DOI QR코드

DOI QR Code

Epigenetic Regulation of Chondrocyte Catabolism and Anabolism in Osteoarthritis

  • Kim, Hyeonkyeong (Department of Biological Sciences, Seoul National University) ;
  • Kang, Donghyun (Department of Biological Sciences, Seoul National University) ;
  • Cho, Yongsik (Department of Biological Sciences, Seoul National University) ;
  • Kim, Jin-Hong (Department of Biological Sciences, Seoul National University)
  • 투고 : 2015.07.15
  • 심사 : 2015.07.18
  • 발행 : 2015.08.31

초록

Osteoarthritis (OA) is one of the most prevalent forms of joint disorder, associated with a tremendous socioeconomic burden worldwide. Various non-genetic and lifestyle-related factors such as aging and obesity have been recognized as major risk factors for OA, underscoring the potential role for epigenetic regulation in the pathogenesis of the disease. OA-associated epigenetic aberrations have been noted at the level of DNA methylation and histone modification in chondrocytes. These epigenetic regulations are implicated in driving an imbalance between the expression of catabolic and anabolic factors, leading eventually to osteoarthritic cartilage destruction. Cellular senescence and metabolic abnormalities driven by OA-associated risk factors appear to accompany epigenetic drifts in chondrocytes. Notably, molecular events associated with metabolic disorders influence epigenetic regulation in chondrocytes, supporting the notion that OA is a metabolic disease. Here, we review accumulating evidence supporting a role for epigenetics in the regulation of cartilage homeostasis and OA pathogenesis.

키워드

참고문헌

  1. Blander, G., and Guarente, L. (2004). The Sir2 family of protein deacetylases. Ann. Rev. Biochem. 73, 417-435. https://doi.org/10.1146/annurev.biochem.73.011303.073651
  2. Bordone, L., Motta, M.C., Picard, F., Robinson, A., Jhala, U.S., Apfeld, J., McDonagh, T., Lemieux, M., McBurney, M., Szilvasi, A., et al. (2006). Sirt1 regulates insulin secretion by repressing UCP2 in pancreatic beta cells. PLoS Biol. 4, e31.
  3. Buckwalter, J.A., and Brown, T.D. (2004). Joint injury, repair, and remodeling: roles in post-traumatic osteoarthritis. Clin. Orthop. Relat. Res. 2004, 7-16.
  4. 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 elementbinding (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. https://doi.org/10.1096/fj.12-206367
  5. Cai, L., and Tu, B.P. (2011). On acetyl-CoA as a gauge of cellular metabolic state. Cold Spring Harb. Symp. Quant. Biol. 76, 195-202.
  6. Caito, S., Rajendrasozhan, S., Cook, S., Chung, S., Yao, H., Friedman, A.E., Brookes, P.S., and Rahman, I. (2010). SIRT1 is a redox-sensitive deacetylase that is post-translationally modified by oxidants and carbonyl stress. FASEB J. 24, 3145-3159. https://doi.org/10.1096/fj.09-151308
  7. Campion, J., Milagro, F.I., and Martinez, J.A. (2009). Individuality and epigenetics in obesity. Obesity Rev. 10, 383-392. https://doi.org/10.1111/j.1467-789X.2009.00595.x
  8. Carlo, M.D., Jr., and Loeser, R.F. (2003). Increased oxidative stress with aging reduces chondrocyte survival: correlation with intracellular glutathione levels. Arthritis. Rheum. 48, 3419-3430. https://doi.org/10.1002/art.11338
  9. Carman, W.J., Sowers, M., Hawthorne, V.M., and Weissfeld, L.A. (1994). Obesity as a risk factor for osteoarthritis of the hand and wrist: a prospective study. Am. J. Epidemiol. 139, 119-129.
