MicroRNA involvement in lupus: The beginning of a new tale

Current Opinion in Rheumatology

Volumn 24, Issue 5, 2012, Pages 489-498

  Liang, Dong ^a   Shen, Nan ^a,b  

^a SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^b CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ESTROGEN; EXPORTIN 5; INTERFERON; INTERLEUKIN 17; INTERLEUKIN 2; INTERLEUKIN 4; LYMPHOTOXIN; MICRORNA; MICRORNA 106A; MICRORNA 124; MICRORNA 125B; MICRORNA 126; MICRORNA 130; MICRORNA 142; MICRORNA 146A; MICRORNA 148A; MICRORNA 155; MICRORNA 181A; MICRORNA 184; MICRORNA 203; MICRORNA 21; MICRORNA 223; MICRORNA 371; MICRORNA 375; MICRORNA 423; MICRORNA 511; MICRORNA 638; MICRORNA 663; RNA POLYMERASE II; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ALLERGIC ENCEPHALOMYELITIS; BIOGENESIS; CELL NUCLEUS; CYTOKINE PRODUCTION; CYTOPLASM; DNA METHYLATION; DOWN REGULATION; EPSTEIN BARR VIRUS INFECTION; HUMAN; IMMUNOMODULATION; LYMPHOCYTE; MULTIPLE SCLEROSIS; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; RHEUMATOID ARTHRITIS; SEX DIFFERENCE; SYSTEMIC LUPUS ERYTHEMATOSUS; TRANSCRIPTION REGULATION; UPREGULATION;

AUTOIMMUNITY; DNA METHYLATION; GENE EXPRESSION REGULATION; HUMANS; INTERFERON TYPE I; LUPUS ERYTHEMATOSUS, SYSTEMIC; MICRORNAS; SIGNAL TRANSDUCTION;

EID: 84864883461     PISSN: 10408711     EISSN: 15316963     Source Type: Journal    
DOI: 10.1097/BOR.0b013e3283563363     Document Type: Review

References (111)

1. Bartel DP. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 2004; 116:281-297.
2. Carrington JC, Ambros V. Role of microRNAs in plant and animal development. Science 2003; 301:336-338.
3. Bartel DP. MicroRNAs: target recognition and regulatory functions. Cell 2009; 136:215-233.
4. Asirvatham AJ, Gregorie CJ, Hu Z, et al. MicroRNA targets in immune genes and the Dicer/Argonaute and ARE machinery components. Mol Immunol 2008; 45:1995-2006.
5. Xiao C, Rajewsky K. MicroRNA control in the immune system: basic principles. Cell 2009; 136:26-36.
6. Inui M, Martello G, Piccolo S. MicroRNA control of signal transduction. Nat Rev Mol Cell Biol 2010; 11:252-263.
7. Luo X, Tsai LM, Shen N, et al. Evidence for microRNA-mediated regulation in rheumatic diseases. Ann Rheum Dis 2010; 69 (Suppl 1):i30-i36.
8. O'Connell RM, Rao DS. Baltimore D. microRNA regulation of inflammatory responses. Annu Rev Immunol 2012; 30:295-312.
9. Lee Y, Kim M, Han J, et al. MicroRNA genes are transcribed by RNA polymerase II. Embo J 2004; 23:4051-4060.
10. Diederichs S, Haber DA. Dual role for argonautes in microRNA processing and posttranscriptional regulation of microRNA expression. Cell 2007; 131:1097-1108.
11. Carthew RW, Sontheimer EJ. Origins and mechanisms of miRNAs and siRNAs. Cell 2009; 136:642-655.
12. Kim VN, Han J, Siomi MC. Biogenesis of small RNAs in animals. Nat Rev Mol Cell Biol 2009; 10:126-139.
13. Zhou H, Huang X, Cui H, et al. miR-155 and its star-form partner miR-155 cooperatively regulate type I interferon production by human plasmacytoid dendritic cells. Blood 2010; 116:5885-5894.
14. Sun Y, Varambally S, Maher CA, et al. Targeting of microRNA-142-3p in dendritic cells regulates endotoxin-induced mortality. Blood 2011; 117:6172-6183.
