A new mechanism for nuclear import by actin-based propulsion used by a baculovirus nucleocapsid

Journal of Cell Science

Volumn 129, Issue 15, 2016, Pages 2905-2911

  Au, Shelly ^a   Wu, Wei ^a   Zhou, Lixin ^a   Theilmann, David A ^b   Panté, Nelly ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b SUMMERLAND RESEARCH AND DEVELOPMENT CENTRE   (Canada)

Author keywords

AcMNPV; Actin; Arp2 3 complex; Baculovirus; Nuclear import

Indexed keywords

ACTIN; ACTIN RELATED PROTEIN 2-3 COMPLEX; DIGITONIN; F ACTIN; G ACTIN; GUANOSINE 5' O (3 THIOTRIPHOSPHATE); IMPORTAZOLE; QUINAZOLINE DERIVATIVE; RAN PROTEIN;

ACTIN POLYMERIZATION; ARTICLE; AUTOGRAPHA CALIFORNICA; CELL NUCLEUS; CYTOPLASM; CYTOSOL; HUMAN; HUMAN CELL; NONHUMAN; NUCLEAR IMPORT; NUCLEAR PORE COMPLEX; PRIORITY JOURNAL; VIRUS NUCLEOCAPSID; BACULOVIRIDAE; CELL MEMBRANE PERMEABILITY; DRUG EFFECTS; HELA CELL LINE; METABOLISM; NUCLEAR PORE; NUCLEOCYTOPLASMIC TRANSPORT; POLYMERIZATION;

ACTIN-RELATED PROTEIN 2-3 COMPLEX; ACTINS; ACTIVE TRANSPORT, CELL NUCLEUS; BACULOVIRIDAE; CELL MEMBRANE PERMEABILITY; CELL NUCLEUS; CYTOSOL; DIGITONIN; GUANOSINE 5'-O-(3-THIOTRIPHOSPHATE); HELA CELLS; HUMANS; NUCLEAR PORE; NUCLEOCAPSID; NUCLEOPOLYHEDROVIRUS; POLYMERIZATION; QUINAZOLINES; RAN GTP-BINDING PROTEIN;

EID: 84988391899     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.191668     Document Type: Article

References (32)

