Review: The role of microRNAs in osteoarthritis and chondrogenesis

Arthritis and Rheumatism

Volumn 65, Issue 8, 2013, Pages 1963-1974

  Le, Linh T T ^a   Swingler, Tracey E ^a   Clark, Ian M ^a  

^a UNIVERSITY OF EAST ANGLIA   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AGGRECAN; ASPARTYL AMINOPEPTIDASE; COLLAGEN; COLLAGENASE 3; DICER; FIBRONECTIN; HYALURONIC ACID; HYPOXIA INDUCIBLE FACTOR 1ALPHA; INTERLEUKIN 1 RECEPTOR ASSOCIATED KINASE 1; MICRORNA; MICRORNA 124A; MICRORNA 145; MICRORNA 146A; MICRORNA 199A; MICRORNA 210; MICRORNA 96; PROTEOGLYCAN; SOMATOMEDIN BINDING PROTEIN 5; TRANSCRIPTION FACTOR RUNX2; TRANSCRIPTION FACTOR SOX5; TRANSCRIPTION FACTOR SOX9; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 6; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; ARTICULAR CARTILAGE; BONE DEVELOPMENT; CARTILAGE CELL; CARTILAGE DEGENERATION; CELL DEDIFFERENTIATION; CHONDROGENESIS; DOWN REGULATION; EMBRYO DEVELOPMENT; GENE FUNCTION; GENE OVEREXPRESSION; INFLAMMATION; MECHANOTRANSDUCTION; OSTEOARTHRITIS; PATHOGENESIS; PRIORITY JOURNAL; REVIEW; RHEUMATOID ARTHRITIS;

ANIMALS; CHONDROCYTES; CHONDROGENESIS; GENE EXPRESSION REGULATION; HUMANS; MECHANOTRANSDUCTION, CELLULAR; MICE; MICRORNAS; OSTEOARTHRITIS; RATS; WEIGHT-BEARING;

EID: 84881343888     PISSN: 00043591     EISSN: 15290131     Source Type: Journal    
DOI: 10.1002/art.37990     Document Type: Review

References (103)

1. Umlauf D, Frank S, Pap T, Bertrand J,. Cartilage biology, pathology, and repair. Cell Mol Life Sci 2010; 67: 4197-211.
2. Goldring M, Tsuchimochi K, Ijiri K,. The control of chondrogenesis. J Cell Biochem 2006; 97: 33-44.
3. Ikeda T, Kamekura S, Mabuchi A, Kou I, Seki S, Takato T, et al. The combination of SOX5, SOX6, and SOX9 (the SOX trio) provides signals sufficient for induction of permanent cartilage. Arthritis Rheum 2004; 50: 3561-73.
4. Barter MJ, Bui C, Young DA,. Epigenetic mechanisms in cartilage and osteoarthritis: DNA methylation, histone modifications and microRNAs. Osteoarthritis Cartilage 2012; 20: 339-49.
5. Loeser RF, Goldring SR, Scanzello CR, Goldring MB,. Osteoarthritis: a disease of the joint as an organ [review]. Arthritis Rheum 2012; 64: 1697-707.
6. Miyaki S, Asahara H,. Macro view of microRNA function in osteoarthritis. Nat Rev Rheumatol 2012; 8: 543-52.
7. Lin L, Shen Q, Zhang C, Chen L, Yu C,. Assessment of the profiling microRNA expression of differentiated and dedifferentiated human adult articular chondrocytes. J Orthop Res 2011; 29: 1578-84.
8. Miyaki S, Nakasa T, Otsuki S, Grogan SP, Higashiyama R, Inoue A, et al. MicroRNA-140 is expressed in differentiated human articular chondrocytes and modulates interleukin-1 responses. Arthritis Rheum 2009; 60: 2723-30.
9. Tuddenham L, Wheeler G, Ntounia-Fousara S, Waters J, Hajihosseini M, Clark I, et al. The cartilage specific microRNA-140 targets histone deacetylase 4 in mouse cells. FEBS Lett 2006; 580: 4214-7.
10. Miyaki S, Sato T, Inoue A, Otsuki S, Ito Y, Yokoyama S, et al. MicroRNA-140 plays dual roles in both cartilage development and homeostasis. Genes Dev 2010; 24: 1173-85.
