miR-155-3p drives the development of autoimmune demyelination by regulation of heat shock protein 40

Journal of Neuroscience

Volumn 35, Issue 50, 2015, Pages 16504-16515

  Mycko, Marcin P ^a   Cichalewska, Maria ^a   Cwiklinska, Hanna ^a   Selmaj, Krzysztof W ^a  

^a MEDICAL UNIVERSITY OF LODZ   (Poland)

Author keywords

Autoimmune demyelination; Experimental autoimmune encephalomyelitis; Heat shock proteins; MicroRNA; Multiple sclerosis; T helper cells

Indexed keywords

HEAT SHOCK PROTEIN 40; MICRORNA; MICRORNA 155 3P; UNCLASSIFIED DRUG; DNA BINDING PROTEIN; DNAJB1 PROTEIN, MOUSE; MIRN155 MICRORNA, MOUSE; RAG2 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOIMMUNE DEMYELINATION; CD4+ T LYMPHOCYTE; CELL DIFFERENTIATION; CONTROLLED STUDY; EXPERIMENTAL AUTOIMMUNE ENCEPHALOMYELITIS; FEMALE; FLOW CYTOMETRY; FLUORESCENCE ACTIVATED CELL SORTING; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNOREGULATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UPREGULATION; WESTERN BLOTTING; ANIMAL; C57BL MOUSE; DEMYELINATING DISEASE; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; KNOCKOUT MOUSE; MULTIPLE SCLEROSIS; PATHOLOGY; PHYSIOLOGY; TH17 CELL;

ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; CELL DIFFERENTIATION; DEMYELINATING AUTOIMMUNE DISEASES, CNS; DNA-BINDING PROTEINS; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; FEMALE; GENE EXPRESSION REGULATION; HSP40 HEAT-SHOCK PROTEINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICRORNAS; MULTIPLE SCLEROSIS; TH17 CELLS;

EID: 84949940488     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2830-15.2015     Document Type: Article

References (43)

