Cryo electron tomography of herpes simplex virus during axonal transport and secondary envelopment in primary neurons

PLoS Pathogens

Volumn 7, Issue 12, 2011, Pages

  Ibiricu, Iosune ^a   Huiskonen, Juha T ^a,b,c   Döhner, Katinka ^d   Bradke, Frank ^e,f   Sodeik, Beate ^d   Grünewald, Kay ^a,c  

^a MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

^b UNIVERSITY OF HELSINKI   (Finland)

^c UNIVERSITY OF OXFORD   (United Kingdom)

^d HANNOVER MEDICAL SCHOOL   (Germany)

^e MAX PLANCK INSTITUTE OF NEUROBIOLOGY   (Germany)

^f GERMAN CENTER FOR NEURODEGENERATIVE DISEASES DZNE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOPROTEIN; MICROTUBULE PROTEIN; MOLECULAR MOTOR; VIRUS PROTEIN;

ARTICLE; CONTROLLED STUDY; CYTOSOL; ELECTRON TOMOGRAPHY; FLUORESCENCE MICROSCOPY; HERPES SIMPLEX VIRUS; INTEGUMENT; NERVE FIBER; NERVE FIBER TRANSPORT; NONHUMAN; PROGENY; VIRION; VIRUS CAPSID; VIRUS ENVELOPE; ANIMAL; CELL CULTURE; HERPES SIMPLEX VIRUS 1; METABOLISM; METHODOLOGY; MICROTUBULE; NERVE CELL; RAT; TRANSPORT VESICLE; ULTRASTRUCTURE; VIROLOGY;

HERPESVIRIDAE; HUMAN HERPESVIRUS 1; MIRIDAE; SIMPLEXVIRUS;

ANIMALS; AXONAL TRANSPORT; AXONS; CAPSID; CELLS, CULTURED; ELECTRON MICROSCOPE TOMOGRAPHY; HERPESVIRUS 1, HUMAN; MICROTUBULES; NEURONS; RATS; TRANSPORT VESICLES; VIRION;

EID: 84855255301     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1002406     Document Type: Article

References (87)

