Significance of epigenetic landscape in cartilage regeneration from the cartilage development and pathology perspective

Stem Cells and Development

Volumn 23, Issue 11, 2014, Pages 1178-1194

  Li, Jingting ^a   Ohliger, James ^a,b   Pei, Ming ^a,b  

^a WEST VIRGINIA UNIVERSITY   (United States)

^b WEST VIRGINIA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GROWTH FACTOR; MICRORNA;

AGING; CARTILAGE CELL; CARTILAGE DEGENERATION; CELL DIFFERENTIATION; CELL PROLIFERATION; DEVELOPMENT; DNA METHYLATION; ENVIRONMENTAL FACTOR; EPIGENETICS; GENE EXPRESSION; HISTONE MODIFICATION; HUMAN; HYPOXIA; INFLAMMATION; NONHUMAN; NUCLEOSOME; OSTEOARTHRITIS; OXIDATIVE STRESS; PATHOLOGY; PRIORITY JOURNAL; REGENERATIVE MEDICINE; REGULATORY MECHANISM; REVIEW; RHEUMATOID ARTHRITIS; STEM CELL; TISSUE ENGINEERING; ANIMAL; CARTILAGE; CARTILAGE DISEASES; CHONDROGENESIS; CYTOLOGY; GENETIC EPIGENESIS; GENETICS; PHYSIOLOGY; PROCEDURES; REGENERATION;

ANIMALS; CARTILAGE; CARTILAGE DISEASES; CHONDROGENESIS; EPIGENESIS, GENETIC; HUMANS; OSTEOARTHRITIS; REGENERATION; TISSUE ENGINEERING;

EID: 84901302679     PISSN: 15473287     EISSN: 15578534     Source Type: Journal    
DOI: 10.1089/scd.2014.0002     Document Type: Review

References (185)

1. Arøen A, S Løken, S Heir, E Alvik, A Ekeland, OG Granlund and L Engebretsen. (2004). Articular cartilage lesions in 993 consecutive knee arthroscopies. Am J Sports Med 32:211-215.
2. Curl WW, J Krome, ES Gordon, J Rushing, BP Smith and GG Poehling. (1997). Cartilage injuries: a review of 31, 516 knee arthroscopies. Arthroscopy 13:456-460.
3. Mandelbaum BR, JE Browne, F Fu, L Micheli, JB Mosely, C Erggelet, T Minas and L Peterson. (1998). Articular cartilage lesions of the knee. Am J Sports Med 26: 853-861.
4. Alford JW. (2005). Cartilage restoration, part 1: basic science, historical perspective, patient evaluation, and treatment options. Am J Sports Med 33:295-306.
5. Alford JW. (2005). Cartilage restoration, part 2: techniques, outcomes, and future directions. Am J Sports Med 33:443-460.
6. Nejadnik H, JH Hui, EP Feng Choong, BC Tai and EH Lee. (2010). Autologous bone marrow-derived mesenchymal stem cells versus autologous chondrocyte implantation: an observational cohort study. Am J Sports Med 38:1110-1116.
7. Boeuf S and W Richter. (2010). Chondrogenesis of mesenchymal stem cells: role of tissue source and inducing factors. Stem Cell Res Ther 1:31.
8. Herlofsen SR, JC Bryne, T Høiby, L Wang, R Issner, X Zhang, MJ Coyne, P Boyle, H Gu, et al. (2013). Genomewide map of quantified epigenetic changes during in vitro chondrogenic differentiation of primary human mesenchymal stem cells. BMC Genomics 14:105.
9. Lawson KA, CJ Teteak, J Zou, J Hacquebord, A Ghatan, A Zielinska-Kwiatkowska, RJ Fernandes, HA Chansky and L Yang. (2013). Mesenchymal-specific knockout of ESET histone methyltransferase causes ectopic hypertrophy and terminal differentiation of articular chondrocytes. J Biol Chem 288:32119-32125.
10. Yannarelli G, N Pacienza, L Cuniberti, J Medin, J Davies and A Keating. (2013). Brief report: The potential role of epigenetics on multipotent cell differentiation capacity of mesenchymal stromal cells. Stem Cells 31:215-220.
11. Issa JP. (2000). CpG-island methylation in aging and cancer. Curr Top Microbiol Immunol 249:101-118.
12. Barter MJ, C Bui and DA Young. (2012). Epigenetic mechanisms in cartilage and osteoarthritis: DNA methylation, histone modifications and microRNAs. Osteoarthritis Cartilage 20:339-349.
13. Reynard LN and J Loughlin. (2012). Genetics and epigenetics of osteoarthritis. Maturitas 71:200-204.
14. Viatte S, D Plant and S Raychaudhuri. (2013). Genetics and epigenetics of rheumatoid arthritis. Nat Rev Rheumatol 9:141-153.
15. Berger SL, T Kouzarides, R Shiekhattar and A Shilatifard. (2009). An operational definition of epigenetics. Genes Dev 23:781-783.
16. Jaenisch R and A Bird. (2003). Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat Genet 33 Suppl:245-254.
17. Feinberg AP. (2007). Phenotypic plasticity and the epigenetics of human disease. Nature 447:433-440.
18. Barros SP and S Offenbacher. (2009). Epigenetics: connecting environment and genotype to phenotype and disease. J Dent Res 88:400-408.
19. Ntanasis-Stathopoulos J, JG Tzanninis, A Philippou and M Koutsilieris. (2013). Epigenetic regulation on gene expression induced by physical exercise. J Musculoskelet Neuronal Interact 13:133-146.
20. Koch CM and Wagner W. (2011). Epigenetic-agingsignature to determine age in different tissues. Aging (Albany NY) 3:1018-1027.