15. Ding S, Liang Y, Zhao M, et al. Decreased miR-142-3p/5p expression causes CD4( +) T cell activation and B cell hyperstimulation in systemic lupus erythematosus. Arthritis Rheum 2012 [Epub 2012].
16. Krutzfeldt J, Rajewsky N, Braich R, et al. Silencing of microRNAs in vivo with 'antagomirs'. Nature 2005; 438:685-689.
17. Vasudevan S, Tong Y, Steitz JA. Cell-cycle control of microRNA-mediated translation regulation. Cell Cycle 2008; 7:1545-1549.
18. Heo I, Joo C, Kim YK, et al. TUT4 in concert with Lin28 suppresses microRNA biogenesis through premicroRNA uridylation. Cell 2009; 138:696-708.
19. Lu S, Sun YH, Chiang VL. Adenylation of plant miRNAs. Nucl Acids Res 2009; 37:1878-1885.
20. Katoh T, Sakaguchi Y, Miyauchi K, et al. Selective stabilization of mammalian microRNAs by 30 adenylation mediated by the cytoplasmic poly(A) polymerase GLD-2. Genes Dev 2009; 23:433-438.
21. Li J, Yang Z, Yu B, et al. Methylation protects miRNAs and siRNAs from a 30-end uridylation activity in Arabidopsis. Curr Biol 2005; 15:1501-1507.
22. Ameres SL, Horwich MD, Hung JH, et al. Target RNA-directed trimming and tailing of small silencing RNAs. Science 2010; 328:1534-1539.
23. Peng Z, Cheng Y, Tan BC, et al. Comprehensive analysis of RNA-Seq data reveals extensive RNA editing in a human transcriptome. Nat Biotechnol 2012; 30:253-260.
24. Kawahara Y, Zinshteyn B, Sethupathy P, et al. Redirection of silencing targets by adenosine-to-inosine editing of miRNAs. Science 2007; 315:1137-1140.
25. Ruggiero T, Trabucchi M, De Santa F, et al. LPS induces KH-type splicing regulatory protein-dependent processing of microRNA-155 precursors in macrophages. Faseb J 2009; 23:2898-2908.
26. Wiesen JL, Tomasi TB. Dicer is regulated by cellular stresses and interferons. Mol Immunol 2009; 46:1222-1228.
27. Cameron JE, Fewell C, Yin Q, et al. Epstein-Barr virus growth/latency III program alters cellular microRNA expression. Virology 2008; 382:257-266.
28. Godshalk SE, Bhaduri-McIntosh S, Slack FJ. Epstein-Barr virus-mediated dysregulation of human microRNA expression. Cell Cycle 2008; 7:3595-3600.
29. Bhat-Nakshatri P, Wang G, Collins NR, et al. Estradiol-regulated microRNAs control estradiol response in breast cancer cells. Nucl Acids Res 2009; 37:4850-4861.
30. Dai R, Phillips RA, Zhang Y, et al. Suppression of LPS-induced Interferongamma and nitric oxide in splenic lymphocytes by select estrogen-regulated microRNAs: a novel mechanism of immune modulation. Blood 2008; 112:4591-4597.
31. Fazi F, Rosa A, Fatica A, et al. A minicircuitry comprised of microRNA-223 and transcription factors NFI-A and C/EBPalpha regulates human granulopoiesis. Cell 2005; 123:819-831.
32. Johnnidis JB, Harris MH, Wheeler RT, et al. Regulation of progenitor cell proliferation and granulocyte function by microRNA-223. Nature 2008; 451:1125-1129.
33. Fontana L, Pelosi E, Greco P, et al. MicroRNAs 17-5p-20a-106a control monocytopoiesis through AML1 targeting and M-CSF receptor upregulation. Nat Cell Biol 2007; 9:775-787.
34. Rosa A, Ballarino M, Sorrentino A, et al. The interplay between the master transcription factor PU.1 and miR-424 regulates human monocyte/macrophage differentiation. Proc Natl Acad Sci USA 2007; 104:19849-19854.
