Identification of novel microRNA signatures linked to experimental autoimmune myasthenia gravis pathogenesis: Down-regulated mir-145 promotes pathogenetic th17 cell response

Journal of Neuroimmune Pharmacology

Volumn 8, Issue 5, 2013, Pages 1287-1302

  Wang, Jiao ^a   Zheng, Shuangshuang ^a,b   Xin, Ning ^a   Dou, Changxin ^a   Fu, Linlin ^a   Zhang, Xiuying ^a   Chen, Jing ^a   Zhang, Yanyan ^a   Geng, Deqin ^a   Xiao, Chenghua ^a   Cui, Guiyun ^a   Shen, Xia ^a   Lu, Yang ^a   Wang, Jinhua ^a   Dong, Ruiguo ^a   Qiao, Yuehua ^a   Zhang, Yong ^a  

^a XUZHOU MEDICAL UNIVERSITY   (China)

^b LISHUI PEOPLE S HOSPITAL   (China)

Author keywords

CD28; EAMG; MicroRNA; NFATc1; Th17 cells

Indexed keywords

CD28 ANTIGEN; CELL PROTEIN; IMMUNOGLOBULIN G; INTERLEUKIN 17; LENTIVIRUS VECTOR; MICRORNA; MICRORNA 145; NFATC1 PROTEIN; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CD4+ CD25+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CLINICAL ARTICLE; COCULTURE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; DOWN REGULATION; DRUG BINDING SITE; DRUG PROTEIN BINDING; DRUG TARGETING; EXPERIMENTAL AUTOIMMUNE MYASTHENIA GRAVIS; FEMALE; HUMAN; IMMUNOGLOBULIN BLOOD LEVEL; IMMUNOREGULATION; IN VITRO STUDY; MALE; MICROARRAY ANALYSIS; MUTATION; NEUROPATHOLOGY; NONHUMAN; NUCLEOTIDE SEQUENCE; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; TH17 CELL; UPREGULATION;

ADULT; ANIMALS; ANTIGENS, CD28; BASE SEQUENCE; BLOTTING, WESTERN; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; FLOW CYTOMETRY; HUMANS; MALE; MICRORNAS; MIDDLE AGED; MYASTHENIA GRAVIS; MYASTHENIA GRAVIS, AUTOIMMUNE, EXPERIMENTAL; NFATC TRANSCRIPTION FACTORS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; RATS; RATS, INBRED LEW; REAL-TIME POLYMERASE CHAIN REACTION; TH17 CELLS; TRANSCRIPTOME; TRANSFECTION;

EID: 84891372389     PISSN: 15571890     EISSN: 15571904     Source Type: Journal    
DOI: 10.1007/s11481-013-9498-9     Document Type: Article

References (59)

