Micrornas in the key events of systemic lupus erythematosus pathogenesis

Biomedical Papers

Volumn 160, Issue 3, 2016, Pages 327-342

  Husakova, Marketa ^a  

^a INSTITUTE OF RHEUMATOLOGY   (Czech Republic)

Author keywords

Adaptive immunity; Estrogen; Genetic predisposition; Innate immunity; microRNA; SLE

Indexed keywords

ESTROGEN; MICRORNA;

ADAPTIVE IMMUNITY; ANIMAL; B LYMPHOCYTE; DISEASE MODEL; GENETIC PREDISPOSITION; GENETICS; HUMAN; IMMUNOLOGY; INNATE IMMUNITY; LUPUS ERYTHEMATOSUS, SYSTEMIC; MOUSE; PHYSIOLOGY; SINGLE NUCLEOTIDE POLYMORPHISM; T LYMPHOCYTE;

ADAPTIVE IMMUNITY; ANIMALS; B-LYMPHOCYTES; DISEASE MODELS, ANIMAL; ESTROGENS; GENETIC PREDISPOSITION TO DISEASE; HUMANS; IMMUNITY, INNATE; LUPUS ERYTHEMATOSUS, SYSTEMIC; MICE; MICRORNAS; POLYMORPHISM, SINGLE NUCLEOTIDE; T-LYMPHOCYTES;

EID: 84988530539     PISSN: 12138118     EISSN: 18047521     Source Type: Journal    
DOI: 10.5507/bp.2016.004     Document Type: Article

References (148)

1. Rahman A, Isemberg DA. Mechanisms of disease Systemic lupus erythematosus. N Engl J Med 2008;358(9):929-39.
2. Wilhelmus S, Bajema IM, Bertsias GK, Boumpas DT, Gordon C, Lightstone L, Tesar V, Jayne DR. Lupus nephritis management guidelines compared. Nephrol Dial Transplant 2015 Apr 28. pii: gfv102. [Epub ahead of print]
3. Fireti M, Heuser W, Bliss J. Efficacy of novel monoclonal antibody belimumab in the treatment of lupus nephritis. J Pharmacol Pharmacother 2015;6(2):71-6.
4. McMurray RW, May W. Sex hormones and systemic lupus erythematosus: review and meta-analysis. Arthritis Rheum 2003;48(8):2100-10.
5. Pons-Estel GJ, Alarcón GS, Scofield L, Reinlib L, Cooper GS.Understanding the epidemiology and progression of systemic lupus erythematosus. Semin Arthritis Rheum 2010;39(4):257-68.
6. Korbet SM, Schwartz MM, Evans J, Lewis EJ, Collaboratice Study Group. Severe lupus nephritis: racial differences in presentation and outcome. J Am Soc Nephrol 2007;18(1):244-54.
7. Gualtierotti R, Biggioggero M, Penatti AE, Meroni PL. Updating on the pathogenesis of systemic lupus erythematosus. Autoimmun Rev 2010;(1):3-7.
8. 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):843-54.
9. Griffiths-Jones S, Grocock RJ, van Dongen S, Bateman A, Enright AJ. miRBase: microRNA sequences, targets and gene nomenclature. Nucleis Acids Res 2006;34(Database isme):D140-4.
10. Kozomara A, Griffiths-Jones S. miRBase: annotating high confidence microRNAs using deep sequencing data. Nucleic Acids Res 2014;42(Database isme):D68-73.
11. Griffiths-Jones S. The microRNA Registry. Nucleic Acids Res 2004 Jan 1;32(Database issue):D109-11.
12. Herranz H, Cohen SM. MicroRNAs and gene regulatory networks: managing the impact of noise in biological systems. Genes Dev 2010;24(13):1339-44.
13. Bertoli G, Cava C, Castiglioni I. MicroRNAs: New Biomarkers for Diagnosis, Prognosis, Therapy Prediction and Therapeutic Tools for Breast Cancer. Theranostics 2015;5(10):1122-43. doi:10.7150/ thno.11543
14. Peng Y, Yu S, Li H, Xiang H, Peng J, Jiang S. MicroRNAs: emerging roles in adipogenesis and obesity. Cell Signal 2014;26(9):1888-96.
15. Churov AV, Oleinik EK, Knip M. MicroRNAs in rheumatoid arthritis: Altered expression and diagnostic potential. Autoimmun Rev 2015;11:1029-37. doi: 10.1016/j.autrev.2015.07.005
16. Chen CZ, Schaffert S, Fragoso R, Loh C. Regulation of immune responses and tolerance: the microRNA perspective. Immunol Rev 2013;253(1):112-28.
17. Weber JA, Baxter DH, Zhang S, Huang DY, Huang KH, Lee MJ, Galas DJ, Wang K. The microRNA spectrum in 12 body fluids.Clin Chem 2010;56(11):1733-41.
18. Steen SO, Iversen LV, Carlsen AL, Burton M, Nielsen CT, Jacobsen S, Heegaard NH. The circulating cell-free microRNA profile in systemic sclerosis is distinct from both healthy controls and systemic lupus erythematosus. J Rheumatol 2015;42(2):214-21.
19. Carlsen AL, Schetter AJ, Nielsen CT, Lood C, Knudsen S, Voss A, Harris CC, Hellmark T, Segelmark M, Jacobsen S, Bengtsson AA, Heegaard NH. Circulating microRNA expression profiles associated with systemic lupus erythematosus. Arthritis Rheum 2013;65(5):1324-34.
