Old foes, new understandings: Nuclear entry of small non-enveloped DNA viruses

Current Opinion in Virology

Volumn 12, Issue , 2015, Pages 59-65

  Fay, Nikta ^a   Panté, Nelly ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

VIRUS NUCLEOPROTEIN; DNA VIRUS; VIRUS DNA;

ADENOVIRIDAE; ELECTRON MICROSCOPY; ENDOCYTOSIS; ENDOPLASMIC RETICULUM; NONHUMAN; NUCLEAR IMPORT; NUCLEAR PORE COMPLEX; PARVOVIRIDAE; PRIORITY JOURNAL; REVIEW; SIMIAN VIRUS 40; VIRUS ENTRY; VIRUS GENOME; ACTIVE TRANSPORT; CELL NUCLEUS; GENETICS; HUMAN; METABOLISM; NUCLEAR PORE; PHYSIOLOGY; VIROLOGY; VIRUS REPLICATION;

ACTIVE TRANSPORT, CELL NUCLEUS; ADENOVIRIDAE; CELL NUCLEUS; DNA VIRUSES; DNA, VIRAL; GENOME, VIRAL; HUMANS; NUCLEAR PORE; PARVOVIRUS; SIMIAN VIRUS 40; VIRUS INTERNALIZATION; VIRUS REPLICATION;

EID: 84926294975     PISSN: 18796257     EISSN: 18796265     Source Type: Journal    
DOI: 10.1016/j.coviro.2015.03.017     Document Type: Review

References (60)

