Targeting of Viral Capsids to Nuclear Pores in a Cell-Free Reconstitution System

Traffic

Volumn 15, Issue 11, 2014, Pages 1266-1281

  Anderson, Fenja ^a   Savulescu, Anca F ^b,e   Rudolph, Kathrin ^a   Schipke, Julia ^a   Cohen, Ilana ^c   Ibiricu, Iosune ^d,f   Rotem, Asaf ^c,g   Grünewald, Kay ^d   Sodeik, Beate ^a   Harel, Amnon ^b  

^a HANNOVER MEDICAL SCHOOL   (Germany)

^b BAR ILAN UNIVERSITY   (Israel)

^c TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

^d UNIVERSITY OF OXFORD   (United Kingdom)

^e DSI CSIR Nanotechnology Innovation Centre   (South Africa)

^f UNIVERSITY OF CALIFORNIA   (United States)

^g HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Herpes simplex virus; Herpesviruses; Nuclear pore; Reconstitution; Xenopus nuclei

Indexed keywords

GREEN FLUORESCENT PROTEIN; CAPSID PROTEIN; PROTEIN BINDING;

ANIMAL CELL; ARTICLE; CELL FREE SYSTEM; CELL NUCLEUS; CONTROLLED STUDY; FIELD EMISSION SCANNING ELECTRON MICROSCOPY; FLUORESCENCE; GENE TARGETING; HERPES SIMPLEX VIRUS; HERPESVIRIDAE; IN VITRO STUDY; NONHUMAN; NUCLEAR IMPORT; NUCLEAR PORE; NUCLEAR PORE COMPLEX; PRIORITY JOURNAL; PROTEIN BINDING; VIRUS CAPSID; VIRUS GENOME; VIRUS MORPHOLOGY; VIRUS REPLICATION; VIRUS TRANSCRIPTION; VIRUS UNCOATING; XENOPUS LAEVIS; ACTIVE TRANSPORT; ANIMAL; HERPES SIMPLEX VIRUS 1; METABOLISM; ULTRASTRUCTURE; VIROLOGY; XENOPUS;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; CAPSID; CAPSID PROTEINS; CELL-FREE SYSTEM; HERPESVIRUS 1, HUMAN; NUCLEAR PORE; PROTEIN BINDING; XENOPUS;

EID: 84911153289     PISSN: 13989219     EISSN: 16000854     Source Type: Journal    
DOI: 10.1111/tra.12209     Document Type: Article

References (89)

