Respective roles of TLR, RIG-I and NLRP3 in influenza virus infection and immunity: impact on vaccine design

References

• La Gruta NL, Kedzierska K, Stambas J, Doherty PC. A question of self-preservation: immunopathology in influenza virus infection. Immunol. Cell Biol.85(2), 85–92 (2007).
   PubMed Web of Science ®Google Scholar
• Janeway CA Jr. The immune system evolved to discriminate infectious nonself from noninfectious self. Immunol. Today13(1), 11–16 (1992).
   PubMedGoogle Scholar
• Janeway CA Jr. How the immune system recognizes invaders. Sci. Am.269(3), 72–79 (1993).
   PubMed Web of Science ®Google Scholar
• Rock KL, Latz E, Ontiveros F, Kono H. The sterile inflammatory response. Ann. Rev. Immunol.28, 321–342 (2010).
   PubMed Web of Science ®Google Scholar
• Sims GP, Rowe DC, Rietdijk ST, Herbst R, Coyle AJ. HMGB1 and RAGE in inflammation and cancer. Ann. Rev. Immunol.28, 367–388 (2010).
   PubMed Web of Science ®Google Scholar
• Takada A, Matsushita S, Ninomiya A, Kawaoka Y, Kida H. Intranasal immunization with formalin-inactivated virus vaccine induces a broad spectrum of heterosubtypic immunity against influenza A virus infection in mice. Vaccine21(23), 3212–3218 (2003).
   PubMed Web of Science ®Google Scholar
• Tumpey TM, Renshaw M, Clements JD, Katz JM. Mucosal delivery of inactivated influenza vaccine induces B-cell-dependent heterosubtypic cross-protection against lethal influenza A H5N1 virus infection. J. Virol.75(11), 5141–5150 (2001).
   PubMed Web of Science ®Google Scholar
• Koyama S, Aoshi T, Tanimoto T et al. Plasmacytoid dendritic cells delineate immunogenicity of influenza vaccine subtypes. Sci. Transl. Med.2(25), 25ra24 (2010).
   PubMed Web of Science ®Google Scholar
• Ichinohe T, Tamura S, Kawaguchi A et al. Cross-protection against H5N1 influenza virus infection is afforded by intranasal inoculation with seasonal trivalent inactivated influenza vaccine. J. Infect. Dis.196(9), 1313–1320 (2007).
   PubMed Web of Science ®Google Scholar
• Ichinohe T, Watanabe I, Ito S et al. Synthetic double-stranded RNA poly(I:C) combined with mucosal vaccine protects against influenza virus infection. J. Virol.79(5), 2910–2919 (2005).
   PubMed Web of Science ®Google Scholar
• Diebold SS, Kaisho T, Hemmi H, Akira S, Reis e Sousa C. Innate antiviral responses by means of TLR7-mediated recognition of single-stranded RNA. Science (NY)303(5663), 1529–1531 (2004).
   PubMed Web of Science ®Google Scholar
• Lund JM, Alexopoulou L, Sato A et al. Recognition of single-stranded RNA viruses by Toll-like receptor 7. Proc. Natl Acad. Sci. USA101(15), 5598–5603 (2004).
   PubMed Web of Science ®Google Scholar
• Kato H, Sato S, Yoneyama M et al. Cell type-specific involvement of RIG-I in antiviral response. Immunity23(1), 19–28 (2005).
   PubMed Web of Science ®Google Scholar
• Rehwinkel J, Tan CP, Goubau D et al. RIG-I detects viral genomic RNA during negative-strand RNA virus infection. Cell140(3), 397–408 (2010).
   PubMed Web of Science ®Google Scholar
• Ichinohe T, Pang IK, Iwasaki A. Influenza virus activates inflammasomes via its intracellular M2 ion channel. Nat. Immunol.11(5), 404–410 (2010).
   PubMed Web of Science ®Google Scholar
• Iwasaki A, Medzhitov R. Regulation of adaptive immunity by the innate immune system. Science (NY)327(5963), 291–295 (2010).
