Overexpression of microRNA-155 increases IL-21 mediated STAT3 signaling and IL-21 production in systemic lupus erythematosus

Arthritis Research and Therapy

Volumn 17, Issue 1, 2015, Pages

  Rasmussen, Tue Kruse ^a,b,c   Andersen, Thomas ^a,c   Bak, Rasmus Otkjær ^a   Yiu, Gloria ^b   Sørensen, Christian Møller ^c   Stengaard Pedersen, Kristian ^c   Mikkelsen, Jacob Giehm ^a   Utz, Paul Joseph ^b   Holm, Christian Kanstrup ^a   Deleuran, Bent ^a,c  

^a AARHUS UNIVERSITY   (Denmark)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c AARHUS UNIVERSITY HOSPITAL   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 21; MICRORNA 155; STAT3 PROTEIN; SUPPRESSOR OF CYTOKINE SIGNALING 1; INTERLEUKIN DERIVATIVE; MICRORNA; MIRN155 MICRORNA, HUMAN; STAT3 PROTEIN, HUMAN;

ADULT; ARTICLE; B LYMPHOCYTE; CD4+ T LYMPHOCYTE; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; FEMALE; HUMAN; HUMAN CELL; MALE; MOLECULAR PATHOLOGY; NATURAL KILLER CELL; PROTEIN PHOSPHORYLATION; QUANTITATIVE ANALYSIS; SIGNAL TRANSDUCTION; SUPPRESSOR OF CYTOKINE SIGNALING 1 GENE; SYSTEMIC LUPUS ERYTHEMATOSUS; BIOSYNTHESIS; CELL CULTURE; GENE EXPRESSION REGULATION; LUPUS ERYTHEMATOSUS, SYSTEMIC; METABOLISM; MIDDLE AGED; MONONUCLEAR CELL; PHYSIOLOGY;

ADULT; CELLS, CULTURED; FEMALE; GENE EXPRESSION REGULATION; HUMANS; INTERLEUKINS; LEUKOCYTES, MONONUCLEAR; LUPUS ERYTHEMATOSUS, SYSTEMIC; MALE; MICRORNAS; MIDDLE AGED; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR;

EID: 84939168844     PISSN: 14786354     EISSN: 14786362     Source Type: Journal    
DOI: 10.1186/s13075-015-0660-z     Document Type: Article

References (41)