1. Grünewald K, Desai P, Winkler DC, Heymann JB, Belnap DM, et al. (2003) Three-dimensional structure of herpes simplex virus from cryo-electron tomography. Science 302: 1396-1398.
2. Maurer UE, Sodeik B, Grünewald K, (2008) Native 3D intermediates of membrane fusion in herpes simplex virus 1 entry. Proc Natl Acad Sci USA 105: 10559-10564.
3. Schrag JD, Prasad BV, Rixon FJ, Chiu W, (1989) Three-dimensional structure of the HSV1 nucleocapsid. Cell 56: 651-660.
4. Booy FP, Newcomb WW, Trus BL, Brown JC, Baker TS, et al. (1991) Liquid-crystalline, phage-like packing of encapsidated DNA in herpes simplex virus. Cell 64: 1007-1015.
5. Newcomb WW, Trus BL, Booy FP, Steven AC, Wall JS, et al. (1993) Structure of the herpes simplex virus capsid. Molecular composition of the pentons and the triplexes. J Mol Biol 232: 499-511.
6. Zhou ZH, Prasad BV, Jakana J, Rixon FJ, Chiu W, (1994) Protein subunit structures in the herpes simplex virus A-capsid determined from 400 kV spot-scan electron cryomicroscopy. J Mol Biol 242: 456-469.
7. Zhou ZH, Dougherty M, Jakana J, He J, Rixon FJ, et al. (2000) Seeing the herpesvirus capsid at 8.5 A. Science 288: 877-880.
8. Trus BL, Cheng N, Newcomb WW, Homa FL, Brown JC, et al. (2004) Structure and polymorphism of the UL6 portal protein of herpes simplex virus type 1. J Virol 78: 12668-12671.
9. Cardone G, Winkler DC, Trus BL, Cheng N, Heuser JE, et al. (2007) Visualization of the herpes simplex virus portal in situ by cryo-electron tomography. Virology 361: 426-434.
10. Chang JT, Schmid MF, Rixon FJ, Chiu W, (2007) Electron cryotomography reveals the portal in the herpesvirus capsid. J Virol 81: 2065-2068.
11. Heymann JB, Cheng N, Newcomb WW, Trus BL, Brown JC, et al. (2003) Dynamics of herpes simplex virus capsid maturation visualized by time-lapse cryo-electron microscopy. Nat Struct Biol 10: 334-341.
12. Newcomb WW, Brown JC, (1991) Structure of the herpes simplex virus capsid: effects of extraction with guanidine hydrochloride and partial reconstitution of extracted capsids. J Virol 65: 613-620.
13. Trus BL, Newcomb WW, Cheng N, Cardone G, Marekov L, et al. (2007) Allosteric signaling and a nuclear exit strategy: binding of UL25/UL17 heterodimers to DNA-Filled HSV-1 capsids. Mol Cell 26: 479-489.
14. Sheaffer AK, Newcomb WW, Gao M, Yu D, Weller SK, et al. (2001) Herpes simplex virus DNA cleavage and packaging proteins associate with the procapsid prior to its maturation. J Virol 75: 687-698.
15. Conway JF, Cockrell SK, Copeland AM, Newcomb WW, Brown JC, et al. (2010) 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 397: 575-586.
16. Radtke K, Kieneke D, Wolfstein A, Michael K, Steffen W, et al. (2010) Plus- and minus-end directed microtubule motors bind simultaneously to herpes simplex virus capsids using different inner tegument structures. PLoS Pathog 6: e1000991.
17. Miranda-Saksena M, Boadle RA, Armati P, Cunningham AL, (2002) In rat dorsal root ganglion neurons, herpes simplex virus type 1 tegument forms in the cytoplasm of the cell body. J Virol 76: 9934-9951.
18. Wolfstein A, Nagel CH, Radtke K, Döhner K, Allan VJ, et al. (2006) The inner tegument promotes herpes simplex virus capsid motility along microtubules in vitro. Traffic 7: 227-237.
19. Mettenleiter TC, Klupp BG, Granzow H, (2009) Herpesvirus assembly: an update. Virus Res 143: 222-234.
20. Möhl BS, Böttcher S, Granzow H, Kuhn J, Klupp BG, et al. (2009) Intracellular localization of the pseudorabies virus large tegument protein pUL36. J Virol 83: 9641-9651.
21. Bucks MA, O'Regan KJ, Murphy MA, Wills JW, Courtney RJ, (2007) Herpes simplex virus type 1 tegument proteins VP1/2 and UL37 are associated with intranuclear capsids. Virology 361: 316-324.
22. Coller KE, Lee JI, Ueda A, Smith GA, (2007) The capsid and tegument of the alphaherpesviruses are linked by an interaction between the UL25 and VP1/2 proteins. J Virol 81: 11790-11797.