   PubMed Web of Science ®Google Scholar
• Le Goffic R, Balloy V, Lagranderie M et al. Detrimental contribution of the Toll-like receptor (TLR)3 to influenza A virus-induced acute pneumonia. PLoS Path.2(6), e53 (2006).
   PubMedGoogle Scholar
• Schmitz N, Kurrer M, Bachmann MF, Kopf M. Interleukin-1 is responsible for acute lung immunopathology but increases survival of respiratory influenza virus infection. J. Virol.79(10), 6441–6448 (2005).
   PubMed Web of Science ®Google Scholar
• Allen IC, Scull MA, Moore CB et al. The NLRP3 inflammasome mediates in vivo innate immunity to influenza A virus through recognition of viral RNA. Immunity30(4), 556–565 (2009).
   PubMed Web of Science ®Google Scholar
• Hemmi H, Kaisho T, Takeuchi O et al. Small anti-viral compounds activate immune cells via the TLR7 MyD88-dependent signaling pathway. Nat. Immunol.3(2), 196–200 (2002).
   PubMed Web of Science ®Google Scholar
• Heil F, Hemmi H, Hochrein H et al. Species-specific recognition of single-stranded RNA via Toll-like receptor 7 and 8. Science (NY)303(5663), 1526–1529 (2004).
   PubMed Web of Science ®Google Scholar
• Bracci L, Canini I, Puzelli S et al. Type I IFN is a powerful mucosal adjuvant for a selective intranasal vaccination against influenza virus in mice and affects antigen capture at mucosal level. Vaccine23(23), 2994–3004 (2005).
   PubMed Web of Science ®Google Scholar
• Ito T, Amakawa R, Kaisho T et al. Interferon-α and interleukin-12 are induced differentially by Toll-like receptor 7 ligands in human blood dendritic cell subsets. J. Exp. Med.195(11), 1507–1512 (2002).
   PubMed Web of Science ®Google Scholar
• Krug A, Towarowski A, Britsch S et al. Toll-like receptor expression reveals CpG DNA as a unique microbial stimulus for plasmacytoid dendritic cells which synergizes with CD40 ligand to induce high amounts of IL-12. Eur. J. Immunol.31(10), 3026–3037 (2001).
   PubMed Web of Science ®Google Scholar
• Hornung V, Rothenfusser S, Britsch S et al. Quantitative expression of Toll-like receptor 1–10 mRNA in cellular subsets of human peripheral blood mononuclear cells and sensitivity to CpG oligodeoxynucleotides. J. Immunol.168(9), 4531–4537 (2002).
   PubMed Web of Science ®Google Scholar
• Jarrossay D, Napolitani G, Colonna M, Sallusto F, Lanzavecchia A. Specialization and complementarity in microbial molecule recognition by human myeloid and plasmacytoid dendritic cells. Eur. J. Immunol.31(11), 3388–3393 (2001).
   PubMed Web of Science ®Google Scholar
• Kadowaki N, Ho S, Antonenko S et al. Subsets of human dendritic cell precursors express different Toll-like receptors and respond to different microbial antigens. J. Exp. Med.194(6), 863–869 (2001).
   PubMed Web of Science ®Google Scholar
• Asselin-Paturel C, Boonstra A, Dalod M et al. Mouse type I IFN-producing cells are immature APCs with plasmacytoid morphology. Nat. Immunol.2(12), 1144–1150 (2001).
   PubMed Web of Science ®Google Scholar
• Lee HK, Lund JM, Ramanathan B, Mizushima N, Iwasaki A. Autophagy-dependent viral recognition by plasmacytoid dendritic cells. Science (NY)315(5817), 1398–1401 (2007).
   PubMed Web of Science ®Google Scholar
• Kumagai Y, Takeuchi O, Kato H et al. Alveolar macrophages are the primary interferon-α producer in pulmonary infection with RNA viruses. Immunity27(2), 240–252 (2007).
