Skip to main content

Advertisement

Log in

miR-23a-3p regulated by LncRNA SNHG5 suppresses the chondrogenic differentiation of human adipose-derived stem cells via targeting SOX6/SOX5

  • Regular Article
  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Abstract

Cartilage generation and degradation are controlled by miRNAs. Our previous study showed miR-23a-3p was downregulated during chondrogenic differentiation in chondrogenic human adipose-derived mesenchymal stem cells (hADSCs). In the present study, we explored the function of miR-23a-3p in chondrogenesis differentiation. The role of miR-23a-3p in chondrogenic differentiation potential of hADSCs was assessed by Alcian blue staining, quantitative real-time polymerase chain reaction (qRT-PCR), and Western blot. We show that miR-23a-3p suppressed the chondrogenic differentiation of hADSCs. LncRNA SNHG5 interacted with miR-23a-3p, and suppression or overexpression of SNHG5 correlates with inhibition and promotion of hADSC chondrogenic differentiation, respectively. We have determined that SNHG5 can sponge miR-23a-3p to regulate the expression of SOX6/SOX5, transcription factors that play essential roles in chondrocyte differentiation. Furthermore, the overexpression of SNHG5 activates the JNK/MAPK/ERK pathway. In conclusion, miR-23a-3p regulated by lncRNA SNHG5 suppresses the chondrogenic differentiation of human adipose-derived stem cells via targeting SOX6/SOX5.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Almalki SG, Agrawal DK (2016) Key transcription factors in the differentiation of mesenchymal stem cells. Differentiation 92:41–51

    Article  CAS  Google Scholar 

  • Andarwulan N, Batari R, Sandrasari DA, Bolling B, Wijaya H (2010) Flavonoid content and antioxidant activity of vegetables from Indonesia. Food Chem 121:1231–1235

    Article  CAS  Google Scholar 

  • Dong S, Yang B, Guo H, Kang F (2012) MicroRNAs regulate osteogenesis and chondrogenesis. Biochem Biophys Res Commun 418:587–591

    Article  CAS  Google Scholar 

  • Dy P, Smits P, Silvester A, Penzo-Mendez A, Dumitriu B, Han Y, de la Motte CA, Kingsley DM, Lefebvre V (2010) Synovial joint morphogenesis requires the chondrogenic action of Sox5 and Sox6 in growth plate and articular cartilage. Dev Biol 341:346–359

    Article  CAS  Google Scholar 

  • Gangaraju VK, Lin H (2009) MicroRNAs: key regulators of stem cells. Nat Rev Mol Cell Biol 10:116–125

    Article  CAS  Google Scholar 

  • Gao J, Yang T, Han J, Yan K, Qiu X, Zhou Y, Fan Q, Ma B (2011) MicroRNA expression during osteogenic differentiation of human multipotent mesenchymal stromal cells from bone marrow. J Cell Biochem 112:1844–1856

    Article  CAS  Google Scholar 

  • Hodges WM, O’Brien F, Fulzele S, Hamrick MW (2017) Function of microRNAs in the osteogenic differentiation and therapeutic application of adipose-derived stem cells (ASCs). Int J Mol Sci 18:2597

    Article  Google Scholar 

  • Im GI (2017) Bone marrow-derived stem/stromal cells and adipose tissue-derived stem/stromal cells: their comparative efficacies and synergistic effects. J Biomed Mater Res A 105:2640–2648

    Article  CAS  Google Scholar 

  • Kang L, Yang C, Song Y, Liu W, Wang K, Li S, Zhang Y (2016a) MicroRNA-23a-3p promotes the development of osteoarthritis by directly targeting SMAD3 in chondrocytes. Biochem Biophys Res Commun 478:467–473

    Article  CAS  Google Scholar 

  • Kang SW, Kim J, Shin DY (2016b) Inhibition of senescence and promotion of the proliferation of chondrocytes from articular cartilage by CsA and FK506 involves inhibition of p38MAPK. Mech Ageing Dev 153:7–13

    Article  CAS  Google Scholar 

  • Kobayashi T, Lu J, Cobb BS, Rodda SJ, McMahon AP, Schipani E, Merkenschlager M, Kronenberg HM (2008) Dicer-dependent pathways regulate chondrocyte proliferation and differentiation. Proc Natl Acad Sci 105:1949–1954

    Article  CAS  Google Scholar 

  • Komarek J, Valis P, Repko M, Chaloupka R, Krbec M (2010) Treatment of deep cartilage defects of the knee with autologous chondrocyte transplantation: long-term results. Acta Chir Orthop Traumatol Cechoslov 77:291–295

    CAS  Google Scholar 

  • Lai RC, Yeo RW, Lim SK (2015) Mesenchymal stem cell exosomes. Semin Cell Dev Biol 40:82–88

    Article  CAS  Google Scholar 

  • Lee W-S, Kim HJ, Kim K-I, Kim GB, Jin W (2019) Intra-articular injection of autologous adipose tissue-derived mesenchymal stem cells for the treatment of knee osteoarthritis: a phase IIb, randomized, placebo-controlled clinical trial. Stem Cells Transl Med 8:504–511

    Article  CAS  Google Scholar 

  • Li X, Liu L, Luo Y, Cui S, Chen W, Zeng A, Shi Y, Luo L (2019) Long noncoding RNA SNHG5 promotes glioma progression via miR-205/E2F3 axis. Biosci Rep 39:1-11

  • Liao JY, Ma LM, Guo YH, Zhang YC, Zhou H, Shao P, Chen YQ, Qu LH (2010) Deep sequencing of human nuclear and cytoplasmic small RNAs reveals an unexpectedly complex subcellular distribution of miRNAs and tRNA 3′ trailers. PLoS One 5:e10563

