The role of epigenetics in osteoarthritis: Current perspective

Current Opinion in Rheumatology

Volumn 29, Issue 1, 2017, Pages 119-129

  Ramos, Yolande F M ^a   Meulenbelt, Ingrid ^a  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Epigenetics; Methylation; Noncoding RNAs; Osteoarthritis; Transcriptome

Indexed keywords

DNA; HISTONE; UNTRANSLATED RNA;

DNA METHYLATION; EPIGENETICS; HISTONE MODIFICATION; HOMEOSTASIS; HUMAN; JOINT; MOLECULAR PATHOLOGY; NONHUMAN; OSTEOARTHRITIS; PRIORITY JOURNAL; REVIEW; TRANSLATION REGULATION; GENETIC EPIGENESIS; GENETIC PREDISPOSITION; GENETICS; PROCEDURES;

DNA METHYLATION; EPIGENESIS, GENETIC; EPIGENOMICS; GENETIC PREDISPOSITION TO DISEASE; HUMANS; OSTEOARTHRITIS; RNA, UNTRANSLATED;

EID: 84991466948     PISSN: 10408711     EISSN: 15316963     Source Type: Journal    
DOI: 10.1097/BOR.0000000000000355     Document Type: Review

References (86)

1. Loeser RF. Aging processes and the development of osteoarthritis. Curr Opin Rheumatol 2013; 25:108-113.
2. Drissi H, Zuscik M, Rosier R, O'Keefe R. Transcriptional regulation of chondrocyte maturation: potential involvement of transcription factors in OA pathogenesis. Mol Aspects Med 2005; 26:169-179.
3. Lotz M, Loeser RF. Effects of aging on articular cartilage homeostasis. Bone 2012; 51:241-248.
4. Goldring MB, Marcu KB. Epigenomic and microRNA-mediated regulation in cartilage development, homeostasis, and osteoarthritis. Trends Mol Med 2012; 18:109-118.
5. Meulenbelt IM, Bhutani N, den Hollander W, et al. The first international workshop on the epigenetics of osteoarthritis. Connect Tissue Res 2016; 30:1-12.
6. JiQ, Xu X, Zhang Q, et al. The IL-1b/AP-1/miR-30a/ADAMTS-5 axis regulates cartilage matrix degradation in human osteoarthritis. J Mol Med (Berl) 2016; 94:771-785.
7. Rushton MD, Reynard LN, Young DA, et al. Methylation quantitative trait locus analysis of osteoarthritis links epigenetics with genetic risk. Hum Mol Genet 2015; 24:7432-7444.
8. 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; 278:27224-27229.
9. Furumatsu T, Tsuda M, Yoshida K, et al. Sox9 and p300 cooperatively regulate chromatin-mediated transcription. J Biol Chem 2005; 280: 35203-35208.
10. Oppenheimer H, Kumar A, Meir H, et al. Set7/9 impacts COL2A1 expression through binding and repression of SirT1 histone deacetylation. J Bone Miner Res 2014; 29:348-360.
11. Otero M, Peng H, El Hachem K, et al. ELF3 modulates type II collagen gene (COL2A1) transcription in chondrocytes by inhibiting SOX9-CBP/p300-driven histone acetyltransferase activity. Connect Tissue Res 2016; 1-12; doi:10. 1080/03008207. 2016. 1200566. [Epub ahead of print]
12. Bomer N, den Hollander W, Ramos YF, et al. Underlying molecular mechanisms of DIO2 susceptibility in symptomatic osteoarthritis. Ann Rheum Dis 2015; 74:1571-1579.
13. Castanõ Betancourt MC, Cailotto F, Kerkhof HJ, et al. Genome-wide association and functional studies identify the DOT1L gene to be involved in cartilage thickness and hip osteoarthritis. Proc Natl Acad Sci USA 2012; 109:8218-8223.
14. Zeggini E, Panoutsopoulou K, Southam L, et al. Identification of new susceptibility loci for osteoarthritis (arcOGEN): a genome-wide association study. Lancet 2012; 380:815-823.