   PubMedGoogle Scholar
• Pichlmair A, Schulz O, Tan CP et al. RIG-I-mediated antiviral responses to single-stranded RNA bearing 5´-phosphates. Science (NY)314(5801), 997–1001 (2006).
   PubMed Web of Science ®Google Scholar
• Guo Z, Chen LM, Zeng H et al. NS1 protein of influenza A virus inhibits the function of intracytoplasmic pathogen sensor, RIG-I. Am. J. Resp. Cell Mol. Biol.36(3), 263–269 (2007).
   PubMed Web of Science ®Google Scholar
• Opitz B, Rejaibi A, Dauber B et al. IFNβ induction by influenza A virus is mediated by RIG-I which is regulated by the viral NS1 protein. Cell. Microbiol.9(4), 930–938 (2007).
   PubMed Web of Science ®Google Scholar
• Mibayashi M, Martinez-Sobrido L, Loo YM, Cardenas WB, Gale M Jr, Garcia-Sastre A. Inhibition of retinoic acid-inducible gene I-mediated induction of β interferon by the NS1 protein of influenza A virus. J. Virol.81(2), 514–524 (2007).
   PubMed Web of Science ®Google Scholar
• Geurts van Kessel CH, Willart MA, van Rijt LS et al. Clearance of influenza virus from the lung depends on migratory langerin+CD11b- but not plasmacytoid dendritic cells. J. Exp. Med.205(7), 1621–1634 (2008).
   PubMedGoogle Scholar
• Iwasaki A, Medzhitov R. Toll-like receptor control of the adaptive immune responses. Nat. Immunol.5(10), 987–995 (2004).
   PubMed Web of Science ®Google Scholar
• Medzhitov R. Toll-like receptors and innate immunity. Nat. Rev.1(2), 135–145 (2001).
   Google Scholar
• Geurts van Kessel CH, Willart MA, Bergen IM et al. Dendritic cells are crucial for maintenance of tertiary lymphoid structures in the lung of influenza virus-infected mice. J. Exp. Med.206(11), 2339–2349 (2009).
   PubMedGoogle Scholar
• Kim TS, Braciale TJ. Respiratory dendritic cell subsets differ in their capacity to support the induction of virus-specific cytotoxic CD8+ T cell responses. PloS One4(1), e4204 (2009).
   PubMed Web of Science ®Google Scholar
• Ballesteros-Tato A, Leon B, Lund FE, Randall TD. Temporal changes in dendritic cell subsets, cross-priming and costimulation via CD70 control CD8(+) T cell responses to influenza. Nat. Immunol.11(3), 216–224 (2010).
   PubMed Web of Science ®Google Scholar
• Belz GT, Smith CM, Kleinert L et al. Distinct migrating and nonmigrating dendritic cell populations are involved in MHC class I-restricted antigen presentation after lung infection with virus. Proc. Natl Acad. Sci. USA101(23), 8670–8675 (2004).
   PubMed Web of Science ®Google Scholar
• McGill J, Van Rooijen N, Legge KL. Protective influenza-specific CD8 T cell responses require interactions with dendritic cells in the lungs. J. Exp. Med.205(7), 1635–1646 (2008).
   PubMed Web of Science ®Google Scholar
• McGill J, Van Rooijen N, Legge KL. IL-15 trans-presentation by pulmonary dendritic cells promotes effector CD8 T cell survival during influenza virus infection. J. Exp. Med.207(3), 521–534 (2010).
   PubMed Web of Science ®Google Scholar
• Lui G, Manches O, Angel J, Molens JP, Chaperot L, Plumas J. Plasmacytoid dendritic cells capture and cross-present viral antigens from influenza-virus exposed cells. PloS One4(9), e7111 (2009).
   PubMed Web of Science ®Google Scholar
• Lopez CB, Moltedo B, Alexopoulou L, Bonifaz L, Flavell RA, Moran TM. TLR-independent induction of dendritic cell maturation and adaptive immunity by negative-strand RNA viruses. J. Immunol.173(11), 6882–6889 (2004).
