Mutations at the base of the icosahedral five-fold cylinders of minute virus of mice induce 3'-to-5' genome uncoating and critically impair entry functions

Journal of Virology

Volumn 86, Issue 1, 2012, Pages 69-80

  Cotmore, Susan F ^a   Tattersall, Peter ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GENOMIC DNA; PROTEIN VP1; PROTEIN VP2; PROTEIN VP3;

3' UNTRANSLATED REGION; 5' UNTRANSLATED REGION; AMINO TERMINAL SEQUENCE; ARTICLE; CATION EXCHANGE; CONTROLLED STUDY; DNA TRANSFER; ENDOSOME; HIGH TEMPERATURE PROCEDURES; IN VITRO STUDY; NONHUMAN; NUCLEOTIDE SEQUENCE; PARVOVIRUS; PHENOTYPIC VARIATION; PRIORITY JOURNAL; PROGENY; PROTEIN DEGRADATION; PROTEIN DOMAIN; TEMPERATURE SENSITIVITY; VIRION; VIRUS ASSEMBLY; VIRUS ENTRY; VIRUS GENOME; VIRUS MUTANT; VIRUS MUTATION; VIRUS RELEASE; VIRUS UNCOATING; VIRUS VIABILITY; WILD TYPE;

ANIMALS; CELL LINE; DNA, SINGLE-STRANDED; DNA, VIRAL; GENOME, VIRAL; MICE; MINUTE VIRUS OF MICE; MUTATION; NUCLEIC ACID CONFORMATION; PARVOVIRIDAE INFECTIONS; RODENT DISEASES; VIRUS ASSEMBLY; VIRUS INTERNALIZATION; VIRUS REPLICATION;

MINUTE VIRUS OF MICE; MIRIDAE;

EID: 84855937996     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.06119-11     Document Type: Article

References (33)

