Analysis of synchronous and asynchronous in vitro infections with homologous murine norovirus strains reveals time-dependent viral interference effects
Ludwig-Begall, Louisa; Di Felice, E.; Toffoli, B.et al.
Ludwig-Begall, Louisa ; Université de Liège - ULiège > Département des maladies infectieuses et parasitaires (DMI) > Virologie vétérinaire et maladies virales animales
Thiry, Etienne ; Université de Liège - ULiège > Département des maladies infectieuses et parasitaires (DMI) > Virologie vétérinaire et maladies virales animales
Language :
English
Title :
Analysis of synchronous and asynchronous in vitro infections with homologous murine norovirus strains reveals time-dependent viral interference effects
Publication date :
2021
Journal title :
Viruses
eISSN :
1999-4915
Publisher :
Multidisciplinary Digital Publishing Institute (MDPI), Switzerland
Harris, J.P.; Edmunds, W.J.; Pebody, R.; Brown, D.W.; Lopman, B.A. Deaths from norovirus among the elderly, England and Wales. Emerg. Infect. Dis. 2008, 14, 1546–1552. [CrossRef]
Brown, J.R.; Gilmour, K.; Breuer, J. Norovirus Infections Occur in B-Cell-Deficient Patients. Clin. Infect. Dis. 2016, 62, 1136–1138. [CrossRef] [PubMed]
Woodward, J.; Gkrania-Klotsas, E.; Kumararatne, D. Chronic norovirus infection and common variable immunodeficiency. Clin. Exp. Immunol. 2017, 188, 363–370. [CrossRef]
Brown, J.R.; Roy, S.; Tutill, H.; Williams, R.; Breuer, J. Super-infections and relapses occur in chronic norovirus infections. J. Clin. Virol. 2017, 96, 44–48. [CrossRef]
Vega, E.; Donaldson, E.; Huynh, J.; Barclay, L.; Lopman, B.; Baric, R.; Vinjé, J. RNA Populations in Immunocompromised Patients as Reservoirs for Novel Norovirus Variants. J. Virol. 2014, 88, 14184–14196. [CrossRef] [PubMed]
Jones, M.K.; Grau, K.R.; Costantini, V.; Kolawole, A.O.; de Graaf, M.; Freiden, P.; Karst, S.M. Human norovirus culture in B cells. Nat. Protoc. 2015, 10, 1939–1947. [CrossRef]
Ettayebi, K.; Crawford, S.E.; Murakami, K.; Broughman, J.R.; Karandikar, U.; Tenge, V.R.; Estes, M.K. Replication of human noroviruses in stem cell–derived human enteroids. Science 2016, 353, 1387–1393. [CrossRef]
Van Dycke, J.; Ny, A.; Conceição-Neto, N.; Maes, J.; Hosmillo, M.; Cuvry, A.; Rocha-Pereira, J. A robust human norovirus replication model in zebrafish larvae. PLoS Pathog. 2019, 15, 1–21. [CrossRef]
Todd, K.V.; Tripp, R.A. Human norovirus: Experimental models of infection. Viruses 2019, 11, 151. [CrossRef] [PubMed]
Arias, A.; Bailey, D.; Chaudhry, Y.; Goodfellow, I. Development of a reverse-genetics system for murine norovirus 3: Long-term persistence occurs in the caecum and colon. J. Gen. Virol. 2012, 93, 1432–1441. [CrossRef]
Yunus, M.A.; Chung, L.M.W.; Chaudhry, Y.; Bailey, D.; Goodfellow, I. Development of an optimized RNA-based murine norovirus reverse genetics system. J. Virol. Methods 2010, 169, 112–118. [CrossRef] [PubMed]
Karst, S.M.; Wobus, C.E.; Lay, M.; Davidson, J.; Virgin, H.W. STAT1-dependent innate immunity to a Norwalk-like virus. Science 2003, 299, 1575–1578. [CrossRef] [PubMed]
Wobus, C.E.; Thackray, L.B.; Virgin, H.W. Murine norovirus: A model system to study norovirus biology and pathogenesis. J. Virol. 2006, 80, 5104–5112. [CrossRef] [PubMed]
Wobus, C.E.; Karst, S.M.; Thackray, L.B.; Chang, K.-O.; Sosnovtsev, S.V.; Belliot, G.; Virgin, H.W., 4th. Replication of Norovirus in Cell Culture Reveals a Tropism for Dendritic Cells and Macrophages. PLoS Biol. 2004, 30, e432. [CrossRef] [PubMed]
Desselberger, U. Caliciviridae other than noroviruses. Viruses 2019, 11, 286. [CrossRef]
Clarke, I.N.; Estes, M.K.; Green, K.Y.; Hansman, G.; Knowles, N.J.; Koopmans, M.K. Virus Taxonomy: Classification and Nomenclature of Viruses: Ninth Report of the International Committee on Taxonomy of Viruses; King, A.M.Q., Adams, M.J., Carstens, E.B., Lefkowitz, E.J., Eds.; Elsevier: San Diego, CA, USA, 2012; pp. 977–986.
