Advertisement

ncRNAs in Inflammatory and Infectious Diseases

  • Leon N. Schulte
  • Wilhelm Bertrams
  • Christina Stielow
  • Bernd Schmeck
Protocol
Part of the Methods in Molecular Biology book series (MIMB, volume 1912)

Abstract

Inflammatory and infectious diseases are among the main causes of morbidity and mortality worldwide. Inflammation is central to maintenance of organismal homeostasis upon infection, tissue damage, and malignancy. It occurs transiently in response to diverse stimuli (e.g., physical, radioactive, infective, pro-allergenic, or toxic), and in some cases may manifest itself in chronic diseases. To limit the potentially deleterious effects of acute or chronic inflammatory responses, complex transcriptional and posttranscriptional regulatory networks have evolved, often involving nonprotein-coding RNAs (ncRNA). MicroRNAs (miRNAs) are a class of posttranscriptional regulators that control mRNA translation and stability. Long ncRNAs (lncRNAs) are a very diverse group of transcripts >200 nt, functioning among others as scaffolds or decoys both in the nucleus and the cytoplasm. By now, it is well established that miRNAs and lncRNAs are implicated in all major cellular processes including control of cell death, proliferation, or metabolism. Extensive research over the last years furthermore revealed a fundamental role of ncRNAs in pathogen recognition and inflammatory responses. This chapter reviews and summarizes the current knowledge on regulatory ncRNA networks in infection and inflammation.

Key words

miRNA lncRNA Infection Inflammation Immunity 

Notes

Acknowledgments

We thank many collaborators for fruitful discussion, especially Annalisa Marsico, Julio Vera Gonzales, Martin Vingron, and Xin Lai. Part of this work has been funded by BMBF (ERACoSysMed2 SysMed-COPD—FKZ 031L0140, JPIAMR Pneumo-AMR-Protect—FKZ 01KI1702, e:Med CAPSYS—FKZ 01X1304E/01ZX1304F), DFG (SFB/TR-84), and LOEWE (LOEWE Medical RNomics—FKZ 519/03/00.001-(0003)) to B.S. and by von Behring-Röntgen-Stiftung (vBR project 63-0036), DFG (SFB/TR-84) and Forschungsförderfonds, Philipps Universität Marburg, to L.N.S. We would like to apologize to all colleagues whose excellent contributions to the field could not be included in this text due to space constraints.

References

  1. 1.
    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.  https://doi.org/10.1016/0092-8674(93)90529-y CrossRefGoogle Scholar
  2. 2.
    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):855–862CrossRefGoogle Scholar
  3. 3.
    Derrien T, Johnson R, Bussotti G, Tanzer A, Djebali S, Tilgner H, Guernec G, Martin D, Merkel A, Knowles DG, Lagarde J, Veeravalli L, Ruan X, Ruan Y, Lassmann T, Carninci P, Brown JB, Lipovich L, Gonzalez JM, Thomas M, Davis CA, Shiekhattar R, Gingeras TR, Hubbard TJ, Notredame C, Harrow J, Guigo R (2012) The GENCODE v7 catalog of human long noncoding RNAs: analysis of their gene structure, evolution, and expression. Genome Res 22(9):1775–1789.  https://doi.org/10.1101/gr.132159.111 CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Moss EG, Lee RC, Ambros V (1997) The cold shock domain protein LIN-28 controls developmental timing in C-elegans and is regulated by the lin-4 RNA. Cell 88(5):637–646.  https://doi.org/10.1016/S0092-8674(00)81906-6 CrossRefPubMedGoogle Scholar
  5. 5.
    Chen CZ, Li L, Lodish HF, Bartel DP (2004) MicroRNAs modulate hematopoietic lineage differentiation. Science 303(5654):83–86.  https://doi.org/10.1126/science.1091903 CrossRefPubMedGoogle Scholar
  6. 6.
    Havelange V, Garzon R (2010) MicroRNAs: emerging key regulators of hematopoiesis. Am J Hematol 85(12):935–942.  https://doi.org/10.1002/ajh.21863 CrossRefPubMedGoogle Scholar
  7. 7.
    Malumbres R, Lossos IS (2010) Expression of miRNAs in lymphocytes: a review. Methods Mol Biol 667:129–143.  https://doi.org/10.1007/978-1-60761-811-9_9 CrossRefPubMedGoogle Scholar
  8. 8.
    Navarro F, Lieberman J (2010) Small RNAs guide hematopoietic cell differentiation and function. J Immunol 184(11):5939–5947.  https://doi.org/10.4049/jimmunol.0902567 CrossRefPubMedGoogle Scholar
  9. 9.
    Sittka A, Schmeck B (2013) MicroRNAs in the lung. Adv Exp Med Biol 774:121–134.  https://doi.org/10.1007/978-94-007-5590-1_7 CrossRefPubMedGoogle Scholar
  10. 10.
    Taganov KD, Boldin MP, Chang KJ, Baltimore D (2006) NF-kappaB-dependent induction of microRNA miR-146, an inhibitor targeted to signaling proteins of innate immune responses. Proc Natl Acad Sci U S A 103(33):12481–12486.  https://doi.org/10.1073/pnas.0605298103 CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Magilnick N, Reyes EY, Wang WL, Vonderfecht SL, Gohda J, Inoue JI, Boldin MP (2017) miR-146a-Traf6 regulatory axis controls autoimmunity and myelopoiesis, but is dispensable for hematopoietic stem cell homeostasis and tumor suppression. Proc Natl Acad Sci U S A 114(34):E7140–E7149.  https://doi.org/10.1073/pnas.1706833114 CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Perry MM, Moschos SA, Williams AE, Shepherd NJ, Larner-Svensson HM, Lindsay MA (2008) Rapid changes in microRNA-146a expression negatively regulate the IL-1beta-induced inflammatory response in human lung alveolar epithelial cells. J Immunol 180(8):5689–5698CrossRefGoogle Scholar
  13. 13.
