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Regulation of microRNA activity in stress

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Abstract

Stressors substantially affect the physiology of cells. Depending on the severity and duration of stress exposure, cells either strive to maintain homeostasis or adapt by adjusting their gene expression patterns. One of the mechanisms to change gene expression is regulating the microRNA (miRNA) levels and activities of microRNA–protein complexes. A fine tuning of the interaction of miRNAs with their mRNA targets determines the specificity of protein synthesis and the quantitative composition of the protein pool in stress. The review considers the mechanisms that regulate miRNA biogenesis, miRNA-mediated mRNA repression, and activity of miRNA–protein complexes in animal cells exposed to various stress factors.

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Abbreviations

miRNA:

microRNA

3'-UTR:

3'-untranslated region

ORF:

open reading frame

HS:

heat shock

ER:

endoplasmic reticulum

References

  1. Kultz D. 2005. Molecular and evolutionary basis of the cellular stress response. Annu. Rev. Physiol. 67, 225–257.

    Article  PubMed  CAS  Google Scholar 

  2. Evgen’ev M., Garbuz D., Zatsepina O. 2013. Heat Shock Proteins and Whole Body Adaptation to Extreme Environments. Berlin: Springer. 218 p.

    Google Scholar 

  3. Szalay M.S., Kovács I.A., Korcsmáros T., Böde C., Csermely P. 2007. Stress-induced rearrangements of cellular networks: Consequences for protection and drug design. FEBS Lett. 581, 3675–3680.

    Article  CAS  PubMed  Google Scholar 

  4. Vigh L., Nakamoto H., Landry J., Gomez-Munoz A., Harwood J.L., Horvath I. 2007. Membrane regulation of the stress response from prokaryotic models to mammalian cells. Ann. NY Acad. Sci. 1113, 40–51.

    Article  CAS  PubMed  Google Scholar 

  5. Toivola D.M., Strnad P., Habtezion A., Omary M.B. 2010. Intermediate filaments take the heat as stress proteins. Trends Cell Biol. 20, 79–91.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Patriarca E.J., Maresca B. 1990. Acquired thermotolerance following heat shock protein synthesis prevents impairment of mitochondrial ATPase activity at elevated temperatures in Saccharomyces cerevisiae. Exp. Cell Res. 190, 57–64.

    Article  CAS  PubMed  Google Scholar 

  7. Buchberger A., Bukau B., Sommer T. 2010. Protein quality control in the cytosol and the endoplasmic reticulum: Brothers in arms. Mol. Cell. 40 (2), 238–252.

    Article  CAS  PubMed  Google Scholar 

  8. Richter K., Haslbeck M., Buchner J. 2010. Life on the verge of death: The heat shock response revisited. Mol. Cell. 40 (2), 253–266.

    Article  CAS  PubMed  Google Scholar 

  9. Raboy B., Sharon G., Parag H.A., Shochat Y., Kulka R.G. 1991. Effect of stress on protein degradation: Role of the ubiquitin system. Acta Biol. Hung. 42, 3–20.

    CAS  PubMed  Google Scholar 

  10. Kroemer G., Marino G., Levine B. 2010. Autophagy and the integrated stress response. Mol. Cell. 40 (2), 280–293.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Voit E.O., Radivoyevitch T. 2000. Biochemical systems analysis of genome-wide expression data. Bioinformatics. 16, 1023–1037.

    Article  CAS  PubMed  Google Scholar 

  12. Malmendal A., Overgaard J., Bundy J.G., Sørensen J.G., Nielsen N.C., Loeschcke V., Holmstrup M. 2006. Metabolomic profiling of heat stress: Hardening and recovery of homeostasis in Drosophila. Am. J. Physiol. Regul. Integr. Comp. Physiol. 291, 205–212.

    Article  CAS  Google Scholar 

  13. Spriggs K.A., Bushell M., Willis A.E. 2010. Translational regulation of gene expression during conditions of cell stress. Mol. Cell. 40 (2), 228–237.

