DOI QR코드

DOI QR Code

Potential Implications of Long Noncoding RNAs in Autoimmune Diseases

  • Keun Hur (Department of Biochemistry and Cell Biology, School of Medicine, Kyungpook National University) ;
  • Sang-Hyon Kim (Division of Rheumatology, Department of Internal Medicine, Keimyung University Dongsan Medical Center, Keimyung University College of Medicine) ;
  • Ji-Min Kim (Division of Rheumatology, Department of Internal Medicine, Keimyung University Dongsan Medical Center, Keimyung University College of Medicine)
  • Received : 2018.11.15
  • Accepted : 2019.02.17
  • Published : 2019.02.28

Abstract

Long noncoding RNAs (lncRNAs) are non-protein coding RNAs of more than 200 nucleotides in length. Despite the term "noncoding", lncRNAs have been reported to be involved in gene expression. Accumulating evidence suggests that lncRNAs play crucial roles in the regulation of immune system and the development of autoimmunity. lncRNAs are expressed in various immune cells including T lymphocytes, B lymphocytes, macrophages, neutrophils, dendritic cells, and NK cells, and are also involved in the differentiation and activation of these immune cells. Here, we review recent studies on the role of lncRNAs in immune regulation and the differential expression of lncRNAs in various autoimmune diseases.

Keywords

Acknowledgement

This work was supported by the National Research Foundation of Korea (NRF) grant funded by the Korea government (MSIP) (No. 2016R1C1B1016617).

References

  1. ENCODE Project Consortium. An integrated encyclopedia of DNA elements in the human genome. Nature 2012;489:57-74.
  2. ENCODE Project ConsortiumBirney E, Stamatoyannopoulos JA, Dutta A, Guigo R, Gingeras TR, Margulies EH, Weng Z, Snyder M, Dermitzakis ET, et al. Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project. Nature 2007;447:799-816. https://doi.org/10.1038/nature05874
  3. Ponting CP, Oliver PL, Reik W. Evolution and functions of long noncoding RNAs. Cell 2009;136:629-641. https://doi.org/10.1016/j.cell.2009.02.006
  4. Singh RP, Massachi I, Manickavel S, Singh S, Rao NP, Hasan S, Mc Curdy DK, Sharma S, Wong D, Hahn BH, et al. The role of miRNA in inflammation and autoimmunity. Autoimmun Rev 2013;12:1160-1165. https://doi.org/10.1016/j.autrev.2013.07.003
  5. Jimenez SA, Piera-Velazquez S. Potential role of human-specific genes, human-specific microRNAs and human-specific non-coding regulatory RNAs in the pathogenesis of systemic sclerosis and Sjogren's syndrome. Autoimmun Rev 2013;12:1046-1051. https://doi.org/10.1016/j.autrev.2013.04.004
  6. Schmitz SU, Grote P, Herrmann BG. Mechanisms of long noncoding RNA function in development and disease. Cell Mol Life Sci 2016;73:2491-2509. https://doi.org/10.1007/s00018-016-2174-5
  7. Kretz M, Webster DE, Flockhart RJ, Lee CS, Zehnder A, Lopez-Pajares V, Qu K, Zheng GX, Chow J, Kim GE, et al. Suppression of progenitor differentiation requires the long noncoding RNA ANCR. Genes Dev 2012;26:338-343. https://doi.org/10.1101/gad.182121.111
  8. Kretz M, Siprashvili Z, Chu C, Webster DE, Zehnder A, Qu K, Lee CS, Flockhart RJ, Groff AF, Chow J, et al. Control of somatic tissue differentiation by the long non-coding RNA TINCR. Nature 2013;493:231-235. https://doi.org/10.1038/nature11661
  9. Feldstein O, Nizri T, Doniger T, Jacob J, Rechavi G, Ginsberg D. The long non-coding RNA ERIC is regulated by E2F and modulates the cellular response to DNA damage. Mol Cancer 2013;12:131.
