Differential microRNA profile and post-transcriptional regulation exist in systemic lupus erythematosus patients with distinct autoantibody specificities

Journal of Clinical Immunology

Volumn 34, Issue 4, 2014, Pages 491-503

  Chauhan, Sudhir Kumar ^a   Singh, Vikas Vikram ^a   Rai, Richa ^a   Rai, Madhukar ^b   Rai, Geeta ^a  

^a BANARAS HINDU UNIVERSITY   (India)

^b BANARAS HINDU UNIVERSITY   (India)

Author keywords

autoantibodies.; dsDNA; extractable nuclear antigens; microRNA; Systemic lupus erythematosus

Indexed keywords

AUTOANTIBODY; DOUBLE STRANDED DNA ANTIBODY; ESTROGEN RECEPTOR; EXTRACTABLE NUCLEAR ANTIGEN ANTIBODY; MICRORNA; PLATELET DERIVED GROWTH FACTOR; UNCLASSIFIED DRUG; ANTINUCLEAR ANTIBODY; CELL NUCLEUS ANTIGEN; DNA;

ADOLESCENT; ADULT; ANTIBODY SPECIFICITY; ARTICLE; CELL CYCLE; CLINICAL ARTICLE; CYTOSKELETON; DOWN REGULATION; FEMALE; GENE EXPRESSION PROFILING; GENE TARGETING; HUMAN; IMMUNE RESPONSE; PRIORITY JOURNAL; SYSTEMIC LUPUS ERYTHEMATOSUS; TRANSCRIPTION REGULATION; CLASSIFICATION; COMPUTER PROGRAM; DNA MICROARRAY; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORK; GENETICS; IMMUNOLOGY; MALE; METABOLISM; MIDDLE AGED; PATHOLOGY; SIGNAL TRANSDUCTION;

ADOLESCENT; ADULT; ANTIBODIES, ANTINUCLEAR; ANTIBODY SPECIFICITY; ANTIGENS, NUCLEAR; DNA; FEMALE; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORKS; HUMANS; LUPUS ERYTHEMATOSUS, SYSTEMIC; MALE; METABOLIC NETWORKS AND PATHWAYS; MICRORNAS; MIDDLE AGED; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION; SOFTWARE;

EID: 84901452242     PISSN: 02719142     EISSN: 15732592     Source Type: Journal    
DOI: 10.1007/s10875-014-0008-5     Document Type: Article

References (76)

