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MicroRNA Regulation in Systemic Lupus Erythematosus Pathogenesis

  • Yan, Sheng (Department of Medicine, Li Ka Shing Faculty of Medicine, The University of Hong Kong) ;
  • Yim, Lok Yan (Department of Medicine, Li Ka Shing Faculty of Medicine, The University of Hong Kong) ;
  • Lu, Liwei (Department of Pathology, Li Ka Shing Faculty of Medicine, The University of Hong Kong) ;
  • Lau, Chak Sing (Department of Medicine, Li Ka Shing Faculty of Medicine, The University of Hong Kong) ;
  • Chan, Vera Sau-Fong (Department of Medicine, Li Ka Shing Faculty of Medicine, The University of Hong Kong)
  • Received : 2014.05.22
  • Accepted : 2014.06.05
  • Published : 2014.06.30
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Abstract

MicroRNAs (miRNAs) are endogenous small RNA molecules best known for their function in post-transcriptional gene regulation. Immunologically, miRNA regulates the differentiation and function of immune cells and its malfunction contributes to the development of various autoimmune diseases including systemic lupus erythematosus (SLE). Over the last decade, accumulating researches provide evidence for the connection between dysregulated miRNA network and autoimmunity. Interruption of miRNA biogenesis machinery contributes to the abnormal T and B cell development and particularly a reduced suppressive function of regulatory T cells, leading to systemic autoimmune diseases. Additionally, multiple factors under autoimmune conditions interfere with miRNA generation via key miRNA processing enzymes, thus further skewing the miRNA expression profile. Indeed, several independent miRNA profiling studies reported significant differences between SLE patients and healthy controls. Despite the lack of a consistent expression pattern on individual dysregulated miRNAs in SLE among these studies, the aberrant expression of distinct groups of miRNAs causes overlapping functional outcomes including perturbed type I interferon signalling cascade, DNA hypomethylation and hyperactivation of T and B cells. The impact of specific miRNA-mediated regulation on function of major immune cells in lupus is also discussed. Although research on the clinical application of miRNAs is still immature, through an integrated approach with advances in next generation sequencing, novel tools in bioinformatics database analysis and new in vitro and in vivo models for functional evaluation, the diagnostic and therapeutic potentials of miRNAs may bring to fruition in the future.

Keywords

References

  1. Carthew, R. W. and E. J. Sontheimer. 2009. Origins and Mechanisms of miRNAs and siRNAs. Cell 136: 642-655. https://doi.org/10.1016/j.cell.2009.01.035
  2. Kim, V. N., J. Han, and M. C. Siomi. 2009. Biogenesis of small RNAs in animals. Nat. Rev. Mol. Cell Biol. 10: 126-139. https://doi.org/10.1038/nrm2632
  3. Inui, M., G. Martello, and S. Piccolo. 2010. MicroRNA control of signal transduction. Nat. Rev. Mol. Cell Biol. 11: 252-263. https://doi.org/10.1038/nrn2804
  4. Bartel, D. P. 2009. MicroRNAs: target recognition and regulatory functions. Cell 136: 215-233. https://doi.org/10.1016/j.cell.2009.01.002
  5. Chen, C. Z., I. Li, H. F. Lodish, and D. P. Bartel. 2004. MicroRNAs modulate hematopoietic lineage differentiation. Science 303: 83-86. https://doi.org/10.1126/science.1091903
  6. Carrington, J. C. and V. Ambros. 2003. Role of microRNAs in plant and animal development. Science 301: 336-338. https://doi.org/10.1126/science.1085242
  7. Baltimore, D., M. P. Boldin, R. M. O'Connell, D. S. Rao, and K. D. Taganov. 2008. MicroRNAs: new regulators of immune cell development and function. Nat. Immunol. 9: 839-845. https://doi.org/10.1038/ni.f.209
  8. O'Connell, R. M., D. S. Rao, A. A. Chaudhuri, and D. Baltimore. 2010. Physiological and pathological roles for microRNAs in the immune system. Nat. Rev. Immunol. 10: 111-122. https://doi.org/10.1038/nri2708
  9. Asirvatham, A. J., C. J. Gregorie, Z. Hu, W. J. Magner, and T. B. Tomasi. 2008. MicroRNA targets in immune genes and the Dicer/Argonaute and ARE machinery components. Mol. Immunol. 45: 1995-2006. https://doi.org/10.1016/j.molimm.2007.10.035
  10. Mak, A., D. A. Isenberg, and C. S. Lau. 2013. Global trends, potential mechanisms and early detection of organ damage in SLE. Nat. Rev. Rheumatol. 9: 301-310.