  10. Chabane, N., Zayed, N., Afif, H., Mfuna-Endam, L., Benderdour, M., Boileau, C., Martel-Pelletier, J., Pelletier, J.P., Duval, N., and Fahmi, H. (2008). Histone deacetylase inhibitors suppress interleukin-1beta-induced nitric oxide and prostaglandin E2 production in human chondrocytes. Osteoarthritis Cartilage 16, 1267-1274. https://doi.org/10.1016/j.joca.2008.03.009
  11. Chatterjee, T.K., Idelman, G., Blanco, V., Blomkalns, A.L., Piegore, M.G., Jr., Weintraub, D.S., Kumar, S., Rajsheker, S., Manka, D., Rudich, S.M., et al. (2011). Histone deacetylase 9 is a negative regulator of adipogenic differentiation. J. Biol. Chem. 286, 27836-27847. https://doi.org/10.1074/jbc.M111.262964
  12. Chen, T.H., Chen, L., Hsieh, M.S., Chang, C.P., Chou, D.T., and Tsai, S.H. (2006). Evidence for a protective role for adiponectin in osteoarthritis. Biochim. Biophys. Acta 1762, 711-718. https://doi.org/10.1016/j.bbadis.2006.06.008
  13. Chen, R., Dioum, E.M., Hogg, R.T., Gerard, R.D., and Garcia, J.A. (2011). Hypoxia increases sirtuin 1 expression in a hypoxiainducible factor-dependent manner. J. Biol. Chem. 286, 13869-13878. https://doi.org/10.1074/jbc.M110.175414
  14. Conaghan, P.G., Vanharanta, H., and Dieppe, P.A. (2005). Is progressive osteoarthritis an atheromatous vascular disease? Ann. Rheum. Dis. 64, 1539-1541. https://doi.org/10.1136/ard.2005.039263
  15. de Kreutzenberg, S.V., Ceolotto, G., Papparella, I., Bortoluzzi, A., Semplicini, A., Dalla Man, C., Cobelli, C., Fadini, G.P., and Avogaro, A. (2010). Downregulation of the longevity-associated protein sirtuin 1 in insulin resistance and metabolic syndrome: potential biochemical mechanisms. Diabetes 59, 1006-1015. https://doi.org/10.2337/db09-1187
  16. de Ruijter, A.J., van Gennip, A.H., Caron, H.N., Kemp, S., and van Kuilenburg, A.B. (2003). Histone deacetylases (HDACs): characterization of the classical HDAC family. Biochem. J. 370, 737-749. https://doi.org/10.1042/bj20021321
  17. Dillon, C.F., Rasch, E.K., Gu, Q., and Hirsch, R. (2006). Prevalence of knee osteoarthritis in the United States: arthritis data from the Third National Health and Nutrition Examination Survey 1991-94. J. Rheumatol. 33, 2271-2279.
  18. Duan, Y., Hao, D., Li, M., Wu, Z., Li, D., Yang, X., and Qiu, G. (2012). Increased synovial fluid visfatin is positively linked to cartilage degradation biomarkers in osteoarthritis. Rheumatol. Int. 32, 985-990. https://doi.org/10.1007/s00296-010-1731-8
  19. Dumond, H., Presle, N., Terlain, B., Mainard, D., Loeuille, D., Netter, P., and Pottie, P. (2003). Evidence for a key role of leptin in osteoarthritis. Arthritis Rheum. 48, 3118-3129. https://doi.org/10.1002/art.11303
  20. Dvir-Ginzberg, M., Gagarina, V., Lee, E.J., and Hall, D.J. (2008). Regulation of cartilage-specific gene expression in human chondrocytes by SirT1 and nicotinamide phosphoribosyltransferase. J. Biol. Chem. 283, 36300-36310. https://doi.org/10.1074/jbc.M803196200
  21. Dvir-Ginzberg, M., Gagarina, V., Lee, E.J., Booth, R., Gabay, O., and Hall, D.J. (2011). Tumor necrosis factor alpha-mediated cleavage and inactivation of SirT1 in human osteoarthritic chondrocytes. Arthritis Rheum. 63, 2363-2373. https://doi.org/10.1002/art.30279
  22. Fernandez-Tajes, J., Soto-Hermida, A., Vazquez-Mosquera, M.E., Cortes-Pereira, E., Mosquera, A., Fernandez-Moreno, M., Oreiro, N., Fernandez-Lopez, C., Fernandez, J.L., Rego-Perez, I., et al. (2014). Genome-wide DNA methylation analysis of articular chondrocytes reveals a cluster of osteoarthritic patients. Ann. Rheum. Dis. 73, 668-677. https://doi.org/10.1136/annrheumdis-2012-202783
  23. Findlay, D.M. (2007). Vascular pathology and osteoarthritis. Rheumatology 46, 1763-1768. https://doi.org/10.1093/rheumatology/kem191
  24. Fujita, N., Matsushita, T., Ishida, K., Kubo, S., Matsumoto, T., Takayama, K., Kurosaka, M., and Kuroda, R. (2011). Potential involvement of SIRT1 in the pathogenesis of osteoarthritis through the modulation of chondrocyte gene expressions. J. Orthop. Res. 29, 511-515. https://doi.org/10.1002/jor.21284
  25. Furumatsu, T., and Asahara, H. (2010). Histone acetylation influences the activity of Sox9-related transcriptional complex. Acta Med. Okayama 64, 351-357.