    Article  CAS  PubMed  Google Scholar 

  14. Leung A.K., Sharp P.A. 2010. microRNA functions in stress responses. Mol. Cell. 40 (2), 205–215.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Kulshreshtha R., Ferracin M., Wojcik S., Garzon R., Alder H., Agosto-Perez F., Davaluri R., Liu Ch., Croce C., Negrini M., Calin G.A., Ivam M. 2007. A microRNA signature of hypoxia. Mol. Cell. Biol. 27 (5), 1859–1867.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Wilmink G., Roth C., Ibey B., Ketchum N., Bernhard J., Cerna C., Roach W. 2010. Identification of microRNAs associated with hyperthermia-induced cellular stress response. Cell Str. Chap. 15, 1027–1038.

    Article  CAS  Google Scholar 

  17. Karginov F., Hannon G. 2013. Remodeling of Ago2- mRNA interactions upon cellular stress reflects miRNA complementarity and correlates with altered translation rates. Genes Dev. 27, 1624–1632.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Kruszka K., Pacak A., Swida-Barteczka A., Przemyslaw N., Alaba S., Wroblewska Z., Karlowski W., Jarmolowski A., Szweykowska-Kulinska Z. 2014. Transcriptionally and post-transcriptionally regulated microRNAs in heat stress response in barley. J. Exp. Bot. 65 (20), 6123–6135.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Funikov S., Ryazansky S., Zelentsova E., Popenko V., Leonova O., Garbuz D., Evgen’ev M., Zatsepina O. 2015. The peculiarities of piRNA expression upon heat shock exposure in Drosophila melanogaster. Mob. Genet. Elements. 5 (5), 72–80.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Bushati N., Cohen S. 2007. microRNA functions. Ann. Rev. Cell Dev. Biol. 23, 175–205.

    Article  CAS  Google Scholar 

  21. Bartel D.P. 2009. MicroRNAs: Target recognition and regulatory functions. Cell. 136, 215–233.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Berezikov E. 2011. Evolution of microRNA diversity and regulation in animals. Nat. Rev. Gen. 12, 846–860.

    Article  CAS  Google Scholar 

  23. Reinhart B.J., Slack F., Basson M., Pasquinelli A., Bettinger J., Rougvie A., Horvitz H.R., Ruvkun G. 2000. The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans. Nature. 403, 901–906.

    Article  CAS  PubMed  Google Scholar 

  24. Karres J.S., Hilgers V., Carrera I., Treisman J., Cohen S.M. 2007. The conserved microRNA miR-8 tunes atrophin levels to prevent neurodegeneration in Drosophila. Cell. 131, 136–145.

    Article  CAS  PubMed  Google Scholar 

  25. Wightman B.I., Ruvkun G. 1993. Posttranscriptional regulation of the heterochronic gene lin-14 by lin-4 mediates temporal pattern formation in C. elegans. Cell. 75, 855–862.

    Article  CAS  PubMed  Google Scholar 

  26. Lee R.C., Feinbaum R.L., Ambros V. 1993. The C.elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell. 75, 843–854.

    Article  CAS  PubMed  Google Scholar 

  27. Abbott A.L., Alvarez-Saavedra E., Miska E.A., Lau N.C., Bartel D.P., Horvitz H.R., Ambros V. 2005. The let-7 microRNA family members mir-48, mir-84 and mir-241 function together to regulate developmental timing in Caenorhabditis elegans. Dev. Cell. 9, 403–414.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Sokol N.S., Xu P., Jan Y.N., Ambros V. 2008. Drosophila let-7 microRNA is required for remodeling of the neuromusculature during metamorphosis. Genes Dev. 22 (12), 1591–1596.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Hipfner D.R., Weigmann K., Cohen S.M. 2002. The bantam gene regulates Drosophila growth. Genetics. 161, 1527–1537.