11. Nakamura Y, Inloes J, Katagiri T, Kobayashi T,. Chondrocyte-specific microRNA-140 regulates endochondral bone development and targets Dnpep to modulate bone morphogenetic protein signaling. Mol Cell Biol 2011; 31: 3019-28.
12. Swingler TE, Wheeler G, Carmont V, Elliott HR, Barter MJ, Abu-Elmagd M, et al. The expression and function of microRNAs in chondrogenesis and osteoarthritis. Arthritis Rheum 2012; 64: 1909-19.
13. Goldring MB, Marcu KB,. Epigenomic and microRNA-mediated regulation in cartilage development, homeostasis, and osteoarthritis. Trends Mol Med 2012; 18: 109-18.
14. Chalfie M,. Mutations that lead to reiterations in the cell lineages of C. elegans. Cell 1981; 24: 59-69.
15. Lee RC, Feinbaum RL, Ambros V,. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 1993; 75: 843-54.
16. Wightman B, Ha I, Ruvkun G,. Posttranscriptional regulation of the heterochronic gene lin-14 by lin-4 mediates temporal pattern formation in C. elegans. Cell 1993; 75: 855-62.
17. Reinhart BJ, Slack FJ, Basson M, Pasquinelli AE, Bettinger JC, Rougvie AE, et al. The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans. Nature 2000; 403: 901-6.
18. Lagos-Quintana M, Rauhut R, Lendeckel W, Tuschl T,. Identification of novel genes coding for small expressed RNAs. Science 2001; 294: 853-8.
19. Lau NC, Lim LP, Weinstein EG, Bartel DP,. An abundant class of tiny RNAs with probable regulatory roles in Caenorhabditis elegans. Science 2001; 294: 858-62.
20. Lee R, Ambros V,. An extensive class of small RNAs in Caenorhabditis elegans. Science 2001; 294: 862-4.
21. Bartel DP,. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 2004; 116: 281-97.
22. Kozomara A, Griffiths-Jones S,. miRBase: integrating microRNA annotation and deep-sequencing data. Nucleic Acids Res 2011; 39: D152-7.
23. Friedman RC, Farh KK, Burge CB, Bartel DP,. Most mammalian mRNAs are conserved targets of microRNAs. Genome Res 2009; 19: 92-105.
24. Chen C, Ridzon DA, Broomer AJ, Zhou Z, Lee DH, Nguyen JT, et al. Real-time quantification of microRNAs by stem-loop RT-PCR. Nucleic Acids Res 2005; 33: e179.
25. Inui M, Martello G, Piccolo S,. MicroRNA control of signal transduction. Nat Rev Mol Cell Biol 2010; 11: 252-63.
26. Rodriguez A, Griffiths-Jones S, Ashurst J, Bradley A,. Identification of mammalian microRNA host genes and transcription units. Genome Res 2004; 14: 1902-10.
27. Lee Y, Jeon K, Lee JT, Kim S, Kim VN,. MicroRNA maturation: stepwise processing and subcellular localization. EMBO J 2002; 21: 4663-70.
28. Lee Y, Kim M, Han J, Yeom KH, Lee S, Baek SH, et al. MicroRNA genes are transcribed by RNA polymerase II. EMBO J 2004; 23: 4051-60.
29. Cai X, Hagedorn C, Cullen B,. Human microRNAs are processed from capped, polyadenylated transcripts that can also function as mRNAs. RNA 2004; 10: 1957-66.
30. Han J, Lee Y, Yeom KH, Kim YK, Jin H, Kim VN,. The Drosha-DGCR8 complex in primary microRNA processing. Genes Dev 2004; 18: 3016-27.
31. Lund E, Guttinger S, Calado A, Dahlberg J, Kutay U,. Nuclear export of microRNA precursors. Science 2004; 303: 95-8.
32. Chendrimada T, Gregory R, Kumaraswamy E, Norman J, Cooch N, Nishikura K, et al. TRBP recruits the Dicer complex to Ago2 for microRNA processing and gene silencing. Nature 2005; 436: 740-4.
