Replication of human norovirus RNA in mammalian cells reveals lack of interferon response

Journal of Virology

Volumn 90, Issue 19, 2016, Pages 8906-8923

  Qu, Lin ^a   Murakami, Kosuke ^a   Broughman, James R ^a   Lay, Margarita K ^a   Guix, Susana ^a   Tenge, Victoria R ^a   Atmar, Robert L ^a   Estes, Mary K ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; ALPHA INTERFERON RECEPTOR; ALPHA INTERFERON RECEPTOR 2; BETA INTERFERON; DOUBLE STRANDED RNA; INTERFERON REGULATORY FACTOR 3; INTERLEUKIN 10 RECEPTOR; INTERLEUKIN 10 RECEPTOR 1; INTERLEUKIN 29; NEUTRALIZING ANTIBODY; ORF1 PROTEIN; ORF2 PROTEIN; POL PROTEIN; POLYPROTEIN; PROTEIN P35; PROTEIN VP1; SHORT HAIRPIN RNA; TOLL LIKE RECEPTOR 3; UNCLASSIFIED DRUG; ANTIVIRUS AGENT; IL29 PROTEIN, HUMAN; INTERFERON; INTERLEUKIN DERIVATIVE; VIRUS RNA;

AMINO ACID SEQUENCE; ARTICLE; CONTROLLED STUDY; HUMAN; HUMAN CELL; NONHUMAN; NOROVIRUS; NUCLEAR LOCALIZATION SIGNAL; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN INDUCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS; RNA REPLICATION; SIGNAL TRANSDUCTION; TRANSLATION INITIATION; VIRUS ENTRY; VIRUS NEUTRALIZATION; CELL LINE; EPITHELIUM CELL; IMMUNE EVASION; IMMUNOLOGY; METABOLISM; PHYSIOLOGY; VIROLOGY; VIRUS REPLICATION;

ANTIVIRAL AGENTS; CELL LINE; EPITHELIAL CELLS; HUMANS; IMMUNE EVASION; INTERFERON TYPE I; INTERLEUKINS; NOROVIRUS; RNA, VIRAL; VIRUS REPLICATION;

EID: 84990249361     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01425-16     Document Type: Article

References (72)

1. Ramani S, Atmar RL, Estes MK. 2014. Epidemiology of human noroviruses and updates on vaccine development. Curr Opin Gastroenterol 30: 25-33. http://dx.doi.org/10.1097/MOG.0000000000000022
2. Payne DC, Vinje J, Szilagyi PG, Edwards KM, Staat MA, Weinberg GA, Hall CB, Chappell J, Bernstein DI, Curns AT, Wikswo M, Shirley SH, Hall AJ, Lopman B, Parashar UD. 2013. Norovirus and medically attended gastroenteritis in U.S. children. NEngl J Med 368:1121-1130. http://dx.doi.org/10.1056/NEJMsa1206589
3. Koo HL, Neill FH, Estes MK, Munoz FM, Cameron A, Dupont HL, Atmar RL. 2013. Noroviruses: the most common pediatric viral enteric pathogen at a large university hospital after introduction of rotavirus vaccination. J Pediatric Infect Dis Soc 2:57-60. http://dx.doi.org/10.1093/jpids/pis070
4. Glass RI, Parashar UD, Estes MK. 2009. Norovirus gastroenteritis. N Engl J Med 361:1776-1785. http://dx.doi.org/10.1056/NEJMra0804575
5. Noel JS, Fankhauser RL, Ando T, Monroe SS, Glass RI. 1999. Identification of a distinct common strain of "Norwalk-like viruses" having a global distribution. J Infect Dis 179:1334-1344. http://dx.doi.org/10.1086/314783
6. Leshem E, Wikswo M, Barclay L, Brandt E, Storm W, Salehi E, DeSalvo T, Davis T, Saupe A, Dobbins G, Booth HA, Biggs C, Garman K, Woron AM, Parashar UD, Vinje J, Hall AJ. 2013. Effects and clinical significance of GII.4 Sydney norovirus, United States, 2012-2013. Emerg Infect Dis 19:1231-1238. http://dx.doi.org/10.3201/eid1908.130458
7. Chan MC, Lee N, Hung TN, Kwok K, Cheung K, Tin EK, Lai RW, Nelson EA, Leung TF, Chan PK. 2015. Rapid emergence and predominance of a broadly recognizing and fast-evolving norovirus GII.17 variant in late 2014. Nat Commun 6:10061. http://dx.doi.org/10.1038/ncomms10061