    CAS  PubMed  PubMed Central  Google Scholar 

  30. Brennecke J., Hipfner D., Stark A., Russell R., Cohen S. 2003. Bantam encodes a developmentally regulated microRNA that controls cell proliferation and regulates the proapoptotic gene hid in Drosophila. Cell. 113 (1), 25–36.

    Article  CAS  PubMed  Google Scholar 

  31. Xu P., Vernooy S.Y., Guo M., Hay B.A. 2003. The Drosophila microRNA miR-14 suppresses cell death and is required for normal fat metabolism. Curr. Biol. 13, 790–795.

    Article  CAS  PubMed  Google Scholar 

  32. Zhao Y., Ransom J.F., Li A., Vedantham V., von Drehle M., Muth A.N., Tsuchihashi T., McManus M.T., Schwartz R.J., Srivastava D. 2007. Dysregulation of cardiogenesis, cardiac conduction, and cell cycle in mice lacking miRNA-1-2. Cell. 129, 303–317.

    Article  CAS  PubMed  Google Scholar 

  33. Smibert P., Lai E. 2008. Lessons from microRNA mutants in worms, flies and mice. Cell Cycle. 7 (16), 2500–2508.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Miska E.A., Alvarez-Saavedra E., Abbott A.L., Lau N.C., Hellman A.B., McGonagle S.M., Bartel D.P., Ambros V.R., Horvitz H.R. 2007. Most Caenorhabditis elegans microRNAs are individually not essential for development or viability. PLoS Genet. 3, e215.

    Article  CAS  Google Scholar 

  35. Simon D., Madison J., Conery A., Thompsonpeer K., Soskis M., Ruvkun G., Kaplan J., Kim J. 2008. The microRNA miR-1 regulates a MEF-2-dependent retrograde signal at neuromuscular junctions. Cell. 133, 903–915.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Li X., Cassidy J.J., Reinke C.A., Fischboeck S., Carthew R.W. 2009. A microRNA imparts robustness against environmental fluctuation during development. Cell. 137, 273–282.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Flynt A.S., Thatcher E.J., Burkewitz K., Li N., Liu Y., Patton J.G. 2009. miR-8 microRNAs regulate the response to osmotic stress in zebrafish embryos. J. Cell Biol. 185, 115–127.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Van Rooij E., Sutherland L.B., Qi X., Richardson J.A., Hill J., Olson E.N. 2007. Control of stress dependent cardiac growth and gene expression by a microRNA. Science. 316, 575–579.

    Article  PubMed  CAS  Google Scholar 

  39. Nehammer C., Podolska A., Mackowiak S., Kagias K., Rocock R. 2015. Specific microRNAs regulate heat stress responses in Caenorhabditis elegans. Sci. Rept. 5, 8866.

    Article  CAS  Google Scholar 

  40. Friedman R., Farh K., Burge C., Bartel D. 2009. Most mammalian mRNAs are conserved targets of microRNAs. Genome Res. 19, 92–105.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Sergeeva A.M., Pinzón Restrepo N., Seitz H. 2013. Quantitative aspects of RNA silencing in metazoans. Biochemistry (Moscow). 78 (6), 613–626.

    Article  CAS  Google Scholar 

  42. Krek A., Grun D., Poy M.N., Wolf R., Rosenberg L., Epstein E.J., MacMenamin P., da Piedade I., Gunsalus K.C., Stoffel M., Rajewsky N. 2005. Combinatorial microRNA target predictions. Nat. Genet. 37, 495–500.

    Article  CAS  PubMed  Google Scholar 

  43. Bak R., Mikkelsen J. 2014. miRNA sponges: soaking up miRNAs for regulation of gene expression. WIREs RNA. 5, 317–333.

    Article  CAS  PubMed  Google Scholar 

  44. Place R., Noonan E. 2014. Non-coding RNAs turn up the heat: An emerging layer of novel regulators in the mammalian heat shock response. Cell Str. Chap. 19(2), 159–172.