20. Tang ZM, Fang M, Wang JP, Cai PC, Wang P, Hu LH. Clinical relevance of plasma miR-21 in new-onset systemic lupus erythematosus patients. J Clin Lab Anal 2014;28(6):446-51.
21. Wang H, Peng W, Ouyang X, Li W, Dai Y. Circulating microRNAs as candidate biomarkers in patients with systemic lupus erythematosus. Trans Res 2012;160(3):198-206.
22. Wang G, Tam LS, Li EK, Kwan BC, Chow KM, Luk CC, Li PK, Szeto CC. Serum and urinary free microRNA level in patients with systemic lupus erythematosus. Lupus 2011;20(5):493-500.
23. Wang G, Tam LS, Li EK, Kwan BC, Chow KM, Luk CC, Li PK, Szeto CC. Serum and urinary cell-free MiR-146a and MiR-155 in patients with systemic lupus erythematosus. J Rheumatol 2010;37(12):2516-22.
24. Dai Y, Huang YS, Tang M, Lv TY, Hu CX, Tan YH, Xu ZM, Yin YB. Microarray analysis of microRNA expression in peripheral blood cells of systemic lupus erythematosus patients. Lupus 2007;16(12):939-46.
25. Liu D, Zhao H, Zhao S, Wang X. MicroRNA expression profiles of peripheral blood mononuclear cells in patients with systemic lupus erythematosus. Acta Histochem 2014;116(5):891-7.
26. Tang Y, Luo X, Cui H, Ni X, Yuan M, Guo Y, Huang X, Zhou H, de Vries N, Tak PP, Chen S, Shen N. MicroRNA-146a contributes to abnormal activation of the type I interferon pathway in human lupus by targeting the key signaling proteins. Arthritis Rheum 2009;60(4):1065-75.
27. Stagakis E, Bertsias G, Verginis P, Nakou M, Hatziapostolou M, Kritikos H, Iliopoulos D, Boumpas DT. Identification of novel microRNA signatures linked to human lupus disease activity and pathogenesis: miR-21 regulates aberrant T cell responses through regulation of PDCD4 expression. Ann Rheum Dis 2011;70(8):1496-506.
28. Chen W, Tan K, Huang J, Yu X, Peng W, Chen Y, Lin X, Chen D, Dai Y. Analysis of microRNAs in patients with systemic lupus erythematosus, using Solexa deep sequencing. Connect Tissue Res 2014;55(3):187-96.
29. Zhu J, Huang X, Su G, Wang L, Wu F, Zhang T, Song G. High expression levels of micrRNA-629, microRNA-525-5p and micrRNA-516-35 in paediatric systemic lupus erythematosus. Clin Rheumatol 2014;33(6):807-15.
30. Pan W, Zhu S, Yuan M, Cui H, Wang L, Luo X, Li J, Zhou H, Tang Y, Shen N. Micro-RNA 21 and microRNA-148a contribute to DNA hypomethylation in lupus CD4+ T cells by directly or indirectly targeting DNA methyltransferase 1. J Immunol 2010;184:6773-81.
31. Libri V, Miesen P, van Rij RP, Buck AH. Regulation of microRNA biogenesis and turnover by animals and their viruses. Cell Mol Life Sci 2013;70(19):3525-44.
32. Londin E, Loher P, Telonis AG, Quann K, Clark P, Jing Y, Hatzimichael E, Kirino Y, Honda S, Lally M, Ramratnam B, Comstock CE, Knudsen KE, Gomella L, Spaeth GL, Hark L, Katz LJ, Witkiewicz A, Rostami A, Jimenez SA, Hollingsworth MA, Yeh JJ, Shaw CA, McKenzie SE, Bray P, Nelson PT, Zupo S, Van Roosbroeck K, Keating MJ, Calin GA, Yeo C, Jimbo M, Cozzitorto J, Brody JR, Delgrosso K, Mattick JS, Fortina P, Rigoutsos I. Analysis of 13 cell types revers evidence for the expression of numerus novel primate- and tissue-specific microRNAs. Proc Natl Acad Sci U S A 2015;112(10):E1106-15.
33. Saini HK, Griffiths-Jones S, Enright AL. Genomic analysis of human microRNA transcripts. Proc Natl Acad Sci U S A 2007;104(45):17719-24.
34. Abdelfattah AM, Park C, Choi MY. Update on non-canonical microR-NAs. Biomol Concepts 2014;5(4):275-87.
35. Lee Y, Kim M, Han J, Yeom KH, Lee S, Baek SH, Kim VN. MicroRNA genes are transcribed by RNA polymerase II. EMBO J 2004;23(20):4051-60.
36. Borchert GM, Lanier W, Davidson BL. RNA polymerase III transcribes human microRNAs. Nat Struct Mol Biol 2006;13(12):1097-101.
37. Lee Y, Ahn C, Han J, Choi H, Kim J, Yim J, Lee J, Provost P, Rådmark O, Kim S, Kim VN. The nuclear RNase III Drosha initiates microRNA processing. Nature 2003;425(6956):415-9.
38. Okada C, Yamashita E, Lee SJ, Shibata S, Katahira J, Nakagawa A, Yoneda Y, Tsukihara T. A high-resolution structure of the pre-microR-NA nuclear export machinery. Science 2009;326(5957):1275-9.
39. Bernstein E, Caudy AA, Hammond SM, Hannon GJ. Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature 2001;409(6818):363-6.