1. Brohawn SG, Partridge JR, Whittle JR, Schwartz TU. The nuclear pore complex has entered the atomic age. Structure 2009;17:1156-1168.
2. Cronshaw JM, Krutchinsky AN, Zhang W, Chait BT, Matunis MJ. Proteomic analysis of the mammalian nuclear pore complex. J Cell Biol 2002;158:915-927.
3. Hetzer MW, Wente SR. Border control at the nucleus: biogenesis and organization of the nuclear membrane and pore complexes. Dev Cell 2009;17:606-616.
4. Frenkiel-Krispin D, Maco B, Aebi U, Medalia O. Structural analysis of a metazoan nuclear pore complex reveals a fused concentric ring architecture. J Mol Biol 2010;395:578-586.
5. Maimon T, Elad N, Dahan I, Medalia O. The human nuclear pore complex as revealed by cryo-electron tomography. Structure 2012;20:998-1006.
6. Cook A, Bono F, Jinek M, Conti E. Structural biology of nucleocytoplasmic transport. Annu Rev Biochem 2007;76:647-671.
7. Pante N, Kann M. Nuclear pore complex is able to transport macromolecules with diameters of about 39nm. Mol Biol Cell 2002;13:425-434.
8. Wente SR, Rout MP. The nuclear pore complex and nuclear transport. Cold Spring Harb Perspect Biol 2010;2:a000562.
9. Strom AC, Weis K. Importin-beta-like nuclear transport receptors. Genome Biol 2001;2:3008.
10. Fried H, Kutay U. Nucleocytoplasmic transport: taking an inventory. Cell Mol Life Sci 2003;60:1659-1688.
11. Görlich D, Pante N, Kutay U, Aebi U, Bischoff FR. Identification of different roles for RanGDP and RanGTP in nuclear protein import. EMBO J 1996;15:5584-5594.
12. Lee SJ, Matsuura Y, Liu SM, Stewart M. Structural basis for nuclear import complex dissociation by RanGTP. Nature 2005;435:693-696.
13. Davison AJ, Eberle R, Ehlers B, Hayward GS, McGeoch DJ, Minson AC, Pellett PE, Roizman B, Studdert MJ, Thiry E. The order Herpesvirales. Arch Virol 2009;154:171-177.
14. Brown JC, Newcomb WW. Herpesvirus capsid assembly: insights from structural analysis. Curr Opin Virol 2011;1:142-149.
15. Rochat RH, Liu X, Murata K, Nagayama K, Rixon FJ, Chiu W. Seeing the portal in herpes simplex virus type 1 B capsids. J Virol 2011;85:1871-1874.
16. Grünewald K, Desai P, Winkler DC, Heymann JB, Belnap DM, Baumeister W, Steven AC. Three-dimensional structure of herpes simplex virus from cryo-electron tomography. Science 2003;302:1396-1398.
17. Loret S, Guay G, Lippe R. Comprehensive characterization of extracellular herpes simplex virus type 1 virions. J Virol 2008;82:8605-8618.
18. Zhou ZH, Chen DH, Jakana J, Rixon FJ, Chiu W. Visualization of tegument-capsid interactions and DNA in intact herpes simplex virus type 1 virions. J Virol 1999;73:3210-3218.
19. Radtke K, Kieneke D, Wolfstein A, Michael K, Steffen W, Scholz T, Karger A, Sodeik B. Plus- and minus-end directed microtubule motors bind simultaneously to herpes simplex virus capsids using different inner tegument structures. PLoS Pathog 2010;6:e1000991.
20. Wolfstein A, Nagel CH, Radtke K, Dohner K, Allan VJ, Sodeik B. The inner tegument promotes herpes simplex virus capsid motility along microtubules in vitro. Traffic 2006;7:227-237.
21. Kelly BJ, Fraefel C, Cunningham AL, Diefenbach RJ. Functional roles of the tegument proteins of herpes simplex virus type 1. Virus Res 2009;145:173-186.
22. Mettenleiter TC, Klupp BG, Granzow H. Herpesvirus assembly: an update. Virus Res 2009;143:222-234.
23. Johnson DC, Baines JD. Herpesviruses remodel host membranes for virus egress. Nat Rev Microbiol 2011;9:382-394.
24. Henaff D, Radtke K, Lippe R. Herpesviruses exploit several host compartments for envelopment. Traffic 2012;13:1443-1449.
25. Schipke J, Pohlmann A, Diestel R, Binz A, Rudolph K, Nagel CH, Bauerfeind R, Sodeik B. The C terminus of the large tegument protein pUL36 contains multiple capsid binding sites that function differently during assembly and cell entry of herpes simplex virus. J Virol 2012;86:3682-3700.
26. Sandbaumhüter M, Dohner K, Schipke J, Binz A, Pohlmann A, Sodeik B, Bauerfeind R. Cytosolic herpes simplex virus capsids not only require binding inner tegument protein pUL36 but also pUL37 for active transport prior to secondary envelopment. Cell Microbiol 2013;15:248-269.