1. Abdelsadik A, Trad A (2011) Toll-like receptors on the fork roads between innate and adaptive immunity. Hum Immunol 72:1188-1193
2. Ambros V (2004) The functions of animal microRNAs. Nature 431(7006):350-355
3. Baggi F, Annoni A, Ubiali F, Milani M, Longhi R, Scaioli W, Cornelio F, Mantegazza R, Antozzi C (2004) Breakdown of tolerance to a self-peptide of acetylcholine receptor alpha-subunit induces experimental myasthenia gravis in rats. J Immunol 172(4):2697-2703
4. Bai Y, Liu R, Huang D, La Cava A, Tang YY, Iwakura Y, Campagnolo DI, Vollmer TL, Ransohoff RM, Shi FD (2008) CCL2 recruitment of IL-6-producing CD11b+ monocytes to the draining lymph nodes during the initiation of Th17-dependent B cell-mediated autoimmunity. Eur J Immunol 38(7):1877-1888
5. Baltimore D, Boldin MP, O'Connell RM, Rao DS, Taganov KD (2008) MicroRNAs: new regulators of immune cell development and function. Nat Immunol 9(8):839-845
6. Bernasconi P, Barberis M, Baggi F, Passerini L, Cannone M, Arnoldi E, Novellino L, Cornelio F, Mantegazza R (2005) Increased toll-like receptor 4 expression in thymus of myasthenic patients with thymitis and thymic involution. Am J Pathol 167(1):129-139
7. Bopp T, Palmetshofer A, Serfling E, Heib V, Schmitt S, Richter C, Klein M, Schild H, Schmitt E, Stassen M (2005) NFATc2 and NFATc3 transcription factors play a crucial role in suppression of CD4+ T lymphocytes by CD4+ CD25+ regulatory T cells. J Exp Med 201(2):181-187
8. Caraher EM, Parenteau M, Gruber H, Scott FW (2000) Flow cytometric analysis of intracellular IFN-gamma, IL-4 and IL-10 in CD3(+)4(+) T-cells from rat spleen. J Immunol Methods 244(1-2):29-40
9. Cheng Z, Qiu S, Jiang L, Zhang A, Bao W, Liu P, Liu J (2013) MiR-320a is downregulated in patients with myasthenia gravis and modulates inflammatory cytokines production by targeting mitogen-activated protein kinase 1. J Clin Immunol 33(3):567-576
10. Collison A, Mattes J, Plank M, Foster PS (2011) Inhibition of house dust mite-induced allergic airways disease by antagonism of microRNA-145 is comparable to glucocorticoid treatment. J Allergy Clin Immunol 128(1):160-167.e4
11. Cordes KR, Sheehy NT, White MP, Berry EC, Morton SU, Muth AN, Lee TH, Miano JM, Ivey KN, Srivastava D (2009) miR-145 and miR-143 regulate smooth muscle cell fate and plasticity. Nature 460(7256):705-710
12. Dai R, Zhang Y, Khan D, Heid B, Caudell D, Crasta O, Ahmed SA (2010) Identification of a common lupus disease-associated microRNA expression pattern in three different murine models of lupus. PLoS One 5(12):e14302
13. Drachman DB (1996) Immunotherapy in neuromuscular disorders: current and future strategies. Muscle Nerve 19(10):1239-1251
14. Du C, Liu C, Kang J, Zhao G, Ye Z, Huang S, Li Z, Wu Z, Pei G (2009) MicroRNA miR-326 regulates TH-17 differentiation and is associated with the pathogenesis of multiple sclerosis. Nat Immunol 10(12):1252-1259
15. Elson CJ, Barker RN (2000) Helper T cells in antibody-mediated, organ-specific autoimmunity. Curr Opin Immunol 12(6):664-669
16. Eulalio A, Huntzinger E, Izaurralde E (2008) Getting to the root of miRNA-mediated gene silencing. Cell 132(1):9-14
17. Feferman T, Aricha R, Menon R, Souroujon MC, Berrih-Aknin S, Fuchs S (2007) DNA microarray in search of new drug targets for myasthenia gravis. Ann N Y Acad Sci 1107:111-117
18. Gomez-Rodriguez J, Sahu N, Handon R, Davidson TS, Anderson SM, Kirby MR, August A, Schwartzberg PL (2009) Differential expression of interleukin-17A and -17F is coupled to T cell receptor signaling via inducible T cell kinase. Immunity 31(4):587-597
19. Howland KC, Ausubel LJ, London CA, Abbas AK (2000) The roles of CD28 and CD40 ligand in T cell activation and tolerance. J Immunol 164(9):4465-4470
