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

Journal of Virology

Volumn 85, Issue 10, 2011, Pages 4822-4827

  Plevka, Pavel ^a   Hafenstein, Susan ^b   Li, Lei ^c   D'Abramo, Anthony ^c   Cotmore, Susan F ^c   Rossmann, Michael G ^a   Tattersall, Peter ^c  

^a PURDUE UNIVERSITY   (United States)

^b PENN STATE COLLEGE OF MEDICINE   (United States)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CAPSID PROTEIN; LEUCINE; PROTEIN VP2; TRYPTOPHAN;

AMINO ACID SUBSTITUTION; AMINO TERMINAL SEQUENCE; ARTICLE; CONTROLLED STUDY; CRYSTAL STRUCTURE; DNA PACKAGING; MOUSE; NONHUMAN; PARVOVIRUS; PRIORITY JOURNAL; VIRUS ENTRY; VIRUS GENOME; VIRUS MUTATION; VIRUS PARTICLE;

AMINO ACID SUBSTITUTION; ANIMALS; CAPSID; CAPSID PROTEINS; CRYSTALLOGRAPHY, X-RAY; DNA, VIRAL; LEUCINE; MINUTE VIRUS OF MICE; MUTATION, MISSENSE; PROTEIN STRUCTURE, QUATERNARY; TRYPTOPHAN; VIRUS ASSEMBLY;

MINUTE VIRUS OF MICE; MIRIDAE; PARVOVIRUS;

EID: 79955438650     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02598-10     Document Type: Article

References (43)