    Perry MM, Williams AE, Tsitsiou E, Larner-Svensson HM, Lindsay MA (2009) Divergent intracellular pathways regulate interleukin-1beta-induced miR-146a and miR-146b expression and chemokine release in human alveolar epithelial cells. FEBS Lett 583(20):3349–3355.  https://doi.org/10.1016/j.febslet.2009.09.038 CrossRefPubMedGoogle Scholar
  14. 14.
    O’Connell RM, Taganov KD, Boldin MP, Cheng GH, Baltimore D (2007) MicroRNA-155 is induced during the macrophage inflammatory response. Proc Natl Acad Sci U S A 104(5):1604–1609.  https://doi.org/10.1073/pnas.0610731104 CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Mantuano E, Brifault C, Lam MS, Azmoon P, Gilder AS, Gonias SL (2016) LDL receptor-related protein-1 regulates NFkappaB and microRNA-155 in macrophages to control the inflammatory response. Proc Natl Acad Sci U S A 113(5):1369–1374.  https://doi.org/10.1073/pnas.1515480113 CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Tili E, Michaille JJ, Cimino A, Costinean S, Dumitru CD, Adair B, Fabbri M, Alder H, Liu CG, Calin GA, Croce CM (2007) Modulation of miR-155 and miR-125b levels following lipopolysaccharide/TNF-alpha stimulation and their possible roles in regulating the response to endotoxin shock. J Immunol 179(8):5082–5089.  https://doi.org/10.4049/jimmunol.179.8.5082 CrossRefPubMedGoogle Scholar
  17. 17.
    Schulte LN, Westermann AJ, Vogel J (2013) Differential activation and functional specialization of miR-146 and miR-155 in innate immune sensing. Nucleic Acids Res 41(1):542–553.  https://doi.org/10.1093/nar/gks1030 CrossRefPubMedGoogle Scholar
  18. 18.
    Janga H, Aznaourova M, Boldt F, Damm K, Grunweller A, Schulte LN (2018) Cas9-mediated excision of proximal DNaseI/H3K4me3 signatures confers robust silencing of microRNA and long non-coding RNA genes. PLoS One 13(2):e0193066.  https://doi.org/10.1371/journal.pone.0193066 CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Moschos SA, Williams AE, Perry MM, Birrell MA, Belvisi MG, Lindsay MA (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 Genomics 8:240.  https://doi.org/10.1186/1471-2164-8-240 CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Neudecker V, Brodsky KS, Clambey ET, Schmidt EP, Packard TA, Davenport B, Standiford TJ, Weng T, Fletcher AA, Barthel L, Masterson JC, Furuta GT, Cai C, Blackburn MR, Ginde AA, Graner MW, Janssen WJ, Zemans RL, Evans CM, Burnham EL, Homann D, Moss M, Kreth S, Zacharowski K, Henson PM, Eltzschig HK (2017) Neutrophil transfer of miR-223 to lung epithelial cells dampens acute lung injury in mice. Sci Transl Med 9(408).  https://doi.org/10.1126/scitranslmed.aah5360 CrossRefGoogle Scholar
  21. 21.
    Kim JH, Suk MH, Yoon DW, Kim HY, Jung KH, Kang EH, Lee SY, Lee SY, Suh IB, Shin C, Shim JJ, In KH, Yoo SH, Kang KH (2008) Inflammatory and transcriptional roles of poly (ADP-ribose) polymerase in ventilator-induced lung injury. Crit Care 12(4):R108.  https://doi.org/10.1186/cc6995 CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Kramer NJ, Wang WL, Reyes EY, Kumar B, Chen CC, Ramakrishna C, Cantin EM, Vonderfecht SL, Taganov KD, Chau N, Boldin MP (2015) Altered lymphopoiesis and immunodeficiency in miR-142 null mice. Blood 125(24):3720–3730.  https://doi.org/10.1182/blood-2014-10-603951 CrossRefPubMedGoogle Scholar
  23. 23.
    Boldin MP, Taganov KD, Rao DS, Yang L, Zhao JL, Kalwani M, Garcia-Flores Y, Luong M, Devrekanli A, Xu J, Sun G, Tay J, Linsley PS, Baltimore D (2011) miR-146a is a significant brake on autoimmunity, myeloproliferation, and cancer in mice. J Exp Med 208(6):1189–1201.  https://doi.org/10.1084/jem.20101823 CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Teng G, Hakimpour P, Landgraf P, Rice A, Tuschl T, Casellas R, Papavasiliou FN (2008) MicroRNA-155 is a negative regulator of activation-induced cytidine deaminase. Immunity 28(5):621–629.  https://doi.org/10.1016/j.immuni.2008.03.015 CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Yang L, Boldin MP, Yu Y, Liu CS, Ea CK, Ramakrishnan P, Taganov KD, Zhao JL, Baltimore D (2012) miR-146a controls the resolution of T cell responses in mice. J Exp Med 209(9):1655–1670.  https://doi.org/10.1084/jem.20112218 CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Rodriguez A, Vigorito E, Clare S, Warren MV, Couttet P, Soond DR, van Dongen S, Grocock RJ, Das PP, Miska EA, Vetrie D, Okkenhaug K, Enright AJ, Dougan G, Turner M, Bradley A (2007) Requirement of bic/microRNA-155 for normal immune function. Science 316(5824):608–611.  https://doi.org/10.1126/science.1139253 CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Huffaker TB, Hu RZ, Runtsch MC, Bake E, Chen XJ, Zhao J, Round JL, Baltimore D, O’Connell RM (2012) Epistasis between microRNAs 155 and 146a during T cell-mediated antitumor immunity. Cell Rep 2(6):1697–1709.  https://doi.org/10.1016/j.celrep.2012.10.025 CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Mehta A, Baltimore D (2016) MicroRNAs as regulatory elements in immune system logic. Nat Rev Immunol 16(5):279–294.  https://doi.org/10.1038/nri.2016.40 CrossRefPubMedGoogle Scholar
  29. 29.