35. Ooi AG, Sahoo D, Adorno M, et al. MicroRNA-125b expands hematopoietic stem cells and enriches for the lymphoid-balanced and lymphoid-biased subsets. Proc Natl Acad Sci USA 2010; 107:21505-21510.
36. Lal A, Pan Y, Navarro F, et al. miR-24-mediated downregulation of H2AX suppresses DNA repair in terminally differentiated blood cells. Nat Struct Mol Biol 2009; 16:492-498.
37. Stittrich AB, Haftmann C, Sgouroudis E, et al. The microRNA miR-182 is induced by IL-2 and promotes clonal expansion of activated helper T lymphocytes. Nat Immunol 2010; 11:1057-1062.
38. Xiao C, Calado DP, Galler G, et al. MiR-150 controls B cell differentiation by targeting the transcription factor c-Myb. Cell 2007; 131:146-159.
39. Koralov SB, Muljo SA, Galler GR, et al. Dicer ablation affects antibody diversity and cell survival in the B lymphocyte lineage. Cell 2008; 132:860-874.
40. Sharma A, Kumar M, Aich J, et al. Posttranscriptional regulation of interleukin-10 expression by hsa-miR-106a. Proc Natl Acad Sci USA 2009; 106:5761-5766.
41. Ponomarev ED, Veremeyko T, Barteneva N, et al. MicroRNA-124 promotes microglia quiescence and suppresses EAE by deactivating macrophages via the C/EBP-alpha-PU.1 pathway. Nat Med 2011; 17:64-70.
42. Ooi AG, Sahoo D, Adorno M, et al. MicroRNA-125b expands hematopoietic stem cells and enriches for the lymphoid-balanced and lymphoid-biased subsets. Proc Natl Acad Sci USA 2010; 107:21505-21510.
43. Mattes J, Collison A, Plank M, et al. Antagonism of microRNA-126 suppresses the effector function of TH2 cells and the development of allergic airways disease. Proc Natl Acad Sci USA 2009; 106:18704-18709.
44. Zhang N, Bevan MJ. Dicer controls CD8 + T-cell activation, migration, and survival. Proc Natl Acad Sci USA 2010; 107:21629-21634.
45. Shaked I, Meerson A, Wolf Y, et al. MicroRNA-132 potentiates cholinergic anti-inflammatory signaling by targeting acetylcholinesterase. Immunity 2009; 31:965-973.
46. Annoni A, Brown BD, Cantore A, et al. In vivo delivery of a microRNAregulated transgene induces antigen-specific regulatory T cells and promotes immunologic tolerance. Blood 2009; 114:5152-5161.
47. Nahid MA, Pauley KM, Satoh M, et al. miR-146a is critical for endotoxininduced tolerance: implication in innate immunity. J Biol Chem 2009; 284:34590-34599.
48. Nahid MA, Satoh M, Chan EK. Mechanistic role of microRNA-146a in endotoxin-induced differential cross-regulation of TLR signaling. J Immunol 2011; 186:1723-1734.
49. Boldin MP, Taganov KD, Rao DS, et al. miR-146a is a significant brake on autoimmunity, myeloproliferation, and cancer in mice. J Exp Med 2011; 208:1189-1201.
50. Chassin C, Kocur M, Pott J, et al. miR-146a mediates protective innate immune tolerance in the neonate intestine. Cell Host Microb 2010; 8:358-368.
51. Jurkin J, Schichl YM, Koeffel R, et al. miR-146a is differentially expressed by myeloid dendritic cell subsets and desensitizes cells to TLR2-dependent activation. J Immunol 2010; 184:4955-4965.
52. Curtale G, Citarella F, Carissimi C, et al. An emerging player in the adaptive immune response: microRNA-146a is a modulator of IL-2 expression and activation-induced cell death in T lymphocytes. Blood 2010; 115:265-273.
53. Nakasa T, Shibuya H, Nagata Y, et al. The inhibitory effect of microRNA-146a expression on bone destruction in collagen-induced arthritis. Arthritis Rheum 2011; 63:1582-1590.
