508
Views
15
CrossRef citations to date
0
Altmetric
Article

Emerging roles of noncoding RNAs in T cell differentiation and functions in autoimmune diseases

&
Pages 232-245 | Received 07 Jun 2019, Accepted 22 Jul 2019, Published online: 14 Aug 2019

References

  • Carninci P, Kasukawa T, Katayama S, et al. The transcriptional landscape of the mammalian genome. Science 2005;309(5740):1559–1563. Epub 2005/09/06.doi: 10.1126/science.1112014.
  • Djebali S, Davis CA, Merkel A, et al. Landscape of transcription in human cells. Nature 2012;489(7414):101–108. Epub 2012/09/08. doi: 10.1038/nature11233.
  • Mattick JS. RNA regulation: a new genetics?. Nat Rev Genet. 2004;5(4):316–323. Epub 2004/05/08. doi: 10.1038/nrg1321.
  • Sakaguchi S, Yamaguchi T, Nomura T, Ono M. Regulatory T cells and immune tolerance. Cell 2008;133(5):775–787. Epub 2008/05/31. doi: 10.1016/j.cell.2008.05.009.
  • Asseman C, Mauze S, Leach MW, Coffman RL, Powrie F. An essential role for interleukin 10 in the function of regulatory T cells that inhibit intestinal inflammation. J Exp Med. 1999;190(7):995–1004. Epub 1999/10/06. doi: 10.1084/jem.190.7.995.
  • Watanabe N, Nakajima H. Coinhibitory molecules in autoimmune diseases. Clin Dev Immunol. 2012;2012:1. Epub 2012/09/22. doi: 10.1155/2012/269756.
  • Costenbader KH, Gay S, Alarcon-Riquelme ME, Iaccarino L, Doria A. Genes, epigenetic regulation and environmental factors: which is the most relevant in developing autoimmune diseases?. Autoimmunity Reviews. 2012;11(8):604–609. Epub 2011/11/02. doi: 10.1016/j.autrev.2011.10.022.
  • Long H, Yin H, Wang L, Gershwin ME, Lu Q. The critical role of epigenetics in systemic lupus erythematosus and autoimmunity. J Autoimmun. 2016;74:118–138. Epub 2016/10/26. doi: 10.1016/j.jaut.2016.06.020.
  • Mercer TR, Dinger ME, Mattick JS. Long non-coding RNAs: insights into functions. Nat Rev Genet. 2009;10(3):155–159. Epub 2009/02/04. doi: 10.1038/nrg2521.
  • Wang KC, Chang HY. Molecular mechanisms of long noncoding RNAs. Molecular Cell. 2011;43(6):904–914. Epub 2011/09/20. doi: 10.1016/j.molcel.2011.08.018.
  • Ponting CP, Oliver PL, Reik W. Evolution and functions of long noncoding RNAs. Cell 2009;136(4):629–641. Epub 2009/02/26. doi: 10.1016/j.cell.2009.02.006.
  • Moran VA, Perera RJ, Khalil AM. Emerging functional and mechanistic paradigms of mammalian long non-coding RNAs. Nucleic Acids Res. 2012;40(14):6391–6400. Epub 2012/04/12. doi: 10.1093/nar/gks296.
  • Guttman M, Amit I, Garber M, et al. Chromatin signature reveals over a thousand highly conserved large non-coding RNAs in mammals. Nature 2009;458(7235):223–227. Epub 2009/02/03. doi: 10.1038/nature07672.
  • Zheng GX, Do BT, Webster DE, Khavari PA, Chang HY. Dicer-microRNA-Myc circuit promotes transcription of hundreds of long noncoding RNAs. Nat Struct Mol Biol. 2014;21(7):585–590. Epub 2014/06/16. doi: 10.1038/nsmb.2842.
  • Li K, Ramchandran R. Natural antisense transcript: a concomitant engagement with protein-coding transcript. Oncotarget 2010;1(6):447–452. Epub 2011/02/12. doi: 10.18632/oncotarget.178.
  • Uesaka M, Nishimura O, Go Y, Nakashima K, Agata K, Imamura T. Bidirectional promoters are the major source of gene activation-associated non-coding RNAs in mammals. BMC Genomics. 2014;15(1):35. Epub 2014/01/21. doi: 10.1186/1471-2164-15-35.