15. Jia G, Fu Y, Zhao X, et al. N6-methyladenosine in nuclear RNA is a major substrate of the obesity-associated FTO. Nat Chem Biol 2011; 7:885-887.
16. Reynard LN, Bui C, Canty-Laird EG, et al. Expression of the osteoarthritisassociated gene GDF5 is modulated epigenetically by DNA methylation. Hum Mol Genet 2011; 20:3450-3460.
17. Hashimoto K, Oreffo RO, Gibson MB, et al. DNA demethylation at specific CpG sites in the IL1B promoter in response to inflammatory cytokines in human articular chondrocytes. Arthritis Rheum 2009; 60:3303-3313.
18. Hashimoto K, Otero M, Imagawa K, et al. Regulated transcription of human matrix metalloproteinase 13 (MMP13) and interleukin-1b (IL1B) genes in chondrocytes depends on methylation of specific proximal promoter CpG sites. J Biol Chem 2013; 288:10061-10072.
19. 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.
20. Li X, Zhen Z, Tang G, et al. miR-29a and miR-140 protect chondrocytes against the anti-proliferation and cell matrix signaling changes by IL-1b. Mol Cells 2016; 39:103-110.
21. Meng F, Zhang Z, Chen W, et al. MicroRNA-320 regulates matrix metalloproteinase-13 expression in chondrogenesis and interleukin-1b-induced chondrocyte responses. Osteoarthritis Cartilage 2016; 24:932-941.
22. Wang G, Zhang Y, Zhao X, et al. MicroRNA-411 inhibited matrix metalloproteinase 13 expression in human chondrocytes. Am J Transl Res 2015; 7:2000-2006.
23. Zhang M, Lu Q, Egan B, et al. Epigenetically mediated spontaneous reduction of NFAT1 expression causes imbalanced metabolic activities of articular chondrocytes in aged mice. Osteoarthritis Cartilage 2016; 24:1274-1283.
24. Ji Q, Xu X, Xu Y, et al. miR-105/Runx2 axis mediates FGF2-induced ADAMTS expression in osteoarthritis cartilage. J Mol Med (Berl) 2016; 94:681-694.
25. 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; 28:1050-1060.
26. Chang T, Xie J, Li H, et al. MicroRNA-30a promotes extracellular matrix degradation in articular cartilage via downregulation of Sox9. Cell Prolif 2016; 49:207-218.
27. Ludwig AK, Zhang P, Cardoso MC. Modifiers and readers of DNA modifications and their impact on genome structure, expression, and stability in disease. Front Genet 2016; 7:115.
28. Slieker RC, Bos SD, Goeman JJ, et al. Identification and systematic annotation of tissue-specific differentially methylated regions using the Illumina 450k array. Epigenetics Chromatin 2013; 6:26.
29. Delgado-Calle J, Fernández AF, Sainz J, et al. Genome-wide profiling of bone reveals differentially methylated regions in osteoporosis and osteoarthritis. Arthritis Rheum 2013; 65:197-205.
30. den Hollander W, Meulenbelt I. DNA methylation in osteoarthritis. Curr Genomics 2015; 16:419-426.
31. Reynard LN. Analysis of genetics and DNA methylation in osteoarthritis: What have we learnt about the disease Semin Cell Dev Biol 2016; S1084-9521(16) 30121-5 http://dx. doi. org/10. 1016/j. semcdb. 2016. 04. 017. [Epub ahead of print]
32. den Hollander W, Ramos YF, Bos SD, et al. Knee and hip articular cartilage have distinct epigenomic landscapes: implications for future cartilage regeneration approaches. Ann Rheum Dis 2014; 73:2208-2212.
33. Jeffries MA, Donica M, Baker LW, et al. Genome-wide DNA methylation study identifies significant epigenomic changes in osteoarthritic cartilage. Arthritis Rheumatol 2014; 66:2804-2815.