40. Gregory RI, Chendrimada TP, Cooch N, Shiekhattar R. Human RISC couples microRNA biogenesis and posttranscriptional gene silencing. Cell 2005;123(4):631-40.
41. Fabian MR, Sonenberg N. The mechanics of miRNA-mediated gene silencing: a look under the hood of miRISC. Nat Struct Mol Biol 2012;19(6):586-93.
42. Zhou H, Rigoutsos I. MiR-103a-3p targets the 5’ UTR of GPRC5A in pancreatic cells. RNA. 2014;20(9):1431-9.
43. Cesana M, Cacchiarelli D, Legnini I, Santini T, Sthandier O, Chinappi M, Tramontano A, Bozzoni, I. A long noncoding RNA controls muscle differentiation by functioning as a competing endogenous RNA. Cell 2011;147(2):358-69.
44. Hansen TB, Jensen TI, Clausen BH, Bramsen JB, Finsen B, Damgaard CK, Kjems J. Natural RNA circles function as efficient microRNA sponges. Nature 2013;495(7441):384-8.
45. Bartel DP MicroRNAs: target recognition and regulatory functions. Cell 2009;136(2):215-33.
46. Friedman RC, Farh KK, Burge CB, Bartel DP. Most mammalian mRNAs are conserved targets of microRNAs. Genome Res 2009;19(1):92-105.
47. Luo X, Yang W, Ye DQ, Cui H, Zhang Y, Hirankarn N, Qian X, Tang Y, Lau YL, de Vries N, Tak PP, Tsao BP, Shen N. A Functional Variant in MicroRNA-146a Promoter Modulates Its Expression and Confers Disease Risk for Systemic Lupus Erythematosus. PLoS Genet 2011;(6):e1002128.
48. Tang Q, Yang Y, Zhao M, Liang G, Wu H, Liu Q, Xie Y, Li D, Dai Y, Yung S, Chan TM, Lu Q Mycophenolic acid upregulates miR-142-3P/5P and miR-146a in lupus CD4+ cells. Lupus 2015;24(9):935-42.
49. Li X, Tian X, Zhang B, Zhang Y, Chen J. Variation in dicer gene is associated with increased survival in T-cell lymphoma. PLoS One 2012;7(12):e51640.
50. Nothnick WB, Healy C, Hing X. Steroidal regulation of uterine miRNAs is associated with modulation of the miRNA biogenesis components Exportin-5 and Dicer1. Endocrine 2010;37(2):265-73.
51. Jakymiw A, Ikeda K, Fritzler MJ, Reeves WH, Satoh M, Chan EK. Autoimmune targeting of key components of RNA interference. Arthritis Res Ther 2006;8(4):R87.
52. Peterson SM, Thompson JA, Ufkin ML, Sathyanarayana P, Liaw L, Congdon CB Common features of microRNA target prediction tools. Front Genet 2014;5:23. doi: 10.3389/fgene.2014.00023. eCollection 2014
53. Hogg DR, Harries LW. Human genetic variation and its effect on miRNA biogenesis, activity and function. Biochem Soc Trans 2014;42(4):1184-9.
54. Nigita G, Veneziano D, Feroo A. A-to-I RNA Editing: Current knowledges sources and computational approaches with speccial emphasis on non-coding NA molecules. Front Bioeng Biotechnol 2015;25(3):37. doi: 10.3389/fbioe.2015.00037. eCollection 2015
55. Katakowski M, Buller B, Wang X, Rogers T, Chopp M. Functional microRNA is transferred between glioma cells. Cancer Res 2010;70(21):8259-63.
56. Hunter MP, Ismail N, Zhang X, Aguda BD, Lee EJ, Yu L, Xiao T, Schafer J, Lee ML, Schmittgen TD, Nana-Sinkam SP, Jarjoura D, Marsh CB. Detection of microRNA expression in human peripheral blood microvesicles. PLoS One 2008;3(11):e3694.
57. Mittelbrunn M, Gutiérrez-Vázquez C, Villarroya-Beltri C, González S, Sánchez-Cabo F, González MÁ, Bernad A, Sánchez-Madrid F.Unidirectional transfer of microRNA-loaded exosomes from T cells to antigen-presenting cells. Nat Commun 2011;2:282.
58. Vickers KC, Palmisano BT, Shoucri BM, Shamburek RD, Remaley AT. MicroRNAs are transported in plasma and delivered to recipient cells by high-density lipoproteins. Nat Cell Biol 2011;13(4):423-33.
59. Arroyo JD, Chevillet JR, Kroh EM, Ruf IK, Pritchard CC, Gibson DF, Mitchell PS, Bennett CF, Pogosova-Agadjanyan EL, Stirewalt DL, Tait JF, Tewari M. Argonaute2 complexes carry a population of circulating microRNAs independent of vesicles in human plasma. Proc Natl Acad Sci USA 2011;108(12):5003-8.
60. Wang K, Zhang S, Weber J, Baxter D, Galas DJ. Export of microRNAs and microRNA-protective protein by mammalian cells. Nucleic Acids Res 2010;38(20):7248-59.
61. Chevillet JR, Kang Q, Ruf IK, Briggs HA, Vojtech LN, Hughes SM, Cheng HH, Arroyo JD, Meredith EK, Gallichotte EN, Pogosova-Agadjanyan EL, Morrissey C, Stirewalt DL, Hladik F, Yu EY, Higano CS, Tewari M. Quantitative and stoichiometric analysis of the microRNA content of exosomes. Proc Natl Acad Sci USA 2014;111(41):14888-93.
