Regulated transcription of human matrix metalloproteinase 13 (MMP13) and interleukin-1β (IL1B) genes in chondrocytes depends on methylation of specific proximal promoter CpG sites

Journal of Biological Chemistry

Volumn 288, Issue 14, 2013, Pages 10061-10072

  Hashimoto, Ko ^a,b   Otero, Miguel ^a   Imagawa, Kei ^c   De Andrés, María C ^c,f   Coico, Jonathan M ^a   Roach, Helmtrud I ^g   Oreffo, Richard O C ^c   Marcu, Kenneth B ^d,e   Goldring, Mary B ^a  

^a HOSPITAL FOR SPECIAL SURGERY   (United States)

^b TOHOKU UNIVERSITY   (Japan)

^c UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

^d RIZZOLI ORTHOPAEDIC INSTITUTE   (Italy)

^e STONY BROOK UNIVERSITY   (United States)

^f Instituto de Salud Carlos III   (Spain)

^g NONE

Author keywords

[No Author keywords available]

Indexed keywords

CHROMATIN IMMUNOPRECIPITATION ASSAY; HUMAN CARTILAGE; HYPOXIA-INDUCIBLE FACTORS; METHYLATION ANALYSIS; MUSCULOSKELETAL DISEASE; PROMOTER ACTIVITIES; TRANSCRIPTIONAL ACTIVITY; TRANSCRIPTIONAL REGULATION;

ALKYLATION; BODY FLUIDS; DIGITAL STORAGE; GENES; METHYLATION; TRANSCRIPTION FACTORS;

TRANSCRIPTION;

COLLAGENASE 3; ELF3 PROTEIN; HYPOXIA INDUCIBLE FACTOR 1ALPHA; HYPOXIA INDUCIBLE FACTOR 2ALPHA; INTERLEUKIN 1BETA; TRANSCRIPTION FACTOR AP 1; TRANSCRIPTION FACTOR GATA 1; TRANSCRIPTION FACTOR RUNX2; TRANSCRIPTION FACTOR SP1; UNCLASSIFIED DRUG; UPSTREAM STIMULATORY FACTOR 1;

ARTICLE; CARTILAGE CELL; CONTROLLED STUDY; CPG ISLAND; DEMETHYLATION; DNA METHYLATION; GENE EXPRESSION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; INTERLEUKIN 1BETA GENE; MMP13 GENE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN MOTIF; SITE DIRECTED MUTAGENESIS; TRANSCRIPTION REGULATION;

CARTILAGE; CHONDROCYTES; CPG ISLANDS; DNA METHYLATION; EPIGENESIS, GENETIC; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HUMANS; INTERLEUKIN-1BETA; INTERLEUKINS; MATRIX METALLOPROTEINASE 13; MODELS, GENETIC; OSTEOARTHRITIS; PLASMIDS; POINT MUTATION; PROMOTER REGIONS, GENETIC; SEQUENCE ANALYSIS, DNA; TRANSCRIPTIONAL ACTIVATION;

EID: 84875999020     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.421156     Document Type: Article

References (67)

