of Science ®Google Scholar
• Hashimoto K, Otero M, Imagawa K, de Andres MC, Coico JM, Roach HI, Oreffo RO, Marcu KB, Goldring MB. Regulated transcription of human matrix metalloproteinase 13 (MMP13) and interleukin-1beta (IL1B) genes in chondrocytes depends on methylation of specific proximal promoter CpG sites. J Biol Chem 2013;288(14):10061–72.
   PubMed Web of Science ®Google Scholar
• Hashimoto K, Oreffo RO, Gibson MB, Goldring MB, Roach HI. DNA demethylation at specific CpG sites in the IL1B promoter in response to inflammatory cytokines in human articular chondrocytes. Arthritis Rheum 2009;60(11):3303–13.
   PubMed Web of Science ®Google Scholar
• Brown C, Gaspar J, Pettit A, Lee R, Gu X, Wang H, Manning C, Voland C, Goldring SR, Goldring MB, Libermann TA, Gravallese EM, Oettgen P. ESE-1 is a novel transcriptional mediator of angiopoietin-1 expression in the setting of inflammation. J Biol Chem 2004;279(13):12794–803.
   PubMed Web of Science ®Google Scholar
• Wang H, Fang R, Cho JY, Libermann TA, Oettgen P. Positive and negative modulation of the transcriptional activity of the ETS factor ESE-1 through interaction with p300, CREB-binding protein, and Ku 70/86. J Biol Chem 2004;279(24):25241–50.
   PubMed Web of Science ®Google Scholar
• Goldring MB, Marcu KB. Epigenomic and microRNA-mediated regulation in cartilage development, homeostasis, and osteoarthritis. Trends Mol Med. 2012;18(2):109–18.
   PubMed Web of Science ®Google Scholar
• Klug M, Rehli M. Functional analysis of promoter CpG methylation using a CpG-free luciferase reporter vector. Epigenetics 2006;1(3):127–30.
   PubMed Web of Science ®Google Scholar
• Munshi N, Agalioti T, Lomvardas S, Merika M, Chen G, Thanos D. Coordination of a transcriptional switch by HMGI(Y) acetylation. Science 2001;293(5532):1133–6.
   PubMed Web of Science ®Google Scholar
• Furumatsu T, Ozaki T, Asahara H. Smad3 activates the Sox9-dependent transcription on chromatin. Int J Biochem Cell Biol 2009;41(5):1198–204.
   PubMed Web of Science ®Google Scholar
• Furumatsu T, Tsuda M, Taniguchi N, Tajima Y, Asahara H. Smad3 induces chondrogenesis through the activation of SOX9 via CREB-binding protein/p300 recruitment. J Biol Chem 2005;280(9):8343–50.
   PubMed Web of Science ®Google Scholar
• Yang C, Shapiro LH, Rivera M, Kumar A, Brindle PK. A role for CREB binding protein and p300 transcriptional coactivators in Ets-1 transactivation functions. Mol Cell Biol 1998;18(4):2218–29.
   PubMed Web of Science ®Google Scholar
• Imamura T, Imamura C, Iwamoto Y, Sandell LJ. Transcriptional Co-activators CREB-binding protein/p300 increase chondrocyte Cd-rap gene expression by multiple mechanisms including sequestration of the repressor CCAAT/enhancer-binding protein. J Biol Chem 2005;280(17):16625–34.
   PubMed Web of Science ®Google Scholar
• Korzus E, Torchia J, Rose DW, Xu L, Kurokawa R, McInerney EM, Mullen TM, Glass CK, Rosenfeld MG. Transcription factor-specific requirements for coactivators and their acetyltransferase functions. Science 1998;279(5351):703–7.
   PubMed Web of Science ®Google Scholar
• Jayaraman G, Srinivas R, Duggan C, Ferreira E, Swaminathan S, Somasundaram K, Williams J, Hauser C, Kurkinen M, Dhar R, Weitzman S, Buttice G, Thimmapaya B. p300/cAMP-responsive element-binding protein interactions with ets-1 and ets-2 in the transcriptional activation of the human stromelysin promoter. J Biol Chem 1999;274(24):17342–52.
   PubMed Web of Science ®Google Scholar
• Kohli RM, Zhang Y. TET enzymes, TDG and the dynamics of DNA demethylation. Nature 2013;502(7472):472–9.
   PubMed Web of Science ®Google Scholar
• Johnson DG, Dent SY. Chromatin: receiver and quarterback for cellular signals. Cell 2013;152(4):685–9.
   PubMed Web of Science ®Google Scholar
• Okano M, Bell DW, Haber DA, Li E. DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell 1999;99(3):247–57.
   PubMed Web of Science ®Google Scholar
• Okano M, Xie S, Li E. Cloning and characterization of a family of novel mammalian DNA (cytosine-5) methyltransferases. Nat Genet 1998;19(3):219–20.
