A slender tract of glycine residues is required for translocation of the VP2 protein N-terminal domain through the parvovirus MVM capsid channel to initiate infection

Biochemical Journal

Volumn 455, Issue 1, 2013, Pages 87-94

  Castellanos, Milagros ^a   Pérez, Rebeca ^a   Rodríguez Huete, Alicia ^a   Grueso, Esther ^a   Almendral, José M ^a   Mateu, Mauricio G ^a  

^a UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

Author keywords

Conformational dynamics; Macromolecular assembly; Peptide translocation; Structure function relationship; Virus entry and infection

Indexed keywords

ALANINE; GLYCINE; PROTEIN VP2;

ARTICLE; CONTROLLED STUDY; HUMAN; HUMAN CELL; HYDROPHOBIC INTERACTION CHROMATOGRAPHY; MUTATION; NONHUMAN; PARVOVIRUS; PARVOVIRUS INFECTION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; VIRION; VIRUS ENTRY; VIRUS INFECTIVITY; VIRUS MORPHOLOGY;

AMINO ACID SUBSTITUTION; ANIMALS; CAPSID; CAPSID PROTEINS; CELL LINE, TUMOR; CELL NUCLEUS; HUMANS; KINETICS; MICE; MINUTE VIRUS OF MICE; MODELS, MOLECULAR; MUTATION; PEPTIDES; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; THERMODYNAMICS; VIRION; VIRUS ASSEMBLY; VIRUS RELEASE;

EID: 84884222071     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20130503     Document Type: Article

References (51)

