Amino acids 78 and 79 of Mammalian Orthoreovirus protein μNS are necessary for stress granule localization, core protein λ2 interaction, and de novo virus replication

Virology

Volumn 448, Issue , 2014, Pages 133-145

  Carroll, Kate ^a   Hastings, Craig ^a   Miller, Cathy L ^a  

^a IOWA STATE UNIVERSITY   (United States)

Author keywords

NS; Innate immunity; Mammalian Orthoreovirus; Replication; Stress granules; Translation

Indexed keywords

AMINO ACID; AMINO ACID 78 AND 79; BINDING PROTEIN; CORE PROTEIN; MUTANT PROTEIN; NONSTRUCTURAL PROTEIN; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ANIMAL CELL; ARTICLE; CELL INCLUSION; CONTROLLED STUDY; GENE SILENCING; GENETIC TRANSFECTION; MAMMALIAN ORTHOREOVIRUS; MUTANT; NONHUMAN; PLASMID; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN LOCALIZATION; REOVIRUS INFECTION; STRESS GRANULE; VIRUS REPLICATION;

EID: 84886413079     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2013.10.009     Document Type: Article

References (63)

1. Agosto M.A., Ivanovic T., Nibert M.L. Mammalian reovirus, a nonfusogenic nonenveloped virus, forms size-selective pores in a model membrane. Proceedings of the National Academy of Sciences of the United States of America 2006, 103:16496-16501.
2. Anderson P., Kedersha N. Visibly stressed: the role of eIF2, TIA-1, and stress granules in protein translation. Cell Stress and Chaperones 2002, 7:213-221.
3. Antczak J.B., Joklik W.K. Reovirus genome segment assortment into progeny genomes studied by the use of monoclonal-antibodies directed against reovirus proteins. Virology 1992, 187:760-776.
4. Arnold M.M., Murray K.E., Nibert M.L. Formation of the factory matrix is an important, though not a sufficient function of nonstructural protein μNS during reovirus infection. Virology 2008, 375:412-423.
5. Barton E.S., Forrest J.C., Connolly J.L., Chappell J.D., Liu Y., Schnell F.J., Nusrat A., Parkos C.A., Dermody T.S. Junction adhesion molecule is a receptor for reovirus. Cell 2001, 104:441-451.
6. Becker M.M., Peters T.R., Dermody T.S. Reovirus σNS and μNS proteins form cytoplasmic inclusion structures in the absence of viral infection. Journal of Virology 2003, 77:5948-5963.
7. Boehme K.W., Ikizler M., Kobayashi T., Dermody T.S. Reverse genetics for mammalian reovirus. Methods 2011, 55:109-113.
8. Broering T.J., Arnold M.M., Miller C.L., Hurt J.A., Joyce P.L., Nibert M.L. Carboxyl-proximal regions of reovirus nonstructural protein μNS necessary and sufficient for forming factory-like inclusions. Journal of Virology 2005, 79:6194-6206.
9. Broering T.J., Kim J., Miller C.L., Piggott C.D., Dinoso J.B., Nibert M.L., Parker J.S. Reovirus nonstructural protein μNS recruits viral core surface proteins and entering core particles to factory-like inclusions. Journal of Virology 2004, 78:1882-1892.
10. Broering T.J., McCutcheon A.M., Centonze V.E., Nibert M.L. Reovirus nonstructural protein μNS binds to core particles but does not inhibit their transcription and capping activities. Journal of Virology 2000, 74:5516-5524.
11. Broering T.J., Parker J.S.L., Joyce P.L., Kim J.H., Nibert M.L. Mammalian reovirus nonstructural protein μNS forms large inclusions and colocalizes with reovirus microtubule-associated protein μ2 in transfected cells. Journal of Virology 2002, 76:8285-8297.
12. Buchholz U.J., Finke S., Conzelmann K.K. Generation of bovine respiratory syncytial virus (BRSV) from cDNA: BRSV NS2 is not essential for virus replication in tissue culture, and the human RSV leader region acts as a functional BRSV genome promoter. Journal of Virology 1999, 73:251-259.
