Advertisement

Cell Stress and Chaperones

, Volume 24, Issue 6, pp 1151–1161 | Cite as

MiR-147 inhibits cyclic mechanical stretch-induced apoptosis in L6 myoblasts via ameliorating endoplasmic reticulum stress by targeting BRMS1

  • Yanxiao Du
  • Feng Yang
  • Di Lv
  • Qiang Zhang
  • Xiao YuanEmail author
Original Paper
  • 74 Downloads

Abstract

Functional orthopedic treatment is effective for the correction of malformation. Studies demonstrated myoblasts undergo proliferation and apoptosis on certain stretch conditions. MicroRNAs (miRNAs) function in RNA silencing and post-transcriptional regulation of gene expression, and participate in various biological processes, including proliferation and apoptosis. One hypothesis suggested that miRNA was involved into the procedure via suppressing its target genes then triggered endoplasmic reticulum stress-induced apoptosis. Therefore, miRNAs play important roles in the regulation of the proliferation and apoptosis of myoblasts. In our study, the miR-147 has been explored. A cyclic mechanical stretch model was established to observe the features of rat L6 myoblasts. The detection of mRNA and protein levels was performed by qRT-PCR and western blot. L6 cell proliferation/apoptosis was checked by CCK-8 assay, DNA fragmentation assay, and caspase-3 activity assay. MiRNA transfections were performed as per the manufacturer’s suggestions: (1) cyclic mechanical stretch induced apoptosis of L6 myoblasts and inhibition of miR-147; (2) miR-147 attenuated cyclic mechanical stretch-induced apoptosis of L6 myoblasts; (3) miR-147 attenuated cyclic mechanical stretch-induced L6 myoblast endoplasmic reticulum stress; (4) BRMS1 was a direct target of miR-147 in L6 myoblasts; (5) miR-147/BRMS1 axis participated in the regulation of cyclic mechanical stress on L6 myoblasts. MiR-147 attenuates endoplasmic reticulum stress by targeting BRMS1 to inhibit cyclic mechanical stretch-induced apoptosis of L6 myoblasts.

Keywords

Cyclic mechanical stretch Myoblast MiR-147 Apoptosis ER-Stress 

Notes

Acknowledgments

The study was supported by the Xuzhou clinical technical backbone training plan (2018).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflicts of interest.

Supplementary material

12192_2019_1037_MOESM1_ESM.docx (441 kb)
ESM 1 (DOCX 441 kb)