  11. Rahman, A., and D. A. Isenberg. 2008. Systemic lupus erythematosus. N. Engl. J. Med. 358: 929-939. https://doi.org/10.1056/NEJMra071297
  12. Tsokos, G. C. 2011. Systemic lupus erythematosus. N. Engl. J. Med. 365: 2110-2121. https://doi.org/10.1056/NEJMra1100359
  13. Luo, X., L. M. Tsai, N. Shen, and D. Yu. 2010. Evidence for microRNA-mediated regulation in rheumatic diseases. Ann. Rheum. Dis. 69 Suppl 1: i30-36. https://doi.org/10.1136/ard.2009.117218
  14. Zhu, S., W. Pan, and Y. Qian. 2013. MicroRNA in immunity and autoimmunity. J. Mol. Med. (Berl). 91: 1039-1050. https://doi.org/10.1007/s00109-013-1043-z
  15. Miao, C. G., Y. Y. Yang, X. He, C. Huang, Y. Huang, L. Zhang, X. W. Lv, Y. Jin, and J. Li. 2013. The emerging role of microRNAs in the pathogenesis of systemic lupus erythematosus. Cell. Signal. 25: 1828-1836. https://doi.org/10.1016/j.cellsig.2013.05.006
  16. Gregory, R. I., K. P. Yan, G. Amuthan, T. Chendrimada, B. Doratotaj, N. Cooch, and R. Shiekhattar. 2004. The Microprocessor complex mediates the genesis of microRNAs. Nature 432: 235-240. https://doi.org/10.1038/nature03120
  17. Lund, E., S. Guttinger, A. Calado, J. E. Dahlberg, and U. Kutay. 2004. Nuclear export of microRNA precursors. Science 303: 95-98. https://doi.org/10.1126/science.1090599
  18. Bartel, D. P. 2004. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116: 281-297. https://doi.org/10.1016/S0092-8674(04)00045-5
  19. Muljo, S. A., K. M. Ansel, C. Kanellopoulou, D. M. Livingston, A. Rao, and K. Rajewsky. 2005. Aberrant T cell differentiation in the absence of Dicer. J. Exp. Med. 202: 261-269. https://doi.org/10.1084/jem.20050678
  20. Chong, M. M., J. P. Rasmussen, A. Y. Rundensky, and D. R. Littman. 2008. The RNAseIII enzyme Drosha is critical in T cells for preventing lethal inflammatory disease. J. Exp. Med. 205: 2005-2017. https://doi.org/10.1084/jem.20081219
  21. Cobb, B. S., T. B. Nesterova, E. Thompson, A. Hertweck, E. O'Connor, J. Godwin, C. B. Wilson, N. Brockdorff, A. G. Fisher, S. T. Smale, and M. Merkenschlager. 2005. T cell lineage choice and differentiation in the absence of the RNase III enzyme Dicer. J. Exp. Med. 201: 1367-1373. https://doi.org/10.1084/jem.20050572
  22. Zhou, X., L. T. Jeker, B. T. Fife, S. Zhu, M. S. Anderson, M. T. McManus, and J. A. Bluestone. 2008. Selective miRNA disruption in T reg cells leads to uncontrolled autoimmunity. J. Exp. Med. 205: 1983-1991. https://doi.org/10.1084/jem.20080707
  23. Liston, A., L. F. Lu, D. O'Carroll, A. Tarakhovsky, and A. Y. Rudensky. 2008. Dicer-dependent microRNA pathway safeguards regulatory T cell function. J. Exp. Med. 205: 1993-2004. https://doi.org/10.1084/jem.20081062
  24. Fontenot, J. D., M. A. Gavin, and A. Y. Rudensky. 2003. Foxp3 programs the development and function of $CD4^+\;CD25^+$ regulatory T cells. Nat. Immunol. 4: 330-336. https://doi.org/10.1038/ni904
