The role of miRNA in inflammation and autoimmunity

Autoimmunity Reviews

Volumn 12, Issue 12, 2013, Pages 1160-1165

  Singh, Ram Pyare ^a   Massachi, Israel ^a   Manickavel, Sudhir ^a   Singh, Satendra ^a   Rao, Nagesh P ^a   Hasan, Sascha ^a   Mc Curdy, Deborah K ^b   Sharma, Sherven ^a   Wong, David ^a   Hahn, Bevra H ^a   Rehimi, Hamida ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b Division of Allergy/Immunology and Pediatric Rheumatology   (United States)

Author keywords

Autoimmunity; Cancer; MicroRNA; Rheumatoid arthritis and Sj gren syndrome; Sex hormones; Systemic lupus erythematosus

Indexed keywords

MICRORNA; SEX HORMONE;

AUTOIMMUNE DISEASE; AUTOIMMUNITY; DISEASE ACTIVITY; HUMAN; INFLAMMATION; MACROPHAGE; MULTIPLE SCLEROSIS; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PLASMACYTOID DENDRITIC CELL; REGULATORY T LYMPHOCYTE; REVIEW; RHEUMATOID ARTHRITIS; SJOEGREN SYNDROME; SPLEEN CELL; SYSTEMIC LUPUS ERYTHEMATOSUS;

AUTOIMMUNITY; CANCER; MICRORNA; RHEUMATOID ARTHRITIS AND SJÖGREN SYNDROME; SEX HORMONES; SYSTEMIC LUPUS ERYTHEMATOSUS;

ANIMALS; AUTOIMMUNE DISEASES; AUTOIMMUNITY; GENE EXPRESSION REGULATION; HUMANS; INFLAMMATION; MICRORNAS;

EID: 84884702252     PISSN: 15689972     EISSN: 18730183     Source Type: Journal    
DOI: 10.1016/j.autrev.2013.07.003     Document Type: Review

References (79)