Karst, S.M.; Zhu, S.; Goodfellow, I.G. The molecular pathology of noroviruses. J. Pathol. 2015, 235, 206–216. [CrossRef]
Thorne, L.G.; Goodfellow, I.G. Norovirus gene expression and replication. J. Gen. Virol. 2014, 95, 278–291. [CrossRef] [PubMed]
McFadden, N.; Bailey, D.; Carrara, G.; Benson, A.; Chaudhry, Y.; Shortland, A.; Goodfellow, I. Norovirus regulation of the innate immune response and apoptosis occurs via the product of the alternative open reading frame 4. PLoS Pathog. 2011, 7, e1002413. [CrossRef] [PubMed]
Parra, G.I. Emergence of norovirus strains: A tale of two genes. Virus. Evol. 2019, 5, 1–9. [CrossRef] [PubMed]
Ludwig-Begall, L.F.; Mauroy, A.; Thiry, E. Norovirus recombinants: Recurrent in the field, recalcitrant in the lab—A scoping review of recombination and recombinant types of noroviruses. J. Gen. Virol. 2018, 99, 970–988. [CrossRef] [PubMed]
Bull, R.A.; Tanaka, M.M.; White, P.A. Norovirus recombination. J. Gen. Virol. 2007, 88, 3347–3359. [CrossRef] [PubMed]
Mathijs, E.; Muylkens, B.; Mauroy, A.; Ziant, D.; Delwiche, T.; Thiry, E. Experimental evidence of recombination in murine noroviruses. J. Gen. Virol. 2010, 91, 2723–2733. [CrossRef]
Mathijs, E.; de Oliveira-Filho, E.F.; Dal Pozzo, F.; Mauroy, A.; Thiry, D.; Massart, F.; Thiry, E. Infectivity of a recombinant murine norovirus (RecMNV) in Balb/cByJ mice. Vet. Microbiol. 2016, 192, 118–122. [CrossRef]
Ludwig-Begall, L.F.; Lu, J.; Hosmillo, M.; De Oliveira-Filho, E.F.; Mathijs, E.; Goodfellow, I.; Thiry, E. Replicative fitness recuperation of a recombinant murine norovirus—In vitro reciprocity of genetic shift and drift. J. Gen. Virol. 2020, 101, 510–522. [CrossRef]
Worobey, M.; Holmes, E.C. Evolutionary aspects of recombination in RNA viruses. J. Gen. Virol. 1999, 80, 2535–2543. [CrossRef]
Lowry, K.; Woodman, A.; Cook, J.; Evans, D.J. Recombination in enteroviruses is a biphasic replicative process involving the generation of greater-than genome length “imprecise” intermediates. PLoS Pathog. 2014, 10, e1004191. [CrossRef]
Bagaya, B.S.; Tian, M.; Nickel, G.C.; Vega, J.F.; Li, Y.; He, P.; Gao, Y. An in vitro Model to Mimic Selection of Replication-Competent HIV-1 Intersubtype Recombination in Dual or Superinfected Patients. J. Mol. Biol. 2017, 429, 2246–2264. [CrossRef] [PubMed]
Banner, L.R.; Mc Lai, M. Random nature of coronavirus RNA recombination in the absence of selection pressure. Virology 1991, 185, 441–445. [CrossRef]
Sackman, A.M.; Reed, D.; Rokyta, D.R. Intergenic incompatibilities reduce fitness in hybrids of extremely closely related bacteriophages. PeerJ 2015, 3, 1320. [CrossRef] [PubMed]
Folimonova, S.Y. Superinfection Exclusion Is an Active Virus-Controlled Function That Requires a Specific Viral Protein. J. Virol. 2012, 86, 5554–5561. [CrossRef]
Bratt, M.A.; Rubin, H. Specific interference among strains of Newcastle disease virus: III. Mechanisms of interference. Virology 1968, 35, 395–407. [CrossRef]
Huang, I.-C.; Li, W.; Sui, J.; Marasco, W.; Choe, H.; Farzan, M. Influenza A Virus Neuraminidase Limits Viral Superinfection. J. Virol. 2008, 82, 4834–4843. [CrossRef]
Bergua, M.; Zwart, M.P.; El-Mohtar, C.; Shilts, T.; Elena, S.F.; Folimonova, S.Y. A viral protein mediates superinfection exclusion at the whole organism level while is not required for exclusion at the cellular level. J. Virol. 2014, 88, 11327–11338. [CrossRef]