  26. Furumatsu, T., Tsuda, M., Yoshida, K., Taniguchi, N., Ito, T., Hashimoto, M., Ito, T., and Asahara, H. (2005). Sox9 and p300 cooperatively regulate chromatin-mediated transcription. J. Biol. Chem. 280, 35203-35208. https://doi.org/10.1074/jbc.M502409200
  27. Gabay, O., Oppenhiemer, H., Meir, H., Zaal, K., Sanchez, C., and Dvir-Ginzberg, M. (2012). Increased apoptotic chondrocytes in articular cartilage from adult heterozygous SirT1 mice. Ann. Rheum. Dis. 71, 613-616. https://doi.org/10.1136/ard.2011.200504
  28. Gabay, O., Sanchez, C., Dvir-Ginzberg, M., Gagarina, V., Zaal, K.J., Song, Y., He, X.H., and McBurney, M.W. (2013). Sirtuin 1 enzymatic activity is required for cartilage homeostasis in vivo in a mouse model. Arthritis Rheum. 65, 159-166. https://doi.org/10.1002/art.37750
  29. Gagarina, V., Gabay, O., Dvir-Ginzberg, M., Lee, E.J., Brady, J.K., Quon, M.J., and Hall, D.J. (2010). SirT1 enhances survival of human osteoarthritic chondrocytes by repressing protein tyrosine phosphatase 1B and activating the insulin-like growth factor receptor pathway. Arthritis Rheum. 62, 1383-1392. https://doi.org/10.1002/art.27369
  30. Gosset, M., Berenbaum, F., Salvat, C., Sautet, A., Pigenet, A., Tahiri, K., and Jacques, C. (2008). Crucial role of visfatin/pre-B cell colony-enhancing factor in matrix degradation and prostaglandin E2 synthesis in chondrocytes: possible influence on osteoarthritis. Arthritis Rheum. 58, 1399-1409. https://doi.org/10.1002/art.23431
  31. Griffin, T.M., and Guilak, F. (2005). The role of mechanical loading in the onset and progression of osteoarthritis. Exerc. Sport Sci. Rev. 33, 195-200. https://doi.org/10.1097/00003677-200510000-00008
  32. Griffin, T.M., Huebner, J.L., Kraus, V.B., and Guilak, F. (2009). Extreme obesity due to impaired leptin signaling in mice does not cause knee osteoarthritis. Arthritis Rheum. 60, 2935-2944. https://doi.org/10.1002/art.24854
  33. Guilak, F. (2011). Biomechanical factors in osteoarthritis. Best practice & research. Clin. Rheumatol. 25, 815-823.
  34. Haberland, M., Carrer, M., Mokalled, M.H., Montgomery, R.L., and Olson, E.N. (2010). Redundant control of adipogenesis by histone deacetylases 1 and 2. J. Biol. Chem. 285, 14663-14670. https://doi.org/10.1074/jbc.M109.081679
  35. Hart, D.J., Doyle, D.V., and Spector, T.D. (1995). Association between metabolic factors and knee osteoarthritis in women: the Chingford Study. J. Rheumatol. 22, 1118-1123.
  36. 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. https://doi.org/10.1002/art.24882
  37. Hashimoto, K., Otero, M., Imagawa, K., de Andres, M.C., Coico, J.M., Roach, H.I., Oreffo, R.O., Marcu, K.B., and Goldring, M.B. (2013). 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. 288, 10061-10072. https://doi.org/10.1074/jbc.M112.421156
  38. Hatzivassiliou, G., Zhao, F., Bauer, D.E., Andreadis, C., Shaw, A.N., Dhanak, D., Hingorani, S.R., Tuveson, D.A., and Thompson, C.B. (2005). ATP citrate lyase inhibition can suppress tumor cell growth. Cancer Cell 8, 311-321. https://doi.org/10.1016/j.ccr.2005.09.008
  39. Heinegard, D., and Saxne, T. (2011). The role of the cartilage matrix in osteoarthritis. Nat. Rev. Rheumatol. 7, 50-56. https://doi.org/10.1038/nrrheum.2010.198
  40. Higashiyama, R., Miyaki, S., Yamashita, S., Yoshitaka, T., Lindman, G., Ito, Y., Sasho, T., Takahashi, K., Lotz, M., and Asahara, H. (2010). Correlation between MMP-13 and HDAC7 expression in human knee osteoarthritis. Mod. Rheumatol. 20, 11-17. https://doi.org/10.3109/s10165-009-0224-7