   PubMedGoogle Scholar
• Koyama S, Ishii KJ, Kumar H et al. Differential role of TLR- and RLR-signaling in the immune responses to influenza A virus infection and vaccination. J. Immunol.179(7), 4711–4720 (2007).
   PubMed Web of Science ®Google Scholar
• Heer AK, Shamshiev A, Donda A et al. TLR signaling fine-tunes anti-influenza B cell responses without regulating effector T cell responses. J. Immunol.178(4), 2182–2191 (2007).
   PubMed Web of Science ®Google Scholar
• Geeraedts F, Goutagny N, Hornung V et al. Superior immunogenicity of inactivated whole virus H5N1 influenza vaccine is primarily controlled by Toll-like receptor signalling. PLoS Pathog.4(8), e1000138 (2008).
   PubMed Web of Science ®Google Scholar
• Seki M, Higashiyama Y, Tomono K et al. Acute infection with influenza virus enhances susceptibility to fatal pneumonia following Streptococcus pneumoniae infection in mice with chronic pulmonary colonization with Pseudomonas aeruginosa. Clin. Exp. Immunol.137(1), 35–40 (2004).
   PubMedGoogle Scholar
• Sun K, Metzger DW. Inhibition of pulmonary antibacterial defense by interferon-γ during recovery from influenza infection. Nat. Med.14(5), 558–564 (2008).
   PubMed Web of Science ®Google Scholar
• Shahangian A, Chow EK, Tian X et al. Type I IFNs mediate development of postinfluenza bacterial pneumonia in mice. J. Clin. Invest.119(7), 1910–1920 (2009).
   PubMed Web of Science ®Google Scholar
• Gunzer M, Riemann H, Basoglu Y et al. Systemic administration of a TLR7 ligand leads to transient immune incompetence due to peripheral-blood leukocyte depletion. Blood106(7), 2424–2432 (2005).
   PubMed Web of Science ®Google Scholar
• Stegemann S, Dahlberg S, Kroger A et al. Increased susceptibility for superinfection with Streptococcus pneumoniae during influenza virus infection is not caused by TLR7-mediated lymphopenia. PloS One4(3), e4840 (2009).
   Google Scholar
• Jamieson AM, Yu S, Annicelli CH, Medzhitov R. Influenza virus-induced glucocorticoids compromise innate host defense against a secondary bacterial infection. Cell Host Microbe7(2), 103–114 (2010).
   PubMedGoogle Scholar
• Didierlaurent A, Goulding J, Patel S et al. Sustained desensitization to bacterial Toll-like receptor ligands after resolution of respiratory influenza infection. J. Exp. Med.205(2), 323–329 (2008).
   PubMed Web of Science ®Google Scholar
• de Jong MD, Simmons CP, Thanh TT et al. Fatal outcome of human influenza A (H5N1) is associated with high viral load and hypercytokinemia. Nat. Med.12(10), 1203–1207 (2006).
   PubMed Web of Science ®Google Scholar
• Itoh Y, Shinya K, Kiso M et al.In vitro and in vivo characterization of new swine-origin H1N1 influenza viruses. Nature460(7258), 1021–1025 (2009).
   PubMed Web of Science ®Google Scholar
• Wolf AI, Buehler D, Hensley SE et al. Plasmacytoid dendritic cells are dispensable during primary influenza virus infection. J. Immunol.182(2), 871–879 (2009).
   PubMed Web of Science ®Google Scholar
• Hammerbeck DM, Burleson GR, Schuller CJ et al. Administration of a dual Toll-like receptor 7 and Toll-like receptor 8 agonist protects against influenza in rats. Antiviral Res.73(1), 1–11 (2007).
   PubMed Web of Science ®Google Scholar
• Yoneyama M, Kikuchi M, Natsukawa T et al. The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses. Nat. Immunol.5(7), 730–737 (2004).
   PubMed Web of Science ®Google Scholar
• Kato H, Takeuchi O, Sato S et al. Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses. Nature441(7089), 101–105 (2006).
