Disulfide bonding among μ1 trimers in mammalian reovirus outer capsid: A late and reversible step in virion morphogenesis

Journal of Virology

Volumn 77, Issue 9, 2003, Pages 5389-5400

  Odegard, Amy L ^a,c   Chandran, Kartik ^a   Liemann, Susanne ^b   Harrison, Stephen C ^a   Nibert, Max L ^a,b  

^a Department of Microbiology ^*  (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYSTEINE; DIMER; PROTEIN MU1; PROTEIN SUBUNIT; SERINE PROTEINASE; UNCLASSIFIED DRUG; VIRUS PROTEIN; CAPSID PROTEIN; DISULFIDE; MU1 PROTEIN, REOVIRUS;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL DEATH; CELL VIABILITY; CONTROLLED STUDY; CRYSTAL STRUCTURE; DISULFIDE BOND; IN VITRO STUDY; MAMMAL; MEASUREMENT; MICROSCOPY; MORPHOGENESIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; REOVIRUS; VIRION; VIRUS CAPSID; VIRUS INFECTION; VIRUS INFECTIVITY; VIRUS PARTICLE; VIRUS PURIFICATION; ANIMAL; ARMYWORM; BACULOVIRUS; CELL CULTURE; CELL LINE; CHEMICAL STRUCTURE; CHEMISTRY; CRYOELECTRON MICROSCOPY; CRYSTALLOGRAPHY; DIMERIZATION; GENETICS; IMAGE PROCESSING; METABOLISM; ORTHOREOVIRUS; PATHOGENICITY; VIROLOGY; VIRUS ASSEMBLY;

ANIMALS; BACULOVIRIDAE; CAPSID; CAPSID PROTEINS; CELL LINE; CELLS, CULTURED; CRYOELECTRON MICROSCOPY; CRYSTALLOGRAPHY; DIMERIZATION; DISULFIDES; IMAGE PROCESSING, COMPUTER-ASSISTED; MICE; MODELS, MOLECULAR; ORTHOREOVIRUS, MAMMALIAN; SPODOPTERA; VIRION; VIRUS ASSEMBLY;

EID: 0037404548     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.77.9.5389-5400.2003     Document Type: Article

References (66)