1. Agbandje-McKenna, M., A. L. Llamas-Saiz, F. Wang, P. Tattersall, and M. G. Rossmann. 1998. Functional implications of the structure of the murine parvovirus, minute virus of mice. Structure 6:1369-1381.
2. Arnold, E., and M. G. Rossmann. 1990. Analysis of the structure of a common cold virus, human rhinovirus 14, refined at a resolution of 3.0 Å. J. Mol. Biol. 211:763-801.
3. Bleker, S., M. Pawlita, and J. A. Kleinschmidt. 2006. Impact of capsid conformation and Rep.-capsid interactions on adeno-associated virus type 2 genome packaging. J. Virol. 80:810-820.
4. Bleker, S., F. Sonntag, and J. A. Kleinschmidt. 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 phospho-lipase A2 activity. J. Virol. 79:2528-2540.
5. Brünger, A. T., et al. 1998. Crystallography and NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr. D Biol. Crystallogr. 54:905-921.
6. Bubeck, D., D. J. Filman, and J. M. Hogle. 2005. Cryo-electron microscopy reconstruction of a poliovirus-receptor-membrane complex. Nat. Struct. Mol. Biol. 12:615-618.
7. Chapman, M. S., and M. G. Rossmann. 1993. Structure, sequence, and function correlations among parvoviruses. Virology 194:491-508.
8. Christensen, J., and P. Tattersall. 2002. Parvovirus initiator protein NS1 and RPA coordinate replication fork progression in a reconstituted DNA replication system. J. Virol. 76:6518-6531.
9. Collaborative Computational Project Number 4. 1994. The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D Biol. Crystallogr. 50:760-763.
10. Cotmore, S. F., A. M. D'Abramo, Jr., C. M. Ticknor, and P. Tattersall. 1999. Controlled conformational transitions in the MVM virion expose the VP1 N-terminus and viral genome without particle disassembly. Virology 254: 169-181.
11. Cotmore, S. F., S. Hafenstein, and P. Tattersall. 2010. Depletion of virion-associated divalent cations induces parvovirus minute virus of mice (MVM) to eject its genome in a 3'-to-5' direction from otherwise intact viral particles. J. Virol. 84:1945-1956.
12. Cotmore, S. F., and P. Tattersall. 2006. Parvoviruses, p. 593-608. In M. DePamphilis (ed.), DNA replication and human disease. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
13. Cotmore, S. F., and P. Tattersall. 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.
14. Cotmore, S. F., and P. Tattersall. 2005. Packaging sense is controlled by the efficiency of the nick site in the right-end replication origin of parvoviruses MSM and LuIII. J. Virol. 79:2287-2300.
15. Cotmore, S. F., and P. Tattersall. 2007. Parvoviral host range and cell entry mechanisms. Adv. Virus Res. 70:183-232.
16. Davis, I. W., et al. 2007. MolProbity: all-atom contacts and structure validation for proteins and nucleic acids. Nucleic Acids Res. 35:W375-W383.
17. Farr, G. A., S. F. Cotmore, and P. Tattersall. 2006. VP2 cleavage and the leucine ring at the base of the fivefold cylinder control pH-dependent exter-nalization of both the VP1 N terminus and the genome of minute virus of mice. J. Virol. 80:161-171.
18. Farr, G. A., and P. Tattersall. 2004. A conserved leucine that constricts the pore through the capsid fivefold cylinder plays a central role in parvoviral infection. Virology 323:243-256.
19. Gorbalenya, A. E., E. V. Koonin, and Y. I. Wolf. 1990. A new superfamily of putative NTP-binding domains encoded by genomes of small DNA and RNA viruses. FEBS Lett. 262:145-148.
20. Hafenstein, S., et al. 2007. Asymmetric binding of transferrin receptor to parvovirus capsids. Proc. Natl. Acad. Sci. U. S. A. 104:6585-6589.
21. Hickman, A. B., D. R Ronning, Z. N. Perez, R. M. Kotin, and F. Dyda. 2004. The nuclease domain of adeno-associated virus rep coordinates replication initiation using two distince DNA recognition interfaces. Mol. Cell 13:13.
22. Iyer, L. M., D. D. Leipe, E. V. Koonin, and L. Aravind. 2004. Evolutionary history and higher order classification of AAA+ ATPases. J. Struct. Biol. 146:11-31.
23. James, J. A., et al. 2003. Crystal structure of the SF3 helicase from adeno-associated virus type 2. Structure 11:1025-1035.
24. Jones, T. A., J. Y. Zou, S. W. Cowan, and M. Kjeldgaard. 1991. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr. A 47:110-119.
25. King, J. A., R. Dubielzig, S. W. Grimm, and J. A. Kleinschmidt. 2001. DNA helicase-mediated packaging of adeno-associated virus type 2 genomes into preformed capsids. EMBO J. 20:3282-3291.
26. Kleywegt, G. J., and R J. Read. 1997. Not your average density. Structure 5:1557-1569.
27. Koonin, E. V., and T. V. Ilyina. 1993. Computer-assisted dissection of rolling circle DNA replication. Biosystems 30:241-268.
28. Kronenberg, S., B. Bottcher, C. W. der Lieth, S. Bleker, and J. A. Kleinschmidt. 2005. A conformational change in the adeno-associated virus type 2 capsid leads to the exposure of hidden VP1 N termini. J. Virol. 79:5296-5303.
29. Llamas-Saiz, A. L., et al. 1997. Structure determination of minute virus of mice. Acta Crystallogr. D Biol. Crystallogr. 53:93-102.
30. Lombardo, E., J. C. Ramírez, J. Garcia, and J. M. Almendral. 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.
31. Maroto, B., N. Valle, R Saffrich, and J. M. Almendral. 2004. Nuclear export of the nonenveloped parvovirus virion is directed by an unordered protein signal exposed on the capsid surface. J. Virol. 78:10685-10694.
32. 2-3-containing DNA. Virology 251:123-131.
33. Myers, M. W., and B. J. Carter. 1980. Assembly of adeno-associated virus. Virology 102:71-82.
34. Nuesch, J. P., S. F. Cotmore, and P. Tattersall. 1995. Sequence motifs in the replicator protein of parvovirus MVM essential for nicking and covalent attachment to the viral origin: identification of the linking tyrosine. Virology 209:122-135.
35. Otwinowski, Z., and W. Minor. 1997. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276:307-326.
36. Richards, R, P. Linser, and R W. Armentrout. 1977. Kinetics of assembly of a parvovirus, minute virus of mice, in synchronized rat brain cells. J. Virol. 22:778-793.
37. Tattersall, P., et al. 2005. Parvoviridae, p. 593-608. In C. M. Fauquet, M. A Mayo, J. Maniloff, U. Desselberger, and L. A. Ball (ed.), Virus taxonomy-Eightht report of the International Committee on Taxonomy of Viruses. Elsevier Academic Press, London, England.
38. Tattersall, P., P. J. Cawte, A. J. Shatkin, and D. C. Ward. 1976. Three structural polypeptides coded for by minute virus of mice, a parvovirus. J. Virol. 20:273-289.
39. Tong, L., and M. G. Rossmann. 1997. Rotation function calculations with GLRF program. Methods Enzymol. 276:594-611.
40. Tsao, J., et al. 1991. The three-dimensional structure of canine parvovirus and its functional implications. Science 251:1456-1464.
41. Xie, Q., et al. 2002. The atomic structure of adeno-associated virus (AAV-2), a vector for human gene therapy. Proc. Natl. Acad. Sci. U. S. A. 99:10405-10410.
42. Yoon-Robarts, M., et al. 2004. Residues within the B' motif are critical for DNA binding by the SF3 helicase Rep40 of adeno-associated virus type 2. J. Biol. Chem. 279:50472-50481.
43. Yuan, W., and C. R. Parrish. 2001. Canine parvovirus capsid assembly and differences in mammalian and insect cells. Virology 279:546-557.