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The Role of microRNAs in the Control and Mechanism of Action of IL-10

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Interleukin-10 in Health and Disease

Part of the book series: Current Topics in Microbiology and Immunology ((CT MICROBIOLOGY,volume 380))

Abstract

Recent studies have shown an important interplay between Interleukin 10 (IL-10) and microRNAs. IL-10 can be directly post-transcriptionally regulated by several microRNA, including miR-106a, miR-4661, miR-98, miR-27, let7 and miR-1423p/5p. miRNA targeting of IL-10 has been suggested to play a role in autoimmune and inflammatory diseases such as SLE, reperfusion injury and asthma. Another miRNA, miR-21, has been shown to indirectly regulate IL-10 via downregulation of the IL-10 inhibitor PDCD4. The targeting of IL-10 in this way has been linked to host defence modulation by Mycobacterium leprae. Viral miRNAs, such as miR-K12-3 from Kaposi’s sarcoma-associated herpesvirus (KSHV), can also decrease IL-10 to promote tumour development. Finally this interplay can operate in a feedback loop, with IL-10 capable of regulating microRNAs, upregulating those that can contribute to exerting the anti-inflammatory response, such as miR-187, and downregulating those that are highly pro-inflammatory, such as miR-155. Understanding the two-way regulation between miRNA and IL-10 is giving rise to new insights into this important cytokine.

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References

  • Asadullah K, Sterry W, Volk HD (2003a) Interleukin-10 therapy–review of a new approach. Pharmacol Rev 55(2):241–269

    Article  CAS  PubMed  Google Scholar 

  • Cai X et al (2005) Kaposi’s sarcoma-associated herpesvirus expresses an array of viral microRNAs in latently infected cells. Proc Natl Acad Sci USA 102(15):5570–5575

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Chen CZ et al (2004) microRNAs modulate hematopoietic lineage differentiation. Science 303(5654):83–86

    Article  CAS  PubMed  Google Scholar 

  • Ding S et al (2012) Decreased microRNA-142-3p/5p expression causes CD4+ T cell activation and B cell hyperstimulation in systemic lupus erythematosus. Arthritis Rheum 64(9):2953–2963

    Article  CAS  PubMed  Google Scholar 

  • Guan H et al (2013) MicroRNA let-7e is associated with the pathogenesis of experimental autoimmune encephalomyelitis. Eur J Immunol 43(1):104–114

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hutchison ER et al (2013) Evidence for miR-181 involvement in neuroinflammatory responses of astrocytes. Glia 61(7):1018–1028

    Google Scholar 

  • Jiang L et al (2012) Altered let-7 expression in Myasthenia gravis and let-7c mediated regulation of IL-10 by directly targeting IL-10 in Jurkat cells. Int Immunopharmacol 14(2):217–223

    Article  CAS  PubMed  Google Scholar 

  • Jing Q et al (2005) Involvement of microRNA in AU-rich element-mediated mRNA instability. Cell 120(5):623–634

    Article  CAS  PubMed  Google Scholar 

  • Kent OA, Mendell JT (2006) A small piece in the cancer puzzle: microRNAs as tumor suppressors and oncogenes. Oncogene 25(46):6188–6196

    Article  CAS  PubMed  Google Scholar 

  • Lagos-Quintana M et al (2001) Identification of novel genes coding for small expressed RNAs. Science 294(5543):853–858

    Article  CAS  PubMed  Google Scholar 

  • Lau NC et al (2001) An abundant class of tiny RNAs with probable regulatory roles in Caenorhabditis elegans. Science 294(5543):858–862

    Article  CAS  PubMed  Google Scholar 

  • Lee RC, Ambros V (2001) An extensive class of small RNAs in Caenorhabditis elegans. Science 294(5543):862–864

    Article  CAS  PubMed  Google Scholar 

  • Lee RC, Feinbaum RL, Ambros V (1993) The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 75(5):843–854

    Article  CAS  PubMed  Google Scholar 

  • Lindsay MA (2008) microRNAs and the immune response. Trends Immunol 29(7):343–351

    Article  CAS  PubMed  Google Scholar 

  • Liu Y et al (2011) MicroRNA-98 negatively regulates IL-10 production and endotoxin tolerance in macrophages after LPS stimulation. FEBS Lett 585(12):1963–1968

    Article  CAS  PubMed  Google Scholar 

  • Liu PT et al (2012) MicroRNA-21 targets the vitamin D-dependent antimicrobial pathway in leprosy. Nat Med 18(2):267–273

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ma F et al (2010) MicroRNA-466l upregulates IL-10 expression in TLR-triggered macrophages by antagonizing RNA-binding protein tristetraprolin-mediated IL-10 mRNA degradation. J Immunol 184(11):6053–6059

    Article  CAS  PubMed  Google Scholar 

  • McCoy CE et al (2010) IL-10 inhibits miR-155 induction by toll-like receptors. J Biol Chem 285(27):20492–20498

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Moschos SA et al (2007) Expression profiling in vivo demonstrates rapid changes in lung microRNA levels following lipopolysaccharide-induced inflammation but not in the anti-inflammatory action of glucocorticoids. BMC Genom 8:240

    Article  Google Scholar 

  • Murray PJ (2006) Understanding and exploiting the endogenous interleukin-10/STAT3-mediated anti-inflammatory response. Curr Opin Pharmacol 6(4):379–386

    Article  CAS  PubMed  Google Scholar 

  • O’Connell RM et al (2007) MicroRNA-155 is induced during the macrophage inflammatory response. Proc Natl Acad Sci USA 104(5):1604–1609