  41. Hong, S., Derfoul, A., Pereira-Mouries, L., and Hall, D.J. (2009). A novel domain in histone deacetylase 1 and 2 mediates repression of cartilage-specific genes in human chondrocytes. FASEB J. 23, 3539-3552. https://doi.org/10.1096/fj.09-133215
  42. Hong, E.H., Yun, H.S., Kim, J., Um, H.D., Lee, K.H., Kang, C.M., Lee, S.J., Chun, J.S., and Hwang, S.G. (2011). Nicotinamide phosphoribosyltransferase is essential for interleukin-1betamediated dedifferentiation of articular chondrocytes via SIRT1 and extracellular signal-regulated kinase (ERK) complex signaling. J. Biol. Chem. 286, 28619-28631. https://doi.org/10.1074/jbc.M111.219832
  43. Honsawek, S., and Chayanupatkul, M. (2010). Correlation of plasma and synovial fluid adiponectin with knee osteoarthritis severity. Arch. Med. Res. 41, 593-598. https://doi.org/10.1016/j.arcmed.2010.11.007
  44. Houard, X., Goldring, M.B., and Berenbaum, F. (2013). Homeostatic mechanisms in articular cartilage and role of inflammation in osteoarthritis. Curr. Rheumatol. Rep. 15, 375. https://doi.org/10.1007/s11926-013-0375-6
  45. Huh, Y.H., Ryu, J.H., and Chun, J.S. (2007). Regulation of type II collagen expression by histone deacetylase in articular chondrocytes. J. Biol. Chem. 282, 17123-17131. https://doi.org/10.1074/jbc.M700599200
  46. 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. Rheumatic Dis. 66, 1616-1621. https://doi.org/10.1136/ard.2007.069377
  47. Imagawa, K., de Andres, M.C., Hashimoto, K., Itoi, E., Otero, M., Roach, H.I., Goldring, M.B., and Oreffo, R.O. (2014). Association of reduced type IX collagen gene expression in human osteoarthritic chondrocytes with epigenetic silencing by DNA hypermethylation. Arthritis Rheumatol. 66, 3040-3051. https://doi.org/10.1002/art.38774
  48. Isabella Dalle - Donne, G.A., Marina Carini, Roberto Colombo, Ranieri Rossi, Aldo Milzani (2006). Protein carbonylation, cellular dysfunction, and disease progre. J. Cell. Mol. Med. 10, 389-406. https://doi.org/10.1111/j.1582-4934.2006.tb00407.x
  49. Iyer, A., Fairlie, D.P., and Brown, L. (2012). Lysine acetylation in obesity, diabetes and metabolic disease. Immunol. Cell Biol. 90, 39-46. https://doi.org/10.1038/icb.2011.99
  50. Jallali, N., Ridha, H., Thrasivoulou, C., Underwood, C., Butler, P.E., and Cowen, T. (2005). Vulnerability to ROS-induced cell death in ageing articular cartilage: the role of antioxidant enzyme activity. Osteoarthritis Cartilage 13, 614-622. https://doi.org/10.1016/j.joca.2005.02.011
  51. Kaelin, W.G., Jr., and McKnight, S.L. (2013). Influence of metabolism on epigenetics and disease. Cell 153, 56-69. https://doi.org/10.1016/j.cell.2013.03.004
  52. Kang, E.H., Lee, Y.J., Kim, T.K., Chang, C.B., Chung, J.H., Shin, K., Lee, E.Y., Lee, E.B., and Song, Y.W. (2010). Adiponectin is a potential catabolic mediator in osteoarthritis cartilage. Arthritis Res. Ther. 12, R231. https://doi.org/10.1186/ar3218
  53. Kim, K.I., Park, Y.S., and Im, G.I. (2013). Changes in the epigenetic status of the SOX-9 promoter in human osteoarthritic cartilage. J. Bone Miner. Res. 28, 1050-1060. https://doi.org/10.1002/jbmr.1843
  54. Kim, J.H., Jeon, J., Shin, M., Won, Y., Lee, M., Kwak, J.S., Lee, G., Rhee, J., Ryu, J.H., Chun, C.H., et al. (2014). Regulation of the catabolic cascade in osteoarthritis by the zinc-ZIP8-MTF1 axis. Cell 156, 730-743. https://doi.org/10.1016/j.cell.2014.01.007
  55. Kim, A.Y., Park, Y.J., Pan, X., Shin, K.C., Kwak, S.H., Bassas, A.F., Sallam, R.M., Park, K.S., Alfadda, A.A., Xu, A., et al. (2015). Obesity-induced DNA hypermethylation of the adiponectin gene mediates insulin resistance. Nat. Commun. 6, 7585. https://doi.org/10.1038/ncomms8585
