The viroporin activity of the minor structural proteins VP2 and VP3 is required for SV40 propagation

Journal of Biological Chemistry

Volumn 288, Issue 4, 2013, Pages 2510-2520

  Giorda, Kristina M ^a   Raghava, Smita ^a   Zhang, MacY W ^a   Hebert, Daniel N ^a  

^a UNIVERSITY OF MASSACHUSETTS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ENDOPLASMIC RETICULUM MEMBRANES; HYDROPHOBIC DOMAINS; MEMBRANE DISRUPTION; MEMBRANE INSERTION; MEMBRANE PROTEINS; MODEL PROTEINS; PORE FORMATION; SIMIAN VIRUS; STRUCTURAL PROTEINS; TRANS-MEMBRANE DOMAINS; VIRAL GENOME; VIRAL INFECTIONS; VIRAL PROPAGATION;

ACTIVATION ANALYSIS; CELL MEMBRANES; CYTOLOGY; HYDROPHOBICITY; MEMBRANES; VIRUSES;

PROTEINS;

PROTEIN VP2; PROTEIN VP3;

ARTICLE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; HOST CELL; HYDROPHOBICITY; INHIBITION KINETICS; MUTATIONAL ANALYSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; SIMIAN VIRUS 40; STRUCTURE ANALYSIS;

ANIMALS; CAPSID PROTEINS; CERCOPITHECUS AETHIOPS; COS CELLS; GENES, VPU; GENOME, VIRAL; GLUTATHIONE TRANSFERASE; HUMAN IMMUNODEFICIENCY VIRUS PROTEINS; MEMBRANE PROTEINS; MODELS, BIOLOGICAL; MUTATION; PLASMIDS; PROTEIN ENGINEERING; PROTEIN STRUCTURE, TERTIARY; SIMIAN VIRUS 40; VIRAL REGULATORY AND ACCESSORY PROTEINS;

EID: 84873808430     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.428425     Document Type: Article

References (40)