62. Perez-Hernandez J, Forner MJ, Pinto C, Chaves FJ, Cortes R, Redon J. Increased Urinary Exosomal MicroRNAs in Patients with Systemic Lupus Erythematosus. PloS One 2015;10(9):e0138618.
63. Ichii O, Otsuka-Kanazawa S, Horino T, Kimura J, Nakamura T, Matsumoto M, Toi M, Kon Y. Decreased miR-26a expression correlates with the progression of podocyte injury in autoimmune glomerulonefritis. PLoS One 2014;9(10):e110383.
64. Guerra SG, Vyse TJ, Cunninghame Graham DS. The genetics of lupus: a functional perspective. Arthritis Res Ther 2012;14(3):211.
65. Leng RX, Wang W, cen H, Zhou M, Feng CC, Zhu Y, Yang XK, Yang M, Zhai Y, Wang XS, Li R, Chen GM, Chen H, Pan HF, Ye DQ. Gene-gene and gene-sex epistatic interactions of MiR146a, IRF5, IKZF1, ETS1 and IL21 in systemic lupus erythematosus. PloS One 2012;7(12):e51090.
66. Fu L, Jin L, Yan L, Shi J, Wang H, Zhou B, Wu X. Comprehensive review of genetic association studies and meta-analysis on miRNA polymorphisms and rheumatoid arthritis and systemic lupus erythematosus susceptibility. Human Immunol 2014;Sep 11 [Epub ahead of print] doi: 10.1016/j.humimm.2014.09.002
67. Zhang J, Yang B, Ying B, Li D, Shi Y, Song X, Cai B, Huang Z, Wu Y, Wang L.Association of pre-microRNAs genetic variants with susceptibility in systemic lupus erythematosus. Mol Biol Rep 2011;38(3):1463-8.
68. International Consortium for Systemic Lupus Erythematosus Genetics (SLEGEN), Harley JB, Alarcón-Riquelme ME, Criswell LA, Jacob CO, Kimberly RP, Moser KL, Tsao BP, Vyse TJ, Langefeld CD, Nath SK, Guthridge JM, Cobb BL, Mirel DB, Marion MC, Williams AH, Divers J, Wang W, Frank SG, Namjou B, Gabriel SB, Lee AT, Gregersen PK, Behrens TW, Taylor KE, Fernando M, Zidovetzki R, Gaffney PM, Edberg JC, Rioux JD, Ojwang JO, James JA, Merrill JT, Gilkeson GS, Seldin MF, Yin H, Baechler EC, Li QZ, Wakeland EK, Bruner GR, Kaufman KM, Kelly JA. Genome-wide association scan in women with systemic lupus erythematosus identifies susceptibility variants in ITGAM, PXK, KIAA1542 and other loci. Nat Genet 2008;40(2):204-10.
69. Gateva V, Sandling JK, Hom G, Taylor KE, Chung SA, Sun X, Ortmann W, Kosoy R, Ferreira RC, Nordmark G, Gunnarsson I, Svenungsson E, Padyukov L, Sturfelt G, Jönsen A, Bengtsson AA, Rantapää-Dahlqvist S, Baechler EC, Brown EE, Alarcón GS, Edberg JC, Ramsey-Goldman R, McGwin G Jr, Reveille JD, Vilá LM, Kimberly RP, Manzi S, Petri MA, Lee A, Gregersen PK, Seldin MF, Rönnblom L, Criswell LA, Syvänen AC, Behrens TW, Graham RR. A large-scale replication study identifies TNIP1, PRDM1, JAZF1, UHRF1BP1 and IL10 as risk loci for systemic lupus erythematosus. Nat Genet 2009;41(11):1228-33.
70. Yang W, Shen N, Ye DQ, Liu Q, Zhang Y, Qian XX, Hirankarn N, Ying D, Pan HF, Mok CC, Chan TM, Wong RW, Lee KW, Mok MY, Wong SN, Leung AM, Li XP, Avihingsanon Y, Wong CM, Lee TL, Ho MH, Lee PP, Chang YK, Li PH, Li RJ, Zhang L, Wong WH, Ng IO, Lau CS, Sham PC, Lau YL, Asian Lupus Genetics Consortium. Genome-wide association study in Asian populations identifies variants in ETS1 and WDFY4 associated with systemic lupus erythematosus. PLoS Genet 2010;6(2):e1000841.
71. Löfgren SE, Frostegård J, Truedsson L, Pons-Estel BA, D'Alfonso S, Witte T, Lauwerys BR, Endreffy E, Kovács L, Vasconcelos C, Martins da Silva B, Kozyrev SV, Alarcón-Riquelme ME..Genetic association of miRNA-146a with systemic lupus erythematosus in Europeans through decreased expression of the gene. Genes Immun 2012;13(3):268-74.
72. Zhong H, Li XL, Li M, Hao LX, Chen RW, Xiang K, Qi XB, Ma RZ, Su B. Replicated associations of TNFAIP3, TNIP1 and ETS1 with systemic lupus erythematosus in a southwestern Chinese population. Arthritis Res Ther 2011;13(6):R186.
73. Tang ZM, Wang P, Chang PP, Hasahya T, Xing H, Wang JP Hu LH. Association between rs2431697 T allele on 5q33.3 and systemic lupus erythematosus: case-control study and meta-analysis. Clin Rheumatol 2015;24(11)1893-902.