1. Scrivo R., Vasile M., Bartosiewicz I., Valesini G. Inflammation as "common soil" of the multifactorial diseases. Autoimmun Rev 2011, 10:369-374.
2. Wei J., Bhattacharyya S., Tourtellotte W.G., Varga J. Fibrosis in systemic sclerosis: emerging concepts and implications for targeted therapy. Autoimmun Rev 2011, 10:267-275.
3. Iborra M., Bernuzzi F., Invernizzi P., Danese S. MicroRNAs in autoimmunity and inflammatory bowel disease: crucial regulators in immune response. Autoimmun Rev 2012, 11:305-314.
4. Carissimi C., Fulci V., Macino G. MicroRNAs: novel regulators of immunity. Autoimmun Rev 2009, 8:520-524.
5. Bartel D.P. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 2004, 116:281-297.
6. Wu L., Fan J., Belasco J.G. MicroRNAs direct rapid deadenylation of mRNA. Proc Natl Acad Sci U S A 2006, 103:4034-4039.
7. Pauley K.M., Cha S., Chan E.K. MicroRNA in autoimmunity and autoimmune diseases. J Autoimmun 2009, 32:189-194.
8. Maillot G., Lacroix-Triki M., Pierredon S., Gratadou L., Schmidt S., Benes V., et al. Widespread estrogen-dependent repression of microRNAs involved in breast tumor cell growth. Cancer Res 2009, 69:8332-8340.
9. Garchow B.G., Encinas O.B., Leung Y.T., Tsao P.Y., Eisenberg R.A., Caricchio R., et al. Silencing of microR6-21 in vivo ameliorates autoimmune splenomegaly in lupus mice. EMBO Mol Med 2011, 3:605-615.
10. Stagakis E., Bertsias G., Verginis P., Nakou M., Hatziapostolou M., Kritikos H., 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(8):1496-1506.
11. Duroux-Richard I., Jorgensen C., Apparailly F. miRNAs and rheumatoid arthritis - promising novel biomarkers. Swiss Med Wkly 2011, 141:w13175.
12. Nakasa T., Miyaki S., Okubo A., Hashimoto M., Nishida K., Ochi M., et al. Expression of microRNA-146 in rheumatoid arthritis synovial tissue. Arthritis Rheum 2008, 58:1284-1292.
13. Pauley K.M., Satoh M., Chan A.L., Bubb M.R., Reeves W.H., Chan E.K. Upregulated miR-146a expression in peripheral blood mononuclear cells from rheumatoid arthritis patients. Arthritis Res Ther 2008, 10:R101.
14. Stanczyk J., Pedrioli D.M., Brentano F., Sanchez-Pernaute O., Kolling C., Gay R.E., et al. Altered expression of MicroRNA in synovial fibroblasts and synovial tissue in rheumatoid arthritis. Arthritis Rheum 2008, 58:1001-1009.
15. Roelofs M.F., Wenink M.H., Brentano F., Abdollahi-Roodsaz S., Oppers-Walgreen B., Barrera P., et al. Type I interferons might form the link between Toll-like receptor (TLR) 3/7 and TLR4-mediated synovial inflammation in rheumatoid arthritis (RA). Ann Rheum Dis 2009, 68:1486-1493.
16. Maciejewska Rodrigues H., Jungel A., Gay R.E., Gay S. Innate immunity, epigenetics and autoimmunity in rheumatoid arthritis. Mol Immunol 2009, 47:12-18.
17. Bluml S., Bonelli M., Niederreiter B., Puchner A., Mayr G., Hayer S., et al. Essential role of microRNA-155 in the pathogenesis of autoimmune arthritis in mice. Arthritis Rheum 2011, 63:1281-1288.
18. Chatzikyriakidou A., Voulgari P.V., Georgiou I., Drosos A.A. miRNAs and related polymorphisms in rheumatoid arthritis susceptibility. Autoimmun Rev 2012, 11:636-641.
19. Chatzikyriakidou A., Voulgari P.V., Georgiou I., Drosos A.A. A polymorphism in the 3'-UTR of interleukin-1 receptor-associated kinase (IRAK1), a target gene of miR-146a, is associated with rheumatoid arthritis susceptibility. Joint Bone Spine 2010, 77:411-413.
20. Taganov K.D., Boldin M.P., Chang K.J., Baltimore D. NF-kappaB-dependent induction of microRNA miR-146, an inhibitor targeted to signaling proteins of innate immune responses. Proc Natl Acad Sci U S A 2006, 103:12481-12486.