Adams, R.H.; Brown, D.T. BHK cells expressing Sindbis virus-induced homologous interference allow the translation of nonstructural genes of superinfecting virus. J. Virol. 1985, 54, 351–357. [CrossRef]
Claus, C.; Tzeng, W.P.; Liebert, U.G.; Frey, T.K. Rubella virus-induced superinfection exclusion studied in cells with persisting replicons. J. Gen. Virol. 2007, 88, 2769–2773. [CrossRef] [PubMed]
Tscherne, D.M.; Evans, M.J.; von Hahn, T.; Jones, C.T.; Stamataki, Z.; McKeating, J.; Rice, C.M. Superinfection exclusion in cells infected with hepatitis C virus. J. Virol. 2007, 81, 3693–3703. [CrossRef] [PubMed]
Lee, Y.-M.; Tscherne, D.M.; Yun, S.-I.; Frolov, I.; Rice, C.M. Dual mechanisms of pestiviral superinfection exclusion at entry and RNA replication. J. Virol. 2005, 79, 3231–3242. [CrossRef]
Zhou, X.; Sun, K.; Zhou, X.; Jackson, A.O.; Li, Z. The Matrix Protein of a Plant Rhabdovirus Mediates Superinfection Exclusion by Inhibiting Viral Transcription. J. Virol. 2019, 93, 1–18. [CrossRef] [PubMed]
Johnson, W.E. Origins and evolutionary consequences of ancient endogenous retroviruses. Nat. Rev. Microbiol. 2019, 17, 355–370. [CrossRef]
Hyde, J.L.; Sosnovtsev, S.V.; Green, K.Y.; Wobus, C.; Virgin, H.W.; Mackenzie, J.M. Mouse norovirus replication is associated with virus-induced vesicle clusters originating from membranes derived from the secretory pathway. J. Virol. 2009, 83, 9709–9719. [CrossRef]
Mauroy, A.; Poel, W.H.; Honing, R.H.-V.; Thys, C.; Thiry, E. Development and application of a SYBR green RT-PCR for first line screening and quantification of porcine sapovirus infection. BMC Vet. Res. 2012, 8, 193. [CrossRef]
Zhang, H.; Cockrell, S.K.; Kolawole, A.O.; Rotem, A.; Serohijos, A.W.R.; Chang, C.B.; Pipas, J.M. Isolation and analysis of rare norovirus recombinants from co-infected mice using drop-based microfluidics. J. Virol. 2015, 89, 1137–1145. [CrossRef]
Mauroy, A.; Taminiau, B.; Nezer, C.; Ghurburrun, E.; Baurain, D.; Daube, G.; Thiry, E. High-throughput sequencing analysis reveals the genetic diversity of different regions of the murine norovirus genome during in vitro replication. Arch. Virol. 2017, 33, 1019–1023. [CrossRef]
Stauffer Thompson, K.A.; Yin, J. Population dynamics of an RNA virus and its defective interfering particles in passage cultures. Virol. J. 2010, 7, 257. [CrossRef]
Pathak, K.B.; Nagy, P.D. Defective interfering RNAs: Foes of viruses and friends of virologists. Viruses 2009, 1, 895–919. [CrossRef] [PubMed]
Voinnet, O. Induction and suppression of RNA silencing: Insights from viral infections. Nat. Rev. Genet. 2005, 3, 206–220. [CrossRef] [PubMed]
Webster, B.; Ott, M.; Greene, W.C. Evasion of superinfection exclusion and elimination of primary viral RNA by an adapted strain of hepatitis C virus. J. Virol. 2013, 87, 13354–13369. [CrossRef]
Schaller, T.; Appel, N.; Koutsoudakis, G.; Kallis, S.; Lohmann, V.; Pietschmann, T.; Bartenschlager, R. Analysis of Hepatitis C Virus Superinfection Exclusion by Using Novel Fluorochrome Gene-Tagged Viral Genomes. J. Virol. 2007, 81, 4591–4603. [CrossRef] [PubMed]
Zou, G.; Zhang, B.; Lim, P.-Y.; Yuan, Z.; Bernard, K.A.; Shi, P.-Y. Exclusion of West Nile Virus Superinfection through RNA Replication. J. Virol. 2009, 83, 11765–11776. [CrossRef] [PubMed]