Skip to main content
SpringerLink
Log in

miRNA Regulation of Chondrogenesis

  • MicroRNAs in Skeletal Development (A Delany, Section Editor)
  • Published:
Current Molecular Biology Reports Aims and scope Submit manuscript

Abstract

Purpose of Review

Knowledge of microRNAs (miRNAs) in cartilage biology is constantly expanding. The purpose of this review is to provide a global view on recent findings and to discuss the future direction of miRNA research in cartilage.

Recent Findings

Physiological roles and mechanisms of action of miRNAs in chondrogenesis have been investigated in animal and cell models. In addition to these efforts to understand basic biology, translational research targeting miRNAs in cartilage diseases, particularly osteoarthritis, has become a major research trend in this field. A few recent in vivo findings using genetic models include demonstrations of the interaction between miR-140 and the PTHrP/Hdac4 pathway, genetic dissection of roles of miR-140 and its host gene, the essential role of miR-214 and miR-199b cluster in endochondral development, regulation of TGF-β signaling by miR-17-92 in mesenchymal progenitor cells, and MEK1 regulation by miR-322 miRNA during skeletal development.

Summary

In recent years, translational research to target miRNAs in cartilage disorders has been vigorously pursued, whereas our basic understanding of miRNAs in chondrogenesis in vivo is still rudimentary. A deeper understanding of the basic biology of miRNAs in the skeletal system is necessary to advance the goal of developing therapies targeting miRNAs or miRNA-related pathways.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

Papers of particular interest, published recently, have been highlighted as: •• Of major importance

  1. Kronenberg HM. Developmental regulation of the growth plate. Nature. 2003;423(6937):332–6.

    CAS  Google Scholar 

  2. Bi W, Deng JM, Zhang Z, Behringer RR, de Crombrugghe B. Sox9 is required for cartilage formation. Nat Genet. 1999;22(1):85–9.

    CAS  PubMed  Google Scholar 

  3. Yoshida CA, Yamamoto H, Fujita T, Furuichi T, Ito K, Inoue K, et al. Runx2 and Runx3 are essential for chondrocyte maturation, and Runx2 regulates limb growth through induction of Indian hedgehog. Genes Dev. 2004;18(8):952–63.

    CAS  PubMed  PubMed Central  Google Scholar 

  4. Takeda S, Bonnamy JP, Owen MJ, Ducy P, Karsenty G. Continuous expression of Cbfa1 in nonhypertrophic chondrocytes uncovers its ability to induce hypertrophic chondrocyte differentiation and partially rescues Cbfa1-deficient mice. Genes Dev. 2001;15(4):467–81.

    CAS  PubMed  PubMed Central  Google Scholar 

  5. Arnold MA, Kim Y, Czubryt MP, Phan D, McAnally J, Qi X, et al. MEF2C transcription factor controls chondrocyte hypertrophy and bone development. Dev Cell. 2007;12(3):377–89.

    CAS  PubMed  Google Scholar 

  6. Clocchiatti A, Di Giorgio E, Demarchi F, Brancolini C. Beside the MEF2 axis: unconventional functions of HDAC4. Cell Signal. 2013;25(1):269–76.

    CAS  PubMed  Google Scholar 

  7. Salazar VS, Gamer LW, Rosen V. BMP signalling in skeletal development, disease and repair. Nat Rev Endocrinol. 2016;12(4):203–21.

    CAS  PubMed  Google Scholar 

  8. Chen Z, Yue SX, Zhou G, Greenfield EM, Murakami S. ERK1 and ERK2 regulate chondrocyte terminal differentiation during endochondral bone formation. J Bone Miner Res. 2015;30(5):765–74.

    CAS  PubMed  PubMed Central  Google Scholar 

  9. Papaioannou G, Petit ET, Liu ES, Baccarini M, Pritchard C, Demay MB. Raf kinases are essential for phosphate induction of ERK1/2 phosphorylation in hypertrophic chondrocytes and normal endochondral bone development. J Biol Chem. 2017;292(8):3164–71.

    CAS  PubMed  PubMed Central  Google Scholar 

  10. Spater D, Hill TP, O’Sullivan RJ, Gruber M, Conner DA, Hartmann C. Wnt9a signaling is required for joint integrity and regulation of Ihh during chondrogenesis. Development. 2006;133(15):3039–49.