  25. Divekar, A. A., S. Dubey, P. R. Gangalum, and R. R. Singh. 2011. Dicer insufficiency and microRNA-155 overexpression in lupus regulatory T cells: an apparent paradox in the setting of an inflammatory milieu. J. Immunol. 186: 924-930. https://doi.org/10.4049/jimmunol.1002218
  26. Belver, L., V. G. de Yebenes, and A. R. Ramiro. 2010. MicroRNAs prevent the generation of autoreactive antibodies. Immunity 33: 713-722. https://doi.org/10.1016/j.immuni.2010.11.010
  27. Xu, S., K. Guo, Q. Zeng, J. Huo, and K. P. Lam. 2012. The RNase III enzyme Dicer is essential for germinal center B-cell formation. Blood 119: 767-776. https://doi.org/10.1182/blood-2011-05-355412
  28. Ademokun, A. and M. Turner. 2008. Regulation of B-cell differentiation by microRNAs and RNA-binding proteins. Biochem. Soc. Trans. 36: 1191-1193. https://doi.org/10.1042/BST0361191
  29. Koralov, S. B., S. A. Muljo, G. R. Galler, A. Krek, T. Chakraborty, C. Kanellopoulou, K. Jensen, B. S. Cobb, M. Merkenschlager, N. Rajewsky, and K. Rajewsky. 2008. Dicer ablation affects antibody diversity and cell survival in the B lymphocyte lineage. Cell 132: 860-874. https://doi.org/10.1016/j.cell.2008.02.020
  30. Wiesen, J. L., and T. B. Tomasi. 2009. Dicer is regulated by cellular stresses and interferons. Mol. Immunol. 46: 1222-1228. https://doi.org/10.1016/j.molimm.2008.11.012
  31. Satoh, M., J. Y. F. Chan, A. Ceribelli, M. Vazquez del-Mercado, and E. K. Chan. 2013. Autoantibodies to Argonaute 2 (Su antigen). Adv. Exp. Med. Biol. 768: 45-59. https://doi.org/10.1007/978-1-4614-5107-5_4
  32. Jakymiw, A., K. Ikeda, M. J. Fritzler, W. H. Reeves, M. Satoh, and E. K. Chan. 2006. Autoimmune targeting of key components of RNA interference. Arthritis Res. Ther. 8: R87. https://doi.org/10.1186/ar1959
  33. Lu, J., G. Getz, E. A. Miska, E. Alvarez-Saavedra, J. Lamb, D. Peck, A. Sweet-Cordero, B. L. Ebert, R. H. Mak, A. A. Ferrando, J. R. Downing, T. Jacks, H. R. Horvitz, and T. R. Golub. 2005. MicroRNA expression profiles classify human cancers. Nature 435: 834-838. https://doi.org/10.1038/nature03702
  34. Wang, H., W. Peng, X. Ouyang, W. Li, and Y. Dai. 2012. Circulating microRNAs as candidate biomarkers in patients with systemic lupus erythematosus. Transl. Res. 160: 198-206. https://doi.org/10.1016/j.trsl.2012.04.002
  35. Carlsen, A. L., A. J. Schetter, C. T. Nielsen, C. Lood, S. Knudsen, A. Voss, C. C. Harris, T. Hellmark, M. Segelmark, S. Jacobsen, A. A. Bengtsson, and N. H. Heegaard. 2013. Circulating microRNA expression profiles associated with systemic lupus erythematosus. Arthritis Rheum. 65: 1324-1334. https://doi.org/10.1002/art.37890