    McDonough JE, Yuan R, Suzuki M, Seyednejad N, Elliott WM, Sanchez PG, Wright AC, Gefter WB, Litzky L, Coxson HO, Pare PD, Sin DD, Pierce RA, Woods JC, McWilliams AM, Mayo JR, Lam SC, Cooper JD, Hogg JC (2011) Small-airway obstruction and emphysema in chronic obstructive pulmonary disease. N Engl J Med 365(17):1567–1575.  https://doi.org/10.1056/NEJMoa1106955 CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Sethi S, Murphy TF (2008) Infection in the pathogenesis and course of chronic obstructive pulmonary disease. N Engl J Med 359(22):2355–2365.  https://doi.org/10.1056/NEJMra0800353 CrossRefPubMedGoogle Scholar
  31. 31.
    Izzotti A, Calin GA, Arrigo P, Steele VE, Croce CM, De Flora S (2009) Downregulation of microRNA expression in the lungs of rats exposed to cigarette smoke. FASEB J 23(3):806–812.  https://doi.org/10.1096/fj.08-121384 CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Izzotti A, Calin GA, Steele VE, Croce CM, De Flora S (2009) Relationships of microRNA expression in mouse lung with age and exposure to cigarette smoke and light. FASEB J 23(9):3243–3250.  https://doi.org/10.1096/fj.09-135251 CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Schembri F, Sridhar S, Perdomo C, Gustafson AM, Zhang XL, Ergun A, Lu JN, Liu G, Zhang XH, Bowers J, Vaziri C, Ott K, Sensinger K, Collins JJ, Brody JS, Getts R, Lenburg ME, Spira A (2009) MicroRNAs as modulators of smoking-induced gene expression changes in human airway epithelium. Proc Natl Acad Sci U S A 106(7):2319–2324.  https://doi.org/10.1073/pnas.0806383106 CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Conickx G, Mestdagh P, Avila Cobos F, Verhamme FM, Maes T, Vanaudenaerde BM, Seys LJ, Lahousse L, Kim RY, Hsu AC, Wark PA, Hansbro PM, Joos GF, Vandesompele J, Bracke KR, Brusselle GG (2017) MicroRNA profiling reveals a role for microRNA-218-5p in the pathogenesis of chronic obstructive pulmonary disease. Am J Respir Crit Care Med 195(1):43–56.  https://doi.org/10.1164/rccm.201506-1182OC CrossRefPubMedGoogle Scholar
  35. 35.
    Davidson MR, Larsen JE, Yang IA, Hayward NK, Clarke BE, Duhig EE, Passmore LH, Bowman RV, Fong KM (2010) MicroRNA-218 is deleted and downregulated in lung squamous cell carcinoma. PLoS One 5(9):e12560.  https://doi.org/10.1371/journal.pone.0012560 CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Sato T, Liu X, Nelson A, Nakanishi M, Kanaji N, Wang X, Kim M, Li Y, Sun J, Michalski J, Patil A, Basma H, Holz O, Magnussen H, Rennard SI (2010) Reduced miR-146a increases prostaglandin E(2)in chronic obstructive pulmonary disease fibroblasts. Am J Respir Crit Care Med 182(8):1020–1029.  https://doi.org/10.1164/rccm.201001-0055OC CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Togo S, Holz O, Liu X, Sugiura H, Kamio K, Wang X, Kawasaki S, Ahn Y, Fredriksson K, Skold CM, Mueller KC, Branscheid D, Welker L, Watz H, Magnussen H, Rennard SI (2008) Lung fibroblast repair functions in patients with chronic obstructive pulmonary disease are altered by multiple mechanisms. Am J Respir Crit Care Med 178(3):248–260.  https://doi.org/10.1164/rccm.200706-929OC CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Osei ET, Florez-Sampedro L, Tasena H, Faiz A, Noordhoek JA, Timens W, Postma DS, Hackett TL, Heijink IH, Brandsma CA (2017) miR-146a-5p plays an essential role in the aberrant epithelial-fibroblast cross-talk in COPD. Eur Respir J 49(5).  https://doi.org/10.1183/13993003.02538-2016 CrossRefGoogle Scholar
  39. 39.
    Van Pottelberge GR, Mestdagh P, Bracke KR, Thas O, van Durme YM, Joos GF, Vandesompele J, Brusselle GG (2011) MicroRNA expression in induced sputum of smokers and patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 183(7):898–906.  https://doi.org/10.1164/rccm.201002-0304OC CrossRefPubMedGoogle Scholar
  40. 40.
    Naz S, Kolmert J, Yang M, Reinke SN, Kamleh MA, Snowden S, Heyder T, Levanen B, Erle DJ, Skold CM, Wheelock AM, Wheelock CE (2017) Metabolomics analysis identifies sex-associated metabotypes of oxidative stress and the autotaxin-lysoPA axis in COPD. Eur Respir J 49(6).  https://doi.org/10.1183/13993003.02322-2016 CrossRefGoogle Scholar
  41. 41.
    Lee JY, Donaldson AV, Lewis A, Natanek SA, Polkey MI, Kemp PR (2017) Circulating miRNAs from imprinted genomic regions are associated with peripheral muscle strength in COPD patients. Eur Respir J 49(4).  https://doi.org/10.1183/13993003.01881-2016 CrossRefGoogle Scholar
  42. 42.
    Garros RF, Paul R, Connolly M, Lewis A, Garfield BE, Natanek SA, Bloch S, Mouly V, Griffiths MJ, Polkey MI, Kemp PR (2017) MicroRNA-542 promotes mitochondrial dysfunction and SMAD activity and is elevated in intensive care unit-acquired weakness. Am J Respir Crit Care Med 196(11):1422–1433.  https://doi.org/10.1164/rccm.201701-0101OC CrossRefPubMedPubMedCentralGoogle Scholar
  43. 43.
    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 106(44):18704–18709.  https://doi.org/10.1073/pnas.0905063106 CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    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–U251.  https://doi.org/10.1016/j.jaci.2011.04.005 CrossRefPubMedGoogle Scholar
  45. 45.