  10. Lekka E, Hall J. Noncoding RNAs in disease. FEBS Lett 2018;592:2884-2900. https://doi.org/10.1002/1873-3468.13182
  11. Zhang Y, Cao X. Long noncoding RNAs in innate immunity. Cell Mol Immunol 2016;13:138-147. https://doi.org/10.1038/cmi.2015.68
  12. Fitzgerald KA, Caffrey DR. Long noncoding RNAs in innate and adaptive immunity. Curr Opin Immunol 2014;26:140-146. https://doi.org/10.1016/j.coi.2013.12.001
  13. Wang P, Xue Y, Han Y, Lin L, Wu C, Xu S, Jiang Z, Xu J, Liu Q, Cao X. The STAT3-binding long noncoding RNA lnc-DC controls human dendritic cell differentiation. Science 2014;344:310-313. https://doi.org/10.1126/science.1251456
  14. Spurlock CF 3rd, Tossberg JT, Guo Y, Collier SP, Crooke PS 3rd, Aune TM. Expression and functions of long noncoding RNAs during human T helper cell differentiation. Nat Commun 2015;6:6932.
  15. Carpenter S, Aiello D, Atianand MK, Ricci EP, Gandhi P, Hall LL, Byron M, Monks B, Henry-Bezy M, Lawrence JB, et al. A long noncoding RNA mediates both activation and repression of immune response genes. Science 2013;341:789-792. https://doi.org/10.1126/science.1240925
  16. Lander ES, Linton LM, Birren B, Nusbaum C, Zody MC, Baldwin J, Devon K, Dewar K, Doyle M, FitzHugh W, et al. Initial sequencing and analysis of the human genome. Nature 2001;409:860-921. https://doi.org/10.1038/35057062
  17. Guttman M, Garber M, Levin JZ, Donaghey J, Robinson J, Adiconis X, Fan L, Koziol MJ, Gnirke A, Nusbaum C, et al. Ab initio reconstruction of cell type-specific transcriptomes in mouse reveals the conserved multi-exonic structure of lincRNAs. Nat Biotechnol 2010;28:503-510. https://doi.org/10.1038/nbt.1633
  18. Kampa D, Cheng J, Kapranov P, Yamanaka M, Brubaker S, Cawley S, Drenkow J, Piccolboni A, Bekiranov S, Helt G, et al. Novel RNAs identified from an in-depth analysis of the transcriptome of human chromosomes 21 and 22. Genome Res 2004;14:331-342. https://doi.org/10.1101/gr.2094104
  19. Carninci P, Kasukawa T, Katayama S, Gough J, Frith MC, Maeda N, Oyama R, Ravasi T, Lenhard B, Wells C, et al. The transcriptional landscape of the mammalian genome. Science 2005;309:1559-1563. https://doi.org/10.1126/science.1112014
  20. Liu B, Sun L, Liu Q, Gong C, Yao Y, Lv X, Lin L, Yao H, Su F, Li D, et al. A cytoplasmic NF-κB interacting long noncoding RNA blocks IκB phosphorylation and suppresses breast cancer metastasis. Cancer Cell 2015;27:370-381. https://doi.org/10.1016/j.ccell.2015.02.004
  21. Zhao J, Sun BK, Erwin JA, Song JJ, Lee JT. Polycomb proteins targeted by a short repeat RNA to the mouse X chromosome. Science 2008;322:750-756. https://doi.org/10.1126/science.1163045
  22. El Bassit G, Patel RS, Carter G, Shibu V, Patel AA, Song S, Murr M, Cooper DR, Bickford PC, Patel NA. MALAT1 in human adipose stem cells modulates survival and alternative splicing of PKCδII in HT22 cells. Endocrinology 2017;158:183-195.
  23. He Y, Meng XM, Huang C, Wu BM, Zhang L, Lv XW, Li J. Long noncoding RNAs: novel insights into hepatocelluar carcinoma. Cancer Lett 2014;344:20-27. https://doi.org/10.1016/j.canlet.2013.10.021
  24. Ferreri AJ, Illerhaus G, Zucca E, Cavalli FInternational Extranodal Lymphoma Study Group. Flows and flaws in primary central nervous system lymphoma. Nat Rev Clin Oncol 2010;7:472.
