1887

Journal of General Virology header logo

Volume 102, Issue 10

Interferon responses to norovirus infections: current and future perspectives Open Access

Abstract

Human noroviruses (HuNoVs) are increasingly becoming the main cause of transmissible gastroenteritis worldwide, with hundreds of thousands of deaths recorded annually. Yet, decades after their discovery, there is still no effective treatment or vaccine. Efforts aimed at developing vaccines or treatment will benefit from a greater understanding of norovirus-host interactions, including the host response to infection. In this review, we provide a concise overview of the evidence establishing the significance of type I and type III interferon (IFN) responses in the restriction of noroviruses. We also critically examine our current understanding of the molecular mechanisms of IFN induction in norovirus-infected cells, and outline the diverse strategies deployed by noroviruses to supress and/or avoid host IFN responses. It is our hope that this review will facilitate further discussion and increase interest in this area.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): calicivirus , immune evasion , innate immunity , interferon , MDA5 , norovirus and RIG-I-like receptors
Funding
This study was supported by the:
  • wellcome trust (Award 207498/Z/17/Z)
    • Principle Award Recipient: IanG Goodfellow
© 2021 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.001660
2021-10-26
2024-04-24
Loading full text...

Full text loading...

/deliver/fulltext/jgv/102/10/jgv001660.html?itemId=/content/journal/jgv/10.1099/jgv.0.001660&mimeType=html&fmt=ahah

References

  1. Pires SM, Fischer-Walker CL, Lanata CF, Devleesschauwer B, Hall AJ et al. Aetiology-specific estimates of the global and regional incidence and mortality of diarrhoeal diseases commonly transmitted through food. PLoS One 2015; 10:e0142927 [View Article] [PubMed]
     [Google Scholar]
  2. Lopman BA, Steele D, Kirkwood CD, Parashar UD. The vast and varied global burden of norovirus: prospects for prevention and control. PLOS Med 2016; 13:e1001999 [View Article] [PubMed]
     [Google Scholar]
  3. Bányai K, Estes MK, Martella V, Parashar UD. Viral gastroenteritis. Lancet 2018; 392:175–186 [View Article] [PubMed]
     [Google Scholar]
  4. Glass RI, Parashar UD, Estes MK. Norovirus Gastroenteritis. N Engl J Med 361:1776–1785 [View Article] [PubMed]
     [Google Scholar]
  5. Green KY. Caliciviridae: The Noroviruses. Knipe D, Howley P. eds In Fields Virology, 6th. edn Philadelphia: Lippincott Williams & Wilkins; 2013 pp 582–608
     [Google Scholar]
  6. Walker FC, Baldridge MT. Interactions between noroviruses, the host, and the microbiota. Curr Opin Virol 37:1–9 [View Article] [PubMed]
     [Google Scholar]
  7. Alwin A, Karst SM. The influence of microbiota-derived metabolites on viral infections. Curr Opin Virol 2021; 49:151–156 [View Article] [PubMed]
     [Google Scholar]
  8. Thiel HJ, König M. Caliciviruses: an overview. Vet Microbiol 1999; 69:55–62 [View Article] [PubMed]
     [Google Scholar]
  9. Karst SM, Wobus CE, Goodfellow IG, Green KY, Virgin HW. Advances in norovirus biology. Cell Host Microbe 2014; 15:668–680 [View Article] [PubMed]
     [Google Scholar]
  10. Clarke IN, Lambden PR. Organization and expression of calicivirus genes. J Infect Dis 2000; 181:S309–16 [View Article] [PubMed]
     [Google Scholar]
  11. McFadden N, Bailey D, Carrara G, Benson A, Chaudhry Y et al. Norovirus regulation of the innate immune response and apoptosis occurs via the product of the alternative open reading frame 4. Basler CF, editor. PLoS Pathog 2011; 7:e1002413 [View Article] [PubMed]
     [Google Scholar]
  12. Oka T, Wang Q, Katayama K, Saif LJ. Comprehensive review of human sapoviruses. Clin Microbiol Rev 2015; 28:32–53 [View Article] [PubMed]
     [Google Scholar]
  13. Conley MJ, McElwee M, Azmi L, Gabrielsen M, Byron O et al. Calicivirus VP2 forms a portal-like assembly following receptor engagement. Nature 2019; 565:377–381 [View Article] [PubMed]
     [Google Scholar]