   PubMed Web of Science ®Google Scholar
• Hornung V, Ellegast J, Kim S et al. 5´-triphosphate RNA is the ligand for RIG-I. Science (NY)314(5801), 994–997 (2006).
   PubMed Web of Science ®Google Scholar
• Schlee M, Roth A, Hornung V et al. Recognition of 5´ triphosphate by RIG-I helicase requires short blunt double-stranded RNA as contained in panhandle of negative-strand virus. Immunity31(1), 25–34 (2009).
   PubMed Web of Science ®Google Scholar
• Rehwinkel J, Reis e Sousa C. RIGorous detection: exposing virus through RNA sensing. Science (NY)327(5963), 284–286 (2010).
   PubMed Web of Science ®Google Scholar
• Kawai T, Takahashi K, Sato S et al. IPS-1, an adaptor triggering RIG-I- and MDA5-mediated type I interferon induction. Nat. Immunol.6(10), 981–988 (2005).
   PubMed Web of Science ®Google Scholar
• Seth RB, Sun L, Ea CK, Chen ZJ. Identification and characterization of MAVS, a mitochondrial antiviral signaling protein that activates NF-κB and IRF 3. Cell122(5), 669–682 (2005).
   PubMed Web of Science ®Google Scholar
• Meylan E, Curran J, Hofmann K et al. Cardif is an adaptor protein in the RIG-I antiviral pathway and is targeted by hepatitis C virus. Nature437(7062), 1167–1172 (2005).
   PubMed Web of Science ®Google Scholar
• Xu LG, Wang YY, Han KJ, Li LY, Zhai Z, Shu HB. VISA is an adapter protein required for virus-triggered IFN-β signaling. Mol. Cell19(6), 727–740 (2005).
   PubMed Web of Science ®Google Scholar
• Moore CB, Bergstralh DT, Duncan JA et al. NLRX1 is a regulator of mitochondrial antiviral immunity. Nature451(7178), 573–577 (2008).
   PubMedGoogle Scholar
• Tattoli I, Carneiro LA, Jehanno M et al. NLRX1 is a mitochondrial NOD-like receptor that amplifies NF-κB and JNK pathways by inducing reactive oxygen species production. EMBO Reports9(3), 293–300 (2008).
   PubMedGoogle Scholar
• Chakravarthy KV, Bonoiu AC, Davis WG et al. Gold nanorod delivery of an ssRNA immune activator inhibits pandemic H1N1 influenza viral replication. Proc. Natl Acad. Sci. USA107(22), 10172–10177 (2010).
   PubMed Web of Science ®Google Scholar
• Ranjan P, Jayashankar L, Deyde V et al. 5´PPP-RNA induced RIG-I activation inhibits drug-resistant avian H5N1 as well as 1918 and 2009 pandemic influenza virus replication. Virol. J.7, 102 (2010).
   PubMedGoogle Scholar
• Talon J, Salvatore M, O’Neill RE et al. Influenza A and B viruses expressing altered NS1 proteins: a vaccine approach. Proc. Natl Acad. Sci. USA97(8), 4309–4314 (2000).
   PubMed Web of Science ®Google Scholar
• Min JY, Krug RM. The primary function of RNA binding by the influenza A virus NS1 protein in infected cells: inhibiting the 2´-5´ oligo (A) synthetase/RNase L pathway. Proc. Natl Acad. Sci. USA103(18), 7100–7105 (2006).
   PubMed Web of Science ®Google Scholar
• Gack MU, Albrecht RA, Urano T et al. Influenza A virus NS1 targets the ubiquitin ligase TRIM25 to evade recognition by the host viral RNA sensor RIG-I. Cell Host Microbe5(5), 439–449 (2009).
   PubMed Web of Science ®Google Scholar
• Gack MU, Shin YC, Joo CH et al. TRIM25 RING-finger E3 ubiquitin ligase is essential for RIG-I-mediated antiviral activity. Nature446(7138), 916–920 (2007).
