Induction of innate immunity and its perturbation by influenza viruses
Received date: 06 Jun 2015
Accepted date: 29 Jun 2015
Published date: 22 Oct 2015
Copyright
Influenza A viruses (IAV) are highly contagious pathogens causing dreadful losses to human and animal, around the globe. IAVs first interact with the host through epithelial cells, and the viral RNA containing a 5′-triphosphate group is thought to be the critical trigger for activation of effective innate immunity via pattern recognition receptors-dependent signaling pathways. These induced immune responses establish the antiviral state of the host for effective suppression of viral replication and enhancing viral clearance. However, IAVs have evolved a variety of mechanisms by which they can invade host cells, circumvent the host immune responses, and use the machineries of host cells to synthesize and transport their own components, which help them to establish a successful infection and replication. In this review, we will highlight the molecular mechanisms of how IAV infection stimulates the host innate immune system and strategies by which IAV evades host responses.
Key words: influenza A virus; innate immunity; immune escape
Mohsan Ullah Goraya , Song Wang , Muhammad Munir , Ji-Long Chen . Induction of innate immunity and its perturbation by influenza viruses[J]. Protein & Cell, 2015 , 6(10) : 712 -721 . DOI: 10.1007/s13238-015-0191-z
1 |
Ablasser A, Poeck H, Anz D, Berger M, Schlee M, Kim S, Bourquin C, Goutagny N, Jiang Z, Fitzgerald KA
|
2 |
Achdout H, Arnon TI, Markel G, Gonen-Gross T, Katz G, Lieberman N, Gazit R, Joseph A, Kedar E, Mandelboim O (2003) Enhanced recognition of human NK receptors after influenza virus infection. J Immunol 171: 915−923
|
3 |
Alexopoulou L, Holt AC, Medzhitov R, Flavell RA (2001) Recognition of double-stranded RNA and activation of NF-kappaB by Toll-like receptor 3. Nature 413: 732−738
|
4 |
Arnon TI, Lev M, Katz G, Chernobrov Y, Porgador A, Mandelboim O (2001) Recognition of viral hemagglutinins by NKp44 but not by NKp30. Eur J Immunol 31: 2680−2689
|
5 |
Becker S, Quay J, Soukup J (1991) Cytokine (tumor necrosis factor, IL-6, and IL-8) production by respiratory syncytial virus-infected human alveolar macrophages. J Immunol 147: 4307−4312
|
6 |
Bergsbaken T, Fink SL, Cookson BT (2009) Pyroptosis: host cell death and inflammation. Nat Rev Microbiol 7: 99−109
|
7 |
Bleiblo F, Michael P, Brabant D, Ramana CV, Tai T, Saleh M, Parrillo JE, Kumar A, Kumar A (2012) The role of immunostimulatory nucleic acids in septic shock. Int J Clin Exp Med 5: 1−23
|
8 |
Carr SM, Carnero E, Garcia-Sastre A, Brownlee GG, Fodor E (2006) Characterization of a mitochondrial-targeting signal in the PB2 protein of influenza viruses. Virology 344: 492−508
|
9 |
Chen Z, Li Y, Krug RM (1999) Influenza A virus NS1 protein targets poly(A)-binding protein II of the cellular 3’-end processing machinery. EMBO J 18: 2273−2283
|
10 |
Chen W, Calvo PA, Malide D, Gibbs J, Schubert U, Bacik I, Basta S, O’Neill R, Schickli J, Palese P
|
11 |
Coloma R, Valpuesta JM, Arranz R, Carrascosa JL, Ortin J, Martin-Benito J (2009) The structure of a biologically active influenza virus ribonucleoprotein complex. PLoS Pathog 5: e1000491
|
12 |
Conenello GM, Zamarin D, Perrone LA, Tumpey T, Palese P (2007) A single mutation in the PB1-F2 of H5N1 (HK/97) and 1918 influenza A viruses contributes to increased virulence. PloS Pathog 3: 1414−1421
|
13 |
Dawson TC, Beck MA, Kuziel WA, Henderson F, Maeda N (2000) Contrasting effects of CCR5 and CCR2 deficiency in the pulmonary inflammatory response to influenza A virus. Am J Pathol 156: 1951−1959
|
14 |