1. Berger, S. L. (2007) The complex language of chromatin regulation during transcription. Nature 447, 407-412
2. Razin, A. (1998) CpG methylation, chromatin structure and gene silencing- a three-way connection. EMBO J. 17, 4905-4908
3. Irvine, R. A., Lin, I. G., and Hsieh, C. L. (2002)DNAmethylation has a local effect on transcription and histone acetylation. Mol. Cell Biol. 22, 6689-6696
4. Nan, X., Ng, H. H., Johnson, C. A., Laherty, C. D., Turner, B. M., Eisenman, R. N., and Bird, A. (1998) Transcriptional repression by the methyl-CpG-binding protein MeCP2 involves a histone deacetylase complex. Nature 393, 386-389
5. Okitsu, C. Y., and Hsieh, C. L. (2007) DNA methylation dictates histone H3K4 methylation. Mol. Cell Biol. 27, 2746-2757
6. Rishi, V., Bhattacharya, P., Chatterjee, R., Rozenberg, J., Zhao, J., Glass, K., Fitzgerald, P., and Vinson, C. (2010) CpG methylation of half-CRE sequences creates C/EBPalpha binding sites that activate some tissue-specific genes. Proc. Natl. Acad. Sci. U.S.A. 107, 20311-20316
7. Wade, P. A., Gegonne, A., Jones, P. L., Ballestar, E., Aubry, F., and Wolffe, A. P. (1999) Mi-2 complex couples DNA methylation to chromatin remodelling and histone deacetylation. Nat. Genet. 23, 62-66
8. Bird, A. (2002) DNA methylation patterns and epigenetic memory. Genes Dev. 16, 6-21
9. Reik, W. (2007) Stability and flexibility of epigenetic gene regulation in mammalian development. Nature 447, 425-432
10. Bui, C., Barter, M. J., Scott, J. L., Xu, Y., Galler, M., Reynard, L. N., Rowan, A. D., and Young, D. A. (2012) 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. 26, 3000-3011
11. Murayama, A., Sakura, K., Nakama, M., Yasuzawa-Tanaka, K., Fujita, E., Tateishi, Y., Wang, Y., Ushijima, T., Baba, T., Shibuya, K., Shibuya, A., Kawabe, Y., and Yanagisawa, J. (2006) A specific CpG site demethylation in the human interleukin 2 gene promoter is an epigenetic memory. EMBO J. 25, 1081-1092
12. Ballestar, E. (2011) Epigenetic alterations in autoimmune rheumatic diseases. Nat. Rev. Rheumatol. 7, 263-271
13. Grabiec, A. M., Krausz, S., de Jager, W., Burakowski, T., Groot, D., Sanders, M. E., Prakken, B. J., Maslinski, W., Eldering, E., Tak, P. P., and Reedquist, K. A. (2010) Histone deacetylase inhibitors suppress inflammatory activation of rheumatoid arthritis patient synovial macrophages and tissue. J. Immunol. 184, 2718-2728
14. Horiuchi, M., Morinobu, A., Chin, T., Sakai, Y., Kurosaka, M., and Kumagai, S. (2009) Expression and function of histone deacetylases in rheumatoid arthritis synovial fibroblasts. J. Rheumatol. 36, 1580-1589
15. Huber, L. C., Brock, M., Hemmatazad, H., Giger, O. T., Moritz, F., Trenkmann, M., Distler, J. H., Gay, R. E., Kolling, C., Moch, H., Michel, B. A., Gay, S., Distler, O., and Jüngel, A. (2007) Histone deacetylase/acetylase activity in total synovial tissue derived from rheumatoid arthritis and osteoarthritis patients. Arthritis. Rheum. 56, 1087-1093
16. Kawabata, T., Nishida, K., Takasugi, K., Ogawa, H., Sada, K., Kadota, Y., Inagaki, J., Hirohata, S., Ninomiya, Y., and Makino, H. (2010) Increased activity and expression of histone deacetylase 1 in relation to tumor necrosis factor-α in synovial tissue of rheumatoid arthritis. Arthritis. Res. Ther. 12, R133
17. Maciejewska-Rodrigues, H., Karouzakis, E., Strietholt, S., Hemmatazad, H., Neidhart, M., Ospelt, C., Gay, R. E., Michel, B. A., Pap, T., Gay, S., and Jüngel, A. (2010) Epigenetics and rheumatoid arthritis: the role of SENP1 in the regulation of MMP-1 expression. J. Autoimmun 35, 15-22
18. Neidhart, M., Rethage, J., Kuchen, S., Künzler, P., Crowl, R. M., Billingham, M. E., Gay, R. E., and Gay, S. (2000) Retrotransposable L1 elements expressed in rheumatoid arthritis synovial tissue: association with genomic DNA hypomethylation and influence on gene expression. Arthritis. Rheum. 43, 2634-2647