1. Bettelli E, Carrier Y, Gao W, Korn T, Strom TB, Oukka M, Weiner HL, Kuchroo VK (2006) Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature 441:235-238
2. Bettelli E, Korn T, Oukka M, Kuchroo VK (2008) Induction and effector functions of T(H)17 cells. Nature 453:1051-1057
3. Bronevetsky Y, Villarino AV, Eisley CJ, Barbeau R, Barczak AJ, Heinz GA, Kremmer E, Heissmeyer V, McManus MT, Erle DJ, Rao A, Ansel KM (2013) T cell activation induces proteasomal degradation of Argonaute and rapid remodeling of the microRNA repertoire. J Exp Med 210:417-432
4. Carrer M, Liu N, Grueter CE, Williams AH, Frisard MI, Hulver MW, Bassel-Duby R, Olson EN (2012) Control of mitochondrial metabolism and systemic energy homeostasis by microRNAs 378 and 378*. Proc Natl Acad Sci U S A 109:15330-15335
5. Chiang HR, Schoenfeld LW, Ruby JG, Auyeung VC, Spies N, Baek D, John-ston WK, Russ C, Luo S, Babiarz JE, Blelloch R, Schroth GP, Nusbaum C, Bartel DP (2010) Mammalian microRNAs: experimental evaluation of novel and previously annotated genes. Genes Dev 24:992-1009
6. Cua DJ, Sherlock J, Chen Y, Murphy CA, Joyce B, Seymour B, Lucian L, To W, Kwan S, Churakova T, Zurawski S, Wiekowski M, Lira SA, Gorman D, Kastelein RA, Sedgwick JD (2003) Interleukin-23 rather than interleukin-12 is the critical cytokine for autoimmune inflammation of the brain. Nature 421:744-748
7. Cwiklinska H, Mycko MP, Luvsannorov O, Walkowiak B, Brosnan CF, Raine CS, Selmaj KW (2003) Heat shock protein 70 associations with myelin basic protein and proteolipid protein in multiple sclerosis brains. Int Immunol 15:241-249
8. Duhen R, Glatigny S, Arbelaez CA, Blair TC, Oukka M, Bettelli E (2013) Cutting edge: the pathogenicity of IFN-gamma-producing Th17 cells is independent of T-bet. J Immunol 190:4478-4482
9. Escobar TM, Kanellopoulou C, Kugler DG, Kilaru G, Nguyen CK, Nagarajan V, Bhairavabhotla RK, Northrup D, Zahr R, Burr P, Liu X, Zhao K, Sher A, Jankovic D, Zhu J, Muljo SA (2014) miR-155 activates cytokine gene expression in Th17 cells by regulating the DNA-binding protein Jarid2 to relieve polycomb-mediated repression. Immunity 40:865-879
10. Escobar T, Yu CR, Muljo SA, Egwuagu CE (2013) STAT3 activates miR-155 in Th17 cells and acts in concert to promote experimental autoimmune uveitis. Invest Ophthalmol Vis Sci 54:4017-4025
11. Eugster HP, Frei K, Kopf M, Lassmann H, Fontana A (1998) IL-6-deficient mice resist myelin oligodendrocyte glycoprotein-induced autoimmune encephalomyelitis. Eur J Immunol 28:2178-2187
12. Galazka G, Jurewicz A, Domowicz M, Cannella B, Raine CS, Selmaj K (2014) HINT1 peptide/Hsp70 complex induces NK-cell-dependent immuno-regulation in a model of autoimmune demyelination. Eur J Immunol 44:3026-3044
13. Ghoreschi K, Laurence A, Yang XP, Tato CM, McGeachy MJ, Konkel JE, Ramos HL, Wei L, Davidson TS, Bouladoux N, Grainger JR, Chen Q, Kanno Y, Watford WT, Sun HW, Eberl G, Shevach EM, Belkaid Y, Cua DJ, Chen W, et al. (2010) Generation of pathogenic T(H)17 cells in the absence of TGF-beta signalling. Nature 467:967-971
14. Ghoreschi K, Laurence A, Yang XP, Hirahara K, O’Shea JJ (2011) T helper 17 cell heterogeneity and pathogenicity in autoimmune disease. Trends Immunol 32:395-401
15. Haasch D, Chen YW, Reilly RM, Chiou XG, Koterski S, Smith ML, Kroeger P, McWeeny K, Halbert DN, Mollison KW, Djuric SW, Trevillyan JM (2002) T cell activation induces a noncoding RNA transcript sensitive to inhibition by immunosuppressant drugs and encoded by the proto-oncogene, BIC. Cell Immunol 217:78-86
16. Hafler DA (2004) Multiple sclerosis. J Clin Invest 113:788-794
17. Hu R, Huffaker TB, Kagele DA, Runtsch MC, Bake E, Chaudhuri AA, Round JL, O’Connell RM (2013) MicroRNA-155 confers encephalogenic potential to Th17 cells by promoting effector gene expression. J Immunol 190:5972-5980
18. Hu R, Kagele DA, Huffaker TB, Runtsch MC, Alexander M, Liu J, Bake E, Su W, Williams MA, Rao DS, Möller T, Garden GA, Round JL, O’Connell RM (2014) miR-155 Promotes T follicular helper cell accumulation during chronic, low-grade inflammation. Immunity 41:605-619.
19. Jindra PT, Bagley J, Godwin JG, Iacomini J (2010) Costimulation-dependent expression of microRNA-214 increases the ability of T cells to proliferate by targeting Pten. J Immunol 185:990-997
20. Jinek M, Doudna JA (2009) A three-dimensional view of the molecular machinery of RNA interference. Nature 457:405-412