1. Aslund, F., and J. Beckwith. 1999. Bridge over troubled waters: sensing stress by disulfide bond formation. Cell 96:751-753.
2. Attoui, H., Q. Fang, F. M. Jaafar, J. F. Cantaloube, P. Biagini, P. De Micco, and X. De Lamballerie. 2002. Common evolutionary origin of aquareoviruses and orthoreoviruses revealed by genome characterization of Golden shiner reovirus, Grass carp reovirus, Striped bass reovirus and golden ide reovirus (genus Aquareovirus, family Reoviridae). J. Gen. Virol. 83:1941-1951.
3. Barton, E. S., J. L. Connolly, J. C. Forrest, J. D. Chappell, and T. S. Dermody. 2000. Utilization of sialic acid as a coreceptor enhances reovirus attachment by multi-step adhesion-strengthening. J. Biol. Chem. 276:2200-2211.
4. Barton, E. S., J. C. Forrest, J. L. Connolly, J. D. Chappell, Y. Liu, F. J. Schnell, A. Nusrat, C. A. Parkos, and T. S. Dermody. 2001. Junction adhesion molecule is a receptor for reovirus. Cell 104:441-451.
5. Bodkin, D. K., M. L. Nibert, and B. N. Fields. 1989. Proteolytic digestion of reovirus in the intestinal lumens of neonatal mice. J. Virol. 63:4676-4681.
6. Braakman, I., H. Hoover-Litty, K. R. Wagner, and A. Helenius. 1991. Folding of influenza hemagglutinin in the endoplasmic reticulum. J. Cell Biol. 114:401-411.
7. Chandran, K., D. L. Farsetta, and M. L. Nibert. 2002. Strategy for nonenveloped virus entry: a hydrophobic conformer of the reovirus membrane penetration protein μ1 mediates membrane disruption. J. Virol. 76:9920-9933.
8. Chandran, K., S. B. Walker, Y. Chen, C. M. Contreras, L. A. Schiff, T. S. Baker, and M. L. Nibert. 1999. In vitro recoating of reovirus cores with baculovirus-expressed outer-capsid proteins μ1 and σ3. J. Virol. 73:3941-3950.
9. Chandran, K., X. Zhang, N. O. Olson, S. B. Walker, J. D. Chappell, T. S. Dermody, T. S. Baker, and M. L. Nibert. 2001. Complete in vitro assembly of the reovirus outer capsid produces highly infectious particles suitable for genetic studies of the receptor-binding protein. J. Virol. 75:5335-5342.
10. Chappell, J. D., A. E. Porta, T. S. Dermody, and T. Stehle. 2002. Crystal structure of reovirus attachment protein σ1 reveals evolutionary relationship to adenovirus fiber. EMBO J. 21:1-11.
11. Cleveland, D. R., H. Zarbl, and S. Millward. 1986. Reovirus guanylyltransferase is L2 gene product lambda 2. J. Virol. 60:307-311.
12. Cleveland, D. W. 1983. Peptide mapping in one dimension by limited proteolysis of sodium dodecyl sulfate-solubilized proteins. Methods Enzymol. 96:222-229.
13. Coombs, K. M. 1998. Stoichiometry of reovirus structural proteins in virus, ISVP, and core particles. Virology 243:218-228.
14. Drayna, D., and B. N. Fields. 1982. Activation and characterization of the reovirus transcriptase: genetic analysis. J. Virol. 41:110-118.
15. Dryden, K. A., D. L. Farsetta, G. Wang, J. M. Keegan, B. N. Fields, T. S. Baker, and M. L. Nibert. 1998. Internal structures containing transcriptaserelated proteins in top component particles of mammalian orthoreovirus. Virology 245:33-46.
16. Dryden, K. A., G. Wang, M. Yeager, M. L. Nibert, K. M. Coombs, D. B. Furlong, B. N. Fields, and T. S. Baker. 1993. Early steps in reovirus infection are associated with dramatic changes in supramolecular structure and protein conformation: analysis of virions and subviral particles by cryoelectron microscopy and image reconstruction. J. Cell Biol. 122:1023-1041.
17. Fausnaugh, J., and A. J. Shatkin. 1990. Active site localization in a viral mRNA capping enzyme. J. Biol. Chem. 265:7669-7672.
18. Furlong, D. B., M. L. Nibert, and B. N. Fields. 1988. Sigma 1 protein of mammalian reoviruses extends from the surfaces of viral particles. J. Virol. 62:246-256.
19. Hazelton, P. R., and K. M. Coombs. 1995. The reovirus mutant tsA279 has temperature-sensitive lesions in the M2 and L2 genes: the M2 gene is associated with decreased viral protein production and blockade in transmembrane transport. Virology 207:46-58.
20. Hooper, J. W., and B. N. Fields. 1996. Role of the μ1 protein in reovirus stability and capacity to cause chromium release from host cells. J. Virol. 70:459-467.