74. Jazdzewski K, Murray EL, Franssila K, Jarzab B, Schoenberg DR, de la Chapelle A. Common SNP in pre-miR-146a decreases mature miR expression and predisposes to papillary thyroid carcinoma. Proc Natl Acad Sci USA 2008;105(20):7269-74.
75. Li C, Fu W, Zhang Y, Zhou L, Mao Z, Lv W, Li J, Zhou Y. Meta-Analysis of MicroRNA-146a rs2910164 G>C Polymorphism Association with Autoimmune Diseases Susceptibility, an Update Based on 24 Studies. Plos One 2015;10(4):e0121918.
76. Ji JD, Cha ES, Lee WJ. Association of miR-146a polymorphisms with systemic lupus erythematosus: a meta-analysis. Lupus 2014;23(10):1023-30.
77. Jiménez-Morales S, Gamboa-Becerra R, Baca V, Del Río-Navarro BE, López-Ley DY, Velázquez-Cruz R, Saldaña-Alvarez Y, Salas-Martínez G, Orozco L. MiR-146a polymorphism is associated with asthma but not with systemic lupus erythematosus and juvenile rheumatoid arthritis in Mexican patients. Tissue Antigens 2012;80(4):317-21.
78. Hughes GC, Choubey D. Modulation of autoimmune rheumatic diseases by oestrogen and progesterone. Nat Rev Rheumatol 2014;10(12):740-51.
79. Smith-Bouvier DL, Divekar AA, Sasidhar M, Du S, Tiwari-Woodruff SK, King JK, Arnold AP, Singh RR, Voskuhl RR A role for sex chromosome complement in the female bias in autoimmune disease. J Exp Med 2008;205(5):1099-108.
80. Dong G, Fan H, Yang Y, Zhao G, You M, Wang T, Hou Y. 17β-Estradiol enhances the activation of IFN-α signalling in B cells by down-regulating the expression of let-7e-5p, miR-98-5p and miR-145a-5p that target IKKε. Biochim Biophs Acta 2015;1852 (8):1585-98.
81. Dai R, Phillips RA, Zhang Y, Khan D, Crasta O, Ansar Ahmed S. Suppression of LPS-induced interferon-gamma and nitric oxide in splenic lymphocytes by select estrogen-regulated microRNAs: a novel mechanism of immune modulation. Blood 2008;112(12):4591-7.
82. Wang C, Ahlford A, Laxman N, Nordmark G, Eloranta ML, Gunnarsson I, Svenungsson E, Padyukov L, Sturfelt G, Jönsen A, Bengtsson AA, Truedsson L, Rantapää-Dahlqvist S, Sjöwall C, Sandling JK, Rönnblom L, Syvänen AC. Contribution of IKBKE and IFIH1 gene variants to SLE susceptibility. Genes Immun 2013;14(4):217-22.
83. Belver L, de Yebenes VG, Ramiro AR. MicroRNA prevent the generation of autoreactive antibodies. Immunity 2010;33(5):713-22.
84. Dai R, McReynolds S, Leroith T, Heid B, Liang Z, Ahmed SA. Sex differences in the expression of lupus-associated miRNAs in splenocytes from lupus-prone NZB/WF1 mice. Biol Sex Differ 2013;4(1):19.
85. Khan D, Dai R, Ansar Ahmed S. Sex differences and estrogen regulation of miRNAs in lupus, a prototypical autoimmune disease. Cell Immunol 2015;294(2):70-9.
86. Cooney CM, Bruner GR, Aberle T, Namjou-Khales B, Myers LK, Feo L, Li S, D'Souza A, Ramirez A, Harley JB, Scofield RH. 46,X,del(X)(q13) Turner's syndrome women with systemic lupus erythematosus in a pedigree multiplex for SLE. Genes Immun 2009;10(5):478-81.
87. Boldin MP, Taganov KD, Rao DS, Yang L, Zhao JL, Kalwani M, Garcia-Flores Y, Luong M, Devrekanli A, Xu J, Sun G, Tay J, Linsley PS, Baltimore D.miR-146a is a significant brake on autoimmunity, myelo-proliferation, and cancer in mice. J Exp Med 2011;208(6):1189-201.
88. . miR-155 deficiency ameliorates autoimmune inflammation of systemic lupus erythemasus by targeting S1pr1 in Faslpr/lpr Mice. J Immunol 2015;194(11):5437-45.
89. Jego G, Palucka AK, Blanck JP, Chalouni C, Pascual V, Banchereau J. Plasmacytoid dendritic cells induce plasma cell differentiation through type I interferon and interleukin 6. Immunity. 2003;19(2):225-34.
90. Li H, Fu YX, Wu Q, Zhou Y, Crossman DK, Yang P, Li J, Luo B, Morel LM, Kabarowski JH, Yagita H, Ware CF, Hsu HC, Mountz JD. Interferon-induced mechanosensing defects impede apoptotic cell clearance in lupus. J Clin Invest 2015;125(7):2877-90.
91. Karrich JJ, Jachimowsky LC, Libouban M, Iyer A, Branwijk K, Taanman-Kueter EW, Nagasawa M, deJong EC, Uitenbogaart CH, Blom B. MicroRNA-146a regulates survival and maturation of human plasmocytoid dendritic cells. Blood 2013;122(17):3001-9.
92. Charrier E, Cordeiro P, Cordeau M, Dardari R, Michaud A, Harnois M, Merindol N, Herblot S, Duval M. Post-transcriptional down-regulation of Toll-like receptor signaling pathway in umbilical cord blood plasmacytoid dendritic cells. Cell Immunol 2012;276(1-2):114-21.