23. Mettenleiter TC, (2006) Intriguing interplay between viral proteins during herpesvirus assembly or: the herpesvirus assembly puzzle. Vet Microbiol 113: 163-169.
24. Diefenbach RJ, Miranda-Saksena M, Douglas MW, Cunningham AL, (2008) Transport and egress of herpes simplex virus in neurons. Rev Med Virol 18: 35-51.
25. Nagel CH, Döhner K, Fathollahy M, Strive T, Borst EM, et al. (2008) Nuclear egress and envelopment of herpes simplex virus capsids analyzed with dual-color fluorescence HSV1(17+). J Virol 82: 3109-3124.
26. Miranda-Saksena M, Boadle RA, Aggarwal A, Tijono B, Rixon FJ, et al. (2009) Herpes simplex virus utilizes the large secretory vesicle pathway for anterograde transport of tegument and envelope proteins and for viral exocytosis from growth cones of human fetal axons. J Virol 83: 3187-3199.
27. Wisner TW, Sugimoto K, Howard PW, Kawaguchi Y, Johnson DC, (2011) Anterograde transport of herpes simplex virus capsids in neurons by both separate and married mechanisms. J Virol 85: 5919-5928.
28. Snyder A, Wisner TW, Johnson DC, (2006) Herpes simplex virus capsids are transported in neuronal axons without an envelope containing the viral glycoproteins. J Virol 80: 11165-11177.
29. Miranda-Saksena M, Wakisaka H, Tijono B, Boadle RA, Rixon F, et al. (2006) Herpes simplex virus type 1 accumulation, envelopment, and exit in growth cones and varicosities in mid-distal regions of axons. J Virol 80: 3592-3606.
30. Enquist LW, Tomishima MJ, Gross S, Smith GA, (2002) Directional spread of an alpha-herpesvirus in the nervous system. Vet Microbiol 86: 5-16.
31. Tomishima MJ, Enquist LW, (2002) In vivo egress of an alphaherpesvirus from axons. J Virol 76: 8310-8317.
32. Snyder A, Polcicova K, Johnson DC, (2008) Herpes simplex virus gE/gI and US9 proteins promote transport of both capsids and virion glycoproteins in neuronal axons. J Virol 82: 10613-10624.
33. Antinone SE, Smith GA, (2006) Two modes of herpesvirus trafficking in neurons: membrane acquisition directs motion. J Virol 80: 11235-11240.
34. Feierbach B, Bisher M, Goodhouse J, Enquist LW, (2007) In vitro analysis of transneuronal spread of an alphaherpesvirus infection in peripheral nervous system neurons. J Virol 81: 6846-6857.
35. Maresch C, Granzow H, Negatsch A, Klupp BG, Fuchs W, et al. (2010) Ultrastructural analysis of virion formation and anterograde intraaxonal transport of the alphaherpesvirus pseudorabies virus in primary neurons. J Virol 84: 5528-5539.
36. Antinone SE, Zaichick SV, Smith GA, (2010) Resolving the assembly state of herpes simplex virus during axon transport by live-cell imaging. J Virol 84: 13019-13030.
37. Huang J, Lazear HM, Friedman HM, (2011) Completely assembled virus particles detected by transmission electron microscopy in proximal and mid-axons of neurons infected with herpes simplex virus type 1, herpes simplex virus type 2 and pseudorabies virus. Virology 409: 12-16.
38. Lyman MG, Enquist LW, (2009) Herpesvirus interactions with the host cytoskeleton. J Virol 83: 2058-2066.
39. Döhner K, Nagel CH, Sodeik B, (2005) Viral stop-and-go along microtubules: taking a ride with dynein and kinesins. Trends Microbiol 13: 320-327.
40. Dodding MP, Way M, (2011) Coupling viruses to dynein and kinesin-1. EMBO J 30: 3527-3539.
41. Smith GA, Gross SP, Enquist LW, (2001) Herpesviruses use bidirectional fast-axonal transport to spread in sensory neurons. Proc Natl Acad Sci USA 98: 3466-3470.
42. Smith GA, Pomeranz L, Gross SP, Enquist LW, (2004) Local modulation of plus-end transport targets herpesvirus entry and egress in sensory axons. Proc Natl Acad Sci USA 101: 16034-16039.
43. Greber UF, Way M, (2006) A superhighway to virus infection. Cell 124: 741-754.
44. Radtke K, Döhner K, Sodeik B, (2006) Viral interactions with the cytoskeleton: a hitchhiker's guide to the cell. Cell Microbiol 8: 387-400.
45. Sodeik B, Ebersold MW, Helenius A, (1997) Microtubule-mediated transport of incoming herpes simplex virus 1 capsids to the nucleus. J Cell Biol 136: 1007-1021.