33. Hutvagner G, Simard M,. Argonaute proteins: key players in RNA silencing. Nat Rev Mol Cell Biol 2008; 9: 22-32.
34. Khvorova A, Reynolds A, Jayasena S,. Functional siRNAs and miRNAs exhibit strand bias. Cell 2003; 115: 209-16.
35. Ro S, Park C, Young D, Sanders K, Yan W,. Tissue-dependent paired expression of miRNAs. Nucleic Acids Res 2007; 35: 5944-53.
36. Lai E,. Micro RNAs are complementary to 3′ UTR sequence motifs that mediate negative post-transcriptional regulation. Nat Genet 2002; 30: 363-4.
37. Sibley CR, Seow Y, Saayman S, Dijkstra KK, El Andaloussi S, Weinberg MS, et al. The biogenesis and characterization of mammalian microRNAs of mirtron origin. Nucleic Acids Res 2012; 40: 438-48.
38. Lau PW, MacRae I,. The molecular machines that mediate microRNA maturation. J Cell Mol Med 2009; 13: 54-60.
39. Lytle JR, Yario TA, Steitz JA,. Target mRNAs are repressed as efficiently by microRNA-binding sites in the 5′ UTR as in the 3′ UTR. Proc Natl Acad Sci U S A 2007; 104: 9667-72.
40. Brennecke J, Stark A, Russell R, Cohen S,. Principles of microRNA-target recognition. PLoS Biol 2005; 3: e85.
41. Fabian MR, Sonenberg N, Filipowicz W,. Regulation of mRNA translation and stability by microRNAs. Ann Rev Biochem 2010; 79: 351-79.
42. Vasudevan S, Tong Y, Steitz J,. Switching from repression to activation: microRNAs can up-regulate translation. Science 2007; 318: 1931-4.
43. Vasudevan S, Steitz JA,. AU-rich-element-mediated upregulation of translation by FXR1 and Argonaute 2. Cell 2007; 128: 1105-18.
44. Harfe BD, McManus MT, Mansfield JH, Hornstein E, Tabin CJ,. The RNaseIII enzyme Dicer is required for morphogenesis but not patterning of the vertebrate limb. Proc Natl Acad Sci U S A 2005; 102: 10898-903.
45. Kobayashi T, Lu J, Cobb B, Rodda S, McMahon A, Schipani E, et al. Dicer-dependent pathways regulate chondrocyte proliferation and differentiation. Proc Natl Acad Sci U S A 2008; 105: 1949-54.
46. Wienholds E, Koudijs MJ, van Eeden FJ, Cuppen E, Plasterk RH,. The microRNA-producing enzyme Dicer1 is essential for zebrafish development. Nat Genet 2003; 35: 217-8.
47. Sorrentino A, Ferracin M, Castelli G, Biffoni M, Tomaselli G, Baiocchi M, et al. Isolation and characterization of CD146+ multipotent mesenchymal stromal cells. Exp Hematol 2008; 36: 1035-46.
48. Suomi S, Taipaleenmaki H, Seppanen A, Ripatti T, Vaananen K, Hentunen T, et al. MicroRNAs regulate osteogenesis and chondrogenesis of mouse bone marrow stromal cells. Gene Regul Syst Bio 2008; 2: 177-91.
49. Lin E, Kong L, Bai XH, Luan Y, Liu CJ,. miR-199a, a bone morphogenic protein 2-responsive MicroRNA, regulates chondrogenesis via direct targeting to Smad1. J Biol Chem 2009; 284: 11326-35.
50. Yang B, Guo H, Zhang Y, Dong S, Ying D,. The microRNA expression profiles of mouse mesenchymal stem cell during chondrogenic differentiation. BMB Rep 2011; 44: 28-33.
51. Yan C, Wang Y, Shen XY, Yang G, Jian J, Wang HS, et al. MicroRNA regulation associated chondrogenesis of mouse MSCs grown on polyhydroxyalkanoates. Biomaterials 2011; 32: 6435-44.
52. Karlsen TA, Shahdadfar A, Brinchmann JE,. Human primary articular chondrocytes, chondroblast-like cells, and dedifferentiated chondrocytes: differences in gene, microRNA, and protein expression and phenotype. Tissue Eng Part C Methods 2011; 17: 219-27.
