JLE

Virologie

MENU

Viral persistence of mammalian reovirus in cell culture: a model of virus-cell coevolution Volume 23, issue 5, Septembre-Octobre 2019

  • [1] Heaton N.S. Revisiting the concept of a cytopathic viral infection. PLoS Pathog. 2017;13:e1006409-e1006416.
  • [2] Excoffon K.J.D.A., Guglielmi K.M., Wetzel J.D. Reovirus preferentially infects the basolateral surface and is released from the apical surface of polarized human respiratory epithelial cells. J Infect Dis. 2008;197:1189-1197.
  • [3] Lai C.M., Mainou B.A., Kim K.S., Dermody T.S. Directional release of reovirus from the apical surface of polarized endothelial cells. MBio. 2013;4:e00049-13.
  • [4] Lee P., Clements D., Helson E., Gujar S. Reovirus in cancer therapy: an evidence-based review. Oncolytic Virother. 2014;3:69-82.
  • [5] Chakrabarty R., Tran H., Selvaggi G., Hagerman A., Thompson B., Coffey M. The oncolytic virus, pelareorep, as a novel anticancer agent: a review. Invest New Drugs. 2015;33:761-774.
  • [6] Mohamed A., Johnston R., Shmulevitz M. Potential for improving potency and specificity of reovirus oncolysis with next-generation reovirus variants. Viruses. 2015;7:6251-6278.
  • [7] Kemp V., Hoeben R., van den Wollenberg D. Exploring reovirus plasticity for improving its use as oncolytic virus. Viruses. 2016;8:4-16.
  • [8] Lanoie D., Côté S., Degeorges E., Lemay G. A single mutation in the mammalian orthoreovirus S1 gene is responsible for increased interferon sensitivity in a virus mutant selected in Vero cells. Virology. 2019;528:73-79.
  • [9] Sandekian V., Lemay G. Amino acids substitutions in σ1 and μ1 outer capsid protein of a Vero cell-adapted mammalian orthoreovirus are required for optimal virus binding and disassembly. Virus Res. 2015;196:20-29.
  • [10] Dermody T.S., Parker J.S.L., Sherry B. Orthoreoviruses. In: Knipe D.M., Howley P.M., eds. Field's virology. Philadelphia: Lippincot, Williams and Wilkins; 2013.
  • [11] Lemay G. Synthesis and translation of viral mRNA in reovirus-infected cells: progress and remaining questions. Viruses. 2018;10:671-725.
  • [12] Danthi P., Guglielmi K.M., Kirchner E., Mainou B., Stehle T., Dermody T.S. From touchdown to transcription: the reovirus cell entry pathway. Curr Top Microbiol Immunol. 2010;343:91-119.
  • [13] Sutherland D.M., Aravamudhan P., Dermody T.S. An orchestra of reovirus receptors: still searching for the conductor. Adv Virus Res. 2018;100:1-24.
  • [14] Golden J.W., Linke J., Schmechel S., Thoemke K., Schiff L.A. Addition of exogenous protease facilitates reovirus infection in many restrictive cells. J Virol. 2002;76:7430-7443.
  • [15] Alain T., Kim T.S., Lun X. Proteolytic disassembly is a critical determinant for reovirus oncolysis. Mol Ther. 2007;15:1512-1521.
  • [16] Nygaard R.M., Lahti L., Boehme K.W. Genetic determinants of reovirus pathogenesis in a murine model of respiratory infection. J Virol. 2013;87:9279-9289.
  • [17] Wetzel J.D., Chappell J.D., Fogo A.B., Dermody T.S. Efficiency of viral entry determines the capacity of murine erythroleukemia cells to support persistent infections by mammalian reoviruses. J Virol. 1997;71:299-306.
  • [18] Marcato P., Shmulevitz M., Pan D., Stoltz D., Lee P.W. Ras transformation mediates reovirus oncolysis by enhancing virus uncoating, particle infectivity, and apoptosis-dependent release. Mol Ther. 2007;15:1522-1530.