  • Seila AC, Calabrese JM, Levine SS, et al. Divergent transcription from active promoters. Science 2008;322(5909):1849–1851. Epub 2008/12/06. doi: 10.1126/science.1162253.
  • Andersson R, Gebhard C, Miguel-Escalada I, et al. An atlas of active enhancers across human cell types and tissues. Nature 2014;507(7493):455–461. Epub 2014/03/29. doi: 10.1038/nature12787.
  • Salzman J, Gawad C, Wang PL, Lacayo N, Brown PO. Circular RNAs are the predominant transcript isoform from hundreds of human genes in diverse cell types. PloS One. 2012;7(2):e30733. Epub 2012/02/10. doi: 10.1371/journal.pone.0030733.
  • Li Z, Huang C, Bao C, et al. Exon-intron circular RNAs regulate transcription in the nucleus. Nat Struct Mol Biol. 2015;22(3):256–264. Epub 2015/02/11. doi: 10.1038/nsmb.2959.
  • Geisler S, Lojek L, Khalil AM, Baker KE, Coller J. Decapping of long noncoding RNAs regulates inducible genes. Molecular Cell. 2012;45(3):279–291. Epub 2012/01/10. doi: 10.1016/j.molcel.2011.11.025.
  • Wery M, Descrimes M, Vogt N, Dallongeville AS, Gautheret D, Morillon A. Nonsense-mediated decay restricts LncRNA levels in yeast unless blocked by double-stranded RNA structure. Molecular Cell. 2016;61(3):379–392. Epub 2016/01/26. doi: 10.1016/j.molcel.2015.12.020.
  • Guttman M, Rinn JL. Modular regulatory principles of large non-coding RNAs. Nature 2012;482(7385):339–346. Epub 2012/02/18. doi: 10.1038/nature10887.
  • Ulitsky I, Bartel DP. lincRNAs: genomics, evolution, and mechanisms. Cell 2013;154(1):26–46. Epub 2013/07/06. doi: 10.1016/j.cell.2013.06.020.
  • Chen YG, Satpathy AT, Chang HY. Gene regulation in the immune system by long noncoding RNAs. Nat Immunol. 2017;18(9):962–972. Epub 2017/08/23. doi: 10.1038/ni.3771.
  • Usui T, Preiss JC, Kanno Y, et al. T-bet regulates Th1 responses through essential effects on GATA-3 function rather than on IFNG gene acetylation and transcription. J Exp Med. 2006;203(3):755–766. Epub 2006/03/08. doi: 10.1084/jem.20052165.
  • Ranzani V, Rossetti G, Panzeri I, et al. The long intergenic noncoding RNA landscape of human lymphocytes highlights the regulation of T cell differentiation by linc-MAF-4. Nat Immunol. 2015;16(3):318–325. Epub 2015/01/27. doi: 10.1038/ni.3093.
  • Collier SP, Collins PL, Williams CL, Boothby MR, Aune TM. Cutting edge: influence of Tmevpg1, a long intergenic noncoding RNA, on the expression of Ifng by Th1 cells. JI. 2012;189(5):2084–2088. Epub 2012/08/02. doi: 10.4049/jimmunol.1200774.
  • Gomez JA, Wapinski OL, Yang YW, et al. The NeST long ncRNA controls microbial susceptibility and epigenetic activation of the interferon-gamma locus. Cell 2013;152(4):743–754. Epub 2013/02/19. doi: 10.1016/j.cell.2013.01.015.
  • Sekimata M, Perez-Melgosa M, Miller SA, et al. CCCTC-binding factor and the transcription factor T-bet orchestrate T helper 1 cell-specific structure and function at the interferon-gamma locus. Immunity 2009;31(4):551–564. Epub 2009/10/13. doi: 10.1016/j.immuni.2009.08.021.
  • Hu G, Tang Q, Sharma S, et al. Expression and regulation of intergenic long noncoding RNAs during T cell development and differentiation. Nat Immunol. 2013;14(11):1190–1198. Epub 2013/09/24. doi: 10.1038/ni.2712.
  • Spurlock CF, Tossberg JT, Guo Y, et al. Expression and functions of long noncoding RNAs during human T helper cell differentiation. Nat Commun. 2015;6(1):6932. Epub 2015/04/24. doi: 10.1038/ncomms7932.
  • Koh BH, Hwang SS, Kim JY, et al. Th2 LCR is essential for regulation of Th2 cytokine genes and for pathogenesis of allergic asthma. Proceedings of the National Academy of Sciences of the United States of America. 2010;107(23):10614–10619. Epub 2010/05/21. doi: 10.1073/pnas.1005383107.