1. Chow, M., Yabrov, R., Bittle, J., Hogle, J. and Baltimore, D. (1985) Synthetic peptides from four separate regions of the poliovirus type capsid protein VP1 induce neutralizing antibodies. Proc. Natl. Acad. Sci. U.S.A. 82, 910-914 (Pubitemid 15142787)
2. Li, Q., Yafal, A. G., Lee, Y. M., Hogle, J. M. and Chow, M. (1994) Poliovirus neutralization by antibodies to internal epitopes of VP4 and VP1 results from reversible exposure of these sequences at physiological temperatures. J. Virol. 68, 3965-3970 (Pubitemid 24177422)
3. Bothner, B., Dong, X. F., Bibbs, L., Johnson, J. E. and Siuzdak, G. (1998) Evidence of viral capsid dynamics using limited proteolysis and mass spectrometry. J. Biol. Chem. 272, 672-676
4. Belnap, D. M., Filman, D. J., Trus, B. L., Cheng, N., Booy, F. P., Conway, F. J., Curry, S., Hiremath, C. N., Tsang, S. K., Steven, A. C. and Hogle, J. M. (2000) Molecular tectonic model of virus structural transitions: The putative cell entry states of poliovirus. J. Virol. 74, 1342-1354 (Pubitemid 30044084)
5. Tuma, R., Coward, L. U., Kirk, M. C., Barnes, S. and Prevelige, Jr, P. E. (2001) Hydrogen-Deuterium exchange as a probe of folding and assembly in viral capsids. J. Mol. Biol. 306, 389-396 (Pubitemid 33027709)
6. Hogle, J. M. (2002) Poliovirus cell entry: Common structural themes in viral cell entry pathways. Annu. Rev. Microbiol. 56, 677-702 (Pubitemid 35217471)
7. Valle, N., Riolobos, R. and Almendral, J. M. (2006) Synthesis, post-Translational modification and trafficking of the parvovirus structural polypeptides. In Parvoviruses (Kerr, J. R., Cotmore, S. F., Bloom, M. E., Linden, R. M. and Parrish, C. R., eds), pp. 291-304, Edward Arnold, London
8. Cotmore, S. F. and Tattersall, P. (2007) Parvoviral host range and cell entry mechanisms. Adv. Virus Res. 70, 183-232
9. Tuthill, T. J., Gropelli, E., Hogle, J. M. and Rowlands, D. J. (2010) Picornaviruses. Curr. Top. Microbiol. Immunol. 343, 43-89
10. Bothner, B. and Hilmer, J. K. (2011) Probing viral capsids in solution. In Structural Virology (Agbandje-McKenna, M. and McKenna, R., eds), pp. 41-61, RSC Publishing, London
11. Mateu, M. G. (2011) Virus engineering: Functionalization and stabilization. Protein Eng. Des. Sel. 24, 53-63
12. Feiss, M. and Rao, V. B. (2012) The bacteriophage DNA packaging machine. Adv. Exp. Med. Biol. 726, 489-509
13. Brown, J. C. and Newcomb, W. W. (2011) Herpesvirus capsid assembly: Insights from structural analysis. Curr. Opin. Virol. 1, 142-149
14. Tijssen, P., Agbandje-McKenna, M., Almendral, J. M., Bergoin, M., Flegel, T. W., Hedman, H., Kleinschmidt, J., Li, Y., Pintel, D. J. and Tattersall, P. (2011) Family Parvoviridae. In ICTV Report 2011, pp. 405-425
15. Agbandje-McKenna, M., Llamas-Saiz, A. L., Wang, F., Tattersall, P. and Rossmann, M. G. (1998) Functional implications of the structure of the murine parvovirus, minute virus of mice. Structure 6, 1369-1381 (Pubitemid 28541881)
16. Kontou, M., Govindasamy, L., Nam, H. J., Bryant, N., Llamas-Saiz, A. L., Foces-Foces, C., Hernando, E., Rubio, M. P., McKenna, R., Almendral, J. M. and Agbandje-McKenna, M. (2005) Structural determinants of tissue tropism and in vivo pathogenicity for the parvovirus minute virus of mice. J. Virol. 79, 10931-10943 (Pubitemid 41170635)
17. Tattersall, P., Shatkin, A. J. and Ward, D. C. (1977) Sequence homology between the structural polypeptides of minute virus of mice. J. Mol. Biol. 111, 375-394 (Pubitemid 8090354)
18. Maroto, B., Valle, N., Saffrich, R. and Almendral, J. M. (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 (Pubitemid 39258394)
19. Mani, B., Baltzer, C., Valle, N., Almendral, J. M., Kempf, C. and Ros, C. (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 (Pubitemid 43062912)
20. Cotmore, S. F., Hafenstein, S. and Tattersall, P. (2010) Depletion of virion-Associated divalent cations induces parvovirus minute virus of mice to eject its genome in a 3-To-5direction from an otherwise intact viral particle. J. Virol. 84, 1945-1956
21. Hernando, E., Llamas-Saiz, A. L., Foces-Foces, C., McKenna, R., Portman, I., Agbandje-McKenna, M. and Almendral, J. M. (2000) Biochemical and physical characterization of parvovirus minute virus of mice virus-Like particles. Virology 267, 299-309 (Pubitemid 30123612)
22. Carreira, A., Menendez, M., Reguera, J., Almendral, J. M. and Mateu, M. G. (2004) In vitro disassembly of a parvovirus capsid and effect on capsid stability of heterologous peptide insertions in surface loops. J. Biol. Chem. 279, 6517-6525 (Pubitemid 38248786)
23. Riolobos, L., Valle, N., Hernando, E., Maroto, B., Kann, M. and Almendral, J. M. (2010) Viral oncolysis that targets Raf-1 signalling control of nuclear transport. J. Virol. 84, 2090-2099
24. Zadori, Z., Szelei, J., Lacoste, M. C., Li, Y., Gariepy, S., Raymond, P., Allaire, M., Nabi, I. R. and Tijssen, P. (2001) A viral phospholipase A2 is required for parvovirus infectivity. Dev. Cell 1, 291-302 (Pubitemid 33653063)
25. Farr, G. A., Zhang, L. G. and 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 (Pubitemid 41692698)
26. Lombardo, E., Ramirez, J. C., Garcia, J. and Almendral, J. M. (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 (Pubitemid 41246219)