1. Agbandje-McKenna M, Llamas-Saiz AL, Wang F, Tattersall P, Rossmann MG. 1998. Functional implications of the structure of the murine parvovirus, minute virus of mice. Structure 6:1369-1381.
2. Bleker S, Sonntag F, Kleinschmidt JA. 2005. Mutational analysis of narrow pores at the fivefold symmetry axes of adeno-associated virus type 2 capsids reveals a dual role in genome packaging and activation of phospholipase A2 activity. J. Virol. 79:2528-2540.
3. Bubeck D, et al. 2005. The structure of the poliovirus 135S cell entry intermediate at 10-angstrom resolution reveals the location of an externalized polypeptide that binds to membranes. J. Virol. 79:7745-7755.
4. Carrasco C, et al. 2009. The capillarity of nanometric water menisci confined inside closed-geometry viral cages. Proc. Natl. Acad. Sci. U. S. A. 106:5475-5480.
5. Chandran K, Parker JS, Ehrlich M, Kirchhausen T, Nibert ML. 2003. The delta region of outer-capsid protein micro 1 undergoes conforma-tional change and release from reovirus particles during cell entry. J. Virol. 77:13361-13375.
6. Cotmore SF, D'Abramo AM, Ticknor CM, Tattersall P. 1999. Controlled conformational transitions in the MVM virion expose the VP1 N-terminus and viral genome without particle disassembly. Virology 254: 169-181.
7. Cotmore SF, Hafenstein S, Tattersall P. 2010. Depletion of virionassociated divalent cations induces parvovirus minute virus of mice to eject its genome in a 3'-to-5' direction from an otherwise intact viral particle. J. Virol. 84:1945-1956.
8. Cotmore SF, Tattersall P. 1987. The autonomously replicating parvoviruses of vertebrates. Adv. Virus Res. 33:91-174.
9. Cotmore SF, Tattersall P. 2005. Encapsidation of minute virus of mice DNA: aspects of the translocation mechanism revealed by the structure of partially packaged genomes. Virology 336:100-112.
10. Cotmore SF, Tattersall P. 2007. Parvoviral host range and cell entry mechanisms. Adv. Virus Res. 70:183-232.
11. Farr GA, Cotmore SF, Tattersall P. 2006. VP2 cleavage and the leucine ring at the base of the fivefold cylinder control pH-dependent externalization of both the VP1 N terminus and the genome of minute virus of mice. J. Virol. 80:161-171.
12. Farr GA, Tattersall P. 2004. A conserved leucine that constricts the pore through the capsid fivefold cylinder plays a central role in parvoviral infection. Virology 323:243-256.
13. Farr GA, Zhang LG, Tattersall P. 2005. Parvoviral virions deploy a capsid-tethered lipolytic enzyme to breach the endosomal membrane during cell entry. Proc. Natl. Acad. Sci. U. S. A. 102:17148-17153.
14. Faust EA, Ward DC. 1979. Incomplete genomes of the parvovirus minute virus of mice: selective conservation of genome termini, including the origin for DNA replication. J. Virol. 32:276-292.
15. Gardiner EM, Tattersall P. 1988. Mapping of the fibrotropic and lymphotropic host range determinants of the parvovirus minute virus of mice. J. Virol. 62:2605-2613.
16. Govindasamy L, et al. 2010. MVM capsid dynamics associated with DNA packaging and VP2 externalization for maturation cleavage, poster P11. XIII International Parvovirus Workshop, Helsinki, Finland.
17. Hernando E, et al. 2000. Biochemical and physical characterization of parvovirus minute virus of mice virus-like particles. Virology 267: 299-309.
18. Hogle JM. 2002. Poliovirus cell entry: common structural themes in viral cell entry pathways. Annu. Rev. Microbiol. 56:677-702.
19. King JA, Dubielzig R, Grimm D, Kleinschmidt JA. 2001. DNA helicasemediated packaging of adeno-associated virus type 2 genomes into preformed capsids. EMBO J. 20:3282-3291.
20. Kontou M, et al. 2005. Structural determinants of tissue tropism and in vivo pathogenicity for the parvovirus minute virus of mice. J. Virol. 79: 10931-10943.
21. Llamas-Saizal, et al. 1997. Structure determination of minute virus of mice. Acta Crystallogr. D Biol. Crystallogr. 53:93-102.
22. Lombardo E, Ramírez JC, Garcia J, Almendral JM. 2002. Complementary roles of multiple nuclear targeting signals in the capsid proteins of the parvovirus minute virus of mice during assembly and onset of infection. J. Virol. 76:7049-7059.
23. Mani B, et al. 2006. Low pH-dependent endosomal processing of the incoming parvovirus minute virus of mice virion leads to externalization of the VP1 N-terminal sequence (N-VP1), N-VP2 cleavage, and uncoating of the full-length genome. J. Virol. 80:1015-1024.
24. Morgan WR, Ward DC. 1986. Three splicing patterns are used to excise the small intron common to all minute virus of mice RNAs. J. Virol. 60:1170-1174.
25. Plevka P, et al. 2011. Structure of a packaging-defective mutant of minute virus of mice indicates that the genome is packaged via a pore at a 5-fold axis. J. Virol. 85:4822-4827.
26. Reguera J, Carreira A, Riolobos L, Almendral JM, Mateu MG. 2004. Role of interfacial amino acid residues in assembly, stability, and conformation of a spherical virus capsid. Proc. Natl. Acad. Sci. U. S. A. 101: 2724-2729.
27. Sonntag F, Bleker S, Leuchs B, Fischer R, Kleinschmidt JA. 2006. Adeno-associated virus type 2 capsids with externalized VP1/VP2 trafficking domains are generated prior to passage through the cytoplasm and are maintained until uncoating occurs in the nucleus. J. Virol. 80: 11040-11054.
28. Suikkanen S, et al. 2003. Exploitation of microtubule cytoskeleton and dynein during parvoviral traffic toward the nucleus. J. Virol. 77: 10270-10279.
29. Tattersall P, Cawte PJ, Shatkin AJ, Ward DC. 1976. Three structural polypeptides coded for by minute virus of mice, a parvovirus. J. Virol. 20:273-289.
30. Tattersall P, Shatkin AJ, Ward DC. 1977. Sequence homology between the structural polypeptides of minute virus of mice. J. Mol. Biol. 111: 375-394.
31. Vihinen-Ranta M, Yuan W, Parrish CR. 2000. Cytoplasmic trafficking of the canine parvovirus capsid and its role in infection and nuclear transport. J. Virol. 74:4853-4859.
32. Yeung DE, et al. 1991. Monoclonal antibodies to the major nonstructural nuclear protein of minute virus of mice. Virology 181:35-45.
33. Zadori Z, et al. 2001. A viral phospholipase A2 is required for parvovirus infectivity. Dev. Cell 1:291-302.