  56. Knudson, C.B., and Knudson, W. (2001). Cartilage proteoglycans. Semin. Cell Dev. Biol. 12, 69-78.
  57. Kornaat, P.R., Sharma, R., van der Geest, R.J., Lamb, H.J., Kloppenburg, M., Hellio le Graverand, M.P., Bloem, J.L., and Watt, I. (2009). Positive association between increased popliteal artery vessel wall thickness and generalized osteoarthritis: is OA also part of the metabolic syndrome? Skeletal Radiol. 38, 1147-1151. https://doi.org/10.1007/s00256-009-0741-7
  58. Koskinen, A., Juslin, S., Nieminen, R., Moilanen, T., Vuolteenaho, K., and Moilanen, E. (2011). Adiponectin associates with markers of cartilage degradation in osteoarthritis and induces production of proinflammatory and catabolic factors through mitogen-activated protein kinase pathways. Arthritis Res. Ther. 13, R184. https://doi.org/10.1186/ar3512
  59. Kouzarides, T. (2007). Chromatin modifications and their function. Cell 128, 693-705. https://doi.org/10.1016/j.cell.2007.02.005
  60. Ku, J.H., Lee, C.K., Joo, B.S., An, B.M., Choi, S.H., Wang, T.H., and Cho, H.L. (2009). Correlation of synovial fluid leptin concentrations with the severity of osteoarthritis. Clin. Rheumatol. 28, 1431-1435. https://doi.org/10.1007/s10067-009-1242-8
  61. Lago, R., Gomez, R., Otero, M., Lago, F., Gallego, R., Dieguez, C., Gomez-Reino, J.J., and Gualillo, O. (2008). A new player in cartilage homeostasis: adiponectin induces nitric oxide synthase type II and pro-inflammatory cytokines in chondrocytes. Osteoarthritis Cartilage 16, 1101-1109. https://doi.org/10.1016/j.joca.2007.12.008
  62. Lawrence, R.C., Felson, D.T., Helmick, C.G., Arnold, L.M., Choi, H., Deyo, R.A., Gabriel, S., Hirsch, R., Hochberg, M.C., Hunder, G.G., et al. (2008). Estimates of the prevalence of arthritis and other rheumatic conditions in the United States. Part II. Arthritis Rheum. 58, 26-35. https://doi.org/10.1002/art.23176
  63. Lefebvre, V., Li, P., and de Crombrugghe, B. (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. https://doi.org/10.1093/emboj/17.19.5718
  64. Ling, C., and Groop, L. (2009). Epigenetics: a molecular link between environmental factors and type 2 diabetes. Diabetes 58, 2718-2725. https://doi.org/10.2337/db09-1003
  65. Liu, Y., Dentin, R., Chen, D., Hedrick, S., Ravnskjaer, K., Schenk, S., Milne, J., Meyers, D.J., Cole, P., Yates, J., 3rd, et al. (2008). A fasting inducible switch modulates gluconeogenesis via activator/coactivator exchange. Nature 456, 269-273. https://doi.org/10.1038/nature07349
  66. Loeser, R.F. (2013). Aging processes and the development of osteoarthritis. Curr. Opin. Rheumatol. 25, 108-113. https://doi.org/10.1097/BOR.0b013e32835a9428
  67. Maly, M.R., Costigan, P.A., and Olney, S.J. (2005). Contribution of psychosocial and mechanical variables to physical performance measures in knee osteoarthritis. Phys. Ther. 85, 1318-1328.
  68. Marwick, J.A., Kirkham, P.A., Stevenson, C.S., Danahay, H., Giddings, J., Butler, K., Donaldson, K., Macnee, W., and Rahman, I. (2004). Cigarette smoke alters chromatin remodeling and induces proinflammatory genes in rat lungs. Am. J. Respir. Cell Mol. Biol. 31, 633-642. https://doi.org/10.1165/rcmb.2004-0006OC
  69. Matsuzaki, T., Matsushita, T., Takayama, K., Matsumoto, T., Nishida, K., Kuroda, R., and Kurosaka, M. (2014). Disruption of Sirt1 in chondrocytes causes accelerated progression of osteoarthritis under mechanical stress and during ageing in mice. Ann. Rheumatic Dis. 73, 1397-1404. https://doi.org/10.1136/annrheumdis-2012-202620
  70. Metallo, C.M., and Vander Heiden, M.G. (2010). Metabolism strikes back: metabolic flux regulates cell signaling. Genes Dev. 24, 2717-2722. https://doi.org/10.1101/gad.2010510
  71. Morano, A., Angrisano, T., Russo, G., Landi, R., Pezone, A., Bartollino, S., Zuchegna, C., Babbio, F., Bonapace, I.M., Allen, B., et al. (2014). Targeted DNA methylation by homologydirected repair in mammalian cells. Transcription reshapes methylation on the repaired gene. Nucleic Acids Res. 42, 804-821. https://doi.org/10.1093/nar/gkt920
  72. Mundermann, A., Dyrby, C.O., and Andriacchi, T.P. (2005). Secondary gait changes in patients with medial compartment knee osteoarthritis: increased load at the ankle, knee, and hip during walking. Arthritis Rheum. 52, 2835-2844. https://doi.org/10.1002/art.21262
  73. Nagai, K., Matsushita, T., Matsuzaki, T., Takayama, K., Matsumoto, T., Kuroda, R., and Kurosaka, M. (2015). Depletion of SIRT6 causes cellular senescence, DNA damage, and telomere dysfunction in human chondrocytes. Osteoarthritis Cartilage 23, 1412-1420. https://doi.org/10.1016/j.joca.2015.03.024