  • [19] Olland A.M., Jané-Valbuena J., Schiff L.A., Nibert M.L., Harrison S.C. Structure of the reovirus outer capsid and dsRNA-binding protein σ3 at 1.8Å resolution. EMBO J. 2001;20:979-989.
  • [20] Liemann S., Chandran K., Baker T.S., Nibert M.L., Harrison S.C. Structure of the reovirus membrane-penetration protein, μ1, in a complex with is protector protein, σ3. Cell. 2002;108:283-295.
  • [21] Zhang X., Ji Y., Zhang L. Features of reovirus outer capsid protein μ1 revealed by electron cryomicroscopy and image reconstruction of the virion at 7.0Å resolution. Structure. 2005;13:1545-1557.
  • [22] Sandekian V., Lim D., Prud’homme P., Lemay G. Transient high level mammalian reovirus replication in a bat epithelial cell line occurs without cytopathic effect. Virus Res. 2013;173:327-335.
  • [23] Montgomery L.B., Kao C.Y., Verdin E., Cahill C., Maratos-Flier E. Infection of a polarized epithelial cell line with wild-type reovirus leads to virus persistence and altered cellular function. J Gen Virol. 1991;72:2939-2946.
  • [24] Verdin E.M., Maratos-Flier E., Carpentier J.L., Kahn C.R. Persistent infection with a nontransforming RNA virus leads to impaired growth factor receptors and response. J Cell Physiol. 1986;128:457-465.
  • [25] Strong J.E., Coffey M.C., Tang D., Sabinin P., Lee P.W. The molecular basis of viral oncolysis: usurpation of the Ras signaling pathway by reovirus. EMBO J. 1998;17:3351-3362.
  • [26] Rudd P., Lemay G. Correlation between interferon sensitivity of reovirus isolates and ability to discriminate between normal and Ras-transformed cells. J Gen Virol. 2005;86:1489-1497.
  • [27] Dermody T.S. Molecular mechanisms of persistent infection by reovirus. Curr Top Microbiol Immunol. 1998;233:1-22.
  • [28] Ahmed R., Canning W.M., Kauffman R.S., Sharpe A.H., Hallum J.V., Fields B.N. Role of the host cell in persistent viral infection: coevolution of L cells and reovirus during persistent infection. Cell. 1981;25:325-332.
  • [29] Baer G.S., Ebert D.H., Chung C.J., Erickson A.H., Dermody T.S. Mutant cells selected during persistent reovirus infection do not express mature cathepsin L and do not support reovirus disassembly. J Virol. 1999;73:9532-9543.
  • [30] Ebert D.H., Kopecky-Bromberg S.A., Dermody T.S. Cathepsin B is inhibited in mutant cells selected during persistent reovirus infection. J Biol Chem. 2004;279:3837-3851.
  • [31] Ahmed R., Fields B.N. Role of the S4 gene in the establishment of persistent reovirus infection in L cells. Cell. 1982;28:605-612.
  • [32] Kauffman R.S., Ahmed R., Fields B.N. Selection of a mutant S1 gene during reovirus persistent infection of L cells: role in maintenance of the persistent state. Virology. 1983;131:79-87.
  • [33] Baer G.S., Dermody T.S. Mutations in reovirus outer-capsid protein σ3 selected during persistent infections of L cells confer resistance to protease inhibitor E64. J Virol. 1997;71:4921-4928.
  • [34] Wetzel J.D., Wilson G.J., Baer G.S. Reovirus variants selected during persistent infections of L cells contain mutations in the viral S1 and S4 genes and are altered in viral disassembly. J Virol. 1997;71:1362-1369.
  • [35] Ebert D.H., Wetzel J.D., Brumbaugh D.E. Adaptation of reovirus to growth in the presence of protease inhibitor E64 segregates with a mutation in the carboxy terminus of viral outer-capsid protein σ3. J Virol. 2001;75:3197-3206.