1. Swaak AJ, Huysen V, Nossent JC, Smeenk RJ. Antinuclear antibody profiles in relation to specific disease manifestations of systemic lupus erythematosus. Clin Rheumatol. 1990;9:82-94.
2. Hoffman IE, Peene I, Meheus L, Huizinga TW, Cebecauer L, Isenberg D, et al. Specific antinuclear antibodies are associated with clinical features in systemic lupus erythematosus. Ann Rheum Dis. 2004;63:1155-8. (Pubitemid 39120371)
3. Clotet B, Guardia J, Pigrau C, Lience E, Murcia C, Pujol R, et al. Incidence and clinical significance of anti-ENA antibodies in systemic lupus erythematosus. Estimation by counterimmunoelectrophoresis. Scand J Rheumatol. 1984;13: 15-20. (Pubitemid 14139757)
4. Jakymiw A, Ikeda K, Fritzler MJ, Reeves WH, Satoh M, Chan EK. Autoimmune targeting of key components of RNA interference. Arthritis Res Ther. 2006;8(4):R87.
5. Zhang S, Semino CE. Design peptide scaffolds for regenerative medicine. Adv Exp Med Biol. 2003;534:147-63. (Pubitemid 41582794)
6. Doench JG, Sharp PA. Specificity of microRNA target selection in translational repression. Genes Dev. 2004;18(5):504-11. (Pubitemid 38372808)
7. Wienholds E, Plasterk RH. MicroRNA function in animal development. FEBS Lett. 2005;579(26):5911-22. (Pubitemid 41487106)
8. Redis RS, Calin S, Yang Y, You MJ, Calin GA. Cell-to-cell miRNA transfer: from body homeostasis to therapy. Pharmacol Ther. 2012;136(2):169-74.
9. Lindsay MA. microRNAs and the immune response. Trends Immunol. 2008;29(7):343-51.
10. Dai Y, Huang YS, Tang M, Lv TY, Hu CX, Tan YH, et al.Microarray analysis of microRNA expression in peripheral blood cells of systemic lupus erythematosus patients. Lupus. 2007;16(12):939-46.
11. Dai Y, Sui W, Lan H, Yan Q, Huang H, Huang Y. Comprehensive analysis of microRNA expression patterns in renal biopsies of lupus nephritis patients. Rheumatol Int. 2009;29(7):749-54.
12. 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(4):1065-75.
13. Te JL, Dozmorov IM, Guthridge JM, Nguyen KL, Cavett JW, Kelly JA, et al. Identification of unique microRNA signature associated with lupus nephritis. PLoS One. 2010;5(5):e10344.
14. 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):1496-506.
15. Chauhan SK, Singh VV, Rai R, Rai M, Rai G. Distinct autoantibody profiles in systemic lupus erythematosus patients are selectively associated with TLR7 and TLR9 upregulation. J Clin Immunol. 2013;33(5):954-64.
16. Rai G, Ray S, Milton J, Yang J, Ren P, Lempicki R, et al. Gene expression profiles in a rabbitmodel of systemic lupus erythematosus autoantibody production. J Immunol. 2010;185(7):4446-56.
17. Mage RG, Rai G. A rabbit model of systemic lupus erythematosus, useful for studies of neuropsychiatric SLE. In: Almoallim H, editor. Systemic lupus erythematosus. Croatia: InTech; 2012. p. 201-16.
18. Hochberg MC. Updating the American College of Rheumatology revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum. 1997;40(9):1725.
19. Gladman DD, Ibañez D, UrowitzMB. Systemic lupus erythematosus disease activity index 2000. J Rheumatol. 2002;29(2):288-91. (Pubitemid 34118775)
20. Fleige S, Pfaffl MW. RNA integrity and the effect on the real-time qRT-PCR performance. Mol Asp Med. 2006;27(2-3):126-39.
21. Lewis BP, Burge CB, Bartel DP. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell. 2005;120(1):15-20. (Pubitemid 40094598)
22. Grimson A, Farh KK, Johnston WK, Garrett-Engele P, Lim LP, Bartel DP. MicroRNA targeting specificity in mammals: determinants beyond seed pairing. Mol Cell. 2007;27(1):91-105. (Pubitemid 46991392)