13. Chandran K., Farsetta D.L., Nibert M.L. Strategy for nonenveloped virus entry: a hydrophobic conformer of the reovirus membrane penetration protein μ1 mediates membrane disruption. Journal of Virology 2002, 76:9920-9933.
14. Chappell J.D., Gunn V.L., Wetzel J.D., Baer G.S., Dermody T.S. Mutations in type 3 reovirus that determine binding to sialic acid are contained in the fibrous tail domain of viral attachment protein σ1. Journal of Virology 1997, 71:1834-1841.
15. Dales S. Replication of animal viruses as studied by electron microscopy. American Journal of Medicine 1965, 38:699.
16. Dang Y.J., Kedersha N., Low W.K., Romo D., Gorospe M., Kaufman R., Anderson P., Liu J.O. Eukaryotic initiation factor 2α-independent pathway of stress granule induction by the natural product pateamine A. Journal of Biological Chemistry 2006, 281:32870-32878.
17. Ebert D.H., Deussing J., Peters C., Dermody T.S. Cathepsin L and cathepsin B mediate reovirus disassembly in murine fibroblast cells. Journal of Biological Chemistry 2002, 277:24609-24617.
18. Garaigorta U., Heim M.H., Boyd B., Wieland S., Chisari F.V. Hepatitis C virus (HCV) induces formation of stress granules whose proteins regulate HCV RNA replication and virus assembly and egress. Journal of Virology 2012, 86:11043-11056.
19. Gilks N., Kedersha N., Ayodele M., Shen L., Stoecklin G., Dember L.M., Anderson P. Stress granule assembly is mediated by prion-like aggregation of TIA-1. Molecular Biology of the Cell 2004, 15:5383-5398.
20. Gillian A.L., Nibert M.L. Amino terminus of reovirus nonstructural protein σNS is important for ssRNA binding and nucleoprotein complex formation. Virology 1998, 240:1-11.
21. Imani F., Jacobs B.L. Inhibitory activity for the interferon-induced protein-kinase is associated with the reovirus serotype-1-σ3-protein. Proceedings of the National Academy of Sciences of the United States of America 1988, 85:7887-7891.
22. Katsafanas G.C., Moss B. Colocalization of transcription and translation within cytoplasmic poxvirus factories coordinates viral expression and subjugates host functions. Cell Host & Microbe 2007, 2:221-228.
23. Kedersha N., Anderson P. Stress granules: sites of mRNA triage that regulate mRNA stability and translatability. Biochemical Society Transactions 2002, 30:963-969.
24. Khaperskyy D.A., Hatchette T.F., McCormick C. Influenza A virus inhibits cytoplasmic stress granule formation. FASEB Journal 2012, 26:1629-1639.
25. Kim W.J., Kim J.H., Jang S.K. Anti-inflammatory lipid mediator 15d-PGJ2 inhibits translation through inactivation of eIF4A. EMBO Journal 2007, 26:5020-5032.
26. Kobayashi T., Chappell J.D., Danthi P., Dermody T.S. Gene-specific inhibition of reovirus replication by RNA interference. Journal of Virology 2006, 80:9053-9063.
27. Kobayashi T., Ooms L.S., Chappell J.D., Dermody T.S. Identification of functional domains in reovirus replication proteins μNS and μ2. Journal of Virology 2009, 83:2892-2906.
28. Kobayashi T., Ooms L.S., Ikizler M., Chappell J.D., Dermody T.S. An improved reverse genetics system for mammalian orthoreoviruses. Virology 2010, 398:194-200.
29. Lindquist M.E., Lifland A.W., Utley T.J., Santangelo P.J., Crowe J.E. Respiratory syncytial virus induces host RNA stress granules to facilitate viral replication. Journal of Virology 2010, 84:12274-12284.
30. Lloyd R.E. How do viruses interact with stress-associated RNA granules?. PLoS Pathogens 2012, 8:e1002741.
