Reversible HuR-microRNA binding controls extracellular export of miR-122 and augments stress response

EMBO Reports

Volumn 17, Issue 8, 2016, Pages 1184-1203

  Mukherjee, Kamalika ^a   Ghoshal, Bartika ^a   Ghosh, Souvik ^a,c   Chakrabarty, Yogaditya ^a   Shwetha, Shivaprasad ^b   Das, Saumitra ^b   Bhattacharyya, Suvendra N ^a  

^a INDIAN INSTITUTE OF CHEMICAL BIOLOGY   (India)

^b INDIAN INSTITUTE OF SCIENCE   (India)

^c UNIVERSITY OF BASEL   (Switzerland)

Author keywords

Ago; extracellular vesicles; HuR; miRNA export; miRNAs; ubiquitination

Indexed keywords

ARGONAUTE 2 PROTEIN; ELAV PROTEIN; INITIATION FACTOR 2ALPHA; MAMMALIAN TARGET OF RAPAMYCIN; MICRORNA 122; 3' UNTRANSLATED REGION; ARGONAUTE PROTEIN; EIF2C2 PROTEIN, HUMAN; ELAV LIKE PROTEIN 1; MICRORNA; MIRN122 MICRORNA, HUMAN; PROTEIN BINDING; TARGET OF RAPAMYCIN KINASE;

3' UNTRANSLATED REGION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUTOPHAGY; BINDING AFFINITY; CELL STRESS; CELL TRANSPORT; CONJUGATION; CONTROLLED STUDY; EXOSOME; HEPATOMA CELL; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; IN VITRO STUDY; IN VIVO STUDY; LIVER CELL; MOUSE; MULTIVESICULAR BODY; NONHUMAN; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN PHOSPHORYLATION; PROTEIN RNA BINDING; REDUCTION; RNA BINDING; STRESS; UBIQUITINATION; BIOLOGICAL MODEL; GENETICS; METABOLISM; PHYSIOLOGICAL STRESS; RNA TRANSPORT; TUMOR CELL LINE;

3' UNTRANSLATED REGIONS; ARGONAUTE PROTEINS; CELL LINE, TUMOR; ELAV-LIKE PROTEIN 1; EXTRACELLULAR VESICLES; HEPATOCYTES; HUMANS; MICRORNAS; MODELS, BIOLOGICAL; PROTEIN BINDING; RNA TRANSPORT; STRESS, PHYSIOLOGICAL; TOR SERINE-THREONINE KINASES; UBIQUITINATION;

EID: 84978786186     PISSN: 1469221X     EISSN: 14693178     Source Type: Journal    
DOI: 10.15252/embr.201541930     Document Type: Article

References (57)