19. Strietholt, S., Maurer, B., Peters, M. A., Pap, T., and Gay, S. (2008) Epigenetic modifications in rheumatoid arthritis. Arthritis. Res. Ther. 10, 219
20. Cheung, K. S., Hashimoto, K., Yamada, N., and Roach, H. I. (2009) Expression of ADAMTS-4 by chondrocytes in the surface zone of human osteoarthritic cartilage is regulated by epigenetic DNA de-methylation. Rheumatol. Int. 29, 525-534
21. da Silva, M. A., Yamada, N., Clarke, N. M., and Roach, H. I. (2009) Cellular and epigenetic features of a young healthy and a young osteoarthritic cartilage compared with aged control and OA cartilage. J. Orthop. Res. 27, 593-601
22. Hashimoto, K., Oreffo, R. O., Gibson, M. B., Goldring, M. B., and Roach, H. I. (2009) DNA demethylation at specific CpG sites in the IL1B promoter in response to inflammatory cytokines in human articular chondrocytes. Arthritis. Rheum. 60, 3303-3313
23. Loeser, R. F., Im, H. J., Richardson, B., Lu, Q., and Chubinskaya, S. (2009) Methylation of the OP-1 promoter: potential role in the age-related decline in OP-1 expression in cartilage. Osteoarthritis Cartilage 17, 513-517
24. Reynard, L. N., Bui, C., Canty-Laird, E. G., Young, D. A., and Loughlin, J. (2011) Expression of the osteoarthritis-associated gene GDF5 is modulated epigenetically by DNA methylation. Hum. Mol. Genet. 20, 3450-3460
25. Roach, H. I., Yamada, N., Cheung, K. S., Tilley, S., Clarke, N. M., Oreffo, R. O., Kokubun, S., and Bronner, F. (2005) 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. 52, 3110-3124
26. Sesselmann, S., Söder, S., Voigt, R., Haag, J., Grogan, S. P., and Aigner, T. (2009) DNA methylation is not responsible for p21WAF1/CIP1 downregulation in osteoarthritic chondrocytes. Osteoarthritis Cartilage 17, 507-512
27. Zimmermann, P., Boeuf, S., Dickhut, A., Boehmer, S., Olek, S., and 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, 2743-2753
28. Goldring, M. B., and Marcu, K. B. (2012) Epigenomic and microRNAmediated regulation in cartilage development, homeostasis, and osteoarthritis. Trends Mol. Med. 18, 109-118
29. Barter, M. J., Bui, C., and Young, D. A. (2012) Epigenetic mechanisms in cartilage and osteoarthritis: DNA methylation, histone modifications and microRNAs. Osteoarthritis Cartilage 20, 339-349
30. Aigner, T., Sachse, A., Gebhard, P. M., and Roach, H. I. (2006) Osteoarthritis: pathobiology-targets and ways for therapeutic intervention. Adv. Drug. Deliv. Rev. 58, 128-149
31. Goldring, M. B., and Goldring, S. R. (2007) Osteoarthritis. J. Cell Physiol. 213, 626-634
32. Roach, H. I., and Aigner, T. (2007) DNA methylation in osteoarthritic chondrocytes: a new molecular target. Osteoarthritis Cartilage 15, 128-137
33. Klug, M., and Rehli, M. (2006) Functional analysis of promoter CpG methylation using a CpG-free luciferase reporter vector. Epigenetics 1, 127-130
34. Goldring, M. B., Birkhead, J. R., Suen, L. F., Yamin, R., Mizuno, S., Glowacki, J., Arbiser, J. L., and Apperley, J. F. (1994) Interleukin-1 β-modulated gene expression in immortalized human chondrocytes. J. Clin. Invest. 94, 2307-2316
35. Otero, M., Plumb, D. A., Tsuchimochi, K., Dragomir, C. L., Hashimoto, K., Peng, H., Olivotto, E., Bevilacqua, M., Tan, L., Yang, Z., Zhan, Y., Oettgen, P., Li, Y., Marcu, K. B., and Goldring, M. B. (2012) E74-like factor 3 (ELF3) impacts on matrix metalloproteinase 13 (MMP13) transcriptional control in articular chondrocytes under pro-inflammatory stress. J. Biol. Chem. 287, 3559-3572
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., and Goldring, M. B. (2005) A novel role for GADD45β as a mediator of MMP-13 gene expression during chondrocyte terminal differentiation. J. Biol. Chem. 280, 38544-38555