  • [36] Wilson G.J., Nason E.L., Hardy C.S. A single mutation in the carboxy terminus of reovirus outer-capsid protein σ3 confers enhanced kinetics of σ3 proteolysis, resistance to inhibitors of viral disassembly, and alterations in σ3 structure. J Virol. 2002;76:9832-9843.
  • [37] Clark K.M., Wetzel J.D., Gu Y. Reovirus variants selected for resistance to ammonium chloride have mutations in viral outer-capsid protein σ3. J Virol. 2006;80:671-681.
  • [38] Doyle J.D., Danthi P., Kendall E.A., Ooms L.S., Wetzel J.D., Dermody T.S. Molecular determinants of proteolytic disassembly of the reovirus outer capsid. J Biol Chem. 2012;287:8029-8038.
  • [39] Schiff L.A. Structure and functions of the orthoreovirus σ3 protein. In: Patton J.T., eds. Segmented double-stranded RNA viruses: structure and molecular biology. Bethesda: Caister Academic Press; 2008.
  • [40] Doyle J.D., Stencel-Baerenwald J.E., Copeland C.A. Diminished reovirus capsid stability alters disease pathogenesis and littermate transmission. PLoS Pathog. 2015;11:e1004693-e1004724.
  • [41] Wilson G.J., Wetzel J.D., Puryear W., Bassel-Duby R., Dermody T.S. Persistent reovirus infections of L cells select mutations in viral attachment protein σ1 that alter oligomer stability. J Virol. 1996;70:6598-6606.
  • [42] Dietrich M.H., Ogden K.M., Long J.M. Structural and functional features of the reovirus σ1 tail. J Virol. 2018;92:e00336-e418.
  • [43] Reiter D.M., Frierson J.M., Halvorson E.E., Kobayashi T., Dermody T.S., Stehle T. Crystal structure of reovirus attachment protein σ1 in complex with sialylated oligosaccharides. PLoS Pathog. 2011;7:e1002166.
  • [44] Chew T., Noyce R., Collins S.E., Hancock M.H., Mossman K.L. Characterization of the interferon regulatory factor 3-mediated antiviral response in a cell line deficient for IFN production. Mol Immunol. 2009;46:393-399.
  • [45] Desmyter J., Melnick J.L., Rawls W.E. Defectiveness of interferon production and of rubella virus interference in a line of African green monkey kidney cells (Vero). J Virol. 1968;2:955-961.
  • [46] Emeny J.M., Morgan M.J. Regulation of the interferon system – evidence that Vero cells have a genetic defect in interferon production. J Gen Virol. 1979;43:247-252.
  • [47] Park S., Choi J., Kang J. Attenuated expression of interferon-induced protein kinase PKR in a simian cell devoid of type I interferons. Mol Cells. 2006;21:21-28.
  • [48] Jabre R., Sandekian V., Lemay G. Amino acid substitutions in σ1 and μ1 outer capsid proteins are selected during mammalian reovirus adaptation to Vero cells. Virus Res. 2013;176:188-198.
  • [49] Lanoie D, Lemay G. Characterization of the different reovirus proteins involved in viral adaptation to Vero cells during viral persistence [in preparation].
  • [50] Sarkar P., Danthi P. The μ1 72-96 loop controls conformational transitions during reovirus cell entry. J Virol. 2013;87:13532-13542.
  • [51] Snyder A.J., Danthi P. Cleavage of the C-terminal fragment of reovirus μ1 is required for optimal infectivity. J Virol. 2018;92:e01848-e1917.
  • [52] Thete D., Snyder A.J., Mainou B.A., Danthi P. Reovirus μ1 protein affects infectivity by altering virus-receptor interactions. J Virol. 2016;90:10951-10962.
  • [53] Thete D., Danthi P. Protein mismatches caused by reassortment influence functions of the reovirus capsid. J Virol. 2018;92:e00858-e918.