   PubMed Web of Science ®Google Scholar
• Walton EL, Francastel C, Velasco G. Maintenance of DNA methylation: Dnmt3b joins the dance. Epigenetics 2011;6(11):1373–7.
   PubMed Web of Science ®Google Scholar
• Barter MJ, Bui C, Young DA. Epigenetic mechanisms in cartilage and osteoarthritis: DNA methylation, histone modifications and microRNAs. Osteoarthritis Cartilage 2012;20(5):339–49.
   PubMed Web of Science ®Google Scholar
• de Andres MC, Imagawa K, Hashimoto K, Gonzalez A, Roach HI, Goldring MB, Oreffo RO. Loss of methylation in CpG sites in the NF-kappaB enhancer elements of inducible nitric oxide synthase is responsible for gene induction in human articular chondrocytes. Arthritis Rheum 2013;65(3):732–42.
   PubMed Web of Science ®Google Scholar
• Jaenisch R, Bird A. Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat Genet 2003;33 Suppl:245–54.
   PubMed Web of Science ®Google Scholar
• Moore LD, Le T, Fan G. DNA methylation and its basic function. Neuropsychopharmacology 2013;38(1):23–38.
   PubMed Web of Science ®Google Scholar
• Vinson C, Chatterjee R. CG methylation. Epigenomics 2012;4(6):655–63.
   PubMed Web of Science ®Google Scholar
• Imagawa K, de Andres MC, Hashimoto K, Pitt D, Itoi E, Goldring MB, Roach HI, Oreffo RO. The epigenetic effect of glucosamine and a nuclear factor-kappa B (NF-kB) inhibitor on primary human chondrocytes–implications for osteoarthritis. Biochem Biophys Res Commun 2011;405(3):362–7.
   PubMed Web of Science ®Google Scholar
• Robertson KD. DNA methylation and human disease. Nat Rev Genet 2005;6(8):597–610.
   PubMed Web of Science ®Google Scholar
• Roach HI, Yamada N, Cheung KS, Tilley S, Clarke NM, Oreffo RO, Kokubun S, Bronner F. Association between the abnormal expression of matrix-degrading enzymes by human osteoarthritic chondrocytes and demethylation of specific CpG sites in the promoter regions. Arthritis Rheum 2005;52(10):3110–24.
   PubMed Web of Science ®Google Scholar
• Jeffries MA, Donica M, Baker LW, Stevenson ME, Annan AC, Humphrey MB, James JA, Sawalha AH. Genome-wide DNA methylation study identifies significant epigenomic changes in osteoarthritic cartilage. Arthritis Rheumatol 2014;66(10):2804–15.
   PubMed Web of Science ®Google Scholar
• Moazedi-Fuerst FC, Hofner M, Gruber G, Weinhaeusel A, Stradner MH, Angerer H, Peischler D, Lohberger B, Glehr M, Leithner A, Sonntagbauer M, Graninger WB. Epigenetic differences in human cartilage between mild and severe OA. J Orthop Res 2014;32(12):1636–45.
   PubMed Web of Science ®Google Scholar
• Bomer N, den Hollander W, Ramos YF, Bos SD, van der Breggen R, Lakenberg N, Pepers BA, van Eeden AE, Darvishan A, Tobi EW, Duijnisveld BJ, van den Akker EB, Heijmans BT, van Roon-Mom WM, Verbeek FJ, van Osch GJ, Nelissen RG, Slagboom PE, Meulenbelt I. Underlying molecular mechanisms of DIO2 susceptibility in symptomatic osteoarthritis. Ann Rheum Dis 2015;74(8):1571–9.
   Google Scholar
• Fernandez-Tajes J, Soto-Hermida A, Vazquez-Mosquera ME, Cortes-Pereira E, Mosquera A, Fernandez-Moreno M, Oreiro N, Fernandez-Lopez C, Fernandez JL, Rego-Perez I, Blanco FJ. Genome-wide DNA methylation analysis of articular chondrocytes reveals a cluster of osteoarthritic patients. Ann Rheum Dis 2014;73(4):668–77.
   Google Scholar
• Rushton MD, Reynard LN, Barter MJ, Refaie R, Rankin KS, Young DA, Loughlin J. Characterization of the cartilage DNA methylome in knee and hip osteoarthritis. Arthritis Rheumatol 2014;66(9):2450–60.
   Google Scholar
• Bradley EW, Carpio LR, McGee-Lawrence ME, Castillejo Becerra C, Amanatullah DF, Ta LE, Otero M, Goldring MB, Kakar S, Westendorf JJ. Phlpp1 facilitates post-traumatic osteoarthritis and is induced by inflammation and promoter demethylation in human osteoarthritis. Osteoarthritis Cartilage 2016;24(6):1021–8.
   Google Scholar
• Takahashi A, de Andres MC, Hashimoto K, Itoi E, Oreffo RO. Epigenetic regulation of interleukin-8, an inflammatory chemokine, in osteoarthritis. Osteoarthritis Cartilage 2015;23(11):1946–54.