  36. Tang, Y., X. Luo, H. Cui, X. Ni, M. Yuan, Y. Guo, X. Huang, H. Zhou, N. de Vries, P. P. Tak, S. Chen, and N. Shen. 2009. MicroRNA-146A contributes to abnormal activation of the type I interferon pathway in human lupus by targeting the key signaling proteins. Arthritis Rheum. 60: 1065-1075. https://doi.org/10.1002/art.24436
  37. Te, J. L., I. M. Dozmorov, J. M. Guthridge, K. L. Nguyen, J. W. Cavett, J. A. Kelly, G. R. Bruner, J. B. Harley, and J. O. Ojwang. 2010. Identification of unique microRNA signature associated with lupus nephritis. PLoS One 5: e10344. https://doi.org/10.1371/journal.pone.0010344
  38. Baechler, E. C., F. M. Batliwalla, G. Karypis, P. M. Gaffney, W. A. Ortmann, K. J. Espe, K. B. Shark, W. J. Grande, K. M. Hughes, V. Kapur, P. K. Gregersen, and T. W. Behrens. 2003. Interferon-inducible gene expression signature in peripheral blood cells of patients with severe lupus. Proc. Natl. Acad. Sci. USA 100: 2610-2615. https://doi.org/10.1073/pnas.0337679100
  39. Bennett, L., A. K. Palucka, E. Arce, V. Cantrell, J. Borvak, J. Banchereau, and V. Pascual. 2003. Interferon and granulopoiesis signatures in systemic lupus erythematosus blood. J. Exp. Med. 197: 711-723. https://doi.org/10.1084/jem.20021553
  40. Obermoser, G. and V. Pascual. 2010. The interferon-alpha signature of systemic lupus erythematosus. Lupus 19: 1012-1019. https://doi.org/10.1177/0961203310371161
  41. Luo, X., L. Zhang, M. Li, W. Zhang, X. Leng, F. Zhang, Y. Zhao, and X. Zeng. 2013. The role of miR-125b in T lymphocytes in the pathogenesis of systemic lupus erythematosus. Clin. Exp. Rheumatol. 31: 263-271.
  42. Lu, M. C., N. S. Lai, H. C. Chen, H. C. Yu, K. Y. Huang, C. H. Tung, H. B. Huang, and C. L. Yu. 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: 91-99. https://doi.org/10.1111/j.1365-2249.2012.04676.x
  43. Zhao, S., Y. Wang, Y. Liang, M. Zhao, H. Long, S. Ding, H. Yin, and Q. Lu. 2011. MicroRNA-126 regulates DNA methylation in $CD4^+$ T cells and contributes to systemic lupus erythematosus by targeting DNA methyltransferase 1. Arthritis Rheum. 63: 1376-1386. https://doi.org/10.1002/art.30196
  44. Stagakis, E., G. Bertsias, P. Verginis, M. Nakou, M. Hatziapostolou, H. Kritikos, D. Iliopoulos, and D. T. Boumpas. 2011. 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. 70: 1496-1506. https://doi.org/10.1136/ard.2010.139857
  45. Pan, W., S. Zhu, M. Yuan, H. Cui, L. Wang, X. Luo, J. Li, H. Zhou, Y. Tang, and N. Shen. 2010. MicroRNA-21 and microRNA-148a contribute to DNA hypomethylation in lupus $CD4^+$ T cells by directly and indirectly targeting DNA methyltransferase 1. J. Immunol. 184: 6773-6781. https://doi.org/10.4049/jimmunol.0904060
  46. Zhu, X., J. Liang, F. Li, Y. Yang, L. Xiang, and J. Xu. 2011. Analysis of associations between the patterns of global DNA hypomethylation and expression of DNA methyltransferase in patients with systemic lupus erythematosus. Int. J. Dermatol. 50: 697-704. https://doi.org/10.1111/j.1365-4632.2010.04804.x