  • Gibbons HR, Shaginurova G, Kim LC, Chapman N, Spurlock CF, 3rd, Aune TM. Divergent lncRNA GATA3-AS1 Regulates GATA3 Transcription in T-Helper 2 Cells. Front Immunol. 2018;9:2512Epub 2018/11/14.doi: 10.3389/fimmu.2018.02512.
  • Teimuri S, Hosseini A, Rezaenasab A, et al. Integrative analysis of lncRNAs in Th17 cell lineage to discover new potential biomarkers and therapeutic targets in autoimmune diseases. Molecular Therapy Nucleic Acids. 2018;12:393–404. Epub 2018/09/10. doi: 10.1016/j.omtn.2018.05.022.
  • Shui X, Chen S, Lin J, Kong J, Zhou C, Wu J. Knockdown of lncRNA NEAT1 inhibits Th17/CD4(+) T cell differentiation through reducing the STAT3 protein level. J Cell Physiol. 2019; Epub 2019/05/24. doi: 10.1002/jcp.28811.
  • Zemmour D, Pratama A, Loughhead SM, Mathis D, Benoist C. Flicr, a long noncoding RNA, modulates Foxp3 expression and autoimmunity. Proc Natl Acad Sci USA. 2017;114(17):E3472–E80. Epub 2017/04/12. doi: 10.1073/pnas.1700946114.
  • Shi X, Sun M, Liu H, Yao Y, Song Y. Long non-coding RNAs: a new frontier in the study of human diseases. Cancer Lett. 2013;339(2):159–166. Epub 2013/06/25. doi: 10.1016/j.canlet.2013.06.013.
  • Li J, Xuan Z, Liu C. Long non-coding RNAs and complex human diseases. Ijms. 2013;14(9):18790–18808. Epub 2013/09/17. doi: 10.3390/ijms140918790.
  • Suarez-Gestal M, Calaza M, Endreffy E, et al. Replication of recently identified systemic lupus erythematosus genetic associations: a case-control study. Arthritis Res Ther. 2009;11(3):R69. Epub 2009/05/16. doi: 10.1186/ar2698.
  • Kino T, Hurt DE, Ichijo T, Nader N, Chrousos GP. Noncoding RNA gas5 is a growth arrest- and starvation-associated repressor of the glucocorticoid receptor. Sci Signal. 2010;3(107):ra8. Epub 2010/02/04. doi: 10.1126/scisignal.2000568.
  • Solus JF, Chung CP, Oeser A, et al. Genetics of serum concentration of IL-6 and TNFalpha in systemic lupus erythematosus and rheumatoid arthritis: a candidate gene analysis. Clin Rheumatol. 2015;34(8):1375–1382. Epub 2015/02/06. doi: 10.1007/s10067-015-2881-6.
  • Song J, Kim D, Han J, Kim Y, Lee M, Jin EJ. PBMC and exosome-derived Hotair is a critical regulator and potent marker for rheumatoid arthritis. Clin Exp Med. 2015;15(1):121–126. Epub 2014/04/12. doi: 10.1007/s10238-013-0271-4.
  • Sonkoly E, Bata-Csorgo Z, Pivarcsi A, et al. Identification and characterization of a novel, psoriasis susceptibility-related noncoding RNA gene, PRINS. J Biol Chem. 2005;280(25):24159–24167. Epub 2005/04/28. doi: 10.1074/jbc.M501704200.
  • Szegedi K, Sonkoly E, Nagy N, et al. The anti-apoptotic protein G1P3 is overexpressed in psoriasis and regulated by the non-coding RNA. PRINS. Exp Dermatol. 2010;19(3):269–278. Epub 2010/04/10. doi: 10.1111/j.1600-0625.2010.01066.x.
  • Holm SJ, Sanchez F, Carlen LM, et al. HLA-Cw*0602 associates more strongly to psoriasis in the Swedish population than variants of the novel 6p21.3 gene PSORS1C3. Acta Derm Venereol. 2005;85(1):2–8. Epub 2005/04/26. doi: 10.1080/00015550410023527.
  • Dong YH, Fu DG. Autoimmune thyroid disease: mechanism, genetics and current knowledge. Eur Rev Med Pharmacol Sci 2014;18(23):3611–3618. Epub 2014/12/24.