    PubMed  Google Scholar 

  11. Canalis E. Wnt signalling in osteoporosis: mechanisms and novel therapeutic approaches. Nat Rev Endocrinol. 2013;9(10):575–83.

    CAS  PubMed  Google Scholar 

  12. van Amerongen R. Alternative Wnt pathways and receptors. Cold Spring Harb Perspect Biol. 2012;4(10).

  13. Bartel DP. Metazoan MicroRNAs. Cell. 2018;173(1):20–51.

    CAS  PubMed  Google Scholar 

  14. Kobayashi T, Lu J, Cobb BS, Rodda SJ, McMahon AP, Schipani E, et al. Dicer-dependent pathways regulate chondrocyte proliferation and differentiation. Proc Natl Acad Sci U S A. 2008;105(6):1949–54.

    CAS  PubMed  PubMed Central  Google Scholar 

  15. Kobayashi T, Papaioannou G, Mirzamohammadi F, Kozhemyakina E, Zhang M, Blelloch R, et al. Early postnatal ablation of the microRNA-processing enzyme, Drosha, causes chondrocyte death and impairs the structural integrity of the articular cartilage. Osteoarthr Cartil. 2015;23(7):1214–20.

    CAS  PubMed  PubMed Central  Google Scholar 

  16. Papaioannou G, Inloes JB, Nakamura Y, Paltrinieri E, Kobayashi T. Let-7 and miR-140 microRNAs coordinately regulate skeletal development. Proc Natl Acad Sci U S A. 2013;110(35):E3291–300.

    CAS  PubMed  PubMed Central  Google Scholar 

  17. Watanabe T, Sato T, Amano T, Kawamura Y, Kawamura N, Kawaguchi H, et al. Dnm3os, a non-coding RNA, is required for normal growth and skeletal development in mice. Dev Dyn. 2008;237(12):3738–48.

    CAS  PubMed  Google Scholar 

  18. 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(11):1173–85.

    CAS  PubMed  PubMed Central  Google Scholar 

  19. Nakamura Y, Inloes JB, 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(14):3019–28.

    CAS  PubMed  PubMed Central  Google Scholar 

  20. Mirzamohammadi F, Papaioannou G, Kobayashi T. MicroRNAs in cartilage development, homeostasis, and disease. Curr Osteoporos Rep. 2014;12(4):410–9.

    PubMed  PubMed Central  Google Scholar 

  21. •• Mirzamohammadi F, Kozlova A, Papaioannou G, Paltrinieri E, Ayturk UM, Kobayashi T. Distinct molecular pathways mediate Mycn and Myc-regulated miR-17-92 microRNA action in Feingold syndrome mouse models. Nat Commun. 2018;9(1):1352 This in vivo study revealed the regulation of TGF-β signaling by miR-17-92 in mesenchymal progenitor cells.

    PubMed  PubMed Central  Google Scholar 

  22. •• Papaioannou G, Mirzamohammadi F, Lisse TS, Nishimori S, Wein MN, Kobayashi T. MicroRNA-140 provides robustness to the regulation of hypertrophic chondrocyte differentiation by the PTHrP-HDAC4 pathway. J Bone Miner Res. 2015;30(6):1044–52 This in vivo study showed the interaction of mir140 with the PTHrP/Hdac4/Mef2c pathway to cooperatively regulate chondrocyte hypertrophy.

    CAS  PubMed  PubMed Central  Google Scholar 

  23. •• Bluhm B, Ehlen HWA, Holzer T, Georgieva VS, Heilig J, Pitzler L, et al. miR-322 stabilizes MEK1 expression to inhibit RAF/MEK/ERK pathway activation in cartilage. Development. 2017;144(19):3562–77 This study revealed that MEK1 is regulated by miR-322 miRNA during skeletal development.

    CAS  PubMed  Google Scholar 

  24. •• Roberto VP, Gavaia P, Nunes MJ, Rodrigues E, Cancela ML, Tiago DM. Evidences for a new role of miR-214 in chondrogenesis. Sci Rep. 2018;8(1):3704 This study revealed the in vivo role of miR-214 in zebrafish through a gain-of-function model.

    PubMed  PubMed Central  Google Scholar 

  25. Pala D, Kapoor M, Woods A, Kennedy L, Liu S, Chen S, et al. Focal adhesion kinase/Src suppresses early chondrogenesis: central role of CCN2. J Biol Chem. 2008;283(14):9239–47.