1. Adam, S. A., Marr, R. S. and Gerace, L. (1990). Nuclear protein import in permeabilized mammalian cells requires soluble cytoplasmic factors. J. Cell Biol. 111, 807-816.
2. Au, S. and Panté, N. (2012). Nuclear transport of baculovirus: revealing the nuclear pore complex passage. J. Struct. Biol. 177, 90-98.
3. Au, S., Cohen, S. and Panté, N. (2010). Microinjection of Xenopus laevis oocytes as a system for studying nuclear transport of viruses. Methods 51, 114-120.
4. Au, S., Wu, W. and Panté, N. (2013). Baculovirus nuclear import: open, nuclear pore complex (NPC) sesame. Viruses 5, 1885-1900.
5. Biswas, S., Blissard, G.W. and Theilmann, D. A. (2016). Trichoplusia ni kinesin-1 associates with Autographa californica multiple nucleopolyhedrovirus nucleocapsid proteins and is required for production of budded virus. J. Virol. 90, 3480-3495.
6. Cassany, A. and Gerace, L. (2009). Reconstitution of nuclear import in permeabilized cells. Methods Mol. Biol. 464, 181-205.
7. Cautain, B., Hill, R., de Pedro, N. and Link, W. (2015). Components and regulation of nuclear transport processes. FEBS J. 282, 445-462.
8. Cohen, S. and Panté, N. (2005). Pushing the envelope: microinjection of Minute virus of mice into Xenopus oocytes causes damage to the nuclear envelope. J. Gen. Virol. 86, 3243-3252.
9. Cohen, S., Behzad, A. R., Carroll, J. B. and Pante, N. (2006). Parvoviral nuclear import: bypassing the host nuclear-transport machinery. J. Gen. Virol. 87, 3209-3213.
10. Dodding, M. P. and Way, M. (2011). Coupling viruses to dynein and kinesin-1. EMBO J. 30, 3527-3539.
11. Fay, N. and Panté, N. (2015a). Nuclear entry of DNA viruses. Front. Microbiol. 6, 467.
12. Fay, N. and Panté, N. (2015b). Old foes, new understandings: nuclear entry of small non-enveloped DNA viruses. Curr. Opin. Virol. 12, 59-65.
13. Firat-Karalar, E. N. and Welch, M. D. (2011). New mechanisms and functions of actin nucleation. Curr. Opin Cell Biol. 23, 4-13.
14. Goley, E. D., Ohkawa, T., Mancuso, J., Woodruff, J. B., D'Alessio, J. A., Cande, W. Z., Volkman, L. E. andWelch, M. D. (2006). Dynamic nuclear actin assembly by Arp2/3 complex and a baculovirus WASP-like protein. Science 314, 464-467.
15. Gorlich, D., Pante, N., Kutay, U., Aebi, U. and Bischoff, F. R. (1996). Identification of different roles for RanGDP and RanGTP in nuclear protein import. EMBO J. 15, 5584-5594.
16. Kumeta, M., Yamaguchi, H., Yoshimura, S. H. and Takeyasu, K. (2012). Karyopherin-independent spontaneous transport of amphiphilic proteins through the nuclear pore. J. Cell Sci. 125, 4979-4984.
17. Kutay, U., Izaurralde, E., Bischoff, F. R., Mattaj, I. W. and Görlich, D. (1997). Dominant-negative mutants of importin-beta block multiple pathways of import and export through the nuclear pore complex. EMBO J. 16, 1153-1163.
18. Lanier, L. M. and Volkman, L. E. (1998). Actin binding and nucleation byAutographa californiaM nucleopolyhedrovirus. Virology 243, 167-177.
19. Machesky, L. M., Insall, R. H. and Volkman, L. E. (2001). WASP homology sequences in baculoviruses. Trends Cell Biol. 11, 286-287.
20. Melchior, F., Paschal, B., Evans, J. and Gerace, L. (1993). Inhibition of nuclear protein import by nonhydrolyzable analogues of GTP and identification of the small GTPase Ran/TC4 as an essential transport factor. J. Cell Biol. 123, 1649-1659.
21. Mohr, D., Frey, S., Fischer, T., Güttler, T. and Görlich, D. (2009). Characterisation of the passive permeability barrier of nuclear pore complexes. EMBO J. 28, 2541-2553.
22. Mueller, J., Pfanzelter, J., Winkler, C., Narita, A., Le Clainche, C., Nemethova, M., Carlier, M.-F., Maeda, Y., Welch, M. D., Ohkawa, T. et al. (2014). Electron tomography and simulation of baculovirus actin comet tails support a tethered filament model of pathogen propulsion. PLoS Biol. 12, e1001765.
23. Nolen, B. J., Tomasevic, N., Russell, A., Pierce, D. W., Jia, Z., McCormick, C. D., Hartman, J., Sakowicz, R. and Pollard, T. D. (2009). Characterization of two classes of small molecule inhibitors of Arp2/3 complex. Nature 460, 1031-1034.
24. Ohkawa, T., Volkman, L. E. and Welch, M. D. (2010). Actin-based motility drives baculovirus transit to the nucleus and cell surface. J. Cell Biol. 190, 187-195.
25. O'Reilly, D. R., Miller, L. K. and Luckow, V. A. (1992). Baculovirus Expression Vectors: A Laboratory Manual. New York: Oxford University Press.
26. Pante, N. and Kann, M. (2002). Nuclear pore complex is able to transport macromolecules with diameters of ~39 nm. Mol. Biol. Cell 13, 425-434.
27. Rabe, B., Vlachou, A., Pante, N., Helenius, A. and Kann, M. (2003). Nuclear import of hepatitis B virus capsids and release of the viral genome. Proc. Natl. Acad. Sci. USA 100, 9849-9854.
28. Rohrmann, G. F. (2013). Baculovirus Molecular Biology, 3rd edn. Bethesda, MD: National Center for Biotechnology Information (US).
29. Soderholm, J. F., Bird, S. L., Kalab, P., Sampathkumar, Y., Hasegawa, K., Uehara-Bingen, M., Weis, K. and Heald, R. (2011). Importazole, a small molecule inhibitor of the transport receptor importin-beta. ACS Chem. Biol. 6, 700-708.
30. Takizawa, C. G., Weis, K. and Morgan, D. O. (1999). Ran-independent nuclear import of cyclin B1-Cdc2 by importin beta. Proc. Natl. Acad. Sci. USA 96, 7938-7943.
31. Wagstaff, K. M. and Jans, D. A. (2009). Importins and beyond: non-conventional nuclear transport mechanisms. Traffic 10, 1188-1198.
32. Wente, S. R. and Rout, M. P. (2010). The nuclear pore complex and nuclear transport. Cold Spring Harb. Perspect. Biol. 2, a000562.