93. Zhou H, Huang X, Cui H, Luo X, Tang Y, Chen S, Wu L, Shen N. miR-155 and its star-form partner miR-155* cooperatively regulate type I interferon production by human plasmacytoid dendritic cells. Blood 2010;116(26):5885-94.
94. Kaga H, Komatsuda A, Omokawa A, Ito M, Teshima K, Tagawa H, Sawada K, Wakui H. Downregulated expression of miR-155, miR-17, and miR-181b, and upregulated expression of activation-induced cytidine deaminase and interferon-α in PBMCs from patients with SLE. Mod Rheumatol 2015;25(6):865-70. doi:10.3109/14397595.20 15.1030102
95. Taganov KD, Boldin MP, Chang KJ, Baltimore D. NF-kappaB-dependent induction of microRNA miR-146, an inhibitor targeted to signaling proteins of innate immune responses. Proc Natl Acad Sci USA 2006;103(33):12481-6.
96. Li Y, Fan X, He X, Sun H, Zou Z, Yuan H, Xu H, Wang C, Shi X. MicroRNA-466l inhibits antiviral innate immune response by targeting interferon-alpha. Cell Mol Immunol 2012;9(6):497-502.
97. Yuan Y, Kasar S, Underbayev C, Vollenweider D, Salerno E, Kotenko SV, Raveche E Role of microRNA-15a in autoantibody production in interferon-augmented murine model of lupus. Mol Immunol 2012;52(2):61-70.
98. Hashad DI, Abdelmagid MH, Elsherif SH. MicroRNA 146a expression in lupus patients with and without renal complications. J Clin Lab Anal 2012;26(1):35-40.
99. Schiffer L, Bethunaickan R, Ramanujam M, Huang W, Schiffer M, Tao H, Madaio MM, Bottinger EP, Davidson A. Activated renal macrophages are markers of disease onset and disease remission in lupus nephritis. J Immunol 2008;180(3):1938-47.
100. Zhang W, Xu W, Xiong S. Blockage of Notch1 signaling aleviates murine lupus via blunting macrophage activation and M2b polarization. J Immunol 2010;184(11):6465-78.
101. Xiao P, Dong C, Yue Y, Xiong S. Dynamic expression of microRNAs in M2b polarized macrophages associated with lupus erythematosus. Gene 2014;547(2):300-9.
102. Konya C, Paz Z, Tsokos GC. The role of T cells in systemic lupus ery-thematosis: an update. Curr Opin Rheumatol 2014;26(5):493-501.
103. Martinez-Ramos R, Garcia-lozano JR, Lucena JM, Castillo-Palma MJ, Garcia-Hernandez F, Rodriguez MC, Nunez-Roldan A, Gonzalez-Escribano MF. Differential expression pattern of microRNAs in CD4+ and CD19+ cells from asymptomatic patients with systemic lupus erythematosus. Lupus 2014;23(4):353-9.
104. Zhao S, Wang Y, Liang Y, Zhao M, Long H, Ding S, Yin H, Lu Q. MicroRNA-126 regulates DNA methylation in CD4+ T cells and contributes to systemic lupus erythematosus by targeting DNA methyltransferase 1. Arthritis Rheum 2011;63(5):1376-86.
105. Qin H, Zhu X, Liang J, Wu J, Yang Y, Wang S, Shi W, Xu J. MicroRNA-29b contributes to DNA hypomethylation of CD4+ T cells in systemic lupus erythematosus by indirectly targeting DNA methyltransferase 1. J Dermatol Sci 2013;69(1):61-7.
106. Zhao M, Liu S, Luo S, Wu H, Tang M, Cheng W, Zhang Q, Zhang P, Yu X, Xia Y, Yi N, Gao F, Wang L, Yung S, Chan TM, Sawalha AH, Richardson B, Gershwin ME, Li N, Lu Q. DNA methylation and mRNA and microRNA expression of SLE CD4+ T cells correlate with disease phenotype. J Autoimm 2014;54(Sl):127-36.
107. Ding S, Liang Y, Zhao M, Liang G, Long H, Zhao S, Wang Y, Yin H, Zhang P, Zhang Q, Lu Q. Decreased micro-RNA-142-3p/5p expression causes CD4+ T cell activation and B cell hyperstimulation in systemic lupus erythematosus. Arthritis Rheum 2012;64(9):2953-63.
108. Yang L, Boldin MP, Yu Y, Liu CS, Ea CK, Ramakrishnan P, Taganov KD, Zhao JL, Baltimore D. MiR-146a controls the resolution of T cell responses in mice. J Exp Med 2012;209(9):1655-70.
109. Saki N, Abroun S, Soleimani M, Hajizamani S, Shahjahani M, Kast RE, Mortazavi Y. Involvement of MicroRNA in T-Cell Differentiation and Malignancy. Int J Hematol Oncol Stem Cell Res 2015;9(1):33-49.
110. Hagiwara E, Gourley MF, Lee S, Klinman DK. Disease severity in patients with systemic lupus erythematosus correlates with an increased ratio of interleukin 10: interferon-gamma-secreting cells in peripheral blood. Arthritis Rheum 1996;39(3):379-85.