de Veer MJ, Holko M, Frevel M, Walker E, Der S, Paranjape JM, Silverman RH, Williams BR (2001) Functional classification of interferon-stimulated genes identified using microarrays. J leukoc Biol 69: 912−920
|
15 |
Dias A, Bouvier D, Crepin T, McCarthy AA, Hart DJ, Baudin F, Cusack S, Ruigrok RW (2009) The cap-snatching endonuclease of influenza virus polymerase resides in the PA subunit. Nature 458: 914−918
|
16 |
Ferko B, Stasakova J, Romanova J, Kittel C, Sereinig S, Katinger H, Egorov A (2004) Immunogenicity and protection efficacy of replication-deficient influenza A viruses with altered NS1 genes. J Virol 78: 13037−13045
|
17 |
Flint SJ, Enquist L, Racaniello VR, Skalka AM (2003) Principles of virology. Molecular biology, pathogenesis, and control of animal viruses, 2nd edn. ASM Press, Washington, DC
|
18 |
Fontana J, Cardone G, Heymann JB, Winkler DC, Steven AC (2012) Structural changes in Influenza virus at low pH characterized by cryo-electron tomography. J Virol 86: 2919−2929
|
19 |
Fournier E, Moules V, Essere B, Paillart JC, Sirbat JD, Isel C, Cavalier A, Rolland JP, Thomas D, Lina B
|
20 |
Gack MU, Shin YC, Joo CH, Urano T, Liang C, Sun L, Takeuchi O, Akira S, Chen Z, Inoue S
|
21 |
Gack MU, Albrecht RA, Urano T, Inn KS, Huang IC, Carnero E, Farzan M, Inoue S, Jung JU, Garcia-Sastre A (2009) Influenza A virus NS1 targets the ubiquitin ligase TRIM25 to evade recognition by the host viral RNA sensor RIG-I. Cell Host Microbe 5: 439−449
|
22 |
Gannage M, Dormann D, Albrecht R, Dengjel J, Torossi T, Ramer PC, Lee M, Strowig T, Arrey F, Conenello G
|
23 |
Garcia-Sastre A, Egorov A, Matassov D, Brandt S, Levy DE, Durbin JE, Palese P, Muster T (1998) Influenza A virus lacking the NS1 gene replicates in interferon-deficient systems. Virology 252: 324−330
|
24 |
Gazit R, Gruda R, Elboim M, Arnon TI, Katz G, Achdout H, Hanna J, Qimron U, Landau G, Greenbaum E
|
25 |
Graef KM, Vreede FT, Lau YF, McCall AW, Carr SM, Subbarao K, Fodor E (2010) The PB2 subunit of the influenza virus RNA polymerase affects virulence by interacting with the mitochondrial antiviral signaling protein and inhibiting expression of beta interferon. J Virol 84: 8433−8445
|
26 |
Grimm D, Staeheli P, Hufbauer M, Koerner I, Martinez-Sobrido L, Solorzano A, Garcia-Sastre A, Haller O, Kochs G (2007) Replication fitness determines high virulence of influenza A virus in mice carrying functional Mx1 resistance gene. Proc Natl Acad Sci USA 104: 6806−6811
|
27 |
Guan R, Ma LC, Leonard PG, Amer BR, Sridharan H, Zhao C, Krug RM, Montelione GT (2011) Structural basis for the sequencespecific recognition of human ISG15 by the NS1 protein of influenza B virus. Proc Natl Acad Sci USA 108: 13468−13473
|
28 |
Guarda G, Zenger M, Yazdi AS, Schroder K, Ferrero I, Menu P, Tardivel A, Mattmann C, Tschopp J (2011) Differential expression of NLRP3 among hematopoietic cells. J Immunol 186: 2529−2534
|
29 |
Guillot L, Le Goffic R, Bloch S, Escriou N, Akira S, Chignard M, Si-Tahar M (2005) 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 280: 5571−5580
|
30 |
Hale BG, Albrecht RA, Garcia-Sastre A (2010) Innate immune evasion strategies of influenza viruses. Future Microbiol 5: 23−41
|
31 |
Hamilton BS, Gludish DW, Whittaker GR (2012) Cleavage activation of the human-adapted influenza virus subtypes by matriptase reveals both subtype and strain specificities. J Virol 86: 10579−10586
|
32 |
Hashimoto Y, Moki T, Takizawa T, Shiratsuchi A, Nakanishi Y (2007) Evidence for phagocytosis of influenza virus-infected, apoptotic cells by neutrophils and macrophages in mice. J Immunol 178: 2448−2457
|
33 |
Hayden MS, Ghosh S (2004) Signaling to NF-kappaB. Genes Dev 18: 2195−2224