  14. Zhu S, Regev D, Watanabe M, Hickman D, Moussatche N et al. Identification of immune and viral correlates of norovirus protective immunity through comparative study of intra-cluster norovirus strains. PLoS Pathog 2013; 9:e1003592 [View Article] [PubMed]
     [Google Scholar]
  15. Zhu S, Jones MK, Hickman D, Han S, Reeves W et al. Norovirus antagonism of B-cell antigen presentation results in impaired control of acute infection. Mucosal Immunol 2016; 9:1559–1570 [View Article] [PubMed]
     [Google Scholar]
  16. Thorne LG, Goodfellow IG. Norovirus gene expression and replication. J Gen Virol 2014; 95:278–291 [View Article] [PubMed]
     [Google Scholar]
  17. Perry JW, Wobus CE. Endocytosis of murine norovirus 1 into murine macrophages is dependent on dynamin II and cholesterol. J Virol 2010; 84:6163–6176 [View Article] [PubMed]
     [Google Scholar]
  18. Santiana M, Ghosh S, Ho BA, Rajasekaran V, Du W-L et al. Vesicle-cloaked virus clusters are optimal units for inter-organismal viral transmission. Cell Host Microbe 2018; 24:208–220 [View Article] [PubMed]
     [Google Scholar]
  19. Wobus CE, Karst SM, Thackray LB, Chang K-O, Sosnovtsev SV et al. Replication of Norovirus in cell culture reveals a tropism for dendritic cells and macrophages. PLoS Biol 2004; 2:e432 [View Article] [PubMed]
     [Google Scholar]
  20. Haga K, Fujimoto A, Takai-Todaka R, Miki M, Doan YH et al. Functional receptor molecules CD300lf and CD300ld within the CD300 family enable murine noroviruses to infect cells. Proc Natl Acad Sci USA 2016; 113:E6248–55 [View Article]
     [Google Scholar]
  21. Orchard RC, Wilen CB, Doench JG, Baldridge MT, McCune BT et al. Discovery of a proteinaceous cellular receptor for a norovirus. Science 353:933–936 [View Article] [PubMed]
     [Google Scholar]
  22. Grau KR, Roth AN, Zhu S, Hernandez A, Colliou N et al. The major targets of acute norovirus infection are immune cells in the gut-associated lymphoid tissue. Nat Microbiol 2017; 2:1586–1591 [View Article] [PubMed]
     [Google Scholar]
  23. Lee S, Wilen CB, Orvedahl A, McCune BT, Kim KW et al. Norovirus cell tropism is determined by combinatorial action of a viral non-structural protein and host cytokine. Cell Host Microbe 2017; 22:449–459 [View Article] [PubMed]
     [Google Scholar]
  24. Wilen CB, Lee S, Hsieh LL, Orchard RC, Desai C et al. Tropism for tuft cells determines immune promotion of norovirus pathogenesis. Science 2018; 360:204–208 [View Article] [PubMed]
     [Google Scholar]
  25. Jones MK, Watanabe M, Zhu S, Graves CL, Keyes LR et al. Enteric bacteria promote human and mouse norovirus infection of B cells. Science 2014; 346:755–759 [View Article] [PubMed]
     [Google Scholar]
  26. Jones MK, Grau KR, Costantini V, Kolawole AO, de Graaf M et al. Human norovirus culture in B cells. Nat Protoc 2015; 10:1939–1947 [View Article] [PubMed]
     [Google Scholar]
  27. Ettayebi K, Crawford SE, Murakami K, Broughman JR, Karandikar U et al. Replication of human noroviruses in stem cell-derived human enteroids. Science 2016; 353:1387–1393 [View Article] [PubMed]
     [Google Scholar]
  28. Ingle H, Peterson ST, Baldridge MT. Distinct effects of type I and III interferons on enteric viruses. Viruses 2018; 10: [View Article]
     [Google Scholar]
  29. Ivashkiv LB, Donlin LT. Regulation of type I interferon responses. Nat Rev Immunol 2014; 14:36–49 [View Article] [PubMed]
     [Google Scholar]
  30. Lazear HM, Schoggins JW, Diamond MS. Shared and distinct functions of type I and type III interferons. Immunity 2019; 50:907–923 [View Article] [PubMed]
     [Google Scholar]
  31. Hoffmann H-H, Schneider WM, Rice CM. Interferons and viruses: An evolutionary arms race of molecular interactions. Trends Immunol 2015; 36:124–138 [View Article] [PubMed]
     [Google Scholar]
  32. Schneider WM, Chevillotte MD, Rice CM. Interferon-stimulated genes: a complex web of host defenses. Annu Rev Immunol 2014; 32:513–545 [View Article] [PubMed]
     [Google Scholar]
  33. Schoggins JW. Recent advances in antiviral interferon-stimulated gene biology. F1000Res 2018; 7:309 [View Article] [PubMed]
     [Google Scholar]