53. Yang B, Guo H, Zhang Y, Chen L, Ying D, Dong S,. MicroRNA-145 regulates chondrogenic differentiation of mesenchymal stem cells by targeting Sox9. PLoS One 2011; 6: e21679.
54. Martinez-Sanchez A, Dudek K, Murphy C,. Regulation of human chondrocyte function through direct inhibition of cartilage master regulator SOX9 by microRNA-145 (miRNA-145). J Biol Chem 2012; 287: 916-24.
55. Dudek K, Lafont J, Martinez-Sanchez A, Murphy C,. Type II collagen expression is regulated by tissue-specific miR-675 in human articular chondrocytes. J Biol Chem 2010; 285: 24381-7.
56. Nicolas FE, Pais H, Schwach F, Lindow M, Kauppinen S, Moulton V, et al. Experimental identification of microRNA-140 targets by silencing and overexpressing miR-140. RNA 2008; 14: 2513-20.
57. Pais H, Nicolas FE, Soond SM, Swingler TE, Clark IM, Chantry A, et al. Analyzing mRNA expression identifies Smad3 as a microRNA-140 target regulated only at protein level. RNA 2010; 16: 489-94.
58. Yamashita S, Miyaki S, Kato Y, Yokoyama S, Sato T, Barrionuevo F, et al. L-Sox5 and Sox6 proteins enhance chondrogenic miR-140 microRNA expression by strengthening dimeric Sox9 activity. J Biol Chem 2012; 287: 22206-15.
59. Yang J, Qin S, Yi C, Ma G, Zhu H, Zhou W, et al. MiR-140 is co-expressed with Wwp2-C transcript and activated by Sox9 to target Sp1 in maintaining the chondrocyte proliferation. FEBS Lett 2011; 585: 2992-7.
60. Xu J, Kang Y, Liao WM, Yu L,. MiR-194 regulates chondrogenic differentiation of human adipose-derived stem cells by targeting Sox5. PLoS One 2012; 7: e31861.
61. Zhong N, Sun J, Min Z, Zhao W, Zhang R, Wang W, et al. MicroRNA-337 is associated with chondrogenesis through regulating TGFBR2 expression. Osteoarthritis Cartilage 2012; 20: 593-602.
62. Kim D, Song J, Kim S, Chun CH, Jin EJ,. MicroRNA-34a regulates migration of chondroblast and IL-1β-induced degeneration of chondrocytes by targeting EphA5. Biochem Biophys Res Commun 2011; 415: 551-7.
63. Kim D, Song J, Jin EJ,. MicroRNA-221 regulates chondrogenic differentiation through promoting proteosomal degradation of Slug by targeting Mdm2. J Biol Chem 2010; 285: 26900-7.
64. Kim D, Song J, Kim S, Chun CH, Sonn J, Jin EJ,. MicroRNA-34a modulates cytoskeletal dynamics through regulating RhoA/Rac1 crosstalk in chondroblasts. J Biol Chem 2012; 287: 12501-9.
65. Song J, Kim D, Jin EJ,. MicroRNA-488 suppresses cell migration through modulation of the focal adhesion activity during chondrogenic differentiation of chick limb mesenchymal cells. Cell Biol Int 2011; 35: 179-85.
66. Kim D, Song J, Kim S, Kang SS, Jin EJ,. MicroRNA-142-3p regulates TGF-β3-mediated region-dependent chondrogenesis by regulating ADAM9. Biochem Biophys Res Commun 2011; 414: 653-9.
67. Iliopoulos D, Malizos K, Oikonomou P, Tsezou A,. Integrative microRNA and proteomic approaches identify novel osteoarthritis genes and their collaborative metabolic and inflammatory networks. PLoS One 2008; 3: e3740.
68. Jones SW, Watkins G, Le Good N, Roberts S, Murphy CL, Brockbank SM, et al. The identification of differentially expressed microRNA in osteoarthritic tissue that modulate the production of TNF-α and MMP13. Osteoarthritis Cartilage 2009; 17: 464-72.
69. Diaz-Prado S, Cicione C, Muinos-Lopez E, Hermida-Gomez T, Oreiro N, Fernandez-Lopez C, et al. Characterization of microRNA expression profiles in normal and osteoarthritic human chondrocytes. BMC Musculoskelet Disord 2012; 13: 144.