  25. Somarowthu S, Legiewicz M, Chillon I, Marcia M, Liu F, Pyle AM. HOTAIR forms an intricate and modular secondary structure. Mol Cell 2015;58:353-361. https://doi.org/10.1016/j.molcel.2015.03.006
  26. Kelley RL, Kuroda MI. Noncoding RNA genes in dosage compensation and imprinting. Cell 2000;103:9-12. https://doi.org/10.1016/S0092-8674(00)00099-4
  27. Zimmerman LM, Vogel LA, Bowden RM. Understanding the vertebrate immune system: insights from the reptilian perspective. J Exp Biol 2010;213:661-671. https://doi.org/10.1242/jeb.038315
  28. Iwasaki A, Medzhitov R. Control of adaptive immunity by the innate immune system. Nat Immunol 2015;16:343-353. https://doi.org/10.1038/ni.3123
  29. Riera Romo M, Perez-Martinez D, Castillo Ferrer C. Innate immunity in vertebrates: an overview. Immunology 2016;148:125-139. https://doi.org/10.1111/imm.12597
  30. Kotzin JJ, Spencer SP, McCright SJ, Kumar DB, Collet MA, Mowel WK, Elliott EN, Uyar A, Makiya MA, Dunagin MC, et al. The long non-coding RNA Morrbid regulates Bim and short-lived myeloid cell lifespan. Nature 2016;537:239-243. https://doi.org/10.1038/nature19346
  31. Manz MG, Boettcher S. Emergency granulopoiesis. Nat Rev Immunol 2014;14:302-314. https://doi.org/10.1038/nri3660
  32. Ginhoux F, Jung S. Monocytes and macrophages: developmental pathways and tissue homeostasis. Nat Rev Immunol 2014;14:392-404. https://doi.org/10.1038/nri3671
  33. Simon HU, Rothenberg ME, Bochner BS, Weller PF, Wardlaw AJ, Wechsler ME, Rosenwasser LJ, Roufosse F, Gleich GJ, Klion AD. Refining the definition of hypereosinophilic syndrome. J Allergy Clin Immunol 2010;126:45-49. https://doi.org/10.1016/j.jaci.2010.03.042
  34. Steinman RM, Hemmi H. Dendritic cells: translating innate to adaptive immunity. Curr Top Microbiol Immunol 2006;311:17-58.
  35. Laouar Y, Welte T, Fu XY, Flavell RA. STAT3 is required for Flt3L-dependent dendritic cell differentiation. Immunity 2003;19:903-912. https://doi.org/10.1016/S1074-7613(03)00332-7
  36. Guttman M, Amit I, Garber M, French C, Lin MF, Feldser D, Huarte M, Zuk O, Carey BW, Cassady JP, et al. Chromatin signature reveals over a thousand highly conserved large non-coding RNAs in mammals. Nature 2009;458:223-227. https://doi.org/10.1038/nature07672
  37. Li Z, Chao TC, Chang KY, Lin N, Patil VS, Shimizu C, Head SR, Burns JC, Rana TM. The long noncoding RNA THRIL regulates TNFα expression through its interaction with hnRNPL. Proc Natl Acad Sci U S A 2014;111:1002-1007. https://doi.org/10.1073/pnas.1313768111
  38. Ng WL, Marinov GK, Liau ES, Lam YL, Lim YY, Ea CK. Inducible RasGEF1B circular RNA is a positive regulator of ICAM-1 in the TLR4/LPS pathway. RNA Biol 2016;13:861-871. https://doi.org/10.1080/15476286.2016.1207036
  39. Krawczyk M, Emerson BM. p50-associated COX-2 extragenic RNA (PACER) activates COX-2 gene expression by occluding repressive NF-κB complexes. eLife 2014;3:e01776.
  40. Atianand MK, Hu W, Satpathy AT, Shen Y, Ricci EP, Alvarez-Dominguez JR, Bhatta A, Schattgen SA, McGowan JD, Blin J, et al. A long noncoding RNA lincRNA-EPS acts as a transcriptional brake to restrain inflammation. Cell 2016;165:1672-1685. https://doi.org/10.1016/j.cell.2016.05.075
  41. Castellanos-Rubio A, Fernandez-Jimenez N, Kratchmarov R, Luo X, Bhagat G, Green PH, Schneider R, Kiledjian M, Bilbao JR, Ghosh S. A long noncoding RNA associated with susceptibility to celiac disease. Science 2016;352:91-95. https://doi.org/10.1126/science.aad0467
  42. Rapicavoli NA, Qu K, Zhang J, Mikhail M, Laberge RM, Chang HY. A mammalian pseudogene lncRNA at the interface of inflammation and anti-inflammatory therapeutics. eLife 2013;2:e00762.
