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PMID: 23596287 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Interleukin-22 reduces lung inflammation during influenza A virus infection and protects against secondary bacterial infection.

Journal of virology ·Vol. 87 ·No. 12 ·2013-06-00 ·Pages 6911-24

Ivanov S, Renneson J, Fontaine J, Barthelemy A, Paget C, Fernandez EM, Blanc F, De Trez C, Van Maele L, Dumoutier L, Huerre MR, Eberl G, Si-Tahar M, Gosset P, Renauld JC, Sirard JC, Faveeuw C, Trottein F

Abstract

Interleukin-22 (IL-22) has redundant, protective, or pathogenic functions during autoimmune, inflammatory, and infectious diseases. Here, we addressed the potential role of IL-22 in host defense and pathogenesis during lethal and sublethal respiratory H3N2 influenza A virus (IAV) infection. We show that IL-22, as well as factors associated with its production, are expressed in the lung tissue during the early phases of IAV infection. Our data indicate that retinoic acid receptor-related orphan receptor-γt (RORγt)-positive αβ and γδ T cells, as well as innate lymphoid cells, expressed enhanced Il22 transcripts as early as 2 days postinfection. During lethal or sublethal IAV infections, endogenous IL-22 played no role in the control of IAV replication and in the development of the IAV-specific CD8(+) T cell response. During lethal infection, where wild-type (WT) mice succumbed to severe pneumonia, the lack of IL-22 did not accelerate or delay IAV-associated pathogenesis and animal death. In stark contrast, during sublethal IAV infection, IL-22-deficient animals had enhanced lung injuries and showed a lower airway epithelial integrity relative to WT littermates. Of importance, the protective effect of endogenous IL-22 in pulmonary damages was associated with a more controlled secondary bacterial infection. Indeed, after challenge with Streptococcus pneumoniae, IAV-experienced Il22(-/-) animals were more susceptible than WT controls in terms of survival rate and bacterial burden in the lungs. Together, IL-22 plays no major role during lethal influenza but is beneficial during sublethal H3N2 IAV infection, where it limits lung inflammation and subsequent bacterial superinfections.

MeSH Terms
Animals Bacterial Infections/immunology,microbiology Coinfection/immunology,microbiology Humans Influenza A Virus, H3N2 Subtype/immunology,pathogenicity Interleukins/immunology Lung/immunology,microbiology,pathology Male Mice Mice, Inbred C57BL Orthomyxoviridae Infections/immunology,mortality,virology Pneumonia/immunology,pathology Respiratory Tract Infections/immunology,microbiology Streptococcus pneumoniae/pathogenicity
Chemicals
Interleukins interleukin-22
Authors & Affiliations
18 authors, click to expand affiliations / ORCID
Ivanov Stoyan
Institut Pasteur de Lille, Centre d'Infection et d'Immunité de Lille, Lille, France.
Renneson Joelle
Fontaine Josette
Barthelemy Adeline
Paget Christophe
Fernandez Elodie Macho
Blanc Fany
De Trez Carl
Van Maele Laurye
Dumoutier Laure
Huerre Michel-René
Eberl Gérard
Si-Tahar Mustapha
Gosset Pierre
Renauld Jean Christophe
Sirard Jean Claude
Faveeuw Christelle
Trottein François
References (80)
80 references, click to expand
  1. IL-22 participates in an innate anti-HIV-1 host-resistance network through acute-phase protein induction.
    J Immunol. 2007 Jan 1;178(1):407-15 PMID: 17182579
  2. Pathological versus protective functions of IL-22 in airway inflammation are regulated by IL-17A.
    J Exp Med. 2010 Jun 7;207(6):1293-305 PMID: 20498020
  3. IL-22BP is regulated by the inflammasome and modulates tumorigenesis in the intestine.
    Nature. 2012 Nov 8;491(7423):259-63 PMID: 23075849
  4. Protective properties of inhaled IL-22 in a model of ventilator-induced lung injury.
    Am J Respir Cell Mol Biol. 2011 Mar;44(3):369-76 PMID: 20463292
  5. The integrins Mac-1 and alpha4beta1 perform crucial roles in neutrophil and T cell recruitment to lungs during Streptococcus pneumoniae infection.
    J Immunol. 2011 May 15;186(10):5907-15 PMID: 21460207
  6. IL-22 increases the innate immunity of tissues.
    Immunity. 2004 Aug;21(2):241-54 PMID: 15308104
  7. Interleukin (IL)-22 and IL-17 are coexpressed by Th17 cells and cooperatively enhance expression of antimicrobial peptides.
    J Exp Med. 2006 Oct 2;203(10):2271-9 PMID: 16982811
  8. Regulation and functions of the IL-10 family of cytokines in inflammation and disease.
    Annu Rev Immunol. 2011;29:71-109 PMID: 21166540
  9. Innate Stat3-mediated induction of the antimicrobial protein Reg3γ is required for host defense against MRSA pneumonia.