70. Tardif G, Hum D, Pelletier JP, Duval N, Martel-Pelletier J,. Regulation of the IGFBP-5 and MMP-13 genes by the microRNAs miR-140 and miR-27a in human osteoarthritic chondrocytes. BMC Musculoskelet Disord 2009; 10: 148.
71. Liang ZJ, Zhuang H, Wang GX, Li Z, Zhang HT, Yu TQ, et al. MiRNA-140 is a negative feedback regulator of MMP-13 in IL-1β-stimulated human articular chondrocyte C28/I2 cells. Inflamm Res 2012; 61: 503-9.
72. Kim SY, Kim Y, Lee HW, Son YH, Lee GY, Lee JW, et al. miR-27a is a negative regulator of adipocyte differentiation via suppressing PPARγ expression. Biochem Biophys Res Commun 2010; 392: 323-8.
73. Akhtar N, Rasheed Z, Ramamurthy S, Anbazhagan AN, Voss FR, Haqqi TM,. MicroRNA-27b regulates the expression of matrix metalloproteinase 13 in human osteoarthritis chondrocytes. Arthritis Rheum 2010; 62: 1361-71.
74. Yamasaki K, Nakasa T, Miyaki S, Ishikawa M, Deie M, Adachi N, et al. Expression of microRNA-146a in osteoarthritis cartilage. Arthritis Rheum 2009; 60: 1035-41.
75. Li J, Huang J, Dai L, Yu D, Chen Q, Zhang X, et al. miR-146a, an IL-1β responsive miRNA, induces vascular endothelial growth factor and chondrocyte apoptosis by targeting Smad4. Arthritis Res Therapy 2012; 14: R75.
76. Li X, Gibson G, Kim JS, Kroin J, Xu S, van Wijnen AJ, et al. MicroRNA-146a is linked to pain-related pathophysiology of osteoarthritis. Gene 2011; 480: 34-41.
77. Neu CP, Khalafi A, Komvopoulos K, Schmid TM, Reddi AH,. Mechanotransduction of bovine articular cartilage superficial zone protein by transforming growth factor β signaling. Arthritis Rheum 2007; 56: 3706-14.
78. Guan YJ, Yang X, Wei L, Chen Q,. MiR-365: a mechanosensitive microRNA stimulates chondrocyte differentiation through targeting histone deacetylase 4. FASEB J 2011; 25: 4457-66.
79. Dunn W, DuRaine G, Reddi AH,. Profiling microRNA expression in bovine articular cartilage and implications for mechanotransduction. Arthritis Rheum 2009; 60: 2333-9.
80. Berenbaum F,. Osteoarthritis as an inflammatory disease (osteoarthritis is not osteoarthrosis!). Osteoarthritis Cartilage 2013; 21: 16-21.
81. Duroux-Richard I, Jorgensen C, Apparailly F,. What do microRNAs mean for rheumatoid arthritis? [review]. Arthritis Rheum 2012; 64: 11-20.
82. Kurowska-Stolarska M, Alivernini S, Ballantine LE, Asquith DL, Millar NL, Gilchrist DS, et al. MicroRNA-155 as a proinflammatory regulator in clinical and experimental arthritis. Proc Natl Acad Sci U S A 2011; 108: 11193-8.
83. Scanzello CR, Plaas A, Crow MK,. Innate immune system activation in osteoarthritis: is osteoarthritis a chronic wound? Curr Opin Rheumatol 2008; 20: 565-72.
84. Sofat N,. Analysing the role of endogenous matrix molecules in the development of osteoarthritis. Int J Exp Pathol 2009; 90: 463-79.
85. Piccinini AM, Midwood KS,. DAMPening inflammation by modulating TLR signalling. Mediators Inflamm 2010; 672395.
86. Marcu KB, Otero M, Olivotto E, Borzi RM, Goldring MB,. NF-κB signaling: multiple angles to target OA. Curr Drug Targets 2010; 11: 599-613.
87. Hashimoto M, Nakasa T, Hikata T, Asahara H,. Molecular network of cartilage homeostasis and osteoarthritis. Med Res Rev 2008; 28: 464-81.