    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.  https://doi.org/10.4049/jimmunol.0803560 CrossRefPubMedPubMedCentralGoogle Scholar
  46. 46.
    Panganiban RP, Wang Y, Howrylak J, Chinchilli VM, Craig TJ, August A, Ishmael FT (2016) Circulating microRNAs as biomarkers in patients with allergic rhinitis and asthma. J Allergy Clin Immunol 137(5):1423–1432.  https://doi.org/10.1016/j.jaci.2016.01.029 CrossRefPubMedGoogle Scholar
  47. 47.
    Rider CF, Yamamoto M, Gunther OP, Hirota JA, Singh A, Tebbutt SJ, Carlsten C (2016) Controlled diesel exhaust and allergen coexposure modulates microRNA and gene expression in humans: effects on inflammatory lung markers. J Allergy Clin Immunol 138(6):1690–1700.  https://doi.org/10.1016/j.jaci.2016.02.038 CrossRefPubMedGoogle Scholar
  48. 48.
    Williams AE, Larner-Svensson H, Perry MM, Campbell GA, Herrick SE, Adcock IM, Erjefalt JS, Chung KF, Lindsay MA (2009) MicroRNA expression profiling in mild asthmatic human airways and effect of corticosteroid therapy. PLoS One 4(6):e5889.  https://doi.org/10.1371/journal.pone.0005889 CrossRefPubMedPubMedCentralGoogle Scholar
  49. 49.
    Kim RY, Horvat JC, Pinkerton JW, Starkey MR, Essilfie AT, Mayall JR, Nair PM, Hansbro NG, Jones B, Haw TJ, Sunkara KP, Nguyen TH, Jarnicki AG, Keely S, Mattes J, Adcock IM, Foster PS, Hansbro PM (2017) MicroRNA-21 drives severe, steroid-insensitive experimental asthma by amplifying phosphoinositide 3-kinase-mediated suppression of histone deacetylase 2. J Allergy Clin Immunol 139(2):519–532.  https://doi.org/10.1016/j.jaci.2016.04.038 CrossRefPubMedGoogle Scholar
  50. 50.
    Hew M, Bhavsar P, Torrego A, Meah S, Khorasani N, Barnes PJ, Adcock I, Chung KF (2006) Relative corticosteroid insensitivity of peripheral blood mononuclear cells in severe asthma. Am J Respir Crit Care Med 174(2):134–141.  https://doi.org/10.1164/rccm.200512-1930OC CrossRefPubMedPubMedCentralGoogle Scholar
  51. 51.
    Rupani H, Martinez-Nunez RT, Dennison P, Lau LC, Jayasekera N, Havelock T, Francisco-Garcia AS, Grainge C, Howarth PH, Sanchez-Elsner T (2016) Toll-like receptor 7 is reduced in severe asthma and linked to an altered microRNA profile. Am J Respir Crit Care Med 194(1):26–37.  https://doi.org/10.1164/rccm.201502-0280OC CrossRefPubMedPubMedCentralGoogle Scholar
  52. 52.
    Sykes A, Edwards MR, Macintyre J, del Rosario A, Bakhsoliani E, Trujillo-Torralbo MB, Kon OM, Mallia P, McHale M, Johnston SL (2012) Rhinovirus 16-induced IFN-alpha and IFN-beta are deficient in bronchoalveolar lavage cells in asthmatic patients. J Allergy Clin Immunol 129(6):1506–1514.e6.  https://doi.org/10.1016/j.jaci.2012.03.044 CrossRefPubMedGoogle Scholar
  53. 53.
    Roponen M, Yerkovich ST, Hollams E, Sly PD, Holt PG, Upham JW (2010) Toll-like receptor 7 function is reduced in adolescents with asthma. Eur Respir J 35(1):64–71.  https://doi.org/10.1183/09031936.00172008 CrossRefPubMedGoogle Scholar
  54. 54.
    Zhou Y, Do DC, Ishmael FT, Squadrito ML, Tang HM, Tang HL, Hsu MH, Qiu L, Li C, Zhang Y, Becker KG, Wan M, Huang SK, Gao P (2018) Mannose receptor modulates macrophage polarization and allergic inflammation through miR-511-3p. J Allergy Clin Immunol 141(1):350–364.e8.  https://doi.org/10.1016/j.jaci.2017.04.049 CrossRefPubMedGoogle Scholar
  55. 55.
    Tsai YM, Hsu SC, Zhang J, Zhou YF, Plunkett B, Huang SK, Gao PS (2013) Functional interaction of cockroach allergens and mannose receptor (CD206) in human circulating fibrocytes. PLoS One 8(5):e64105.  https://doi.org/10.1371/journal.pone.0064105 CrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    Squadrito ML, Pucci F, Magri L, Moi D, Gilfillan GD, Ranghetti A, Casazza A, Mazzone M, Lyle R, Naldini L, De Palma M (2012) miR-511-3p modulates genetic programs of tumor-associated macrophages. Cell Rep 1(2):141–154.  https://doi.org/10.1016/j.celrep.2011.12.005 CrossRefPubMedGoogle Scholar
  57. 57.
    Johansson K, Malmhall C, Ramos-Ramirez P, Radinger M (2017) MicroRNA-155 is a critical regulator of type 2 innate lymphoid cells and IL-33 signaling in experimental models of allergic airway inflammation. J Allergy Clin Immunol 139(3):1007–1016.e9.  https://doi.org/10.1016/j.jaci.2016.06.035 CrossRefPubMedGoogle Scholar
  58. 58.
    Malmhall C, Alawieh S, Lu Y, Sjostrand M, Bossios A, Eldh M, Radinger M (2014) MicroRNA-155 is essential for T(H)2-mediated allergen-induced eosinophilic inflammation in the lung. J Allergy Clin Immunol 133(5):1429–1438., 1438.e1–7.  https://doi.org/10.1016/j.jaci.2013.11.008 CrossRefPubMedGoogle Scholar
  59. 59.
