Reovirus nonstructural protein σ1s is required for establishment of viremia and systemic dissemination

Proceedings of the National Academy of Sciences of the United States of America

Volumn 106, Issue 47, 2009, Pages 19986-19991

  Boehme, Karl W ^a   Guglielmi, Kristen M ^a   Dermody, Terence S ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Mice; Pathogenesis; Tropism; Vector design

Indexed keywords

NONSTRUCTURAL PROTEIN OMEGA1S; PROTEIN OMEGA1S; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN; CENTRAL NERVOUS SYSTEM; GENE DISRUPTION; HEART; INOCULATION; INTESTINE; LIVER; MESENTERY LYMPH NODE; MOUSE; NEWBORN; NONHUMAN; NULL ALLELE; PATHOGENESIS; PEYER PATCH; PRIORITY JOURNAL; PROTEIN FUNCTION; REOVIRUS; STRAIN DIFFERENCE; TRANSLATION INITIATION; VIREMIA; VIROGENESIS; VIRUS DETECTION; VIRUS MUTANT; VIRUS REPLICATION; VIRUS STRAIN; VIRUS TITRATION; VIRUS VIRULENCE; WILD TYPE;

ANIMALS; ANIMALS, NEWBORN; BRAIN; CELLS, CULTURED; MAMMALIAN ORTHOREOVIRUS 3; MICE; MICE, INBRED C57BL; ORTHOREOVIRUS, MAMMALIAN; REOVIRIDAE INFECTIONS; VIRAL NONSTRUCTURAL PROTEINS; VIREMIA; VIRUS REPLICATION;

ANIMALIA; MURINAE; MUS; ORTHOREOVIRUS;

EID: 73949092033     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0907412106     Document Type: Article

References (50)