  • McFarland HF, Martin R. Multiple sclerosis: a complicated picture of autoimmunity. Nat Immunol. 2007;8(9):913–919. Epub 2007/08/23. doi: 10.1038/ni1507.
  • Santoro M, Nociti V, Lucchini M, et al. Expression Profile of Long Non-Coding RNAs in Serum of Patients with Multiple Sclerosis. J Mol Neurosci. 2016;59(1):18–23. Epub 2016/04/02. doi: 10.1007/s12031-016-0741-8.
  • Khalil AM, Guttman M, Huarte M, et al. Many human large intergenic noncoding RNAs associate with chromatin-modifying complexes and affect gene expression. Pnas. 2009;106(28):11667–11672. Epub 2009/07/03. doi: 10.1073/pnas.0904715106.
  • Imamura K, Imamachi N, Akizuki G, et al. Long noncoding RNA NEAT1-dependent SFPQ relocation from promoter region to paraspeckle mediates IL8 expression upon immune stimuli. Molecular Cell. 2014;53(3):393–406. Epub 2014/02/11. doi: 10.1016/j.molcel.2014.01.009.
  • Fox RI. Sjogren's syndrome. Lancet 2005;366(9482):321–331. Epub 2005/07/26. doi: 10.1016/S0140-6736(05)66990-5.
  • Gaidamakov S, Maximova OA, Chon H, et al. Targeted deletion of the gene encoding the La autoantigen (Sjogren's syndrome antigen B) in B cells or the frontal brain causes extensive tissue loss. Mol Cell Biol. 2014;34(1):123–131. Epub 2013/11/06. doi: 10.1128/MCB.01010-13.
  • Wallace C, Smyth DJ, Maisuria-Armer M, , et al. The imprinted DLK1-MEG3 gene region on chromosome 14q32.2 alters susceptibility to type 1 diabetes. Nat Genet. 2010;42(1):68–71. Epub 2009/12/08. doi: 10.1038/ng.493.
  • Millis MP, Bowen D, Kingsley C, , et al. Variants in the plasmacytoma variant translocation gene (PVT1) are associated with end-stage renal disease attributed to type 1 diabetes. Diabetes 2007;56(12):3027–3032. Epub 2007/09/21. doi: 10.2337/db07-0675.
  • Baumgart DC, Sandborn WJ. Crohn's disease. Lancet 2012;380(9853):1590–1605. Epub 2012/08/24. doi: 10.1016/S0140-6736(12)60026-9.
  • Qiao YQ, Huang ML, Xu AT, et al. LncRNA DQ786243 affects Treg related CREB and Foxp3 expression in Crohn's disease. J Biomed Sci. 2013;20(1):87. Epub 2013/12/03. doi: 10.1186/1423-0127-20-87.
  • Lee RC, Feinbaum RL, Ambros V. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 1993;75(5):843–854. Epub 1993/12/03. doi: 10.1016/0092-8674(93)90529-Y.
  • Wightman B, Ha I, Ruvkun G. Posttranscriptional regulation of the heterochronic gene lin-14 by lin-4 mediates temporal pattern formation in C. elegans. Cell 1993;75(5):855–862. Epub 1993/12/03. doi: 10.1016/0092-8674(93)90530-4.
  • Hoefig KP, Heissmeyer V. MicroRNAs grow up in the immune system. Curr Opin Immunol. 2008;20(3):281–287. Epub 2008/06/17. doi: 10.1016/j.coi.2008.05.005.
  • Baek D, Villen J, Shin C, et al. The impact of microRNAs on protein output. Nature 2008;455(7209):64–71. Epub 2008/08/01. doi: 10.1038/nature07242.
  • Baumjohann D, Ansel KM. MicroRNA-mediated regulation of T helper cell differentiation and plasticity. Nat Rev Immunol. 2013;13(9):666–678. Epub 2013/08/03. doi: 10.1038/nri3494.
  • Pauley KM, Cha S, Chan EK. MicroRNA in autoimmunity and autoimmune diseases. J Autoimmun. 2009;32(3-4):189–194. Epub 2009/03/24. doi: 10.1016/j.jaut.2009.02.012.
  • Chen JQ, Papp G, Szodoray P, Zeher M. The role of microRNAs in the pathogenesis of autoimmune diseases. Autoimmun Rev. 2016;15(12):1171–1180. Epub 2016/09/18. doi: 10.1016/j.autrev.2016.09.003.