    J Exp Med. 2013 Mar 11;210(3):551-61 PMID: 23401489
  10. IL-22 from conventional NK cells is epithelial regenerative and inflammation protective during influenza infection.
    Mucosal Immunol. 2013 Jan;6(1):69-82 PMID: 22739232
  11. Influenza enhances susceptibility to natural acquisition of and disease due to Streptococcus pneumoniae in ferrets.
    J Infect Dis. 2010 Oct 15;202(8):1287-95 PMID: 20822454
  12. Interleukin-17-producing gammadelta T cells selectively expand in response to pathogen products and environmental signals.
    Immunity. 2009 Aug 21;31(2):321-30 PMID: 19682928
  13. Lowering the threshold of lung innate immune cell activation alters susceptibility to secondary bacterial superinfection.
    J Infect Dis. 2011 Oct 1;204(7):1086-94 PMID: 21881124
  14. Protection against Streptococcus pneumoniae serotype 1 acute infection shows a signature of Th17- and IFN-γ-mediated immunity.
    Immunobiology. 2012 Apr;217(4):420-9 PMID: 22204818
  15. IL-22 mediates host defense against an intestinal intracellular parasite in the absence of IFN-γ at the cost of Th17-driven immunopathology.
    J Immunol. 2012 Mar 1;188(5):2410-8 PMID: 22266282
  16. Proinflammatory role of the Th17 cytokine interleukin-22 in collagen-induced arthritis in C57BL/6 mice.
    Arthritis Rheum. 2009 Feb;60(2):390-5 PMID: 19180498
  17. Mucosal administration of flagellin protects mice from Streptococcus pneumoniae lung infection.
    Infect Immun. 2010 Oct;78(10):4226-33 PMID: 20643849
  18. Interleukin-22 mediates early host defense against attaching and effacing bacterial pathogens.
    Nat Med. 2008 Mar;14(3):282-9 PMID: 18264109
  19. Class II cytokine receptors and their ligands: key antiviral and inflammatory modulators.
    Nat Rev Immunol. 2003 Aug;3(8):667-76 PMID: 12974481
  20. IL-22 attenuates IL-25 production by lung epithelial cells and inhibits antigen-induced eosinophilic airway inflammation.
    J Allergy Clin Immunol. 2011 Nov;128(5):1067-76.e1-6 PMID: 21794904
  21. A role for mucosal IL-22 production and Th22 cells in HIV-associated mucosal immunopathogenesis.
    Mucosal Immunol. 2012 Nov;5(6):670-80 PMID: 22854709
  22. IL-22 production is regulated by IL-23 during Listeria monocytogenes infection but is not required for bacterial clearance or tissue protection.
    PLoS One. 2011 Feb 15;6(2):e17171 PMID: 21347242
  23. Potential role of invariant NKT cells in the control of pulmonary inflammation and CD8+ T cell response during acute influenza A virus H3N2 pneumonia.
    J Immunol. 2011 May 15;186(10):5590-602 PMID: 21490153
  24. Airway immune homeostasis and implications for influenza-induced inflammation.
    Trends Immunol. 2011 Jul;32(7):328-34 PMID: 21612981
  25. Interleukin 22 (IL-22) plays a protective role in T cell-mediated murine hepatitis: IL-22 is a survival factor for hepatocytes via STAT3 activation.
    Hepatology. 2004 May;39(5):1332-42 PMID: 15122762
  26. The expanding family of innate lymphoid cells: regulators and effectors of immunity and tissue remodeling.
    Nat Immunol. 2011 Jan;12(1):21-7 PMID: 21113163
  27. Interleukin-22 but not interleukin-17 provides protection to hepatocytes during acute liver inflammation.
    Immunity. 2007 Oct;27(4):647-59 PMID: 17919941
  28. High systemic levels of interleukin-10, interleukin-22 and C-reactive protein in Indian patients are associated with low in vitro replication of HIV-1 subtype C viruses.
    Retrovirology. 2010 Mar 09;7:15 PMID: 20211031
  29. Redundant and pathogenic roles for IL-22 in mycobacterial, protozoan, and helminth infections.
    J Immunol. 2010 Apr 15;184(8):4378-90 PMID: 20220096
  30. The innate immune response to pneumococcal lung infection: the untold story.
    Trends Immunol. 2004 Mar;25(3):143-9 PMID: 15036042
  31. Innate lymphoid cells--a proposal for uniform nomenclature.
    Nat Rev Immunol. 2013 Feb;13(2):145-9 PMID: 23348417
  32. STAT3 links IL-22 signaling in intestinal epithelial cells to mucosal wound healing.
    J Exp Med. 2009 Jul 6;206(7):1465-72 PMID: 19564350
  33. New look at an old problem: bacterial superinfection after influenza.
    Am J Pathol. 2010 Feb;176(2):536-9 PMID: 20019194
  34. IL-22 ameliorates intestinal inflammation in a mouse model of ulcerative colitis.
    J Clin Invest. 2008 Feb;118(2):534-44 PMID: 18172556
  35. Human interleukin-10-related T cell-derived inducible factor: molecular cloning and functional characterization as an hepatocyte-stimulating factor.