  34. Fensterl V, Chattopadhyay S, Sen GC. No love lost between viruses and interferons. Annu Rev Virol 2015; 2:549–572 [View Article] [PubMed]
     [Google Scholar]
  35. Rehwinkel J, Gack MU. RIG-I-like receptors: their regulation and roles in RNA sensing. Nat Rev Immunol 2020; 20:537–551 [View Article]
     [Google Scholar]
  36. Carty M, Guy C, Bowie AG. Detection of Viral Infections by Innate Immunity Biochemical Pharmacology. Elsevier Inc; 2021
     [Google Scholar]
  37. Iwasaki A. A virological view of innate immune recognition. Annu Rev Microbiol 2012; 66:177–196 [View Article] [PubMed]
     [Google Scholar]
  38. Gürtler C, Bowie AG. Innate immune detection of microbial nucleic acids. Trends Microbiol 2013; 21:413–420 [View Article] [PubMed]
     [Google Scholar]
  39. Bruns AM, Horvath CM. Antiviral RNA recognition and assembly by RLR family innate immune sensors. Cytokine Growth Factor Rev [Internet 2014; 25:507–512
     [Google Scholar]
  40. Shepardson KM, Schwarz B, Larson K, Morton RV, Avera J et al. duction of antiviral immune response through recognition of the repeating subunit pattern of viral capsids is toll-like receptor 2 depAntiviral Immune Response through Recognition of the Repeating Subunit Pattern of Viral Capsids Is Toll-Like Receptor 2 Dependent. mBio 2017; 8:e01356-17 DOI: DOI: 10.1128/mBio.01356-17 [PubMed]
     [Google Scholar]
  41. Wu J, Chen ZJ. Innate immune sensing and signaling of cytosolic nucleic acids. Annu Rev Immunol 2014; 32:461–488 [View Article] [PubMed]
     [Google Scholar]
  42. Wang P, Zhu S, Yang L, Cui S, Pan W et al. Nlrp6 regulates intestinal antiviral innate immunity. Science 2015; 350:826–830 [View Article] [PubMed]
     [Google Scholar]
  43. Aguirre S, Luthra P, Sanchez-Aparicio MT, Maestre AM, Patel J et al. Dengue virus NS2B protein targets cGAS for degradation and prevents mitochondrial DNA sensing during infection. Nat Microbiol 2017; 2:17037 [View Article] [PubMed]
     [Google Scholar]
  44. Aguirre S, Fernandez-Sesma A. Collateral damage during dengue virus infection: making sense of DNA by cGAS. Gack MU, editor. J Virol 2017; 91: [View Article] [PubMed]
     [Google Scholar]
  45. Aarreberg LD, Esser-Nobis K, Driscoll C, Shuvarikov A, Roby JA et al. Interleukin-1β Induces mtDNA release to activate innate immune signaling via cGAS-STING. Mol Cell 2019; 74:801–815 [View Article] [PubMed]
     [Google Scholar]
  46. McCartney SA, Thackray LB, Gitlin L, Gilfillan S, Virgin HW et al. MDA-5 recognition of a murine norovirus. PLoS Pathog 2008; 4:e1000108 [View Article]
     [Google Scholar]
  47. MacDuff DA, Baldridge MT, Qaqish AM, Nice TJ, Darbandi AD et al. HOIL1 Is Essential for the Induction of Type I and III Interferons by MDA5 and Regulates Persistent Murine Norovirus Infection. Pfeiffer JK, editor. J Virol 2018; 92: [View Article] [PubMed]
     [Google Scholar]
  48. Koltsida O, Hausding M, Stavropoulos A, Koch S, Tzelepis G et al. IL-28A (IFN-λ2) modulates lung DC function to promote Th1 immune skewing and suppress allergic airway disease. EMBO Mol Med 2011; 3:348–361 [View Article] [PubMed]
     [Google Scholar]
  49. Selvakumar TA, Bhushal S, Kalinke U, Wirth D, Hauser H et al. Identification of a Predominantly Interferon-λ-Induced Transcriptional Profile in Murine Intestinal Epithelial Cells. Front Immunol 2017; 8:1302 [View Article] [PubMed]
     [Google Scholar]
  50. Hemann EA, Green R, Turnbull JB, Langlois RA, Savan R et al. Interferon-λ modulates dendritic cells to facilitate T cell immunity during infection with influenza A virus. Nat Immunol 2019; 20:1035–1045 [View Article] [PubMed]
     [Google Scholar]
  51. Karst SM, Wobus CE, Lay M, Davidson J, Virgin HW. STAT1-dependent innate immunity to a norwalk-like virus. Science 2003; 299:1575–1578 [View Article] [PubMed]
     [Google Scholar]
  52. Karst SM. The role of type I interferon in regulating norovirus infections. J Clin Cell Immunol 20111–5
     [Google Scholar]
  53. Pattabhi S, Knoll ML, Gale M, Loo Y-M. DHX15 is a coreceptor for RLR signaling that promotes antiviral defense against RNA virus infection. J Interferon Cytokine Res 2019; 39:331–346 [View Article] [PubMed]