  43. Ranzani V, Rossetti G, Panzeri I, Arrigoni A, Bonnal RJ, Curti S, Gruarin P, Provasi E, Sugliano E, Marconi M, 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;16:318-325. https://doi.org/10.1038/ni.3093
  44. Hu G, Tang Q, Sharma S, Yu F, Escobar TM, Muljo SA, Zhu J, Zhao K. Expression and regulation of intergenic long noncoding RNAs during T cell development and differentiation. Nat Immunol 2013;14:1190-1198. https://doi.org/10.1038/ni.2712
  45. Lee GR, Fields PE, Griffin TJ 4th, Flavell RA. Regulation of the Th2 cytokine locus by a locus control region. Immunity 2003;19:145-153. https://doi.org/10.1016/S1074-7613(03)00179-1
  46. Vigneau S, Rohrlich PS, Brahic M, Bureau JF. Tmevpg1, a candidate gene for the control of Theiler's virus persistence, could be implicated in the regulation of gamma interferon. J Virol 2003;77:5632-5638. https://doi.org/10.1128/JVI.77.10.5632-5638.2003
  47. 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. J Immunol 2012;189:2084-2088. https://doi.org/10.4049/jimmunol.1200774
  48. Collier SP, Henderson MA, Tossberg JT, Aune TM. Regulation of the Th1 genomic locus from Ifng through Tmevpg1 by T-bet. J Immunol 2014;193:3959-3965. https://doi.org/10.4049/jimmunol.1401099
  49. Gomez JA, Wapinski OL, Yang YW, Bureau JF, Gopinath S, Monack DM, Chang HY, Brahic M, Kirkegaard K. The NeST long ncRNA controls microbial susceptibility and epigenetic activation of the interferon-γ locus. Cell 2013;152:743-754. https://doi.org/10.1016/j.cell.2013.01.015
  50. Wang Y, Zhong H, Xie X, Chen CY, Huang D, Shen L, Zhang H, Chen ZW, Zeng G. Long noncoding RNA derived from CD244 signaling epigenetically controls CD8+ T-cell immune responses in tuberculosis infection. Proc Natl Acad Sci U S A 2015;112:E3883-E3892. https://doi.org/10.1073/pnas.1501662112
  51. Willingham AT, Orth AP, Batalov S, Peters EC, Wen BG, Aza-Blanc P, Hogenesch JB, Schultz PG. A strategy for probing the function of noncoding RNAs finds a repressor of NFAT. Science 2005;309:1570-1573. https://doi.org/10.1126/science.1115901
  52. Sharma S, Findlay GM, Bandukwala HS, Oberdoerffer S, Baust B, Li Z, Schmidt V, Hogan PG, Sacks DB, Rao A. Dephosphorylation of the nuclear factor of activated T cells (NFAT) transcription factor is regulated by an RNA-protein scaffold complex. Proc Natl Acad Sci U S A 2011;108:11381-11386. https://doi.org/10.1073/pnas.1019711108
  53. Jiang R, Tang J, Chen Y, Deng L, Ji J, Xie Y, Wang K, Jia W, Chu WM, Sun B. The long noncoding RNA lnc-EGFR stimulates T-regulatory cells differentiation thus promoting hepatocellular carcinoma immune evasion. Nat Commun 2017;8:15129.