  74. Nasu, Y., Nishida, K., Miyazawa, S., Komiyama, T., Kadota, Y., Abe, N., Yoshida, A., Hirohata, S., Ohtsuka, A., and Ozaki, T. (2008). Trichostatin A, a histone deacetylase inhibitor, suppresses synovial inflammation and subsequent cartilage destruction in a collagen antibody-induced arthritis mouse model. Osteoarthritis Cartilage 16, 723-732. https://doi.org/10.1016/j.joca.2007.10.014
  75. Nishikawa, K., Iwamoto, Y., Kobayashi, Y., Katsuoka, F., Kawaguchi, S., Tsujita, T., Nakamura, T., Kato, S., Yamamoto, M., Takayanagi, H., et al. (2015). DNA methyltransferase 3a regulates osteoclast differentiation by coupling to an Sadenosylmethionine-producing metabolic pathway. Nat. Med. 21, 281-287. https://doi.org/10.1038/nm.3774
  76. Oliveria, S.A., Felson, D.T., Cirillo, P.A., Reed, J.I., and Walker, A.M. (1999). Body weight, body mass index, and incident symptomatic osteoarthritis of the hand, hip, and knee. Epidemiology 10, 161-166. https://doi.org/10.1097/00001648-199903000-00013
  77. Oppenheimer, H., Gabay, O., Meir, H., Haze, A., Kandel, L., Liebergall, M., Gagarina, V., Lee, E.J., and Dvir-Ginzberg, M. (2012). 75-kd sirtuin 1 blocks tumor necrosis factor alphamediated apoptosis in human osteoarthritic chondrocytes. Arthritis Rheum. 64, 718-728. https://doi.org/10.1002/art.33407
  78. Oppenheimer, H., Kumar, A., Meir, H., Schwartz, I., Zini, A., Haze, A., Kandel, L., Mattan, Y., Liebergall, M., and Dvir-Ginzberg, M. (2014). Set7/9 impacts COL2A1 expression through binding and repression of SirT1 histone deacetylation. J. Bone Miner. Res. 29, 348-360. https://doi.org/10.1002/jbmr.2052
  79. Osoata, G.O., Yamamura, S., Ito, M., Vuppusetty, C., Adcock, I.M., Barnes, P.J., and Ito, K. (2009). Nitration of distinct tyrosine residues causes inactivation of histone deacetylase 2. Biochem. Biophys. Res. Commun. 384, 366-371. https://doi.org/10.1016/j.bbrc.2009.04.128
  80. Otero, M., Lago, R., Lago, F., Reino, J.J., and Gualillo, O. (2005). Signalling pathway involved in nitric oxide synthase type II activation in chondrocytes: synergistic effect of leptin with interleukin-1. Arthritis Res. Ther. 7, R581-591. https://doi.org/10.1186/ar1708
  81. Picard, F., Kurtev, M., Chung, N., Topark-Ngarm, A., Senawong, T., Machado De Oliveira, R., Leid, M., McBurney, M.W., and Guarente, L. (2004). Sirt1 promotes fat mobilization in white adipocytes by repressing PPAR-gamma. Nature 429, 771-776. https://doi.org/10.1038/nature02583
  82. Poschl, 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. Rheumatic Dis. 64, 477-480.
  83. Pradhan, S., and Esteve, P.-O. (2003). Mammalian DNA (cytosine-5) methyltransferases and their expression. Clin. Immunol. 109, 6-16. https://doi.org/10.1016/S1521-6616(03)00204-3
  84. Puenpatom, R.A., and Victor, T.W. (2009). Increased prevalence of metabolic syndrome in individuals with osteoarthritis: an analysis of NHANES III data. Postgrad. Med. 121, 9-20. https://doi.org/10.3810/pgm.2009.11.2073
  85. Razin, A. (1998). CpG methylation, chromatin structure and gene silencing-a three-way connection. EMBO J. 17, 4905-4908. https://doi.org/10.1093/emboj/17.17.4905
  86. 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. https://doi.org/10.1093/hmg/ddr253
  87. 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. https://doi.org/10.1002/art.21300
  88. Rodova, M., Lu, Q., Li, Y., Woodbury, B.G., Crist, J.D., Gardner, B.M., Yost, J.G., Zhong, X.B., Anderson, H.C., and Wang, J. (2011). Nfat1 regulates adult articular chondrocyte function through its age-dependent expression mediated by epigenetic histone methylation. J. Bone Miner. Res. 26, 1974-1986. https://doi.org/10.1002/jbmr.397
  89. Ruiz-Romero, C., Calamia, V., Mateos, J.s., Carreira, V., Martínez-Gomariz, M., Fernández, M.F., and Blanco, F.J. (2009). Mitochondrial dysregulation of osteoarthritic human articular chondrocytes analyzed by proteomics a decrease in mitochondrial superoxide dismutase points to a redox imbalance. Mol. Cell. Proteomics 8, 172-189. https://doi.org/10.1074/mcp.M800292-MCP200
  90. Saito, T., Fukai, A., Mabuchi, A., Ikeda, T., Yano, F., Ohba, S., Nishida, N., Akune, T., Yoshimura, N., Nakagawa, T., et al. (2010). Transcriptional regulation of endochondral ossification by HIF-2alpha during skeletal growth and osteoarthritis development. Nat. Med. 16, 678-686. https://doi.org/10.1038/nm.2146
  91. Schipani, E., Ryan, H.E., Didrickson, S., Kobayashi, T., Knight, M., and Johnson, R.S. (2001). Hypoxia in cartilage: HIF-1alpha is essential for chondrocyte growth arrest and survival. Genes Dev. 15, 2865-2876.