1. S.R. Wente, and M.P. Rout The nuclear pore complex and nuclear transport Cold Spring Harb Perspect Biol 2 2010 a000562
2. S. Cohen, S. Au, and N. Pante How viruses access the nucleus Biochim Biophys Acta 1813 2011 1634 1645
3. A.J. Fulcher, and D.A. Jans Regulation of nucleocytoplasmic trafficking of viral proteins: an integral role in pathogenesis? Biochim Biophys Acta 1813 2011 2176 2190
4. L. Caly, K.M. Wagstaff, and D.A. Jans Nuclear trafficking of proteins from RNA viruses: potential target for antivirals? Antiviral Res 95 2012 202 206
5. N. Pante, and M. Kann Nuclear pore complex is able to transport macromolecules with diameters of about 39 nm Mol Biol Cell 13 2002 425 434
6. S. Au, and N. Pante Nuclear transport of baculovirus: revealing the nuclear pore complex passage J Struct Biol 177 2012 90 98
7. K.A. Matreyek, and A. Engelman Viral and cellular requirements for the nuclear entry of retroviral preintegration nucleoprotein complexes Viruses 5 2013 2483 2511
8. F. Di Nunzio New insights in the role of nucleoporins: a bridge leading to concerted steps from HIV-1 nuclear entry until integration Virus Res 178 2013 187 196
9. E.C. Hutchinson, and E. Fodor Transport of the influenza virus genome from nucleus to nucleus Viruses 5 2013 2424 2446
10. S. Boulo, H. Akarsu, R.W. Ruigrok, and F. Baudin Nuclear traffic of influenza virus proteins and ribonucleoprotein complexes Virus Res 124 2007 12 21
11. A.J. Eisfeld, G. Neumann, and Y. Kawaoka At the centre: influenza A virus ribonucleoproteins Nat Rev Microbiol 13 2015 28 41
12. I. Liashkovich, W. Hafezi, J.M. Kuhn, H. Oberleithner, and V. Shahin Nuclear delivery mechanism of herpes simplex virus type 1 genome J Mol Recognit 24 2011 414 421
13. P.M. Ojala, B. Sodeik, M.W. Ebersold, U. Kutay, and A. Helenius Herpes simplex virus type 1 entry into host cells: reconstitution of capsid binding and uncoating at the nuclear pore complex in vitro Mol Cell Biol 20 2000 4922 4931
14. L.C. Trotman, N. Mosberger, M. Fornerod, R.P. Stidwill, and U.F. Greber Import of adenovirus DNA involves the nuclear pore complex receptor CAN/Nup214 and histone H1 Nat Cell Biol 3 2001 1092 1100
15. B. Rabe, A. Vlachou, N. Pante, A. Helenius, and M. Kann Nuclear import of hepatitis B virus capsids and release of the viral genome Proc Natl Acad Sci U S A 100 2003 9849 9854
16. A.A. Labokha, and A. Fassati Viruses challenge selectivity barrier of nuclear pores Viruses 5 2013 2410 2423
17. O. Kobiler, N. Drayman, V. Butin-Israeli, and A. Oppenheim Virus strategies for passing the nuclear envelope barrier Nucleus 3 2012 526 539
18. V. Le Sage, and A.J. Mouland Viral subversion of the nuclear pore complex Viruses 5 2013 2019 2042
19. U.F. Greber, M. Suomalainen, R.P. Stidwill, K. Boucke, M.W. Ebersold, and A. Helenius The role of the nuclear pore complex in adenovirus DNA entry EMBO J 16 1997 5998 6007
20. S. Strunze, M.F. Engelke, I.H. Wang, D. Puntener, K. Boucke, S. Schleich, M. Way, P. Schoenenberger, C.J. Burckhardt, and U.F. Greber Kinesin-1-mediated capsid disassembly and disruption of the nuclear pore complex promote virus infection Cell Host Microbe 10 2011 210 223
21. Y. Cai, B.B. Singh, A. Aslanukov, H. Zhao, and P.A. Ferreira The docking of kinesins, KIF5B and KIF5C, to Ran-binding protein 2 (RanBP2) is mediated via a novel RanBP2 domain J Biol Chem 276 2001 41594 41602
22. K.I. Cho, H. Yi, R. Desai, A.R. Hand, A.L. Haas, and P.A. Ferreira RANBP2 is an allosteric activator of the conventional kinesin-1 motor protein, KIF5B, in a minimal cell-free system EMBO Rep 10 2009 480 486
23. A. Monette, N. Pante, and A.J. Mouland HIV-1 remodels the nuclear pore complex J Cell Biol 193 2011 619 631
24. S. Cohen, I. Etingov, and N. Pante Effect of viral infection on the nuclear envelope and nuclear pore complex Int Rev Cell Mol Biol 299 2012 117 159
25. Y. Xue, J.S. Johnson, D.A. Ornelles, J. Lieberman, and D.A. Engel Adenovirus protein VII functions throughout early phase and interacts with cellular proteins SET and pp32 J Virol 79 2005 2474 2483
26. H. Wodrich, A. Cassany, M.A. D'Angelo, T. Guan, G. Nemerow, and L. Gerace Adenovirus core protein pVII is translocated into the nucleus by multiple import receptor pathways J Virol 80 2006 9608 9618
27. C.E. Hindley, F.J. Lawrence, and D.A. Matthews A role for transportin in the nuclear import of adenovirus core proteins and DNA Traffic 8 2007 1313 1322
28. A. Lachish-Zalait, C.K. Lau, B. Fichtman, E. Zimmerman, A. Harel, M.R. Gaylord, D.J. Forbes, and M. Elbaum Transportin mediates nuclear entry of DNA in vertebrate systems Traffic 10 2009 1414 1428
29. A.C. Saphire, T. Guan, E.C. Schirmer, G.R. Nemerow, and L. Gerace Nuclear import of adenovirus DNA in vitro involves the nuclear protein import pathway and hsc70 J Biol Chem 275 2000 4298 4304
30. A. Dhanoya, T. Wang, E. Keshavarz-Moore, A. Fassati, and B.M. Chain Importin-7 mediates nuclear trafficking of DNA in mammalian cells Traffic 14 2013 165 175
31. J. Hansen, K. Qing, and A. Srivastava Infection of purified nuclei by adeno-associated virus 2 Mol Ther 4 2001 289 296