54. Etzrodt M, Cortez-Retamozo V, Newton A, et al. Regulation of monocyte functional heterogeneity by miR-146a and Relb. Cell Rep 2012; 1:317-324.
55. Liu X, Zhan Z, Xu L, et al. MicroRNA-148/152 impair innate response and antigen presentation of TLR-triggered dendritic cells by targeting CaMKIIalpha. J Immunol 2010; 185:7244-7251.
56. Thai TH, Calado DP, Casola S, et al. Regulation of the germinal center response by microRNA-155. Science 2007; 316:604-608.
57. Rodriguez A, Vigorito E, Clare S, et al. Requirement of bic/microRNA-155 for normal immune function. Science 2007; 316:608-611.
58. Ceppi M, Pereira PM, Dunand-Sauthier I, et al. MicroRNA-155 modulates the interleukin-1 signaling pathway in activated human monocyte-derived dendritic cells. Proc Natl Acad Sci USA 2009; 106:2735-2740.
59. Martinez-Nunez RT, Louafi F, Friedmann PS, et al. MicroRNA-155 modulates the pathogen binding ability of dendritic cells (DCs) by down-regulation of DC-specific intercellular adhesion molecule-3 grabbing nonintegrin (DCSIGN). J Biol Chem 2009; 284:16334-16342.
60. O'Connell RM, Chaudhuri AA, Rao DS, et al. Inositol phosphatase SHIP1 is a primary target of miR-155. Proc Natl Acad Sci USA 2009; 106:7113-7118.
61. Lu LF, Thai TH, Calado DP, et al. Foxp3-dependent microRNA155 confers competitive fitness to regulatory T cells by targeting SOCS1 protein. Immunity 2009; 30:80-91.
62. Sonkoly E, Janson P, Majuri ML, et al. MiR-155 is overexpressed in patients with atopic dermatitis and modulates T-cell proliferative responses by targeting cytotoxic T lymphocyte-associated antigen 4. J Allergy Clin Immunol 2010; 126:581-589 e1-20.
63. Wang P, Hou J, Lin L, et al. Inducible microRNA-155 feedback promotes type I IFN signaling in antiviral innate immunity by targeting suppressor of cytokine signaling 1. J Immunol 2010; 185:6226-6233.
64. Martinez-Nunez RT, Louafi F, Sanchez-Elsner T. The interleukin 13 (IL-13) pathway in human macrophages is modulated by microRNA-155 via direct targeting of interleukin 13 receptor alpha1 (IL13Ralpha1). J Biol Chem 2011; 286:1786-1794.
65. Louafi F, Martinez-Nunez RT, Sanchez-Elsner T. MicroRNA-155 targets SMAD2 and modulates the response of macrophages to transforming growth factor-{beta}. J Biol Chem 2010; 285:41328-41336.
66. Dunand-Sauthier I, Santiago-Raber ML, Capponi L, et al. Silencing of c-Fos expression by microRNA-155 is critical for dendritic cell maturation and function. Blood 2011; 117:4490-4500.
67. Kurowska-Stolarska M, Alivernini S, Ballantine LE, et al. MicroRNA-155 as a proinflammatory regulator in clinical and experimental arthritis. Proc Natl Acad Sci USA 2011; 108:11193-11198.
68. Divekar AA, Dubey S, Gangalum PR, et al. Dicer insufficiency and microRNA-155 overexpression in lupus regulatory T cells: an apparent paradox in the setting of an inflammatory milieu. J Immunol 2011; 186:924-930.
69. Grigoryev YA, Kurian SM, Hart T, et al. MicroRNA regulation of molecular networks mapped by global microRNA, mRNA, and protein expression in activated T lymphocytes. J Immunol 2011; 187:2233-2243.
70. Weitzel RP, Lesniewski ML, Haviernik P, et al. microRNA 184 regulates expression of NFAT1 in umbilical cord blood CD4 + T cells. Blood 2009; 113:6648-6657.
71. Stanczyk J, Ospelt C, Karouzakis E, et al. Altered expression of microRNA-203 in rheumatoid arthritis synovial fibroblasts and its role in fibroblast activation. Arthritis Rheum 2011; 63:373-381.
