DNA demethylation at specific CpG sites in the IL1B promoter in response to inflammatory cytokines in human articular chondrocytes

Arthritis and Rheumatism

Volumn 60, Issue 11, 2009, Pages 3303-3313

  Hashimoto, Ko ^a   Oreffo, Richard O C ^a   Gibson, Marc B ^a   Goldring, Mary B ^b   Roach, Helmtrud I ^a  

^a UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

^b HOSPITAL FOR SPECIAL SURGERY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

5 AZA 2' DEOXYCYTIDINE; BISULFITE; COLLAGENASE 3; CYTOKINE; DNA; DNA METHYLTRANSFERASE 1; INTERLEUKIN 1BETA; MESSENGER RNA; ONCOSTATIN M; RNA; TUMOR NECROSIS FACTOR ALPHA;

ARTICLE; CARTILAGE; CARTILAGE CELL; CONTROLLED STUDY; CPG ISLAND; DEMETHYLATION; DNA EXTRACTION; DNA METHYLATION; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMUR HEAD; FEMUR NECK; GENOME; HUMAN; HUMAN CELL; HUMAN TISSUE; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA EXTRACTION;

AZACITIDINE; CARTILAGE, ARTICULAR; CELLS, CULTURED; CHONDROCYTES; CPG ISLANDS; CYTOKINES; DNA (CYTOSINE-5-)-METHYLTRANSFERASE; DNA METHYLATION; HUMANS; INTERLEUKIN-1BETA; MATRIX METALLOPROTEINASE 13; MATRIX METALLOPROTEINASE 3; ONCOSTATIN M; OSTEOARTHRITIS, HIP; PROMOTER REGIONS, GENETIC; RNA, MESSENGER; TUMOR NECROSIS FACTOR-ALPHA;

EID: 70350561846     PISSN: 00043591     EISSN: 15290131     Source Type: Journal    
DOI: 10.1002/art.24882     Document Type: Article

References (50)