21. Da Silva MA, N Yamada, NMP Clarke and HI Roach (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. Loeser RF, HJ Im, B Richardson, Q Lu and S Chubinskaya. (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.
23. Donmez G and L Guarente. (2010). Aging and disease: connections to sirtuins. Aging Cell 9:285-290.
24. Gabay O, KJ Zaal, C Sanchez, M Dvir-Ginzberg, V Gagarina, Y Song, XH He and MW McBurney. (2013). Sirt1-deficient mice exhibit an altered cartilage phenotype. Joint Bone Spine 80:613-620.
25. Moon MH, JK Jeong, YJ Lee, JW Seol, CJ Jackson and SY Park. (2013). SIRT1, a class III histone deacetylase, regulates TNF-α-induced inflammation in human chondrocytes. Osteoarthritis Cartilage 21:470-480.
26. Takayama K, K Ishida, T Matsushita, N Fujita, S Hayashi, K Sasaki, K Tei, S Kubo, T Matsumoto, et al. (2009). SIRT1 regulation of apoptosis of human chondrocytes. Arthritis Rheum 60:2731-2740.
27. Gagarina V, O Gabay, M Dvir-Ginzberg, EJ Lee, JK Brady, MJ Quon and DJ Hall. (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.
28. Li J and M Pei. (2012). Cell senescence: a challenge in cartilage engineering and regeneration. Tissue Eng Part B Rev 18:270-287.
29. You H, W Ding and CB Rountree. (2010). Epigenetic regulation of cancer stem cell marker CD133 by transforming growth factor-beta. Hepatology 51:1635-1644.
30. Pan Q, Y Wu, T Lin, H Yao, Z Yang, G Gao, E Song and H Shen. (2009). Bone morphogenetic protein-2 induces chromatin remodeling and modification at the proximal promoter of Sox9 gene. Biochem Biophys Res Commun 379:356-361.
31. Milagro FI, J Campión, P Cordero, E Goyenechea, AM Gómez-Uriz, I Abete, MA Zulet and JA Martínez. (2011). A dual epigenomic approach for the search of obesity biomarkers: DNA methylation in relation to diet-induced weight loss. FASEB J 25:1378-1389.
32. Chung TL, RM Brena, G Kolle, SM Grimmond, BP Berman, PW Laird, MF Pera and EJ Wolvetang. (2010). Vitamin C promotes widespread yet specific DNA demethylation of the epigenome in human embryonic stem cells. Stem Cells 28:1848-1855.
33. Esteban MA and D Pei. (2012). Vitamin C improves the quality of somatic cell reprogramming. Nat Genet 44:366-367.
34. Thoms BL, KA Dudek, JE Lafont and CL Murphy. (2013). Hypoxia promotes the production and inhibits the destruction of human articular cartilage. Arthritis Rheum 65:1302-1312.
35. Hashimoto K, M Otero, K Imagawa, MC de Andrés, JM Coico, HI Roach, ROC Oreffo, KB Marcu and MB Goldring. (2013). Regulated transcription of human matrix metalloproteinase 13 (MMP13) and interleukin-1β (IL1B) genes in chondrocytes depends on methylation of specific proximal promoter CpG sites. J Biol Chem 288: 10061-10072.
36. Okazaki K and E Maltepe. (2006). Oxygen, epigenetics and stem cell fate. Regen Med 1:71-83.
37. Yang J, I Ledaki, H Turley, KC Gatter, JC Montero, JL Li and AL Harris. (2009). Role of hypoxia-inducible factors in epigenetic regulation via histone demethylases. Ann N Y Acad Sci 1177:185-197.
38. De Santa F, MG Totaro, E Prosperini, S Notarbartolo, G Testa and G Natoli. (2007). The histone H3 lysine-27 demethylase Jmjd3 links inflammation to inhibition of polycomb-mediated gene silencing. Cell 130:1083-1094.
39. Palacios D, C Mozzetta, S Consalvi, G Caretti, V Saccone, V Proserpio, VE Marquez, S Valente, A Mai, et al. (2010). TNF/p38α/polycomb signaling to Pax7 locus in satellite cells links inflammation to the epigenetic control of muscle regeneration. Cell Stem Cell 7:455-469.
40. Kelly DJ and CR Jacobs. (2010). The role of mechanical signals in regulating chondrogenesis and osteogenesis of mesenchymal stem cells. Birth Defects Res C Embryo Today 90:75-85.
41. Fletcher DA and RD Mullins. (2010). Cell mechanics and the cytoskeleton. Nature 463:485-492.
42. Li Y, JS Chu, K Kurpinski, X Li, DM Bautista, L Yang, KL Sung and S Li. (2011). Biophysical regulation of histone acetylation in mesenchymal stem cells. Biophys J 100:1902-1909.
43. Arnsdorf E, P Tummala and A Castillo. (2010). The epigenetic mechanism of mechanically induced osteogenic differentiation. J Biomech 43:2881-2886.
44. Kanazawa T, T Furumatsu, M Hachioji, T Oohashi, Y Ninomiya and T Ozaki. (2012). Mechanical stretch enhances COL2A1 expression on chromatin by inducing SOX9 nuclear translocalization in inner meniscus cells. J Orthop Res 30:468-474.
45. Mendelsohn AR and JW Larrick. (2013). Rejuvenation of adult stem cells: is age-associated dysfunction epigenetic? Rejuvenation Res 16:152-157.
46. Feng B, MA Ruiz and S Chakrabarti. (2013). Oxidativestress- induced epigenetic changes in chronic diabetic complications. Can J Physiol Pharmacol 91:213-220.
47. Kim GH, JJ Ryan and SL Archer. (2013). The role of redox signaling in epigenetics and cardiovascular disease. Antioxid Redox Signal 18:1920-1936.