     [Google Scholar]
  54. Subba-Reddy C, Goodfellow I, Kao CC. VPg-primed RNA synthesis of norovirus RNA-dependent RNA polymerases by using a novel cell-based assay. J Virol 2011; 85:13027–13037 [View Article] [PubMed]
     [Google Scholar]
  55. Lee W, Lee S-H, Kim M, Moon J-S, Kim G-W et al. Vibrio vulnificus quorum-sensing molecule cyclo(Phe-Pro) inhibits RIG-I-mediated antiviral innate immunity. Nat Commun 2018; 9:1606 [View Article] [PubMed]
     [Google Scholar]
  56. Guix S, Asanaka M, Katayama K, Crawford SE, Neill FH et al. Norwalk virus RNA is infectious in mammalian cells. J Virol 2007; 81:12238–12248 [View Article] [PubMed]
     [Google Scholar]
  57. Susanna G, Estes MK. Caliciviridae and Astroviridae. Brasier A, García-Sastre A, Lemon S. eds In Cellular Signaling and Innate Immune Responses to RNA Virus Infections, 1st. edn Washington, DC: ASM Press; 2009 pp 389–402
     [Google Scholar]
  58. Arthur SE, Sorgeloos F, Hosmillo M, Goodfellow IG. Epigenetic suppression of interferon lambda receptor expression leads to enhanced human norovirus replication in vitro. MBio 2019; 10: [View Article] [PubMed]
     [Google Scholar]
  59. Sarvestani ST, Cotton B, Fritzlar S, O’Donnell TB, Mackenzie JM. Norovirus infection: replication, manipulation of host, and interaction with the host immune response. J Interf Cytokine Res 2016; 36:215–225 [View Article]
     [Google Scholar]
  60. Zhu Z, Wang G, Yang F, Cao W, Mao R et al. Foot-and-mouth disease virus viroporin 2B antagonizes RIG-I-mediated antiviral effects by inhibition of its protein expression. J Virol 2016; 90:11106–11121 [View Article] [PubMed]
     [Google Scholar]
  61. Li P, Zhang X, Cao W, Yang F, Du X et al. RIG-I is responsible for activation of type I interferon pathway in Seneca Valley virus-infected porcine cells to suppress viral replication. Virol J 2018; 15:162 [View Article] [PubMed]
     [Google Scholar]
  62. Francisco E, Suthar M, Gale M, Rosenfeld AB, Racaniello VR. Cell-type specificity and functional redundancy of RIG-I-like receptors in innate immune sensing of Coxsackievirus B3 and encephalomyocarditis virus. Virology 2019; 528:7–18 [View Article] [PubMed]
     [Google Scholar]
  63. Chhabra P, Ranjan P, Cromeans T, Sambhara S, Vinjé J. Critical role of RIG-I and MDA5 in early and late stages of Tulane virus infection. J Gen Virol 2017; 98:1016–1026 [View Article] [PubMed]
     [Google Scholar]
  64. Dubois H, Sorgeloos F, Sarvestani ST, Martens L, Saeys Y et al. Nlrp3 inflammasome activation and Gasdermin D-driven pyroptosis are immunopathogenic upon gastrointestinal norovirus infection. Baldridge M, editor. PLOS Pathog 2019; 15:e1007709 [View Article] [PubMed]
     [Google Scholar]
  65. Franz KM, Neidermyer WJ, Tan Y-J, Whelan SPJ, Kagan JC. Sting-dependent translation inhibition restricts RNA virus replication. Proc Natl Acad Sci U S A 2018; 115:E2058–E2067 [View Article] [PubMed]
     [Google Scholar]
  66. Ponterio E, Mariotti S, Tabolacci C, Ruggeri FM, Nisini R. Virus like particles of GII.4 norovirus bind Toll Like Receptors 2 and 5. Immunol Lett 2019; 215:40–44 [View Article] [PubMed]
     [Google Scholar]
  67. Thackray L, Duan E, Lazear H, Kambal A, Schreiber R et al. Critical role for interferon regulatory factor 3 (IRF-3) and IRF-7 in type I interferon-mediated control of murine norovirus replication. J Virol 2012; 86:13515–13523 [View Article] [PubMed]
     [Google Scholar]
  68. Baldridge MT, Turula H, Wobus CE. Norovirus regulation by host and microbe. Trends Mol Med 2016; 22:1047–1059 [View Article] [PubMed]
     [Google Scholar]
  69. Khan M, Syed GH, Kim S-J, Siddiqui A. Hepatitis B virus-induced parkin-dependent recruitment of linear ubiquitin assembly complex (LUBAC) to mitochondria and attenuation of innate immunity. PLoS Pathog 2016; 12:e1005693 [View Article] [PubMed]
     [Google Scholar]
  70. Inn K-S, Gack MU, Tokunaga F, Shi M, Wong L-Y et al. Linear ubiquitin assembly complex negatively regulates RIG-I- and TRIM25-Mediated Type I interferon induction. Mol Cell 2011; 41:354–365 [View Article] [PubMed]