31. Luongo C.L., Reinisch K.M., Harrison S.C., Nibert M.L. Identification of the guanylyltransferase region and active site in reovirus mRNA capping protein λ2. Journal of Biological Chemistry 2000, 275:2804-2810.
32. Mazroui R., Sukarieh R., Bordeleau M.E., Kaufman R.J., Northcote P., Tanaka J., Gallouzi I., Pelletier J. Inhibition of ribosome recruitment induces stress granule formation independently of eukaryotic initiation factor 2α phosphorylation. Molecular Biology of the Cell 2006, 17:4212-4219.
33. McCutcheon A.M., Broering T.J., Nibert M.L. Mammalian reovirus M3 gene sequences and conservation of coiled-coil motifs near the carboxyl terminus of the μNS protein. Virology 1999, 264:16-24.
34. McEwen E., Kedersha N., Song B.B., Scheuner D., Gilks N., Han A.P., Chen J.J., Anderson P., Kaufman R.J. Heme-regulated inhibitor kinase-mediated phosphorylation of eukaryotic translation initiation factor 2 inhibits translation, induces stress granule formation, and mediates survival upon arsenite exposure. Journal of Biological Chemistry 2005, 280:16925-16933.
35. Mendez I.I., Hermann L.L., Hazelton P.R., Coombs K.M. A comparative analysis of Freon substitutes in the purification of reovirus and calicivirus. Journal of Virological Methods 2000, 90:59-67.
36. Miller C.L., Arnold M.M., Broering T.J., Hastings C.E., Nibert M.L. Localization of mammalian orthoreovirus proteins to cytoplasmic factory-like structures via nonoverlapping regions of μNS. Journal of Virology 2010, 84:867-882.
37. Miller C.L., Broering T.J., Parker J.S., Arnold M.M., Nibert M.L. Reovirus σNS protein localizes to inclusions through an association requiring the μNS amino terminus. Journal of Virology 2003, 77:4566-4576.
38. Miller C.L., Parker J.S., Dinoso J.B., Piggott C.D., Perron M.J., Nibert M.L. Increased ubiquitination and other covariant phenotypes attributed to a strain- and temperature-dependent defect of reovirus core protein μ2. Journal of Virology 2004, 78:10291-10302.
39. Mokas S., Mills J.R., Garreau C., Fournier M.J., Robert F., Arya P., Kaufman R.J., Pelletier J., Mazroui R. Uncoupling stress granule assembly and translation initiation inhibition. Molecular Biology of the Cell 2009, 20:2673-2683.
40. Mora M., Partin K., Bhatia M., Partin J., Carter C. Association of reovirus proteins with the structural matrix of infected-cells. Virology 1987, 159:265-277.
41. Nibert M.L., Fields B.N. A carboxy-terminal fragment of protein μ1/μ1C is present in infectious subvirion particles of mammalian reoviruses and is proposed to have a role in penetration. Journal of Virology 1992, 66:6408-6418.
42. Onomoto K., Jogi M., Yoo J.-S., Narita R., Morimoto S., et al. Critical role of an antiviral stress granule containing RIG-I and PKR in viral detection and innate immunity. PLoS ONE 2012, 7(8):e43031. http://dx.doi.org/10.1371/j.pone.0043031.
43. Pain V.M. Initiation of protein synthesis in eukaryotic cells. European Journal of Biochemistry 1996, 236:747-771.
44. Parashar U.D., Burton A., Lanata C., Boschi-Pinto C., Shibuya K., Steele D., Birmingham M., Glass R.I. Global mortality associated with rotavirus disease among children in 2004. Journal of Infectious Diseases 2009, 200:S9-S15.
45. Parker J.S.L., Broering T.J., Kim J., Higgins D.E., Nibert M.L. Reovirus core protein μ2 determines the filamentous morphology of viral inclusion bodies by interacting with and stabilizing microtubules. Journal of Virology 2002, 76:4483-4496.