    Article  CAS  Google Scholar 

  45. Neilson J.R., Sandberg R. 2010. Heterogeneity in mammalian RNA 3' end formation. Exp. Cell Res. 316, 1357–1364.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. O’Connell R.M., Rao D.S., Chaudhuri A.A., Baltimore D. 2010. Physiological and pathological roles for microRNAs in the immune system. Nat. Rev. Immunol. 10, 111–122.

    Article  PubMed  CAS  Google Scholar 

  47. O’Connell R.M., Taganov K.D., Boldin M.P., Cheng G., Baltimore D. 2007. MicroRNA-155 is induced during the macrophage inflammatory response. Proc. Natl. Acad. Sci. U. S. A. 104, 1604–1609.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  48. Karcher D., Bock R. 2002. Temperature sensitivity of RNA editing and intron splicing reactions in the plastid ndhB transcript. Curr. Genet. 41, 48–52.

    Article  CAS  PubMed  Google Scholar 

  49. Stocker J., Huang H.W., Wang H.M., Chang H.W., Chiu C.C., Cho C.L., Tseng C. 2013. Reduction of RNA A-to-I editing in Drosophila acclimated to heat shock. Kaohsiung J. Med. Sci. 29, 478–483.

    Article  PubMed  Google Scholar 

  50. Savva Y.A., Jepson J.E., Sahin A., Sugden A.U., Dorsky J.S., Alpert L., Lawrence C., Reenan R.A. 2012. Auto-regulatory RNA editing fine-tunes mRNA re-coding and complex behaviour in Drosophila. Nat. Commun. 3, 790.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  51. Rieder L., Sawa Y., Reyna M., Chang Y., Dorsky J., Rezaei A., Reenan R. 2015. Dynamic response of RNA editing to temperature in Drosophila. BMC Biol. 13. doi 10.1186/s12915-014-0111-3

  52. Yang Q., Li W., She H., Dou J., Duong D., Du Y., Yang Sh., Seyfried N., Fu H., Gao G., Mao Z. 2015. Stress induces p38 MAPK-mediated phosphorylation and inhibition of Drosha-dependent cell survival. Mol. Cell. 57, 721–734.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Shen J., Xia W., Khotskaya Y.B., Huo L., Nakanishi K., Lim S.O., Du Y., Wang Y., Chang W.C., Chen C.H., Hsu J.L., Wu Y., Lam Y.C., James B.P., Liu X., et al. 2013. EGFR modulates microRNA maturation in response to hypoxia through phosphorylation of AGO2. Nature. 497, 383–387.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Leung A., Vyas S., Rood J., Bhutkar A., Sharp Ph., Chang P. 2011. Poly(ADP-ribose) regulates stress responses and microRNA activity in the cytoplasm. Mol. Cell. 42, 489–499.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Bhattacharyya S., Habermacher R., Martine U., Closs E., Filipowicz W. 2006. Relief of microRNA-mediated translational repression in human cells subjected to stress. Cell. 125, 1111–1124.

    Article  CAS  PubMed  Google Scholar 

  56. Fukuoka M., Yoshida M., Eda A., Takahashi M., Hohjoh H. 2014. Gene silencing mediated by endogenous microRNAs under heat stress conditions in mammalian cells. PLoS ONE. 9 (7), e103130.

    Article  CAS  Google Scholar 

  57. Kundu P., Fabian M., Sonenberg N., Bhattacharyya S., Filipowicz W. 2012. HuR protein attenuates miRNAmediated repression by promoting miRISC dissociation from the target RNA. Nuceic. Acids Res. 40 (11), 5088–5100.

    Article  CAS  Google Scholar 

  58. Srikantan S., Tominaga K., Gorospe M. 2012. Functional interplay between RNA-binding protein HuR and microRNAs. Curr. Protein Pept. Sci. 13 (4), 372–379.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Jacobsen A., Wen J., Marks D., Krogh A. 2010. Signatures of RNA binding proteins globally coupled to effective microRNA target sites. Genome Res. 20 (8), 1010–1019.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Brennan C.M., Steitz J.A. 2001. HuR and mRNA stability. Cell. Mol. Life Sci. 58, 266–277.