21. Li J., Wan Y., Guo Q., Zou L., Zhang J., Fang Y., et al. Altered microRNA expression profile with miR-146a upregulation in CD4+ T cells from patients with rheumatoid arthritis. Arthritis Res Ther 2010, 12:R81.
22. Lu L.F., Boldin M.P., Chaudhry A., Lin L.L., Taganov K.D., Hanada T., et al. Function of miR-146a in controlling Treg cell-mediated regulation of Th1 responses. Cell 2010, 142:914-929.
23. Curtale G., Citarella F., Carissimi C., Goldoni M., Carucci N., Fulci V., 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.
24. Murata K., Yoshitomi H., Tanida S., Ishikawa M., Nishitani K., Ito H., et al. Plasma and synovial fluid microRNAs as potential biomarkers of rheumatoid arthritis and osteoarthritis. Arthritis Res Ther 2010, 12:R86.
25. Nagata Y., Nakasa T., Mochizuki Y., Ishikawa M., Miyaki S., Shibuya H., et al. Induction of apoptosis in the synovium of mice with autoantibody-mediated arthritis by the intraarticular injection of double-stranded MicroRNA-15a. Arthritis Rheum 2009, 60:2677-2683.
26. Alsaleh G., Suffert G., Semaan N., Juncker T., Frenzel L., Gottenberg J.E., et al. Bruton's tyrosine kinase is involved in miR-346-related regulation of IL-18 release by lipopolysaccharide-activated rheumatoid fibroblast-like synoviocytes. J Immunol 2009, 182:5088-5097.
27. Nakamachi Y., Kawano S., Takenokuchi M., Nishimura K., Sakai Y., Chin T., et al. MicroRNA-124a is a key regulator of proliferation and monocyte chemoattractant protein 1 secretion in fibroblast-like synoviocytes from patients with rheumatoid arthritis. Arthritis Rheum 2009, 60:1294-1304.
28. Semaan N., Frenzel L., Alsaleh G., Suffert G., Gottenberg J.E., Sibilia J., et al. miR-346 controls release of TNF-alpha protein and stability of its mRNA in rheumatoid arthritis via tristetraprolin stabilization. PLoS One 2011, 6:e19827.
29. Stanczyk J., Ospelt C., Karouzakis E., Filer A., Raza K., Kolling C., et al. Altered expression of microRNA-203 in rheumatoid arthritis synovial fibroblasts and its role in fibroblast activation. Arthritis Rheum 2011, 63:373-381.
30. Hahn B.H., McMahon M.A., Wilkinson A., Wallace W.D., Daikh D.I., Fitzgerald J.D., et al. American College of Rheumatology guidelines for screening, treatment, and management of lupus nephritis. Arthritis Care Res (Hoboken) 2012, 64:797-808.
31. Lau C.S., Mak A. The socioeconomic burden of SLE. Nat Rev Rheumatol 2009, 5:400-404.
32. Rahman A., Isenberg D.A. Systemic lupus erythematosus. N Engl J Med 2008, 358:929-939.
33. Ceribelli A., Yao B., Dominguez-Gutierrez P.R., Nahid M.A., Satoh M., Chan E.K. MicroRNAs in systemic rheumatic diseases. Arthritis Res Ther 2011, 13:229.
34. Pan W., Zhu S., Yuan M., Cui H., Wang L., Luo X., 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.
35. Tang Y., Luo X., Cui H., Ni X., Yuan M., Guo Y., 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.
36. Zhao S., Wang Y., Liang Y., Zhao M., Long H., Ding S., 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.
37. Zhao X., Tang Y., Qu B., Cui H., Wang S., Wang L., et al. MicroRNA-125a contributes to elevated inflammatory chemokine RANTES levels via targeting KLF13 in systemic lupus erythematosus. Arthritis Rheum 2010, 62:3425-3435.
38. Dai Y., Huang Y.S., Tang M., Lv T.Y., Hu C.X., Tan Y.H., et al. Microarray analysis of microRNA expression in peripheral blood cells of systemic lupus erythematosus patients. Lupus 2007, 16:939-946.