21. Kampinga HH, Craig EA (2010) The HSP70 chaperone machinery: J proteins as drivers of functional specificity. Nat Rev Mol Cell Biol 11:579-592
22. Lee Y, Awasthi A, Yosef N, Quintana FJ, Xiao S, Peters A, Wu C, Kleinewiet-feld M, Kunder S, Hafler DA, Sobel RA, Regev A, Kuchroo VK (2012) Induction and molecular signature of pathogenic TH17 cells. Nat Immunol 13:991-999
23. Lee Y, Collins M, Kuchroo VK (2014) Unexpected targets and triggers of autoimmunity. J Clin Immunol 34:S56-S60
24. Lewkowicz P, Cwiklińska H, Mycko MP, Cichalewska M, Domowicz M, Lewkowicz N, Jurewicz A, Selmaj KW (2015) Dysregulated RNA-induced silencing complex (RISC) assembly within CNS corresponds with abnormal miRNA expression during autoimmune demyelination. J Neurosci 35:7521-7537
25. Loeb GB, Khan AA, Canner D, Hiatt JB, Shendure J, Darnell RB, Leslie CS, Rudensky AY (2012) Transcriptome-wide miR-155 binding map reveals widespread noncanonical microRNA targeting. Mol Cell 48:760-770
26. Lu LF, Thai TH, Calado DP, Chaudhry A, Kubo M, Tanaka K, Loeb GB, Lee H, Yoshimura A, Rajewsky K, Rudensky AY (2009) Foxp3-dependent microRNA155 confers competitive fitness to regulatory T cells by targeting SOCS1 protein. Immunity 30:80-91
27. Mansilla MJ, Costa C, Eixarch H, Tepavcevic V, Castillo M, Martin R, Lubetzki C, Aigrot MS, Montalban X, Espejo C (2014) Hsp70 regulates immune response in experimental autoimmune encephalomyelitis. PLoS One 9:e105737
28. Meijer HA, Smith EM, Bushell M (2014) Regulation of miRNA strand se-lection: follow the leader? Biochem Soc Trans 42:1135-1140
29. Murugaiyan G, Beynon V, Mittal A, Joller N, Weiner HL (2011) Silencing microRNA-155 ameliorates experimental autoimmune encephalomyelitis. J Immunol 187:2213-2221
30. Mycko MP, Cwiklinska H, Szymanski J, Szymanska B, Kudla G, Kilianek L, Odyniec A, Brosnan CF, Selmaj KW (2004) Inducible heat shock protein 70 promotes myelin autoantigen presentation by the HLA class II. J Immunol 172:202-213
31. Mycko MP, Cwiklinska H, Walczak A, Libert C, Raine CS, Selmaj KW (2008) A heat shock protein gene (Hsp70.1) is critically involved in the generation of the immune response to myelin antigen. Eur J Immunol 38:1999-2013
32. Mycko MP, Cichalewska M, Machlanska A, Cwiklinska H, Mariasiewicz M, Selmaj KW (2012) MicroRNA-301a regulation of a T-helper 17 immune response controls autoimmune demyelination. Proc Natl Acad Sci USA 109:E1248-E1257
33. O’Connell RM, Kahn D, Gibson WS, Round JL, Scholz RL, Chaudhuri AA, Kahn ME, Rao DS, Baltimore D (2010) MicroRNA-155 promotes autoimmune inflammation by enhancing inflammatory T cell development. Immunity 33:607-619
34. Oertli M, Engler DB, Kohler E, Koch M, Meyer TF, Muller A (2011) MicroRNA-155 is essential for the T cell-mediated control of Helicobacter pylori infection and for the induction of chronic gastritis and colitis. J Immunol 187:3578-3586
35. Rauch JN, Gestwicki JE (2014) Binding of human nucleotide exchange factors to heat shock protein 70 (Hsp70) generates functionally distinct complexes in vitro. J Biol Chem 289:1402-1414
36. Ro S, Park C, Young D, Sanders KM, Yan W (2007) Tissue-dependent paired expression of miRNAs. Nucleic Acids Res 35:5944-5953
37. Rodriguez A, Vigorito E, Clare S, Warren MV, Couttet P, Soond DR, van Dongen S, Grocock RJ, Das PP, Miska EA, Vetrie D, Okkenhaug K, En-right AJ, Dougan G, Turner M, Bradley A (2007) Requirement of bic/microRNA-155 for normal immune function. Science 316:608-611.
38. Selbach M, Schwanhäusser B, Thierfelder N, Fang Z, Khanin R, Rajewsky N (2008) Widespread changes in protein synthesis induced by microRNAs. Nature 455:58-63
39. Sospedra M, Martin R (2005) Immunology of multiple sclerosis. Annu Rev Immunol 23:683-747
40. Tarassishin L, Loudig O, Bauman A, Shafit-Zagardo B, Suh HS, Lee SC (2011) Interferon regulatory factor 3 inhibits astrocyte inflammatory gene expression through suppression of the proinflammatory miR-155 and miR-155*. Glia 59:1911-1922
41. Wang Y, Juranek S, Li H, Sheng G, Wardle GS, Tuschl T, Patel DJ (2009) Nucleation, propagation and cleavage of target RNAs in Ago silencing complexes. Nature 461:754-761
42. Xiao C, Rajewsky K (2009) MicroRNA control in the immune system: basic principles. Cell 136:26-36
43. Zhou H, Huang X, Cui H, Luo X, Tang Y, Chen S, Wu L, Shen N (2010) miR-155 and its star-form partner miR-155* cooperatively regulate type I interferon production by human plasmacytoid dendritic cells. Blood 116: 5885-5894