21. Huismans, H., and W. K. Joklik. 1976. Reovirus-coded polypeptides in infected cells: isolation of two native monomeric polypeptides with affinity for single-stranded and double-stranded RNA, respectively. Virology 70:411-424.
22. Ishizu, K. I., H. Watanabe, S. I. Han, S. N. Kanesashi, M. Hoque, H. Yajima, K. Kataoka, and H. Handa. 2001. Roles of disulfide linkage and calcium ion-mediated interactions in assembly and disassembly of virus-like particles composed of simian virus 40 VP1 capsid protein. J. Virol. 75:61-72.
23. Jané-Valbuena, J., M. L. Nibert, S. M. Spencer, S. B. Walker, T. S. Baker, Y. Chen, V. E. Centonze, and L. A. Schiff. 1999. Reovirus virion-like particles obtained by recoating infectious subvirion particles with baculovirus-expressed σ3 protein: an approach for analyzing σ3 functions during virus entry. J. Virol. 73:2963-2973.
24. Jayasuriya, A. K., M. L. Nibert, and B. N. Fields. 1988. Complete nucleotide sequence of the M2 gene segment of reovirus type 3 clearing and analysis of its protein product μ1. Virology 163:591-602.
25. Jayasuriya, A. K. A. 1991. Ph.D. thesis. Harvard University, Cambridge, Mass.
26. Kadokura, H., and J. Beckwith. 2001. The expanding world of oxidative protein folding. Nat. Cell Biol. 3:E247-E249.
27. Kraulis, P. J. 1991. MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallogr. 24:946-950.
28. Krishnaswamy, S., and M. G. Rossmann. 1990. Structural refinement and analysis of Mengo virus. J. Mol. Biol. 211:803-844.
29. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
30. Lee, P. W. K., E. C. Hayes, and W. K. Joklik. 1981. Protein σ1 is the reovirus cell attachment protein. Virology 108:156-163.
31. Li, M., P. Beard, P. A. Estes, M. K. Lyon, and R. L. Garcea. 1998. Intercapsomeric disulfide bonds in papillomavirus assembly and disassembly. J. Virol. 72:2160-2167.
32. Li, P. P., A. Nakanishi, S. W. Clark, and H. Kasamatsu. 2002. Formation of transitory intrachain and interchain disulfide bonds accompanies the folding and oligomerization of simian virus 40 Vp1 in the cytoplasm. Proc. Natl. Acad. Sci. USA 99:1353-1358.
33. Li, P. P., A. Nakanishi, M. A. Tran, A. M. Salazar, R. C. Liddington, and H. Kasamatsu. 2000. Role of simian virus 40 Vp1 cysteines in virion infectivity. J. Virol. 74:11388-11393.
34. Liemann, S., K. Chandran, T. S. Baker, M. L. Nibert, and S. C. Harrison. 2002. Structure of the reovirus membrane-penetration protein, μ1, in a complex with its protector protein, σ3. Cell 108:283-295.
35. Logan, D., R. Abu-Ghazaleh, W. Blakemore, S. Curry, T. Jackson, A. King, S. Lea, R. Lewis, J. Newman, N. Parry, et al. 1993. Structure of a major immunogenic site on foot-and-mouth disease virus. Nature 362:566-568.
36. Lucia-Jandris, P., J. W. Hooper, and B. N. Fields. 1993. Reovirus M2 gene is associated with chromium release from mouse L cells. J. Virol. 67:5339-5345.
37. Mallick, P., D. R. Boutz, D. Eisenberg, and T. O. Yeates. 2002. Genomic evidence that the intracellular proteins of archaeal microbes contain disulfide bonds. Proc. Natl. Acad. Sci. USA 99:9679-9684.
38. Mao, Z. X., and W. K. Joklik. 1991. Isolation and enzymatic characterization of protein λ2, the reovirus guanylyltransferase. Virology 185:377-386.
39. Martin, L. J. 2001. Neuronal cell death in nervous system development, disease, and injury. Int. J. Mol. Med. 7:455-478.
40. McGrath, W. J., K. S. Aherne, and W. F. Mangel. 2002. In the virion, the 11-amino-acid peptide cofactor pVIc is covalently linked to the adenovirus proteinase. Virology 296:234-240.
41. Merritt, E. A., and M. E. P. Murphy. 1994. Raster 3D version 2.0. A program for photorealistic molecular graphics. Acta Crystallogr. Sect. D. Biol. Crystallogr. 50:869-873.
42. Metcalf, P., M. Cyrklaff, and M. Adrian. 1991. The three-dimensional structure of reovirus obtained by cryo-electron microscopy. EMBO J. 10:3129-3136.
43. Middleton, J. K., T. F. Severson, K. Chandran, A. L. Gillian, J. Yin, and M. L. Nibert. 2002. Thermostability of reovirus disassembly intermediates (ISVPs) correlates with genetic, biochemical, and thermodynamic properties of major surface protein μ1. J. Virol. 76:1051-1061.