  47. Richardson, B., L. Scheinbart, J. Strahler, L. Gross, S. Hanash, and M. Johnson. 1990. Evidence for impaired T cell DNA methylation in systemic lupus erythematosus and rheumatoid arthritis. Arthritis Rheum. 33: 1665-1673. https://doi.org/10.1002/art.1780331109
  48. Zhang, Y., M. Zhao, A. H. Sawalha, B. Richardson, and Q. Lu. 2013. Impaired DNA methylation and its mechanisms in $CD4^+T$ cells of systemic lupus erythematosus. J. Autoimmun. 41: 92-99. https://doi.org/10.1016/j.jaut.2013.01.005
  49. Qin, H., X. Zhu, J. Liang, J. Wu, Y. Yang, S. Wang, W. Shi, and J. Xu. 2013. MicroRNA-29b contributes to DNA hypomethylation of $CD4^+$ T cells in systemic lupus erythematosus by indirectly targeting DNA methyltransferase 1. J. Dermatol. Sci. 69: 61-67. https://doi.org/10.1016/j.jdermsci.2012.10.011
  50. Dai, Y., Y. S. Huang, M. Tang, T. Y. Lv, C. X. Hu, Y. H. Tan, Z. M. Xu, and Y. B. Yin. 2007. Microarray analysis of microRNA expression in peripheral blood cells of systemic lupus erythematosus patients. Lupus 16: 939-946. https://doi.org/10.1177/0961203307084158
  51. Sheedy, F. J., E. Palsson-McDermott, E. J. Hennessy, C. Martin, J. J. O'Leary, Q. Ruan, D. S. Johnson, Y. Chen, and L. A. O'Neill. 2010. Negative regulation of TLR4 via targeting of the proinflammatory tumor suppressor PDCD4 by the microRNA miR-21. Nat. Immunol. 11: 141-147. https://doi.org/10.1038/ni.1828
  52. Ding, S., Y. Liang, M. Zhao, G. Liang, H. Long, S. Zhao, Y. Wang, H. Yin, P. Zhang, Q. Zhang, and Q. Lu. 2012. Decreased microRNA-142-3p/5p expression causes $CD4^+$ T cell activation and B cell hyperstimulation in systemic lupus erythematosus. Arthritis Rheum. 64: 2953-2963. https://doi.org/10.1002/art.34505
  53. Cannons, J. L., H. Qi, K. T. Lu, M. Dutta, J. Gomez-Rodriguez, J. Cheng, E. K. Wakeland, R. N. Germain, and P. L. Schwartzberg. 2010. Optimal germinal center responses require a multistage T cell: B cell adhesion process involving integrins, SLAM-associated protein, and CD84. Immunity 32: 253-265. https://doi.org/10.1016/j.immuni.2010.01.010
  54. Komori, H., H. Furukawa, S. Mori, M. R. Ito, M. Terada, M. C. Zhang, N. Ishii, N. Sakuma, M. Nose, and M. Ono. 2006. A signal adaptor SLAM-associated protein regulates spontaneous autoimmunity and Fas-dependent lymphoproliferation in MRL-Faslpr lupus mice. J. Immunol. 176: 395-400. https://doi.org/10.4049/jimmunol.176.1.395
  55. Alcocer-Varela, J. and D. Alarcon-Segovia. 1982. Decreased production of and response to interleukin-2 by cultured lymphocytes from patients with systemic lupus erythematosus. J. Clin. Invest. 69: 1388-1392. https://doi.org/10.1172/JCI110579
  56. Boyman, O. and J. Sprent. 2012. The role of interleukin-2 during homeostasis and activation of the immune system. Nat. Rev. Immunol. 12: 180-190.