    CAS  PubMed  PubMed Central  Google Scholar 

  26. Ding HL, Hooper JE, Batzel P, Eames BF, Postlethwait JH, Artinger KB, et al. MicroRNA profiling during craniofacial development: potential roles for Mir23b and Mir133b. Front Physiol. 2016;7:281.

    PubMed  PubMed Central  Google Scholar 

  27. de Pontual L, Yao E, Callier P, Faivre L, Drouin V, Cariou S, et al. Germline deletion of the miR-17 approximately 92 cluster causes skeletal and growth defects in humans. Nat Genet. 2011;43(10):1026–30.

    PubMed  PubMed Central  Google Scholar 

  28. Nakamura Y, Yamamoto K, He X, Otsuki B, Kim Y, Murao H, et al. Wwp2 is essential for palatogenesis mediated by the interaction between Sox9 and mediator subunit 25. Nat Commun. 2011;2:251.

    PubMed  PubMed Central  Google Scholar 

  29. Zou W, Chen X, Shim JH, Huang Z, Brady N, Hu D, et al. The E3 ubiquitin ligase Wwp2 regulates craniofacial development through mono-ubiquitylation of Goosecoid. Nat Cell Biol. 2011;13(1):59–65.

    CAS  PubMed  Google Scholar 

  30. •• Inui M, Mokuda S, Sato T, Tamano M, Takada S, Asahara H. Dissecting the roles of miR-140 and its host gene. Nat Cell Biol. 2018;20(5):516–8 This study identified the distinct roles of miR-140 and its host gene.

    CAS  PubMed  Google Scholar 

  31. Catalanotti F, Reyes G, Jesenberger V, Galabova-Kovacs G, de Matos Simoes R, Carugo O, et al. A Mek1-Mek2 heterodimer determines the strength and duration of the Erk signal. Nat Struct Mol Biol. 2009;16(3):294–303.

    CAS  PubMed  Google Scholar 

  32. Kara N, Wei C, Commanday AC, Patton JG. miR-27 regulates chondrogenesis by suppressing focal adhesion kinase during pharyngeal arch development. Dev Biol. 2017;429(1):321–34.

    CAS  PubMed  PubMed Central  Google Scholar 

  33. Kobayashi T, Koslova A. Lin28a overexpression reveals the role of Erk signaling in articular cartilage development. Development. 2018;145(15).

    PubMed  Google Scholar 

  34. Yao Y, Wang Y. ATDC5: an excellent in vitro model cell line for skeletal development. J Cell Biochem. 2013;114(6):1223–9.

    CAS  PubMed  Google Scholar 

  35. Gebauer M, Saas J, Sohler F, Haag J, Soder S, Pieper M, et al. Comparison of the chondrosarcoma cell line SW1353 with primary human adult articular chondrocytes with regard to their gene expression profile and reactivity to IL-1beta. Osteoarthr Cartil. 2005;13(8):697–708.

    CAS  PubMed  Google Scholar 

  36. Haas AR, Tuan RS. Murine C3H10T1/2 multipotential cells as an in vitro model of mesenchymal chondrogenesis. Methods Mol Biol. 2000;137:383–9.

    CAS  PubMed  Google Scholar 

  37. Jee YH, Wang J, Yue S, Jennings M, Clokie SJH, Nilsson O, et al. Mir-374-5p, mir-379-5p, and mir-503-5p regulate proliferation and hypertrophic differentiation of growth plate chondrocytes in male rats. Endocrinology. 2018;159:1469–78.

    Google Scholar 

  38. Hou C, Meng F, Zhang Z, Kang Y, Chen W, Huang G, et al. The role of MicroRNA-381 in chondrogenesis and interleukin-1-beta induced chondrocyte responses. Cell Physiol Biochem. 2015;36(5):1753–66.

    CAS  PubMed  Google Scholar 

  39. Gu YL, Rong XX, Wen LT, Zhu GX, Qian MQ. miR-195 inhibits the proliferation and migration of chondrocytes by targeting GIT1. Mol Med Rep. 2017;15(1):194–200.

    CAS  PubMed  Google Scholar 

  40. Meng F, Zhang Z, Chen W, Huang G, He A, Hou C, et al. MicroRNA-320 regulates matrix metalloproteinase-13 expression in chondrogenesis and interleukin-1beta-induced chondrocyte responses. Osteoarthr Cartil. 2016;24(5):932–41.

