Thermostabilizing mutations in reovirus outer-capsid protein μ1 selected by heat inactivation of infectious subvirion particles

Virology

Volumn 361, Issue 2, 2007, Pages 412-425

  Middleton, Jason K ^a,b   Agosto, Melina A ^c,d   Severson, Tonya F ^b   Yin, John ^a,b   Nibert, Max L ^c,d  

^a University of Wisconsin Madison   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d HARVARD UNIVERSITY   (United States)

Author keywords

Disassembly; Orthoreovirus; Reoviridae; Thermostability; Uncoating

Indexed keywords

PROTEINASE; VIRUS CAPSID ANTIGEN; VIRUS ENZYME;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; CORRELATION ANALYSIS; HEAT TOLERANCE; MUTATIONAL ANALYSIS; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; REOVIRUS; TEMPERATURE; THERMOSTABILITY; VIRAL GENETICS; VIRION; VIRUS CAPSID; VIRUS INFECTIVITY; VIRUS MUTATION; VIRUS STRAIN;

ANIMALS; CAPSID PROTEINS; CELL LINE; HEAT; MODELS, MOLECULAR; MOLECULAR WEIGHT; MUTATION; ORTHOREOVIRUS; REOVIRIDAE INFECTIONS; VIRULENCE; VIRUS INACTIVATION;

MAMMALIA; MIRIDAE; ORTHOREOVIRUS; REOVIRIDAE;

EID: 34147164393     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2006.11.024     Document Type: Article

References (51)