8. de Graaf M, van Beek J, Vennema H, Podkolzin AT, Hewitt J, Bucardo F, Templeton K, Mans J, Nordgren J, Reuter G, Lynch M, Rasmussen LD, Iritani N, Chan MC, Martella V, Ambert-Balay K, Vinje J, White PA, Koopmans MP. 2015. Emergence of a novel GII.17 norovirus-end of the GII.4 era? Euro Surveill 20(26):pii 21178. http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId21178
9. Kavanagh O, Estes MK, Reeck A, Raju RM, Opekun AR, Gilger MA, Graham DY, Atmar RL. 2011. Serological responses to experimental Norwalk virus infection measured using a quantitative duplex timeresolved fluorescence immunoassay. Clin Vaccine Immunol 18:1187-1190. http://dx.doi.org/10.1128/CVI.00039-11
10. Czako R, Atmar RL, Opekun AR, Gilger MA, Graham DY, Estes MK. 2012. Serum hemagglutination inhibition activity correlates with protection from gastroenteritis in persons infected with Norwalk virus. Clin Vaccine Immunol 19:284-287. http://dx.doi.org/10.1128/CVI.05592-11
11. Ajami NJ, Barry MA, Carrillo B, Muhaxhiri Z, Neill FH, Prasad BV, Opekun AR, Gilger MA, Graham DY, Atmar RL, Estes MK. 2012. Antibody responses to norovirus genogroup GI.1 and GII.4 proteases in volunteers administered Norwalk virus. Clin Vaccine Immunol 19:1980-1983. http://dx.doi.org/10.1128/CVI.00411-12
12. Souza M, Cheetham SM, Azevedo MS, Costantini V, Saif LJ. 2007. Cytokine and antibody responses in gnotobiotic pigs after infection with human norovirus genogroup II.4 (HS66 strain). J Virol 81:9183-9192. http://dx.doi.org/10.1128/JVI.00558-07
13. Souza M, Azevedo MS, Jung K, Cheetham S, Saif LJ. 2008. Pathogenesis and immune responses in gnotobiotic calves after infection with the genogroup II.4-HS66 strain of human norovirus. J Virol 82:1777-1786. http://dx.doi.org/10.1128/JVI.01347-07
14. Karst SM, Wobus CE, Lay M, Davidson J, Virgin HW, 4th. 2003. STAT1-dependent innate immunity to a Norwalk-like virus. Science 299: 1575-1578. http://dx.doi.org/10.1126/science.1077905
15. Wobus CE, Karst SM, Thackray LB, Chang KO, Sosnovtsev SV, Belliot G, Krug A, Mackenzie JM, Green KY, Virgin HW. 2004. Replication of Norovirus in cell culture reveals a tropism for dendritic cells and macrophages. PLoS Biol 2:e432. http://dx.doi.org/10.1371/journal.pbio.0020432
16. Lay MK, Atmar RL, Guix S, Bharadwaj U, He H, Neill FH, Sastry KJ, Yao Q, Estes MK. 2010. Norwalk virus does not replicate in human macrophages or dendritic cells derived from the peripheral blood of susceptible humans. Virology 406:1-11. http://dx.doi.org/10.1016/j.virol.2010.07.001
17. Jones MK, Watanabe M, Zhu S, Graves CL, Keyes LR, Grau KR, Gonzalez-Hernandez MB, Iovine NM, Wobus CE, Vinje J, Tibbetts SA, Wallet SM, Karst SM. 2014. Enteric bacteria promote human and mouse norovirus infection of B cells. Science 346:755-759. http://dx.doi.org/10.1126/science.1257147
18. Taube S, Kolawole AO, Hohne M, Wilkinson JE, Handley SA, Perry JW, Thackray LB, Akkina R, Wobus CE. 2013. A mouse model for human norovirus. mBio 4:e00450-13