27. Vihinen-Ranta, M., Wang, D., Weichert, W. S. and Parrish, C. R. (2002) The VP1 N-Terminal sequence of canine parvovirus affects nuclear transport of capsids and efficient cell infection. J. Virol. 76, 1884-1891 (Pubitemid 34094635)
28. Sonntag, F., Bleker, S., Leuchs, B., Fischer, R. and Kleinschmidt, J. A. (2006) Adeno-Associated virus type 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 (Pubitemid 44706545)
29. Maroto, B., Ramirez, J. C. and Almendral, J. M. (2000) Phosphorylation status of the parvovirus minute virus of mice particle: Mapping and biological relevance of the major phosphorylation sites. J. Virol. 74, 10892-10902 (Pubitemid 32223953)
30. Śanchez-Mart́?nez, C., Grueso, E., Carroll, M., Rommelaere, J. and Almendral, J. M. (2012) Essential role of the unordered VP2 N-Terminal domain of the parvovirus MVM capsid in nuclear assembly and endosomal enlargement of the virion fivefold channel for cell entry. Virology, 432, 45-56
31. Tsao, J., Chapman, M. S., Agbandje, M., Keller, W., Smith, K., Wu, H., Luo, M., Smith, T. J., Rossmann, M. G., Compans, R. W. and Parrish, C. R. (1991) The three-Dimensional structure of canine parvovirus and its functional implications. Science 251, 1456-1464 (Pubitemid 121000431)
32. Chapman, M. S. and Rossmann, M. G. (1993) Structure, sequence, and function correlations among parvoviruses. Virology 194, 491-508
33. Wu, H. and Rossmann, M. G. (1993) The canine parvovirus empty capsid structure. J. Mol. Biol. 233, 231-244 (Pubitemid 23297593)
34. Simpson, A. A., Chipman, P. R., Baker, T. S., Tijssen, P. and Rossmann, M. G. (1998) The structure of an insect parvovirus (Galleria mellonella densovirus) at 3.7A° resolution. Structure 6, 1355-1367 (Pubitemid 28541880)
35. Kaufmann, B., Chipman, P. R., Kostyuchenko, V. A., Modrow, S. and Rossmann, M. G. (2008) Visualization of the externalized VP2 N termini of infectious parvovirus B19. J. Virol. 82, 7306-7312 (Pubitemid 352031199)
36. Gardiner, E. M. and Tattersall, P. (1988) Mapping of the fibrotropic and lymphotropic host range determinants of the parvovirus minute virus of mice. J. Virol. 62, 2605-2613
37. Reguera, J., Carreira, A., Riolobos, L., Almendral, J. M. and Mateu, M. G. (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 (Pubitemid 38327678)
38. Lombardo, E., Ramirez, J. C., Agbandje-McKenna, M. and Almendral, J. M. (2000) A β-Stranded motif drives capsid protein oligomers of the parvovirus minute virus of mice into the nucleus for viral assembly. J. Virol. 74, 3804-3814 (Pubitemid 30180323)
39. Riolobos, L., Reguera, J., Mateu, M. G. and Almendral, J. M. (2006) Nuclear transport of trimeric assembly intermediates exerts a morphogenetic control on the icosahedral parvovirus capsid. J. Mol. Biol. 357, 1026-1038
40. Kaufmann, B., Ĺopez-Bueno, A., Mateu, M. G., Chipman, P. R., Nelson, C. D., Parrish, C. R., Almendral, J. M. and Rossmann, M. G. (2007) Minute virus of mice, a parvovirus, in complex with the Fab fragment of a neutralizing monoclonal antibody. J. Virol. 81, 9851-9858 (Pubitemid 350067688)
41. Rubio, M. P., Ĺopez-Bueno, A. and Almendral, J. M. (2005) Virulent variants emerging in mice infected with the apathogenic prototype strain of the parvovirus minute virus of mice exhibit a capsid with low avidity for a primary receptor. J. Virol. 79, 11280-11290 (Pubitemid 41170670)
42. Xie, Q. and Chapman, M. S. (1996) Canine parvovirus capsid structure, analyzed at 2.9A° resolution. J. Mol. Biol. 264, 497-520 (Pubitemid 27010741)
43. Farr, G. A. and 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 (Pubitemid 38748472)
44. King, J. A., Dubielzig, R., Grimm, S. W. and Kleinschmidt, J. A. (2001) DNA helicase-Mediated packaging of adeno-Associated virus type genomes into preformed capsids. EMBO J. 20, 3282-3291 (Pubitemid 32612015)
45. Plevka, P., Susan Hafenstein, S., Li, L, D?Abramo, A., Cotmore, S. F., Rossmann, M. G. and Tattersall, P. (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
46. Nelson, C. D., Minkkinen, E., Bergkvist, M., Hoelzer, K., Fisher, M., Bothner, B. and Parrish, C. R. (2008) Detecting small changes and additional peptides in the canine parvovirus capsid structure. J. Virol 82, 10397-10407 (Pubitemid 352691145)
47. Castellanos, M., Ṕerez, R., Carrasco, C., Hernando-Ṕerez, M., Ǵomez-Herrero, J., De Pablo, P. J. and Mateu, M. G. (2012) Mechanical elasticity as a physical signature of conformational dynamics in a virus particle. Proc. Natl. Acad. Sci. U.S.A. 109, 12028-12033
48. Cotmore, S. F., D?Abramo, Jr, A. M., Ticknor, C. M. and Tattersall, P. (1999) Controlled conformational transitions in the MVM virion expose the VP1 N-Terminus and viral genome withour particle disassembly. Virology 254, 169-181 (Pubitemid 29391724)
49. Tullis, G. E., Burger, L. R. and Pintel, D. J. (1992) The trypsin-Sensitive RVER domain in the capsid proteins of minute virus of mice is required for efficient cell binding and viral infection but not for proteolytic processing in vivo. Virology 191, 846-857 (Pubitemid 23022489)
50. Cotmore, S. F. and Tattersall, P. (2012) 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. J. Virol. 86, 69-80
51. Farr, G. A., Cotmore, S. F. and 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