  54. Sehgal L, Mathur R, Braun FK, Wise JF, Berkova Z, Neelapu S, Kwak LW, Samaniego F. FAS-antisense 1 lncRNA and production of soluble versus membrane Fas in B-cell lymphoma. Leukemia 2014;28:2376-2387. https://doi.org/10.1038/leu.2014.126
  55. Jacobson DL, Gange SJ, Rose NR, Graham NM. Epidemiology and estimated population burden of selected autoimmune diseases in the United States. Clin Immunol Immunopathol 1997;84:223-243. https://doi.org/10.1006/clin.1997.4412
  56. Eaton WW, Rose NR, Kalaydjian A, Pedersen MG, Mortensen PB. Epidemiology of autoimmune diseases in Denmark. J Autoimmun 2007;29:1-9. https://doi.org/10.1016/j.jaut.2007.05.002
  57. Rahman A, Isenberg DA. Systemic lupus erythematosus. N Engl J Med 2008;358:929-939. https://doi.org/10.1056/NEJMra071297
  58. Summers SA, Hoi A, Steinmetz OM, O'Sullivan KM, Ooi JD, Odobasic D, Akira S, Kitching AR, Holdsworth SR. TLR9 and TLR4 are required for the development of autoimmunity and lupus nephritis in pristane nephropathy. J Autoimmun 2010;35:291-298. https://doi.org/10.1016/j.jaut.2010.05.004
  59. Lartigue A, Colliou N, Calbo S, Francois A, Jacquot S, Arnoult C, Tron F, Gilbert D, Musette P. Critical role of TLR2 and TLR4 in autoantibody production and glomerulonephritis in lpr mutation-induced mouse lupus. J Immunol 2009;183:6207-6216. https://doi.org/10.4049/jimmunol.0803219
  60. Nockher WA, Wigand R, Schoeppe W, Scherberich JE. Elevated levels of soluble CD14 in serum of patients with systemic lupus erythematosus. Clin Exp Immunol 1994;96:15-19. https://doi.org/10.1111/j.1365-2249.1994.tb06222.x
  61. Zhang F, Wu L, Qian J, Qu B, Xia S, La T, Wu Y, Ma J, Zeng J, Guo Q, et al. Identification of the long noncoding RNA NEAT1 as a novel inflammatory regulator acting through MAPK pathway in human lupus. J Autoimmun 2016;75:96-104. https://doi.org/10.1016/j.jaut.2016.07.012
  62. Suarez-Gestal M, Calaza M, Endreffy E, Pullmann R, Ordi-Ros J, Sebastiani GD, Ruzickova S, Jose Santos M, Papasteriades C, Marchini M, et al. Replication of recently identified systemic lupus erythematosus genetic associations: a case-control study. Arthritis Res Ther 2009;11:R69.
  63. 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:ra8.
  64. Haywood ME, Rose SJ, Horswell S, Lees MJ, Fu G, Walport MJ, Morley BJ. Overlapping BXSB congenic intervals, in combination with microarray gene expression, reveal novel lupus candidate genes. Genes Immun 2006;7:250-263. https://doi.org/10.1038/sj.gene.6364294
  65. Wu GC, Li J, Leng RX, Li XP, Li XM, Wang DG, Pan HF, Ye DQ. Identification of long non-coding RNAs Gas5, linc0597 and lnc-DC in plasma as novel biomarkers for systemic lupus erythematosus. Oncotarget 2017;8:23650-23663. https://doi.org/10.18632/oncotarget.15569
  66. McInnes IB, Schett G. The pathogenesis of rheumatoid arthritis. N Engl J Med 2011;365:2205-2219. https://doi.org/10.1056/NEJMra1004965
  67. Picerno V, Ferro F, Adinolfi A, Valentini E, Tani C, Alunno A. One year in review: the pathogenesis of rheumatoid arthritis. Clin Exp Rheumatol 2015;33:551-558.
  68. Zamanpoor M. The genetic pathogenesis, diagnosis and therapeutic insight of rheumatoid arthritis. Clin Genet 2018.
  69. Deng J, Yang M, Jiang R, An N, Wang X, Liu B. Long non-coding RNA HOTAIR regulates the proliferation, self-renewal capacity, tumor formation and migration of the cancer stem-like cell (CSC) subpopulation enriched from breast cancer cells. PLoS One 2017;12:e0170860.
  70. Di W, Li Q, Shen W, Guo H, Zhao S. The long non-coding RNA HOTAIR promotes thyroid cancer cell growth, invasion and migration through the miR-1-CCND2 axis. Am J Cancer Res 2017;7:1298-1309.