1. Campanero-Rhodes, M. A., Smith, A., Chai, W., Sonnino, S., Mauri, L., Childs, R. A., Zhang, Y., Ewers, H., Helenius, A., Imberty, A., and Feizi, T. (2007) N-glycolyl GM1 ganglioside as a receptor for simian virus 40. J. Virol. 81, 12846-12858
2. Tsai, B., Gilbert, J. M., Stehle, T., Lencer, W., Benjamin, T. L., and Rapoport, T. A. (2003) Gangliosides are receptors for murine polyoma virus and SV40. EMBO J. 22, 4346-4355
3. Anderson, H. A., Chen, Y., and Norkin, L. C. (1996) Bound simian virus 40 translocates to caveolin-enriched membrane domains, and its entry is inhibited by drugs that selectively disrupt caveolae. Mol. Biol. Cell 7, 1825-1834
4. Schelhaas, M., Malmström, J., Pelkmans, L., Haugstetter, J., Ellgaard, L., Grünewald, K., and Helenius, A. (2007) Simian Virus 40 depends on ER protein folding and quality control factors for entry into host cells. Cell 131, 516-529
5. Reddy, V. B., Thimmappaya, B., Dhar, R., Subramanian, K. N., Zain, B. S., Pan, J., Ghosh, P. K., Celma, M. L., and Weissman, S. M. (1978) The genome of simian virus 40. Science 200, 494-502
6. Fiers, W., Contreras, R., Haegemann, G., Rogiers, R., Van de Voorde, A., Van Heuverswyn, H., Van Herreweghe, J., Volckaert, G., and Ysebaert, M. (1978) Complete nucleotide sequence of SV40 DNA. Nature 273, 113-120
7. Stehle, T., Gamblin, S. J., Yan, Y., and Harrison, S. C. (1996) The structure of simian virus 40 refined at 3.1 A resolution. Structure 4, 165-182
8. Chen, X. S., Stehle, T., and Harrison, S. C. (1998) Interaction of polyomavirus internal protein VP2 with the major capsid protein VP1 and implications for participation of VP2 in viral entry. EMBO J. 17, 3233-3240
9. Pelkmans, L., Püntener, D., and Helenius, A. (2002) Local actin polymerization and dynamin recruitment in SV40-induced internalization of caveolae. Science 296, 535-539
10. Damm, E. M., Pelkmans, L., Kartenbeck, J., Mezzacasa, A., Kurzchalia, T., and Helenius, A. (2005) Clathrin- and caveolin-1-independent endocytosis: entry of simian virus 40 into cells devoid of caveolae. J. Cell Biol. 168, 477-488
11. Engel, S., Heger, T., Mancini, R., Herzog, F., Kartenbeck, J., Hayer, A., and Helenius, A. (2011) The role of endosomes in SV40 entry and infection. J. Virol. 85, 4198-4211
12. Geiger, R., Andritschke, D., Friebe, S., Herzog, F., Luisoni, S., Heger, T., and Helenius, A. (2011) BAP31 and BiP are essential for dislocation of SV40 from the endoplasmic reticulum to the cytosol. Nat. Cell Biol. 13, 1305-1314
13. Kawano, M. A., Inoue, T., Tsukamoto, H., Takaya, T., Enomoto, T., Takahashi, R. U., Yokoyama, N., Yamamoto, N., Nakanishi, A., Imai, T., Wada, T., Kataoka, K., and Handa, H. (2006) The VP2/VP3 minor capsid protein of simian virus 40 promotes the in vitro assembly of the major capsid protein VP1 into particles. J. Biol. Chem. 281, 10164-10173
14. Daniels, R., Rusan, N. M., Wadsworth, P., and Hebert, D. N. (2006) SV40 VP2 and VP3 Insertion into ER Membranes Is Controlled by the Capsid Protein VP1: Implications for DNA Translocation out of the ER. Mol. Cell 24, 955-966
15. Raghava, S., Giorda, K. M., Romano, F. B., Heuck, A. P., and Hebert, D. N. (2011) The SV40 Late Protein VP4 Is a Viroporin that Forms Pores to Disrupt Membranes for Viral Release. PLoS Pathog. 7, e1002116
16. Giorda, K. M., Raghava, S., and Hebert, D. N. (2012) The Simian Virus 40 Late Viral Protein VP4 Disrupts the Nuclear Envelope for Viral Release. J. Virol. 86, 3180-3192
17. Lundin, C., Kim, H., Nilsson, I., White, S. H., and von Heijne, G. (2008) Molecular code for protein insertion in the endoplasmic reticulum membrane is similar for N(in)-C(out) and N(out)-C(in) transmembrane helices. Proc. Natl. Acad. Sci. U.S.A. 105, 15702-15707
18. Hessa, T., Kim, H., Bihlmaier, K., Lundin, C., Boekel, J., Andersson, H., Nilsson, I., White, S. H., and von Heijne, G. (2005) Recognition of transmembrane helices by the endoplasmic reticulum translocon. Nature 433, 377-381