  • [54] Derrien M., Hooper J.W., Fields B.N. The M2 gene segment is involved in the capacity of reovirus type 3 Abney to induce the oily fur syndrome in neonatal mice, a S1 gene segment-associated phenotype. Virology. 2003;305:25-30.
  • [55] Tyler K.L., Squier M.K.T., Brown A.L. Linkage between reovirus-induced apoptosis and inhibition of cellular DNA synthesis: role of the S1 and M2 genes. J Virol. 1996;70:7984-7991.
  • [56] Hrdy D.B., Rubin D.H., Fields B.N. Molecular basis of reovirus neurovirulence: role of the M2 gene in avirulence. Proc Natl Acad Sci U S A. 1982;79:1298-1302.
  • [57] Clarke P., Meintzer S.M., Widmann C., Johnson G.L., Tyler K.L. Reovirus infection activates JNK and the JNK-dependent transcription factor c-Jun. J Virol. 2001;75:11275-11283.
  • [58] Rodgers S.E., Barton E.S., Oberhaus S.M. Reovirus-induced apoptosis of MDCK cells is not linked to viral yield and is blocked by Bcl-2. J Virol. 1997;71:2540-2546.
  • [59] Danis C., Lemay G. Protein synthesis in different cell lines infected with orthoreovirus serotype 3: inhibition of host-cell protein synthesis correlates with accelerated viral multiplication and cell killing. Biochem Cell. 1993;71:81-85.
  • [60] Alain T., Kim M., Johnston R.N. The oncolytic effect of reovirus on tumour cells that have survived reovirus cell killing . Br J Cancer. 2006;95:1020-1027. in vivoin vitro
  • [61] Kim M., Egan C., Alain T. Acquired resistance to reoviral oncolysis in Ras-transformed fibrosarcoma cells. Oncogene. 2007;26:4124-4134.
  • [62] Kim M., Garant K.A., zur Nieden N.I. Attenuated reovirus displays oncolysis with reduced host toxicity. Br J Cancer. 2011;104:290-299.
  • [63] Taber R., Alexander V., Whitford W. Persistent reovirus infection of CHO cells resulting in virus resistance. J Virol. 1976;17:513-524.
  • [64] Barton E.S., Forrest J.C., Connolly J.L. Junction adhesion molecule is a receptor for reovirus. Cell. 2001;104:441-451.
  • [65] Konopka-Anstadt J.L., Mainou B.A., Sutherland D.M., Sekine Y., Strittmatter S.M., Dermody T.S. The Nogo receptor NgR1 mediates infection by mammalian reovirus. Cell Host Microbe. 2014;15:681-691.
  • [66] Danis C., Mabrouk T., Garzon S., Lemay G. Establishment of persistent reovirus infection in SC1 cells: absence of protein synthesis inhibition and increased level of double-stranded RNA-activated protein kinase. Virus Res. 1993;27:253-265.
  • [67] Danis C., Mabrouk T., Faure M., Lemay G. Interferon has no protective effect during acute or persistent reovirus infection of mouse SC1 fibroblasts. Virus Res. 1997;51:139-149.
  • [68] Ahmed R., Graham A.F. Persistent infections in L cells with temperature-sensitive mutants of reovirus. J Virol. 1977;23:250-262.
  • [69] Dermody T.S., Nibert M.L., Wetzel J.D., Tong X., Fields B.N. Cells and viruses with mutations affecting viral entry are selected during persistent infections of L cells with mammalian reoviruses. J Virol. 1993;67:2055-2063.
  • [70] Canning W.M., Fields B.N. Ammonium chloride prevents lytic growth of reovirus and helps to establish persistent infection in mouse L cells. Science. 1983;219:987-988.
  • [71] Brown E.G., Nibert M.L., Fields B.N. The L2 gene of reovirus serotype 3 controls the capacity to interfere, accumulate deletions and establish persistent infection. In: Compans R.W., Bishop D.H.L., eds. Double-stranded RNA viruses. New York: Elsevier Biomedical; 1983.