1. Bartel DP (2009) MicroRNAs: target recognition and regulatory functions. Cell 136: 215–233
2. Iorio MV, Croce CM (2012) MicroRNA dysregulation in cancer: diagnostics, monitoring and therapeutics. A comprehensive review. EMBO Mol Med 4: 143–159
3. Mendell JT, Olson EN (2012) MicroRNAs in stress signaling and human disease. Cell 148: 1172–1187
4. Lu J, Getz G, Miska EA, Alvarez-Saavedra E, Lamb J, Peck D, Sweet-Cordero A, Ebert BL, Mak RH, Ferrando AA et al (2005) MicroRNA expression profiles classify human cancers. Nature 435: 834–838
5. Filipowicz W, Bhattacharyya SN, Sonenberg N (2008) Mechanisms of post-transcriptional regulation by microRNAs: are the answers in sight? Nat Rev Genet 9: 102–114
6. Huntzinger E, Izaurralde E (2011) Gene silencing by microRNAs: contributions of translational repression and mRNA decay. Nat Rev Genet 12: 99–110
7. Bushati N, Cohen SM (2007) microRNA functions. Annu Rev Cell Dev Biol 23: 175–205
8. Hatfield SD, Shcherbata HR, Fischer KA, Nakahara K, Carthew RW, Ruohola-Baker H (2005) Stem cell division is regulated by the microRNA pathway. Nature 435: 974–978
9. Sood P, Krek A, Zavolan M, Macino G, Rajewsky N (2006) Cell-type-specific signatures of microRNAs on target mRNA expression. Proc Natl Acad Sci USA 103: 2746–2751
10. Ghosh S, Bose M, Ray A, Bhattacharyya SN (2015) Polysome arrest restricts miRNA turnover by preventing their exosomal export in growth retarded mammalian cells. Mol Biol Cell 26: 1072–1083
11. Krol J, Busskamp V, Markiewicz I, Stadler MB, Ribi S, Richter J, Duebel J, Bicker S, Fehling HJ, Schubeler D et al (2010) Characterizing light-regulated retinal microRNAs reveals rapid turnover as a common property of neuronal microRNAs. Cell 141: 618–631
12. Gallo A, Tandon M, Alevizos I, Illei GG (2012) The majority of microRNAs detectable in serum and saliva is concentrated in exosomes. PLoS One 7: e30679
13. Turchinovich A, Burwinkel B (2012) Distinct AGO1 and AGO2 associated miRNA profiles in human cells and blood plasma. RNA Biol 9: 1066–1075
14. Chen X, Liang H, Zhang J, Zen K, Zhang CY (2012) Secreted microRNAs: a new form of intercellular communication. Trends Cell Biol 22: 125–132
15. Cortez MA, Bueso-Ramos C, Ferdin J, Lopez-Berestein G, Sood AK, Calin GA (2011) MicroRNAs in body fluids–the mix of hormones and biomarkers. Nat Rev Clin Oncol 8: 467–477
16. Wagner J, Riwanto M, Besler C, Knau A, Fichtlscherer S, Roxe T, Zeiher AM, Landmesser U, Dimmeler S (2013) Characterization of levels and cellular transfer of circulating lipoprotein-bound microRNAs. Arterioscler Thromb Vasc Biol 33: 1392–1400
17. Vickers KC, Palmisano BT, Shoucri BM, Shamburek RD, Remaley AT (2011) MicroRNAs are transported in plasma and delivered to recipient cells by high-density lipoproteins. Nat Cell Biol 13: 423–433
18. Liang H, Yan X, Pan Y, Wang Y, Wang N, Li L, Liu Y, Chen X, Zhang CY, Gu H et al (2015) MicroRNA-223 delivered by platelet-derived microvesicles promotes lung cancer cell invasion via targeting tumor suppressor EPB41L3. Mol Cancer 14: 58
19. Montecalvo A, Larregina AT, Shufesky WJ, Stolz DB, Sullivan ML, Karlsson JM, Baty CJ, Gibson GA, Erdos G, Wang Z et al (2012) Mechanism of transfer of functional microRNAs between mouse dendritic cells via exosomes. Blood 119: 756–766
20. Mittelbrunn M, Gutierrez-Vazquez C, Villarroya-Beltri C, Gonzalez S, Sanchez-Cabo F, Gonzalez MA, Bernad A, Sanchez-Madrid F (2011) Unidirectional transfer of microRNA-loaded exosomes from T cells to antigen-presenting cells. Nat Commun 2: 282
21. Kosaka N, Iguchi H, Yoshioka Y, Takeshita F, Matsuki Y, Ochiya T (2010) Secretory mechanisms and intercellular transfer of microRNAs in living cells. J Biol Chem 285: 17442–17452