    Bartemes KR, Iijima K, Kobayashi T, Kephart GM, McKenzie AN, Kita H (2012) IL-33-responsive lineage- CD25+ CD44(hi) lymphoid cells mediate innate type 2 immunity and allergic inflammation in the lungs. J Immunol 188(3):1503–1513.  https://doi.org/10.4049/jimmunol.1102832 CrossRefPubMedGoogle Scholar
  60. 60.
    Yamazumi Y, Sasaki O, Imamura M, Oda T, Ohno Y, Shiozaki-Sato Y, Nagai S, Suyama S, Kamoshida Y, Funato K, Yasui T, Kikutani H, Yamamoto K, Dohi M, Koyasu S, Akiyama T (2016) The RNA binding protein Mex-3B is required for IL-33 induction in the development of allergic airway inflammation. Cell Rep 16(9):2456–2471.  https://doi.org/10.1016/j.celrep.2016.07.062 CrossRefPubMedGoogle Scholar
  61. 61.
    Buchet-Poyau K, Courchet J, Le Hir H, Seraphin B, Scoazec JY, Duret L, Domon-Dell C, Freund JN, Billaud M (2007) Identification and characterization of human Mex-3 proteins, a novel family of evolutionarily conserved RNA-binding proteins differentially localized to processing bodies. Nucleic Acids Res 35(4):1289–1300.  https://doi.org/10.1093/nar/gkm016 CrossRefPubMedPubMedCentralGoogle Scholar
  62. 62.
    Polikepahad S, Knight JM, Naghavi AO, Oplt T, Creighton CJ, Shaw C, Benham AL, Kim J, Soibam B, Harris RA, Coarfa C, Zariff A, Milosavljevic A, Batts LM, Kheradmand F, Gunaratne PH, Corry DB (2010) Proinflammatory role for let-7 microRNAS in experimental asthma. J Biol Chem 285(39):30139–30149.  https://doi.org/10.1074/jbc.M110.145698 CrossRefPubMedPubMedCentralGoogle Scholar
  63. 63.
    Kumar M, Ahmad T, Sharma A, Mabalirajan U, Kulshreshtha A, Agrawal A, Ghosh B (2011) Let-7 microRNA-mediated regulation of IL-13 and allergic airway inflammation. J Allergy Clin Immunol 128(5):1077–1085.e1–10.  https://doi.org/10.1016/j.jaci.2011.04.034 CrossRefPubMedGoogle Scholar
  64. 64.
    Garbacki N, Di Valentin E, Huynh-Thu VA, Geurts P, Irrthum A, Crahay C, Arnould T, Deroanne C, Piette J, Cataldo D, Colige A (2011) MicroRNAs profiling in murine models of acute and chronic asthma: a relationship with mRNAs targets. PLoS One 6(1):e16509.  https://doi.org/10.1371/journal.pone.0016509 CrossRefPubMedPubMedCentralGoogle Scholar
  65. 65.
    Sun Q, Liu L, Mandal J, Molino A, Stolz D, Tamm M, Lu S, Roth M (2016) PDGF-BB induces PRMT1 expression through ERK1/2 dependent STAT1 activation and regulates remodeling in primary human lung fibroblasts. Cell Signal 28(4):307–315.  https://doi.org/10.1016/j.cellsig.2016.01.004 CrossRefPubMedGoogle Scholar
  66. 66.
    Sun Q, Liu L, Roth M, Tian J, He Q, Zhong B, Bao R, Lan X, Jiang C, Sun J, Yang X, Lu S (2015) PRMT1 upregulated by epithelial proinflammatory cytokines participates in COX2 expression in fibroblasts and chronic antigen-induced pulmonary inflammation. J Immunol 195(1):298–306.  https://doi.org/10.4049/jimmunol.1402465 CrossRefPubMedGoogle Scholar
  67. 67.
    Oglesby IK, Bray IM, Chotirmall SH, Stallings RL, O'Neill SJ, McElvaney NG, Greene CM (2010) miR-126 is downregulated in cystic fibrosis airway epithelial cells and regulates TOM1 expression. J Immunol 184(4):1702–1709.  https://doi.org/10.4049/jimmunol.0902669 CrossRefPubMedGoogle Scholar
  68. 68.
    Yamakami M, Yoshimori T, Yokosawa H (2003) Tom1, a VHS domain-containing protein, interacts with tollip, ubiquitin, and clathrin. J Biol Chem 278(52):52865–52872.  https://doi.org/10.1074/jbc.M306740200 CrossRefPubMedGoogle Scholar
  69. 69.
    Burns K, Clatworthy J, Martin L, Martinon F, Plumpton C, Maschera B, Lewis A, Ray K, Tschopp J, Volpe F (2000) Tollip, a new component of the IL-1RI pathway, links IRAK to the IL-1 receptor. Nat Cell Biol 2(6):346–351.  https://doi.org/10.1038/35014038 CrossRefPubMedGoogle Scholar
  70. 70.
    Yamakami M, Yokosawa H (2004) Tom1 (target of Myb1) is a novel negative regulator of interleukin-1-and tumor necrosis factor-induced signaling pathways. Biol Pharm Bull 27(4):564–566.  https://doi.org/10.1248/bpb.27.564 CrossRefPubMedGoogle Scholar
  71. 71.
    Dean TP, Dai Y, Shute JK, Church MK, Warner JO (1993) Interleukin-8 concentrations are elevated in bronchoalveolar lavage, sputum, and sera of children with cystic fibrosis. Pediatr Res 34(2):159–161.  https://doi.org/10.1203/00006450-199308000-00010 CrossRefPubMedGoogle Scholar
  72. 72.
    Richman-Eisenstat JB, Jorens PG, Hebert CA, Ueki I, Nadel JA (1993) Interleukin-8: an important chemoattractant in sputum of patients with chronic inflammatory airway diseases. Am J Phys 264(4 Pt 1):L413–L418.  https://doi.org/10.1152/ajplung.1993.264.4.L413 CrossRefGoogle Scholar
  73. 73.