   PubMed Web of Science ®Google Scholar
• Bui C, Barter MJ, Scott JL, Xu Y, Galler M, Reynard LN, Rowan AD, Young DA. cAMP response element-binding (CREB) recruitment following a specific CpG demethylation leads to the elevated expression of the matrix metalloproteinase 13 in human articular chondrocytes and osteoarthritis. FASEB J 2012;26(7):3000–11.
   PubMed Web of Science ®Google Scholar
• da Silva MA, Yamada N, Clarke NM, Roach HI. Cellular and epigenetic features of a young healthy and a young osteoarthritic cartilage compared with aged control and OA cartilage. J Orthop Res 2009;27(5):593–601.
   PubMed Web of Science ®Google Scholar
• Scott JL, Gabrielides C, Davidson RK, Swingler TE, Clark IM, Wallis GA, Boot-Handford RP, Kirkwood TB, Taylor RW, Young DA. Superoxide dismutase downregulation in osteoarthritis progression and end-stage disease. Ann Rheum Dis 2010;69(8):1502–10.
   PubMed Web of Science ®Google Scholar
• Kim KI, Park YS, Im GI. Changes in the epigenetic status of the SOX-9 promoter in human osteoarthritic cartilage. J Bone Miner Res 2013;28(5):1050–60.
   PubMed Web of Science ®Google Scholar
• Reynard LN, Bui C, Syddall CM, Loughlin J. CpG methylation regulates allelic expression of GDF5 by modulating binding of SP1 and SP3 repressor proteins to the osteoarthritis susceptibility SNP rs143383. Hum Genet 2014;133(8):1059–73.
   Google Scholar
• Papathanasiou I, Kostopoulou F, Malizos KN, Tsezou A. DNA methylation regulates sclerostin (SOST) expression in osteoarthritic chondrocytes by bone morphogenetic protein 2 (BMP-2) induced changes in Smads binding affinity to the CpG region of SOST promoter. Arthritis Res Ther 2015;17:160.
   PubMed Web of Science ®Google Scholar
• Zimmermann P, Boeuf S, Dickhut A, Boehmer S, Olek S, Richter W. Correlation of COL10A1 induction during chondrogenesis of mesenchymal stem cells with demethylation of two CpG sites in the COL10A1 promoter. Arthritis Rheum 2008;58(9):2743–53.
   PubMed Web of Science ®Google Scholar
• Imagawa K, de Andres MC, Hashimoto K, Itoi E, Otero M, Roach HI, Goldring MB, Oreffo RO. Association of reduced type IX collagen gene expression in human osteoarthritic chondrocytes with epigenetic silencing by DNA hypermethylation. Arthritis Rheumatol 2014;66(11):3040–51.
   PubMed Web of Science ®Google Scholar
• Poschl E, Fidler A, Schmidt B, Kallipolitou A, Schmid E, Aigner T. DNA methylation is not likely to be responsible for aggrecan down regulation in aged or osteoarthritic cartilage. Ann Rheum Dis 2005;64(3):477–80.
   PubMed Web of Science ®Google Scholar
• Sesselmann S, Soder S, Voigt R, Haag J, Grogan SP, Aigner T. DNA methylation is not responsible for p21WAF1/CIP1 down-regulation in osteoarthritic chondrocytes. Osteoarthritis Cartilage 2009;17(4):507–12.
   PubMed Web of Science ®Google Scholar
• Rishi V, Bhattacharya P, Chatterjee R, Rozenberg J, Zhao J, Glass K, Fitzgerald P, Vinson C. CpG methylation of half-CRE sequences creates C/EBPalpha binding sites that activate some tissue-specific genes. Proc Natl Acad Sci USA. 2010;107(47):20311–6.
   PubMed Web of Science ®Google Scholar
• Wu J, Duan R, Cao H, Field D, Newnham CM, Koehler DR, Zamel N, Pritchard MA, Hertzog P, Post M, Tanswell AK, Hu J. Regulation of epithelium-specific Ets-like factors ESE-1 and ESE-3 in airway epithelial cells: potential roles in airway inflammation. Cell Res 2008;18(6):649–63.
   PubMed Web of Science ®Google Scholar
• Green BB, Houseman EA, Johnson KC, Guerin DJ, Armstrong DA, Christensen BC, Marsit CJ. Hydroxymethylation is uniquely distributed within term placenta, and is associated with gene expression. FASEB J 2016 Apr 26. pii: fj.201600310R. [Epub ahead of print]
   Google Scholar
• Taylor SE, Li YH, Smeriglio P, Rath M, Wong WH, Bhutani N. Stable 5-Hydroxymethylcytosine (5hmC) acquisition marks gene activation during chondrogenic differentiation. J Bone Miner Res 2016;31(3):524–34.
   PubMed Web of Science ®Google Scholar