22. Pegtel DM, Cosmopoulos K, Thorley-Lawson DA, van Eijndhoven MA, Hopmans ES, Lindenberg JL, de Gruijl TD, Wurdinger T, Middeldorp JM (2010) Functional delivery of viral miRNAs via exosomes. Proc Natl Acad Sci USA 107: 6328–6333
23. Skog J, Wurdinger T, van Rijn S, Meijer DH, Gainche L, Sena-Esteves M, Curry WT Jr, Carter BS, Krichevsky AM, Breakefield XO (2008) Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat Cell Biol 10: 1470–1476
24. Valadi H, Ekstrom K, Bossios A, Sjostrand M, Lee JJ, Lotvall JO (2007) Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol 9: 654–659
25. Basu S, Bhattacharyya SN (2014) Insulin-like growth factor-1 prevents miR-122 production in neighbouring cells to curtail its intercellular transfer to ensure proliferation of human hepatoma cells. Nucleic Acids Res 42: 7170–7185
26. Leung AK, Sharp PA (2010) MicroRNA functions in stress responses. Mol Cell 40: 205–215
27. Stern-Ginossar N, Gur C, Biton M, Horwitz E, Elboim M, Stanietsky N, Mandelboim M, Mandelboim O (2008) Human microRNAs regulate stress-induced immune responses mediated by the receptor NKG2D. Nat Immunol 9: 1065–1073
28. Franco-Zorrilla JM, Valli A, Todesco M, Mateos I, Puga MI, Rubio-Somoza I, Leyva A, Weigel D, Garcia JA, Paz-Ares J (2007) Target mimicry provides a new mechanism for regulation of microRNA activity. Nat Genet 39: 1033–1037
29. Bhattacharyya SN, Habermacher R, Martine U, Closs EI, Filipowicz W (2006) Relief of microRNA-mediated translational repression in human cells subjected to stress. Cell 125: 1111–1124
30. Meisner NC, Filipowicz W (2010) Properties of the regulatory RNA-binding protein HuR and its role in controlling miRNA repression. Adv Exp Med Biol 700: 106–123
31. Young LE, Moore AE, Sokol L, Meisner-Kober N, Dixon DA (2012) The mRNA stability factor HuR inhibits microRNA-16 targeting of COX-2. Mol Cancer Res 10: 167–180
32. Poria DK, Guha A, Nandi I, Ray PS (2016) RNA-binding protein HuR sequesters microRNA-21 to prevent translation repression of proinflammatory tumor suppressor gene programmed cell death 4. Oncogene 35: 1703–1715
33. Thiaville MM, Pan YX, Gjymishka A, Zhong C, Kaufman RJ, Kilberg MS (2008) MEK signaling is required for phosphorylation of eIF2alpha following amino acid limitation of HepG2 human hepatoma cells. J Biol Chem 283: 10848–10857
34. Ghislat G, Patron M, Rizzuto R, Knecht E (2012) Withdrawal of essential amino acids increases autophagy by a pathway involving Ca2+/calmodulin-dependent kinase kinase-beta (CaMKK-beta). J Biol Chem 287: 38625–38636
35. Mukherjee N, Corcoran DL, Nusbaum JD, Reid DW, Georgiev S, Hafner M, Ascano M Jr, Tuschl T, Ohler U, Keene JD (2011) Integrative regulatory mapping indicates that the RNA-binding protein HuR couples pre-mRNA processing and mRNA stability. Mol Cell 43: 327–339
36. Kundu P, Fabian MR, Sonenberg N, Bhattacharyya SN, Filipowicz W (2012) HuR protein attenuates miRNA-mediated repression by promoting miRISC dissociation from the target RNA. Nucleic Acids Res 40: 5088–5100
37. Gibbings DJ, Ciaudo C, Erhardt M, Voinnet O (2009) Multivesicular bodies associate with components of miRNA effector complexes and modulate miRNA activity. Nat Cell Biol 11: 1143–1149
38. Abdelmohsen K, Srikantan S, Yang X, Lal A, Kim HH, Kuwano Y, Galban S, Becker KG, Kamara D, de Cabo R et al (2009) Ubiquitin-mediated proteolysis of HuR by heat shock. EMBO J 28: 1271–1282
39. Zhou HL, Geng C, Luo G, Lou H (2013) The p97-UBXD8 complex destabilizes mRNA by promoting release of ubiquitinated HuR from mRNP. Genes Dev 27: 1046–1058
40. Yoon JH, Abdelmohsen K, Kim J, Yang X, Martindale JL, Tominaga-Yamanaka K, White EJ, Orjalo AV, Rinn JL, Kreft SG et al (2013) Scaffold function of long non-coding RNA HOTAIR in protein ubiquitination. Nat Commun 4: 2939