1. Goldring MB, Goldring SR. Osteoarthritis. J Cell Physiol 2007;213:626-634
2. Aigner T, Sachse A, Gebhard PM, Roach HI. Osteoarthritis: pathobiology-targets and ways for therapeutic intervention. Adv Drug Deliv Rev 2006;58:128-149
3. Valdes AM, Doherty M, Spector TD. The additive effect of individual genes in predicting risk of knee osteoarthritis. Ann Rheum Dis 2008;67:124-127
4. Jaenisch R, Bird A. Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat Genet 2003;33 Suppl:245-254 (Pubitemid 36278835)
5. Bird A. DNA methylation patterns and epigenetic memory. Genes Dev 2002;16:6-21. (Pubitemid 34049633)
6. Reik W. Stability and flexibility of epigenetic gene regulation in mammalian development. Nature 2007;447:425-432 (Pubitemid 46816749)
7. Berger SL. The complex language of chromatin regulation during transcription. Nature 2007;447:407-412 (Pubitemid 46816746)
8. Attwood JT, Yung RL, Richardson BC. DNA methylation and the regulation of gene transcription. Cell Mol Life Sci 2002;59:241-257 (Pubitemid 34169512)
9. Martin C, Zhang Y. Mechanisms of epigenetic inheritance. Curr Opin Cell Biol 2007;19:266-272
10. Fujita N, Watanabe S, Ichimura T, Tsuruzoe S, Shinkai Y, Tachibana M, et al. Methyl-CpG binding domain 1 (MBD1) interacts with the Suv39h1-HP1 heterochromatic complex for DNA methylation-based transcriptional repression. J Biol Chem 2003;278:24132-24138 (Pubitemid 36830249)
11. Fuks F, Hurd PJ, Wolf D, Nan X, Bird AP, Kouzarides T. The methyl-CpG-binding protein MeCP2 links DNA methylation to histone methylation. J Biol Chem 2003;278:4035-4040 (Pubitemid 36801137)
12. Goldring MB, Berenbaum F. The regulation of chondrocyte function by proinflammatory mediators: prostaglandins and nitric oxide. Clin Orthop Relat Res 2004;S37-46. (Pubitemid 39362799)
13. Goldring SR, Goldring MB. The role of cytokines in cartilage matrix degeneration in osteoarthritis. Clin Orthop Relat Res 2004;S27-36.
14. Aida Y, Maeno M, Suzuki N, Namba A, Motohashi M, Matsumoto M, et al. The effect of IL-1β on the expression of inflammatory cytokines and their receptors in human chondrocytes. Life Sci 2006;79:764-771 (Pubitemid 43975126)
15. Sato T, Konomi K, Yamasaki S, Aratani S, Tsuchimochi K, Yokouchi M, et al. Comparative analysis of gene expression profiles in intact and damaged regions of human osteoarthritic cartilage. Arthritis Rheum 2006;54:808-817
16. Aigner T, Fundel K, Saas J, Gebhard PM, Haag J, Weiss T, et al. Large-scale gene expression profiling reveals major pathogenetic pathways of cartilage degeneration in osteoarthritis. Arthritis Rheum 2006;54:3533-3544 (Pubitemid 44737165)
17. Roach HI, Tilley S. The pathogenesis of osteoarthritis. In: Bronner F and Farach-Carson MC editors. Bone and osteoarthritis. Topics in bone biology. Vol.4. New York: Springer; 2007; p. 1-18.
18. Feinberg AP. Phenotypic plasticity and the epigenetics of human disease. Nature 2007;447:433-440 (Pubitemid 46816750)
19. Roach HI, Yamada N, Cheung KS, Tilley S, Clarke NM, Oreffo RO, et al. 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;52:3110-3124 (Pubitemid 41447092)
20. Cheung KS, Hashimoto K, Yamada N, Roach HI. Expression of ADAMTS-4 by chondrocytes in the surface zone of human osteoarthritic cartilage is regulated by epigenetic DNA demethylation. Rheumatol Int 2009;29:525-534
21. Iliopoulos D, Malizos KN, Tsezou A. Epigenetic regulation of leptin affects MMP-13 expression in osteoarthritic chondrocytes: possible molecular target for osteoarthritis therapeutic intervention. Ann Rheum Dis 2007;66:1616-1621 (Pubitemid 350205450)
22. Loeser RF, Im HJ, Richardson B, Lu Q, Chubinskaya S. Methylation of the OP-1 promoter: potential role in the age-related decline in OP-1 expression in cartilage. Osteoarthritis Cartilage 2009;17:513-517
23. Saas J, Haag J, Rueger D, Chubinskaya S, Sohler F, Zimmer R, et al. IL-1β, but not BMP-7, leads to a dramatic change in the gene expression pattern of human adult articular chondrocytes - portraying the gene expression pattern in two donors. Cytokine 2006;36:90-99 (Pubitemid 46049017)
24. Barksby HE, Hui W, Wappler I, Peters HH, Milner JM, Richards CD, et al. Interleukin-1 in combination with oncostatin M upregulates multiple genes in chondrocytes: implications for cartilage destruction and repair. Arthritis Rheum 2006;54:540-550 (Pubitemid 43228630)
25. 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;27:593-601.
26. Haaf T. The effects of 5-azacytidine and 5-azadeoxycytidine on chromosome structure and function: implications for methylation-associated cellular processes. Pharmacol Ther 1995;65:19-46. (Pubitemid 24381835)
27. Hashimoto K, Kokubun S, Itoi E, Roach HI. Improved quantification of DNA methylation using methylation-sensitive restriction enzymes and real-time PCR. Epigenetics 2007;2:86-91. (Pubitemid 351682001)
28. Preradovic A, Kleinpeter G, Feichtinger H, Balaun E, Krugluger W. Quantitation of collagen I, collagen II and aggrecan mRNA and expression of the corresponding proteins in human nucleus pulposus cells in monolayer cultures. Cell Tissue Res 2005;321:459-464 (Pubitemid 41206998)