23. Hara M, Kitani A, Harigai M, Hirose T, Norioka K, Hirose W, et al. Differential abnormality in cell-cycle stage of peripheral B cells from patients with systemic lupus erythematosus. Rheumatol Int. 1987;7(2):83-7. (Pubitemid 17121626)
24. Suranyi P, Matyus L, Sonkoly I, Szegedi G. Cellular DNA content of T helper, T suppressor and B lymphocytes in SLE. Clin Exp Immunol. 1984;58(1):37-41. (Pubitemid 14029121)
25. Verheijen R, Kuijpers H, Vooijs P, Van Venrooij W, Ramaekers F. Distribution of the 70K U1 RNA-associated protein during interphase and mitosis. Correlation with other U RNP particles and proteins of the nuclear matrix. J Cell Sci. 1986;86:173-90. (Pubitemid 17215089)
26. Takasaki Y, Deng JS, Tan EM. A nuclear antigen associated with cell proliferation and blast transformation. J Exp Med. 1981;154(6): 1899-909.
27. Linsley PS, Schelter J, Burchard J, Kibukawa M, Martin MM, Bartz SR, et al. Transcripts targeted by the microRNA-16 family cooperatively regulate cell cycle progression. Mol Cell Biol. 2007;27(6): 2240-52. (Pubitemid 46418479)
28. Liu Q, Fu H, Sun F, Zhang H, Tie Y, Zhu J, et al. miR-16 family induces cell cycle arrest by regulating multiple cell cycle genes. Nucleic Acids Res. 2008;36(16):5391-404.
29. Qin X,Wang X,Wang Y, Tang Z, Cui Q, Xi J, et al. MicroRNA-19a mediates the suppressive effect of laminar flow on cyclin D1 expression in human umbilical vein endothelial cells. Proc Natl Acad Sci U S A. 2010;107(7):3240-4.
30. Sachdeva M, Zhu S, Wu F, Wu H, Walia V, Kumar S, et al. p53 represses c-Myc through induction of the tumor suppressor miR-145. Proc Natl Acad Sci U S A. 2009;106(9):3207-12.
31. Tang Y, Ma X, Zhang H, Gu Z, Hou Y, Gilkeson GS, et al. Gene expression profile reveals abnormalities of multiple signaling pathways in mesenchymal stem cell derived from patients with systemic lupus erythematosus. Clin Dev Immunol. 2012;2012:826182.
32. Ghiran IC, Zeidel ML, Shevkoplyas SS, Burns JM, Tsokos GC, Kyttaris VC. Systemic lupus erythematosus serum deposits C4d on red blood cells, decreases red blood cell membrane deformability, and promotes nitric oxide production. Arthritis Rheum. 2011;63(2): 503-12.
33. Lee HM, Sugino H, Nishimoto N. Cytokine networks in systemic lupus erythematosus. J Biomed Biotechnol. 2010;2010:676284.
34. Jacob N, Stohl W. Cytokine disturbances in systemic lupus erythematosus. Arthritis Res Ther. 2011;13(4):228.
35. Davas EM, Tsirogianni A, Kappou I, Karamitsos D, Economidou I, Dantis PC. Serum IL-6, TNFalpha, p55 srTNFalpha, p75srTNFalpha, srIL-2alpha levels and disease activity in systemic lupus erythematosus. Clin Rheumatol. 1999;18(1):17-22. (Pubitemid 29104747)
36. Grondal G, Gunnarsson I, Ronnelid J, Rogberg S, Klareskog L, Lundberg I. Cytokine production, serum levels and disease activity in systemic lupus erythematosus. Clin Exp Rheumatol. 2000;18(5): 565-70.
37. Kurowska-Stolarska M, Alivernini S, Ballantine LE, Asquith DL, Millar NL, Gilchrist DS, et al. MicroRNA-155 as a proinflammatory regulator in clinical and experimental arthritis. Proc Natl Acad Sci U S A. 2011;108(27):11193-8.
38. Liu X, Zhan Z, Xu L, Ma F, Li D, Guo Z, et al. MicroRNA-148/152 impair innate response and antigen presentation of TLR-triggered dendritic cells by targeting CaMKIIalpha. J Immunol. 2010;185(12): 7244-51.
39. Petrocca F, Vecchione A, Croce CM. Emerging role of miR-106b-25/miR-17-92 clusters in the control of transforming growth factor beta signaling. Cancer Res. 2008;68(20):8191-4.