34. Jeffries MA, Donica M, Baker LW, et al. Genome-wide DNA methylation study identifies significant epigenomic changes in osteoarthritic subchondral bone and similarity to overlying cartilage. Arthritis Rheumatol 2016; 68:1403-1414.
35. Zhang Y, Fukui N, Yahata M, et al. Genome-wide DNA methylation profile implicates potential cartilage regeneration at the late stage of knee osteoarthritis. Osteoarthritis Cartilage 2016; 24:835-843.
36. Rushton MD, Young DA, Loughlin J, Reynard LN. Differential DNA methylation and expression of inflammatory and zinc transporter genes defines subgroups of osteoarthritic hip patients. Ann Rheum Dis 2015; 74:1778-1782.
37. den Hollander W, Ramos YF, Bomer N, et al. Transcriptional associations of osteoarthritis-mediated loss of epigenetic control in articular cartilage. Arthritis Rheumatol 2015; 67:2108-2116.
38. Taylor SE, Li YH, Smeriglio P, et al. Stable 5-hydroxymethylcytosine (5hmC) acquisition marks gene activation during chondrogenic differentiation. J Bone Miner Res 2016; 31:524-534. First study assessing genome wide 5hmC marks during skeletal development in mice.
39. Haseeb A, Makki MS, Haqqi TM. Modulation of ten-eleven translocation 1 (TET1), isocitrate dehydrogenase (IDH) expression, a-ketoglutarate (a-KG), and DNA hydroxymethylation levels by interleukin-1b in primary human chondrocytes. J Biol Chem 2014; 289:6877-6885.
40. Loughlin J. Genetic contribution to osteoarthritis development: current state of evidence. Curr Opin Rheumatol 2015; 27:284-288.
41. Vojta A, Dobrinić P, Tadić V, et al. Repurposing the CRISPR-Cas9 system for targeted DNA methylation. Nucleic Acids Res 2016; 44:5615-5628.
42. Esteller M. Non-coding RNAs in human disease. Nat Rev Genet 2011; 12:861-874.
43. Dole NS, Delany AM. MicroRNA variants as genetic determinants of bone mass. Bone 2016; 84:57-68.
44. Seeliger C, Balmayor ER, van Griensven GM. miRNAs related to skeletal diseases. Stem Cells Dev 2016; 25:1261-1281.
45. Gulyaeva LF, Kushlinskiy NE. Regulatory mechanisms of microRNA expression. J Transl Med 2016; 14:143.
46. Tu M, Li Y, Zeng C, et al. MicroRNA-127-5p regulates osteopontin expression and osteopontin-mediated proliferation of human chondrocytes. Sci Rep 2016; 6:25032.
47. Hu W, Zhang W, Li F, et al. miR-139 is up-regulated in osteoarthritis and inhibits chondrocyte proliferation and migration possibly via suppressing EIF4G2 and IGF1R. Biochem Biophys Res Commun 2016; 474:296-302.
48. Wang X, Guo Y, Wang C, et al. MicroRNA-142-3p inhibits chondrocyte apoptosis and inflammation in osteoarthritis by targeting HMGB1. Inflammation 2016; 39:1718-1728.
49. D'Adamo S, Alvarez-Garcia O, Muramatsu Y, et al. MicroRNA-155 suppresses autophagy in chondrocytes by modulating expression of autophagy proteins. Osteoarthritis Cartilage 2016; 24:1082-1091.
50. Rasheed Z, Rasheed N, Al-Shobaili HA. Epigallocatechin-3-O-gallate upregulates microRNA-199a-3p expression by down-regulating the expression of cyclooxygenase-2 in stimulated human osteoarthritis chondrocytes. J Cell Mol Med 2016; doi: 10. 1111/jcmm. 12897. [Epub ahead of print]
51. Kang L, Yang C, Song Y, et al. MicroRNA-23a-3p promotes the development of osteoarthritis by directly targeting SMAD3 in chondrocytes. Biochem Biophys Res Commun 2016; 478:467-473.