    Article  Google Scholar 

  • Lin GL, Hankenson KD (2011) Integration of BMP, Wnt, and notch signaling pathways in osteoblast differentiation. J Cell Biochem 112:3491–3501

    Article  CAS  Google Scholar 

  • Miura Y (2016) Human bone marrow mesenchymal stromal/stem cells: current clinical applications and potential for hematology. Int J Hematol 103:122–128

    Article  CAS  Google Scholar 

  • Niethammer TR, Pietschmann MF, Ficklscherer A, Gulecyuz MF, Hammerschmid F, Muller PE (2016) Incomplete defect filling after third generation autologous chondrocyte implantation. Arch Med Sci 12:785–792

    Article  Google Scholar 

  • Park SJ, Cheon EJ, Kim HA (2013) MicroRNA-558 regulates the expression of cyclooxygenase-2 and IL-1β-induced catabolic effects in human articular chondrocytes. Osteoarthr Cartil 21:981–989

    Article  CAS  Google Scholar 

  • Peng S, Cao L, He S, Zhong Y, Ma H, Zhang Y, Shuai C (2018) An overview of long noncoding RNAs involved in bone regeneration from mesenchymal stem cells. Stem Cells Int 2018:8273648

    Article  Google Scholar 

  • Pereira D, Peleteiro B, Araujo J, Branco J, Santos RA, Ramos E (2011) The effect of osteoarthritis definition on prevalence and incidence estimates: a systematic review. Osteoarthr Cartil 19:1270–1285

    Article  CAS  Google Scholar 

  • Pers Y-M, Quentin J, Feirreira R, Espinoza F, Abdellaoui N, Erkilic N, Cren M, Dufourcq-Lopez E, Pullig O, Nöth U, Jorgensen C, Louis-Plence P (2018) Injection of adipose-derived stromal cells in the knee of patients with severe osteoarthritis has a systemic effect and promotes an anti-inflammatory phenotype of circulating immune cells. Theranostics 8:5519–5528

    Article  CAS  Google Scholar 

  • Polymeri A, Giannobile WV, Kaigler D (2016) Bone marrow stromal stem cells in tissue engineering and regenerative medicine. Horm Metab Res 48:700–713

    Article  CAS  Google Scholar 

  • Salmena L, Poliseno L, Tay Y, Kats L, Pandolfi PP (2011) A ceRNA hypothesis: the Rosetta Stone of a hidden RNA language? Cell 146:353–358

    Article  CAS  Google Scholar 

  • Schäffler A, Büchler C (2007) Concise review: adipose tissue-derived stromal cells-basic and clinical implications for novel cell-based therapies. Stem Cells 25:818–827

    Article  Google Scholar 

  • Schulze-Tanzil G (2009) Activation and dedifferentiation of chondrocytes: implications in cartilage injury and repair. Ann Anat 191:325–338

    Article  CAS  Google Scholar 

  • Smits P, Dy P, Mitra S, Lefebvre V (2004) Sox5 and Sox6 are needed to develop and maintain source, columnar, and hypertrophic chondrocytes in the cartilage growth plate. J Cell Biol 164:747–758

    Article  CAS  Google Scholar 

  • Wang P, Mao Z, Pan Q, Lu R, Huang X, Shang X, Zhang R, You H (2018) Histone deacetylase-4 and histone deacetylase-8 regulate interleukin-1beta-induced cartilage catabolic degradation through MAPK/JNK and ERK pathways. Int J Mol Med 41:2117–2127

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wu DM, Wang S, Wen X, Han XR, Wang YJ, Shen M, Fan SH, Zhang ZF, Shan Q, Li MQ, Hu B, Lu J, Chen GQ, Zheng YL (2018) LncRNA SNHG15 acts as a ceRNA to regulate YAP1-Hippo signaling pathway by sponging miR-200a-3p in papillary thyroid carcinoma. Cell Death Dis 9:947

    Article  Google Scholar 

  • Yang Z, Hao J, Hu ZM (2015) MicroRNA expression profiles in human adipose-derived stem cells during chondrogenic differentiation. Int J Mol Med 35:579–586

    Article  CAS  Google Scholar 

  • Yang Z, Li R, Ao J, Wa QD, Zhang Y, Chen L, Wen J, Chen B, Pan W, Li B, Tian XB (2018) miR-1307-3p suppresses the chondrogenic differentiation of human adipose-derived stem cells by targeting BMPR2. Int J Mol Med 42:3115–3124

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu Y, Liu T, Song K, Fan X, Ma X, Cui Z (2008) Adipose-derived stem cell: a better stem cell than BMSC. Cell Biochem Funct 26:664–675

    Article  CAS  Google Scholar 

Download references

Funding

This work was supported by National Natural Science Foundation of China (31660265, 31960208, 81060145, and 81560356), Youth Fund of Guizhou Provincial People’s Hospital (GZSYQN(2015)06), Subsidy Foundation of National Natural Science Foundation of Guizhou Provincial People’s Hospital (Guizhou Science and Technology Platform (2017)5724), and Science and Technology Foundation of Guizhou Province (Guizhou Science and Technology J Word (2015)2096).

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Bo Li or Xiaobin Tian.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All procedures performed in studies involving human participants were following the ethical standards of the Ethics Committee of Tianjin Haihe Hospital and written informed consent was obtained from all the patients.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yang, Z., Ren, Z., She, R. et al. miR-23a-3p regulated by LncRNA SNHG5 suppresses the chondrogenic differentiation of human adipose-derived stem cells via targeting SOX6/SOX5. Cell Tissue Res 383, 723–733 (2021). https://doi.org/10.1007/s00441-020-03289-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00441-020-03289-4

Keywords

Navigation