48. Mercer TR and JS Mattick. (2013). Structure and function of long noncoding RNAs in epigenetic regulation. Nat Struct Mol Biol 20:300-307.
49. Hong E and AH Reddi. (2013). Dedifferentiation and redifferentiation of articular chondrocytes from surface and middle zones: changes in microRNAs-221/-222, -140, and -143/145 expression. Tissue Eng Part A 19:1015-1022.
50. Zhang Z, Y Kang, H Zhang, X Duan, J Liu, X Li and W Liao. (2012). Expression of microRNAs during chondrogenesis of human adipose-derived stem cells. Osteoarthritis Cartilage 20:1638-1646.
51. Wagner W, S Bork, G Lepperdinger, S Joussen, N Ma, D Strunk and C Koch. (2010). How to track cellular aging of mesenchymal stromal cells? Aging (Albany NY) 2:224-230.
52. Schellenberg A, Q Lin, H Schüler, CM Koch, S Joussen, B Denecke, G Walenda, N Pallua, C V Suschek, M Zenke and W Wagner. (2011). Replicative senescence of mesenchymal stem cells causes DNA-methylation changes which correlate with repressive histone marks. Aging (Albany NY) 3:873-888.
53. Yu JM, X Wu, JM Gimble, X Guan, MA Freitas and BA Bunnell. (2011). Age-related changes in mesenchymal stem cells derived from rhesus macaque bone marrow. Aging Cell 10:66-79.
54. Hackl M, S Brunner, K Fortschegger, C Schreiner, L Micutkova, C Mück, GT Laschober, G Lepperdinger, N Sampson, et al. (2010). miR-17, miR-19b, miR-20a, and miR-106a are down-regulated in human aging. Aging Cell 9:291-296.
55. Wagner W, P Horn, M Castoldi, A Diehlmann, S Bork, R Saffrich, V Benes, J Blake, S Pfister, V Eckstein and AD Ho. (2008). Replicative senescence of mesenchymal stem cells: a continuous and organized process. PLoS One 3: e2213.
56. Fabbri M, R Garzon, A Cimmino, Z Liu, N Zanesi, E Callegari, S Liu, H Alder, S Costinean, et al. (2007). MicroRNA-29 family reverts aberrant methylation in lung cancer by targeting DNA methyltransferases 3A and 3B. Proc Natl Acad Sci U S A 104:15805-15810.
57. Kim YJ, SH Hwang, SY Lee, KK Shin, HH Cho, YC Bae and JS Jung. (2012). miR-486-5p induces replicative senescence of human adipose tissue-derived mesenchymal stem cells and its expression is controlled by high glucose. Stem Cells Dev 21:1749-1760.
58. Marasa BS, S Srikantan, JL Martindale, MM Kim, EK Lee, M Gorospe and K Abdelmohsen. (2010). MicroRNA profiling in human diploid fibroblasts uncovers miR-519 role in replicative senescence. Aging (Albany NY) 2:333-343.
59. Ukai T, M Sato, H Akutsu, A Umezawa and J Mochida. (2012). MicroRNA-199a-3p, microRNA-193b, and microRNA- 320c are correlated to aging and regulate human cartilage metabolism. J Orthop Res 30:1915-1922.
60. Yu Z, Y Li, H Fan, Z Liu and RG Pestell. (2012). miRNAs regulate stem cell self-renewal and differentiation. Front Genet 3:191.
61. Butz H, K Rácz, L Hunyady and A Patócs. (2012). Crosstalk between TGF-b signaling and the microRNA machinery. Trends Pharmacol Sci 33:382-393.
62. Swingler TE, G Wheeler, V Carmont, HR Elliott, MJ Barter, M Abu-Elmagd, ST Donell, RP Boot-Handford, MK Hajihosseini, et al. (2012). The expression and function of microRNAs in chondrogenesis and osteoarthritis. Arthritis Rheum 64:1909-1919.
63. Pais H, FE Nicolas, SM Soond, TE Swingler, IM Clark, A Chantry, V Moulton and T Dalmay. (2010). Analyzing mRNA expression identifies Smad3 as a microRNA- 140 target regulated only at protein level. RNA 16:489-494.
64. Pando R, N Even-Zohar, B Shtaif, L Edry, N Shomron, M Phillip and G Gat-Yablonski. (2012). MicroRNAs in the growth plate are responsive to nutritional cues: association between miR-140 and SIRT1. J Nutr Biochem 23:1474-1481.
65. Kulshreshtha R, M Ferracin, SE Wojcik, R Garzon, H Alder, FJ Agosto-Perez, R Davuluri, C-G Liu, CM Croce, et al. (2007). A microRNA signature of hypoxia. Mol Cell Biol 27:1859-1867.
66. Foja S, M Jung, B Harwardt, D Riemann, O Pelz- Ackermann, and IS Schroeder (2013). Hypoxia supports reprogramming of mesenchymal stromal cells via induction of embryonic stem cell-specific microRNA-302 cluster and pluripotency-associated genes. Cell Reprogram 15:68-79.
67. Chang W, CY Lee, JH Park, MS Park, LS Maeng, CS Yoon, MY Lee, KC Hwang and YA Chung. (2013). Survival of hypoxic human mesenchymal stem cells is enhanced by a positive feedback loop involving miR-210 and hypoxia-inducible factor. J Vet Sci 14:69-76.
68. Cicchillitti L, V Di Stefano, E Isaia, L Crimaldi, P Fasanaro, V Ambrosino, A Antonini, MC Capogrossi, C Gaetano, G Piaggio and F Martelli. (2012). Hypoxiainducible factor 1-a induces miR-210 in normoxic differentiating myoblasts. J Biol Chem 287:44761-44771.