   PubMed Web of Science ®Google Scholar
• Martinon F, Mayor A, Tschopp J. The inflammasomes: guardians of the body. Ann. Rev. Immunol.27, 229–265 (2009).
   PubMed Web of Science ®Google Scholar
• Bergsbaken T, Fink SL, Cookson BT. Pyroptosis: host cell death and inflammation. Nat. Rev. Microbiol.7(2), 99–109 (2009).
   PubMed Web of Science ®Google Scholar
• Ting JP, Willingham SB, Bergstralh DT. NLRs at the intersection of cell death and immunity. Nat. Rev.8(5), 372–379 (2008).
   Google Scholar
• Mariathasan S, Monack DM. Inflammasome adaptors and sensors: intracellular regulators of infection and inflammation. Nat. Rev.7(1), 31–40 (2007).
   Google Scholar
• Ichinohe T, Lee HK, Ogura Y, Flavell R, Iwasaki A. Inflammasome recognition of influenza virus is essential for adaptive immune responses. J. Exp. Med.206(1), 79–87 (2009).
   PubMed Web of Science ®Google Scholar
• Thomas PG, Dash P, Aldridge JR Jr et al. The intracellular sensor NLRP3 mediates key innate and healing responses to influenza A virus via the regulation of caspase-1. Immunity30(4), 566–575 (2009).
   PubMed Web of Science ®Google Scholar
• Schroder K, Tschopp J. The inflammasomes. Cell140(6), 821–832 (2010).
   PubMed Web of Science ®Google Scholar
• Tschopp J, Schroder K. NLRP3 inflammasome activation: the convergence of multiple signalling pathways on ROS production? Nat. Rev.10(3), 210–215 (2010).
   Google Scholar
• Sutterwala FS, Ogura Y, Szczepanik M et al. Critical role for NALP3/CIAS1/cryopyrin in innate and adaptive immunity through its regulation of caspase-1. Immunity24(3), 317–327 (2006).
   PubMed Web of Science ®Google Scholar
• Eisenbarth SC, Colegio OR, O’Connor W, Sutterwala FS, Flavell RA. Crucial role for the NALP3 inflammasome in the immunostimulatory properties of aluminium adjuvants. Nature453(7198), 1122–1126 (2008).
   PubMed Web of Science ®Google Scholar
• Watanabe H, Gaide O, Petrilli V et al. Activation of the IL-1β-processing inflammasome is involved in contact hypersensitivity. J. Invest. Dermatol.127(8), 1956–1963 (2007).
   PubMed Web of Science ®Google Scholar
• Kool M, Petrilli V, De Smedt T et al. Cutting edge: alum adjuvant stimulates inflammatory dendritic cells through activation of the NALP3 inflammasome. J. Immunol.181(6), 3755–3759 (2008).
   PubMed Web of Science ®Google Scholar
• McKee AS, Munks MW, MacLeod MK et al. Alum induces innate immune responses through macrophage and mast cell sensors, but these sensors are not required for alum to act as an adjuvant for specific immunity. J. Immunol.183(7), 4403–4414 (2009).
   PubMed Web of Science ®Google Scholar
• Franchi L, Nunez G. The NLRP3 inflammasome is critical for aluminium hydroxide-mediated IL-1β secretion but dispensable for adjuvant activity. Eur. J. Immunol.38(8), 2085–2089 (2008).
   PubMed Web of Science ®Google Scholar
• Ichinohe T, Kawaguchi A, Tamura S et al. Intranasal immunization with H5N1 vaccine plus Poly I:Poly C12U, a Toll-like receptor agonist, protects mice against homologous and heterologous virus challenge. Microbes Infect.9(11), 1333–1340 (2007).
   PubMed Web of Science ®Google Scholar
• Ichinohe T, Ainai A, Ami Y et al. Intranasal administration of adjuvant-combined vaccine protects monkeys from challenge with the highly pathogenic influenza A H5N1 virus. J. Med. Virol.82(10), 1754–1761 (2010).
   PubMed Web of Science ®Google Scholar