    Article  CAS  PubMed  Google Scholar 

  61. Srikantan S., Abdelmohsen K., Lee E.K., Tominaga K., Subaran S.S., Kuwano Y., Kulshrestha R., Panchakshari R., Kim H.H., Yang X., Martindale J.L., Marasa B., Kim M.M., Wersto R.P., Indig F.E., et al. 2011. Translational control of Top2A influences doxorubicin efficacy. Mol. Cell. Biol. 31, 3790–3801.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Tominaga K., Srikantan S., Lee E.K., Subaran S.S., Martindale J.L., Abdelmohsen K., Gorospe M. 2011. Competitive regulation of Nucleolin expression by HuR and miR-494. Mol. Cell. Biol. 31, 4219–4231.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Young L.E., Moore A.E., Sokol L., Meisner-Kober N., Dixon D.A. 2011. The mRNA stability factor HuR inhibits microRNA-16 targeting of cyclooxygenase-2. Mol. Cancer Res. 10 (1), 167–180.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  64. Epis M.R., Barker A., Giles K.M., Beveridge D.J., Leedman P.J. 2011. The RNA-binding protein HuR opposes the repression of ERBB-2 expression by miR-331-3p in prostate cancer cells. J. Biol. Chem. 286 (48), 41442–41454.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Kim H.H., Kuwano Y., Srikantan S., Lee E.K., Martindale J.L., Gorospe M. 2009. HuR recruits let-7/RISC to repress c-Myc expression. Genes Dev. 23, 1743–1748.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Glorian V., Maillot G., Polè s S., Iacovoni J.S., Favre G., Vagner S. 2011. HuR-dependent loading of miRNA RISC to the mRNA encoding the Ras-related small GTPase RhoB controls its translation during UV-induced apoptosis. Cell Death Differ. 18, 1692–1701.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Vasudevan S., Tong Y., Steitz J. 2007. Switching from repression to activation: MicroRNAs can up-regulate translation. Science. 318, 1931–1934.

    Article  CAS  PubMed  Google Scholar 

  68. Kedde M., Strasser M., Boldajipour B., Vrielink O., Slanchev K., Le Sage C., Nagel R., Voorhoeve P., Van Duijse J., Ørom U., Lund A., Perrakis A., Raz E., Agami R. 2007. RNA-binding protein Dnd1 inhibits microRNA access to target mRNA. Cell. 131 (7), 1273–1286.

    Article  CAS  PubMed  Google Scholar 

  69. Hammell C., Lubin I., Boag P., Blackwell T., Ambros V. 2009. nhl-2 Modulates microRNA activity in Caenorhabditis elegans. Cell. 136 (5), 926–938.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Lim D.H., Oh C.T., Lee L., Hong J.S., Noh S.H., Hwang S., Kim S., Han S.J., Lee Y.S. 2011. The endogenous siRNA pathway in Drosophila impacts stress resistance and lifespan by regulating metabolic homeostasis. FEBS Lett. 585, 3079–3085.

    Article  CAS  PubMed  Google Scholar 

  71. Mori M.A., Raghavan P., Thomou T., Boucher J., Robida-Stubbs S., Macotela Y., Russell S.J., Kirkland J.L., Blackwell T.K., Kahn C.R. 2012. Role of microRNA processing in adipose tissue in stress defense and longevity. Cell Metab. 16, 336–347.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Wiesen J.L., Tomasi T.B. 2009. Dicer is regulated by cellular stresses and interferons. Mol. Immunol. 46, 1222–1228.

    Article  CAS  PubMed  Google Scholar 

  73. Spiro Z., Arslan M., Somogyvari M., Nguyen M., Smolders A., Dancso B., Nemeth N., Elek Z., Braeckman B., Csermely P., Soti C. 2012. RNA interference links oxidative stress to the inhibition of heat stress adaptation. Antioxid. Redox Sign. 17, 890–901.