20. Hughes BW, Moro De Casillas ML, Kaminski HJ (2004) Pathophysiology of myasthenia gravis. Semin Neurol 24(1):21-30
21. Iborra M, Bernuzzi F, Invernizzi P, Danese S (2012) MicroRNAs in autoimmunity and inflammatory bowel disease: Crucial regulators in immune response. Autoimmun Rev 11(5):305-314
22. Jaretzki A 3rd, Barohn RJ, Ernstoff RM, Kaminski HJ, Keesey JC, Penn AS, Sanders DB (2000) Myasthenia gravis: recommendations for clinical research standards. Task Force of the Medical Scientific Advisory Board of the Myasthenia Gravis Foundation of America. Neurology 55(1):16-23
23. Kong QF, Sun B, Wang GY, Zhai DX, Mu LL, Wang DD, Wang JH, Li R, Li HL (2009) BM stromal cells ameliorate experimental autoimmune myasthenia gravis by altering the balance of Th cells through the secretion of IDO. Eur J Immunol 39(3):800-809
24. Kramer JM, Gaffen SL (2007) Interleukin-17: a new paradigm in inflammation, autoimmunity, and therapy. J Periodontol 78(6):1083-1093
25. Lai L, Song Y, Liu Y, Chen Q, Han Q, Chen W, Pan T, Zhang Y, Cao X, Wang Q (2013) MicroRNA-92a negatively regulates Toll-like receptor (TLR)-triggered inflammatory response in macrophages by targeting MKK4 kinase. J Biol Chem 288(11):7956-7967
26. Lenschow DJ, Walunas TL, Bluestone JA (1996) CD28/B7 system of T cell costimulation. Annu Rev Immunol 14:233-258
27. Linsley PS, Ledbetter JA (1993) The role of the CD28 receptor during T cell responses to antigen. Annu Rev Immunol 11:191-212
28. Liu XK, Lin X, Gaffen SL (2004) Crucial role for nuclear factor of activated T cells in T cell receptor-mediated regulation of human interleukin-17. J Biol Chem 279(50):52762-52771
29. Liu G, Friggeri A, Yang Y, Park YJ, Tsuruta Y, Abraham E (2009) miR-147, a microRNA that is induced upon Toll-like receptor stimulation, regulates murine macrophage inflammatory responses. Proc Natl Acad Sci U S A 106(37):15819-15824
30. Lohr J, Knoechel B, Wang JJ, Villarino AV, Abbas AK (2006) Role of IL-17 and regulatory T lymphocytes in a systemic autoimmune disease. J Exp Med 203(13):2785-2791
31. Love TM, Moffett HF, Novina CD (2008) Not miR-ly small RNAs: big potential for microRNAs in therapy. J Allergy Clin Immunol 121(2):309-319
32. Lu TX, Munitz A, Rothenberg ME (2009) MicroRNA-21 is up-regulated in allergic airway inflammation and regulates IL-12p35 expression. J Immunol 182(8):4994-5002
33. Lu MC, Lai NS, Chen HC, Yu HC, Huang KY, Tung CH, Huang HB, Yu CL (2013) 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 171(1):91-99
34. Lyons AB (2000) Analysing cell division in vivo and in vitro using flow cytometric measurement of CFSE dye dilution. J Immunol Methods 243(1-2):147-154
35. Mattes J, Collison A, Plank M, Phipps S, Foster PS (2009) Antagonism of microRNA-126 suppresses the effector function of TH2 cells and the development of allergic airways disease. Proc Natl Acad Sci U S A A106(44):18704-18709
36. Miao CG, Yang YY, He X, Xu T, Huang C, Huang Y, Zhang L, Lv XW, Jin Y, Li J (2013) New advances of microRNAs in the pathogenesis of rheumatoid arthritis, with a focus on the crosstalk between DNA methylation and the microRNA machinery. Cell Signal 25(5):1118-1125
37. Murugaiyan G, Beynon V, Mittal A, Joller N, Weiner HL (2011) Silencing microRNA-155 ameliorates experimental autoimmune encephalomyelitis. J Immunol 187(5):2213-2221
38. Nahid MA, Yao B, Dominguez-Gutierrez PR, Kesavalu L, Satoh M, Chan EK (2013) Regulation of TLR2-mediated tolerance and cross-tolerance through IRAK4 modulation by miR-132 and miR-212. J Immunol 190(3):1250-1263
39. Nakasa T, Miyaki S, Okubo A, Hashimoto M, Nishida K, Ochi M, Asahara H (2008) Expression of microRNA-146 in rheumatoid arthritis synovial tissue. Arthritis Rheum 58(5):1284-1292