69. Kim HW, HK Haider, S Jiang and M Ashraf. (2009). Ischemic preconditioning augments survival of stem cells via miR-210 expression by targeting caspase-8-associated protein. J Biol Chem 284:33161-33168.
70. Steck E, S Boeuf, J Gabler, N Werth, P Schnatzer, S Diederichs and W Richter. (2012). Regulation of H19 and its encoded microRNA-675 in osteoarthritis and under anabolic and catabolic in vitro conditions. J Mol Med (Berl) 90:1185-1195.
71. Bhaumik D, GK Scott, S Schokrpur, CK Patil, A V Orjalo, F Rodier, GJ Lithgow and J Campisi. (2009). MicroRNAs miR-146a/b negatively modulate the senescence-associated inflammatory mediators IL-6 and IL-8. Aging (Albany NY) 1:402-411.
72. Niimoto T, T Nakasa, M Ishikawa, A Okuhara, B Izumi, M Deie, O Suzuki, N Adachi and M Ochi. (2010). MicroRNA- 146a expresses in interleukin-17 producing T cells in rheumatoid arthritis patients. BMC Musculoskelet Disord 11:209.
73. Dai L, X Zhang, X Hu, C Zhou and Y Ao. (2012). Silencing of microRNA-101 prevents IL-1β-induced extracellular matrix degradation in chondrocytes. Arthritis Res Ther 14:R268.
74. Miyaki S, T Nakasa, S Otsuki, SP Grogan, R Higashiyama, A Inoue, Y Kato, T Sato, MK Lotz and H Asahara. (2009). MicroRNA-140 is expressed in differentiated human articular chondrocytes and modulates interleukin-1 responses. Arthritis Rheum 60:2723-2730.
75. Liang ZJ, H Zhuang, GX Wang, Z Li, HT Zhang, TQ Yu and BD Zhang. (2012). MiRNA-140 is a negative feedback regulator of MMP-13 in IL-1β-stimulated human articular chondrocyte C28/I2 cells. Inflamm Res 61:503-509.
76. Matsukawa T, T Sakai, T Yonezawa, H Hiraiwa, T Hamada, M Nakashima, Y Ono, S Ishizuka, H Nakahara, et al. (2013). MicroRNA-125b regulates the expression of aggrecanase-1 (ADAMTS-4) in human osteoarthritic chondrocytes. Arthritis Res Ther 15:R28.
77. Akhtar N and TM Haqqi. (2012). MicroRNA-199a* regulates the expression of cyclooxygenase-2 in human chondrocytes. Ann Rheum Dis 71:1073-1080.
78. Abouheif MM, T Nakasa, H Shibuya, T Niimoto, W Kongcharoensombat and M Ochi. (2010). Silencing microRNA- 34a inhibits chondrocyte apoptosis in a rat osteoarthritis model in vitro. Rheumatology (Oxford) 49: 2054-2060.
79. Kim D, J Song, S Kim, CH Chun and EJ Jin. (2011). MicroRNA-34a regulates migration of chondroblast and IL-1β-induced degeneration of chondrocytes by targeting EphA5. Biochem Biophys Res Commun 415:551-557.
80. Dunn W, G DuRaine and AH Reddi. (2009). Profiling microRNA expression in bovine articular cartilage and implications for mechanotransduction. Arthritis Rheum 60:2333-2339.
81. Guan Y, X Yang, L Wei and Q Chen. (2011). MiR-365: a mechanosensitive microRNA stimulates chondrocyte differentiation through targeting histone deacetylase. FASEB J 25:4457-4466.
82. Mendias CL, JP Gumucio and EB Lynch. (2012). Mechanical loading and TGF-β change the expression of multiple miRNAs in tendon fibroblasts. J Appl Physiol 113:56-62.
83. Chen Z, TP Shentu, L Wen, DA Johnson and JY Shyy. (2013). Regulation of SIRT1 by oxidative stress-responsive miRNAs and a systematic approach to identify its role in the endothelium. Antioxid Redox Signal 19:1522-1538.
84. Howell JC, E Chun, AN Farrell, EY Hur, CM Caroti, PM Iuvone and R Haque. (2013). Global microRNA expression profiling: curcumin (diferuloylmethane) alters oxidative stress-responsive microRNAs in human ARPE-19 cells. Mol Vis 19:544-560.
85. Lin Y, X Liu, Y Cheng, J Yang, Y Huo and C Zhang. (2009). Involvement of MicroRNAs in hydrogen peroxidemediated gene regulation and cellular injury response in vascular smooth muscle cells. J Biol Chem 284:7903-7913.
86. Ling M, Y Li, Y Xu, Y Pang, L Shen, R Jiang, Y Zhao, X Yang, J Zhang, et al. (2012). Regulation of miRNA-21 by reactive oxygen species-activated ERK/NF-kB in arseniteinduced cell transformation. Free Radic Biol Med 52: 1508-1518.
87. Li Y, H Shelat and YJ Geng. (2012). IGF-1 prevents oxidative stress induced-apoptosis in induced pluripotent stem cells which is mediated by microRNA-1. Biochem Biophys Res Commun 426:615-619.
88. Kim JH, SG Park, SY Song, JK Kim and JH Sung. (2013). Reactive oxygen species-responsive miR-210 regulates proliferation and migration of adipose-derived stem cells via PTPN2. Cell Death Dis 4:e588.
89. Hackett CH, L Greve, KD Novakofski and LA Fortier. (2012). Comparison of gene-specific DNA methylation patterns in equine induced pluripotent stem cell lines with cells derived from equine adult and fetal tissues. Stem Cells Dev 21:1803-1811.
