Skip to main content
SpringerLink
Log in

miR-1228 prevents cellular apoptosis through targeting of MOAP1 protein

  • Original Paper
  • Published:
Apoptosis Aims and scope Submit manuscript

Abstract

Apoptosis is a critical cellular process that balances the effects of cell proliferation and cell death. MicroRNAs play important roles in cell growth, differentiation, and apoptosis. In this study, we observed a reduction of miR-1228 expression in apoptotic cells. Enforced miR-1228 expression can reduce MOAP1 expression and delay the progression of stress-induced cell apoptosis. Rescue experiment demonstrated that miR-1228 inhibition of cellular apoptosis is significantly attenuated by repressing MOAP1 expression, suggesting the direct interaction between miR-1228 and MOAP1 protein. Taken together, this study provides evidences that miR-1228 plays an inhibitory role in stress-induced cellular apoptosis. miR-1228 may become a critical therapeutic target for apoptosis relevant diseases in the future.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116:281–297

    Article  PubMed  CAS  Google Scholar 

  2. Calin GA, Sevignani C, Dan Dumitru C, Hyslop T, Noch E, Yendamuri S, Shimizu M, Rattan S, Bullrich F, Negrini M, Croce CM (2004) Human microRNA genes are frequently located at fragile sites and genomic regions involved in cancers. Proc Natl Acad Sci USA 101:2999–3004

    Google Scholar 

  3. Iorio MV, Ferracin M, Liu CG, Veronese A, Spizzo R, Sabbioni S, Magri E, Pedriali M, Fabbri M, Campiglio M, Ménard S, Palazzo JP, Rosenberg A, Musiani P, Volinia S, Nenci I, Calin GA, Querzoli P, Negrini M, Croce CM (2005) MicroRNA gene expression deregulation in human breast cancer. Cancer Res 65:7065–7070

    Article  PubMed  CAS  Google Scholar 

  4. Volinia S, Calin GA, Liu CG, Ambs S, Cimmino A, Petrocca F, Visone R, Iorio M, Roldo C, Ferracin M, Prueitt RL, Yanaihara N, Lanza G, Scarpa A, Vecchione A, Negrini M, Harris CC, Croce CM (2006) A microRNA expression signature of human solid tumors defines cancer gene targets. Proc Natl Acad Sci USA 103:2257–2261

    Article  PubMed  CAS  Google Scholar 

  5. Fesus L, Davies PJ, Piacentini M (1991) Apoptosis: molecular mechanisms in programmed cell death. Eur J Cell Biol 56:170–177

    PubMed  CAS  Google Scholar 

  6. Cimmino A, Calin GA, Fabbri M, Iorio MV, Ferracin M, Shimizu M, Wojcik SE, Aqeilan RI, Zupo S, Dono M, Rassenti L, Alder H, Volinia S, Liu C, Kipps TJ, Negrini M, Croce CM (2005) miR-15 and miR-16 induce apoptosis by targeting BCL2. Proc Natl Acad Sci USA 102:13944–13949

    Article  PubMed  CAS  Google Scholar 

  7. Wang Y, Lee AT, Ma JZ, Wang J, Ren J, Yang Y, Tantoso E, Li KB, Ooi LL, Tan P, Lee CG (2008) Profiling microRNA expression in hepatocellular carcinoma reveals microRNA-224 up-regulation and apoptosis inhibitor-5 as a microRNA-224-specific target. J Biol Chem 283:13205–13215

    Article  PubMed  CAS  Google Scholar 

  8. Li J, Huang H, Sun L, Yang M, Pan C, Chen W, Wu D, Lin Z, Zeng C, Yao Y, Zhang P, Song E (2009) MiR-21 indicates poor prognosis in tongue squamous cell carcinomas as an apoptosis inhibitor. Clin Cancer Res 15:3998–4008