|
34 |
Herold S, von Wulffen W, Steinmueller M, Pleschka S, Kuziel WA, Mack M, Srivastava M, Seeger W, Maus UA, Lohmeyer J (2006) Alveolar epithelial cells direct monocyte transepithelial migration upon influenza virus infection: impact of chemokines and adhesion molecules. J Immunol 177: 1817−1824
|
35 |
Holt PG, Strickland DH, Wikstrom ME, Jahnsen FL (2008) Regulation of immunological homeostasis in the respiratory tract. Nat Rev Immunol 8: 142−152
|
36 |
Horimoto T, Kawaoka Y (2001) Pandemic threat posed by avian influenza A viruses. Clin Microbiol Rev 14: 129−149
|
37 |
Horimoto T, Kawaoka Y (2005) Influenza: lessons from past pandemics, warnings from current incidents. Nat Rev Microbiol 3: 591−600
|
38 |
Ichinohe T, Pang IK, Iwasaki A (2010) Influenza virus activates inflammasomes via its intracellular M2 ion channel. Nat Immunol 11: 404−410
|
39 |
Inglis SC, Carroll AR, Lamb RA, Mahy BW (1976) Polypeptides specified by the influenza virus genome I. Evidence for eight distinct gene products specified by fowl plague virus. Virology 74: 489−503
|
40 |
Iwai A, Shiozaki T, Kawai T, Akira S, Kawaoka Y, Takada A, Kida H, Miyazaki T (2010) Influenza A virus polymerase inhibits type I interferon induction by binding to interferon beta promoter stimulator 1. J Biol Chem 285: 32064−32074
|
41 |
Jagger BW, Wise HM, Kash JC, Walters KA, Wills NM, Xiao YL, Dunfee RL, Schwartzman LM, Ozinsky A, Bell GL
|
42 |
Jayasekera JP, Vinuesa CG, Karupiah G, King NJ (2006) Enhanced antiviral antibody secretion and attenuated immunopathology during influenza virus infection in nitric oxide synthase-2-deficient mice. J Gen Virol 87: 3361−3371
|
43 |
Jia D, Rahbar R, Chan RW, Lee SM, Chan MC, Wang BX, Baker DP, Sun B, Peiris JS, Nicholls JM
|
44 |
Kawai T, Akira S (2011) Toll-like receptors and their crosstalk with other innate receptors in infection and immunity. Immunity 34: 637−650
|
45 |
Kessler DS, Veals SA, Fu XY, Levy DE (1990) Interferon-alpha regulates nuclear translocation and DNA-binding affinity of ISGF3, a multimeric transcriptional activator. Genes Dev 4: 1753−1765
|
46 |
Kim HM, Lee YW, Lee KJ, Kim HS, Cho SW, van Rooijen N, Guan Y, Seo SH (2008) Alveolar macrophages are indispensable for controlling influenza viruses in lungs of pigs. J Virol 82: 4265−4274
|
47 |
Klenk HD, Cox NJ, Lamb RA, Mahy BW, Nakamura K, Nuttall PA, Palese P, Rott R (2004) Orthomyxoviridae. In ICTVdB-The Universal Virus Database. Columbia University, In New York
|
48 |
Klumpp K, Ruigrok RW, Baudin F (1997) Roles of the influenza virus polymerase and nucleoprotein in forming a functional RNP structure. EMBO J 16: 1248−1257
|
49 |
Krug RM, Lamb RA (2001) Orthomyxoviridae: the viruses and their replication, 4th edn. Lippincott Williams & Wilkins, Baltimore
|
50 |
Lamb RA, Choppin PW (1976) Synthesis of influenza virus proteins in infected cells: translation of viral polypeptides, including three P polypeptides, from RNA produced by primary transcription. Virology 74: 504−519
|
51 |
Le Goffic R, Pothlichet J, Vitour D, Fujita T, Meurs E, Chignard M, Si-Tahar M (2007) Cutting Edge: Influenza A virus activates TLR3- dependent inflammatory and RIG-I-dependent antiviral responses in human lung epithelial cells. J Immunol 178: 3368−3372
|
52 |
Lee SM, Kok KH, Jaume M, Cheung TK, Yip TF, Lai JC, Guan Y, Webster RG, Jin DY, Peiris JS (2014) Toll-like receptor 10 is involved in induction of innate immune responses to influenza virus infection. Proc Natl Acad Sci USA 111: 3793−3798
|
53 |
Leung HS, Li OT, Chan RW, Chan MC, Nicholls JM, Poon LL (2012) Entry of influenza A Virus with a alpha2,6-linked sialic acid binding preference requires host fibronectin. J Virol 86: 10704−10713