27. Antinone SE, Smith GA. Retrograde axon transport of herpes simplex virus and pseudorabies virus: a live-cell comparative analysis. J Virol 2010;84:1504-1512.
28. Coller KE, Lee JI, Ueda A, Smith GA. The capsid and tegument of the alphaherpesviruses are linked by an interaction between the UL25 and VP1/2 proteins. J Virol 2007;81:11790-11797.
29. Granzow H, Klupp BG, Mettenleiter TC. Entry of pseudorabies virus: an immunogold-labeling study. J Virol 2005;79:3200-3205.
30. Luxton GW, Haverlock S, Coller KE, Antinone SE, Pincetic A, Smith GA. Targeting of herpesvirus capsid transport in axons is coupled to association with specific sets of tegument proteins. Proc Natl Acad Sci USA 2005;102:5832-5837.
31. Maurer UE, Sodeik B, Grunewald K. Native 3D intermediates of membrane fusion in herpes simplex virus 1 entry. Proc Natl Acad Sci USA 2008;105:10559-10564.
32. Döhner K, Wolfstein A, Prank U, Echeverri C, Dujardin D, Vallee R, Sodeik B. Function of dynein and dynactin in herpes simplex virus capsid transport. Mol Biol Cell 2002;13:2795-2809.
33. Sodeik B, Ebersold MW, Helenius A. Microtubule-mediated transport of incoming herpes simplex virus 1 capsids to the nucleus. J Cell Biol 1997;136:1007-1021.
34. Batterson W, Furlong D, Roizman B. Molecular genetics of herpes simplex virus. VIII. further characterization of a temperature-sensitive mutant defective in release of viral DNA and in other stages of the viral reproductive cycle. J Virol 1983;45:397-407.
35. Granzow H, Weiland F, Jons A, Klupp BG, Karger A, Mettenleiter TC. Ultrastructural analysis of the replication cycle of pseudorabies virus in cell culture: a reassessment. J Virol 1997;71:2072-2082.
36. Miyamoto K, Morgan C. Structure and development of viruses as observed in the electron microscope. XI. Entry and uncoating of herpes simplex virus. J Virol 1971;8:910-918.
37. Ojala PM, Sodeik B, Ebersold MW, Kutay U, Helenius A. 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 2000;20:4922-4931.
38. Peng L, Ryazantsev S, Sun R, Zhou ZH. Three-dimensional visualization of gammaherpesvirus life cycle in host cells by electron tomography. Structure 2010;18:47-58.
39. Rode K, Dohner K, Binz A, Glass M, Strive T, Bauerfeind R, Sodeik B. Uncoupling uncoating of herpes simplex virus genomes from their nuclear import and gene expression. J Virol 2011;85:4271-4283.
40. Newcomb WW, Booy FP, Brown JC. Uncoating the herpes simplex virus genome. J Mol Biol 2007;370:633-642.
41. Labokha AA, Gradmann S, Frey S, Hulsmann BB, Urlaub H, Baldus M, Gorlich D. Systematic analysis of barrier-forming FG hydrogels from Xenopus nuclear pore complexes. EMBO J 2013;32:204-218.
42. Roos WH, Ivanovska IL, Evilevitch A, Wuite GJ. Viral capsids: mechanical characteristics, genome packaging and delivery mechanisms. Cell Mol Life Sci 2007;64:1484-1497.
43. Yang K, Homa F, Baines JD. Putative terminase subunits of herpes simplex virus 1 form a complex in the cytoplasm and interact with portal protein in the nucleus. J Virol 2007;81:6419-6433.
44. Roos WH, Radtke K, Kniesmeijer E, Geertsema H, Sodeik B, Wuite GJ. Scaffold expulsion and genome packaging trigger stabilization of herpes simplex virus capsids. Proc Natl Acad Sci USA 2009;106:9673-9678.
45. Newmeyer DD, Forbes DJ. Nuclear import can be separated into distinct steps in vitro: nuclear pore binding and translocation. Cell 1988;52:641-653.
46. Newport J. Nuclear reconstitution in vitro: stages of assembly around protein-free DNA. Cell 1987;48:205-217.
47. Harel A, Orjalo AV, Vincent T, Lachish-Zalait A, Vasu S, Shah S, Zimmerman E, Elbaum M, Forbes DJ. Removal of a single pore subcomplex results in vertebrate nuclei devoid of nuclear pores. Mol Cell 2003;11:853-864.
48. Savulescu AF, Shorer H, Kleifeld O, Cohen I, Gruber R, Glickman MH, Harel A. Nuclear import of an intact preassembled proteasome particle. Mol Biol Cell 2011;22:880-891.