    Article  PubMed  CAS  Google Scholar 

  9. Berezikov E, Chung WJ, Willis J, Cuppen E, Lai EC (2007) Mammalian mirtron genes. Mol Cell 28:328–336

    Article  PubMed  CAS  Google Scholar 

  10. Guled M, Lahti L, Lindholm PM, Salmenkivi K, Bagwan I, Nicholson AG, Knuutila S (2009) CDKN2A, NF2, and JUN are dysregulated among other genes by miRNAs in malignant mesothelioma—A miRNA microarray analysis. Genes Chromosomes Cancer 48:615–623

    Article  PubMed  CAS  Google Scholar 

  11. Borgan E, Navon R, Vollan HK, Schlichting E, Sauer T, Yakhini Z, Lingjærde OC, Sørlie T, Børresen-Dale AL (2011) Ischemia caused by time to freezing induces systematic microRNA and mRNA responses in cancer tissue. Mol Oncol 5:564–576

    Article  PubMed  CAS  Google Scholar 

  12. Lee YM, Cho HJ, Lee SY, Yun SC, Kim JH, Lee SY, Kwon SJ, Choi E, Na MJ, Kang JK, Son JW (2011) MicroRNA-23a: a novel serum based diagnostic biomarker for lung adenocarcinoma. Tuberc Respir Dis 71:8–14

    Article  Google Scholar 

  13. Bae S, Lee EM, Cha HJ, Kim K, Yoon Y, Lee H, Kim J, Kim YJ, Lee HG, Jeung HK, Min YH, An S (2011) Resveratrol alters microRNA expression profiles in A549 human non-small cell lung cancer cells. Mol Cells 32:243–249

    Article  PubMed  CAS  Google Scholar 

  14. Wei MC, Zong WX, Cheng EHY, Lindsten T, Panoutsakopoulou V, Ross AJ, Roth KA, MacGregor GR, Thompson CB, Korsmeyer SJ (2001) Proapoptotic BAX and BAK: a requisite gateway to mitochondrial dysfunction and death. Science 292:727–730

    Article  PubMed  CAS  Google Scholar 

  15. Chen C, Ridzon DA, Broomer AJ, Zhou Z, Lee DH, Nguyen JT, Bardisin M, Xu NL, Mahuvakar VR, Andersen MR, Lao KQ, Livak KJ, Guegler KJ (2005) Real-time quantification of microRNAs by stem-loop RT-PCR. Nucleic Acids Res 33:e179

    Article  PubMed  Google Scholar 

  16. Wang XW (2008) miRDB: a microRNA target prediction and functional annotation database with a wiki interface. RNA 14:1012–1017

    Article  PubMed  CAS  Google Scholar 

  17. Betel D, Wilson M, Gabow A, Marks DS, Sander C (2008) The microRNA.org resource: targets and expression. Nucleic Acids Res 36:D149–D153

    Article  PubMed  CAS  Google Scholar 

  18. Reed JC (2000) Mechanisms of apoptosis. Am J Pathol 157:1415–1430

    Article  PubMed  CAS  Google Scholar 

  19. Liu Y, Huo ZX, Yan B, Lin X, Zhou Z, Liang X, Zhu W, Liang D, Li L, Liu Y, Zhao H, Sun Y, Chen YH (2010) Prolyl hydroxylase 3 interacts with Bcl-2 to regulate doxorubicin-induced apoptosis in H9c2 cells. Biochem Biophys Res Commun 401:231–237

    Article  PubMed  CAS  Google Scholar 

  20. Yan B, Kong M, Chen YH (2011) Prevention of apoptosis by the interaction between FIH1 and Bax. Mol Cell Biochem 348:1–9

    Article  PubMed  CAS  Google Scholar 

  21. Tan KO, Tan KML, Chan SL, Yee KSY, Bévort M, Ang KC, Yu VC (2001) MAP-1, a novel proapoptotic protein containing a BH3-like motif that associates with Bax through its Bcl-2 homology domains. J Biol Chem 276:2802–2807