32. S. Au, S. Cohen, and N. Pante Microinjection of Xenopus laevis oocytes as a system for studying nuclear transport of viruses Methods 51 2010 114 120
33. S. Cohen, and N. Pante Pushing the envelope: microinjection of Minute virus of mice into Xenopus oocytes causes damage to the nuclear envelope J Gen Virol 86 2005 3243 3252
34. S. Cohen, A.R. Behzad, J.B. Carroll, and N. Pante Parvoviral nuclear import: bypassing the host nuclear-transport machinery J Gen Virol 87 2006 3209 3213
35. S. Cohen, A.K. Marr, P. Garcin, and N. Pante Nuclear envelope disruption involving host caspases plays a role in the parvovirus replication cycle J Virol 85 2011 4863 4874
36. M. Porwal, S. Cohen, K. Snoussi, R. Popa-Wagner, F. Anderson, N. Dugot-Senant, H. Wodrich, C. Dinsart, J.A. Kleinschmidt, and N. Pante Parvoviruses cause nuclear envelope breakdown by activating key enzymes of mitosis PLoS Pathog 9 2013 e1003671
37. P. Muhlhausser, and U. Kutay An in vitro nuclear disassembly system reveals a role for the RanGTPase system and microtubule-dependent steps in nuclear envelope breakdown J Cell Biol 178 2007 595 610
38. C.L. Woodward, S. Prakobwanakit, S. Mosessian, and S.A. Chow Integrase interacts with nucleoporin NUP153 to mediate the nuclear import of human immunodeficiency virus type 1 J Virol 83 2009 6522 6533
39. J. Kartenbeck, H. Stukenbrok, and A. Helenius Endocytosis of simian virus 40 into the endoplasmic reticulum J Cell Biol 109 1989 2721 2729
40. M. Schelhaas, J. Malmstrom, L. Pelkmans, J. Haugstetter, L. Ellgaard, K. Grunewald, and A. Helenius Simian Virus 40 depends on ER protein folding and quality control factors for entry into host cells Cell 131 2007 516 529
41. T. Inoue, and B. Tsai How viruses use the endoplasmic reticulum for entry, replication, and assembly Cold Spring Harb Perspect Biol 5 2013 a013250
42. T. Inoue, and B. Tsai A large and intact viral particle penetrates the endoplasmic reticulum membrane to reach the cytosol PLoS Pathog 7 2011 e1002037
43. R. Geiger, D. Andritschke, S. Friebe, F. Herzog, S. Luisoni, T. Heger, and A. Helenius BAP31 and BiP are essential for dislocation of SV40 from the endoplasmic reticulum to the cytosol Nat Cell Biol 13 2011 1305 1314
44. H. Byun, Y. Gou, A. Zook, M.M. Lozano, and J.P. Dudley ERAD and how viruses exploit it Front Microbiol 5 2014 330
45. C.P. Walczak, M.S. Ravindran, T. Inoue, and B. Tsai A cytosolic chaperone complexes with dynamic membrane J-proteins and mobilizes a nonenveloped virus out of the endoplasmic reticulum PLoS Pathog 10 2014 e1004007
46. K.M. Giorda, S. Raghava, M.W. Zhang, and D.N. Hebert The viroporin activity of the minor structural proteins VP2 and VP3 is required for SV40 propagation J Biol Chem 288 2013 2510 2520
47. A. Nakanishi, J. Clever, M. Yamada, P.P. Li, and H. Kasamatsu Association with capsid proteins promotes nuclear targeting of simian virus 40 DNA Proc Natl Acad Sci U S A 93 1996 96 100
48. A. Nakanishi, D. Shum, H. Morioka, E. Otsuka, and H. Kasamatsu Interaction of the Vp3 nuclear localization signal with the importin alpha 2/beta heterodimer directs nuclear entry of infecting simian virus 40 J Virol 76 2002 9368 9377
49. A. Nakanishi, N. Itoh, P.P. Li, H. Handa, R.C. Liddington, and H. Kasamatsu Minor capsid proteins of simian virus 40 are dispensable for nucleocapsid assembly and cell entry but are required for nuclear entry of the viral genome J Virol 81 2007 3778 3785
50. D. Kuksin, and L.C. Norkin Disassociation of the SV40 genome from capsid proteins prior to nuclear entry Virol J 9 2012 158
51. K. Hummeler, N. Tomassini, and F. Sokol Morphological aspects of the uptake of simian virus 40 by permissive cells J Virol 6 1970 87 93
52. R.L. Mackay, and R.A. Consigli Early events in polyoma virus infection: attachment, penetration, and nuclear entry J Virol 19 1976 620 636
53. V. Butin-Israeli, O. Ben-nun-Shaul, I. Kopatz, S.A. Adam, T. Shimi, R.D. Goldman, and A. Oppenheim Simian virus 40 induces lamin A/C fluctuations and nuclear envelope deformation during cell entry Nucleus 2 2007 320 330
54. V. Butin-Israeli, N. Drayman, and A. Oppenheim Simian virus 40 infection triggers a balanced network that includes apoptotic, survival, and stress pathways J Virol 84 2010 3431 3442
55. C.M. de Noronha, M.P. Sherman, H.W. Lin, M.V. Cavrois, R.D. Moir, R.D. Goldman, and W.C. Greene Dynamic disruptions in nuclear envelope architecture and integrity induced by HIV-1 Vpr Science 294 2001 1105 1108
56. M. Segura-Totten, and K.L. Wilson Virology HIV - breaking the rules for nuclear entry Science 294 2001 1016 1017
57. L.T. Burns, and S.R. Wente Trafficking to uncharted territory of the nuclear envelope Curr Opin Cell Biol 24 2012 341 349
58. A. Rose, and C. Schlieker Alternative nuclear transport for cellular protein quality control Trends Cell Biol 22 2012 509 514
59. C.W. Stackpole Herpes-type virus of the frog renal adenocarcinoma. I. Virus development in tumor transplants maintained at low temperature J Virol 4 1969 75 93
60. S.D. Speese, J. Ashley, V. Jokhi, J. Nunnari, R. Barria, Y. Li, B. Ataman, A. Koon, Y.T. Chang, and Q. Li Nuclear envelope budding enables large ribonucleoprotein particle export during synaptic Wnt signaling Cell 149 2012 832 846