1. Baer G.S., and 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. 71 (1997) 4921-4928
2. Bodkin D., Nibert M.L., and Fields B.N. Proteolytic digestion of reovirus in the intestinal lumens of neonatal mice. J. Virol. 63 (1989) 4676-4681
3. Borsa J., Copps T.P., Sargent M.D., Long D.G., and Chapman J.D. New intermediate subviral particles in the in vitro uncoating of reovirus virions by chymotrypsin. J. Virol. 11 (1973) 552-564
4. Borsa J., Long D.G., Sargent M.D., Copps T.P., and Chapman J.D. Reovirus transcriptase activation in vitro: involvement of an endogenous uncoating activity in the second stage of the process. Intervirology 4 (1974) 171-188
5. Carr C.M., Chaudhry C., and Kim P.S. Influenza hemagglutinin is spring-loaded by a metastable native conformation. Proc. Natl. Acad. Sci. U.S.A. 94 (1997) 14306-14313
6. Chandran K., and Nibert M.L. Protease cleavage of reovirus capsid protein μ1/μ1C is blocked by alkyl sulfate detergents, yielding a new type of infectious subvirion particle. J. Virol. 72 (1998) 467-475
7. Chandran K., Walker S.B., Chen Y., Contreras C.M., Schiff L.A., Baker T.S., and Nibert M.L. In vitro recoating of reovirus cores with baculovirus-expressed outer-capsid proteins μ1 and σ3. J. Virol. 73 (1999) 3941-3950
8. Chandran K., Zhang X., Olson N.H., Walker S.B., Chappell J.D., Dermody T.S., Baker T.S., and Nibert M.L. 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 (2001) 5335-5342
9. Chandran K., Farsetta D.L., and Nibert M.L. Strategy for nonenveloped virus entry: a hydrophobic conformer of the reovirus membrane penetration protein μ1 mediates membrane disruption. J. Virol. 76 (2002) 9920-9933
10. Chandran K., Parker J.S.L., Ehrlich M., Kirchhausen T., and Nibert M.L. The δ region of outer-capsid protein μ1 undergoes conformational change and release from reovirus particles during cell entry. J. Virol. 77 (2003) 13361-13375
11. Chang C.T., and Zweerink H.J. Fate of parental reovirus in infected cell. Virology 46 (1971) 544-555
12. Chappell J.D., Barton E.S., Smith T.H., Baer G.S., Duong D.T., Nibert M.L., and Dermody T.S. Cleavage susceptibility of reovirus attachment protein σ1 during proteolytic disassembly of virions is determined by a sequence polymorphism in the σ1 neck. J. Virol. 72 (1998) 8205-8213
13. Coombs K.M. Stoichiometry of reovirus structural proteins in virus, ISVP, and core particles. Virology 243 (1998) 218-228
14. Curry S., Chow M., and Hogle J.M. The poliovirus 135S particle is infectious. J. Virol. 70 (1996) 7125-7131
15. Derrien M., Hooper J.W., and Fields B.N. The M2 gene segment is involved in the capacity of reovirus type 3Abney to induce the oily fur syndrome in neonatal mice, a S1 gene segment-associated phenotype. Virology 305 (2003) 25-30
16. Drayna D., and Fields B.N. Genetic studies on the mechanism of chemical and physical inactivation of reovirus. J. Gen. Virol. 63 (1982) 149-159
17. Dryden K.A., Wang G., Yeager M., Nibert M.L., Coombs K.M., Furlong D.B., Fields B.N., and Baker T.S. 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 (1993) 1023-1041
18. Ebert D.H., Deussing J., Peters C., and Dermody T.S. Cathepsin L and cathepsin B mediate reovirus disassembly in murine fibroblast cells. J. Biol. Chem. 277 (2002) 24609-24617
19. Furlong D.B., Nibert M.L., and Fields B.N. Sigma 1 protein of mammalian reoviruses extends from the surfaces of viral particles. J. Virol. 62 (1988) 246-256
20. Golden J.W., Bahe J.A., Lucas W.T., Nibert M.L., and Schiff L.A. Cathepsin S supports acid-independent infection by some reoviruses. J. Biol. Chem. 279 (2004) 8547-8557
21. Hooper J.W., and Fields B.N. Role of the μ1 protein in reovirus stability and capacity to cause chromium release from host cells. J. Virol. 70 (1996) 459-467
22. Jané-Valbuena J., Nibert M.L., Spencer S.M., Walker S.B., Baker T.S., Chen Y., Centonze V.E., and Schiff L.A. 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 (1999) 2963-2973
23. Jayasuriya A.K., Nibert M.L., and Fields B.N. Complete nucleotide sequence of the M2 gene segment of reovirus Type 3 Dearing and analysis of its protein product μ1. Virology 163 (1988) 591-602
24. Joklik W.K. Studies on the effect of chymotrypsin on reovirions. Virology 49 (1972) 700-715
25. Lehmann M., and Wyss M. Engineering proteins for thermostability: the use of sequence alignments versus rational design and directed evolution. Curr. Opin. Biotechnol. 12 (2001) 371-375
26. Liemann S., Chandran K., Nibert M.L., and Harrison S.C. Structure of the reovirus membrane-penetration protein, μ1, in a complex with is protector protein, σ3. Cell 108 (2002) 283-295