    Bonfield TL, Panuska JR, Konstan MW, Hilliard KA, Hilliard JB, Ghnaim H, Berger M (1995) Inflammatory cytokines in cystic fibrosis lungs. Am J Respir Crit Care Med 152(6 Pt 1):2111–2118.  https://doi.org/10.1164/ajrccm.152.6.8520783 CrossRefPubMedGoogle Scholar
  74. 74.
    Bhattacharyya S, Balakathiresan NS, Dalgard C, Gutti U, Armistead D, Jozwik C, Srivastava M, Pollard HB, Biswas R (2011) Elevated miR-155 promotes inflammation in cystic fibrosis by driving hyperexpression of interleukin-8. J Biol Chem 286(13):11604–11615.  https://doi.org/10.1074/jbc.M110.198390 CrossRefPubMedPubMedCentralGoogle Scholar
  75. 75.
    Gillen AE, Gosalia N, Leir SH, Harris A (2011) MicroRNA regulation of expression of the cystic fibrosis transmembrane conductance regulator gene. Biochem J 438(1):25–32.  https://doi.org/10.1042/BJ20110672 CrossRefPubMedPubMedCentralGoogle Scholar
  76. 76.
    Megiorni F, Cialfi S, Dominici C, Quattrucci S, Pizzuti A (2011) Synergistic post-transcriptional regulation of the cystic fibrosis transmembrane conductance regulator (CFTR) by miR-101 and miR-494 specific binding. PLoS One 6(10):e26601.  https://doi.org/10.1371/journal.pone.0026601 CrossRefPubMedPubMedCentralGoogle Scholar
  77. 77.
    Sonneville F, Ruffin M, Coraux C, Rousselet N, Le Rouzic P, Blouquit-Laye S, Corvol H, Tabary O (2017) MicroRNA-9 downregulates the ANO1 chloride channel and contributes to cystic fibrosis lung pathology. Nat Commun 8(1):710.  https://doi.org/10.1038/s41467-017-00813-z CrossRefPubMedPubMedCentralGoogle Scholar
  78. 78.
    Ruffin M, Voland M, Marie S, Bonora M, Blanchard E, Blouquit-Laye S, Naline E, Puyo P, Le Rouzic P, Guillot L, Corvol H, Clement A, Tabary O (2013) Anoctamin 1 dysregulation alters bronchial epithelial repair in cystic fibrosis. Biochim Biophys Acta 1832(12):2340–2351.  https://doi.org/10.1016/j.bbadis.2013.09.012 CrossRefPubMedGoogle Scholar
  79. 79.
    Schulte LN, Eulalio A, Mollenkopf HJ, Reinhardt R, Vogel J (2011) Analysis of the host microRNA response to Salmonella uncovers the control of major cytokines by the let-7 family. EMBO J 30(10):1977–1989.  https://doi.org/10.1038/emboj.2011.94 CrossRefPubMedPubMedCentralGoogle Scholar
  80. 80.
    Griss K, Bertrams W, Sittka-Stark A, Seidel K, Stielow C, Hippenstiel S, Suttorp N, Eberhardt M, Wilhelm J, Vera J, Schmeck B (2016) MicroRNAs constitute a negative feedback loop in Streptococcus pneumoniae-induced macrophage activation. J Infect Dis 214(2):288–299.  https://doi.org/10.1093/infdis/jiw109 CrossRefPubMedGoogle Scholar
  81. 81.
    Jung AL, Stoiber C, Herkt CE, Schulz C, Bertrams W, Schmeck B (2016) Legionella pneumophila-derived outer membrane vesicles promote bacterial replication in macrophages. PLoS Pathog 12(4):e1005592.  https://doi.org/10.1371/journal.ppat.1005592 CrossRefPubMedPubMedCentralGoogle Scholar
  82. 82.
    Maudet C, Mano M, Sunkavalli U, Sharan M, Giacca M, Forstner KU, Eulalio A (2014) Functional high-throughput screening identifies the miR-15 microRNA family as cellular restriction factors for Salmonella infection. Nat Commun 5:4718.  https://doi.org/10.1038/ncomms5718 CrossRefPubMedGoogle Scholar
  83. 83.
    Sahu SK, Kumar M, Chakraborty S, Banerjee SK, Kumar R, Gupta P, Jana K, Gupta UD, Ghosh Z, Kundu M, Basu J (2017) MicroRNA 26a (miR-26a)/KLF4 and CREB-C/EBPbeta regulate innate immune signaling, the polarization of macrophages and the trafficking of Mycobacterium tuberculosis to lysosomes during infection. PLoS Pathog 13(5):e1006410.  https://doi.org/10.1371/journal.ppat.1006410 CrossRefPubMedPubMedCentralGoogle Scholar
  84. 84.
    Kapoor R, Arora S, Ponia SS, Kumar B, Maddika S, Banerjea AC (2015) The miRNA miR-34a enhances HIV-1 replication by targeting PNUTS/PPP1R10, which negatively regulates HIV-1 transcriptional complex formation. Biochem J 470(3):293–302.  https://doi.org/10.1042/BJ20150700 CrossRefPubMedGoogle Scholar
  85. 85.
    Jopling CL, Yi M, Lancaster AM, Lemon SM, Sarnow P (2005) Modulation of hepatitis C virus RNA abundance by a liver-specific MicroRNA. Science 309(5740):1577–1581.  https://doi.org/10.1126/science.1113329 CrossRefPubMedGoogle Scholar
  86. 86.
    Lu J, Wu X, Hong M, Tobias P, Han J (2013) A potential suppressive effect of natural antisense IL-1beta RNA on lipopolysaccharide-induced IL-1beta expression. J Immunol 190(12):6570–6578.  https://doi.org/10.4049/jimmunol.1102487 CrossRefPubMedPubMedCentralGoogle Scholar
  87. 87.
    Ilott NE, Heward JA, Roux B, Tsitsiou E, Fenwick PS, Lenzi L, Goodhead I, Hertz-Fowler C, Heger A, Hall N, Donnelly LE, Sims D, Lindsay MA (2014) Long non-coding RNAs and enhancer RNAs regulate the lipopolysaccharide-induced inflammatory response in human monocytes. Nat Commun 5:3979.  https://doi.org/10.1038/ncomms4979 CrossRefGoogle Scholar
  88. 88.