1. Nathanson N, Tyler KL (1997) Entry, dissemination, shedding, and transmission of viruses, in Viral Pathogenesis, ed Nathanson N (Lippincott-Raven, Philadelphia, PA), pp 13-33.
2. Fenner F (1949) Mousepox (infectious ectromelia of mice): A review. J Immunol 63:341-373.
3. Nibert ML, Schiff LA (2001) Reoviruses and their replication, in Fields Virology, eds Knipe DM, Howley PM, et al. (Lippincott Williams &Wilkins, Philadelphia, PA), 4th Ed, pp 1679-1728.
4. Tyler KL (2001) Mammalian reoviruses, in Fields Virology, eds Knipe DM, Howley PM, et al. (Lippincott Williams & Wilkins, Philadelphia, PA), 4th Ed, pp 1729-1745.
5. Weiner HL, Drayna D, Averill DR Jr, Fields BN (1977) Molecular basis of reovirus virulence: Role of the S1 gene. Proc Natl Acad Sci USA 74:5744-5748.
6. Weiner HL, Powers ML, Fields BN (1980) Absolute linkage of virulence and central nervous system tropism of reoviruses to viral hemagglutinin. J Infect Dis 141:609-616.
7. Tyler KL, McPhee DA, Fields BN (1986) Distinct pathways of viral spread in the host determined by reovirus S1 gene segment. Science 233:770-774.
8. Morrison LA, Sidman RL, Fields BN (1991) Direct spread of reovirus from the intestinal lumen to the central nervous system through vagal autonomic nerve fibers. Proc Natl Acad Sci USA 88:3852-3856.
9. Tardieu M, Weiner HL (1982) Viral receptors on isolated murine and human ependymal cells. Science 215:419-421.
10. Dichter MA,Weiner HL (1984) Infection of neuronal cell cultures with reovirus mimics in vitro patterns of neurotropism. Ann Neurol 16:603-610.
11. Sarkar G, et al. (1985) Identification of a new polypeptide coded by reovirus gene S1. J Virol 54:720-725.
12. Weiner HL, Ault KA, Fields BN (1980) Interaction of reovirus with cell surface receptors. I. Murine and human lymphocytes have a receptor for the hemagglutinin of reovirus type 3. J Immunol 124:2143-2148.
13. Ernst H, Shatkin AJ (1985) Reovirus hemagglutinin mRNA codes for two polypeptides in overlapping reading frames. Proc Natl Acad Sci USA 82:48-52.
14. Jacobs BL, Atwater JA, Munemitsu SM, Samuel CE (1985) Biosynthesis of reovirus-specified polypeptides. The s1 mRNA synthesized in vivo is structurally and functionally indistinguishable from in vitro-synthesized s1 mRNA and encodes two polypeptides, sigma 1a and sigma 1bNS. Virology 147:9-18.
15. Cashdollar LW, Chmelo RA, Wiener JR, Joklik WK (1985) Sequences of the S1 genes of the three serotypes of reovirus. Proc Natl Acad Sci USA 82:24-28.
16. Rodgers SE, Connolly JL, Chappell JD, Dermody TS (1998) Reovirus growth in cell culture does not require the full complement of viral proteins: Identification of a σ1s-null mutant. J Virol 72:8597-8604.
17. Poggioli GJ, Dermody TS, Tyler KL (2001) Reovirus-induced 1s-dependent G2/M cell cycle arrest results from inhibition of p34cdc2. J Virol 75:7429-7434.
18. Poggioli GJ, Keefer CJ, Connolly JL, Dermody TS, Tyler KL (2000) Reovirus-induced G2/M cell cycle arrest requires σ1s and occurs in the absence of apoptosis. J Virol 74:9562-9570.
19. Hoyt CC, et al. (2005) Nonstructural protein sigma1s is a determinant of reovirus virulence and influences the kinetics and severity of apoptosis induction in the heart and central nervous system. J Virol 79:2743-2753.
20. Kobayashi T, et al. (2007) A plasmid-based reverse genetics system for animal double-stranded RNA viruses. Cell Host Microbe 1:147-157.
21. Bodkin DK, Fields BN (1989) Growth and survival of reovirus in intestinal tissue: Role of the L2 and S1 genes. J Virol 63:1188-1193.
22. Bodkin DK, Nibert ML, FieldsBN(1989) Proteolytic digestion of reovirus in the intestinal lumens of neonatal mice. J Virol 63:4676-4681.
23. Cenatiempo Y, et al. (1984) Two initiation sites detected in the small s1 species of reovirus mRNA by dipeptide synthesis in vitro. Proc Natl Acad Sci USA 81:1084-1088.
24. Cashdollar LW, Blair P, Van Dyne S (1989) Identification of the σ1s protein in reovirus serotype 2-infected cells with antibody prepared against a bacterial fusion protein. Virology 168:183-186.
25. Belli BA, Samuel CE (1991) Biosynthesis of reovirus-specified polypeptides: Expression of reovirus S1 encoded sigma 1NS protein in transfected and infected cells as measured with serotype specific polyclonal antibody. Virology 185:698-709.
26. Barro M, Patton JT (2005) Rotavirus nonstructural protein 1 subverts innate immune response by inducing degradation of IFN regulatory factor 3. Proc Natl Acad Sci USA 102:4114-4119.
27. Wiertz E, et al. (1996) The human cytomegalovirus US11 gene product dislocates MHC class I heavy chains from the endoplasmic reticulum to the cytosol. Cell 84:769-779.
28. Celma CC, Roy P (2009) A viral nonstructural protein regulates bluetongue virus trafficking and release. J Virol 83:6806-6816.
29. Beaton AR, Rodriguez J, Reddy YK, Roy P (2002) The membrane trafficking protein calpactin forms a complex with bluetongue virus protein NS3 and mediates virus release. Proc Natl Acad Sci USA 99:13154-13159.
30. Schiff LA, Nibert ML, Tyler KL (2007) Orthoreoviruses and their replication, in Fields Virology, eds Knipe DM, Howley PM, et al. (Lippincott Williams&Wilkins, Philadelphia, PA), 5th Ed vol 2, pp 1853-1915.
31. Blom N, Gammeltoft S, Brunak S (1999) Sequence and structure-based prediction of eukaryotic protein phosphorylation sites. J Mol Biol 294:1351-1362.
32. Puntervoll P, et al. (2003) ELM server: A new resource for investigating short functional sites in modular eukaryotic proteins. Nucleic Acids Res 31:3625-3630.
33. Obenauer JC, Cantley LC, Yaffe MB (2003) Scansite 2.0: Proteome-wide prediction of cell signaling interactions using short sequence motifs. Nucleic Acids Res 31:3635-3641.
34. Strong JE, Tang D, LeePWK(1993) Evidence that the epidermal growth factor receptor on host cells confers reovirus infection efficiency. Virology 197:405-411.
35. Hashiro G, Loh PC, Yau JT (1977) The preferential cytotoxicity of reovirus for certain transformed cell lines. Arch Virol 54:307-315.
36. Strong JE, Coffey MC, Tang D, Sabinin P, Lee PW (1998) The molecular basis of viral oncolysis: Usurpation of the Ras signaling pathway by reovirus. EMBO J 17:3351-3362.
37. Strong JE, Lee PW (1996) The v-erbB oncogene confers enhanced cellular susceptibility to reovirus infection. J Virol 70:612-616.
38. Gu J, et al. (2007) H5N1 infection of the respiratory tract and beyond: A molecular pathology study. Lancet 370:1137-1145.
39. de Jong MD,et al. (2006) Fatal outcome of human influenza A (H5N1) is associated with high viral load and hypercytokinemia. Nat Med 12:1203-1207.
40. Kuiken T, et al. (2003) Newly discovered coronavirus as the primary cause of severe acute respiratory syndrome. Lancet 362:263-270.
41. Pallansch MA, Roos RP (2001) Enteroviruses: Polioviruses, coxsacieviruses, echoviruses, in Fields Virology, eds Knipe DM, Howley PM, et al. (Lippincott-Raven Press, Philadelphia, PA), 4th Ed, pp 723-775.
42. Antar AAR, et al. (2009) Junctional adhesion molecule-A is required for hematogenous dissemination of reovirus. Cell Host Microbe 5:59-71.
43. Furlong DB, Nibert ML, Fields BN (1988) Sigma 1 protein of mammalian reoviruses extends from the surfaces of viral particles. J Virol 62:246-256.
44. Smith RE, Zweerink HJ, Joklik WK (1969) Polypeptide components of virions, top component and cores of reovirus type 3. Virology 39:791-810.
45. Virgin HW IV, Bassel-Duby R, Fields BN, Tyler KL (1988) Antibody protects against lethal infection with the neurally spreading reovirus type 3 (Dearing). J Virol 62:4594-4604.
46. Barton ES, Connolly JL, Forrest JC, Chappell JD, Dermody TS (2001) Utilization of sialic acid as a coreceptor enhances reovirus attachment by multistep adhesion strengthening. J Biol Chem 276:2200-2211.
47. Danthi P, Coffey CM, Parker JS, Abel TW, Dermody TS (2008) Independent regulation of reovirus membrane penetration and apoptosis by the μ1 φ domain. PLoS Pathog 4:e1000248.
48. Harlin H, Reffey SB, Duckett CS, Lindsten T, Thompson CB (2001) Characterization of XIAP-deficient mice. Mol Cell Biol 21:3604-3608.
49. Tyler KL, Bronson RT, Byers KB, Fields BN (1985) Molecular basis of viral neurotropism: Experimental reovirus infection. Neurology 35:88-92.
50. Richardson BA, Overbaugh J (2005) Basic statistical considerations in virological experiments. J Virol 79:669-676.