    CAS  PubMed  Google Scholar 

  41. Chen W, Chen L, Zhang Z, Meng F, Huang G, Sheng P, et al. MicroRNA-455-3p modulates cartilage development and degeneration through modification of histone H3 acetylation. Biochim Biophys Acta. 2016;1863(12):2881–91.

    CAS  PubMed  Google Scholar 

  42. Anderson BA, McAlinden A. miR-483 targets SMAD4 to suppress chondrogenic differentiation of human mesenchymal stem cells. J Orthop Res. 2017;35(11):2369–77.

    CAS  PubMed  PubMed Central  Google Scholar 

  43. Wu Z, Qiu X, Gao B, Lian C, Peng Y, Liang A, et al. Melatonin-mediated miR-526b-3p and miR-590-5p upregulation promotes chondrogenic differentiation of human mesenchymal stem cells. J Pineal Res. 2018;65:e12483.

    PubMed  Google Scholar 

  44. Yoshizuka M, Nakasa T, Kawanishi Y, Hachisuka S, Furuta T, Miyaki S, et al. Inhibition of microRNA-222 expression accelerates bone healing with enhancement of osteogenesis, chondrogenesis, and angiogenesis in a rat refractory fracture model. J Orthop Sci. 2016;21(6):852–8.

    PubMed  Google Scholar 

  45. Budd E, de Andres MC, Sanchez-Elsner T, Oreffo ROC. MiR-146b is down-regulated during the chondrogenic differentiation of human bone marrow derived skeletal stem cells and up-regulated in osteoarthritis. Sci Rep. 2017;7:46704.

    PubMed  PubMed Central  Google Scholar 

  46. Mao G, Zhang Z, Huang Z, Chen W, Huang G, Meng F, et al. MicroRNA-92a-3p regulates the expression of cartilage-specific genes by directly targeting histone deacetylase 2 in chondrogenesis and degradation. Osteoarthr Cartil. 2017;25(4):521–32.

    CAS  PubMed  Google Scholar 

  47. Mao G, Wu P, Zhang Z, Zhang Z, Liao W, Li Y, et al. MicroRNA-92a-3p regulates Aggrecanase-1 and Aggrecanase-2 expression in chondrogenesis and IL-1beta-induced catabolism in human articular chondrocytes. Cell Physiol Biochem. 2017;44(1):38–52.

    PubMed  Google Scholar 

  48. Wa Q, Liu Y, Huang S, He P, Zuo J, Li X, et al. miRNA-140 inhibits C3H10T1/2 mesenchymal stem cell proliferation by targeting CXCL12 during transforming growth factor-beta3-induced chondrogenic differentiation. Mol Med Rep. 2017;16(2):1389–94.

    CAS  PubMed  Google Scholar 

  49. Barter MJ, Tselepi M, Gomez R, Woods S, Hui W, Smith GR, et al. Genome-wide MicroRNA and gene analysis of mesenchymal stem cell chondrogenesis identifies an essential role and multiple targets for miR-140-5p. Stem Cells. 2015;33(11):3266–80.

    CAS  PubMed  PubMed Central  Google Scholar 

  50. Tian Y, Guo R, Shi B, Chen L, Yang L, Fu Q. MicroRNA-30a promotes chondrogenic differentiation of mesenchymal stem cells through inhibiting delta-like 4 expression. Life Sci. 2016;148:220–8.

    CAS  PubMed  Google Scholar 

  51. Lolli A, Narcisi R, Lambertini E, Penolazzi L, Angelozzi M, Kops N, et al. Silencing of antichondrogenic microRNA-221 in human mesenchymal stem cells promotes cartilage repair in vivo. Stem Cells. 2016;34(7):1801–11.

    CAS  PubMed  Google Scholar 

  52. Xue Z, Meng Y, Ge J. miR-127-5p promotes chondrogenic differentiation in rat bone marrow mesenchymal stem cells. Exp Ther Med. 2017;14(2):1481–6.

    CAS  PubMed  PubMed Central  Google Scholar 

  53. Zhang L, Sun X, Chen S, Yang C, Shi B, Zhou L, et al. Long noncoding RNA DANCR regulates miR-1305-Smad 4 axis to promote chondrogenic differentiation of human synovium-derived mesenchymal stem cells. Biosci Rep. 2017;37(4).

  54. Verbus EA, Kenyon JD, Sergeeva O, Awadallah A, Yuan L, Welter JF, et al. Expression of miR-145-5p during chondrogenesis of mesenchymal stem cells. J Stem Cell Res (Overl Park). 2017;1(3):1–10.