49. Macaulay C, Forbes DJ. Assembly of the nuclear pore: biochemically distinct steps revealed with NEM, GTP gamma S, and BAPTA. J Cell Biol 1996;132:5-20.
50. Chan RC, Forbes DI. In vitro study of nuclear assembly and nuclear import using Xenopus egg extracts. Methods Mol Biol 2006;322:289-300.
51. Radtke K, Anderson F, Sodeik B. A precipitation-based assay to analyze interactions of viral particles with cytosolic host factors. Methods Mol Biol 2014;1144:191-208.
52. Newcomb WW, Brown JC. Time-dependent transformation of the herpesvirus tegument. J Virol 2009;83:8082-8089.
53. Newcomb WW, Brown JC. Structure and capsid association of the herpesvirus large tegument protein UL36. J Virol 2010;84:9408-9414.
54. Harel A, Chan RC, Lachish-Zalait A, Zimmerman E, Elbaum M, Forbes DJ. Importin beta negatively regulates nuclear membrane fusion and nuclear pore complex assembly. Mol Biol Cell 2003;14:4387-4396.
55. Wente SR, Rout MP, Blobel G. A new family of yeast nuclear pore complex proteins. J Cell Biol 1992;119:705-723.
56. Desai P, Person S. Incorporation of the green fluorescent protein into the herpes simplex virus type 1 capsid. J Virol 1998;72:7563-7568.
57. Döhner K, Radtke K, Schmidt S, Sodeik B. Eclipse phase of herpes simplex virus type 1 infection: efficient dynein-mediated capsid transport without the small capsid protein VP26. J Virol 2006;80:8211-8224.
58. Kann M, Sodeik B, Vlachou A, Gerlich WH, Helenius A. Phosphorylation-dependent binding of hepatitis B virus core particles to the nuclear pore complex. J Cell Biol 1999;145:45-55.
59. Cohen S, Pante N. Pushing the envelope: microinjection of Minute virus of mice into Xenopus oocytes causes damage to the nuclear envelope. J Gen Virol 2005;86:3243-3252.
60. Porwal M, Cohen S, Snoussi K, Popa-Wagner R, Anderson F, Dugot-Senant N, Wodrich H, Dinsart C, Kleinschmidt JA, Pante N, Kann M. Parvoviruses cause nuclear envelope breakdown by activating key enzymes of mitosis. PLoS Pathog 2013;9:e1003671.
61. Schmitz A, Schwarz A, Foss M, Zhou L, Rabe B, Hoellenriegel J, Stoeber M, Pante N, Kann M. Nucleoporin 153 arrests the nuclear import of hepatitis B virus capsids in the nuclear basket. PLoS Pathog 2010;6:e1000741.
62. Finlay DR, Forbes DJ. Reconstitution of biochemically altered nuclear pores: transport can be eliminated and restored. Cell 1990;60:17-29.
63. Walther TC, Fornerod M, Pickersgill H, Goldberg M, Allen TD, Mattaj IW. The nucleoporin Nup153 is required for nuclear pore basket formation, nuclear pore complex anchoring and import of a subset of nuclear proteins. EMBO J 2001;20:5703-5714.
64. Rotem A, Gruber R, Shorer H, Shaulov L, Klein E, Harel A. Importin beta regulates the seeding of chromatin with initiation sites for nuclear pore assembly. Mol Biol Cell 2009;20:4031-4042.
65. Shaulov L, Harel A. Improved visualization of vertebrate nuclear pore complexes by field emission scanning electron microscopy. Structure 2012;20:407-413.
66. Ibiricu I, Huiskonen JT, Dohner K, Bradke F, Sodeik B, Grunewald K. Cryo electron tomography of herpes simplex virus during axonal transport and secondary envelopment in primary neurons. PLoS Pathog 2011;7:e1002406.
67. Cardone G, Newcomb WW, Cheng N, Wingfield PT, Trus BL, Brown JC, Steven AC. The UL36 tegument protein of herpes simplex virus 1 has a composite binding site at the capsid vertices. J Virol 2012;86:4058-4064.
68. Newcomb WW, Jones LM, Dee A, Chaudhry F, Brown JC. Role of a reducing environment in disassembly of the herpesvirus tegument. Virology 2012;431:71-79.
69. Cockrell SK, Huffman JB, Toropova K, Conway JF, Homa FL. Residues of the UL25 protein of herpes simplex virus that are required for its stable interaction with capsids. J Virol 2011;85:4875-4887.
70. Conway JF, Cockrell SK, Copeland AM, Newcomb WW, Brown JC, Homa FL. Labeling and localization of the herpes simplex virus capsid protein UL25 and its interaction with the two triplexes closest to the penton. J Mol Biol 2010;397:575-586.