References

  1. Akimoto T et al (2005) Mechanical stretch inhibits myoblast-to-adipocyte differentiation through Wnt signaling. Biochem Biophys Res Commun 329:381–385.  https://doi.org/10.1016/j.bbrc.2005.01.136 CrossRefPubMedGoogle Scholar
  2. Barnouti ZP, Owtad P, Shen G, Petocz P, Darendeliler MA (2011) The biological mechanisms of PCNA and BMP in TMJ adaptive remodeling. Angle Orthod 81:91–99.  https://doi.org/10.2319/091609-522.1 CrossRefPubMedGoogle Scholar
  3. Carthew RW, Sontheimer EJ (2009) Origins and mechanisms of miRNAs and siRNAs. Cell 136:642–655.  https://doi.org/10.1016/j.cell.2009.01.035 CrossRefPubMedPubMedCentralGoogle Scholar
  4. Chen R, Feng L, Ruan M, Liu X, Adriouch S, Liao H (2013) Mechanical-stretch of C2C12 myoblasts inhibits expression of Toll-like receptor 3 (TLR3) and of autoantigens associated with inflammatory myopathies. PLoS One 8:e79930.  https://doi.org/10.1371/journal.pone.0079930 CrossRefPubMedPubMedCentralGoogle Scholar
  5. Chimonidou M, Kallergi G, Georgoulias V, Welch DR, Lianidou ES (2013) Breast cancer metastasis suppressor-1 promoter methylation in primary breast tumors and corresponding circulating tumor cells. Mol Cancer Res 11:1248–1257.  https://doi.org/10.1158/1541-7786.MCR-13-0096 CrossRefPubMedGoogle Scholar
  6. Croce CM (2009) Causes and consequences of microRNA dysregulation in cancer. Nat Rev Genet 10:704–714.  https://doi.org/10.1038/nrg2634 CrossRefPubMedPubMedCentralGoogle Scholar
  7. Cucina A, Fuso A, Coluccia P, Cavallaro A (2008) Nicotine inhibits apoptosis and stimulates proliferation in aortic smooth muscle cells through a functional nicotinic acetylcholine receptor. J Surg Res 150:227–235.  https://doi.org/10.1016/j.jss.2007.10.019 CrossRefPubMedGoogle Scholar
  8. Dam AD, Mitchell AS, Quadrilatero J (2013) Induction of mitochondrial biogenesis protects against caspase-dependent and caspase-independent apoptosis in L6 myoblasts. Biochim Biophys Acta 1833:3426–3435.  https://doi.org/10.1016/j.bbamcr.2013.04.014 CrossRefPubMedGoogle Scholar
  9. Deng G, Sui G (2013) Noncoding RNA in oncogenesis: a new era of identifying key players. Int J Mol Sci 14:18319–18349.  https://doi.org/10.3390/ijms140918319 CrossRefPubMedPubMedCentralGoogle Scholar
  10. Diniz GP, Wang DZ (2016) Regulation of skeletal muscle by microRNAs. Compr Physiol 6:1279–1294.  https://doi.org/10.1002/cphy.c150041 CrossRefPubMedGoogle Scholar
  11. Erdem A, Kilic N, Eroz B (2009) Changes in soft tissue profile and electromyographic activity after activator treatment. Aust Orthod J 25:116–122PubMedGoogle Scholar
  12. Fu S, Yin L, Lin X, Lu J, Wang X (2018) Effects of cyclic mechanical stretch on the proliferation of L6 myoblasts and its mechanisms: PI3K/Akt and MAPK signal pathways regulated by IGF-1 receptor. Int J Mol Sci 19.  https://doi.org/10.3390/ijms19061649 CrossRefGoogle Scholar
  13. Hicks MR et al (2018) ERBB3 and NGFR mark a distinct skeletal muscle progenitor cell in human development and hPSCs. Nat Cell Biol 20:46–57.  https://doi.org/10.1038/s41556-017-0010-2 CrossRefPubMedGoogle Scholar
  14. Hua W, Zhang M, Wang Y, Yu L, Zhao T, Qiu X, Wang L (2016) Mechanical stretch regulates microRNA expression profile via NF-kappaB activation in C2C12 myoblasts. Mol Med Rep 14:5084–5092.  https://doi.org/10.3892/mmr.2016.5907 CrossRefPubMedPubMedCentralGoogle Scholar
  15. Iwakawa HO, Tomari Y (2015) The functions of microRNAs: mRNA decay and translational repression trends. Cell Biol 25:651–665.  https://doi.org/10.1016/j.tcb.2015.07.011 CrossRefGoogle Scholar
  16. Jia LX et al (2015) Mechanical stretch-induced endoplasmic reticulum stress, apoptosis and inflammation contribute to thoracic aortic aneurysm and dissection. J Pathol 236:373–383.  https://doi.org/10.1002/path.4534 CrossRefPubMedPubMedCentralGoogle Scholar
  17. Liu Y, Smith PW, Jones DR (2006) Breast cancer metastasis suppressor 1 functions as a corepressor by enhancing histone deacetylase 1-mediated deacetylation of RelA/p65 and promoting apoptosis. Mol Cell Biol 26:8683–8696.  https://doi.org/10.1128/MCB.00940-06 CrossRefPubMedPubMedCentralGoogle Scholar
  18. Liu G, Friggeri A, Yang Y, Park YJ, Tsuruta Y, Abraham E (2009) miR-147, a microRNA that is induced upon Toll-like receptor stimulation, regulates murine macrophage inflammatory responses. Proc Natl Acad Sci U S A 106:15819–15824.  https://doi.org/10.1073/pnas.0901216106 CrossRefPubMedPubMedCentralGoogle Scholar
  19. Liu J, Wang Y, Yuan X, Feng Y, Liu H (2010) Cyclic-stretch induces the apoptosis of myoblast by activation of caspase-3 protease in a magnitude-dependent manner. Int J Biochem Cell Biol 42:2004–2011.  https://doi.org/10.1016/j.biocel.2010.08.013 CrossRefPubMedGoogle Scholar
  20. Lui JC (2017) Regulation of body growth by microRNAs. Mol Cell Endocrinol 456:2–8.  https://doi.org/10.1016/j.mce.2016.10.024 CrossRefPubMedGoogle Scholar