52. Rasheed Z, Al-Shobaili HA, Rasheed N, et al. MicroRNA-26a-5p regulates the expression of inducible nitric oxide synthase via activation of NF-kB pathway in human osteoarthritis chondrocytes. Arch Biochem Biophys 2016; 594:61-67.
53. Le LT, Swingler TE, Crowe N, et al. The microRNA-29 family in cartilage homeostasis and osteoarthritis. J Mol Med (Berl) 2016; 94:583-596.
54. Li Z, Meng D, Li G, et al. Overexpression of microRNA-210 promotes chondrocyte proliferation and extracellular matrix deposition by targeting HIF-3a in osteoarthritis. Mol Med Rep 2016; 13:2769-2776.
55. Lolli A, Narcisi R, Lambertini E, et al. Silencing of antichondrogenic microRNA-221 in human mesenchymal stem cells promotes cartilage repair in vivo. Stem Cells 2016; 34:1801-1811.
56. Wei M, Xie Q, Zhu J, et al. MicroRNA-33 suppresses CCL2 expression in chondrocytes. Biosci Rep 2016; 36:e00332.
57. Yan S, Wang M, Zhao J, et al. MicroRNA-34a affects chondrocyte apoptosis and proliferation by targeting the SIRT1/p53 signaling pathway during the pathogenesis of osteoarthritis. Int J Mol Med 2016; 38:201-209.
58. Yang X, Guan Y, Tian S, et al. Mechanical and IL-1b responsive miR-365 contributes to osteoarthritis development by targeting histone deacetylase 4. Int J Mol Sci 2016; 17:436.
59. Park KW, Lee KM, Yoon DS, et al. Inhibition of microRNA-449a prevents IL-1b-induced cartilage destruction via SIRT1. Osteoarthritis Cartilage 2016. S1063-4584(16) 30176-5. doi:10. 1016/j. joca. 2016. 07. 002.
60. Zhang G, Sun Y, Wang Y, et al. MiR-502-5p inhibits IL-1b-induced chondrocyte injury by targeting TRAF2. Cell Immunol 2016; 302:50-57.
61. Cui X, Wang S, Cai H, et al. Overexpression of microRNA-634 suppresses survival and matrix synthesis of human osteoarthritis chondrocytes by targeting PIK3R1. Sci Rep 2016; 6:23117.
62. Xu J, Liu Y, Deng M, et al. MicroRNA221-3p modulates Ets-1 expression in synovial fibroblasts from patients with osteoarthritis of temporomandibular joint. Osteoarthritis Cartilage 2016; S1063-4584(16) 30143-1. doi 10. 1016/j. joca. 2016. 011. [Epub ahead of print]
63. Li YH, Tavallaee G, Tokar T, et al. Identification of synovial fluid microRNA signature in knee osteoarthritis: differentiating early-and late-stage knee osteoarthritis. Osteoarthritis Cartilage 2016; 24:1577-1586.
64. Prasadam I, Batra J, Perry S, et al. Systematic identification, characterization and target gene analysis of microRNAs involved in osteoarthritis subchondral bone pathogenesis. Calcif Tissue Int 2016; 99:43-55.
65. Rasheed Z, Al-Shobaili HA, Rasheed N, et al. Integrated study of globally expressed microRNAs in IL-1b-stimulated human osteoarthritis chondrocytes and osteoarthritis relevant genes: a microarray and bioinformatics analysis. Nucleosides Nucleotides Nucleic Acids 2016; 35:335-355.
66. Genemaras AA, Ennis H, Kaplan L, Huang CY. Inflammatory cytokines induce specific time-and concentration-dependent MicroRNA release by chondrocytes, synoviocytes, and meniscus cells. J Orthop Res 2016; 34:779-790.
67. Xu JF, Zhang SJ, Zhao C, et al. Altered microRNA expression profile in synovial fluid from patients with knee osteoarthritis with treatment of hyaluronic acid. Mol Diagn Ther 2015; 19:299-308.