    Article  PubMed Central  PubMed  Google Scholar 

  • O’Connell RM et al (2009) Inositol phosphatase SHIP1 is a primary target of miR-155. Proc Natl Acad Sci USA 106(17):7113–7118

    Article  PubMed Central  PubMed  Google Scholar 

  • O’Connell RM et al (2010) MicroRNA-155 promotes autoimmune inflammation by enhancing inflammatory T cell development. Immunity 33(4):607–619

    Article  PubMed Central  PubMed  Google Scholar 

  • Poole E et al (2011) Virally induced changes in cellular microRNAs maintain latency of human cytomegalovirus in CD34(+) progenitors. J Gen Virol 92(Pt 7):1539–1549

    Article  CAS  PubMed  Google Scholar 

  • Powell MJ et al (2000) Posttranscriptional regulation of IL-10 gene expression through sequences in the 3’-untranslated region. J Immunol 165(1):292–296

    Article  CAS  PubMed  Google Scholar 

  • Qin Z et al (2010) Pivotal advance: Kaposi’s sarcoma-associated herpesvirus (KSHV)-encoded microRNA specifically induce IL-6 and IL-10 secretion by macrophages and monocytes. J Leukoc Biol 87(1):25–34

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Rodriguez A et al (2007) Requirement of bic/microRNA-155 for normal immune function. Science 316(5824):608–611

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Rossato M et al (2012) IL-10-induced microRNA-187 negatively regulates TNF-alpha, IL-6, and IL-12p40 production in TLR4-stimulated monocytes. Proc Natl Acad Sci USA 109(45):E3101–E3110

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Samols MA et al (2005) Cloning and identification of a microRNA cluster within the latency-associated region of Kaposi’s sarcoma-associated herpesvirus. J Virol 79(14):9301–9305

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Schaefer JS et al (2011) Selective upregulation of microRNA expression in peripheral blood leukocytes in IL-10-/- mice precedes expression in the colon. J Immunol 187(11):5834–5841

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Schickel R et al (2008) microRNAs: key players in the immune system, differentiation, tumorigenesis and cell death. Oncogene 27(45):5959–5974

    Article  CAS  PubMed  Google Scholar 

  • Sharma A et al (2009) Posttranscriptional regulation of interleukin-10 expression by hsa-miR-106a. Proc Natl Acad Sci USA 106(14):5761–5766

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Sharma A et al (2012) Antagonism of mmu-mir-106a attenuates asthma features in allergic murine model. J Appl Physiol 113(3):459–464

    Article  CAS  PubMed  Google Scholar 

  • Sheedy FJ et al (2010) Negative regulation of TLR4 via targeting of the proinflammatory tumor suppressor PDCD4 by the microRNA miR-21. Nat Immunol 11(2):141–147

    Article  CAS  PubMed  Google Scholar 

  • Shinomiya S et al (2001) Regulation of TNFalpha and interleukin-10 production by prostaglandins I(2) and E(2): studies with prostaglandin receptor-deficient mice and prostaglandin E-receptor subtype-selective synthetic agonists. Biochem Pharmacol 61(9):1153–1160

    Article  CAS  PubMed  Google Scholar 

  • Stagakis E et al (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(8):1496–1506

    Article  CAS  PubMed  Google Scholar 

  • Swaminathan S et al (2012) Differential regulation of the Let-7 family of microRNAs in CD4+ T cells alters IL-10 expression. J Immunol 188(12):6238–6246

    Article  CAS  PubMed  Google Scholar 

  • Taganov KD et al (2006) NF-kappaB-dependent induction of microRNA miR-146, an inhibitor targeted to signaling proteins of innate immune responses. Proc Natl Acad Sci USA 103(33):12481–12486

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Thai TH et al (2007) Regulation of the germinal center response by microRNA-155. Science 316(5824):604–608

    Article  CAS  PubMed  Google Scholar 

  • Tone M et al (2000) IL-10 gene expression is controlled by the transcription factors Sp1 and Sp3. J Immunol 165(1):286–291

    Article  CAS  PubMed  Google Scholar 

  • Wightman B, Ha I, Ruvkun G (1993) Posttranscriptional regulation of the heterochronic gene lin-14 by lin-4 mediates temporal pattern formation in C. elegans. Cell 75(5):855–862

    Article  CAS  PubMed  Google Scholar 

  • Yeh CH et al (2012) microRNA-27a regulates cardiomyocytic apoptosis during cardioplegia-induced cardiac arrest by targeting interleukin 10-related pathways. Shock 38(6):607–614

    Article  CAS  PubMed  Google Scholar 

Download references

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Authors and Affiliations

  1. Department of Biochemistry and Immunology, Trinity Biomedical Sciences Institute, Dublin 2, Ireland

    Susan R. Quinn & Luke A. O’Neill

Authors
  1. Susan R. Quinn
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  2. Luke A. O’Neill
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Correspondence to Susan R. Quinn .

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Editors and Affiliations

  1. Deutsches Rheuma-Forschungszentrum Berlin, Berlin, Germany

    Simon Fillatreau

  2. Div. of Immunoregulation, The MRC National Institute for Medical Research, London, United Kingdom

    Anne O'Garra

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© 2014 Springer-Verlag Berlin Heidelberg

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Quinn, S.R., O’Neill, L.A. (2014). The Role of microRNAs in the Control and Mechanism of Action of IL-10. In: Fillatreau, S., O'Garra, A. (eds) Interleukin-10 in Health and Disease. Current Topics in Microbiology and Immunology, vol 380. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-662-43492-5_7

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