    Google Scholar 

  55. Gong M, Liang T, Jin S, Dai X, Zhou Z, Gao M, et al. Methylation-mediated silencing of miR-124 facilitates chondrogenesis by targeting NFATc1 under hypoxic conditions. Am J Transl Res. 2017;9(9):4111–24.

    PubMed  PubMed Central  Google Scholar 

  56. Chen W, Sheng P, Huang Z, Meng F, Kang Y, Huang G, et al. MicroRNA-381 regulates chondrocyte hypertrophy by inhibiting histone deacetylase 4 expression. Int J Mol Sci. 2016;17(9).

    PubMed Central  Google Scholar 

  57. Xiao J, Chen X, Xu L, Zhang Y, Yin Q, Wang F. PDGF regulates chondrocyte proliferation through activation of the GIT1- and PLCgamma1-mediated ERK1/2 signaling pathway. Mol Med Rep. 2014;10(5):2409–14.

    CAS  PubMed  Google Scholar 

  58. Zhang Z, Hou C, Meng F, Zhao X, Zhang Z, Huang G, et al. MiR-455-3p regulates early chondrogenic differentiation via inhibiting Runx2. FEBS Lett. 2015;589(23):3671–8.

    CAS  PubMed  Google Scholar 

  59. Lin Z, McClure MJ, Zhao J, Ramey AN, Asmussen N, Hyzy SL, et al. MicroRNA contents in matrix vesicles produced by growth plate chondrocytes are cell maturation dependent. Sci Rep. 2018;8(1):3609.

    PubMed  PubMed Central  Google Scholar 

  60. Feng C, Liu M, Fan X, Yang M, Liu H, Zhou Y. Intermittent cyclic mechanical tension altered the microRNA expression profile of human cartilage endplate chondrocytes. Mol Med Rep. 2018;17(4):5238–46.

    CAS  PubMed  PubMed Central  Google Scholar 

  61. Lim J, Tu X, Choi K, Akiyama H, Mishina Y, Long F. BMP-Smad4 signaling is required for precartilaginous mesenchymal condensation independent of Sox9 in the mouse. Dev Biol. 2015;400(1):132–8.

    CAS  PubMed  PubMed Central  Google Scholar 

  62. Zhang J, Tan X, Li W, Wang Y, Wang J, Cheng X, et al. Smad4 is required for the normal organization of the cartilage growth plate. Dev Biol. 2005;284(2):311–22.

    CAS  PubMed  Google Scholar 

  63. Gao W, Lin M, Liang A, Zhang L, Chen C, Liang G, et al. Melatonin enhances chondrogenic differentiation of human mesenchymal stem cells. J Pineal Res. 2014;56(1):62–70.

    CAS  PubMed  Google Scholar 

  64. 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(26):22206–15.

    CAS  PubMed  PubMed Central  Google Scholar 

  65. So AY, Zhao JL, Baltimore D. The Yin and Yang of microRNAs: leukemia and immunity. Immunol Rev. 2013;253(1):129–45.

    PubMed  PubMed Central  Google Scholar 

  66. Nakasa T, Miyaki S, Okubo A, Hashimoto M, Nishida K, Ochi M, et al. Expression of microRNA-146 in rheumatoid arthritis synovial tissue. Arthritis Rheum. 2008;58(5):1284–92.

    CAS  PubMed  PubMed Central  Google Scholar 

  67. Artavanis-Tsakonas S, Rand MD, Lake RJ. Notch signaling: cell fate control and signal integration in development. Science. 1999;284(5415):770–6.

    CAS  PubMed  Google Scholar 

  68. Hosaka Y, Saito T, Sugita S, Hikata T, Kobayashi H, Fukai A, et al. Notch signaling in chondrocytes modulates endochondral ossification and osteoarthritis development. Proc Natl Acad Sci U S A. 2013;110(5):1875–80.

    CAS  PubMed  PubMed Central  Google Scholar 

  69. Liang J, Xu L, Zhou F, Liu AM, Ge HX, Chen YY, et al. MALAT1/miR-127-5p regulates osteopontin (OPN)-mediated proliferation of human chondrocytes through PI3K/Akt pathway. J Cell Biochem. 2018;119(1):431–9.

    CAS  PubMed  Google Scholar 

  70. Zhong L, Huang X, Karperien M, Post JN. Correlation between gene expression and osteoarthritis progression in human. Int J Mol Sci. 2016;17(7):1126.