68. Kosaka N, Yoshioka Y, Hagiwara K, et al. Trash or Treasure: extracellular microRNAs and cell-to-cell communication. Front Genet 2013; 4:173.
69. Chevillet JR, Lee I, Briggs HA, et al. Issues and prospects of microRNA-based biomarkers in blood and other body fluids. Molecules 2014; 19:6080-6105.
70. Weilner S, Grillari-Voglauer R, Redl H, et al. The role of microRNAs in cellular senescence and age-related conditions of cartilage and bone. Acta Orthop 2015; 86:92-99.
71. Beyer C, Zampetaki A, Lin NY, et al. Signature of circulating microRNAs in osteoarthritis. Ann Rheum Dis 2015; 74:e18.
72. Hoernes TP, Erlacher MD. Translating the epitranscriptome. Wiley Interdiscip Rev RNA 2016; doi:10. 1002/wrna. 1375. [Epub ahead of print]
73. Chou CH, Wu CC, Song IW, et al. Genome-wide expression profiles of subchondral bone in osteoarthritis. Arthritis Res Ther 2013; 15:R190.
74. Carpio LR, Westendorf JJ. Histone deacetylases in cartilage homeostasis and osteoarthritis. Curr Rheumatol Rep 2016; 18:52.
75. Dvir-Ginzberg M, Mobasheri A, Kumar A. The role of sirtuins in cartilage homeostasis and osteoarthritis. Curr Rheumatol Rep 2016; 18:43.
76. Swygert SG, Peterson CL. Chromatin dynamics: interplay between remodeling enzymes and histone modifications. Biochim Biophys Acta 2014; 1839:728-736.
77. El Mansouri FE, Nebbaki SS, Kapoor M, et al. Lysine-specific demethylase 1-mediated demethylation of histone H3 lysine 9 contributes to interleukin 1binduced microsomal prostaglandin E synthase 1 expression in human osteoarthritic chondrocytes. Arthritis Res Ther 2014; 16:R113.
78. Dvir-Ginzberg M, Gagarina V, Lee EJ, Hall DJ. Regulation of cartilage-specific gene expression in human chondrocytes by SirT1 and nicotinamide phosphoribosyltransferase. J Biol Chem 2008; 283:36300-36310.
79. Fujita N, Matsushita T, Ishida K, et al. Potential involvement of SIRT1 in the pathogenesis of osteoarthritis through the modulation of chondrocyte gene expressions. J Orthop Res 2011; 29:511-515.
80. Chen L, Wu Y, Wu Y, et al. The inhibition of EZH2 ameliorates osteoarthritis development through the Wnt/b-catenin pathway. Sci Rep 2016; 6:29176.
81. Ramos YF, den Hollander W, Bovee JV, et al. Genes involved in the osteoarthritis process identified through genome wide expression analysis in articular cartilage; the RAAK study. PLoS ONE 2014; 9: e103056.
82. Xu Y, Barter MJ, Swan DC, et al. Identification of the pathogenic pathways in osteoarthritic hip cartilage: commonality and discord between hip and knee OA. Osteoarthritis Cartilage 2012; 20:1029-1038.
83. Jones B, Su H, Bhat A, et al. The histone H3K79 methyltransferase Dot1L is essential for mammalian development and heterochromatin structure. PLoS Genet 2008; 4:e1000190.
84. Yapp C, Carr AJ, Price A, et al. H3K27me3 demethylases regulate in vitro chondrogenesis and chondrocyte activity in osteoarthritis. Arthritis Res Ther 2016; 18:158.
85. Önder Ö, Sidoli S, Carroll M, Garcia BA. Progress in epigenetic histone modification analysis by mass spectrometry for clinical investigations. Expert Rev Proteomics 2015; 12:499-517.
86. Lai X, Wolkenhauer O, Vera J. Understanding microRNA-mediated gene regulatory networks through mathematical modelling. Nucleic Acids Res 2016; 44:6019-6035.