41. Koppers-Lalic D, Hackenberg M, Bijnsdorp IV, van Eijndhoven MA, Sadek P, Sie D, Zini N, Middeldorp JM, Ylstra B, de Menezes RX et al (2014) Nontemplated nucleotide additions distinguish the small RNA composition in cells from exosomes. Cell Rep 8: 1649–1658
42. Lima WF, Wu H, Nichols JG, Sun H, Murray HM, Crooke ST (2009) Binding and cleavage specificities of human Argonaute2. J Biol Chem 284: 26017–26028
43. Tan GS, Garchow BG, Liu X, Yeung J, Morris JP, Cuellar TL, McManus MT, Kiriakidou M (2009) Expanded RNA-binding activities of mammalian Argonaute 2. Nucleic Acids Res 37: 7533–7545
44. Dai W, Zhang G, Makeyev EV (2012) RNA-binding protein HuR autoregulates its expression by promoting alternative polyadenylation site usage. Nucleic Acids Res 40: 787–800
45. Katzmann DJ, Babst M, Emr SD (2001) Ubiquitin-dependent sorting into the multivesicular body pathway requires the function of a conserved endosomal protein sorting complex, ESCRT-I. Cell 106: 145–155
46. Keller S, Sanderson MP, Stoeck A, Altevogt P (2006) Exosomes: from biogenesis and secretion to biological function. Immunol Lett 107: 102–108
47. Luna JM, Scheel TK, Danino T, Shaw KS, Mele A, Fak JJ, Nishiuchi E, Takacs CN, Catanese MT, de Jong YP et al (2015) Hepatitis C virus RNA functionally sequesters miR-122. Cell 160: 1099–1110
48. Shwetha S, Kumar A, Mullick R, Vasudevan D, Mukherjee N, Das S (2015) HuR displaces polypyrimidine tract binding protein to facilitate la binding to the 3' untranslated region and enhances hepatitis C virus replication. J Virol 89: 11356–11371
49. Villarroya-Beltri C, Gutierrez-Vazquez C, Sanchez-Cabo F, Perez-Hernandez D, Vazquez J, Martin-Cofreces N, Martinez-Herrera DJ, Pascual-Montano A, Mittelbrunn M, Sanchez-Madrid F (2013) Sumoylated hnRNPA2B1 controls the sorting of miRNAs into exosomes through binding to specific motifs. Nat Commun 4: 2980
50. Cha DJ, Franklin JL, Dou Y, Liu Q, Higginbotham JN, Demory Beckler M, Weaver AM, Vickers K, Prasad N, Levy S et al (2015) KRAS-dependent sorting of miRNA to exosomes. eLife 4: e07197
51. Ostrowski M, Carmo NB, Krumeich S, Fanget I, Raposo G, Savina A, Moita CF, Schauer K, Hume AN, Freitas RP et al (2010) Rab27a and Rab27b control different steps of the exosome secretion pathway. Nat Cell Biol 12: 19–30
52. de la Mata M, Gaidatzis D, Vitanescu M, Stadler MB, Wentzel C, Scheiffele P, Filipowicz W, Grosshans H (2015) Potent degradation of neuronal miRNAs induced by highly complementary targets. EMBO Rep 16: 500–511
53. Squadrito ML, Baer C, Burdet F, Maderna C, Gilfillan GD, Lyle R, Ibberson M, De Palma M (2014) Endogenous RNAs modulate microRNA sorting to exosomes and transfer to acceptor cells. Cell Rep 8: 1432–1446
54. Mazumder A, Bose M, Chakraborty A, Chakrabarti S, Bhattacharyya SN (2013) A transient reversal of miRNA-mediated repression controls macrophage activation. EMBO Rep 14: 1008–1016
55. Thery C, Amigorena S, Raposo G, Clayton A (2006) Isolation and characterization of exosomes from cell culture supernatants and biological fluids. Curr Protoc Cell Biol Chapter 3: Unit 3.22
56. Ji H, Greening DW, Barnes TW, Lim JW, Tauro BJ, Rai A, Xu R, Adda C, Mathivanan S, Zhao W et al (2013) Proteome profiling of exosomes derived from human primary and metastatic colorectal cancer cells reveal differential expression of key metastatic factors and signal transduction components. Proteomics 13: 1672–1686
57. Tauro BJ, Greening DW, Mathias RA, Ji H, Mathivanan S, Scott AM, Simpson RJ (2012) Comparison of ultracentrifugation, density gradient separation, and immunoaffinity capture methods for isolating human colon cancer cell line LIM1863-derived exosomes. Methods 56: 293–304