111. Fan W, Liang D, Tang Y, Qu B, Cui H, Luo X, Huang X, Chen S, Higgs BW, Jallal B, Yao Y, Harley JB, Shen N. Identification of microRNA-31 as a novel regulator contributing to impaired interleukin-2 production in T cells from patients with systemic lupus erythematosus. Arthritis Rheum 2012;64(11):3715-25.
112. Lu LF, Thai TH, Calado DP, Chaudhry A, Kubo M, Tanaka K, Loeb GB, Lee H, Yoshimura A, Rajewsky K, Rudensky AY. Foxp3-dependent microRNA155 confers competitive fitness to regulatory T ells by targeting SOCS1 protein. Immunity 2009;30(1):80-91.
113. Garchow BG, Bartulos Encinas O, Leung YT, Tsao PY, Eisenberg RA, Caricchio R, Obad S, Petri A, Kauppinen S, Kiriakidou M.Silencing of microRNA-21 in vivo ameliorates autoimmune splenomegaly in lupus mice. EMBO Mol Med 2011;3(10):605-15.
114. Lu MC, Yu CL, Chen HC, Yu HC, Huang HB, Lai NS. Aberrant T cell expression of Ca2+ influx-regulated miRNAs in patients with systemic lupus erythematosus promotes lupus pathogenesis. Rheumatology 2015;54(2):343-8.
115. Lu MC, Lai NS, Chen HC, Yu HC, Huang KY, Tung CH, Huang HB, Yu CL. Decreased microRNA(miR)-145 and increased miR-224 expression in T cells from patients with systemic lupus erythematosus involved in lupus immunopathogenesis. Clin Exp Immunol 2013;171(1):91-9.
116. + regulatory T cells through PI3K/AKT pathway. J Cell Mol Med 2013;17(2):252-64.
117. Rouas R, Fayyad-Kazan H, El Zein N, Lewalle P, Rothé F, Simion A, Akl H, Mourtada M, El Rifai M, Burny A, Romero P, Martiat P, Badran B. Human natural Treg microRNA signature: role of microRNA-31 and microRNA-21 in FOXP3 expression. Eur J Immunol 2009;39(6):1608-18.
118. Luo X, Zhang L, Li M, Zhang W, Leng W, Zhang F, Zhao Y, Zeng X. The role of miR-125b in T lymphocytes in the pathogenesis of systemic lupus erythematosus. Clin Exp Rheumatol 2013;31(2):263-71.
119. Zhao X, Tang Y, Qu B, Cui H, Wang S, Wang L, Luo X, Huang X, Li J, Chen S, Shen N MicroRNA-125a contributes to elevated inflammatory chemokine RANTES levels via targeting KLF13 in systemic lupus erythematosus. Arthritis Rheum 2010;62(11):3425-35.
120. Kang SG, Liu WH, Lu P, Jin HY, Lim HW, Shepherd J, Fremgen D, Verdin E, Oldstone MB, Qi H, Teijaro JR, Xiao C. MicroRNAs of the miR-17 approximately 92 family are critical regulators of T(FH) differentiation. Nat Immunol 2013;14(8):849-57.
121. Takahashi H, Kanno T, Nakayamada S, Hirahara K, Sciumè G, Muljo SA, Kuchen S, Casellas R, Wei L, Kanno Y, O'Shea JJ. TGF-beta and retinoic acid induce the microRNA miR-10a, which targets Bcl-6 and constrains the plasticity of helper T cells. Nat Immunol 2012;13(6):587-95.
122. Chauhan SK, Singh VV, Rai R, Rai M, Rai G. Differential microRNA profile and post-transcriptional regulation exist in systemic lupus erythematosus patients with distinct autoantibody species. J Clin Immunol 2014;34(4):491-503.
123. Pratama A, Srivastava M, Williams NJ, Papa I, Lee SK, Dinh XT, Hutloff A, Jordan MA, Zhao JL, Casellas R, Athanasopoulos V, Vinuesa CG. MicroRNA-146a regulates ICOS-ICOSL signalling to limit accumulation of T follicular helper cells and germinal centres. Nat Commun 2015;6:6436.
124. Koralov SB, Muljo SA, Galler GR, Krek A, Chakraborty T, Kanellopoulou C, Jensen K, Cobb BS, Merkenschlager M, Rajewsky N, Rajewsky K. Dicer ablation affects antibody diversity and cell survival in the B lymphocyte lineage. Cell 2008;132(5):860-74.
125. Xu S, Guo K, Zeng Q, Huo J, Lam KP. The RNase III enzyme Dicer is es- sential for germinal center B-cell formation. Blood 2012;119(3):767-76.
126. Georgantas RW 3rd, Hildreth R, Morisot S, Alder J, Liu CG, Heimfeld S, Calin GA, Croce CM, Civin CI. CD34+ hematopoietic stem-progenitor cell microRNA expression and function: a circuit diagram of differentiation control. Proc Natl Acad Sci 2007;104(8):2750-5.
127. Mehta A, Mann M, Zhao JL, Marinov GK, Majumdar D, Garcia-Flores Y, Du X, Erikci E, Chowdhury K, Baltimore D. The microRNA-212/132 cluster regulates B cell development by targeting Sox4. J Exp Med 2015;212(10):1679-92.
128. Ventura A, Young AG, Winslow MM, Lintault L, Meissner A, Erkeland SJ, Newman J, Bronson RT, Crowley D, Stone JR, Jaenisch R, Sharp PA, Jacks T. Targeted deletion reveals essential and overlapping functions of the miR-17 through 92 family of miRNA clusters. Cell 2008;132(5):875-86.
