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Differential microRNA Profile and Post-Transcriptional Regulation Exist in Systemic Lupus Erythematosus Patients with Distinct Autoantibody Specificities

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Abstract

Purpose

Systemic lupus erythematosus (SLE) patients have anti-nuclear autoantibodies directed against dsDNA and RNA-associated antigens (extractable nuclear antigens; ENA). In this study, we investigated the differences in microRNA (miRNA) expression and its biological implications in SLE patients with distinct autoantibody specificities.

Methods

The SLE patients were grouped into three subsets based on the type of autoantibodies present in their sera (anti-ENA+ group with autoantibodies against ENA alone; anti-dsDNA+ group having autoantibodies against dsDNA only, and anti-ENA+dsDNA+ group having autoantibodies to both dsDNA and ENA). Global miRNA expression profiling was done for each of these three groups using TaqMan® low density miRNA arrays.

Results

We report that different sets of miRNAs are dysregulated in SLE patients with different autoantibody specificities. Further, Ingenuity pathway analysis (IPA) software revealed specific biological pathways that were targeted by miRNAs dysregulated in different SLE subsets. Molecules involved in cell cycle and cytoskeleton remodeling were the prime targets of miRNAs dysregulated in anti-ENA+ patients whereas miRNAs dysregulated in anti-dsDNA+ patients were found to be implicated in multiple cytokine signaling pathways. IPA analysis of gene targets of miRNAs commonly dysregulated in all three SLE subsets identified several metabolic-, hormone-, and interferon-related pathways to be affected.

Conclusion

The differential miRNA expression in patients with distinct autoantibodies is suggestive of different regulatory mechanisms operating among them. Based on these observations, we are hopeful that this ‘sub-grouping’ approach could be used to identify other defective processes associated with varying disease manifestations in SLE and may be considered when designing therapeutic interventions.

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References

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  PubMed Central  PubMed  Google Scholar 

  5. Zhang S, Semino CE. Design peptide scaffolds for regenerative medicine. Adv Exp Med Biol. 2003;534:147–63.

    Article  CAS  PubMed  Google Scholar 

  6. Doench JG, Sharp PA. Specificity of microRNA target selection in translational repression. Genes Dev. 2004;18(5):504–11.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  7. Wienholds E, Plasterk RH. MicroRNA function in animal development. FEBS Lett. 2005;579(26):5911–22.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  9. Lindsay MA. microRNAs and the immune response. Trends Immunol. 2008;29(7):343–51.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  PubMed Central  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  16. Rai G, Ray S, Milton J, Yang J, Ren P, Lempicki R, et al. Gene expression profiles in a rabbit model of systemic lupus erythematosus autoantibody production. J Immunol. 2010;185(7):4446–56.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  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.

    Google Scholar 

  18. Hochberg MC. Updating the American College of Rheumatology revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum. 1997;40(9):1725.

    Article  CAS  PubMed  Google Scholar 

  19. Gladman DD, Ibañez D, Urowitz MB. Systemic lupus erythematosus disease activity index 2000. J Rheumatol. 2002;29(2):288–91.

    PubMed  Google Scholar 

  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.

    Article  CAS  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    CAS  PubMed Central  PubMed  Google Scholar 

  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.

    CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  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.

    Article  PubMed Central  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  33. Lee HM, Sugino H, Nishimoto N. Cytokine networks in systemic lupus erythematosus. J Biomed Biotechnol. 2010;2010:676284.

    PubMed Central  PubMed  Google Scholar 

  34. Jacob N, Stohl W. Cytokine disturbances in systemic lupus erythematosus. Arthritis Res Ther. 2011;13(4):228.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  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.

    Article  PubMed Central  PubMed  Google Scholar 

  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.

    Article  PubMed Central  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  47. Harley JB, James JA. Epstein-Barr virus infection induces lupus autoimmunity. Bull NYU Hosp Jt Dis. 2006;64(1–2):45–50.

    PubMed  Google Scholar 

  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.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  50. Wu G, Yu F, Xiao Z, Xu K, Xu J, Tang W, et al. Hepatitis B virus X protein downregulates expression of the miR-16 family in malignant hepatocytes in vitro. Br J Cancer. 2011;105(1):146–53.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    CAS  PubMed Central  PubMed  Google Scholar 

  60. Zhang R, Xing M, Ji X, Gu L, Yang X, Wang H, et al. Interferon-alpha 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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  62. Arasappan D, Tong W, Mummaneni P, Fang H, Amur S. Meta-analysis 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.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  64. Seitz HM, Matsushima GK. Dendritic cells in systemic lupus erythematosus. Int Rev Immunol. 2010;29(2):184–209.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  66. McMurray RW, May W. Sex hormones and systemic lupus erythematosus: review and meta-analysis. Arthritis Rheum. 2003;48(8):2100–10.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  68. Lahita RG, Bradlow HL, Kunkel HG, Fishman J. Alterations of estrogen metabolism in systemic lupus erythematosus. Arthritis Rheum. 1979;22(11):1195–8.

    Article  CAS  PubMed  Google Scholar 

  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.

    CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  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.

    Article  PubMed Central  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  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.

    PubMed Central  PubMed  Google Scholar 

  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.

    Article  PubMed Central  PubMed  Google Scholar 

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Acknowledgments

This study was supported by a grant (BT/PR4619/MED/30/834/2012) from the Department of Biotechnology, New Delhi, India. SKC is supported by senior research fellowship from Indian Council of Medical Research, New Delhi. The funding source had no involvement in study design, collection, analysis and interpretation of data, in the writing of the report as well as in the decision to submit the paper for publication. We thank Dr. Rose G Mage, NIAID, NIH, Bethesda for critical reading of the manuscript and providing help with IPA software.

Conflict of Interest

The authors declare that they have no conflict of interest.

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Authors and Affiliations

  1. Department of Molecular and Human Genetics, Banaras Hindu University, Varanasi, 221005, India

    Sudhir Kumar Chauhan, Vikas Vikram Singh, Richa Rai & Geeta Rai

  2. Department of Medicine, Institute of Medical Sciences, Banaras Hindu University, Varanasi, India

    Madhukar Rai

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  1. Sudhir Kumar Chauhan
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Chauhan, S.K., Singh, V.V., Rai, R. et al. Differential microRNA Profile and Post-Transcriptional Regulation Exist in Systemic Lupus Erythematosus Patients with Distinct Autoantibody Specificities. J Clin Immunol 34, 491–503 (2014). https://doi.org/10.1007/s10875-014-0008-5

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