    Article  CAS  Google Scholar 

  74. Anderson P., Kedersha N. 2008. Stress granules: the Tao of RNA triage. Trends Biochem. Sci. 33 (3), 141–150.

    Article  CAS  PubMed  Google Scholar 

  75. Sonenberg N., Hinnebusch A.G. 2009. Regulation of translation initiation in eukaryotes: Mechanisms and biological targets. Cell. 136, 731–745.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Sengupta S., Peterson T.R., Sabatini D.M. 2010. Regulation of the mTOR complex 1 pathway by nutrients, growth factors, and stress. Mol. Cell. 40, 310–322.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Gilks N., Kedersha N., Ayodele M., Shen L., Stoecklin G., Dember L.M., Anderson P. 2004. Stress granule assembly is mediated by prion-like aggregation of TIA-1. Mol. Biol. Cell. 15, 5383–5398.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Emde A., Hornstein E. 2014. miRNAs at the interface of cellular stress and disease. EMBO J. 33, 1428–1437.

    CAS  PubMed  PubMed Central  Google Scholar 

  79. Koscianska E., Starega-Roslan J., Krzyzosiak W.J. 2011. The role of Dicer protein partners in the processing of microRNA precursors. PLoS ONE. 6, e28548.

    Article  CAS  Google Scholar 

  80. Leung A., Calabrese J.M., Sharp P. 2006. Quantitative analysis of Argonaute protein reveals microRNAdependent localization to stress granules. Proc. Natl. Acad. Sci. U. S. A. 103 (48), 18125–18130.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Pare J., Lopez-Orozco J., Hobman T. 2011. MicroRNA-binding is required for recruitment of human Argonaute 2 to stress granules and P-bodies. Biochem. Biophys. Res. Commun. 414 (4), 259–264.

    Article  CAS  PubMed  Google Scholar 

  82. Detzer A., Engel C., Wunsche W., Sczakiel G. 2011. Cell stress is related to re-localization of Argonaute 2 and to decresed RNA interference in human cells. Nucleic Acids Res. 39 (7), 2727–2741.

    Article  CAS  PubMed  Google Scholar 

  83. Decker C., Parker R. 2012. P-bodies and stress granules: possible roles in the control of translation and mRNA degradation. Cold Spr. Harb. Persp. Biol. 4 (9), a012286.

    Google Scholar 

  84. Kedersha N., Stoecklin G., Ayodele M., Yacono P., Lykke-Andersen J., Fritzler M.J., Scheuner D., Kaufman R.J., Golan D., Anderson P. 2006. Stress granules and processing bodies are dynamically linked sites of mRNP remodeling. J. Cell Biol. 169 (6), 871–884.

    Article  CAS  Google Scholar 

  85. Kulkarni M., Ozgur S., Stoecklin G. 2010. On track with P-bodies. Biochem. Soc. Transact. 38, 242–251.

    Article  CAS  Google Scholar 

  86. Liu J., Rivas F., Wohlschlegel J., Yates J. III, Parker R., Hannon G. 2005. A role for the P-body component GW182 in microRNA function. Nat. Cell Biol. 7 (12), 1261–1266.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  87. Eulalio A., Tritschler F., Izaurralde E. 2009. The GW182 protein family in animal cells: New insights into domains required for miRNA-mediated gene silencing. RNA. 15, 1433–1442.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Zeng Y., Sankala H., Zhang X., Graves P.R. 2008. Phosphorylation of Argonaute 2 at serine-387 facilitates its localization to processing bodies. Biochem. J. 413, 429–436.

    Article  CAS  PubMed  Google Scholar 

  89. Gibbings D., Ciaudo C., Erhardt M., Voinnet O. 2009. Multivesicular bodies associate with components of miRNA effector complexes and modulate miRNA activity. Nat. Cell Biol. 11 (9), 1143–1151.

    Article  CAS  PubMed  Google Scholar 

  90. Dedov I., Smirnova O., Golyshev A. 2012. Endoplasmic reticulum stress: A cytological scenario of human disease pathogenesis. Probl. Endokrinol. 5, 57–65.