     [Google Scholar]
  71. Chattopadhyay S, Kuzmanovic T, Zhang Y, Wetzel JL, Sen GC. Ubiquitination of the Transcription Factor IRF-3 Activates RIPA, the Apoptotic pathway that protects mice from viral pathogenesis. Immunity 2016; 44:1151 [View Article] [PubMed]
     [Google Scholar]
  72. Levenson EA, Martens C, Kanakabandi K, Turner C, Virtaneva K et al. Comparative transcriptomic response of primary and immortalized macrophages to murine norovirus infection. J Immunol 2018; 200:4157–4169 [View Article] [PubMed]
     [Google Scholar]
  73. Lin SC, Qu L, Ettayebi K, Crawford SE, Blutt SE et al. Human norovirus exhibits strain-specific sensitivity to host interferon pathways in human intestinal enteroids. Proc Natl Acad Sci U S A 2020; 117:23782–23793 [View Article] [PubMed]
     [Google Scholar]
  74. Rehwinkel J, Tan CP, Goubau D, Schulz O, Pichlmair A et al. RIG-I detects viral genomic rna during negative-strand rna virus infection. Cell 2010; 140:397–408 [View Article] [PubMed]
     [Google Scholar]
  75. tenOever BR, Sharma S, Zou W, Sun Q, Grandvaux N et al. Activation of TBK1 and IKKε kinases by vesicular stomatitis virus infection and the role of viral ribonucleoprotein in the development of interferon antiviral immunity. J Virol 2004; 78:10636–10649 [View Article] [PubMed]
     [Google Scholar]
  76. Hidmark AS, McInerney GM, Nordström EKL, Douagi I, Werner KM et al. Early alpha/beta interferon production by myeloid dendritic cells in response to UV-inactivated virus requires viral entry and interferon regulatory factor 3 but not MYd88. J Virol 2005; 79:10376–10385 [View Article] [PubMed]
     [Google Scholar]
  77. Yu P, Li Y, Li Y, Miao Z, Wang Y et al. Murine norovirus replicase augments RIG-I-like receptors-mediated antiviral interferon response. Antiviral Res 2020182
     [Google Scholar]
  78. Nikonov A, Mölder T, Sikut R, Kiiver K, Männik A et al. RIG-I and MDA-5 detection of viral RNA-dependent RNA polymerase activity restricts positive-strand RNA virus replication. PLoS Pathog 2013; 9:e1003610 [View Article] [PubMed]
     [Google Scholar]
  79. Malathi K, Dong B, Gale M, Silverman RH. Small self-RNA generated by RNase L amplifies antiviral innate immunity. Nature 2007; 448:816–819 [View Article] [PubMed]
     [Google Scholar]
  80. Samanta M, Iwakiri D, Kanda T, Imaizumi T, Takada K. EB virus-encoded RNAs are recognized by RIG-I and activate signaling to induce type I IFN. EMBO J 2006; 25:4207–4214 [View Article] [PubMed]
     [Google Scholar]
  81. Plumet S, Herschke F, Bourhis J-M, Valentin H, Longhi S et al. Cytosolic 5’-triphosphate ended viral leader transcript of measles virus as activator of the RIG I-mediated interferon response. PLoS One 2007; 2:e279 [View Article] [PubMed]
     [Google Scholar]
  82. Luthra P, Sun D, Silverman RH, He B. Activation of IFN-β expression by a viral mRNA through RNase L and MDA5. Proc Natl Acad Sci U S A 2011; 108:2118–2123 [View Article] [PubMed]
     [Google Scholar]
  83. Changotra H, Jia Y, Moore TN, Liu G, Kahan SM et al. Type I and type II interferons inhibit the translation of murine norovirus proteins. J Virol 2009; 83:5683–5692 [View Article] [PubMed]
     [Google Scholar]
  84. Emmott E, Sorgeloos F, Caddy SL, Vashist S, Sosnovtsev S et al. Norovirus-mediated modification of the translational landscape via virus and host-induced cleavage of translation initiation factors. Mol Cell Proteomics 2017; 16:S215–29 [View Article] [PubMed]
     [Google Scholar]
  85. Baldridge MT, Lee S, Brown JJ, McAllister N, Urbanek K et al. Expression of Ifnlr1 on intestinal epithelial cells is critical to the antiviral effects of interferon lambda against norovirus and reovirus. J Virol 2017; 91: [View Article] [PubMed]
     [Google Scholar]
  86. Mumphrey SM, Changotra H, Moore TN, Heimann-Nichols ER, Wobus CE et al. Murine norovirus 1 infection is associated with histopathological changes in immunocompetent hosts, but clinical disease is prevented by STAT1-dependent interferon responses. J Virol 2007; 81:3251–3263 [View Article] [PubMed]