19. Karandikar UC, Crawford SE, Ajami NJ, Murakami K, Kou B, Ettayebi K, Papanicolaou GA, Jongwutiwes U, Perales MA, Shia J, Mercer D, Finegold MJ, Vinje J, Atmar RL, Estes MK. 12 July 2016. Detection of human norovirus in intestinal biopsies from immunocompromised transplant patients. J Gen Virol http://dx.doi.org/10.1099/jgv.0.000545
20. Alhatlani B, Vashist S, Goodfellow I. 2015. Functions of the 5= and 3= ends of calicivirus genomes. Virus Res 206:134-143. http://dx.doi.org/10.1016/j.virusres.2015.02.002
21. Glass PJ, White LJ, Ball JM, Leparc-Goffart I, Hardy ME, Estes MK. 2000. Norwalk virus open reading frame 3 encodes a minor structural protein. J Virol 74:6581-6591. http://dx.doi.org/10.1128/JVI.74.14.6581-6591.2000
22. Jiang X, Wang M, Wang K, Estes MK. 1993. Sequence and genomic organization of Norwalk virus. Virology 195:51-61. http://dx.doi.org/10.1006/viro.1993.1345
23. Vongpunsawad S, Venkataram Prasad BV, Estes MK. 2013. Norwalk virus minor capsid protein VP2 associates within the VP1 shell domain. J Virol 87:4818-4825. http://dx.doi.org/10.1128/JVI.03508-12
24. Thorne LG, Goodfellow IG. 2014. Norovirus gene expression and replication. J Gen Virol 95:278-291. http://dx.doi.org/10.1099/vir.0.059634-0
25. Kawai T, Akira S. 2007. Antiviral signaling through pattern recognition receptors. J Biochem 141:137-145
26. Akira S, Uematsu S, Takeuchi O. 2006. Pathogen recognition and innate immunity. Cell 124:783-801. http://dx.doi.org/10.1016/j.cell.2006.02.015
27. Rauch I, Muller M, Decker T. 2013. The regulation of inflammation by interferons and their STATs. JAKSTAT 2:e23820. http://dx.doi.org/10.4161/jkst.23820
28. de Weerd NA, Nguyen T. 2012. The interferons and their receptors-distribution and regulation. Immunol Cell Biol 90:483-491. http://dx.doi.org/10.1038/icb.2012.9
29. Thackray LB, Duan E, Lazear HM, Kambal A, Schreiber RD, Diamond MS, Virgin HW. 2012. Critical role for interferon regulatory factor 3 (IRF-3) and IRF-7 in type I interferon-mediated control of murine norovirus replication. J Virol 86:13515-13523. http://dx.doi.org/10.1128/JVI.01824-12
30. McCartney SA, Thackray LB, Gitlin L, Gilfillan S, Virgin HW, Colonna M. 2008. MDA-5 recognition of a murine norovirus. PLoS Pathog 4:e1000108. http://dx.doi.org/10.1371/journal.ppat.1000108
31. Baldridge MT, Nice TJ, McCune BT, Yokoyama CC, Kambal A, Wheadon M, Diamond MS, Ivanova Y, Artyomov M, Virgin HW. 2015. Commensal microbes and interferon-lambda determine persistence of enteric murine norovirus infection. Science 347:266-269. http://dx.doi.org/10.1126/science.1258025
32. Nice TJ, Baldridge MT, McCune BT, Norman JM, Lazear HM, Artyomov M, Diamond MS, Virgin HW. 2015. Interferon-lambda cures persistent murine norovirus infection in the absence of adaptive immunity. Science 347:269-273. http://dx.doi.org/10.1126/science.1258100
33. Guix S, Asanaka M, Katayama K, Crawford SE, Neill FH, Atmar RL, Estes MK. 2007. Norwalk virus RNA is infectious in mammalian cells. J Virol 81:12238-12248. http://dx.doi.org/10.1128/JVI.01489-07
34. Katayama K, Murakami K, Sharp TM, Guix S, Oka T, Takai-Todaka R, Nakanishi A, Crawford SE, Atmar RL, Estes MK. 2014. Plasmidbased human norovirus reverse genetics system produces reportertagged progeny virus containing infectious genomic RNA. Proc Natl Acad Sci U S A 111:E4043-4052. http://dx.doi.org/10.1073/pnas.1415096111