|
54 |
Li S, Min JY, Krug RM, Sen GC (2006) Binding of the influenza A virus NS1 protein to PKR mediates the inhibition of its activation by either PACT or double-stranded RNA. Virology 349: 13−21
|
55 |
Lin KL, Suzuki Y, Nakano H, Ramsburg E, Gunn MD (2008) CCR2+ monocyte-derived dendritic cells and exudate macrophages produce influenza-induced pulmonary immune pathology and mortality. J Immunol 180: 2562−2572
|
56 |
Loo YM, Gale M Jr (2011) Immune signaling by RIG-I-like receptors. Immunity 34: 680−692
|
57 |
Loo YM, Fornek J, Crochet N, Bajwa G, Perwitasari O, Martinez-Sobrido L, Akira S, Gill MA, Garcia-Sastre A, Katze MG
|
58 |
Lund JM, Alexopoulou L, Sato A, Karow M, Adams NC, Gale NW, Iwasaki A, Flavell RA (2004) Recognition of single-stranded RNA viruses by Toll-like receptor 7. Proc Natl Acad Sci USA 101: 5598−5603
|
59 |
Mandelboim O, Lieberman N, Lev M, Paul L, Arnon TI, Bushkin Y, Davis DM, Strominger JL, Yewdell JW, Porgador A (2001) Recognition of hemagglutinins on virus-infected cells by NKp46 activates lysis by human NK cells. Nature 409: 1055−1060
|
60 |
Martinon F, Mayor A, Tschopp J (2009) The inflammasomes: guardians of the body. Annu Rev Immunol 27: 229−265
|
61 |
McAuley JL, Tate MD, MacKenzie-Kludas CJ, Pinar A, Zeng W, Stutz A, Latz E, Brown LE, Mansell A (2013) Activation of the NLRP3 inflammasome by IAV virulence protein PB1-F2 contributes to severe pathophysiology and disease. PLoS Pathog 9: e1003392
|
62 |
Medina RA, Garcia-Sastre A (2011) Influenza A viruses: new research developments. Nat Rev Microbiol 9: 590−603
|
63 |
Mendelson M, Tekoah Y, Zilka A, Gershoni-Yahalom O, Gazit R, Achdout H, Bovin NV, Meningher T, Mandelboim M, Mandelboim O
|
64 |
Mukaigawa J, Nayak DP(1991) Two signals mediate nuclear localization of influenza virus (A/WSN/33) polymerase basic protein 2. J Virol 65: 245−253
|
65 |
Munir M (2010) TRIM proteins: another class of viral victims. Sci Signal 3: jc2
|
66 |
Nemeroff ME, Barabino SM, Li Y, Keller W, Krug RM (1998) Influenza virus NS1 protein interacts with the cellular 30 kDa subunit of CPSF and inhibits 3’end formation of cellular premRNAs. Mol Cell 1: 991−1000
|
67 |
O’Neill RE, Jaskunas R, Blobel G, Palese P, Moroianu J (1995) Nuclear import of influenza virus RNA can be mediated by viral nucleoprotein and transport factors required for protein import. J Biol Chem 270: 22701−22704
|
68 |
Ouyang J, Zhu X, Chen Y, Wei H, Chen Q, Chi X, Qi B, Zhang L, Zhao Y, Gao, George F
|
69 |
Paget C, Ivanov S, Fontaine J, Blanc F, Pichavant M, Renneson J, Bialecki E, Pothlichet J, Vendeville C, Barba-Spaeth G
|
70 |
Palese P (2004) Influenza: old and new threats. Nat Med 10: S82−S87
|
71 |
Pang IK, Iwasaki A (2011) Inflammasomes as mediators of immunity against influenza virus. Trends Immunol 32: 34−41
|
72 |
Perrone LA, Plowden JK, Garcia-Sastre A, Katz JM, Tumpey TM (2008) H5N1 and 1918 pandemic influenza virus infection results in early and excessive infiltration of macrophages and neutrophils in the lungs of mice. PLoS Pathog 4: e1000115
|
73 |
Pichlmair A, Schulz O, Tan CP, Naslund TI, Liljestrom P, Weber F, Reis e Sousa C (2006) RIG-I-mediated antiviral responses to single-stranded RNA bearing 5’-phosphates. Science 314: 997−1001
|
74 |
Pinto LH, Holsinger LJ, Lamb RA (1992) Influenza virus M2 protein has ion channel activity. Cell 69: 517−528
|
75 |
Pothlichet J, Meunier I, Davis BK, Ting JP, Skamene E, von Messling V, Vidal SM (2013) Type I IFN triggers RIG-I/TLR3/NLRP3-dependent inflammasome activation in influenza A virus infected cells. PLoS Pathog 9: e1003256
|
76 |