     [Google Scholar]
  87. Niendorf S, Klemm U, Mas Marques A, Bock C-T, Höhne M. Infection with the persistent murine norovirus strain MNV-S99 Suppresses IFN-beta release and activation of stat1 In Vitro. PLoS One 2016; 11:e0156898 [View Article] [PubMed]
     [Google Scholar]
  88. Borg C, Jahun AS, Thorne L, Sorgeloos F, Bailey D et al. Murine norovirus virulence factor 1 (vf1) protein contributes to viral fitness during persistent infection. bioRxiv 2019646281 [View Article]
     [Google Scholar]
  89. Nice TJ, Baldridge MT, McCune BT, Norman JM, Lazear HM et al. Interferon-λ cures persistent murine norovirus infection in the absence of adaptive immunity. Science 2015; 347:269–273 [View Article] [PubMed]
     [Google Scholar]
  90. Qu L, Murakami K, Broughman JR, Lay MK, Guix S et al. Replication of human norovirus RNA in mammalian cells reveals lack of interferon response. J Virol 2016; 90:8906–8923 [View Article] [PubMed]
     [Google Scholar]
  91. Newman KL, Moe CL, Kirby AE, Flanders WD, Parkos CA et al. Human norovirus infection and the acute serum cytokine response. Clin Exp Immunol 2015; 182:195–203 [View Article] [PubMed]
     [Google Scholar]
  92. Cutler AJ, Waldron-Lynch F, Oliveira J, Ferreira RC, Challis B et al. Capturing the systemic immune signature of a norovirus infection: An n-of-1 case study within a clinical trial. Wellcome Open Res 2017; 2:28 [View Article] [PubMed]
     [Google Scholar]
  93. Souza M, Cheetham SM, Azevedo MSP, Costantini V, Saif LJ. Cytokine and antibody responses in gnotobiotic pigs after infection with human norovirus genogroup II.4 (HS66 Strain. J Virol 2007; 81:9183–9192 [View Article] [PubMed]
     [Google Scholar]
  94. Hosmillo M, Chaudhry Y, Nayak K, Sorgeloos F, Koo BK et al. Norovirus replication in human intestinal epithelial cells is restricted by the interferon-induced JAK/STAT signaling pathway and rna polymerase ii-mediated transcriptional responses. mBio 2020; 11: [View Article] [PubMed]
     [Google Scholar]
  95. Lin L, Han J, Yan T, Li L, Li J et al. Replication and transcriptionomic analysis of human noroviruses in human intestinal enteroids. Am J Transl Res 2019; 11:3365–3374 [PubMed]
     [Google Scholar]
  96. Odendall C, Dixit E, Stavru F, Bierne H, Franz KM et al. Diverse intracellular pathogens activate type III interferon expression from peroxisomes. Nat Immunol 2014; 15:717–726 [View Article] [PubMed]
     [Google Scholar]
  97. Rocha-Pereira J, Jacobs S, Noppen S, Verbeken E, Michiels T et al. Interferon lambda (IFN-λ) efficiently blocks norovirus transmission in a mouse model. Antiviral Res 2018; 149:7–15 [View Article] [PubMed]
     [Google Scholar]
  98. Nice TJ, Osborne LC, Tomov VT, Artis D, Wherry EJ et al. Type I Interferon receptor deficiency in dendritic cells facilitates systemic murine norovirus persistence despite enhanced adaptive immunity. PLoS Pathog 2016; 12:e1005684 [View Article] [PubMed]
     [Google Scholar]
  99. Rodriguez MR, Monte K, Thackray LB, Lenschow DJ. ISG15 functions as an interferon-mediated antiviral effector early in the murine norovirus life cycle. J Virol 2014; 88:9277–9286 [View Article] [PubMed]
     [Google Scholar]
  100. Ng YC, Kim YW, Lee J-S, Lee SJ, Jung Song M. Antiviral activity of Schizonepeta tenuifolia briquet against noroviruses via induction of antiviral interferons. J Microbiol 2018; 56:683–689 [View Article] [PubMed]
     [Google Scholar]
  101. Enosi Tuipulotu D, Netzler NE, Lun JH, Mackenzie JM, White PA. TLR7 agonists display potent antiviral effects against norovirus infection via innate stimulation. Antimicrob Agents Chemother 2018; 62: [View Article] [PubMed]
     [Google Scholar]
  102. Jung K, Wang Q, Kim Y, Scheuer K, Zhang Z et al. The effects of simvastatin or interferon-α on infectivity of human norovirus using a gnotobiotic pig model for the study of antivirals. PLoS One 2012; 7:e41619 [View Article]
     [Google Scholar]
  103. Chang K-O, Sosnovtsev SV, Belliot G, King AD, Green KY. Stable expression of a Norwalk virus RNA replicon in a human hepatoma cell line. Virology 2006; 353:463–473 [View Article] [PubMed]