90. Redaelli S, A Bentivegna, D Foudah, M Miloso, J Redondo, G Riva, S Baronchelli, L Dalprà and G Tredici. (2012). From cytogenomic to epigenomic profiles: monitoring the biologic behavior of in vitro cultured human bone marrow mesenchymal stem cells. Stem Cell Res Ther 3:47.
91. Vacanti V, E Kong, G Suzuki, K Sato, JM Canty and T Lee. (2005). Phenotypic changes of adult porcine mesenchymal stem cells induced by prolonged passaging in culture. J Cell Physiol 205:194-201.
92. Li Z, C Liu, Z Xie, P Song, RC Zhao, L Guo, Z Liu and Y Wu. (2011). Epigenetic dysregulation in mesenchymal stem cell aging and spontaneous differentiation. PLoS One 6:e20526.
93. Liu TM, YN Wu, XM Guo, JH Hui, EH Lee and B Lim. (2009). Effects of ectopic Nanog and Oct4 overexpression on mesenchymal stem cells. Stem Cells Dev 18:1013-1022.
94. Marinovic-Kulisic S, G Juric-Lekic, M Vikic-Topic, V Lokosek, V Radujkovic, F Bulic-Jakus, A Katusic, M Vlahovic, L Serman and N Sincic. (2011). 5-azacytidine enhances proliferation in transplanted rat fetal epiglottis. Front Biosci (Elite Ed) 3:581-590.
95. Vogelauer M, L Rubbi, I Lucas, BJ Brewer and M Grunstein. (2002). Histone acetylation regulates the time of replication origin firing. Mol Cell 10:1223-1233.
96. Lagger G, D O'Carroll, M Rembold, H Khier, J Tischler, G Weitzer, B Schuettengruber, C Hauser, R Brunmeir, T Jenuwein and C Seiser. (2002). Essential function of histone deacetylase 1 in proliferation control and CDK inhibitor repression. EMBO J 21:2672-2681.
97. Wang Y, T Chen, H Yan, H Qi, C Deng, T Ye, S Zhou and FR Li. (2013). Role of histone deacetylase inhibitors in the aging of human umbilical cord mesenchymal stem cells. J Cell Biochem 114:2231-2239.
98. Villasante A, D Piazzolla, H Li, G Gomez-Lopez, M Djabali and M Serrano. (2011). Epigenetic regulation of Nanog expression by Ezh2 in pluripotent stem cells. Cell Cycle 10:1488-1498.
99. Cakouros D, S Isenmann, L Cooper, A Zannettino, P Anderson, C Glackin and S Gronthos. (2012). Twist-1 induces Ezh2 recruitment regulating histone methylation along the Ink4A/Arf locus in mesenchymal stem cells. Mol Cell Biol 32:1433-1441.
100. So AY, JW Jung, S Lee, HS Kim and KS Kang. (2011). DNA methyltransferase controls stem cell aging by regulating BMI1 and EZH2 through microRNAs. PLoS One 6:e19503.
101. Hupkes M, EP Van Someren, SH Middelkamp, E Piek, EJ Van Zoelen and KJ Dechering. (2011). DNA methylation restricts spontaneous multi-lineage differentiation of mesenchymal progenitor cells, but is stable during growth factor-induced terminal differentiation. Biochim Biophys Acta 1813:839-849.
102. El-Serafi AT, RO Oreffo and HI Roach. (2011). Epigenetic modifiers influence lineage commitment of human bone marrow stromal cells: differential effects of 5-azadeoxycytidine and trichostatin A. Differentiation 81: 35-41.
103. Ezura Y, I Sekiya, H Koga, T Muneta and M Noda. (2009). Methylation status of CpG islands in the promoter regions of signature genes during chondrogenesis of human synovium-derived mesenchymal stem cells. Arthritis Rheum 60:1416-1426.
104. Kim SY and GI Im. (2011). The expressions of the SOX trio, PTHrP (parathyroid hormone-related peptide)/IHH (Indian hedgehog protein) in surgically induced osteoarthritis of the rat. Cell Biol Int 35:529-535.
105. Chen J, H Liu, J Liu, J Qi, B Wei, J Yang, H Liang, Y Chen, J Chen, et al. (2013). H3K9 methylation is a barrier during somatic cell reprogramming into iPSCs. Nat Genet 45:34-42.
106. Rodova M, Q Lu, Y Li, BG Woodbury, JD Crist, BM Gardner, JG Yost, XB Zhong, HC Anderson and J Wang. (2011). Nfat1 regulates adult articular chondrocyte function through its age-dependent expression mediated by epigenetic histone methylation. J Bone Miner Res 26: 1974-1986.
107. Spaapen F, GG van den Akker, MM Caron, P Prickaerts, C Rofel, VE Dahlmans, DA Surtel, Y Paulis, F Schweizer, et al. (2013). The immediate early gene product EGR1 and polycomb group proteins interact in epigenetic programming during chondrogenesis. PLoS One 8:e58083.
108. Furumatsu T, M Tsuda, K Yoshida, N Taniguchi, T Ito, M Hashimoto, T Ito and H Asahara. (2005). Sox9 and p300 cooperatively regulate chromatin-mediated transcription. J Biol Chem 280:35203-35208.
109. Zimmermann P, S Boeuf, A Dickhut, S Boehmer, S Olek and W Richter. (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.
110. Ideno H, A Shimada, K Imaizumi, H Kimura, M Abe, K Nakashima and A Nifuji. (2013). Predominant expression of H3K9 methyltransferases in prehypertrophic and hypertrophic chondrocytes during mouse growth plate cartilage development. Gene Expr Patterns 13:84-90.