    PubMed Central  Google Scholar 

  71. Zhang X, Wang C, Zhao J, Xu J, Geng Y, Dai L, et al. miR-146a facilitates osteoarthritis by regulating cartilage homeostasis via targeting Camk2d and Ppp3r2. Cell Death Dis. 2017;8(4):e2734.

    CAS  PubMed  PubMed Central  Google Scholar 

  72. Zhong JH, Li J, Liu CF, Liu N, Bian RX, Zhao SM, et al. Effects of microRNA-146a on the proliferation and apoptosis of human osteoarthritis chondrocytes by targeting TRAF6 through the NF-kappaB signalling pathway. Biosci Rep. 2017;37(2).

  73. Ko JY, Lee MS, Lian WS, Weng WT, Sun YC, Chen YS, et al. MicroRNA-29a counteracts synovitis in knee osteoarthritis pathogenesis by targeting VEGF. Sci Rep. 2017;7(1):3584.

    PubMed  PubMed Central  Google Scholar 

  74. Wang Z, Hu J, Pan Y, Shan Y, Jiang L, Qi X, et al. miR-140-5p/miR-149 affects chondrocyte proliferation, apoptosis, and autophagy by targeting FUT1 in osteoarthritis. Inflammation. 2018;41(3):959–71.

    CAS  PubMed  Google Scholar 

  75. Li C, Hu Q, Chen Z, Shen B, Yang J, Kang P, et al. MicroRNA-140 suppresses human chondrocytes hypertrophy by targeting SMAD1 and controlling the bone morphogenetic protein pathway in osteoarthritis. Am J Med Sci. 2018;355(5):477–87.

    PubMed  Google Scholar 

  76. 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(9):2723–30.

    CAS  PubMed  PubMed Central  Google Scholar 

  77. Si HB, Zeng Y, Liu SY, Zhou ZK, Chen YN, Cheng JQ, et al. Intra-articular injection of microRNA-140 (miRNA-140) alleviates osteoarthritis (OA) progression by modulating extracellular matrix (ECM) homeostasis in rats. Osteoarthr Cartil. 2017;25(10):1698–707.

    PubMed  Google Scholar 

  78. Hu G, Zhao X, Wang C, Geng Y, Zhao J, Xu J, et al. MicroRNA-145 attenuates TNF-alpha-driven cartilage matrix degradation in osteoarthritis via direct suppression of MKK4. Cell Death Dis. 2017;8(10):e3140.

    CAS  PubMed  PubMed Central  Google Scholar 

  79. Ni Z, Shang X, Tang G, Niu L. Expression of miR-206 in human knee articular chondrocytes and effects of miR-206 on proliferation and apoptosis of articular chondrocytes. Am J Med Sci. 2018;355(3):240–6.

    PubMed  Google Scholar 

  80. Song J, Kang YH, Yoon S, Chun CH, Jin EJ. HIF-1alpha:CRAT:miR-144-3p axis dysregulation promotes osteoarthritis chondrocyte apoptosis and VLCFA accumulation. Oncotarget. 2017;8(41):69351–61.

    PubMed  PubMed Central  Google Scholar 

  81. Wang Y, Yang T, Liu Y, Zhao W, Zhang Z, Lu M, et al. Decrease of miR-195 promotes chondrocytes proliferation and maintenance of chondrogenic phenotype via targeting FGF-18 pathway. Int J Mol Sci. 2017;18(5).

    PubMed Central  Google Scholar 

  82. Zhang W, Zhong B, Zhang C, Luo C, Zhan Y. miR-373 regulates inflammatory cytokine-mediated chondrocyte proliferation in osteoarthritis by targeting the P2X7 receptor. FEBS Open Bio. 2018;8(3):325–31.

    PubMed  PubMed Central  Google Scholar 

  83. Bartlett R, Stokes L, Sluyter R. The P2X7 receptor channel: recent developments and the use of P2X7 antagonists in models of disease. Pharmacol Rev. 2014;66(3):638–75.

    CAS  PubMed  Google Scholar 

  84. Ntoumou E, Tzetis M, Braoudaki M, Lambrou G, Poulou M, Malizos K, et al. Serum microRNA array analysis identifies miR-140-3p, miR-33b-3p and miR-671-3p as potential osteoarthritis biomarkers involved in metabolic processes. Clin Epigenetics. 2017;9:127.