  • [72] Fernandez de Castro I., Zamora P.F., Ooms L. Reovirus forms neo-organelles for progeny particle assembly within reorganized cell membranes. MBio. 2013;5:e00931-e1013.
  • [73] Bird S.W, Maynard N.D., Covert M.W., Kirkegaard K. Nonlytic viral spread enhanced by autophagy components. Proc Natl Acad Sci U S A. 2014;111:13081-13086.
  • [74] Bird S.W., Kirkegaard K. Escape of non-enveloped virus from intact cells. Virology. 2015;479-480:444-449.
  • [75] Jackson W.T. Viruses and the autophagy pathway. Virology. 2015;479-480:450-456.
  • [76] Münz C. Autophagy proteins in viral exocytosis and anti-viral immune responses. Viruses. 2017;9:288-310.
  • [77] Münz C. The autophagic machinery in viral exocytosis. Front Microbiol. 2017;8:461-468.
  • [78] Kemp V., Dautzenberg I., Limpens R., van den Wollenberg D., Hoeben R. Oncolytic reovirus infection is facilitated by the autophagic machinery. Viruses. 2017;9:266-315.
  • [79] Thirukkumaran C.M., Shi Z.Q., Luider J. Reovirus modulates autophagy during oncolysis of multiple myeloma. Autophagy. 2013;9:413-414.
  • [80] Talloczy Z., Jiang W.X., Virgin H.W. Regulation of starvation- and virus-induced autophagy by the eIF2α kinase signaling pathway. Proc Natl Acad Sci U S A. 2002;99:190-195.
  • [81] Matsuzaki N., Hinshaw V.S., Fields B.N., Greene M.I. Cell receptors for the mammalian reovirus: reovirus-specific T-cell hybridomas can become persistently infected and undergo autoimmune stimulation. J Virol. 1986;60:259-266.
  • [82] Dermody T.S., Chappell J.D., Hofler J.G., Kramp W., Tyler K.L. Eradication of persistent reovirus infection from a B-cell hybridoma. Virology. 1995;212:272-276.
  • [83] Haller B.L., Barkon M.L., Li X.Y. Brain- and intestine-specific variants of reovirus serotype 3 strain Dearing are selected during chronic infection of severe combined immunodeficient mice. J Virol. 1995;69:3933-3937.
  • [84] Morrison L.A., Fields B.N., Dermody T.S. Prolonged replication in the mouse central-nervous-system of reoviruses isolated from persistently infected cell-cultures. J Virol. 1993;67:3019-3026.
  • [85] Brochu-Lafontaine V., Lemay G. Addition of exogenous polypeptides on the mammalian reovirus outer capsid using reverse genetics. J Virol Methods. 2012;179:342-350.
  • [86] Rouault É., Lemay G. Incorporation of epitope-tagged viral σ3 proteins to reovirus virions. Can J Microbiol. 2003;49:407-417.
  • [87] Demidenko A.A., Blattman J.N., Blattman N.N., Greenberg P.D., Nibert M.L. Engineering recombinant reoviruses with tandem repeats and a tetravirus 2A-like element for exogenous polypeptide expression. Proc Natl Acad Sci U S A. 2013;110:e1867-e1876.
  • [88] Boehme K.W., Ikizler M., Iskarpatyoti J.A. Engineering recombinant reoviruses to display gp41 membrane-proximal external-region epitopes from HIV-1. mSphere. 2016;1:e00086-16.
  • [89] Shmulevitz M, Gujar S.A., Ahn D.G., Mohamed A., Lee P.W.K. Reovirus variants with mutations in genome segments S1 and L2 exhibit enhanced virion infectivity and superior oncolysis. J Virol. 2012;86:7403-7413.
  • [90] van den Wollenberg D.J.M., Dautzenberg I.J.C., van den Hengel S.K., Cramer S.J., de Groot R.J., Hoeben R.C. Isolation of reovirus T3D mutants capable of infecting human tumor cells independent of junction adhesion molecule-A. PLoS One. 2012;7:e48064.