129. Jensen K, Brusletto BS, Aass HC, Olstad OK, Kierulf P, Gautvik KM. Transcriptional profiling of mRNAs and microRNAs in human bone marrow precursor B cells identifies subset- and age-specific variations. PLoS One 2013;8(7):e70721.
130. Mok Y, Schwierzeck V, Thomas DC, Vigorito E, Rayner TF, Jarvis LB, Prosser HM, Bradley A, Withers DR, Mårtensson IL, Corcoran LM, Blenkiron C, Miska EA, Lyons PA, Smith KG MiR-210 is induced by Oct-2, regulates B cells, and inhibits autoantibody production. J Immunol 2013;191(6):3037-48.
131. Fernando TR, Rodriquez-Malave NI, Rao DS. MicroRNA in B cell development and malignancy. J Hematol Oncol 2012;5(1):7.
132. Teng G, Hakimpour P, Landgraf P, Rice A, Tuschl T, Casellas R, Papavasiliou FN. MicroRNA-155 is a negative regulator of activation-induced cytidine deaminase. Immunity 2008;28(5):621-9.
133. de Yébenes VG, Belver L, Pisano DG, González S, Villasante A, Croce C, He L, Ramiro AR miR-181b negatively regulates activation-induced cytidine deaminase in B cells. J Exp Med 2008;205(10):2199-206.
134. Zhang J, Jima DD, Jacobs C, Fischer R, Gottwein E, Huang G, Lugar PL, Lagoo AS, Rizzieri DA, Friedman DR, Weinberg JB, Lipsky PE, Dave SS. Patterns of microRNA expression characterize stages of human B-cell differentiation. Blood 2009;113(19):4586-94.
135. Lu D, Nakagawa R, Lazzaro S, Staudacher P, Abreu-Goodger C, Henely T, Boiani S, Leyland R, Galloway A, Andrews S, Butche G, Nutt SL, Turner M, Vigorito E. The miR-155-PU.1 axis acts on Pax5 to enable efficient terminal B cell differentiation. J Exp Med 2014;211(11):2183-98.
136. Malumbres R, Sarosiek KA, Cubedo E, Ruiz JW, Jiang X, Gascoyne RD, Tibshirani R, Lossos IS. Differentiation stage-specific expression of microRNAs in B lymphocytes and diffuse large B-cell lymphomas. Blood 2009;113(16):3754-64.
137. Yu M, Liang W, Wen S, Zhao T, Zhu MX, Li HH, Long Q, Wang M, Cheng X, Liao YH, Yuan J. EphB2 contributes to human naive B-cell activation and is regulated by miR-185. FASEB J 2014;28(8):3609-17.
138. Diaz M. The role of activation-induced deaminase in lupus nephritis. Autoimmunity 2013;46(2):115-20.
139. Guo Q, Zhang J, Li J, Zou L, Zhang J, Xie Z, Fu X, Jiang S, Chen G, Jia Q, Li F, Wan Y, Wu Y. Forced miR-146a expression causes autoimmune lymphoproliferative syndrome in mice via downregulation of Fas in germinal center B cells. Blood 2013;121(24):4875-83.
140. Dai R, Zhang Y, Khan D, Heid B, Caudell D, Crasta O, Ahmed SA. Identification of a common lupus disease-associated microRNA expression pattern in three different murine models of lupus. PLoS One 2010;5(12):e14302.
141. Thai TH, Patterson HC, Pham DH, Kis-Toth K, Kaminski DA, Tsokos GC. Deletion of microRNA-155 reduces autoantibody responses and alleviates lupus-like disease in the Fas(lpr) mouse. Proc Natl Acad Sci USA 2013;110(50):20194-9.
142. Liu Y, Dong J, Mu R, Gao Y, Tan X, Li Y, Li Z, Yang G. MicroRNA-30a promotes B cell hyperactivity in patients with systemic lupus erythematosus by direct interaction with Lyn. Arthritis Rheum 2013;65(6):1603-11.
143. Luo S, Lieu Y, Liang G, Zhao M, Wu H, Lianf Y, Qiu X, Tan Y, Dai Y, Zung S, C TM, Lu Q. The role of microRNA-1246 in the regulation of B cell activation and the pathogenesis of systemic lupus erythematosus. Clin Epigenetics 2015;7(1):24.
144. Wu XN, Ye YX, Niu JW, Li Y, Li X, You X, Chen H, Zhao LD, Zeng XF, Zhang FC, Tang FL, He W, Cao XT, Zhang X, Lipsky PE. Defective PTEN regulation contributes to B cell hyperresponsiveness in systemic lupus erythematosus. Sci Transl Med 2014;6(246):246ra99.
145. . MicroRNA Profiling of B Cell Subsets from Systemic Lupus Erythematosus Patients Reveals Promising Novel Biomarkers. Int J Mol Sci 2015;16(8):16953-65.
146. Anzelon AN, Wu H, Rickert RC. Pten inactivation alters peripheral B lymphocyte fate and reconstitutes CD19 functions. Nat Immunol 2003;4(3):287-94.
147. Koval ED, Shaner C, Zhang P, du Maine X, Fischer K, Tay J, Chau BN, Wu GF, Miller TM. Method for widespread microRNA-155 inhibition prolongs survival in ALS-model mice. Hum Mol genet 2013;22(20):4127-35.
148. van Rooij E, Kauppinen S. Development of microRNA therapeutics is coming of age. EMBO Mol Med 2014;6(7):851-64.