    Article  PubMed  CAS  Google Scholar 

  22. Hammell M (2010) Computational methods to identify miRNA targets. Semin Cell Dev Biol 21:738–744

    Article  PubMed  CAS  Google Scholar 

  23. Asangani IA, Rasheed SA, Nikolova DA, Leupold JH, Colburn NH, Post S, Allgayer H (2008) MicroRNA-21 post-transcriptionally downregulates tumor suppressor Pdcd4 and stimulates invasion, intravasation and metastasis in colorectal cancer. Oncogene 27:2128–2136

    Article  PubMed  CAS  Google Scholar 

  24. Raver-Shapira N, Marciano E, Meiri E, Spector Y, Rosenfeld N, Moskovits N, Bentwich Z, Oren M (2007) Transcriptional activation of miR-34a contributes to p53-mediated apoptosis. Mol Cell 26:731–743

    Article  PubMed  CAS  Google Scholar 

  25. Meng F, Henson R, Wehbe-Janek H, Smith H, Ueno Y, Patel T (2007) The microRNA let-7a modulates interleukin-6-dependent STAT-3 survival signaling in malignant human cholangiocytes. J Biol Chem 282:8256–8264

    Article  PubMed  CAS  Google Scholar 

  26. Yang BF, Lu YJ, Wang ZG (2009) MicroRNAs and apoptosis: implications in the molecular therapy of human disease. Clin Exp Pharmacol Physiol 36:951–960

    Article  PubMed  CAS  Google Scholar 

  27. Tan SH, Ida H, Goh BC, Hsieh W, Loh M, Ito Y (2006) Analyses of promoter hypermethylation for RUNX3 and other tumor suppressor genes in nasopharyngeal carcinoma. Anticancer Res 26:4287–4292

    PubMed  CAS  Google Scholar 

  28. Baksh S, Tommasi S, Fenton S, Yu VC, Martins LM, Pfeifer GP, Latif F, Downward J, Neel BG (2005) The tumor suppressor RASSF1A and MAP-1 link death receptor signaling to Bax conformational change and cell death. Mol Cell 18:637–650

    Article  PubMed  CAS  Google Scholar 

  29. Vos MD, Dallol A, Eckfeld K, Allen NPC, Donninger H, Hesson LB, Calvisi D, Latif F, Clark GJ (2006) The RASSF1A tumor suppressor activates Bax via MOAP-1. J Biol Chem 281:4557–4563

    Article  PubMed  CAS  Google Scholar 

  30. McManus MT (2003) MicroRNAs and cancer. Semin Cancer Biol 13:253–258

    Article  PubMed  CAS  Google Scholar 

  31. Chung WJ, Agius P, Westholm JO, Chen M, Okamura K, Robine N, Leslie CS, Lai EC (2011) Computational and experimental identification of mirtrons in Drosophila melanogaster and Caenorhabditis elegans. Genome Res 21:286–300

    Article  PubMed  CAS  Google Scholar 

  32. Ruby JG, Jan CH, Bartel DP (2007) Intronic microRNA precursors that bypass Drosha processing. Nature 448:83–86

    Article  PubMed  CAS  Google Scholar 

  33. Czech B, Hannon GJ (2011) Small RNA sorting: matchmaking for Argonautes. Nat Rev Genet 12:19–31

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgment

This work was supported by the Doctoral Fund (B-8812-11-0197 to B.Y.).

Author information

Authors and Affiliations

  1. Key laboratory of Freshwater Aquatic Genetic Resources, Shanghai Ocean University, Ministry of Agriculture, Shanghai, 201306, China

    Biao Yan & Jin-liang Zhao

Authors
  1. Biao Yan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jin-liang Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Biao Yan or Jin-liang Zhao.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Yan, B., Zhao, Jl. miR-1228 prevents cellular apoptosis through targeting of MOAP1 protein. Apoptosis 17, 717–724 (2012). https://doi.org/10.1007/s10495-012-0710-9

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10495-012-0710-9

Keywords

Search

Navigation