  57. Fan, W., D. Liang, Y. Tang, B. Qu, H. Cui, X. Luo, X. Huang, S. Chen, B. W. Higgs, B. Jallal, Y. Yao, J. B. Harley, and N. Shen. 2012. 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. 64: 3715-3725. https://doi.org/10.1002/art.34596
  58. Xue, F., H. Li, J. Zhang, J. Lu, Y. Xia, and Q. Xia. 2013. miR-31 regulates interleukin 2 and kinase suppressor of ras 2 during T cell activation. Genes Immun. 14: 127-131. https://doi.org/10.1038/gene.2012.58
  59. Helms, W. S., J. L. Jeffrey, D. A. Holmes, M. B. Townsend, N. A. Clipstone, and L. Su. 2007. Modulation of NFAT-dependent gene expression by the RhoA signaling pathway in T cells. J. Leukoc. Biol. 82: 361-369. https://doi.org/10.1189/jlb.0206120
  60. Rouas, R., H. Fayyad-Kazan, N. El Zein, P. Lewalle, F. Rothe, A. Simion, H. Akl, M. Mourtada, M. El Rifai, A. Burny, P. Romero, P. Martiat, and B. Badran. 2009. Human natural Treg microRNA signature: role of microRNA-31 and microRNA-21 in FOXP3 expression. Eur. J. Immunol. 39: 1608-1618. https://doi.org/10.1002/eji.200838509
  61. Zhao, X., Y. Tang, B. Qu, H. Cui, S. Wang, L. Wang, X. Luo, X. Huang, J. Li, S. Chen, and N. Shen. 2010. MicroRNA-125a contributes to elevated inflammatory chemokine RANTES levels via targeting KLF13 in systemic lupus erythematosus. Arthritis Rheum. 62: 3425-3435. https://doi.org/10.1002/art.27632
  62. Lu, M. M., J. Wang, H. F. Pan, G. M. Chen, J. Li, H. Cen, C. C. Feng, and D. Q. Ye. 2012. Increased serum RANTES in patients with systemic lupus erythematosus. Rheumatol. Int. 32: 1231-1233. https://doi.org/10.1007/s00296-010-1761-2
  63. Song, A., Y. F. Chen, K. Thamatrakoln, T. A. Storm, and A. M. Krensky. 1999. RFLAT-1: a new zinc finger transcription factor that activates RANTES gene expression in T lymphocytes. Immunity 10: 93-103. https://doi.org/10.1016/S1074-7613(00)80010-2
  64. Liu, Y., J. Dong, R. Mu, Y. Gao, X. Tan, Y. Li, Z. Li, and G. Yang. 2013. MicroRNA-30a promotes B cell hyperactivity in patients with systemic lupus erythematosus by direct interaction with Lyn. Arthritis Rheum. 65: 1603-1611. https://doi.org/10.1002/art.37912
  65. Liossis, S. N., E. E. Solomou, M. A. Dimopoulos, P. Panayiotidis, M. M. Mavrikakis, and P. P. Sfikakis. 2001. B-cell kinase lyn deficiency in patients with systemic lupus erythematosus. J. Investig. Med. 49: 157-165. https://doi.org/10.2310/6650.2001.34042
  66. Flores-Borja, F., P. S. Kabouridis, E. C. Jury, D. A. Isenberg, and R. A. Mageed. 2005. Decreased Lyn expression and translocation to lipid raft signaling domains in B lymphocytes from patients with systemic lupus erythematosus. Arthritis Rheum. 52: 3955-3965. https://doi.org/10.1002/art.21416
  67. Zan, H. and P. Casali. 2013. Regulation of Aicda expression and AID activity. Autoimmunity 46: 83-101. https://doi.org/10.3109/08916934.2012.749244
  68. Diaz, M. 2013. The role of activation-induced deaminase in lupus nephritis. Autoimmunity 46: 115-120. https://doi.org/10.3109/08916934.2012.750303