  21. Ning X, Wang C, Zhang M, Wang K (2019) Ectopic expression of miR-147 inhibits stem cell marker and epithelial-mesenchymal transition (EMT)-related protein expression in colon cancer cells. Oncol Res 27:399–406.  https://doi.org/10.3727/096504018X15179675206495 CrossRefPubMedGoogle Scholar
  22. Owtad P, Potres Z, Shen G, Petocz P, Darendeliler MA (2011) A histochemical study on condylar cartilage and glenoid fossa during mandibular advancement. Angle Orthod 81:270–276.  https://doi.org/10.2319/021710-99.1 CrossRefPubMedGoogle Scholar
  23. Shen J, Niu W, Zhang H, Jun M, Zhang H (2018) Downregulation of microRNA-147 inhibits cell proliferation and increases the chemosensitivity of gastric cancer cells to 5-fluorouracil by directly targeting PTEN. Oncol Res 26:901–911.  https://doi.org/10.3727/096504017X15061902533715 CrossRefPubMedGoogle Scholar
  24. Song J, Hu B, Qu H, Bi C, Huang X, Zhang M (2012) Mechanical stretch modulates microRNA 21 expression, participating in proliferation and apoptosis in cultured human aortic smooth muscle cells. PLoS One 7:e47657.  https://doi.org/10.1371/journal.pone.0047657 CrossRefPubMedPubMedCentralGoogle Scholar
  25. Song J et al (2018a) Cleavage of caspase-12 at Asp94, mediated by endoplasmic reticulum stress (ERS), contributes to stretch-induced apoptosis of myoblasts. J Cell Physiol 233:9473–9487.  https://doi.org/10.1002/jcp.26840 CrossRefPubMedGoogle Scholar
  26. Song SE et al (2018b) Tomatidine inhibits tumor necrosis factor-alpha-induced apoptosis in C2C12 myoblasts via ameliorating endoplasmic reticulum stress. Mol Cell Biochem 444:17–25.  https://doi.org/10.1007/s11010-017-3226-3 CrossRefPubMedGoogle Scholar
  27. Strasser A, Huang DC, Vaux DL (1997) The role of the bcl-2/ced-9 gene family in cancer and general implications of defects in cell death control for tumourigenesis and resistance to chemotherapy. Biochim Biophys Acta 1333:F151–F178PubMedGoogle Scholar
  28. Wei K et al (2015) Herb-partitioned moxibustion and the miRNAs related to Crohn's disease: a study based on rat models. Evid Based Complement Alternat Med 2015:265238.  https://doi.org/10.1155/2015/265238 CrossRefPubMedPubMedCentralGoogle Scholar
  29. Wei Y et al (2016) Role of miR-181a-5p and endoplasmic reticulum stress in the regulation of myogenic differentiation. Gene 592:60–70.  https://doi.org/10.1016/j.gene.2016.07.056 CrossRefPubMedGoogle Scholar
  30. White NM, Fatoohi E, Metias M, Jung K, Stephan C, Yousef GM (2011) Metastamirs: a stepping stone towards improved cancer management. Nat Rev Clin Oncol 8:75–84.  https://doi.org/10.1038/nrclinonc.2010.173 CrossRefPubMedGoogle Scholar
  31. Xing WJ et al (2015) MRTF-A and STAT3 promote MDA-MB-231 cell migration via hypermethylating BRSM1 IUBMB. Life 67:202–217.  https://doi.org/10.1002/iub.1362 CrossRefPubMedGoogle Scholar
  32. Yagci A, Uysal T, Kara S, Okkesim S (2010) The effects of myofunctional appliance treatment on the perioral and masticatory muscles in class II, division 1 patients. World J Orthod 11:117–122PubMedGoogle Scholar
  33. Yamamoto K, Ito S, Hanafusa H, Shimizu K, Ouchida M (2015) Uncovering direct targets of MiR-19a involved in lung cancer progression. PLoS One 10:e0137887.  https://doi.org/10.1371/journal.pone.0137887 CrossRefPubMedPubMedCentralGoogle Scholar
  34. Yoshida H (2007) ER stress and diseases. FEBS J 274:630–658.  https://doi.org/10.1111/j.1742-4658.2007.05639.x CrossRefPubMedGoogle Scholar
  35. You J, He X, Ding H, Zhang T (2015) BRMS1 regulates apoptosis in non-small cell lung cancer cells. Cell Biochem Biophys 71:465–472.  https://doi.org/10.1007/s12013-014-0226-8 CrossRefPubMedGoogle Scholar
  36. Zhang Y et al (2014) Effect of BRMS1 on tumorigenicity and metastasis of human rectal cancer. Cell Biochem Biophys 70:505–509.  https://doi.org/10.1007/s12013-014-9948-x CrossRefPubMedGoogle Scholar
  37. Zhang Q et al (2016) Caspase-12 is involved in stretch-induced apoptosis mediated endoplasmic reticulum stress. Apoptosis 21:432–442.  https://doi.org/10.1007/s10495-016-1217-6 CrossRefPubMedGoogle Scholar
  38. Zhang HM, Qiao QD, Xie HF, Wei JX (2017) Breast cancer metastasis suppressor 1 (BRMS1) suppresses prostate cancer progression by inducing apoptosis and regulating invasion. Eur Rev Med Pharmacol Sci 21:68–75PubMedGoogle Scholar

Copyright information

© Cell Stress Society International 2019

Authors and Affiliations

  • Yanxiao Du
    • 1
    • 2
  • Feng Yang
    • 3
    • 4
  • Di Lv
    • 2
  • Qiang Zhang
    • 5
  • Xiao Yuan
    • 1
    • 5
    Email author
  1. 1.Nanjing Medical UniversityNanjingChina
  2. 2.Department of StomatologyQingdao Central HospitalQingdaoChina
  3. 3.School of StomatologyXuzhou Medical UniversityXuzhouChina
  4. 4.Department of StomatologyThe Affiliated Hospital of Xuzhou Medical UniversityXuzhouChina
  5. 5.Department of Orthodontics IIThe Affiliated Hospital of Qingdao UniversityQingdaoChina

Personalised recommendations