37. Peng, H., Tan, L., Osaki, M., Zhan, Y., Ijiri, K., Tsuchimochi, K., Otero, M., Wang, H., Choy, B. K., Grall, F. T., Gu, X., Libermann, T. A., Oettgen, P., and Goldring, M. B. (2008) ESE-1 is a potent repressor of type II collagen gene (COL2A1) transcription in human chondrocytes. J. Cell Physiol. 215, 562-573
38. Hashimoto, K., Kokubun, S., Itoi, E., and Roach, H. I. (2007) Improved quantification of DNA methylation using methylation-sensitive restriction enzymes and real-time PCR. Epigenetics 2, 86-91
39. Goldring, M. B., Otero, M., Plumb, D. A., Dragomir, C., Favero, M., El Hachem, K., Hashimoto, K., Roach, H. I., Olivotto, E., Borzì, R. M., and Marcu, K. B. (2011) Roles of inflammatory and anabolic cytokines in cartilage metabolism: signals and multiple effectors converge upon MMP-13 regulation in osteoarthritis. Eur. Cell Mater. 21, 202-220
40. Jiménez, M. J., Balbín, M., López, J. M., Alvarez, J., Komori, T., and López-Otín, C. (1999) Collagenase 3 is a target of Cbfa1, a transcription factor of the runt gene family involved in bone formation. Mol. Cell Biol. 19, 4431-4442
41. Liacini, A., Sylvester, J., Li, W. Q., and Zafarullah, M. (2002) Inhibition of interleukin-1-stimulated MAP kinases, activating protein-1 (AP-1) and nuclear factor κ B (NF-κB) transcription factors down-regulates matrix metalloproteinase gene expression in articular chondrocytes. Matrix Biol. 21, 251-262
42. Mengshol, J. A., Vincenti, M. P., and Brinckerhoff, C. E. (2001) IL-1 induces collagenase-3 (MMP-13) promoter activity in stably transfected chondrocytic cells: requirement for Runx-2 and activation by p38 MAPK and JNK pathways. Nucleic Acids Res. 29, 4361-4372
43. 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., and Kawaguchi, H. (2010) Transcriptional regulation of endochondral ossification by HIF-2α during skeletal growth and osteoarthritis development. Nat. Med. 16, 678-686
44. Yang, S., Kim, J., Ryu, J. H., Oh, H., Chun, C. H., Kim, B. J., Min, B. H., and Chun, J. S. (2010) Hypoxia-inducible factor-2β is a catabolic regulator of osteoarthritic cartilage destruction. Nat. Med. 16, 687-693
45. Mitchell, P. G., Magna, H. A., Reeves, L. M., Lopresti-Morrow, L. L., Yocum, S. A., Rosner, P. J., Geoghegan, K. F., and Hambor, J. E. (1996) Cloning, expression, and type II collagenolytic activity of matrix metalloproteinase- 13 from human osteoarthritic cartilage. J. Clin. Invest. 97, 761-768
46. Reboul, P., Pelletier, J. P., Tardif, G., Cloutier, J. M., and Martel-Pelletier, J. (1996) The new collagenase, collagenase-3, is expressed and synthesized by human chondrocytes but not by synoviocytes. A role in osteoarthritis. J. Clin. Invest. 97, 2011-2019
47. Neuhold, L. A., Killar, L., Zhao, W., Sung, M. L., Warner, L., Kulik, J., Turner, J., Wu, W., Billinghurst, C., Meijers, T., Poole, A. R., Babij, P., and DeGennaro, L. J. (2001) Postnatal expression in hyaline cartilage of constitutively active human collagenase-3 (MMP-13) induces osteoarthritis in mice. J. Clin. Invest. 107, 35-44
48. Little, C. B., Barai, A., Burkhardt, D., Smith, S. M., Fosang, A. J., Werb, Z., Shah, M., and Thompson, E. W. (2009) Matrix metalloproteinase 13-deficient mice are resistant to osteoarthritic cartilage erosion but not chondrocyte hypertrophy or osteophyte development. Arthritis Rheum. 60, 3723-3733
49. Inada, M., Wang, Y., Byrne, M. H., Rahman, M. U., Miyaura, C., López- Otín, C., and Krane, S. M. (2004) Critical roles for collagenase-3 (Mmp13) in development of growth plate cartilage and in endochondral ossification. Proc. Natl. Acad. Sci. U.S.A. 101, 17192-17197