46. Qin Q., Carroll K., Hastings C., Miller C.L. Mammalian orthoreovirus escape from host translational shutoff correlates with stress granule disruption and is independent of eIF2α phosphorylation and PKR. Journal of Virology 2011, 85:8798-8810.
47. Qin Q., Hastings C., Miller C.L. Mammalian orthoreovirus particles induce and are recruited into stress granules at early times postinfection. Journal of Virology 2009, 83:11090-11101.
48. Rhim J.S., Mayor H.D., Jordan L.E. Cytochemical, fluorescent-antibody and electron microscopic studies on growth of reovirus (ECHO 10) in tissue culture. Virology 1962, 17:342-355.
49. Samuel C.E., Duncan R., Knutson G.S., Hershey J.W.B. Mechanism of interferon action-increased phosphorylation of protein-synthesis initiation-factor eIF2α in interferon-treated, reovirus-infected mouse-L929 fibroblasts in vitro and in vivo. Journal of Biological Chemistry 1984, 259:3451-3457.
50. Schmechel S., Chute M., Skinner P., Anderson R., Schiff L. Preferential translation of reovirus mRNA by a σ3-dependent mechanism. Virology 1997, 232:62-73.
51. Schwartz-Cornil I., Mertens P., Contreras P.C., Hemati V., Pascale B., Bréard F., Mellor E., MacLachlan P.S., James N., Zientara S. Bluetongue virus: virology, pathogenesis and immunity. Veterinary Research 2008, 39:46.
52. Shatkin A.J., Both G.W. Reovirus messenger-RNA-transcription and translation. Cell 1976, 7:305-313.
53. Smith J.A., Schmechel S.C., Raghavan A., Abelson M., Reilly C., Katze M.G., Kaufman R.J., Bohjanen P.R., Schiff L.A. Reovirus induces and benefits from an integrated cellular stress response. Journal of Virology 2006, 80:2019-2033.
54. Smith J.A., Schmechel S.C., Williams B.R.G., Silverman R.H., Schiff L.A. Involvement of the interferon-regulated antiviral proteins PKR and RNase L in reovirus-induced shutoff of cellular translation. Journal of Virology 2005, 79:2240-2250.
55. Tao Y.Z., Farsetta D.L., Nibert M.L., Harrison S.C. RNA synthesis in a cage-structural studies of reovirus polymerase λ3. Cell 2002, 111:733-745.
56. Tourriere H., Chebli K., Zekri L., Courselaud B., Blanchard J.M., Bertrand E., Tazi J. The RasGAP-associated endoribonuclease G3BP assembles stress granules. Journal of Cell Biology 2003, 160:823-831.
57. Virgin H.W., Mann M.A., Fields B.N., Tyler K.L. Monoclonal-antibodies to reovirus reveal structure-function-relationships between capsid proteins and genetics of susceptibility to antibody action. Journal of Virology 1991, 65:6772-6781.
58. White J.P., Cardenas A.M., Marissen W.E., Lloyd R.E. Inhibition of cytoplasmic mRNA stress granule formation by a viral proteinase. Cell Host & Microbe 2007, 2:295-305.
59. White J.P., Lloyd R.E. Poliovirus unlinks TIA1 aggregation and mRNA stress granule formation. Journal of Virology 2011, 85:12442-12454.
60. Yi Z.G., Pan T.T., Wu X.F., Song W.H., Wang S.S., Xu Y., Rice C.M., MacDonald M.R., Yuan Z.H. Hepatitis C virus co-opts Ras-GTPase-activating protein-binding protein 1 for its genome replication. Journal of Virology 2011, 85:6996-7004.
61. Yue Z.Y., Shatkin A.J. Double-stranded RNA-dependent protein kinase (PKR) is regulated by reovirus structural proteins. Virology 1997, 234:364-371.
62. Zhang L., Chandran K., Nibert M.L., Harrison S.C. Reovirus μ1 structural rearrangements that mediate membrane penetration. Journal of Virology 2006, 80:12367-12376.
63. Zweerink H.J., Joklik W.K. Studies on intracellular synthesis of reovirus-specified proteins. Virology 1970, 41:501-518.