39. Chan V.S., Nie Y.J., Shen N., Yan S., Mok M.Y., Lau C.S. Distinct roles of myeloid and plasmacytoid dendritic cells in systemic lupus erythematosus. Autoimmun Rev 2012, 11:890-897.
40. Dai R., Ahmed S.A. MicroRNA, a new paradigm for understanding immunoregulation, inflammation, and autoimmune diseases. Transl Res 2011, 157:163-179.
41. Te J.L., Dozmorov I.M., Guthridge J.M., Nguyen K.L., Cavett J.W., Kelly J.A., et al. Identification of unique microRNA signature associated with lupus nephritis. PLoS One 2010, 5:e10344.
42. Divekar A.A., Dubey S., Gangalum P.R., Singh R.R. 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.
43. Wang G., Tam L.S., Li E.K., Kwan B.C., Chow K.M., Luk C.C., et al. Serum and urinary cell-free MiR-146a and MiR-155 in patients with systemic lupus erythematosus. J Rheumatol 2010, 37:2516-2522.
44. Yao Y.S.K., Laurindo F., Saerno E., Raveche E. MicroRNAs (miR16 and MiR146a) regulation of lupus development in NZB/WF1 mouse model. J Immunol 2010, 184:87.9.
45. Lashine Y.A., Seoudi A.M., Salah S., Abdelaziz A.I. 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.
46. Tandon M., Gallo A., Jang S.I., Illei G.G., Alevizos I. Deep sequencing of short RNAs reveals novel microRNAs in minor salivary glands of patients with Sjogren's syndrome. Oral Dis 2012, 18:127-131.
47. Li G., Shi P., Wang Y. Evolutionary dynamics of the ABCA chromosome 17q24 cluster genes in vertebrates. Genomics 2007, 89:385-391.
48. Alevizos I., Illei G.G. MicroRNAs in Sjogren's syndrome as a prototypic autoimmune disease. Autoimmun Rev 2010, 9:618-621.
49. Jimenez S.A., 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.
50. Liang C., Xiong K., Szulwach K.E., Zhang Y., Wang Z., Peng J., et al. Sjogren syndrome antigen B (SSB)/La promotes global microRNA expression by binding microRNA precursors through stem-loop recognition. J Biol Chem 2013, 288:723-736.
51. Rosati G. The prevalence of multiple sclerosis in the world: an update. Neurol Sci 2001, 22:117-139.
52. Frohman E.M., Racke M.K., Raine C.S. Multiple sclerosis-the plaque and its pathogenesis. N Engl J Med 2006, 354:942-955.
53. Lindberg R.L., Hoffmann F., Mehling M., Kuhle J., Kappos L. Altered expression of miR-17-5p in CD4+ lymphocytes of relapsing-remitting multiple sclerosis patients. Eur J Immunol 2010, 40:888-898.
54. Cox M.B., Cairns M.J., Gandhi K.S., Carroll A.P., Moscovis S., Stewart G.J., et al. MicroRNAs miR-17 and miR-20a inhibit T cell activation genes and are under-expressed in MS whole blood. PLoS One 2010, 5:e12132.
55. Tufekci K.U., Oner M.G., Genc S., Genc K. MicroRNAs and multiple sclerosis. Autoimmun Dis 2011, 2011:807426.
56. Du C., Liu C., Kang J., Zhao G., Ye Z., Huang S., et al. MicroRNA miR-326 regulates TH-17 differentiation and is associated with the pathogenesis of multiple sclerosis. Nat Immunol 2009, 10:1252-1259.
57. Thamilarasan M., Koczan D., Hecker M., Paap B., Zettl U.K. MicroRNAs in multiple sclerosis and experimental autoimmune encephalomyelitis. Autoimmun Rev 2012, 11:174-179.
58. Gandhi R., Healy B., Gholipour T., Egorova S., Musallam A., Shuja M., et al. Circulating microRNAs as biomarkers for disease staging in multiple sclerosis. Ann Neurol 2013, 73:729-740.
59. Sun X., Qin S., Fan C., Xu C., Du N., Ren H. Let-7: a regulator of the ERalpha signaling pathway in human breast tumors and breast cancer stem cells. Oncol Rep 2013, 29:2079-2087.
60. Mestdagh P., Bostrom A.K., Impens F., Fredlund E., Van Peer G., De Antonellis P., et al. The miR-17-92 microRNA cluster regulates multiple components of the TGF-beta pathway in neuroblastoma. Mol Cell 2010, 40:762-773.