50. Fan, Z., Tardif, G., Boileau, C., Bidwell, J. P., Geng, C., Hum, D., Watson, A., Pelletier, J. P., Lavigne, M., and Martel-Pelletier, J. (2006) Identification in human osteoarthritic chondrocytes of proteins binding to the novel regulatory site AGRE in the human matrix metalloprotease 13 proximal promoter. Arthritis Rheum. 54, 2471-2480
51. Cogswell, J. P., Godlevski, M. M., Wisely, G. B., Clay, W. C., Leesnitzer, L. M., Ways, J. P., and Gray, J. G. (1994) NF-κB regulates IL-1 β transcription through a consensus NF-κB binding site and a nonconsensus CRE-like site. J. Immunol. 153, 712-723
52. Hiscott, J., Marois, J., Garoufalis, J., D'Addario, M., Roulston, A., Kwan, I., Pepin, N., Lacoste, J., Nguyen, H., and Bensi, G. (1993) Characterization of a functional NF-κB site in the human interleukin 1 β promoter: evidence for a positive autoregulatory loop. Mol. Cell Biol. 13, 6231-6240
53. Kirillov, A., Kistler, B., Mostoslavsky, R., Cedar, H., Wirth, T., and Bergman, Y. (1996) A role for nuclear NF-κB in B-cell-specific demethylation of the Igκ locus. Nat. Genet. 13, 435-441
54. Iliopoulos, D., Malizos, K. N., and Tsezou, A. (2007) Epigenetic regulation of leptin affects MMP-13 expression in osteoarthritic chondrocytes: possible molecular target for osteoarthritis therapeutic intervention. Ann. Rheum. Dis. 66, 1616-1621
55. Pöschl, E., Fidler, A., Schmidt, B., Kallipolitou, A., Schmid, E., and Aigner, T. (2005) DNA methylation is not likely to be responsible for aggrecan down regulation in aged or osteoarthritic cartilage. Ann. Rheum. Dis. 64, 477-480
56. Eckhardt, F., Lewin, J., Cortese, R., Rakyan, V. K., Attwood, J., Burger, M., Burton, J., Cox, T. V., Davies, R., Down, T. A., Haefliger, C., Horton, R., Howe, K., Jackson, D. K., Kunde, J., Koenig, C., Liddle, J., Niblett, D., Otto, T., Pettett, R., Seemann, S., Thompson, C., West, T., Rogers, J., Olek, A., Berlin, K., and Beck, S. (2006) DNA methylation profiling of human chromosomes 6, 20 and 22. Nat. Genet. 38, 1378-1385
57. Harris, A. L. (2002) Hypoxia-a key regulatory factor in tumour growth. Nat. Rev. Cancer 2, 38-47
58. Huang, L. E., and Bunn, H. F. (2003) Hypoxia-inducible factor and its biomedical relevance. J. Biol. Chem. 278, 19575-19578
59. Pescador, N., Cuevas, Y., Naranjo, S., Alcaide, M., Villar, D., Landázuri, M. O., and Del Peso, L. (2005) Identification of a functional hypoxiaresponsive element that regulates the expression of the egl nine homologue 3 (egln3/phd3) gene. Biochem. J. 390, 189-197
60. Saito, T., and Kawaguchi, H. (2010) HIF-2α as a possible therapeutic target of osteoarthritis. Osteoarthritis Cartilage 18, 1552-1556
61. Semenza, G. L. (2000) HIF-1 and human disease: one highly involved factor. Genes Dev. 14, 1983-1991
62. Ema, M., Morita, M., Ikawa, S., Tanaka, M., Matsuda, Y., Gotoh, O., Saijoh, Y., Fujii, H., Hamada, H., Kikuchi, Y., and Fujii-Kuriyama, Y. (1996) Two new members of the murine Sim gene family are transcriptional repressors and show different expression patterns during mouse embryogenesis. Mol. Cell Biol. 16, 5865-5875
63. Moffett, P., Reece, M., and Pelletier, J. (1997) The murine Sim-2 gene product inhibits transcription by active repression and functional interference. Mol. Cell Biol. 17, 4933-4947
64. Woods, S., Farrall, A., Procko, C., and Whitelaw, M. L. (2008) The bHLH/Per-Arnt-Sim transcription factor SIM2 regulates muscle transcript myomesin2 via a novel, non-canonical E-box sequence. Nucleic Acids Res. 36, 3716-3727
65. Carvin, C. D., Parr, R. D., and Kladde, M. P. (2003) Site-selective in vivo targeting of cytosine-5 DNA methylation by zinc-finger proteins. Nucleic Acids Res. 31, 6493-6501
66. Smith, A. E., and Ford, K. G. (2007) Specific targeting of cytosine methylation to DNA sequences in vivo. Nucleic Acids Res. 35, 740-754
67. Dawson, M. A., and Kouzarides, T. (2012) Cancer epigenetics: from mechanism to therapy. Cell 150, 12-27