  71. 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;15:121-126. https://doi.org/10.1007/s10238-013-0271-4
  72. Stuhlmuller B, Kunisch E, Franz J, Martinez-Gamboa L, Hernandez MM, Pruss A, Ulbrich N, Erdmann VA, Burmester GR, Kinne RW. Detection of oncofetal h19 RNA in rheumatoid arthritis synovial tissue. Am J Pathol 2003;163:901-911. https://doi.org/10.1016/S0002-9440(10)63450-5
  73. Spurlock CF 3rd, Tossberg JT, Matlock BK, Olsen NJ, Aune TM. Methotrexate inhibits NF-κB activity via long intergenic (noncoding) RNA-p21 induction. Arthritis Rheumatol 2014;66:2947-2957. https://doi.org/10.1002/art.38805
  74. Lu MC, Yu HC, Yu CL, Huang HB, Koo M, Tung CH, Lai NS. Increased expression of long noncoding RNAs LOC100652951 and LOC100506036 in T cells from patients with rheumatoid arthritis facilitates the inflammatory responses. Immunol Res 2016;64:576-583. https://doi.org/10.1007/s12026-015-8756-8
  75. Mo BY, Guo XH, Yang MR, Liu F, Bi X, Liu Y, Fang LK, Luo XQ, Wang J, Bellanti JA, et al. Long non-coding RNA GAPLINC promotes tumor-like biologic behaviors of fibroblast-like synoviocytes as microRNA sponging in rheumatoid arthritis patients. Front Immunol 2018;9:702.
  76. Findlay AR, Goyal NA, Mozaffar T. An overview of polymyositis and dermatomyositis. Muscle Nerve 2015;51:638-656. https://doi.org/10.1002/mus.24566
  77. Lega JC, Fabien N, Reynaud Q, Durieu I, Durupt S, Dutertre M, Cordier JF, Cottin V. The clinical phenotype associated with myositis-specific and associated autoantibodies: a meta-analysis revisiting the so-called antisynthetase syndrome. Autoimmun Rev 2014;13:883-891. https://doi.org/10.1016/j.autrev.2014.03.004
  78. Dau PC. Plasma exchange in polymyositis and dermatomyositis. N Engl J Med 1992;327:1030-1031. https://doi.org/10.1056/NEJM199210013271413
  79. Satoh T, Okano T, Matsui T, Watabe H, Ogasawara T, Kubo K, Kuwana M, Fertig N, Oddis CV, Kondo H, et al. Novel autoantibodies against 7SL RNA in patients with polymyositis/dermatomyositis. J Rheumatol 2005;32:1727-1733.
  80. Cojocaru M, Cojocaru IM, Chicos B. New insights into antisynthetase syndrome. Maedica (Buchar) 2016;11:130-135.
  81. Peng QL, Zhang YM, Yang HB, Shu XM, Lu X, Wang GC. Transcriptomic profiling of long non-coding RNAs in dermatomyositis by microarray analysis. Sci Rep 2016;6:32818.
  82. Mavragani CP, Moutsopoulos HM. Sjogren's syndrome. Annu Rev Pathol 2014;9:273-285. https://doi.org/10.1146/annurev-pathol-012513-104728
  83. Both T, Dalm VA, van Hagen PM, van Daele PL. Reviewing primary Sjogren's syndrome: beyond the dryness - from pathophysiology to diagnosis and treatment. Int J Med Sci 2017;14:191-200. https://doi.org/10.7150/ijms.17718
  84. Martin-Nares E, Hernandez-Molina G. Novel autoantibodies in Sjogren's syndrome: a comprehensive review. Autoimmun Rev 2019;18:192-198. https://doi.org/10.1016/j.autrev.2018.09.003
  85. Tzioufas AG, Kapsogeorgou EK, Moutsopoulos HM. Pathogenesis of Sjogren's syndrome: what we know and what we should learn. J Autoimmun 2012;39:4-8. https://doi.org/10.1016/j.jaut.2012.01.002
  86. Wang J, Peng H, Tian J, Ma J, Tang X, Rui K, Tian X, Wang Y, Chen J, Lu L, et al. Upregulation of long noncoding RNA TMEVPG1 enhances T helper type 1 cell response in patients with Sjogren syndrome. Immunol Res 2016;64:489-496. https://doi.org/10.1007/s12026-015-8715-4
  87. Zhang Y, Xu YZ, Sun N, Liu JH, Chen FF, Guan XL, Li A, Wang F, Zhao QF, Wang HY, et al. Long noncoding RNA expression profile in fibroblast-like synoviocytes from patients with rheumatoid arthritis. Arthritis Res Ther 2016;18:227.