111. Vega RB, K Matsuda, J Oh, AC Barbosa, X Yang, E Meadows, J McAnally, C Pomajzl, JM Shelton, et al. (2004). Histone deacetylase 4 controls chondrocyte hypertrophy during skeletogenesis. Cell 119:555-566.
112. Pei M, D Chen, J Li and L Wei. (2009). Histone deacetylase 4 promotes TGF-beta1-induced synovium-derived stem cell chondrogenesis but inhibits chondrogenically differentiated stem cell hypertrophy. Differentiation 78: 260-268.
113. Guan Y, Q Chen, X Yang, P Haines, M Pei, R Terek, X Wei, T Zhao and L Wei. (2012). Subcellular relocation of histone deacetylase 4 regulates growth plate chondrocyte differentiation through Ca2 + /calmodulindependent kinase IV. Am J Physiol Cell Physiol 303: C33-C40.
114. Henikoff S. (2008). Nucleosome destabilization in the epigenetic regulation of gene expression. Nat Rev Genet 9:15-26.
115. Dorn ES and JG Cook. (2011). Nucleosomes in the neighborhood: New roles for chromatin modifications in replication origin control. Epigenetics 6:552-559.
116. Struhl K and E Segal. (2013). Determinants of nucleosome positioning. Nat Struct Mol Biol 20:267-273.
117. Herbig U, WA Jobling, BP Chen, DJ Chen and JM Sedivy. (2004). Telomere shortening triggers senescence of Human Cells through a Pathway Involving ATM, p53, and p21(CIP1), but Not p16(INK4a). Mol Cell 14:501-513.
118. Wang S, C Hu and J Zhu. (2010). Distinct and temporal roles of nucleosomal remodeling and histone deacetylation in the repression of the hTERT gene. Mol Biol Cell 21:821-832.
119. Teif VB, Y Vainshtein, M Caudron-Herger, JP Mallm, C Marth, T Höfer and K Rippe. (2012). Genome-wide nucleosome positioning during embryonic stem cell development. Nat Struct Mol Biol 19:1185-1192.
120. Badylak SF, DJ Weiss, A Caplan and P Macchiarini. (2012). Engineered whole organs and complex tissues. Lancet 379:943-952.
121. Benders KE, PR van Weeren, SF Badylak, DB Saris, WJ Dhert and J Malda. (2013). Extracellular matrix scaffolds for cartilage and bone regeneration. Trends Biotechnol 31:169-176.
122. Yang Q, J Peng, Q Guo, J Huang, L Zhang, J Yao, F Yang, S Wang, W Xu, A Wang and S Lu. (2008). A cartilage ECM-derived 3-D porous acellular matrix scaffold for in vivo cartilage tissue engineering with PKH26- labeled chondrogenic bone marrow-derived mesenchymal stem cells. Biomaterials 29:2378-2387.
123. Cole BJ, J Farr, CS Winalski, T Hosea, J Richmond, B Mandelbaum and PG De Deyne. (2011). Outcomes after a single-stage procedure for cell-based cartilage repair: a prospective clinical safety trial with 2-year follow-up. Am J Sports Med 39:1170-1179.
124. Kang H, J Peng, S Lu, S Liu, L Zhang, J Huang, X Sui, B Zhao, A Wang, et al. (2012). In vivo cartilage repair using adipose-derived stem cell-loaded decellularized cartilage ECM scaffolds. J Tissue Eng Regen Med DOI: 10.1002/ term.1538
125. Pei M, JT Li, M Shoukry and Y Zhang. (2011). A review of decellularized stem cell matrix: a novel cell expansion system for cartilage tissue engineering. Eur Cell Mater 22:333-343; discussion 343.
126. Lin H, G Yang, J Tan and RS Tuan. (2012). Influence of decellularized matrix derived from human mesenchymal stem cells on their proliferation, migration and multi-lineage differentiation potential. Biomaterials 33:4480-4489.
127. Jones BA and M Pei. (2012). Synovium-derived stem cells: a tissue-specific stem cell for cartilage engineering and regeneration. Tissue Eng Part B Rev 18:301-311.
128. Li J and M Pei (2011). Optimization of an in vitro threedimensional microenvironment to reprogram synoviumderived stem cells for cartilage tissue engineering. Tissue Eng Part A 17:703-712.
129. He F, X Chen and M Pei. (2009). Reconstruction of an in vitro tissue-specific microenvironment to rejuvenate synovium-derived stem cells for cartilage tissue engineering. Tissue Eng Part A 15:3809-3821.
130. Pei M, Y Zhang, J Li and D Chen. (2013). Antioxidation of decellularized stem cell matrix promotes human synovium- derived stem cell-based chondrogenesis. Stem Cells Dev 22:889-900.
131. Pei M, F He and VL Kish. (2011). Expansion on extracellular matrix deposited by human bone marrow stromal cells facilitates stem cell proliferation and tissue-specific lineage potential. Tissue Eng Part A 17:3067-3076.
132. Pei M and F He. (2012). Extracellular matrix deposited by synovium-derived stem cells delays replicative senescent chondrocyte dedifferentiation and enhances redifferentiation. J Cell Physiol 227:2163-2174.
133. Pei M, F He and L Wei. (2011). Three-dimensional cell expansion substrate for cartilage tissue engineering and regeneration: a comparison in decellularized matrix deposited by synovium-derived stem cells and chondrocytes. J Tissue Sci Eng 2:104.
134. Pei M, M Shoukry, J Li, SD Daffner, JC France and SE Emery. (2012). Modulation of in vitro microenvironment facilitates synovium-derived stem cell-based nucleus pulposus tissue regeneration. Spine (Phila Pa 1976) 37:1538-1547.
135. He F and M Pei. (2012). Rejuvenation of nucleus pulposus cells using extracellular matrix deposited by synoviumderived stem cells. Spine (Phila Pa 1976) 37:459-469.