72. Zhu S, Pan W, Song X, et al. The microRNA miR-23b suppresses IL-17-associated autoimmune inflammation by targeting TAB2, TAB3 and IKKalpha. Nat Med 2012. [Epub 2012].
73. Lal A, Navarro F, Maher CA, et al. miR-24 Inhibits cell proliferation by targeting E2F2, MYC, and other cell-cycle genes via binding to 'seedless' 30UTR microRNA recognition elements. Mol Cell 2009; 35:610-625.
74. Ma F, Xu S, Liu X, et al. The microRNA miR-29 controls innate and adaptive immune responses to intracellular bacterial infection by targeting interferongamma. Nat Immunol 2011; 12:861-869.
75. Biton M, Levin A, Slyper M, et al. Epithelial microRNAs regulate gut mucosal immunity via epithelium-T cell crosstalk. Nat Immunol 2011; 12:239-246.
76. Tserel L, Runnel T, Kisand K, et al. MicroRNA expression profiles of human blood monocyte-derived dendritic cells and macrophages reveal miR-511 as putative positive regulator of Toll-like receptor 4. J Biol Chem 2011; 286:26487-26495.
77. Schulte LN, Eulalio A, Mollenkopf HJ, et al. Analysis of the host microRNA response to Salmonella uncovers the control of major cytokines by the let-7 family. Embo J 2011; 30:1977-1989.
78. Zhang M, Liu F, Jia H, et al. Inhibition of microRNA let-7i depresses maturation and functional state of dendritic cells in response to lipopolysaccharide stimulation via targeting suppressor of cytokine signaling 1. J Immunol 2011; 187:1674-1683.
79. Chen CZ, Li L, Lodish HF, et al. MicroRNAs modulate hematopoietic lineage differentiation. Science 2004; 303:83-86.
80. Li QJ, Chau J, Ebert PJ, et al. miR-181a is an intrinsic modulator of T cell sensitivity and selection. Cell 2007; 129:147-161.
81. Fujii Y, Fujii K, Tanaka Y. Attempt to correct abnormal signal transduction in T lymphocytes from systemic lupus erythematosus patients. Autoimmun Rev 2006; 5:143-144.
82. Lashine YA, Seoudi AM, Salah S, et al. Expression signature of microRNA-181-a reveals its crucial role in the pathogenesis of paediatric systemic lupus erythematosus. Clin Exp Rheumatol 2011; 29:351-357.
83. O'Connell RM, Kahn D, Gibson WS, et al. MicroRNA-155 promotes autoimmune inflammation by enhancing inflammatory T cell development. Immunity 2010; 33:607-619.
84. Qian Y, Kang Z, Liu C, et al. IL-17 signaling in host defense and inflammatory diseases. Cell Mol Immunol 2010; 7:328-333.
85. Iwakura Y, Ishigame H, Saijo S, et al. Functional specialization of interleukin-17 family members. Immunity 2011; 34:149-162.
86. Onishi RM, Gaffen SL. Interleukin-17 and its target genes: mechanisms of interleukin-17 function in disease. Immunology 2010; 129:311-321.
87. Lu J, Getz G, Miska EA, et al. MicroRNA expression profiles classify human cancers. Nature 2005; 435:834-838.
88. Dai Y, Huang YS, Tang M, et al. Microarray analysis of microRNA expression in peripheral blood cells of systemic lupus erythematosus patients. Lupus 2007; 16:939-946.
89. Dai Y, Sui W, Lan H, et al. Comprehensive analysis of microRNA expression patterns in renal biopsies of lupus nephritis patients. Rheumatol Int 2009; 29:749-754.
90. Te JL, Dozmorov IM, Guthridge JM, et al. Identification of unique microRNA signature associated with lupus nephritis. PloS one 2010; 5:e10344.
91. Lu J, Kwan BC, Lai FM, et al. Glomerular and tubulointerstitial miR-638, miR-198 and miR-146a expression in lupus nephritis. Nephrology (Carlton) 2012; 17:346-351.
92. Tang Y, Luo X, Cui H, et al. MicroRNA-146A contributes to abnormal activation of the type I interferon pathway in human lupus by targeting the key signaling proteins. Arthritis Rheum 2009; 60:1065-1075.