  69. Jiang, C., J. Foley, N. Clayton, G. Kissling, M. Jokinen, R. Herbert, and M. Diaz. 2007. Abrogation of lupus nephritis in activation-induced deaminase-deficient MRL/lpr mice. J. Immunol. 178: 7422-7431. https://doi.org/10.4049/jimmunol.178.11.7422
  70. Dorsett, Y., K. M. McBride, M. Jankovic, A. Gazumyan, T. H. Thai, D. F. Robbiani, M. Di Virgilio, B. Reina San-Martin, G. Heidkamp, T. A. Schwickert, T. Eisenreich, K. Rajewsky, and M. C. Nussenzweig. 2008. MicroRNA-155 suppresses activation-induced cytidine deaminase-mediated Myc-Igh translocation. Immunity 28: 630-638. https://doi.org/10.1016/j.immuni.2008.04.002
  71. Teng, G., P. Hakimpour, P. Landgraf, A. Rice, T. Tuschl, R. Casellas, and F. N. Papavasiliou. 2008. MicroRNA-155 is a negative regulator of activation-induced cytidine deaminase. Immunity 28: 621-629. https://doi.org/10.1016/j.immuni.2008.03.015
  72. De Yebenes, V. G., L. Belver, D. G. Pisano, S. Gonzalez, A. Villasante, C. Croce, L. He, and A. R. Ramiro. 2008. miR-181b negatively regulates activation-induced cytidine deaminase in B cells. J. Exp. Med. 205: 2199-2206. https://doi.org/10.1084/jem.20080579
  73. Dai, R., Y. Zhang, D. Khan, B. Heid, D. Caudell, O. Crasta, and S. A. Ahmed. 2010. Identification of a common lupus disease-associated microRNA expression pattern in three different murine models of lupus. PLoS One 5: e14302. https://doi.org/10.1371/journal.pone.0014302
  74. Thai, T. H., H. C. Patterson, D. H. Pham, K. Kis-Toth, D. A. Kaminski, and G. C. Tsokos. 2013. Deletion of microRNA-155 reduces autoantibody responses and alleviates lupus-like disease in the Fas(lpr) mouse. Proc. Natl. Acad. Sci. USA 110: 20194-20199. https://doi.org/10.1073/pnas.1317632110
  75. Yuan, Y., S. Kasar, C. Underbayev, D. Vollenweider, E. Salerno, S. V Kotenko, and E. Raveche. 2012. Role of microRNA-15a in autoantibody production in interferon- augmented murine model of lupus. Mol. Immunol. 52: 61-70. https://doi.org/10.1016/j.molimm.2012.04.007
  76. Boldin, M. P., K. D. Taganov, D. S. Rao, L. Yang, J. L. Zhao, M. Kalwani, Y. Garcia-Flores, M. Luong, A. Devrekanli, J. Xu, G. Sun, J. Tay, P. S. Linsley, and D. Baltimore. 2011. miR-146a is a significant brake on autoimmunity, myeloproliferation, and cancer in mice. J. Exp. Med. 208: 1189-1201. https://doi.org/10.1084/jem.20101823
  77. Hou, J., P. Wang, L. Lin, X. Liu, F. Ma, H. An, Z. Wang, and X. Cao. 2009. MicroRNA-146a feedback inhibits RIG-I-dependent Type I IFN production in macrophages by targeting TRAF6, IRAK1, and IRAK2. J. Immunol. 183: 2150-2158. https://doi.org/10.4049/jimmunol.0900707
  78. Luo, X., W. Yang, D. Q. Ye, H. Cui, Y. Zhang, N. Hirankarn, X. Qian, Y. Tang, Y. L. Lau, N. de Vries, P. P. Tak, B. P. Tsao, and N. Shen. 2011. A functional variant in microRNA-146a promoter modulates its expression and confers disease risk for systemic lupus erythematosus. PLoS Genet. 7: e1002128. https://doi.org/10.1371/journal.pgen.1002128