  92. Schwer, B., and Verdin, E. (2008). Conserved metabolic regulatory functions of sirtuins. Cell Metab. 7, 104-112. https://doi.org/10.1016/j.cmet.2007.11.006
  93. Sesselmann, S., Soder, S., Voigt, R., Haag, J., Grogan, S., and Aigner, T. (2009). DNA methylation is not responsible for p21WAF1/CIP1 down-regulation in osteoarthritic chondrocytes. Osteoarthritis Cartilage 17, 507-512. https://doi.org/10.1016/j.joca.2008.09.006
  94. Sterner, D.E., and Berger, S.L. (2000). Acetylation of histones and transcription-related factors. Microbiol. Mol. Biol. Rev. 64, 435-459. https://doi.org/10.1128/MMBR.64.2.435-459.2000
  95. Tateishi, K., Okada, Y., Kallin, E.M., and Zhang, Y. (2009). Role of Jhdm2a in regulating metabolic gene expression and obesity resistance. Nature 458, 757-761. https://doi.org/10.1038/nature07777
  96. Troeberg, L., and Nagase, H. (2012). Proteases involved in cartilage matrix degradation in osteoarthritis. Biochim. Biophys. Acta 1824, 133-145. https://doi.org/10.1016/j.bbapap.2011.06.020
  97. Vega, R.B., Matsuda, K., Oh, J., Barbosa, A.C., Yang, X., Meadows, E., McAnally, J., Pomajzl, C., Shelton, J.M., Richardson, J.A., et al. (2004). Histone deacetylase 4 controls chondrocyte hypertrophy during skeletogenesis. Cell 119, 555-566. https://doi.org/10.1016/j.cell.2004.10.024
  98. Wang, J., Gardner, B.M., Lu, Q., Rodova, M., Woodbury, B.G., Yost, J.G., Roby, K.F., Pinson, D.M., Tawfik, O., and Anderson, H.C. (2009). Transcription factor Nfat1 deficiency causes osteoarthritis through dysfunction of adult articular chondrocytes. J. Pathol. 219, 163-172. https://doi.org/10.1002/path.2578
  99. Wellen, K.E., Hatzivassiliou, G., Sachdeva, U.M., Bui, T.V., Cross, J.R., and Thompson, C.B. (2009). ATP-citrate lyase links cellular metabolism to histone acetylation. Science 324, 1076-1080. https://doi.org/10.1126/science.1164097
  100. Wluka, A.E., Lombard, C.B., and Cicuttini, F.M. (2013). Tackling obesity in knee osteoarthritis. Nat. Rev. Rheumatol. 9, 225-235. https://doi.org/10.1038/nrrheum.2012.224
  101. Yammani, R.R., and Loeser, R.F. (2012). Extracellular nicotinamide phosphoribosyltransferase (NAMPT/visfatin) inhibits insulin-like growth factor-1 signaling and proteoglycan synthesis in human articular chondrocytes. Arthritis Res. Ther. 14, R23. https://doi.org/10.1186/ar3705
  102. 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-2alpha is a catabolic regulator of osteoarthritic cartilage destruction. Nat. Med. 16, 687-693. https://doi.org/10.1038/nm.2153
  103. Yang, S., Ryu, J.H., Oh, H., Jeon, J., Kwak, J.S., Kim, J.H., Kim, H.A., Chun, C.H., and Chun, J.S. (2015). NAMPT (visfatin), a direct target of hypoxia-inducible factor-2alpha, is an essential catabolic regulator of osteoarthritis. Ann. Rheumatic Dis. 74, 595-602.