40. He M, Xu Z, Ding T, Kuang DM, Zheng L. MicroRNA-155 regulates inflammatory cytokine production in tumor-associated macrophages via targeting C/EBPbeta. Cell Mol Immunol. 2009;6(5):343-52.
41. Sharma A, Kumar M, Aich J, Hariharan M, Brahmachari SK, Agrawal A, et al. Posttranscriptional regulation of interleukin-10 expression by hsa-miR-106a. Proc Natl Acad Sci U S A. 2009;106(14):5761-6.
42. Jones MR, Quinton LJ, Blahna MT, Neilson JR, Fu S, Ivanov AR, et al. Zcchc11-dependent uridylation of microRNA directs cytokine expression. Nat Cell Biol. 2009;11(9):1157-63.
43. Morita E, Sandrin V, McCullough J, Katsuyama A, Baci Hamilton I, Sundquist WI. ESCRT-III protein requirements for HIV-1 budding. Cell Host Microbe. 2011;9(3):235-42.
44. Ushijima Y, Luo C, Kamakura M, Goshima F, Kimura H, Nishiyama Y. Herpes simplex virus UL56 interacts with and regulates the Nedd4-family ubiquitin ligase Itch. Virol J. 2010;7:179.
45. Wang MQ, Kim W, Gao G, Torrey TA, Morse 3rd HC, De Camilli P, et al. Endophilins interact with Moloney murine leukemia virus Gag and modulate virion production. J Biol. 2003;3(1):4.
46. Poole BD, Scofield RH, Harley JB, James JA. Epstein-Barr virus and molecular mimicry in systemic lupus erythematosus. Autoimmunity. 2006;39(1):63-70. (Pubitemid 43878521)
47. Harley JB, James JA. Epstein-Barr virus infection induces lupus autoimmunity. Bull NYU Hosp Jt Dis. 2006;64(1-2):45-50. (Pubitemid 44625532)
48. Forte E, Salinas RE, Chang CT, Zhou T, Linnstaedt SD, Gottwein E, et al. The Epstein-Barr Virus (EBV)-induced tumor suppressor MicroRNA MiR-34a is growth promoting in EBV-infected B cells. J Virol. 2012;86(12):6889-98.
49. Wang Y, Jiang L, Ji X, Yang B, Zhang Y, Fu XD. Hepatitis B viral RNA directly mediates down-regulation of the tumor suppressor MicroRNA miR-15a/miR-16-1 in hepatocytes. J Biol Chem. 2013;288(25):18484-93.
50. Wu G,Yu F,Xiao Z, XuK, Xu J, TangW, et al.Hepatitis B virusX protein downregulates expression of the miR-16 family in malignant hepatocytes in vitro. Br J Cancer. 2011;105(1):146-53.
51. Yin Q, McBride J, Fewell C, Lacey M, Wang X, Lin Z, et al. MicroRNA-155 is an Epstein-Barr virus-induced gene that modulates Epstein-Barr virus-regulated gene expression pathways. J Virol. 2008;82(11):5295-306. (Pubitemid 351705237)
52. Lu F, Weidmer A, Liu CG, Volinia S, Croce CM, Lieberman PM. Epstein-Barr virus-induced miR-155 attenuates NF-kappaB signaling and stabilizes latent virus persistence. J Virol. 2008;82(21):10436-43. (Pubitemid 352691173)
53. Otsuka M, Jing Q, Georgel P, New L, Chen JM, Mols J, et al. Hypersusceptibility to vesicular stomatitis virus infection in Dicer1- deficient mice is due to impaired miR24 and miR93 expression. Immunity. 2007;27(1):123-34. (Pubitemid 47089021)
54. Sibbitt Jr WL, Likar L, Spellman CW, Bankhurst AD. Impaired natural killer cell function in systemic lupus erythematosus. Relationship to interleukin-2 production. Arthritis Rheum. 1983;26(11):1316-20. (Pubitemid 14231476)
55. Park YW, Kee SJ, Cho YN, Lee EH, Lee HY, Kim EM, et al. Impaired differentiation and cytotoxicity of natural killer cells in systemic lupus erythematosus. Arthritis Rheum. 2009;60(6):1753-63.
56. Sullivan RP, Leong JW, Schneider SE, Keppel CR, Germino E, French AR, et al. MicroRNA-deficient NK cells exhibit decreased survival but enhanced function. J Immunol. 2012;188(7):3019-30.
57. Bezman NA, Cedars E, Steiner DF, Blelloch R, Hesslein DG, Lanier LL. Distinct requirements of microRNAs in NK cell activation, survival, and function. J Immunol. 2010;185(7):3835-46.