  79. Karrich, J. J., L. C. Jachimowski, M. Libouban, A. Iyer, K. Brandwijk, E. W. Taanman-Kueter, M. Nagasawa, E. C. de Jong, C. H. Uittenbogaart, and B. Blom. 2013. MicroRNA-146a regulates survival and maturation of human plasmacytoid dendritic cells. Blood 122: 3001-3009. https://doi.org/10.1182/blood-2012-12-475087
  80. Chan, V. S., Y. J. Nie, N. Shen, S. Yan, M. Y. Mok, and C. S. Lau. 2012. Distinct roles of myeloid and plasmacytoid dendritic cells in systemic lupus erythematosus. Autoimmun. Rev. 11: 890-897. https://doi.org/10.1016/j.autrev.2012.03.004
  81. Charrier, E., P. Cordeiro, M. Cordeau, R. Dardari, A. Michaud, M. Harnois, N. Merindol, S. Herblot, and M. Duval. 2012. Post-transcriptional down-regulation of Toll-like receptor signaling pathway in umbilical cord blood plasmacytoid dendritic cells. Cell. Immunol. 276: 114-121. https://doi.org/10.1016/j.cellimm.2012.04.010
  82. Jin, O., S. Kavikondala, L. Sun, R. Fu, M. Y. Mok, A. Chan, J. Yeung, and C. S. Lau. 2008. Systemic lupus erythematosus patients have increased number of circulating plasmacytoid dendritic cells, but decreased myeloid dendritic cells with deficient CD83 expression. Lupus 17: 654-662. https://doi.org/10.1177/0961203308089410
  83. Jin, O., S. Kavikondala, M. Y. Mok, L. Sun, J. Gu, R. Fu, A. Chan, J. Yeung, Y. Nie, and C. S. Lau. 2010. Abnormalities in circulating plasmacytoid dendritic cells in patients with systemic lupus erythematosus. Arthritis Res. Ther. 12: R137. https://doi.org/10.1186/ar3075
  84. Pan, Y., T. Jia, Y. Zhang, K. Zhang, R. Zhang, J. Li, and L. Wang. 2012. MS2 VLP-based delivery of microRNA-146a inhibits autoantibody production in lupus-prone mice. Int. J. Nanomedicine 7: 5957-5967.
  85. Garchow, B. G., O. Bartulos Encinas, Y. T. Leung, P. Y. Tsao, R. A. Eisenberg, R. Caricchio, S. Obad, A. Petri, S. Kauppinen, and M. Kiriakidou. 2011. Silencing of microRNA-21 in vivo ameliorates autoimmune splenomegaly in lupus mice. EMBO Mol. Med. 3: 605-615. https://doi.org/10.1002/emmm.201100171
  86. Keller, A., P. Leidinger, A. Bauer, A. Elsharawy, J. Haas, C. Backes, A. Wendschlag, N. Giese, C. Tjaden, K. Ott, J. Werner, T. Hackert, K. Ruprecht, H. Huwer, J. Huebers, G. Jacobs, P. Rosenstiel, H. Dommisch, A. Schaefer, J. Muller-Quernheim, B. Wullich, B. Keck, N. Graf, J. Reichrath, B. Vogel, A. Nebel, S. U. Jager, P. Staehler, I. Amarantos, V. Boisguerin, C. Staehler, M. Beier, M. Scheffler, M. W. Buchler, J. Wischhusen, S. F. M. Haeusler, J. Dietl, S. Hofmann, H. P. Lenhof, S. Schreiber, H. A. Katus, W. Rottbauer, B. Meder, J. D. Hoheisel, A. Franke, and E. Meese. 2011. Toward the blood-borne miRNome of human diseases. Nat. Methods 8: 841-843. https://doi.org/10.1038/nmeth.1682
  87. Su, X., C. Qian, Q. Zhang, J. Hou, Y. Gu, Y. Han, Y. Chen, M. Jiang, and X. Cao. 2013. miRNomes of haematopoietic stem cells and dendritic cells identify miR-30b as a regulator of Notch1. Nat. Commun. 4: 2903.

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