35. Atmar RL, Opekun AR, Gilger MA, Estes MK, Crawford SE, Neill FH, Ramani S, Hill H, Ferreira J, Graham DY. 2014. Determination of the 50% human infectious dose for Norwalk virus. J Infect Dis 209:1016-1022. http://dx.doi.org/10.1093/infdis/jit620
36. Atmar RL, Opekun AR, Gilger MA, Estes MK, Crawford SE, Neill FH, Graham DY. 2008. Norwalk virus shedding after experimental human infection. Emerg Infect Dis 14:1553-1557. http://dx.doi.org/10.3201/eid1410.080117
37. Asanaka M, Atmar RL, Ruvolo V, Crawford SE, Neill FH, Estes MK. 2005. Replication and packaging of Norwalk virus RNA in cultured mammalian cells. Proc Natl Acad Sci U S A 102:10327-10332. http://dx.doi.org/10.1073/pnas.0408529102
38. Jiang X, Wang M, Graham DY, Estes MK. 1992. Expression, selfassembly, and antigenicity of the Norwalk virus capsid protein. J Virol 66:6527-6532
39. Sharp TM. 2010. Norwalk virus nonstructural protein p22 is a novel inhibitor of cellular protein secretion. PhD dissertation. Baylor College of Medicine, Houston, TX
40. Kou B, Crawford SE, Ajami NJ, Czako R, Neill FH, Tanaka TN, Kitamoto N, Palzkill TG, Estes MK, Atmar RL. 2015. Characterization of cross-reactive norovirus-specific monoclonal antibodies. Clin Vaccine Immunol 22:160-167. http://dx.doi.org/10.1128/CVI.00519-14
41. Qu L, Vongpunsawad S, Atmar RL, Prasad BV, Estes MK. 2014. Development of a Gaussia luciferase-based human norovirus protease reporter system: cell type-specific profile of Norwalk virus protease precursors and evaluation of inhibitors. J Virol 88:10312-10326. http://dx.doi.org/10.1128/JVI.01111-14
42. Li K, Chen Z, Kato N, Gale M, Jr, Lemon SM. 2005. Distinct poly(I-C) and virus-activated signaling pathways leading to interferon-beta production in hepatocytes. J Biol Chem 280:16739-16747. http://dx.doi.org/10.1074/jbc. M414139200
43. Qu L, Feng Z, Yamane D, Liang Y, Lanford RE, Li K, Lemon SM. 2011. Disruption of TLR3 signaling due to cleavage of TRIF by the hepatitis A virus protease-polymerase processing intermediate, 3CD. PLoS Pathog 7:e1002169. http://dx.doi.org/10.1371/journal.ppat.1002169
44. Rohayem J, Robel I, Jager K, Scheffler U, Rudolph W. 2006. Proteinprimed and de novo initiation of RNA synthesis by norovirus 3Dpol. J Virol 80:7060-7069. http://dx.doi.org/10.1128/JVI.02195-05
45. McCormick CJ, Salim O, Lambden PR, Clarke IN. 2008. Translation termination reinitiation between open reading frame 1 (ORF1) and ORF2 enables capsid expression in a bovine norovirus without the need for production of viral subgenomic RNA. J Virol 82:8917-8921. http://dx.doi.org/10.1128/JVI.02362-07
46. Noyce RS, Taylor K, Ciechonska M, Collins SE, Duncan R, Mossman KL. 2011. Membrane perturbation elicits an IRF3-dependent, interferonindependent antiviral response. J Virol 85:10926-10931. http://dx.doi.org/10.1128/JVI.00862-11
47. Kim MJ, Latham AG, Krug RM. 2002. Human influenza viruses activate an interferon-independent transcription of cellular antiviral genes: outcome with influenzaAvirus is unique. Proc Natl Acad SciUSA99:10096-10101 http://dx.doi.org/10.1073/pnas.152327499