  • Li QJ, Chau J, Ebert PJ, et al. miR-181a is an intrinsic modulator of T cell sensitivity and selection. Cell 2007;129(1):147–161. Epub 2007/03/27. doi: 10.1016/j.cell.2007.03.008.
  • O'Connell RM, Kahn D, Gibson WS, et al. MicroRNA-155 promotes autoimmune inflammation by enhancing inflammatory T cell development. Immunity 2010;33(4):607–619. Epub 2010/10/05. doi: 10.1016/j.immuni.2010.09.009.
  • Lu LF, Thai TH, Calado DP, et al. Foxp3-dependent microRNA155 confers competitive fitness to regulatory T cells by targeting SOCS1 protein. Immunity 2009;30(1):80–91. Epub 2009/01/16. doi: 10.1016/j.immuni.2008.11.010.
  • Na SY, Park MJ, Park S, Lee ES. MicroRNA-155 regulates the Th17 immune response by targeting Ets-1 in Behcet’s disease. Clinical and Experimental Rheumatology 2016;34(6 Suppl 102):S56–S63. Epub 2016/10/30.
  • Escobar TM, Kanellopoulou C, Kugler DG, et al. miR-155 activates cytokine gene expression in Th17 cells by regulating the DNA-binding protein Jarid2 to relieve polycomb-mediated repression. Immunity 2014;40(6):865–879. Epub 2014/05/27. doi: 10.1016/j.immuni.2014.03.014.
  • Rodriguez A, Vigorito E, Clare S, et al. Requirement of bic/microRNA-155 for normal immune function. Science 2007;316(5824):608–611. Epub 2007/04/28. doi: 10.1126/science.1139253.
  • Lu LF, Boldin MP, Chaudhry A, et al. Function of miR-146a in controlling Treg cell-mediated regulation of Th1 responses. Cell 2010;142(6):914–929. Epub 2010/09/21. doi: 10.1016/j.cell.2010.08.012.
  • Li B, Wang X, Choi IY, et al. miR-146a modulates autoreactive Th17 cell differentiation and regulates organ-specific autoimmunity. J Clin Invest. 2017;127(10):3702–3716. Epub 2017/09/06. doi: 10.1172/JCI94012.
  • Medina PP, Nolde M, Slack FJ. OncomiR addiction in an in vivo model of microRNA-21-induced pre-B-cell lymphoma. Nature 2010;467(7311):86–90. Epub 2010/08/10. doi: 10.1038/nature09284.
  • Sheedy FJ, Palsson-McDermott E, Hennessy EJ, et al. Negative regulation of TLR4 via targeting of the proinflammatory tumor suppressor PDCD4 by the microRNA miR-21. Nat Immunol. 2010;11(2):141–147. Epub 2009/12/01. doi: 10.1038/ni.1828.
  • Sawant DV, Wu H, Kaplan MH, Dent AL. The Bcl6 target gene microRNA-21 promotes Th2 differentiation by a T cell intrinsic pathway. Mol Immunol. 2013;54(3-4):435–442. Epub 2013/02/19. doi: 10.1016/j.molimm.2013.01.006.
  • Murugaiyan G, da Cunha AP, Ajay AK, et al. MicroRNA-21 promotes Th17 differentiation and mediates experimental autoimmune encephalomyelitis. J Clin Invest. 2015;125(3):1069–1080. Epub 2015/02/03. doi: 10.1172/JCI74347.
  • Singh Y, Garden OA, Lang F, Cobb BS. MicroRNAs regulate T-cell production of interleukin-9 and identify hypoxia-inducible factor-2alpha as an important regulator of T helper 9 and regulatory T-cell differentiation. Immunology 2016;149(1):74–86. Epub 2016/06/10. doi: 10.1111/imm.12631.
  • McCoy CE. miR-155 Dysregulation and Therapeutic Intervention in Multiple Sclerosis. Adv Exp Med Biol 2017;1024:111–131. Epub 2017/09/19. doi: 10.1007/978-981-10-5987-2_5.
  • Su LC, Huang AF, Jia H, , et al. Role of microRNA-155 in rheumatoid arthritis. Int J Rheum Dis. 2017;20(11):1631–1637. Epub 2017/11/07. doi: 10.1111/1756-185X.13202.