     [Google Scholar]
  104. Chang K-O, George DW. Interferons and ribavirin effectively inhibit Norwalk virus replication in replicon-bearing cells. J Virol 2007; 81:12111–12118 [View Article] [PubMed]
     [Google Scholar]
  105. Dang W, Xu L, Yin Y, Chen S, Wang W et al. IRF-1, RIG-I and MDA5 display potent antiviral activities against norovirus coordinately induced by different types of interferons. Antiviral Res 2018; 155:48–59 [View Article] [PubMed]
     [Google Scholar]
  106. MMH L, MacDonald MR, Rice CM. To translate, or not to translate: viral and host mRNA regulation by interferon-stimulated genes. Trends Cell Biol 2015; 25:320–329 [View Article] [PubMed]
     [Google Scholar]
  107. Orchard RC, Sullender ME, Dunlap BF, Balce DR, Doench JG et al. Identification of antinorovirus genes in human cells using genome-wide CRISPR activation screening. J Virol 2018; 93: [View Article] [PubMed]
     [Google Scholar]
  108. Mears H, Emmott E, Chaudhry Y, Hosmillo M, Goodfellow IG. Sweeney TR. Ifit1 regulates norovirus infection and enhances the interferon response in murine macrophage-like cells [version 1; peer review: 1 approved, 2 approved with reservations. Wellcome Open Res 2019; 4:
     [Google Scholar]
  109. Nice TJ, Strong DW, McCune BT, Pohl CS, Virgin HW. A single-amino-acid change in murine norovirus NS1/2 is sufficient for colonic tropism and persistence. J Virol 2013; 87:327–334 [View Article] [PubMed]
     [Google Scholar]
  110. Borin BN, Tang W, Nice TJ, McCune BT, Virgin HW et al. Murine norovirus protein NS1/2 aspartate to glutamate mutation, sufficient for persistence, reorients side chain of surface exposed tryptophan within a novel structured domain. Proteins Struct Funct Bioinforma 2014; 82:1200–1209 [View Article]
     [Google Scholar]
  111. Nice TJ, Robinson BA, Van Winkle JA. The role of interferon in persistent viral infection: insights from murine norovirus. Trends Microbiol 2018; 26:510–524 [View Article] [PubMed]
     [Google Scholar]
  112. Mahlakõiv T, Hernandez P, Gronke K, Diefenbach A, Staeheli P. Leukocyte-derived IFN-α/β and epithelial IFN-λ constitute a compartmentalized mucosal defense system that restricts enteric virus infections. Greenberg HB, editor. PLoS Pathog 2015; 11:e1004782 [View Article] [PubMed]
     [Google Scholar]
  113. Lee S, Liu H, Wilen CB, Sychev ZE, Desai C et al. A secreted viral nonstructural protein determines intestinal norovirus pathogenesis. Cell Host Microbe 2019; 25:845–857 [View Article]
     [Google Scholar]
  114. Kuyumcu-Martinez M, Belliot G, Sosnovtsev SV, Chang K-O, Green KY et al. Calicivirus 3C-like proteinase inhibits cellular translation by cleavage of poly(A)-binding protein. J Virol 2004; 78:8172–8182 [View Article] [PubMed]
     [Google Scholar]
  115. Chaudhry Y, Nayak A, Bordeleau M-E, Tanaka J, Pelletier J et al. Caliciviruses differ in their functional requirements for EIF4F components. J Biol Chem 2006; 281:25315–25325 [View Article] [PubMed]
     [Google Scholar]
  116. Chung L, Bailey D, Leen EN, Emmott EP, Chaudhry Y et al. Norovirus translation requires an interaction between the C Terminus of the genome-linked viral protein VPg and eukaryotic translation initiation factor 4G. J Biol Chem 2014; 289:21738–21750 [View Article] [PubMed]
     [Google Scholar]
  117. Fritzlar S, Aktepe TE, Chao YW, Kenney ND, McAllaster MR et al. Mouse norovirus infection arrests host cell translation uncoupled from the stress granule-PKR-eIF2α Axis. MBio 2019; 10: [View Article] [PubMed]
     [Google Scholar]
  118. Hosmillo M, Lu J, McAllaster MR, Eaglesham JB, Wang X et al. Noroviruses subvert the core stress granule component G3BP1 to promote viral VPg-dependent translation. Elife 2019; 8: [View Article] [PubMed]
     [Google Scholar]
  119. Brocard M, Iadevaia V, Klein P, Hall B, Lewis G et al. Norovirus infection results in eIF2α independent host translation shut-off and remodels the G3BP1 interactome evading stress granule formation. PLoS Pathog 2020; 16:e1008250 [View Article] [PubMed]
     [Google Scholar]