136. Li J, KC Hansen, Y Zhang, C Dong, CZ Dinu, M Dzieciatkowska and M Pei. (2014). Rejuvenation of chondrogenic potential in a young stem cell microenvironment. Biomaterials 35:642-653.
137. Pei M, F He, J Li, JE Tidwell, AC Jones and EB McDonough. (2013). Repair of large animal partialthickness cartilage defects through intraarticular injection of matrix-rejuvenated synovium-derived stem cells. Tissue Eng Part A 19:1144-1154.
138. Li J, F He and M Pei. (2011). Creation of an in vitro microenvironment to enhance human fetal synovium- derived stem cell chondrogenesis. Cell Tissue Res 345: 357-365.
139. Choi HR, KA Cho, HT Kang, J Bin Lee, M Kaeberlein, Y Suh, IK Chung and SC Park. (2011). Restoration of senescent human diploid fibroblasts by modulation of the extracellular matrix. Aging Cell 10:148-157.
140. Hong E and AH Reddi. (2012). MicroRNAs in chondrogenesis, articular cartilage, and osteoarthritis: implications for tissue engineering. Tissue Eng Part B Rev 18: 445-453.
141. Buechli ME, J Lamarre and TG Koch. (2013). Micro- RNA-140 expression during chondrogenic differentiation of equine cord blood-derived mesenchymal stromal cells. Stem Cells Dev 22:1288-1296.
142. Miyaki S, T Sato, A Inoue, S Otsuki, Y Ito, S Yokoyama, Y Kato, F Takemoto, T Nakasa, et al. (2010). MicroRNA- 140 plays dual roles in both cartilage development and homeostasis. Genes Dev 24:1173-1185.
143. Karlsen TA, RB Jakobsen, TS Mikkelsen and JE Brinchmann. (2013). microRNA-140 targets RALA and regulates chondrogenic differentiation of human mesenchymal stem cells by translational enhancement of SOX9 and ACAN. Stem Cells Dev 23:290-304.
144. Yang B, H Guo, Y Zhang, L Chen, D Ying and S Dong. (2011). MicroRNA-145 regulates chondrogenic differentiation of mesenchymal stem cells by targeting Sox9. PLoS One 6:e21679.
145. Martinez-Sanchez A, KA Dudek and CL Murphy. (2012). Regulation of human chondrocyte function through direct inhibition of cartilage master regulator SOX9 by micro- RNA-145 (miRNA-145). J Biol Chem 287:916-924.
146. Paik S, HS Jung, S Lee, DS Yoon, MS Park and JW Lee. (2012). miR-449a regulates the chondrogenesis of human mesenchymal stem cells through direct targeting of lymphoid enhancer-binding factor-1. Stem Cells Dev 21: 3298-3308.
147. De Andrés MC, E Kingham, K Imagawa, A Gonzalez, HI Roach, DI Wilson and RO Oreffo. (2013). Epigenetic regulation during fetal femur development: DNA methylation matters. PLoS One 8:e54957.
148. Van den Berg WB. (2011). Osteoarthritis year 2010 in review: pathomechanisms. Osteoarthritis Cartilage 19: 338-341.
149. Loughlin J. (2005). The genetic epidemiology of human primary osteoarthritis: current status. Expert Rev Mol Med 7:1-12.
150. Reynard LN and J Loughlin. (2013). The genetics and functional analysis of primary osteoarthritis susceptibility. Expert Rev Mol Med 15:e2.
151. Fraga MF and M Esteller. (2007). Epigenetics and aging: the targets and the marks. Trends Genet 23:413-418.
152. Skinner MK, M Manikkam and C Guerrero-Bosagna. (2010). Epigenetic transgenerational actions of environmental factors in disease etiology. Trends Endocrinol Metab 21:214-222.
153. Im G and Y Choi. (2013). Epigenetics in osteoarthritis and its implication for future therapeutics. Expert Opin Biol Ther 13:713-721.
154. Miyaki S and H Asahara. (2012). Macro view of micro- RNA function in osteoarthritis. Nat Rev Rheumatol 8: 543-552.
155. Goldring MB and KB Marcu. (2012). Epigenomic and microRNA- mediated regulation in cartilage development, homeostasis, and osteoarthritis. Trends Mol Med 18:109-118.
156. Tuddenham L, G Wheeler, S Ntounia-Fousara, J Waters, MK Hajihosseini, I Clark and T Dalmay. (2006). The cartilage specific microRNA-140 targets histone deacetylase 4 in mouse cells. FEBS Lett 580:4214-4217.
157. Akhtar N, Z Rasheed, S Ramamurthy, AN Anbazhagan, FR Voss and TM Haqqi. (2010). MicroRNA-27b regulates the expression of matrix metalloproteinase 13 in human osteoarthritis chondrocytes. Arthritis Rheum 62:1361-1371.
158. Santini P, L Politi, PD Vedova, R Scandurra and A Scotto d'Abusco. (2013). The inflammatory circuitry of miR-149 as a pathological mechanism in osteoarthritis. Rheumatol Int DOI: 10.1007/s00296-013-2754-8.
159. Dvir-Ginzberg M, V Gagarina, EJ Lee, R Booth, O Gabay and DJ Hall. (2011). Tumor necrosis factor a-mediated cleavage and inactivation of SirT1 in human osteoarthritic chondrocytes. Arthritis Rheum 63:2363-2373.
160. Gabay O and C Sanchez. (2012). Epigenetics, sirtuins and osteoarthritis. Joint Bone Spine 79:570-573.
161. Gabay O, H Oppenhiemer, H Meir, K Zaal, C Sanchez and M Dvir-Ginzberg. (2012). Increased apoptotic chondrocytes in articular cartilage from adult heterozygous SirT1 mice. Ann Rheum Dis 71:613-616.