    Krawczyk M, Emerson BM (2014) p50-associated COX-2 extragenic RNA (PACER) activates COX-2 gene expression by occluding repressive NF-kappaB complexes. eLife 3:e01776.  https://doi.org/10.7554/eLife.01776 CrossRefPubMedPubMedCentralGoogle Scholar
  89. 89.
    Carpenter S, Aiello D, Atianand MK, Ricci EP, Gandhi P, Hall LL, Byron M, Monks B, Henry-Bezy M, Lawrence JB, O’Neill LA, Moore MJ, Caffrey DR, Fitzgerald KA (2013) A long noncoding RNA mediates both activation and repression of immune response genes. Science 341(6147):789–792.  https://doi.org/10.1126/science.1240925 CrossRefPubMedPubMedCentralGoogle Scholar
  90. 90.
    Tong Q, Gong AY, Zhang XT, Lin C, Ma S, Chen J, Hu G, Chen XM (2016) LincRNA-Cox2 modulates TNF-alpha-induced transcription of Il12b gene in intestinal epithelial cells through regulation of Mi-2/NuRD-mediated epigenetic histone modifications. FASEB J 30(3):1187–1197.  https://doi.org/10.1096/fj.15-279166 CrossRefPubMedGoogle Scholar
  91. 91.
    Hu G, Gong AY, Wang Y, Ma S, Chen X, Chen J, Su CJ, Shibata A, Strauss-Soukup JK, Drescher KM, Chen XM (2016) LincRNA-Cox2 promotes late inflammatory gene transcription in macrophages through modulating SWI/SNF-mediated chromatin remodeling. J Immunol 196(6):2799–2808.  https://doi.org/10.4049/jimmunol.1502146 CrossRefPubMedPubMedCentralGoogle Scholar
  92. 92.
    Lu Y, Liu X, Xie M, Liu M, Ye M, Li M, Chen XM, Li X, Zhou R (2017) The NF-kappaB-responsive long noncoding RNA FIRRE regulates posttranscriptional regulation of inflammatory gene expression through interacting with hnRNPU. J Immunol 199(10):3571–3582.  https://doi.org/10.4049/jimmunol.1700091 CrossRefPubMedPubMedCentralGoogle Scholar
  93. 93.
    Rapicavoli NA, Qu K, Zhang J, Mikhail M, Laberge RM, Chang HY (2013) A mammalian pseudogene lncRNA at the interface of inflammation and anti-inflammatory therapeutics. elife 2:e00762.  https://doi.org/10.7554/eLife.00762 CrossRefPubMedPubMedCentralGoogle Scholar
  94. 94.
    Li Z, Chao TC, Chang KY, Lin N, Patil VS, Shimizu C, Head SR, Burns JC, Rana TM (2014) The long noncoding RNA THRIL regulates TNFalpha expression through its interaction with hnRNPL. Proc Natl Acad Sci U S A 111(3):1002–1007.  https://doi.org/10.1073/pnas.1313768111 CrossRefPubMedGoogle Scholar
  95. 95.
    Atianand MK, Hu W, Satpathy AT, Shen Y, Ricci EP, Alvarez-Dominguez JR, Bhatta A, Schattgen SA, McGowan JD, Blin J, Braun JE, Gandhi P, Moore MJ, Chang HY, Lodish HF, Caffrey DR, Fitzgerald KA (2016) A long noncoding RNA lincRNA-EPS acts as a transcriptional brake to restrain inflammation. Cell 165(7):1672–1685.  https://doi.org/10.1016/j.cell.2016.05.075 CrossRefPubMedPubMedCentralGoogle Scholar
  96. 96.
    Castellanos-Rubio A, Fernandez-Jimenez N, Kratchmarov R, Luo X, Bhagat G, Green PH, Schneider R, Kiledjian M, Bilbao JR, Ghosh S (2016) A long noncoding RNA associated with susceptibility to celiac disease. Science 352(6281):91–95.  https://doi.org/10.1126/science.aad0467 CrossRefPubMedPubMedCentralGoogle Scholar
  97. 97.
    Hu G, Tang Q, Sharma S, Yu F, Escobar TM, Muljo SA, Zhu J, Zhao K (2013) Expression and regulation of intergenic long noncoding RNAs during T cell development and differentiation. Nat Immunol 14(11):1190–1198.  https://doi.org/10.1038/ni.2712 CrossRefPubMedPubMedCentralGoogle Scholar
  98. 98.
    Spurlock CF 3rd, Tossberg JT, Guo Y, Collier SP, Crooke PS 3rd, Aune TM (2015) Expression and functions of long noncoding RNAs during human T helper cell differentiation. Nat Commun 6:6932.  https://doi.org/10.1038/ncomms7932 CrossRefPubMedPubMedCentralGoogle Scholar
  99. 99.
    Ranzani V, Rossetti G, Panzeri I, Arrigoni A, Bonnal RJ, Curti S, Gruarin P, Provasi E, Sugliano E, Marconi M, De Francesco R, Geginat J, Bodega B, Abrignani S, Pagani M (2015) The long intergenic noncoding RNA landscape of human lymphocytes highlights the regulation of T cell differentiation by linc-MAF-4. Nat Immunol 16(3):318–325.  https://doi.org/10.1038/ni.3093 CrossRefPubMedPubMedCentralGoogle Scholar
  100. 100.
    Huang W, Thomas B, Flynn RA, Gavzy SJ, Wu L, Kim SV, Hall JA, Miraldi ER, Ng CP, Rigo F, Meadows S, Montoya NR, Herrera NG, Domingos AI, Rastinejad F, Myers RM, Fuller-Pace FV, Bonneau R, Chang HY, Acuto O, Littman DR (2015) DDX5 and its associated lncRNA Rmrp modulate TH17 cell effector functions. Nature 528(7583):517–522.  https://doi.org/10.1038/nature16193 CrossRefPubMedPubMedCentralGoogle Scholar
  101. 101.