    Article  Google Scholar 

  91. Zverev Ya., Bryukhanov V. 2012. Endoplasmic reticulum stress in the eyes of a nephrologist. Nefrologiya. 16 (3), 54–71.

    Google Scholar 

  92. Chen Y., Brandizzi F. 2013. IRE1: ER stress sensor and cell fate executor. Trends Cell Biol. 23 (11), 547–555.

    Article  CAS  PubMed  Google Scholar 

  93. Calfon M., Zeng H., Urano F., Till J., Hubbard S., Harding H., Clark S., Ron D. 2002. IRE1 couples endoplasmic reticulum load to secretory capacity by processing the XBP-1 mRNA. Nature. 415, 92–96.

    Article  CAS  PubMed  Google Scholar 

  94. Lee A.H., Chu G.C., Iwakoshi N.N., Glimcher L.H. 2005. XBP-1 is required for biogenesis of cellular secretory machinery of exocrine glands. EMBO J. 24, 4368–4380.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Byrd A.E., Aragon I.V., Brewer J.W. 2012. MicroRNA-30c-2* limits expression of proadaptive factor XBP1 in the unfolded protein response. J. Cell Biol. 196, 689–698.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Duan Q., Wang X., Gong W., Ni L., Chen C., He X., Chen F., Yang L., Wang P., Wang D.W. 2012. ER stress negatively modulates the expression of the miR-199a/214 cluster to regulates tumor survival and progression in human hepatocellular cancer. PLoS ONE. 7 (2), e31518.

    Article  CAS  Google Scholar 

  97. Shuda M., Kondoh N., Imazeki N., Tanaka K., Okada T., Mori K., Hada A., Arai M., Wakatsuki T., Matsubara O., Yamamoto N., Yamamoto M. 2003. Activation of the ATF6, XBP1 and GRP78 genes in human hepatocellular carcinoma: A possible involvement of the ER stress pathway in hepatocarcinogenesis. J. Hepatol. 38, 605–614.

    Article  CAS  PubMed  Google Scholar 

  98. Byrd A., Brewer J. 2013. Micro(RNA) managing endoplasmic reticulum stress. IMBMB Life. 65 (5), 373–381.

    Article  CAS  PubMed  Google Scholar 

  99. Bartoszewski R., Brewer J. W., Rab A., Crossman D.K., Bartoszewska S., Kapoor N., Fuller C., Collawn J., Bebok Z. 2011. The unfolded protein response (UPR)- activated transcription factor X-box-binding protein 1 (XBP1) induces microRNA-346 expression that targets the human antigen peptide transporter 1 (TAP1) mRNA and governs immune regulatory genes. J. Biol. Chem. 286, 41862–41870.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Lankat-Buttgereit B., Tampe R. 2002. The transporter associated with antigen processing: Function and implications in human diseases. Physiol. Rev. 82, 187–204.

    Article  CAS  PubMed  Google Scholar 

  101. Granados D.P., Tanguay P.-L., Hardy M.-P., Caron E., de Verteuil D., Meloche S. Perreault C. 2009. ER stress affects processing of MHC class I-associated peptides. BMC Immunol. 10, 10.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  102. Upton J.P., Wang L., Han D., Wang E.S., Huskey N.E., Lim L., Truitt M., McManus M.T., Ruggero D., Goga A., Papa F., Oakes S.A. 2012. IRE1a cleaves select microRNAs during ER stress to derepress translation of proapoptotic caspase-2. Science. 338, 818–822.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Correspondence to S. Yu. Funikov.

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Original Russian Text © S.Yu. Funikov, O.G. Zatcepina, 2017, published in Molekulyarnaya Biologiya, 2017, Vol. 51, No. 4, pp. 561–572.

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Funikov, S.Y., Zatcepina, O.G. Regulation of microRNA activity in stress. Mol Biol 51, 496–505 (2017). https://doi.org/10.1134/S0026893317030050

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