48. Brownell J, Bruckner J, Wagoner J, Thomas E, Loo YM, Gale M, Jr, Liang TJ, Polyak SJ. 2014. Direct, interferon-independent activation of the CXCL10 promoter by NF-κB and interferon regulatory factor 3 during hepatitis C virus infection. J Virol 88:1582-1590. http://dx.doi.org/10.1128/JVI.02007-13
49. Colamonici OR, Domanski P, Sweitzer SM, Larner A, Buller RM. 1995. Vaccinia virus B18R gene encodes a type I interferon-binding protein that blocks interferon alpha transmembrane signaling. J Biol Chem 270: 15974-15978. http://dx.doi.org/10.1074/jbc.270.27.15974
50. Weber F, Wagner V, Rasmussen SB, Hartmann R, Paludan SR. 2006. Double-stranded RNA is produced by positive-strand RNA viruses and DNA viruses but not in detectable amounts by negative-strand RNA viruses. J Virol 80:5059-5064. http://dx.doi.org/10.1128/JVI.80.10.5059-5064.2006
51. Fernandez-Vega V, Sosnovtsev SV, Belliot G, King AD, Mitra T, Gorbalenya A, Green KY. 2004. Norwalk virus N-terminal nonstructural protein is associated with disassembly of the Golgi complex in transfected cells. J Virol 78:4827-4837. http://dx.doi.org/10.1128/JVI.78.9.4827-4837.2004
52. Ettayebi K, Hardy ME. 2003. 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 77:11790-11797 http://dx.doi.org/10.1128/JVI.77.21.11790-11797.2003
53. Yang Y, Liang Y, Qu L, Chen Z, Yi M, Li K, Lemon SM. 2007. Disruption of innate immunity due to mitochondrial targeting of a picornaviral protease precursor. Proc Natl Acad Sci U S A 104:7253-7258. http://dx.doi.org/10.1073/pnas.0611506104
54. Hidmark AS, McInerney GM, Nordstrom EK, Douagi I, Werner KM, Liljestrom P, Karlsson Hedestam GB. 2005. 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 79:10376-10385. http://dx.doi.org/10.1128/JVI.79.16.10376-10385.2005
55. Hare DN, Collins SE, Mukherjee S, Loo YM, Gale M, Jr, Janssen LJ, Mossman KL. 2016. Membrane perturbation-associated Ca2+ signaling and incoming genome sensing are required for the host response to lowlevel enveloped virus particle entry. J Virol 90:3018-3027. http://dx.doi.org/10.1128/JVI.02642-15
56. Spiegel M, Weber F. 2006. Inhibition of cytokine gene expression and induction of chemokine genes in non-lymphatic cells infected with SARS coronavirus. Virol J 3:17. http://dx.doi.org/10.1186/1743-422X-3-17
57. Chang KO, George DW. 2007. Interferons and ribavirin effectively inhibit Norwalk virus replication in replicon-bearing cells. J Virol 81:12111-12118 http://dx.doi.org/10.1128/JVI.00560-07
58. Chang KO, Sosnovtsev SV, Belliot G, King AD, Green KY. 2006. Stable expression of a Norwalk virus RNA replicon in a human hepatoma cell line. Virology 353:463-473. http://dx.doi.org/10.1016/j.virol.2006.06.006
59. Changotra H, Jia Y, Moore TN, Liu G, Kahan SM, Sosnovtsev SV, Karst SM. 2009. Type I and type II interferons inhibit the translation of murine norovirus proteins. J Virol 83:5683-5692. http://dx.doi.org/10.1128/JVI.00231-09
60. Lindesmith L, Moe C, Lependu J, Frelinger JA, Treanor J, Baric RS. 2005. Cellular and humoral immunity following Snow Mountain virus challenge. J Virol 79:2900-2909. http://dx.doi.org/10.1128/JVI.79.5.2900-2909.2005