61. Liu Z.L., Wang H., Liu J., Wang Z.X. MicroRNA-21 (miR-21) expression promotes growth, metastasis, and chemo- or radioresistance in non-small cell lung cancer cells by targeting PTEN. Mol Cell Biochem 2013, 372:35-45.
62. Schmitt M.J., Margue C., Behrmann I., Kreis S. MiRNA-29: a microRNA family with tumor-suppressing and immune-modulating properties. Curr Mol Med 2013, 13:572-585.
63. Xiong Y., Fang J.H., Yun J.P., Yang J., Zhang Y., Jia W.H., et al. Effects of microRNA-29 on apoptosis, tumorigenicity, and prognosis of hepatocellular carcinoma. Hepatology 2010, 51:836-845.
64. Han Y.C., Park C.Y., Bhagat G., Zhang J., Wang Y., Fan J.B., et al. microRNA-29a induces aberrant self-renewal capacity in hematopoietic progenitors, biased myeloid development, and acute myeloid leukemia. J Exp Med 2010, 207:475-489.
65. Ahmed S.A., Hissong B.D., Verthelyi D., Donner K., Becker K., Karpuzoglu-Sahin E. Gender and risk of autoimmune diseases: possible role of estrogenic compounds. Environ Health Perspect 1999, 107(Suppl. 5):681-686.
66. Whitacre C.C. Sex differences in autoimmune disease. Nat Immunol 2001, 2:777-780.
67. Gourdy P., Araujo L.M., Zhu R., Garmy-Susini B., Diem S., Laurell H., et al. Relevance of sexual dimorphism to regulatory T cells: estradiol promotes IFN-gamma production by invariant natural killer T cells. Blood 2005, 105:2415-2420.
68. Karpuzoglu-Sahin E., Hissong B.D., Ansar Ahmed S. Interferon-gamma levels are upregulated by 17-beta-estradiol and diethylstilbestrol. J Reprod Immunol 2001, 52:113-127.
69. Khan D., Dai R., Karpuzoglu E., Ahmed S.A. Estrogen increases, whereas IL-27 and IFN-gamma decrease, splenocyte IL-17 production in WT mice. Eur J Immunol 2010, 40:2549-2556.
70. Panchanathan R., Shen H., Zhang X., Ho S.M., Choubey D. Mutually positive regulatory feedback loop between interferons and estrogen receptor-alpha in mice: implications for sex bias in autoimmunity. PLoS One 2010, 5:e10868.
71. Yang L., Boldin M.P., Yu Y., Liu C.S., Ea C.K., Ramakrishnan P., et al. miR-146a controls the resolution of T cell responses in mice. J Exp Med 2012, 209:1655-1670.
72. Ichii O., Otsuka S., Sasaki N., Namiki Y., Hashimoto Y., Kon Y. Altered expression of microRNA miR-146a correlates with the development of chronic renal inflammation. Kidney Int 2012, 81:280-292.
73. Dai R., Phillips R.A., Zhang Y., Khan D., Crasta O., Ahmed S.A. 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, 112:4591-4597.
74. Yamagata K., Fujiyama S., Ito S., Ueda T., Murata T., Naitou M., et al. Maturation of microRNA is hormonally regulated by a nuclear receptor. Mol Cell 2009, 36:340-347.
75. Leivonen S.K., Makela R., Ostling P., Kohonen P., Haapa-Paananen S., Kleivi K., et al. Protein lysate microarray analysis to identify microRNAs regulating estrogen receptor signaling in breast cancer cell lines. Oncogene 2009, 28:3926-3936.
76. Lu Z., Liu M., Stribinskis V., Klinge C.M., Ramos K.S., Colburn N.H., et al. MicroRNA-21 promotes cell transformation by targeting the programmed cell death 4 gene. Oncogene 2008, 27:4373-4379.
77. Si M.L., Zhu S., Wu H., Lu Z., Wu F., Mo Y.Y. miR-21-mediated tumor growth. Oncogene 2007, 26:2799-2803.
78. Zhang Y., Wu L., Wang Y., Zhang M., Li L., Zhu D., et al. Protective role of estrogen-induced miRNA-29 expression in carbon tetrachloride-induced mouse liver injury. J Biol Chem 2012, 287:14851-14862.
79. Incorvaia E., Sicouri L., Petersen-Mahrt S.K., Schmitz K.M. Hormones and AID: balancing immunity and autoimmunity. Autoimmunity 2013, 46:128-137.