162. Elmali N, I Esenkaya, A Harma, K Ertem, Y Turkoz and B Mizrak. (2005).
163. Eo SH, H Cho and SJ Kim. (2013). Resveratrol inhibits nitric oxide-induced apoptosis via the NF-kappa B pathway in rabbit articular chondrocytes. Biomol Ther (Seoul) 21:364-370.
164. Yuan HF, C Zhai, XL Yan, DD Zhao, JX Wang, Q Zeng, L Chen, X Nan, LJ He, et al. (2012). SIRT1 is required for long-term growth of human mesenchymal stem cells. J Mol Med (Berl) 90:389-400.
165. Im HJ, X Li, D Chen, D Yan, J Kim, MB Ellman, GS Stein, B Cole, R Kc, G Cs-Szabo and AJ van Wijnen. (2012). Biological effects of the plant-derived polyphenol resveratrol in human articular cartilage and chondrosarcoma cells. J Cell Physiol 227:3488-3497.
166. Shakibaei M, T John, C Seifarth and A Mobasheri. (2007). Resveratrol inhibits IL-1 beta-induced stimulation of caspase-3 and cleavage of PARP in human articular chondrocytes in vitro. Ann N Y Acad Sci 1095:554-563.
167. Sheu SY, WS Chen, JS Sun, FH Lin and T Wu. (2013). Biological characterization of oxidized hyaluronic acid/ resveratrol hydrogel for cartilage tissue engineering. J Biomed Mater Res A 101:3457-3466.
168. Volk SW, AS Kapatkin, ME Haskins, RM Walton and M D'Angelo. (2003). Gelatinase activity in synovial fluid and synovium obtained from healthy and osteoarthritic joints of dogs. Am J Vet Res 64:1225-1233.
169. Labrie M and Y St-Pierre. (2013). Epigenetic regulation of mmp-9 gene expression. Cell Mol Life Sci 70:3109-3124.
170. Bui C, MJ Barter, JL Scott, Y Xu, M Galler, LN Reynard, AD Rowan and DA Young. (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.
171. Imagawa K, MC de Andrés, K Hashimoto, D Pitt, E Itoi, MB Goldring, HI Roach and RO Oreffo. (2011). The epigenetic effect of glucosamine and a nuclear factor-kappa B (NF-κB) inhibitor on primary human chondrocytes-implications for osteoarthritis. Biochem Biophys Res Commun 405:362-367.
172. Klein K, C Ospelt and S Gay. (2012). Epigenetic contributions in the development of rheumatoid arthritis. Arthritis Res Ther 14:227.
173. Duroux-richard I, C Jorgensen and F Apparailly. (2012). What do microRNAs mean for rheumatoid arthritis? Arthritis Rheum 64:11-20.
174. Ammari M, C Jorgensen and F Apparailly. (2013). Impact of microRNAs on the understanding and treatment of rheumatoid arthritis. Curr Opin Rheumatol 25:225-233.
175. Stanczyk J, C Ospelt, E Karouzakis, A Filer, K Raza, C Kolling, R Gay, CD Buckley, PP Tak, S Gay and D Kyburz. (2011). Altered expression of microRNA-203 in rheumatoid arthritis synovial fibroblasts and its role in fibroblast activation. Arthritis Rheum 63:373-381.
176. Stanczyk J, DM Pedrioli, F Brentano, O Sanchez- Pernaute, C Kolling, RE Gay, M Detmar, S Gay and D Kyburz. (2008). Altered expression of MicroRNA in synovial fibroblasts and synovial tissue in rheumatoid arthritis. Arthritis Rheum 58:1001-1009.
177. Ceribelli A, MA Nahid, M Satoh and EK Chan. (2011). MicroRNAs in rheumatoid arthritis. FEBS Lett 585:3667-3674.
178. Miao C, Y Yang, X He, T Xu, C Huang, Y Huang, L Zhang, XW Lv, Y Jin and J Li. (2013). New advances of microRNAs in the pathogenesis of rheumatoid arthritis, with a focus on the crosstalk between DNA methylation and the microRNA machinery. Cell Signal 25:1118-1125.
179. Nakano K, DL Boyle and GS Firestein. (2013). Regulation of DNA methylation in rheumatoid arthritis synoviocytes. J Immunol 190:1297-1303.
180. Nakano K, JW Whitaker, DL Boyle, W Wang and GS Firestein. (2013). DNA methylome signature in rheumatoid arthritis. Ann Rheum Dis 72:110-117.
181. Karouzakis E, RE Gay, BA Michel, S Gay and M Neidhart. (2009). DNA hypomethylation in rheumatoid arthritis synovial fibroblasts. Arthritis Rheum 60:3613-3622.
182. Ballestar E. (2011). Epigenetic alterations in autoimmune rheumatic diseases. Nat Rev Rheumatol 7:263-271.
183. De la Rica L, JM Urquiza, D Gómez-Cabrero, AB Islam, N López-Bigas, J Tegnér, RE Toes and E Ballestar. (2013). Identification of novel markers in rheumatoid arthritis through integrated analysis of DNA methylation and microRNA expression. J Autoimmun 41:6-16.
184. Niederer F, C Ospelt, F Brentano, MO Hottiger, RE Gay, S Gay, M Detmar and D Kyburz. (2011). SIRT1 overexpression in the rheumatoid arthritis synovium contributes to proinflammatory cytokine production and apoptosis resistance. Ann Rheum Dis 70:1866-1873.
185. Klein K and S Gay. (2013). Epigenetic modifications in rheumatoid arthritis, a review. Curr Opin Pharmacol 13: 420-425.