71. Pasdeloup D, Blondel D, Isidro AL, Rixon FJ. Herpesvirus capsid association with the nuclear pore complex and viral DNA release involve the nucleoporin CAN/Nup214 and the capsid protein pUL25. J Virol 2009;83:6610-6623.
72. Preston VG, Murray J, Preston CM, McDougall IM, Stow ND. The UL25 gene product of herpes simplex virus type 1 is involved in uncoating of the viral genome. J Virol 2008;82:6654-6666.
73. Trus BL, Newcomb WW, Cheng N, Cardone G, Marekov L, Homa FL, Brown JC, Steven AC. Allosteric signaling and a nuclear exit strategy: binding of UL25/UL17 heterodimers to DNA-Filled HSV-1 capsids. Mol Cell 2007;26:479-489.
74. Abaitua F, Hollinshead M, Bolstad M, Crump CM, O'Hare P. A Nuclear localization signal in herpesvirus protein VP1-2 is essential for infection via capsid routing to the nuclear pore. J Virol 2012;86:8998-9014.
75. Copeland AM, Newcomb WW, Brown JC. Herpes simplex virus replication: roles of viral proteins and nucleoporins in capsid-nucleus attachment. J Virol 2009;83:1660-1668.
76. Jovasevic V, Liang L, Roizman B. Proteolytic cleavage of VP1-2 is required for release of herpes simplex virus 1 DNA into the nucleus. J Virol 2008;82:3311-3319.
77. Roberts AP, Abaitua F, O'Hare P, McNab D, Rixon FJ, Pasdeloup D. Differing roles of inner tegument proteins pUL36 and pUL37 during entry of herpes simplex virus type 1. J Virol 2009;83:105-116.
78. Cohen GH, Ponce de Leon M, Diggelmann H, Lawrence WC, Vernon SK, Eisenberg RJ. Structural analysis of the capsid polypeptides of herpes simplex virus types 1 and 2. J Virol 1980;34:521-531.
79. Eisenberg RJ, Long D, Ponce de Leon M, Matthews JT, Spear PG, Gibson MG, Lasky LA, Berman P, Golub E, Cohen GH. Localization of epitopes of herpes simplex virus type 1 glycoprotein D. J Virol 1985;53:634-644.
80. Thurlow JK, Murphy M, Stow ND, Preston VG. Herpes simplex virus type 1 DNA-packaging protein UL17 is required for efficient binding of UL25 to capsids. J Virol 2006;80:2118-2126.
81. Leege T, Granzow H, Fuchs W, Klupp BG, Mettenleiter TC. Phenotypic similarities and differences between UL37-deleted pseudorabies virus and herpes simplex virus type 1. J Gen Virol 2009;90:1560-1568.
82. Whittaker GR, Riggio MP, Halliburton IW, Killington RA, Allen GP, Meredith DM. Antigenic and protein sequence homology between VP13/14, a herpes simplex virus type 1 tegument protein, and gp10, a glycoprotein of equine herpesvirus 1 and 4. J Virol 1991;65:2320-2326.
83. Kremer JR, Mastronarde DN, McIntosh JR. Computer visualization of three-dimensional image data using IMOD. J Struct Biol 1996;116:71-76.
84. Heymann JB, Belnap DM. Bsoft: image processing and molecular modeling for electron microscopy. J Struct Biol 2007;157:3-18.
85. Cheng N, Trus BL, Belnap DM, Newcomb WW, Brown JC, Steven AC. Handedness of the herpes simplex virus capsid and procapsid. J Virol 2002;76:7855-7859.
86. Allen TD, Rutherford SA, Murray S, Sanderson HS, Gardiner F, Kiseleva E, Goldberg MW, Drummond SP. Generation of cell-free extracts of Xenopus eggs and demembranated sperm chromatin for the assembly and isolation of in vitro-formed nuclei for Western blotting and scanning electron microscopy (SEM). Nat Protoc 2007;2:1173-1179.
87. Loret S, Lippe R. Biochemical analysis of infected cell polypeptide (ICP)0, ICP4, UL7 and UL23 incorporated into extracellular herpes simplex virus type 1 virions. J Gen Virol 2012;93:624-634.
88. Roizman B, Campadelli-Fiume G. Alphaherpes viral genes and their functions. In: Arvin A, Campadelli-Fiume G, Mocarski E, Moore PS, Roizman B, Whitley R, Yamanishi K, editors. Human Herpesviruses, Biology, Therapy and Immunoprophylaxis. New York: Cambridge University Press; 2007, pp. 70-92.
89. Toropova K, Huffman JB, Homa FL, Conway JF. The herpes simplex virus 1 UL17 protein is the second constituent of the capsid vertex-specific component required for DNA packaging and retention. J Virol 2011;85:7513-7522.