    CAS  PubMed  PubMed Central  Google Scholar 

  85. Hou C, Yang Z, Kang Y, Zhang Z, Fu M, He A, et al. MiR-193b regulates early chondrogenesis by inhibiting the TGF-beta2 signaling pathway. FEBS Lett. 2015;589(9):1040–7.

    CAS  PubMed  Google Scholar 

  86. Kung LHW, Ravi V, Rowley L, Angelucci C, Fosang AJ, Bell KM, et al. Cartilage microRNA dysregulation during the onset and progression of mouse osteoarthritis is independent of aggrecanolysis and overlaps with candidates from end-stage human disease. Arthritis Rheumatol. 2018;70(3):383–95.

    CAS  PubMed  Google Scholar 

  87. Kolhe R, Hunter M, Liu S, Jadeja RN, Pundkar C, Mondal AK, et al. Gender-specific differential expression of exosomal miRNA in synovial fluid of patients with osteoarthritis. Sci Rep. 2029;7(1):2017.

    Google Scholar 

  88. Li J, Wang L, Liu Z, Zu C, Xing F, Yang P, et al. MicroRNA-494 inhibits cell proliferation and invasion of chondrosarcoma cells in vivo and in vitro by directly targeting SOX9. Oncotarget. 2015;6(28):26216–29.

    PubMed  PubMed Central  Google Scholar 

  89. Zhang P, Li J, Song Y, Wang X. MiR-129-5p inhibits proliferation and invasion of chondrosarcoma cells by regulating SOX4/Wnt/beta-catenin signaling pathway. Cell Physiol Biochem. 2017;42(1):242–53.

    CAS  PubMed  Google Scholar 

  90. Lu N, Lin T, Wang L, Qi M, Liu Z, Dong H, et al. Association of SOX4 regulated by tumor suppressor miR-30a with poor prognosis in low-grade chondrosarcoma. Tumour Biol. 2015;36(5):3843–52.

    CAS  PubMed  Google Scholar 

  91. Mahboudi H, Soleimani M, Enderami SE, Kehtari M, Ardeshirylajimi A, Eftekhary M, et al. Enhanced chondrogenesis differentiation of human induced pluripotent stem cells by MicroRNA-140 and transforming growth factor beta 3 (TGFbeta3). Biologicals. 2018;52:30–6.

    CAS  PubMed  Google Scholar 

  92. Shiraishi K, Kamei N, Takeuchi S, Yanada S, Mera H, Wakitani S, et al. Quality evaluation of human bone marrow mesenchymal stem cells for cartilage repair. Stem Cells Int. 2017;2017:8740294.

    PubMed  PubMed Central  Google Scholar 

  93. Gori M, Trombetta M, Santini D, Rainer A. Tissue engineering and microRNAs: future perspectives in regenerative medicine. Expert Opin Biol Ther. 2015;15(11):1601–22.

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. College of Medicine, University of Central Florida, NFRMC 1147 NW 64th Terrace, Gainesville, FL, 32605, USA

    Garyfallia Papaioannou

  2. Internal Medicine Residency Program, North Florida Regional Medical Center, NFRMC 1147 NW 64th Terrace, Gainesville, FL, 32605, USA

    Garyfallia Papaioannou

  3. Endocrine Unit, Massachusetts General Hospital, 55 Fruit Street, Boston, MA, 02114, USA

    Anastasia Kozlova & Tatsuya Kobayashi

  4. Harvard Medical School, 55 Fruit Street, Boston, MA, 02114, USA

    Anastasia Kozlova & Tatsuya Kobayashi

Authors
  1. Garyfallia Papaioannou
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Anastasia Kozlova
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Tatsuya Kobayashi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Garyfallia Papaioannou or Tatsuya Kobayashi.

Ethics declarations

Conflict of Interest

Garyfallia Papaioannou, Anastasia Kozlova, and Tatsuya Kobayashi each declare no potential conflicts of interest.

Human and Animal Rights and Informed Consent

This article does not contain any studies with human or animal subjects performed by any of the authors.

Additional information

This article is part of the Topical Collection on MicroRNAs in Skeletal Development

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Papaioannou, G., Kozlova, A. & Kobayashi, T. miRNA Regulation of Chondrogenesis. Curr Mol Bio Rep 4, 208–217 (2018). https://doi.org/10.1007/s40610-018-0104-z

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s40610-018-0104-z

Keywords

Search

Navigation