19. Daniels, R., Rusan, N. M., Wilbuer, A. K., Norkin, L. C., Wadsworth, P., and Hebert, D. N. (2006) Simian virus 40 late proteins possess lytic properties that render them capable of permeabilizing cellular membranes. J. Virol. 80, 6575-6587
20. Brogden, K. A. (2005) Antimicrobial peptides: pore formers or metabolic inhibitors in bacteria? Nat. Rev. Microbiol. 3, 238-250
21. Scherrer, R., Cabrera Beaman, T., and Gerhardt, P. (1971) Macromolecular sieving by the dormant spore of Bacillus cereus. J. Bacteriol. 108, 868-873
22. von Heijne, G. (2006) Membrane-protein topology. Nat. Rev. Mol. Cell Biol. 7, 909-918
23. Claros, M. G., and von Heijne, G. (1994) TopPred II: an improved software for membrane protein structure predictions. Comput. Appl. Biosci. 10, 685-686
24. Shen, H., and Chou, J. J. (2008) MemBrain: improving the accuracy of predicting transmembrane helices. PLoS One 3, e2399
25. Jones, D. T. (2007) Improving the accuracy of transmembrane protein topology prediction using evolutionary information. Bioinformatics 23, 538-544
26. Hessa, T., Meindl-Beinker, N. M., Bernsel, A., Kim, H., Sato, Y., Lerch- Bader, M., Nilsson, I., White, S. H., and von Heijne, G. (2007) Molecular code for transmembrane-helix recognition by the Sec61 translocon. Nature 450, 1026-1030
27. Moore, K. E., and Miura, S. (1987) A small hydrophobic domain anchors leader peptidase to the cytoplasmic membrane of Escherichia coli. J. Biol. Chem. 262, 8806-8813
28. Drayman, N., Kler, S., Ben-nun-Shaul, O., and Oppenheim, A. (2010) Rapid method for SV40 titration. J. Virol. Methods 164, 145-147
29. Sedman, S. A., Good, P. J., and Mertz, J. E. (1989) Leader-encoded open reading frames modulate both the absolute and relative rates of synthesis of the virion proteins of simian virus 40. J. Virol. 63, 3884-3893
30. Good, P. J., Welch, R. C., Barkan, A., Somasekhar, M. B., and Mertz, J. E. (1988) Both VP2 and VP3 are synthesized from each of the alternative spliced late 19S RNA species of simian virus 40. J. Virol. 62, 944-953
31. Yu, Y., and Alwine, J. C. (2006) 19S late mRNAs of simian virus 40 have an internal ribosome entry site upstream of the virion structural protein 3 coding sequence. J. Virol. 80, 6553-6558
32. Lai, C. J., Dhar, R., and Khoury, G. (1978) Mapping the spliced and unspliced late lytic SV40 RNAs. Cell 14, 971-982
33. Streuli, C. H., and Griffin, B. E. (1987) Myristic acid is coupled to a structural protein of polyoma virus and SV40. Nature 326, 619-622
34. Johne, R., Buck, C. B., Allander, T., Atwood, W. J., Garcea, R. L., Imperiale, M. J., Major, E. O., Ramqvist, T., and Norkin, L. C. (2011) Taxonomical developments in the family Polyomaviridae. Arch. Virol. 156, 1627-1634
35. Liddington, R. C., Yan, Y., Moulai, J., Sahli, R., Benjamin, T. L., and Harrison, S. C. (1991) Structure of Simian virus 40 at 3.8-Å resolution. Nature 354, 278-284
36. Martin, K., and Helenius, A. (1991) Nuclear transport of influenza virus ribonucleoproteins: the viral matrix protein (M1) promotes export and inhibits import. Cell 67, 117-130
37. Rossman, J. S., Jing, X., Leser, G. P., and Lamb, R. A. (2010) Influenza virus M2 protein mediates ESCRT-independent membrane scission. Cell 142, 902-913
38. Boson, B., Granio, O., Bartenschlager, R., and Cosset, F. L. (2011) A concerted action of hepatitis C virus p7 and nonstructural protein 2 regulates core localization at the endoplasmic reticulum and virus assembly. PLoS Pathog. 7, e1002144
39. Jones, C. T., Murray, C. L., Eastman, D. K., Tassello, J., and Rice, C. M. (2007) Hepatitis C virus p7 and NS2 proteins are essential for production of infectious virus. J. Virol. 81, 8374-8383
40. Suzuki, T., Orba, Y., Okada, Y., Sunden, Y., Kimura, T., Tanaka, S., Nagashima, K., Hall, W. W., and Sawa, H. (2010) The human polyoma JC virus agnoprotein acts as a viroporin. PLoS Pathog. 6, e1000801