44. Mirazimi, A., and L. Svensson. 2000. ATP is required for correct folding and disulfide bond formation of rotavirus VP7. J. Virol. 74:8048-8052.
45. Nibert, M. L., and B. N. Fields. 1992. 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. J. Virol. 66:6408-6418.
46. Nibert, M. L., and L. A. Schiff. 2001. Reoviruses and their replication, p. 1679-1728. In D. M. Knipe and P. M. Howley (ed.), Fields virology, 4th ed. Lippincott Williams & Wilkins, Philadelphia, Pa.
47. Nibert, M. L., L. A. Schiff, and B. N. Fields. 1991. Mammalian reoviruses contain a myristoylated structural protein. J. Virol. 65:1960-1967.
48. Patton, J. T., J. Hua, and E. A. Mansell. 1993. Location of intrachain disulfide bonds in the VP5* and VP8* trypsin cleavage fragments of the rhesus rotavirus spike protein VP4. J. Virol. 67:4848-4855.
49. Pias, E. K., and T. Y. Aw. 2002. Apoptosis in mitotic competent undifferentiated cells is induced by cellular redox imbalance independent of reactive oxygen species production. FASEB J. 16:781-790.
50. Qiu, T., R. H. Lu, J. Zhang, and Z. Y. Zhu. 2001. Molecular characterization and expression of the M6 gene of grass carp hemorrhage virus (GCHV), an aquareovirus. Arch. Virol. 146:1391-1397.
51. Reinisch, K. M., M. L. Nibert, and S. C. Harrison. 2000. Structure of the reovirus core at 3.6 Å resolution. Nature 404:960-967.
52. Rietsch, A., and J. Beckwith. 1998. The genetics of disulfide bond metabolism. Annu. Rev. Genet. 32:163-184.
53. Schmidt, U., R. Rudolph, and G. Bohm. 2000. Mechanism of assembly of recombinant murine polyomavirus-like particles. J. Virol. 74:1658-1662.
54. Segal, M. S., J. M. Bye, J. F. Sambrook, and M. J. Gething. 1992. Disulfide bond formation during the folding of influenza virus hemagglutinin. J. Cell Biol. 118:227-244.
55. Senkevich, T. G., C. L. White, E. V. Koonin, and B. Moss. 2002. Complete pathway for protein disulfide bond formation encoded by poxviruses. Proc. Natl. Acad. Sci. USA 99:6667-6672.
56. Senkevich, T. G., C. L. White, E. V. Koonin, and B. Moss. 2000. A viral member of the ERV1/ALR protein family participates in a cytoplasmic pathway of disulfide bond formation. Proc. Natl. Acad. Sci. USA 97:12068-12073.
57. Shing, M., and K. M. Coombs. 1996, Assembly of the reovirus outer capsid requires μ1/σ3 interactions which are prevented by misfolded σ3 protein in temperature-sensitive mutant tsG453. Virus Res. 46:19-29.
58. Smith, R. E., H. J. Zweerink, and W. K. Joklik. 1969. Polypeptide components of virions, top component and cores of reovirus type 3. Virology 39:791-810.
59. Spencer, S. M., J. Y. Sgro, K. A. Dryden, T. S. Baker, and M. L. Nibert. 1997. IRIS explorer software for radial-depth cueing reovirus particles and other macromolecular structures determined by cryoelectron microscopy and image reconstruction. J. Struct. Biol. 120:11-21.
60. Strong, J. E., G. Leone, R. Duncan, R. K. Sharma, and P. W. K. Lee. 1991. Biochemical and biophysical characterization of the reovirus cell attachment protein σ1: evidence that it is a homotrimer. Virology 184:23-32.
61. Sturzenbecker, L. J., M. Nibert, D. Furlong, and B. N. Fields. 1987. Intracellular digestion of reovirus particles requires a low pH and is an essential step in the viral infectious cycle. J. Virol. 61:2351-2361.
62. Tijssen, P., and E. Kurstak. 1981. Biochemical, biophysical, and biological properties of densonucleosis virus (parvovirus). III. Common sequences of structural proteins. J. Virol. 37:17-23.
63. Tyler, K. L., P. Clarke, R. L. DeBiasi, D. Kominsky, and G. J. Poggioli. 2001. Reoviruses and the host cell. Trends Microbiol. 9:560-564.
64. White, C. K., and H. J. Zweerink. 1976. Studies on the structure of reovirus cores: selective removal of polypeptide λ2. Virology 70:171-180.
65. White, C. L., T. G. Senkevich, and B. Moss. 2002. Vaccinia virus G4L glutaredoxin is an essential intermediate of a cytoplasmic disulfide bond pathway required for virion assembly. J. Virol. 76:467-472.
66. Wiener, J. R., and W. K. Joklik. 1988. Evolution of reovirus genes: a comparison of serotype 1, 2, and 3 M2 genome segments, which encode the major structural capsid protein μ1C. Virology 163:603-613.