46. Döhner K, Wolfstein A, Prank U, Echeverri C, Dujardin D, et al. (2002) Function of dynein and dynactin in herpes simplex virus capsid transport. Mol Biol Cell 13: 2795-2809.
47. Culver-Hanlon TL, Lex SA, Stephens AD, Quintyne NJ, King SJ, (2006) A microtubule-binding domain in dynactin increases dynein processivity by skating along microtubules. Nat Cell Biol 8: 264-270.
48. Luxton GW, Haverlock S, Coller KE, Antinone SE, Pincetic A, et al. (2005) Targeting of herpesvirus capsid transport in axons is coupled to association with specific sets of tegument proteins. Proc Natl Acad Sci USA 102: 5832-5837.
49. Luxton GW, Lee JI, Haverlock-Moyns S, Schober JM, Smith GA, (2006) The pseudorabies virus VP1/2 tegument protein is required for intracellular capsid transport. J Virol 80: 201-209.
50. Roberts AP, Abaitua F, O'Hare P, McNab D, Rixon FJ, et al. (2009) Differing roles of inner tegument proteins pUL36 and pUL37 during entry of herpes simplex virus type 1. J Virol 83: 105-116.
51. Douglas MW, Diefenbach RJ, Homa FL, Miranda-Saksena M, Rixon FJ, et al. (2004) Herpes simplex virus type 1 capsid protein VP26 interacts with dynein light chains RP3 and Tctex1 and plays a role in retrograde cellular transport. J Biol Chem 279: 28522-28530.
52. Desai P, Person S, (1998) Incorporation of the green fluorescent protein into the herpes simplex virus type 1 capsid. J Virol 72: 7563-7568.
53. Antinone SE, Shubeita GT, Coller KE, Lee JI, Haverlock-Moyns S, et al. (2006) The Herpesvirus capsid surface protein, VP26, and the majority of the tegument proteins are dispensable for capsid transport toward the nucleus. J Virol 80: 5494-5498.
54. Döhner K, Radtke K, Schmidt S, Sodeik B, (2006) Eclipse phase of herpes simplex virus type 1 infection: Efficient dynein-mediated capsid transport without the small capsid protein VP26. J Virol 80: 8211-8224.
55. Diefenbach RJ, Miranda-Saksena M, Diefenbach E, Holland DJ, Boadle RA, et al. (2002) Herpes simplex virus tegument protein US11 interacts with conventional kinesin heavy chain. J Virol 76: 3282-3291.
56. Zhou ZH, Chen DH, Jakana J, Rixon FJ, Chiu W, (1999) Visualization of tegument-capsid interactions and DNA in intact herpes simplex virus type 1 virions. J Virol 73: 3210-3218.
57. Lucic V, Förster F, Baumeister W, (2005) Structural studies by electron tomography: from cells to molecules. Annu Rev Biochem 74: 833-865.
58. Adrian M, Dubochet J, Lepault J, McDowall AW, (1984) Cryo-electron microscopy of viruses. Nature 308: 32-36.
59. Dubochet J, Adrian M, Chang JJ, Homo JC, Lepault J, et al. (1988) Cryo-electron microscopy of vitrified specimens. Q Rev Biophys 21: 129-228.
60. Wozniak MA, Shipley SJ, Combrinck M, Wilcock GK, Itzhaki RF, (2005) Productive herpes simplex virus in brain of elderly normal subjects and Alzheimer's disease patients. J Med Virol 75: 300-306.
61. Chen DH, Jakana J, McNab D, Mitchell J, Zhou ZH, et al. (2001) The pattern of tegument-capsid interaction in the herpes simplex virus type 1 virion is not influenced by the small hexon-associated protein VP26. J Virol 75: 11863-11867.
62. Trus BL, Homa FL, Booy FP, Newcomb WW, Thomsen DR, et al. (1995) Herpes simplex virus capsids assembled in insect cells infected with recombinant baculoviruses: structural authenticity and localization of VP26. J Virol 69: 7362-7366.
63. Garvalov BK, Zuber B, Bouchet-Marquis C, Kudryashev M, Gruska M, et al. (2006) Luminal particles within cellular microtubules. J Cell Biol 174: 759-765.
64. Desai PJ, (2000) A null mutation in the UL36 gene of herpes simplex virus type 1 results in accumulation of unenveloped DNA-filled capsids in the cytoplasm of infected cells. J Virol 74: 11608-11618.
65. Lee JH, Vittone V, Diefenbach E, Cunningham AL, Diefenbach RJ, (2008) Identification of structural protein-protein interactions of herpes simplex virus type 1. Virology 378: 347-354.
66. Miranda-Saksena M, Armati P, Boadle RA, Holland DJ, Cunningham AL, (2000) Anterograde transport of herpes simplex virus type 1 in cultured, dissociated human and rat dorsal root ganglion neurons. J Virol 74: 1827-1839.