    Zemmour D, Pratama A, Loughhead SM, Mathis D, Benoist C (2017) Flicr, a long noncoding RNA, modulates Foxp3 expression and autoimmunity. Proc Natl Acad Sci U S A 114(17):E3472–E3480.  https://doi.org/10.1073/pnas.1700946114 CrossRefPubMedPubMedCentralGoogle Scholar
  102. 102.
    Yan MD, Hong CC, Lai GM, Cheng AL, Lin YW, Chuang SE (2005) Identification and characterization of a novel gene Saf transcribed from the opposite strand of Fas. Hum Mol Genet 14(11):1465–1474.  https://doi.org/10.1093/hmg/ddi156 CrossRefPubMedGoogle Scholar
  103. 103.
    Sehgal L, Mathur R, Braun FK, Wise JF, Berkova Z, Neelapu S, Kwak LW, Samaniego F (2014) FAS-antisense 1 lncRNA and production of soluble versus membrane Fas in B-cell lymphoma. Leukemia 28(12):2376–2387.  https://doi.org/10.1038/leu.2014.126 CrossRefPubMedPubMedCentralGoogle Scholar
  104. 104.
    Gomez JA, Wapinski OL, Yang YW, Bureau JF, Gopinath S, Monack DM, Chang HY, Brahic M, Kirkegaard K (2013) The NeST long ncRNA controls microbial susceptibility and epigenetic activation of the interferon-gamma locus. Cell 152(4):743–754.  https://doi.org/10.1016/j.cell.2013.01.015 CrossRefPubMedPubMedCentralGoogle Scholar
  105. 105.
    Pawar K, Hanisch C, Palma Vera SE, Einspanier R, Sharbati S (2016) Down regulated lncRNA MEG3 eliminates mycobacteria in macrophages via autophagy. Sci Rep 6:19416.  https://doi.org/10.1038/srep19416 CrossRefPubMedPubMedCentralGoogle Scholar
  106. 106.
    Zhang Q, Chen CY, Yedavalli VS, Jeang KT (2013) NEAT1 long noncoding RNA and paraspeckle bodies modulate HIV-1 posttranscriptional expression. MBio 4(1):e00596–e00512.  https://doi.org/10.1128/mBio.00596-12 CrossRefPubMedPubMedCentralGoogle Scholar
  107. 107.
    Ouyang J, Zhu X, Chen Y, Wei H, Chen Q, Chi X, Qi B, Zhang L, Zhao Y, Gao GF, Wang G, Chen JL (2014) NRAV, a long noncoding RNA, modulates antiviral responses through suppression of interferon-stimulated gene transcription. Cell Host Microbe 16(5):616–626.  https://doi.org/10.1016/j.chom.2014.10.001 CrossRefPubMedGoogle Scholar
  108. 108.
    Nishitsuji H, Ujino S, Yoshio S, Sugiyama M, Mizokami M, Kanto T, Shimotohno K (2016) Long noncoding RNA #32 contributes to antiviral responses by controlling interferon-stimulated gene expression. Proc Natl Acad Sci U S A 113(37):10388–10393.  https://doi.org/10.1073/pnas.1525022113 CrossRefPubMedPubMedCentralGoogle Scholar
  109. 109.
    Wang Y, Zhong H, Xie X, Chen CY, Huang D, Shen L, Zhang H, Chen ZW, Zeng G (2015) Long noncoding RNA derived from CD244 signaling epigenetically controls CD8+ T-cell immune responses in tuberculosis infection. Proc Natl Acad Sci U S A 112(29):E3883–E3892.  https://doi.org/10.1073/pnas.1501662112 CrossRefPubMedPubMedCentralGoogle Scholar
  110. 110.
    Imam H, Bano AS, Patel P, Holla P, Jameel S (2015) The lncRNA NRON modulates HIV-1 replication in a NFAT-dependent manner and is differentially regulated by early and late viral proteins. Sci Rep 5:8639.  https://doi.org/10.1038/srep08639 CrossRefPubMedPubMedCentralGoogle Scholar
  111. 111.
    Li J, Chen C, Ma X, Geng G, Liu B, Zhang Y, Zhang S, Zhong F, Liu C, Yin Y, Cai W, Zhang H (2016) Long noncoding RNA NRON contributes to HIV-1 latency by specifically inducing tat protein degradation. Nat Commun 7:11730.  https://doi.org/10.1038/ncomms11730 CrossRefPubMedPubMedCentralGoogle Scholar
  112. 112.
    Carnero E, Barriocanal M, Prior C, Pablo Unfried J, Segura V, Guruceaga E, Enguita M, Smerdou C, Gastaminza P, Fortes P (2016) Long noncoding RNA EGOT negatively affects the antiviral response and favors HCV replication. EMBO Rep 17(7):1013–1028.  https://doi.org/10.15252/embr.201541763 CrossRefPubMedPubMedCentralGoogle Scholar
  113. 113.
    Wang P, Xu J, Wang Y, Cao X (2017) An interferon-independent lncRNA promotes viral replication by modulating cellular metabolism. Science 358(6366):1051–1055.  https://doi.org/10.1126/science.aao0409 CrossRefPubMedGoogle Scholar
  114. 114.
    Campbell M, Kim KY, Chang PC, Huerta S, Shevchenko B, Wang DH, Izumiya C, Kung HJ, Izumiya Y (2014) A lytic viral long noncoding RNA modulates the function of a latent protein. J Virol 88(3):1843–1848.  https://doi.org/10.1128/JVI.03251-13 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Leon N. Schulte
    • 1
  • Wilhelm Bertrams
    • 1
  • Christina Stielow
    • 1
  • Bernd Schmeck
    • 1
  1. 1.Institute for Lung Research, Universities of Giessen and Marburg Lung Center, Member of the German Center for Lung Research (DZL)Philipps-University MarburgMarburgGermany

Personalised recommendations