29. Toda Y, Tsukada J, Misago M, Kominato Y, Auron PE, Tanaka Y, et al. Autocrine induction of the human pro-IL-1β gene promoter by IL-1β in monocytes. J Immunol 2002;168:1984-1991 (Pubitemid 34135802)
30. Zhang Y, Saccani S, Shin H, Nikolajczyk BS. Dynamic protein associations define two phases of IL-1β transcriptional activation. J Immunol 2008;181:503-512
31. Shirakawa F, Saito K, Bonagura CA, Galson DL, Fenton MJ, Webb AC, et al. The human prointerleukin 1β gene requires DNA sequences both proximal and distal to the transcription start site for tissue-specific induction. Mol Cell Biol 1993;13:1332-1344 (Pubitemid 23068068)
32. Bensi G, Mora M, Raugei G, Buonamassa DT, Rossini M, Melli M. An inducible enhancer controls the expression of the human interleukin 1β gene. Cell Growth Differ 1990;1:491-497
33. Kominato Y, Galson D, Waterman WR, Webb AC, Auron PE. Monocyte expression of the human prointerleukin 1β gene (IL1B) is dependent on promoter sequences which bind the hematopoietic transcription factor Spi-1/PU.1. Mol Cell Biol 1995;15:58-68. (Pubitemid 24379901)
34. Liacini A, Sylvester J, Li WQ, Huang W, Dehnade F, Ahmad M, et al. Induction of matrix metalloproteinase-13 gene expression by TNF-α is mediated by MAP kinases, AP-1, and NF-κB transcription factors in articular chondrocytes. Exp Cell Res 2003;288:208-217
35. Granet C, Maslinski W, Miossec P. Increased AP-1 and NF-κB activation and recruitment with the combination of the proinflammatory cytokines IL-1β, tumor necrosis factor α and IL-17 in rheumatoid synoviocytes. Arthritis Res Ther 2004;6:R190-8.
36. Griffin BD, Moynagh PN. Persistent interleukin-1β signaling causes long term activation of NFκB in a promoter-specific manner in human glial cells. J Biol Chem 2006;281:10316-10326
37. Mercurio F, Manning AM. Multiple signals converging on NF-κB. Curr Opin Cell Biol 1999;11:226-232
38. Kirillov A, Kistler B, Mostoslavsky R, Cedar H, Wirth T, Bergman Y. A role for nuclear NF-κB in B-cell-specific demethylation of the Ig κ locus. Nat Genet 1996;13:435-441 (Pubitemid 26256617)
39. Yan Y, Dalmasso G, Nguyen HT, Obertone TS, Charrier-Hisamuddin L, Sitaraman SV, et al. Nuclear factor-κB is a critical mediator of Ste20-like proline-/alanine-rich kinase regulation in intestinal inflammation. Am J Pathol 2008;173:1013-1028
40. Buryskova M, Pospisek M, Grothey A, Simmet T, Burysek L. Intracellular interleukin-1α functionally interacts with histone acetyltransferase complexes. J Biol Chem 2004;279:4017-4026 (Pubitemid 38198984)
41. Rowan AD, Hui W, Cawston TE, Richards CD. Adenoviral gene transfer of interleukin-1 in combination with oncostatin M induces significant joint damage in a murine model. Am J Pathol 2003;162:1975-1984 (Pubitemid 36613054)
42. El Mabrouk M, Sylvester J, Zafarullah M. Signaling pathways implicated in oncostatin M-induced aggrecanase-1 and matrix metalloproteinase-13 expression in human articular chondrocytes. Biochim Biophys Acta 2007;1773:309-320 (Pubitemid 46298770)
43. Hui W, Rowan AD, Richards CD, Cawston TE. Oncostatin M in combination with tumor necrosis factor α induces cartilage damage and matrix metalloproteinase expression in vitro and in vivo. Arthritis Rheum 2003;48:3404-3418 (Pubitemid 37531907)
44. Moos V, Fickert S, Muller B, Weber U, Sieper J. Immunohistological analysis of cytokine expression in human osteoarthritic and healthy cartilage. J Rheumatol 1999;26:870-879 (Pubitemid 29195675)
45. Tetlow LC, Adlam DJ, Woolley DE. Matrix metalloproteinase and proinflammatory cytokine production by chondrocytes of human osteoarthritic cartilage: associations with degenerative changes. Arthritis Rheum 2001;44:585-594
46. Fan Z, Soder S, Oehler S, Fundel K, Aigner T. Activation of interleukin-1 signaling cascades in normal and osteoarthritic articular cartilage. Am J Pathol 2007;171:938-946 (Pubitemid 47440992)
47. Clements KM, Price JS, Chambers MG, Visco DM, Poole AR, Mason RM. Gene deletion of either interleukin-1β, interleukin-1β-converting enzyme, inducible nitric oxide synthase, or stromelysin 1 accelerates the development of knee osteoarthritis in mice after surgical transection of the medial collateral ligament and partial medial meniscectomy. Arthritis Rheum 2003;48:3452-3463
48. Glasson SS. In vivo osteoarthritis target validation utilizing genetically-modified mice. Curr Drug Targets 2007;8:367-376
49. Butler DM, Malfait AM, Mason LJ, Warden PJ, Kollias G, Maini RN, et al. DBA/1 mice expressing the human TNF-a transgene develop a severe, erosive arthritis: characterization of the cytokine cascade and cellular composition. J Immunol 1997;159:2867-2876 (Pubitemid 127681309)
50. Goldring MB, Otero M, Tsuchimochi K, Ijiri K, Li Y. Defining the roles of inflammatory and anabolic cytokines in cartilage metabolism. Ann Rheum Dis 2008;67 Suppl 3:iii75-82.