88. Ceppi M, Pereira PM, Dunand-Sauthier I, Barras E, Reith W, Santos MA, et al. MicroRNA-155 modulates the interleukin-1 signaling pathway in activated human monocyte-derived dendritic cells. Proc Natl Acad Sci U S A 2009; 106: 2735-40.
89. Taganov KD, Boldin MP, Chang KJ, Baltimore D,. NF-κB-dependent induction of microRNA miR-146, an inhibitor targeted to signaling proteins of innate immune responses. Proc Natl Acad Sci U S A 2006; 103: 12481-6.
90. Okuhara A, Nakasa T, Shibuya H, Niimoto T, Adachi N, Deie M, et al. Changes in microRNA expression in peripheral mononuclear cells according to the progression of osteoarthritis. Mod Rheumatol 2012; 22: 446-57.
91. Abouheif M, Nakasa T, Shibuya H, Niimoto T, Kongcharoensombat W, Ochi M,. Silencing microRNA-34a inhibits chondrocyte apoptosis in a rat osteoarthritis model in vitro. Rheumatology (Oxford) 2010; 49: 2054-60.
92. Gilad S, Meiri E, Yogev Y, Benjamin S, Lebanony D, Yerushalmi N, et al. Serum microRNAs are promising novel biomarkers. PLoS One 2008; 3: e3148.
93. Kosaka N, Iguchi H, Ochiya T,. Circulating microRNA in body fluid: a new potential biomarker for cancer diagnosis and prognosis. Cancer Sci 2010; 101: 2087-92.
94. Arroyo JD, Chevillet JR, Kroh EM, Ruf IK, Pritchard CC, Gibson DF, et al. Argonaute2 complexes carry a population of circulating microRNAs independent of vesicles in human plasma. Proc Natl Acad Sci U S A 2011; 108: 5003-8.
95. Lawrie CH, Gal S, Dunlop HM, Pushkaran B, Liggins AP, Pulford K, et al. Detection of elevated levels of tumour-associated microRNAs in serum of patients with diffuse large B-cell lymphoma. Br J Haematol 2008; 141: 672-5.
96. Murata K, Yoshitomi H, Tanida S, Ishikawa M, Nishitani K, Ito H, et al. Plasma and synovial fluid microRNAs as potential biomarkers of rheumatoid arthritis and osteoarthritis. Arthritis Res Ther 2010; 12: R86.
97. Wieland HA, Michaelis M, Kirschbaum BJ, Rudolphi KA,. Osteoarthritis-an untreatable disease? [published erratum appears in Nat Rev Drug Discov 2005;4:543]. Nat Rev Drug Discov 2005; 4: 331-4.
98. Elmen J, Lindow M, Schutz S, Lawrence M, Petri A, Obad S, et al. LNA-mediated microRNA silencing in non-human primates. Nature 2008; 452: 896-9.
99. Kongcharoensombat W, Nakasa T, Ishikawa M, Nakamae A, Deie M, Adachi N, et al. The effect of microRNA-21 on proliferation and matrix synthesis of chondrocytes embedded in atelocollagen gel. Knee Surg Sports Traumatol Arthrosc 2010; 18: 1679-84.
100. ElSharawy A, Keller A, Flachsbart F, Wendschlag A, Jacobs G, Kefer N, et al. Genome-wide miRNA signatures of human longevity. Aging Cell 2012; 11: 607-16.
101. Noren Hooten N, Abdelmohsen K, Gorospe M, Ejiogu N, Zonderman AB, Evans MK,. microRNA expression patterns reveal differential expression of target genes with age. PLoS One 2010; 5: e10724.
102. Olivieri F, Spazzafumo L, Santini G, Lazzarini R, Albertini MC, Rippo MR, et al. Age-related differences in the expression of circulating microRNAs: miR-21 as a new circulating marker of inflammaging. Mech Ageing Dev 2012; 133: 675-85.
103. Litherland GJ, Dixon C, Lakey RL, Robson T, Jones D, Young DA, et al. Synergistic collagenase expression and cartilage collagenolysis are phosphatidylinositol 3-kinase/Akt signaling-dependent. J Biol Chem 2008; 283: 14221-9.