93. Stagakis E, Bertsias G, Verginis P, et al. 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; 70:1496-1506.
94. Zhao S, Wang Y, Liang Y, et al. MicroRNA-126 regulates DNA methylation in CD4 + T cells and contributes to systemic lupus erythematosus by targeting DNA methyltransferase 1. Arthritis Rheum 2011; 63:1376-1386.
95. Pan W, Zhu S, Yuan M, et al. MicroRNA-21 and microRNA-148a contribute to DNA hypomethylation in lupus CD4 + T cells by directly and indirectly targeting DNA methyltransferase 1. J Immunol 2010; 184:6773-6781.
96. Dai R, Zhang Y, Khan D, et al. Identification of a common lupus diseaseassociated microRNA expression pattern in three different murine models of lupus. PloS one 2010; 5:e14302.
97. Zhao X, Tang Y, Qu B, et al. MicroRNA-125a contributes to elevated inflammatory chemokine RANTES levels via targeting KLF13 in systemic lupus erythematosus. Arthritis Rheum 2010; 62:3425-3435.
98. Zhao S, Wang Y, Liang Y, et al. MicroRNA-126 regulates DNA methylation in CD4 + T cells and contributes to systemic lupus erythematosus by targeting DNA methyltransferase 1. Arthritis Rheum 2011; 63:1376-1386.
99. Fan W, Liang D, Tang Y, et al. Identification of microRNA-31 as a novel regulator contributing to impaired IL-2 production in T cells from patients with systemic lupus erythematosus. Arthritis Rheum 2012 (in press).
100. Luo X, Yang W, Ye DQ, et al. A functional variant in microRNA-146a promoter modulates its expression and confers disease risk for systemic lupus erythematosus. PLoS Genet 2011; 7:e1002128.
101. Yang W, Shen N, Ye DQ, et al. Genome-wide association study in Asian populations identifies variants in ETS1 and WDFY4 associated with systemic lupus erythematosus. PLoS Genet 2010; 6:e1000841.
102. Lofgren SE, Frostegard J, Truedsson L, et al. Genetic association of miRNA-146a with systemic lupus erythematosus in Europeans through decreased expression of the gene. Genes Immun 2012; 13:268-274.
103. Eriksson C, Eneslatt K, Ivanoff J, et al. Abnormal expression of chemokine receptors on T-cells from patients with systemic lupus erythematosus. Lupus 2003; 12:766-774.
104. Lu MM, Wang J, Pan HF, et al. Increased serum RANTES in patients with systemic lupus erythematosus. Rheumatol Int 2012; 32:1231-1233.
105. Krensky AM, Ahn YT. Mechanisms of disease: regulation of RANTES (CCL5) in renal disease. Nat Clin Pract Nephrol 2007; 3:164-170.
106. Richardson B, Scheinbart L, Strahler J, et al. Evidence for impaired T cell DNA methylation in systemic lupus erythematosus and rheumatoid arthritis. Arthritis Rheum 1990; 33:1665-1673.
107. Javierre BM, Fernandez AF, Richter J, et al. Changes in the pattern of DNA methylation associate with twin discordance in systemic lupus erythematosus. Genome Res 2010; 20:170-179.
108. Jeffries M, Dozmorov M, Tang Y, et al. Genome-wide DNA methylation patterns in CD4 + T cells from patients with systemic lupus erythematosus. Epigenetics 2011; 6:593-601.
109. Garchow BG, Encinas OB, Leung YT, et al. Silencing of microR6-21 in vivo ameliorates autoimmune splenomegaly in lupus mice. EMBO Mol Med 2011; 3:605-615.
110. Wahid F, Shehzad A, Khan T, et al. MicroRNAs: synthesis, mechanism, function, and recent clinical trials. Biochim Biophys Acta 2010; 1803:1231-1243.
111. Kasinski AL, Slack FJ. Epigenetics and genetics. MicroRNAs en route to the clinic: progress in validating and targeting microRNAs for cancer therapy. Nat Rev Cancer 2011; 11:849-864.