67. Negatsch A, Granzow H, Maresch C, Klupp BG, Fuchs W, et al. (2010) Ultrastructural analysis of virion formation and intraaxonal transport of herpes simplex virus type 1 in primary rat neurons. J Virol 84: 13031-13035.
68. Gazzola M, Burckhardt CJ, Bayati B, Engelke M, Greber UF, et al. (2009) A stochastic model for microtubule motors describes the in vivo cytoplasmic transport of human adenovirus. PLoS Comput Biol 5: e1000623.
69. Klupp BG, Granzow H, Keil GM, Mettenleiter TC, (2006) The capsid-associated UL25 protein of the alphaherpesvirus pseudorabies virus is nonessential for cleavage and encapsidation of genomic DNA but is required for nuclear egress of capsids. J Virol 80: 6235-6246.
70. Baines JD, Cunningham C, Nalwanga D, Davison A, (1997) The U(L)15 gene of herpes simplex virus type 1 contains within its second exon a novel open reading frame that is translated in frame with the U(L)15 gene product. J Virol 71: 2666-2673.
71. Trus BL, Gibson W, Cheng N, Steven AC, (1999) Capsid structure of simian cytomegalovirus from cryoelectron microscopy: evidence for tegument attachment sites. J Virol 73: 2181-2192.
72. Negatsch A, Mettenleiter TC, Fuchs W, (2011) Herpes simplex virus type 1 strain KOS carries a defective US9 and a mutated US8A gene. J Gen Virol 92: 167-172.
73. Lyman MG, Curanovic D, Enquist LW, (2008) Targeting of pseudorabies virus structural proteins to axons requires association of the viral Us9 protein with lipid rafts. PLoS Pathog 4: e1000065.
74. Ben-Harush K, Maimon T, Patla I, Villa E, Medalia O, (2010) Visualizing cellular processes at the molecular level by cryo-electron tomography. J Cell Sci 123: 7-12.
75. Forster F, Hegerl R, (2007) Structure determination in situ by averaging of tomograms. Methods Cell Biol 79: 741-767.
76. Toropova K, Huffman JB, Homa FL, Conway JF, (2011) 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 85: 7513-7522.
77. Thurlow JK, Murphy M, Stow ND, Preston VG, (2006) Herpes simplex virus type 1 DNA-packaging protein UL17 is required for efficient binding of UL25 to capsids. J Virol 80: 2118-2126.
78. Cockrell SK, Huffman JB, Toropova K, Conway JF, Homa FL, (2011) Residues of the UL25 protein of herpes simplex virus that are required for its stable interaction with capsids. J Virol 85: 4875-4887.
79. Pasdeloup D, Blondel D, Isidro AL, Rixon FJ, (2009) Herpesvirus capsid association with the nuclear pore complex and viral DNA release involve the nucleoporin CAN/Nup214 and the capsid protein pUL25. J Virol 83: 6610-6623.
80. Klupp BG, Fuchs W, Granzow H, Nixdorf R, Mettenleiter TC, (2002) Pseudorabies virus UL36 tegument protein physically interacts with the UL37 protein. J Virol 76: 3065-3071.
81. Vittone V, Diefenbach E, Triffett D, Douglas MW, Cunningham AL, et al. (2005) Determination of interactions between tegument proteins of herpes simplex virus type 1. J Virol 79: 9566-9571.
82. Ko DH, Cunningham AL, Diefenbach RJ, (2010) The major determinant for addition of tegument protein pUL48 (VP16) to capsids in herpes simplex virus type 1 is the presence of the major tegument protein pUL36 (VP1/2). J Virol 84: 1397-1405.
83. Witte H, Neukirchen D, Bradke F, (2008) Microtubule stabilization specifies initial neuronal polarization. J Cell Biol 180: 619-632.
84. Perdue ML, Kemp MC, Randall CC, O'Callaghan DJ, (1974) Studies of the molecular anatomy of the L-M cell strain of equine herpes virus type 1: proteins of the nucleocapsid and intact virion. Virology 59: 201-216.
85. Kremer JR, Mastronarde DN, McIntosh JR, (1996) Computer visualization of three-dimensional image data using IMOD. J Struct Biol 116: 71-76.
86. Heymann JB, Belnap DM, (2007) Bsoft: image processing and molecular modeling for electron microscopy. J Struct Biol 157: 3-18.
87. Cheng N, Trus BL, Belnap DM, Newcomb WW, Brown JC, et al. (2002) Handedness of the herpes simplex virus capsid and procapsid. J Virol 76: 7855-7859.