  • Stanczyk J, Pedrioli DM, Brentano F, et al. Altered expression of MicroRNA in synovial fibroblasts and synovial tissue in rheumatoid arthritis. Arthritis Rheum. 2008;58(4):1001–1009. Epub 2008/04/03. doi: 10.1002/art.23386.
  • Coit P, Dozmorov MG, Merrill JT, et al. Epigenetic reprogramming in Naive CD4+ T cells favoring T cell activation and non-Th1 effector T cell immune response as an early event in Lupus Flares. Arthritis Rheumatol. 2016;68(9):2200–2209. Epub 2016/04/26. doi: 10.1002/art.39720.
  • Singh UP, Murphy AE, Enos RT, et al. miR-155 deficiency protects mice from experimental colitis by reducing T helper type 1/type 17 responses. Immunology 2014;143(3):478–489. Epub 2014/06/04. doi: 10.1111/imm.12328.
  • Assmann TS, Recamonde-Mendoza M, De Souza BM, Crispim D. MicroRNA expression profiles and type 1 diabetes mellitus: systematic review and bioinformatic analysis. Endocr Connect. 2017;6(8):773–790. Epub 2017/10/08. doi: 10.1530/EC-17-0248.
  • Ji JD, Cha ES, Lee WJ. Association of miR-146a polymorphisms with systemic lupus erythematosus: a meta-analysis. Lupus 2014;23(10):1023–1030. Epub 2014/05/08. doi: 10.1177/0961203314534512.
  • Alipoor B, Ghaedi H, Meshkani R, et al. Association of MiR-146a expression and Type 2 diabetes mellitus: a meta-analysis. Int J Mol Cell Med. 2017;6(3):156–163. Epub 2018/04/24.doi: 10.22088/acadpub.BUMS.6.3.156.
  • Martin NA, Molnar V, Szilagyi GT, et al. Experimental demyelination and axonal loss are reduced in microRNA-146a deficient mice. Front Immunol. 2018;9:490Epub 2018/03/30.doi: 10.3389/fimmu.2018.00490.
  • Pauley KM, Satoh M, Chan AL, , et al. Upregulated miR-146a expression in peripheral blood mononuclear cells from rheumatoid arthritis patients. Arthritis Res Ther. 2008;10(4):R101. Epub 2008/09/02. doi: 10.1186/ar2493.
  • Fenoglio C, Cantoni C, De Riz M, et al. Expression and genetic analysis of miRNAs involved in CD4+ cell activation in patients with multiple sclerosis. Neurosci Lett. 2011;504(1):9–12. Epub 2011/08/31. doi: 10.1016/j.neulet.2011.08.021.
  • Guinea-Viniegra J, Jimenez M, Schonthaler HB, et al. Targeting miR-21 to treat psoriasis. Sci Transl Med. 2014;6(225):225re1. Epub 2014/02/28. doi: 10.1126/scitranslmed.3008089.
  • Fisher K, Lin J. MicroRNA in inflammatory bowel disease: Translational research and clinical implication. Wjg. 2015;21(43):12274–12282. Epub 2015/11/26. doi: 10.3748/wjg.v21.i43.12274.
  • Tang X, Yin K, Zhu H, et al. Correlation between the expression of MicroRNA-301a-3p and the proportion of Th17 cells in patients with rheumatoid arthritis. Inflammation 2016;39(2):759–767. Epub 2016/01/20. doi: 10.1007/s10753-016-0304-8.
  • Du C, Liu C, Kang J, et al. MicroRNA miR-326 regulates TH-17 differentiation and is associated with the pathogenesis of multiple sclerosis. Nat Immunol. 2009;10(12):1252–1259. Epub 2009/10/20. doi: 10.1038/ni.1798.
  • Ahmadian-Elmi M, Bidmeshki Pour A, Naghavian R, et al. miR-27a and miR-214 exert opposite regulatory roles in Th17 differentiation via mediating different signaling pathways in peripheral blood CD4+ T lymphocytes of patients with relapsing-remitting multiple sclerosis. Immunogenetics 2016;68(1):43–54. Epub 2015/11/14. doi: 10.1007/s00251-015-0881-y.
  • Guan H, Singh UP, Rao R, et al. Inverse correlation of expression of microRNA-140-5p with progression of multiple sclerosis and differentiation of encephalitogenic T helper type 1 cells. Immunology 2016;147(4):488–498. Epub 2016/01/19. doi: 10.1111/imm.12583.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.