  120. Bidet K, Dadlani D, Garcia-Blanco MA. G3BP1, G3BP2 and CAPRIN1 are required for translation of interferon stimulated mRNAs and are targeted by a dengue virus non-coding RNA. PLoS Pathog 2014; 10:e1004242 [View Article] [PubMed]
     [Google Scholar]
  121. Bidet K, Dadlani D, Garcia-Blanco MA. Correction: G3BP1, G3BP2 and CAPRIN1 are required for translation of interferon stimulated mRNAs and are targeted by a dengue virus non-coding RNA. PLOS Pathog 2017; 13:e1006295 [View Article] [PubMed]
     [Google Scholar]
  122. Alam U, Kennedy D. G3BP1 and G3BP2 regulate translation of interferon-stimulated genes: IFITM1, IFITM2 and IFITM3 in the cancer cell line MCF7. Mol Cell Biochem 2019; 459:189–204 [View Article] [PubMed]
     [Google Scholar]
  123. Fernandez-Vega V, Sosnovtsev S, Belliot G, King AD, Mitra T et al. Norwalk Virus N-terminal nonstructural protein is associated with disassembly of the golgi complex in transfected cells. J Virol 2004; 78:4827–4837 [View Article] [PubMed]
     [Google Scholar]
  124. Ettayebi K, Hardy ME. Norwalk virus nonstructural protein p48 forms a complex with the SNARE regulator VAP-A and prevents cell surface expression of vesicular stomatitis virus G protein. J Virol 2003; 77:11790–11797 [View Article] [PubMed]
     [Google Scholar]
  125. Sharp TM, Guix S, Katayama K, Crawford SE, Estes MK. Inhibition of cellular protein secretion by norwalk virus nonstructural protein p22 requires a mimic of an endoplasmic reticulum export signal. PLoS One 2010; 5:e13130 [View Article] [PubMed]
     [Google Scholar]
  126. Sharp TM, Crawford SE, Ajami NJ, Neill FH, Atmar RL et al. Secretory pathway antagonism by calicivirus homologues of Norwalk virus nonstructural protein p22 is restricted to noroviruses. Virol J 2012; 9:181 [View Article] [PubMed]
     [Google Scholar]
  127. McCune BT, Tang W, Lu J, Eaglesham JB, Thorne L et al. Noroviruses co-opt the function of host proteins VAPA and VAPB for replication via a phenylalanine-phenylalanine-acidic-tract-motif mimic in nonstructural viral protein NS1/2. mBio 2017; 8: [View Article] [PubMed]
     [Google Scholar]
  128. Roth AN, Karst SM. Norovirus mechanisms of immune antagonism. Curr Opin Virol 2015; 16:24–30 [View Article] [PubMed]
     [Google Scholar]
  129. Chiang H-S, Zhao Y, Song J-H, Liu S, Wang N et al. GEF-H1 controls microtubule-dependent sensing of nucleic acids for antiviral host defenses. Nat Immunol 2014; 15:63–71 [View Article] [PubMed]
     [Google Scholar]
  130. Fritzlar S, White PA, Mackenzie JM. The microtubule-associated innate immune sensor GEF-H1 does not influence mouse norovirus replication in murine macrophages. Viruses 2019; 11:47 [View Article]
     [Google Scholar]
  131. Souza M, Azevedo MSP, Jung K, Cheetham S, Saif LJ. Pathogenesis and immune responses in gnotobiotic calves after infection with the genogroup II.4-HS66 strain of human norovirus. J Virol 2008; 82:1777–1786 [View Article] [PubMed]
     [Google Scholar]
  132. Van Dycke J, Ny A, Conceição-Neto N, Maes J, Hosmillo M et al. A robust human norovirus replication model in zebrafish larvae. Suthar M, editor. PLoS Pathog 2019; 15:e1008009 [View Article] [PubMed]
     [Google Scholar]
  133. Robinson BA, Van Winkle JA, McCune BT, Peters AM, Nice TJ. Caspase-mediated cleavage of murine norovirus ns1/2 potentiates apoptosis and is required for persistent infection of intestinal epithelial cells. PLOS Pathog 2019; 15: [View Article]
     [Google Scholar]
  134. Yu P, Li Y, Li Y, Miao Z, Peppelenbosch MP et al. Guanylate-binding protein 2 orchestrates innate immune responses against murine norovirus and is antagonized by the viral protein NS7. J Biol Chem 2020; 295:8036–8047 [View Article]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.001660
Loading
Interferon responses to norovirus infections: current and future perspectives
J. Gen. Virol. 102, 001660 (2021); https://doi.org/10.1099/jgv.0.001660
/content/journal/jgv/10.1099/jgv.0.001660
/content/journal/jgv/10.1099/jgv.0.001660
Loading

Data & Media loading...

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error