40. Osserman KE, Genkins G (1971) Studies in myasthenia gravis: review of a twenty-year experience in over 1200 patients. Mt Sinai J Med 38(6):497-537
41. Pauley KM, Satoh M, Chan AL, Bubb MR, Reeves WH, Chan EK (2008) Upregulated miR-146a expression in peripheral blood mononuclear cells from rheumatoid arthritis patients. Arthritis Res Ther 10(4):R101
42. Porter CM, Clipstone NA (2002) Sustained NFAT signaling promotes a Th1-like pattern of gene expression in primary murine CD4+ T cells. J Immunol 168(10):4936-4945
43. Rehmsmeier M, Steffen P, Hochsmann M, Giegerich R (2004) Fast and effective prediction of microRNA/target duplexes. RNA 10(10):1507-1517
44. Roche JC, Capablo JL, Larrad L, Gervas-Arruga J, Ara JR, Sánchez A, Alarcia R (2011) Increased serum interleukin-17 levels in patients with myasthenia gravis. Muscle Nerve 44(2):278-280
45. Sachdeva M, Mo YY (2010) MicroRNA-145 suppresses cell invasion and metastasis by directly targeting mucin 1. Cancer Res 70(1):378-387
46. Salomon B, Bluestone JA (2001) Complexities of CD28/B7: CTLA-4 costimulatory pathways in autoimmunity and transplantation. Annu Rev Immunol 19:225-252
47. Sheng JR, Li L, Ganesh BB, Vasu C, Prabhakar BS, Meriggioli MN (2006) Suppression of experimental autoimmune myasthenia gravis by granulocyte- macrophage colony-stimulating factor is associated with an expansion of FoxP3+ regulatory T cells. J Immunol 177(8):5296-5306
48. Shi FD, He B, Li H, Matusevicius D, Link H, Ljunggren HG (1998) Differential requirements for CD28 and CD40 ligand in the induction of experimental autoimmune myasthenia gravis. Eur J Immunol 28(11):3587-3593
49. Shi B, Sepp-Lorenzino L, Prisco M, Linsley P, deAngelis T, Baserga R (2007) Micro RNA 145 targets the insulin receptor substrate-1 and inhibits the growth of colon cancer cells. J Biol Chem 282(45):32582-32590
50. Sonkoly E, Wei T, Janson PC, Sääf A, Lundeberg L, Tengvall-Linder M, Norstedt G, Alenius H, Homey B, Scheynius A, Ståhle M, Pivarcsi A (2007) MicroRNAs: novel regulators involved in the pathogenesis of psoriasis? PLoS One 2(7):e610
51. Vincent A, Palace J, Hilton-Jones D (2001) Myasthenia gravis. Lancet 357(9274):2122-2128
52. Wang W, Milani M, Ostlie N, Okita D, Agarwal RK, Caspi RR, Conti-Fine BM (2007) C57BL/6 mice genetically deficient in IL-12/IL-23 and IFN-gamma are susceptible to experimental autoimmune myasthenia gravis, suggesting a pathogenic role of non-Th1 cells. J Immunol 178(11):7072-7080
53. Wang YZ, Yan M, Tian FF, Zhang JM, Liu Q, Yang H, Zhou WB, Li J (2013) Possible involvement of toll-like receptors in the pathogenesis of myasthenia gravis. Inflammation 36(1):121-130
54. Winter J, Jung S, Keller S, Gregory RI, Diederichs S (2009) Many roads to maturity: microRNA biogenesis pathways and their regulation. Nat Cell Biol 11(3):228-234
55. Wu Y, Borde M, Heissmeyer V, Feuerer M, Lapan AD, Stroud JC, Bates DL, Guo L, Han A, Ziegler SF, Mathis D, Benoist C, Chen L, Rao A (2006) FOXP3 controls regulatory T cell function through cooperation with NFAT. Cell 126(2):375-387
56. Xiao C, Rajewsky K (2009) MicroRNA control in the immune system: basic principles. Cell 136(1):26-36
57. Yamaguchi S, Yamahara K, Homma K, Suzuki S, Fujii S, Morizane R, Monkawa T, Matsuzaki Y, Kangawa K, Itoh H (2011) The role of microRNA-145 in human embryonic stem cell differentiation into vascular cells. Atherosclerosis 219(2):468-474
58. Yang B, Guo H, Zhang Y, Chen L, Ying D, Dong S (2011) MicroRNA-145 regulates chondrogenic differentiation of mesenchymal stem cells by targeting Sox9. PLoS One 6(7):e21679
59. Zhang Y, Yang H, Xiao B, Wu M, Zhou W, Li J, Li G, Christadoss P (2009) Dendritic cells transduced with lentiviral-mediated RelB-specific ShRNAs inhibit the development of experimental autoimmune myasthenia gravis. Mol Immunol 46(4):657-667