27. Lonberg-Holm K., Gosser L.B., and Shimshick E.J. Interaction of liposomes with subviral particles of poliovirus type 2 and rhinovirus type 2. J. Virol. 19 (1976) 746-749
28. Luria S.E., and Delbrück M. Mutations of bacteria from virus sensitivity to virus resistance. Genetics 28 (1943) 491-511
29. McCutcheon A.M., Broering T.J., and Nibert M.L. Mammalian reovirus M3 gene sequences and conservation of coiled-coil motifs near the carboxyl terminus of the μNS protein. Virology 264 (1999) 16-24
30. Middleton J.K., Severson T.F., Chandran K., Gillian A.L., Yin J., and Nibert M.L. Thermostability of reovirus disassembly intermediates (ISVPs) correlates with genetic, biochemical, and thermodynamic properties of major surface protein μ1. J. Virol. 76 (2002) 1051-1061
31. Nibert M.L., and 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. J. Virol. 66 (1992) 6408-6418
32. Nibert M.L., Schiff L.A., and Fields B.N. Mammalian reoviruses contain a myristoylated structural protein. J. Virol. 65 (1991) 1960-1970
33. Nibert M.L., Chappell J.D., and Dermody T.S. Infectious subvirion particles of reovirus Type 3 Dearing exhibit a loss in infectivity and contain a cleaved σ1 protein. J. Virol. 69 (1995) 5057-5067
34. Nibert M.L., Odegard A.L., Agosto M.A., Chandran K., and Schiff L.A. Putative autocleavage of reovirus μ1 protein in concert with outer-capsid disassembly and activation for membrane permeabilization. J. Mol. Biol. 345 (2005) 461-474
35. Odegard A.L., Chandran K., Zhang X., Parker J.S.L., Baker T.S., and Nibert M.L. Putative autocleavage of outer capsid protein μ1, allowing release of myristoylated peptide μ1N during particle uncoating, is critical for cell entry by reovirus. J. Virol. 78 (2004) 8732-8745
36. Perl D., and Schmid F.X. Some like it hot: the molecular determinants of protein thermostability. ChemBioChem 3 (2002) 39-44
37. Querol E., Perez-Pons J.A., and Mozo-Villarias A. Analysis of protein conformational characteristics related to thermostability. Protein Eng. 9 (1996) 265-271
38. Silverstein S.C., Schonberg M., Levin D.H., and Acs G. The reovirus replicative cycle: conservation of parental RNA and protein. Proc. Natl. Acad. Sci. U.S.A. 67 (1970) 275-281
39. Sturzenbecker L.J., Nibert M.L., Furlong D.B., and Fields B.N. Intracellular digestion of reovirus particles requires a low pH and is an essential step in the viral infectious cycle. J. Virol. 61 (1987) 2351-2361
40. Tsang S.K., Danthi P., Chow M., and Hogle J.M. Stabilization of poliovirus by capsid-binding antiviral drugs is due to entropic effects. J. Mol. Biol. 296 (2000) 335-340
41. Tsang S.K., McDermott B.M., Racaniello V.R., and Hogle J.M. Kinetic analysis of the effect of poliovirus receptor on viral uncoating: the receptor as a catalyst. J. Virol. 75 (2001) 4984-4989
42. van den Burg B., and Eijsink V.G. Selection of mutations for increased protein stability. Curr. Opin. Biotechnol. 13 (2002) 333-337
43. Vieille C., and Zeikus G.J. Hyperthermophilic enzymes: sources, uses, and molecular mechanisms for thermostability. Microbiol. Mol. Biol. Rev. 65 (2001) 1-43
44. Virgin IV H.W., Bassel-Duby R., and Tyler K.L. Antibody protects against lethal infection with the neurally spreading reovirus type 3 (Dearing). J. Virol. 62 (1988) 4594-4604
45. Wallin M., Ekstrom M., and Garoff H. The fusion-controlling disulfide bond isomerase in retrovirus Env is triggered by protein destabilization. J. Virol. 79 (2005) 1678-1685
46. Wessner D.R., and Fields B.N. Isolation and genetic characterization of ethanol-resistant reovirus mutants. J. Virol. 67 (1993) 2442-2447
47. Wetz K., and Kucinski T. Influence of different ionic and pH environments on structural alterations of poliovirus and their possible relation to virus uncoating. J. Gen. Virol. 72 (1991) 2541-2544
48. Wharton S.A., Skehel J.J., and Wiley D.C. Studies of influenza haemagglutinin-mediated membrane fusion. Virology 149 (1986) 27-35
49. Wiener J.R., and Joklik W.K. 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 (1988) 603-613
50. Zhang X., Ji Y., Zhang L., Harrison S.C., Marinescu D.C., Nibert M.L., and Baker T.S. Features of reovirus outer capsid protein μ1 revealed by electron cryomicroscopy and image reconstruction of the virion at 7.0 Å resolution. Structure 13 (2005) 1545-1557
51. Zhang L., Chandran K., Nibert M.L., and Harrison S.C. Reovirus μ1 structural rearrangements that mediate membrane penetration. J. Virol. 80 (2006) 12367-12376