58. Liu X,Wang Y, Sun Q, Yan J, Huang J, Zhu S, et al. Identification of microRNA transcriptome involved in human natural killer cell activation. Immunol Lett. 2012;143(2):208-17.
59. Kim T, Kanayama Y, Negoro N, Okamura M, Takeda T, Inoue T. Serum levels of interferons in patients with systemic lupus erythematosus. Clin Exp Immunol. 1987;70(3):562-9. (Pubitemid 18013195)
60. Zhang R, Xing M, Ji X, Gu L, Yang X, Wang H, et al. Interferonalpha and interleukin-6 in SLE serum induce the differentiation and maturation of dendritic cells derived from CD34+ hematopoietic precursor cells. Cytokine. 2010;50(2):195-203.
61. 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(5):2610-5. (Pubitemid 36297546)
62. Arasappan D, Tong W, Mummaneni P, Fang H, Amur S. Metaanalysis of microarray data using a pathway-based approach identifies a 37-gene expression signature for systemic lupus erythematosus in human peripheral blood mononuclear cells. BMC Med. 2011;9:65.
63. Blanco P, Palucka AK, Gill M, Pascual V, Banchereau J. Induction of dendritic cell differentiation by IFN-alpha in systemic lupus erythematosus. Science. 2001;294(5546):1540-3. (Pubitemid 33063928)
64. Seitz HM, Matsushima GK. Dendritic cells in systemic lupus erythematosus. Int Rev Immunol. 2010;29(2):184-209.
65. Rosenberger CM, Podyminogin RL, Navarro G, Zhao GW, Askovich PS, Weiss MJ, et al. miR-451 regulates dendritic cell cytokine responses to influenza infection. J Immunol. 2012;189(12):5965-75.
66. McMurray RW, May W. Sex hormones and systemic lupus erythematosus: review and meta-analysis. Arthritis Rheum. 2003;48(8): 2100-10. (Pubitemid 36959189)
67. Cutolo M, Capellino S, Sulli A, Serioli B, Secchi ME, Villaggio B, et al. Estrogens and autoimmune diseases. Ann N Y Acad Sci. 2006;1089:538-47. (Pubitemid 47092097)
68. Lahita RG, Bradlow HL, Kunkel HG, Fishman J. Alterations of estrogen metabolism in systemic lupus erythematosus. Arthritis Rheum. 1979;22(11):1195-8. (Pubitemid 10163784)
69. Lahita RG, Bradlow HL, Fishman J, Kunkel HG. Abnormal estrogen and androgen metabolism in the human with systemic lupus erythematosus. Am J Kidney Dis. 1982;2(1 Suppl 1):206-11. (Pubitemid 13230795)
70. Jungers P, Nahoul K, Pelissier C, Dougados M, Tron F, Bach JF. Low plasma androgens in women with active or quiescent systemic lupus erythematosus. Arthritis Rheum. 1982;25(4):454-7. (Pubitemid 12158956)
71. Lahita RG, Bradlow HL, Ginzler E, Pang S, New M. Low plasma androgens in women with systemic lupus erythematosus. Arthritis Rheum. 1987;30(3):241-8. (Pubitemid 17098574)
72. Mo W, Zhang J, Li X, Meng D, Gao Y, Yang S, et al. Identification of novel AR-targeted microRNAs mediating androgen signalling through critical pathways to regulate cell viability in prostate cancer. PLoS One. 2013;8(2):e56592.
73. Cheung L, Gustavsson C, Norstedt G, Tollet-Egnell P. Sex-different and growth hormone-regulated expression of microRNA in rat liver. BMC Mol Biol. 2009;10:13.
74. Wu T, Xie C, Han J, Ye Y,Weiel J, Li Q, et al.Metabolic disturbances associated with systemic lupus erythematosus. PLoS One. 2012;7(6): e37210.
75. Li KJ, Wu CH, Hsieh SC, Lu MC, Tsai CY, Yu CL. Deranged bioenergetics and defective redox capacity in T lymphocytes and neutrophils are related to cellular dysfunction and increased oxidative stress in patients with active systemic lupus erythematosus. Clin Dev Immunol. 2012;2012:548516.
76. Iliopoulos D, Malizos KN, Oikonomou P, Tsezou A. Integrative MicroRNA and proteomic approaches identify novel osteoarthritis genes and their collaborative metabolic and inflammatory networks. PLoS One. 2008;3(11):e3740.