Satterly N, Tsai PL, van Deursen J, Nussenzveig DR, Wang Y, Faria PA, Levay A, Levy DE, Fontoura BM (2007) Influenza virus targets the mRNA export machinery and the nuclear pore complex. Proc Natl Acad Sci USA 104: 1853−1858
|
77 |
Schaap IA, Eghiaian F, des Georges A, Veigel C (2012) Effect of envelope proteins on the mechanical properties of influenza virus. J Biol Chem 287: 41078−41088
|
78 |
Sharma K, Tripathi S, Ranjan P, Kumar P, Garten R, Deyde V, Katz JM, Cox NJ, Lal RB, Sambhara S
|
79 |
Solorzano A, Webby RJ, Lager KM, Janke BH, Garcia-Sastre A, Richt JA (2005) Mutations in the NS1 protein of swine influenza virus impair anti-interferon activity and confer attenuation in pigs. J Virol 79: 7535−7543
|
80 |
Steel J, Lowen AC, Pena L, Angel M, Solorzano A, Albrecht R, Perez DR, Garcia-Sastre A, Palese P (2009) Live attenuated influenza viruses containing NS1 truncations as vaccine candidates against H5N1 highly pathogenic avian influenza. J Virol 83: 1742−1753
|
81 |
Stohr K (2002) Influenza—WHO cares. Lancet Infect Dis 2: 517
|
82 |
Thomas PG, Dash P, Aldridge JR Jr, Ellebedy AH, Reynolds C, Funk AJ, Martin WJ, Lamkanfi M, Webby RJ, Boyd KL
|
83 |
Tumpey TM, Garcia-Sastre A, Taubenberger JK, Palese P, Swayne DE, Pantin-Jackwood MJ, Schultz-Cherry S, Solorzano A, Van Rooijen N, Katz JM
|
84 |
Upham JP, Pickett D, Irimura T, Anders EM, Reading PC (2010) Macrophage receptors for influenza A virus: role of the macrophage galactose-type lectin and mannose receptor in viral entry. J Virol 84: 3730−3737
|
85 |
van Riel D, Leijten LM, van der Eerden M, Hoogsteden HC, Boven LA, Lambrecht BN, Osterhaus AD, Kuiken T (2011) Highly pathogenic avian influenza virus H5N1 infects alveolar macrophages without virus production or excessive TNF-alpha induction. PLoS Pathog 7: e1002099
|
86 |
Varga ZT, Ramos I, Hai R, Schmolke M, Garcia-Sastre A, Fernandez-Sesma A, Palese P (2011) The influenza virus protein PB1-F2 inhibits the induction of type I interferon at the level of the MAVS adaptor protein. PLoS Pathog 7: e1002067
|
87 |
Wang S, Li H, Chen Y, Wei H, Gao GF, Liu H, Huang S, Chen JL (2012) Transport of influenza virus neuraminidase (NA) to host cell surface is regulated by ARHGAP21 and Cdc42 proteins. J Biol Chem 287: 9804−9816
|
88 |
Wang S, Chi X, Wei H, Chen Y, Chen Z, Huang S, Chen JL (2014) Influenza A virus-induced degradation of eukaryotic translation initiation factor 4B contributes to viral replication by suppressing IFITM3 protein expression. J Virol 88: 8375−8385
|
89 |
Wei H, Wang S, Chen Q, Chen Y, Chi X, Zhang L, Huang S, Gao GF, Chen JL (2014) Suppression of interferon lambda signaling by SOCS-1 results in their excessive production during influenza virus infection. PLoS Pathog 10: e1003845
|
90 |
Whittaker GR, Digard P (2006) Entry and intracellular transport of influenza virus. In: Kawaoka Y (ed) Influenza virology: current topics. Caister Academic Press, Norfolk
|
91 |
Wise HM, Foeglein A, Sun J, Dalton RM, Patel S, Howard W, Anderson EC, Barclay WS, Digard P (2009) A complicated message: identification of a novel PB1-related protein translated from influenza A virus segment 2 mRNA. J Virol 83: 8021−8031
|
92 |
Yasukawa H, Misawa H, Sakamoto H, Masuhara M, Sasaki A, Wakioka T, Ohtsuka S, Imaizumi T, Matsuda T, Ihle JN
|
93 |
Zebedee SL, Lamb RA (1988) Influenza A virus M2 protein: monoclonal antibody restriction of virus growth and detection of M2 in virions. J Virol 62: 2762−2772
|
94 |
Zhirnov OP, Poyarkov SV, Vorob’eva IV, Safonova OA, Malyshev NA, Klenk HD (2007) Segment NS of influenza A virus contains an additional gene NSP in positive-sense orientation. Doklady Biochem Biophys 414: 127−133
|
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