61. Gonzalez-Hernandez MB, Liu T, Blanco LP, Auble H, Payne HC, Wobus CE. 2013. Murine norovirus transcytosis across an in vitro polarized murine intestinal epithelial monolayer is mediated by M-like cells. J Virol 87:12685-12693. http://dx.doi.org/10.1128/JVI.02378-13
62. Gonzalez-Hernandez MB, Liu T, Payne HC, Stencel-Baerenwald JE, Ikizler M, Yagita H, Dermody TS, Williams IR, Wobus CE. 2014. Efficient norovirus and reovirus replication in the mouse intestine requires microfold (M) cells. J Virol 88:6934-6943. http://dx.doi.org/10.1128/JVI.00204-14
63. Kolawole AO, Gonzalez-Hernandez MB, Turula H, Yu C, Elftman MD, Wobus CE. 2016. Oral norovirus infection is blocked in mice lacking Peyer's patches and mature M cells. J Virol 90:1499-1506. http://dx.doi.org/10.1128/JVI.02872-15
64. Li XD, Sun L, Seth RB, Pineda G, Chen ZJ. 2005. Hepatitis C virus protease NS3/4A cleaves mitochondrial antiviral signaling protein offthe mitochondria to evade innate immunity. Proc Natl Acad Sci U S A 102: 17717-17722. http://dx.doi.org/10.1073/pnas.0508531102
65. Sillanpaa M, Kaukinen P, Melen K, Julkunen I. 2008. Hepatitis C virus proteins interfere with the activation of chemokine gene promoters and downregulate chemokine gene expression. J Gen Virol 89:432-443. http://dx.doi.org/10.1099/vir.0.83316-0
66. Versteeg GA, Bredenbeek PJ, van den Worm SH, Spaan WJ. 2007. Group 2 coronaviruses prevent immediate early interferon induction by protection of viral RNA from host cell recognition. Virology 361:18-26. http://dx.doi.org/10.1016/j.virol.2007.01.020
67. Zhou H, Perlman S. 2007. Mouse hepatitis virus does not induce beta interferon synthesis and does not inhibit its induction by double-stranded RNA. J Virol 81:568-574. http://dx.doi.org/10.1128/JVI.01512-06
68. Roth-Cross JK, Martinez-Sobrido L, Scott EP, Garcia-Sastre A, Weiss SR. 2007. Inhibition of the alpha/beta interferon response by mouse hepatitis virus at multiple levels. J Virol 81:7189-7199. http://dx.doi.org/10.1128/JVI.00013-07
69. Neufeldt CJ, Joyce MA, Van Buuren N, Levin A, Kirkegaard K, Gale M, Jr, Tyrrell DL, Wozniak RW. 2016. The hepatitis C virus-induced membranous web and associated nuclear transport machinery limit access of pattern recognition receptors to viral replication sites. PLoS Pathog 12: e1005428. http://dx.doi.org/10.1371/journal.ppat.1005428
70. Uchida L, Espada-Murao LA, Takamatsu Y, Okamoto K, Hayasaka D, Yu F, Nabeshima T, Buerano CC, Morita K. 2014. The dengue virus conceals double-stranded RNA in the intracellular membrane to escape from an interferon response. Sci Rep 4:7395. http://dx.doi.org/10.1038/srep07395
71. Koetzner CA, Kuo L, Goebel SJ, Dean AB, Parker MM, Masters PS. 2010. Accessory protein 5a is a major antagonist of the antiviral action of interferon against murine coronavirus. J Virol 84:8262-8274. http://dx.doi.org/10.1128/JVI.00385-10
72. Sumpter R, Jr, Loo YM, Foy E, Li K, Yoneyama M, Fujita T, Lemon SM, Gale M, Jr. 2005. Regulating intracellular antiviral defense and permissiveness to hepatitis C virus RNA replication through a cellular RNA helicase, RIG-I. J Virol 79:2689-2699. http://dx.doi.org/10.1128/JVI.79.5.2689-2699.2005