1. Tsokos GC. Systemic lupus erythematosus. N Engl J Med. 2011;365:2110-21.
2. Price JV, Haddon DJ, Kemmer D, Delepine G, Mandelbaum G, Jarrell JA, et al. Protein microarray analysis reveals BAFF-binding autoantibodies in systemic lupus erythematosus. J Clin Invest. 2013;123:5135-45.
3. Tangsombatvisit S, Xu G, Yu J, Levy D, Baechler EC, Gozani O, et al. On silico peptide microarrays for high-resolution mapping of antibody epitopes and diverse protein-protein interactions. Nat Med. 2012;18:1434-40.
4. Yu D, Vinuesa CG. The elusive identity of T follicular helper cells. Trends Immunol. 2010;31:377-83.
5. Tangye SG, Ma CS, Brink R, Deenick EK. The good, the bad and the ugly - TFH cells in human health and disease. Nat Rev Immunol. 2013;13:412-26.
6. DolffS, Abdulahad WH, Westra J, Doornbos-van der Meer B, Limburg PC, Kallenberg CGM, et al. Increase in IL-21 producing T-cells in patients with systemic lupus erythematosus. Arthritis Res Ther. 2011;13:R157.
7. Pratama A, Vinuesa CG. Control of TFH cell numbers: why and how? Immunol Cell Biol. 2013;92:40-8.
8. Vinuesa CG, Linterman MA, Goodnow CC, Randall KL. T cells and follicular dendritic cells in germinal center B-cell formation and selection. Immunol Rev. 2010;237:72-89.
9. Ettinger R, Kuchen S, Lipsky PE. The role of IL-21 in regulating B-cell function in health and disease. Immunol Rev. 2008;223:60-86.
10. Vinuesa CG, Cook MC, Angelucci C, Athanasopoulos V, Rui L, Hill KM, et al. A RING-type ubiquitin ligase family member required to repress follicular helper T cells and autoimmunity. Nature. 2005;435:452-8.
11. Ozaki K, Spolski R, Ettinger R, Kim H-P, Wang G, Qi C-F, et al. Regulation of B cell differentiation and plasma cell generation by IL-21, a novel inducer of Blimp-1 and Bcl-6. J Immunol. 2004;173:5361-71.
12. Ettinger R, Sims GP, Fairhurst A-M, Robbins R, da Silva YS, Spolski R, et al. IL-21 induces differentiation of human naive and memory B cells into antibody-secreting plasma cells. J Immunol. 2005;175:7867-79.
13. Victora GD, Schwickert TA, Fooksman DR, Kamphorst AO, Meyer-Hermann M, Dustin ML, et al. Germinal center dynamics revealed by multiphoton microscopy with a photoactivatable fluorescent reporter. Cell. 2009;143:592-605.
14. Caprioli F, Sarra M, Caruso R, StolfiC, Fina D, Sica G, et al. Autocrine regulation of IL-21 production in human T lymphocytes. J Immunol. 2008;180:1800-7.
15. Nurieva R, Yang XO, Martinez G, Zhang Y, Panopoulos AD, Ma L, et al. Essential autocrine regulation by IL-21 in the generation of inflammatory T cells. Nature. 2007;448:480-3.
16. O'Shea JJ, Murray PJ. Cytokine signaling modules in inflammatory responses. Immunity. 2008;28:477-87.
17. Hale MB, Krutzik PO, Samra SS, Crane JM, Nolan GP, Unutmaz D. Stage dependent aberrant regulation of cytokine-STAT signaling in murine systemic lupus erythematosus. PLoS One. 2009;4:e6756.
18. Liu Y, Dong J, Mu R, Gao Y, Tan X, Li Y, et al. MicroRNA-30a promotes B cell hyperactivity in patient with SLE by direct interaction with LYN. Arthritis Rheum. 2013;65:1603-11.
19. Amarilyo G, La Cava A. miRNA in systemic lupus erythematosus. Clin Immunol. 2012;144:26-31.
20. Thai T-H, Patterson HC, Pham D-H, Kis-Toth K, Kaminski DA, Tsokos GC. Deletion of microRNA-155 reduces autoantibody responses and alleviates lupus-like disease in the Faslpr mouse. Proc Natl Acad Sci U S A. 2013;110:20194-9.
21. Jiang S, Zhang H-W, Lu M-H, He X-H, Li Y, Gu H, et al. MicroRNA-155 functions as an OncomiR in breast cancer by targeting the suppressor of cytokine signaling 1 gene. Cancer Res. 70:3119-27.
22. O'Shea JJJ, Holland SMS, Staudt LML. JAKs and STATs in immunity, immunodeficiency, and cancer. N Engl J Med. 2013;368:161-70.
23. Hochberg MC. Updating the American College of Rheumatology revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum. 1997;40:1725.
24. Bombardier C, Gladman DD, Urowitz MB, Caron D, Chang CH. Derivation of the SLEDAI. A disease activity index for lupus patients. The Committee on Prognosis Studies in SLE. Arthritis Rheum. 1992;35:630-40.
25. Gladman D, Ginzler E, Goldsmith C, Fortin P, Liang M, Sanchez Guerrero J, et al. The development and initial validation of the Systemic Lupus International Collaborating Clinics/American College of Rheumatology damage index for systemic lupus erythematosus. Arthritis Rheum. 1996;39:363-9.
26. van der Fits L, van Kester MS, Qin Y, Out-Luiting JJ, Smit F, Zoutman WH, et al. MicroRNA-21 expression in CD4+ T cells is regulated by STAT3 and is pathologically involved in Sézary syndrome. J Invest Dermatol. 2011;131:762-8.
27. Bak RO, Hollensen AK, Primo MN, Sørensen CD, Mikkelsen JG. Potent microRNA suppression by RNA Pol II-transcribed "Tough Decoy" inhibitors. RNA. 2013;19:280-93.
28. Nakou M, Papadimitraki ED, Fanouriakis A, Bertsias GK, Choulaki C, Goulidaki N, et al. Interleukin-21 is increased in active systemic lupus erythematosus patients and contributes to the generation of plasma B cells. Clin Exp Rheumatol. 2013;31:172-9.
29. Bubier JA, Sproule TJ, Foreman O, Spolski R, Shaffer DJ, Morse HC, et al. A critical role for IL-21 receptor signaling in the pathogenesis of systemic lupus erythematosus in BXSB-Yaa mice. Proc Natl Acad Sci U S A. 2009;106:1518-23.
30. Sakaguchi MM, Oka MM, Iwasaki TT, Fukami YY, Nishigori CC. Role and regulation of STAT3 phosphorylation at Ser727 in melanocytes and melanoma cells. J Invest Dermatol. 2012;132:1877-85.
31. Guo HH, Ingolia NTN, Weissman JSJ, Bartel DPD. Mammalian microRNAs predominantly act to decrease target mRNA levels. Nature. 2010;466:835-40.
32. Suto A, Kashiwakuma D, Kagami S-I, Hirose K, Watanabe N, Yokote K, et al. Development and characterization of IL-21-producing CD4+ T cells. J Exp Med. 2008;205:1369-79.
33. Eto D, Lao C, DiToro D, Barnett B, Escobar TC, Kageyama R, et al. IL-21 and IL-6 are critical for different aspects of B cell immunity and redundantly induce optimal follicular helper CD4 T cell (Tfh) differentiation. PLoS One. 2011;6:e17739.
34. Baechler EC, Batliwalla FM, Karypis G, Gaffney PM, Ortmann WA, Espe KJ, et al. Interferon-inducible gene expression signature in peripheral blood cells of patients with severe lupus. Proc Natl Acad Sci U S A. 2003;100:2610-5.
35. Zeng R, Spolski R, Casas E, Zhu W, Levy DE, Leonard WJ. The molecular basis of IL-21-mediated proliferation. Blood. 2007;109:4135-42.
36. Huang XX, Guo YY, Bao CC, Shen NN. Multidimensional single cell based STAT phosphorylation profiling identifies a novel biosignature for evaluation of systemic lupus erythematosus activity. PLoS One. 2011;6:e21671.
37. Shen N, Liang D, Tang Y, de Vries N, Tak P-P. MicroRNAs-novel regulators of systemic lupus erythematosus pathogenesis. Nat Rev Rheumatol. 2012;8:701-9.
38. Chen C-Z, Schaffert S, Fragoso R, Loh C. Regulation of immune responses and tolerance: the microRNA perspective. Immunol Rev. 2013;253:112-28.
39. Escobar T, Yu CR, Muljo SA, Egwuagu CE. STAT3 activates miR-155 in Th17 cells and acts in concert to promote experimental autoimmune Uveitis. Invest Ophthalmol Vis Sci. 2013;54:4017-25.
40. O'Connell RM, Kahn D, Gibson WS, Round JL, Scholz RL, Chaudhuri AA, et al. MicroRNA-155 promotes autoimmune inflammation by enhancing inflammatory T cell development. Immunity. 2009;33:607-19.
41. 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;70:1496-506.