    Proc Natl Acad Sci U S A. 2000 Aug 29;97(18):10144-9 PMID: 10954742
  36. Emerging role of interleukin-22 in autoimmune diseases.
    Cytokine Growth Factor Rev. 2013 Feb;24(1):51-7 PMID: 22906768
  37. IL-22 mediates mucosal host defense against Gram-negative bacterial pneumonia.
    Nat Med. 2008 Mar;14(3):275-81 PMID: 18264110
  38. Interleukin-22 (IL-22) production by pulmonary Natural Killer cells and the potential role of IL-22 during primary influenza virus infection.
    J Virol. 2010 Aug;84(15):7750-9 PMID: 20504940
  39. In vivo equilibrium of proinflammatory IL-17+ and regulatory IL-10+ Foxp3+ RORgamma t+ T cells.
    J Exp Med. 2008 Jun 9;205(6):1381-93 PMID: 18504307
  40. Interleukin-1 and IL-23 induce innate IL-17 production from gammadelta T cells, amplifying Th17 responses and autoimmunity.
    Immunity. 2009 Aug 21;31(2):331-41 PMID: 19682929
  41. Innate lymphoid cells promote lung-tissue homeostasis after infection with influenza virus.
    Nat Immunol. 2011 Nov;12(11):1045-54 PMID: 21946417
  42. Dual Role of IL-22 in allergic airway inflammation and its cross-talk with IL-17A.
    Am J Respir Crit Care Med. 2011 May 1;183(9):1153-63 PMID: 21297073
  43. IL-22 signaling contributes to West Nile encephalitis pathogenesis.
    PLoS One. 2012;7(8):e44153 PMID: 22952908
  44. Interleukin (IL)-23 mediates Toxoplasma gondii-induced immunopathology in the gut via matrixmetalloproteinase-2 and IL-22 but independent of IL-17.
    J Exp Med. 2009 Dec 21;206(13):3047-59 PMID: 19995958
  45. CD4(+) lymphoid tissue-inducer cells promote innate immunity in the gut.
    Immunity. 2011 Jan 28;34(1):122-34 PMID: 21194981
  46. Innate lymphoid cells promote anatomical containment of lymphoid-resident commensal bacteria.
    Science. 2012 Jun 8;336(6086):1321-5 PMID: 22674331
  47. γδ T cells protect against lung fibrosis via IL-22.
    J Exp Med. 2010 Sep 27;207(10):2239-53 PMID: 20855496
  48. High expression of IL-22 suppresses antigen-induced immune responses and eosinophilic airway inflammation via an IL-10-associated mechanism.
    J Immunol. 2011 Nov 15;187(10):5077-89 PMID: 21998459
  49. Interleukin-22-producing natural killer cells and lymphoid tissue inducer-like cells in mucosal immunity.
    Immunity. 2009 Jul 17;31(1):15-23 PMID: 19604490
  50. IL-22 is required for imiquimod-induced psoriasiform skin inflammation in mice.
    J Immunol. 2012 Jan 1;188(1):462-9 PMID: 22131335
  51. General method for the modification of different BAC types and the rapid generation of BAC transgenic mice.
    Genesis. 2004 Jan;38(1):39-50 PMID: 14755803
  52. Key role for respiratory CD103(+) dendritic cells, IFN-γ, and IL-17 in protection against Streptococcus pneumoniae infection in response to α-galactosylceramide.
    J Infect Dis. 2012 Sep 1;206(5):723-34 PMID: 22723642
  53. The pathology of influenza virus infections.
    Annu Rev Pathol. 2008;3:499-522 PMID: 18039138
  54. A proinflammatory role for interleukin-22 in the immune response to hepatitis B virus.
    Gastroenterology. 2011 Nov;141(5):1897-906 PMID: 21708106
  55. Innate lymphoid cells: emerging insights in development, lineage relationships, and function.
    Annu Rev Immunol. 2012;30:647-75 PMID: 22224763
  56. Identity, regulation and in vivo function of gut NKp46+RORγt+ and NKp46+RORγt- lymphoid cells.
    EMBO J. 2011 Jun 17;30(14):2934-47 PMID: 21685873
  57. The role of interleukin-22 in hepatitis C virus infection.
    Cytokine. 2008 Mar;41(3):209-16 PMID: 18191408
  58. Lethal synergism of 2009 pandemic H1N1 influenza virus and Streptococcus pneumoniae coinfection is associated with loss of murine lung repair responses.
    mBio. 2011 Sep 20;2(5): PMID: 21933918
  59. IL-22 defines a novel immune pathway of antifungal resistance.
    Mucosal Immunol. 2010 Jul;3(4):361-73 PMID: 20445503
  60. IL-22 is expressed by Th17 cells in an IL-23-dependent fashion, but not required for the development of autoimmune encephalomyelitis.