  104. Yusuf, E., Ioan-Facsinay, A., Bijsterbosch, J., Klein-Wieringa, I., Kwekkeboom, J., Slagboom, P.E., Huizinga, T.W., and Kloppenburg, M. (2011). Association between leptin, adiponectin and resistin and long-term progression of hand osteoarthritis. Ann. Rheumatic Dis. 70, 1282-1284. https://doi.org/10.1136/ard.2010.146282
  105. Zhong, H., May, M.J., Jimi, E., and Ghosh, S. (2002). The phosphorylation status of nuclear NF-kappa B determines its association with CBP/p300 or HDAC-1. Mol. Cell 9, 625-636. https://doi.org/10.1016/S1097-2765(02)00477-X
  106. Zhong, H.M., Ding, Q.H., Chen, W.P., and Luo, R.B. (2013). Vorinostat, a HDAC inhibitor, showed anti-osteoarthritic activities through inhibition of iNOS and MMP expression, p38 and ERK phosphorylation and blocking NF-kappaB nuclear translocation. Int. Immunopharmacol. 17, 329-335. https://doi.org/10.1016/j.intimp.2013.06.027
  107. Zhuo, Q., Yang, W., Chen, J., and Wang, Y. (2012). Metabolic syndrome meets osteoarthritis. Nat. Rev. Rheumatol. 8, 729-737. https://doi.org/10.1038/nrrheum.2012.135
  108. 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. https://doi.org/10.1002/art.23736

피인용 문헌

  1. Molecular mechanisms underlying osteoarthritis development: Notch and NF-κB vol.19, pp.1, 2017, https://doi.org/10.1186/s13075-017-1296-y
  2. Epigenetic modifications of interleukin-6 in synovial fibroblasts from osteoarthritis patients vol.7, 2017, https://doi.org/10.1038/srep43592
  3. Epigenetics of cartilage diseases vol.83, pp.5, 2016, https://doi.org/10.1016/j.jbspin.2015.10.004
  4. 3′-Sialyllactose protects against osteoarthritic development by facilitating cartilage homeostasis 2017, https://doi.org/10.1111/jcmm.13292
  5. Protective effects of aucubin on osteoarthritic chondrocyte model induced by hydrogen peroxide and mechanical stimulus vol.17, pp.1, 2017, https://doi.org/10.1186/s12906-017-1581-y
  6. miR-181a Modulates Chondrocyte Apoptosis by Targeting Glycerol-3-Phosphate Dehydrogenase 1-Like Protein (GPD1L) in Osteoarthritis vol.23, 2017, https://doi.org/10.12659/MSM.899228
  7. TWIST1 induces MMP3 expression through up-regulating DNA hydroxymethylation and promotes catabolic responses in human chondrocytes vol.7, 2017, https://doi.org/10.1038/srep42990
  8. Interplay of Inflammatory Mediators with Epigenetics and Cartilage Modifications in Osteoarthritis vol.6, pp.2296-4185, 2018, https://doi.org/10.3389/fbioe.2018.00022
  9. Model of Osteoarthritis vol.27, pp.11, 2018, https://doi.org/10.1177/0963689718804130
  10. Exosomal miR-95-5p regulates chondrogenesis and cartilage degradation via histone deacetylase 2/8 pp.15821838, 2018, https://doi.org/10.1111/jcmm.13808
  11. Modulation of matrix metabolism by ATP-citrate lyase in articular chondrocytes vol.293, pp.31, 2018, https://doi.org/10.1074/jbc.RA118.002261
  12. Intra-Articular Injection of Hydrolyzed Collagen to Treat Symptoms of Knee Osteoarthritis. A Functional In Vitro Investigation and a Pilot Retrospective Clinical Study vol.8, pp.7, 2015, https://doi.org/10.3390/jcm8070975
  13. Formononetin Antagonizes the Interleukin-1β-Induced Catabolic Effects Through Suppressing Inflammation in Primary Rat Chondrocytes vol.42, pp.4, 2015, https://doi.org/10.1007/s10753-019-01005-1
  14. Understanding the Observed Sex Discrepancy in the Prevalence of Osteoarthritis vol.7, pp.9, 2015, https://doi.org/10.2106/jbjs.rvw.18.00182
  15. Extracellular vesicles: Potential role in osteoarthritis regenerative medicine vol.21, pp.None, 2020, https://doi.org/10.1016/j.jot.2019.10.012
  16. Effects of occlusion modification on the remodelling of degenerative mandibular condylar processes vol.26, pp.3, 2015, https://doi.org/10.1111/odi.13274
  17. Characterization and miRNA Profiling of Extracellular Vesicles from Human Osteoarthritic Subchondral Bone Multipotential Stromal Cells (MSCs) vol.2021, pp.None, 2021, https://doi.org/10.1155/2021/7232773
  18. Experimental Therapeutics for the Treatment of Osteoarthritis vol.13, pp.None, 2021, https://doi.org/10.2147/jep.s237479
  19. Histone Modifications and Chondrocyte Fate: Regulation and Therapeutic Implications vol.9, pp.None, 2021, https://doi.org/10.3389/fcell.2021.626708
  20. Disease-modifying therapeutic strategies in osteoarthritis: current status and future directions vol.53, pp.11, 2021, https://doi.org/10.1038/s12276-021-00710-y
  21. Supercritical carbon dioxide decellularized porcine cartilage graft with PRP attenuated OA progression and regenerated articular cartilage in ACLT‐induced OA rats vol.15, pp.12, 2021, https://doi.org/10.1002/term.3252
  22. CircRNA-MSR Regulates LPS-Induced C28/I2 Chondrocyte Injury through miR-643/MAP2K6 Signaling Pathway vol.13, pp.2, 2015, https://doi.org/10.1177/19476035211044826
  23. Cathelicidin antimicrobial peptide (CAMP) gene promoter methylation induces chondrocyte apoptosis vol.15, pp.1, 2015, https://doi.org/10.1186/s40246-021-00321-8