    J Immunol. 2007 Dec 15;179(12):8098-104 PMID: 18056351
  61. Interleukin-22 drives endogenous thymic regeneration in mice.
    Science. 2012 Apr 6;336(6077):91-5 PMID: 22383805
  62. IL-22 and TNF-α represent a key cytokine combination for epidermal integrity during infection with Candida albicans.
    Eur J Immunol. 2011 Jul;41(7):1894-901 PMID: 21469124
  63. Interleukin-22 is produced by invariant natural killer T lymphocytes during influenza A virus infection: potential role in protection against lung epithelial damages.
    J Biol Chem. 2012 Mar 16;287(12):8816-29 PMID: 22294696
  64. Interleukin-22, a T(H)17 cytokine, mediates IL-23-induced dermal inflammation and acanthosis.
    Nature. 2007 Feb 8;445(7128):648-51 PMID: 17187052
  65. Serotypes and clonal types of penicillin-susceptible streptococcus pneumoniae causing invasive disease in children in five Latin American countries.
    Microb Drug Resist. 2005 Fall;11(3):195-204 PMID: 16201921
  66. IL-23 and IL-17A, but not IL-12 and IL-22, are required for optimal skin host defense against Candida albicans.
    J Immunol. 2010 Nov 1;185(9):5453-62 PMID: 20921529
  67. Insights into the interaction between influenza virus and pneumococcus.
    Clin Microbiol Rev. 2006 Jul;19(3):571-82 PMID: 16847087
  68. A previously unrecognized H-2D(b)-restricted peptide prominent in the primary influenza A virus-specific CD8(+) T-cell response is much less apparent following secondary challenge.
    J Virol. 2000 Apr;74(8):3486-93 PMID: 10729122
  69. Lambda and alpha interferons inhibit hepatitis B virus replication through a common molecular mechanism but with different in vivo activities.
    Virology. 2010 Jun 5;401(2):197-206 PMID: 20303135
  70. IL-17 and IL-22: siblings, not twins.
    Trends Immunol. 2010 Sep;31(9):354-61 PMID: 20691634
  71. IL-22 is produced by γC-independent CD25+ CCR6+ innate murine spleen cells upon inflammatory stimuli and contributes to LPS-induced lethality.
    Eur J Immunol. 2011 Apr;41(4):1075-85 PMID: 21400499
  72. Postinfluenza bacterial pneumonia: host defenses gone awry.
    J Interferon Cytokine Res. 2010 Sep;30(9):643-52 PMID: 20726789
  73. Interleukin-22: a cytokine produced by T, NK and NKT cell subsets, with importance in the innate immune defense and tissue protection.
    Cytokine Growth Factor Rev. 2010 Oct;21(5):365-79 PMID: 20870448
  74. Involvement of toll-like receptor 3 in the immune response of lung epithelial cells to double-stranded RNA and influenza A virus.
    J Biol Chem. 2005 Feb 18;280(7):5571-80 PMID: 15579900
  75. TLR5 signaling stimulates the innate production of IL-17 and IL-22 by CD3(neg)CD127+ immune cells in spleen and mucosa.
    J Immunol. 2010 Jul 15;185(2):1177-85 PMID: 20566828
  76. Border patrol: regulation of immunity, inflammation and tissue homeostasis at barrier surfaces by IL-22.
    Nat Immunol. 2011 May;12(5):383-90 PMID: 21502992
  77. Th22 cells represent a distinct human T cell subset involved in epidermal immunity and remodeling.
    J Clin Invest. 2009 Dec;119(12):3573-85 PMID: 19920355
  78. Recognition of Streptococcus pneumoniae by the innate immune system.
    Cell Microbiol. 2012 Apr;14(4):460-6 PMID: 22212419
  79. Predominant role of bacterial pneumonia as a cause of death in pandemic influenza: implications for pandemic influenza preparedness.
    J Infect Dis. 2008 Oct 1;198(7):962-70 PMID: 18710327
  80. Bench-to-bedside review: bacterial pneumonia with influenza - pathogenesis and clinical implications.
    Crit Care. 2010;14(2):219 PMID: 20459593
Article Info
Journal
Journal of virology
Abbr.
J Virol
ISSN
1098-5514
Published
2013-06-00
Epub
2013-00-17
Pages
6911-24
Language
English
Region
United States
NLM ID
0113724
PMCID
PMC3676141
Subset
IM
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