Three-dimensional imaging of viral infections

Annual Review of Virology

Volumn 1, Issue 1, 2014, Pages 453-473

  Risco, Cristina ^a   De Castro, Isabel Fernández ^a   Sanz Sánchez, Laura ^a   Narayan, Kedar ^b   Grandinetti, Giovanna ^b   Subramaniam, Sriram ^b  

^a CENTRO NACIONAL DE BIOTECNOLOGÍA   (Spain)

^b NATIONAL CANCER INSTITUTE   (United States)

Author keywords

3D electron microscopy; Virus egress; Virus entry; Virus factory; Virus replication; Virus cell interactions

Indexed keywords

ARTICLE; CELL ORGANELLE; CELL TRANSFER; ELECTRON TOMOGRAPHY; MOLECULAR IMAGING; NONHUMAN; PRIORITY JOURNAL; SCANNING ELECTRON MICROSCOPY; THREE DIMENSIONAL IMAGING; TRANSMISSION ELECTRON MICROSCOPY; VIRUS ENTRY; VIRUS INFECTION; VIRUS MORPHOGENESIS; VIRUS RELEASE; VIRUS REPLICATION; VIRUS TRANSMISSION;

EID: 85017030086     PISSN: 2327056X     EISSN: 23270578     Source Type: Journal    
DOI: 10.1146/annurev-virology-031413-085351     Document Type: Article

References (151)

1. Studer D,Humbel BM, Chiquet M. 2008. Electron microscopy of high-pressure frozen samples: bridging the gap between cellular ultrastructure and atomic resolution. Histochem. Cell Biol. 130:877-89
2. Hurbain I, Sachse M. 2011. The future is cold: cryo-preparation methods for transmission electron microscopy of cells. Biol. Cell 103:405-20
3. Lučić V, Förster F, Baumeister W. 2005. Structural studies by electron tomography: from cells to molecules. Annu. Rev. Biochem. 74:833-65
4. Holmes KV. 1975. Scanning electron microscopic studies of virus-infected cells. I. Cytopathic effects and maturation of vesicular stomatitis virus in L2 cells. J. Virol. 15:355-62
5. Gonda MA, Gilden RV, Hsu KC. 1979. An unlabeled antibody macromolecule technique using hemocyanin for the identification of type B and type C retrovirus envelope and cell surface antigens by correlative fluorescence, transmission electron, and scanning electron microscopy. J. Histochem. Cytochem. 27:1445-54
6. Szajner P, Weisberg AS, Lebowitz J, Heuser J, Moss B. 2005. External scaffold of spherical immature poxvirus particles is made of protein trimers, forming a honeycomb lattice. J. Cell Biol. 170:971-81
7. Zauberman N, Mutsafi Y, Ben Halevy D, Shimoni E, Klein E, et al. 2008. Distinct DNA exit and packaging portals in the virus Acanthamoeba polyphaga mimivirus. PLoS Biol. 6:e114
8. Wild P, Senn C, Manera CL, Sutter E, Schraner EM, et al. 2009. Exploring the nuclear envelope of herpes simplex virus 1-infected cells by high-resolution microscopy. J. Virol. 83:408-19
9. 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 302:1396-98
10. Cyrklaff M, Risco C, Fernández JJ, Jiménez MV, Estéban M, et al. 2005. Cryo-electron tomography of vaccinia virus. Proc. Natl. Acad. Sci. USA 102:2772-77
11. Kopek BG, Perkins G, Miller DJ, Ellisman MH, Ahlquist P. 2007. Three-dimensional analysis of a viral RNA replication complex reveals a virus-induced mini-organelle. PLoS Biol. 5:e220
12. Iwasaki K, Omura T. 2010. Electron tomography of the supramolecular structure of virus-infected cells. Curr. Opin. Struct. Biol. 20:632-39
13. Fu C-Y, Johnson JE. 2011. Viral life cycles captured in three-dimensions with electron microscopy tomography. Curr. Opin. Virol. 1:125-33
14. Earl LA, Lifson JD, Subramaniam S. 2013. Catching HIV 'in the act' with 3D electron microscopy. Trends Microbiol. 21:397-404
15. Fernández de Castro I, Volonté L, Risco C. 2013. Virus factories: biogenesis and structural design. Cell. Microbiol. 15:24-34
16. Paul D, Bartenschlager R. 2013. Architecture and biogenesis of plus-strand RNA virus replication factories. World J. Virol. 2:32-48
17. Heymann JAW, Shi D, Kim S, Bliss D, Milne JLS, Subramaniam S. 2009. 3D imaging of mammalian cells with ion-abrasion scanning electron microscopy. J. Struct. Biol. 166:1-7
18. Murphy GE, Narayan K, Lowekamp BC, Hartnell LM, Heymann JAW, et al. 2011. Correlative 3D imaging of whole mammalian cells with light and electron microscopy. J. Struct. Biol. 176:268-78
19. Narayan K, Danielson CM, Lagarec K, Lowekamp BC, Coffman P, et al. 2014. Multi-resolution correlative focused ion beam scanning electron microscopy: applications to cell biology. J. Struct. Biol. 185:278-84
20. Mercer J, Helenius A. 2008. Vaccinia virus uses macropinocytosis to enter host cells. Science 320:531-35
21. Mercer J, Helenius A. 2009. Virus entry by macropinocytosis. Nat. Cell Biol. 11:510-20
22. Cyrklaff M, Linaroudis A, Boicu M, Chlanda P, Baumeister W, et al. 2007. Whole cell cryo-electron tomography reveals distinct disassembly intermediates of vaccinia virus. PLoS ONE 2:e420
23. Peng L, Ryazantsev S, Sun R, Zhou ZH. 2010. Three-dimensional visualization of gammaherpesvirus life cycle in host cells by electron tomography. Structure 18:47-58
24. Sougrat R, Bartesaghi A, Lifson JD, Bennett AE, Bess JW, et al. 2007. Electron tomography of the contact between T cells and SIV/HIV-1: implications for viral entry. PLoS Pathog. 3:e63
25. Kuhmann SE, Platt EJ, Kozak SL, Kabat D. 2000. Cooperation of multipleCCR5 coreceptors is required for infections by human immunodeficiency virus type 1 J Virol 74:7005-15
26. Maurer UE, Sodeik B, Grünewald K. 2008. Native 3D intermediates of membrane fusion in herpes simplex virus 1 entry. Proc. Natl. Acad. Sci. USA 105:10559-64
27. Novoa RR, Calderita G, Arranz R, Fontana J, Granzow H, Risco C. 2005. Virus factories: associations of cell organelles for viral replication and morphogenesis. Biol. Cell 97:147-72
28. Netherton CL, Wileman T. 2011. Virus factories, double membrane vesicles and viroplasm generated in animal cells. Curr. Opin. Virol. 1:381-87
29. Wileman T. 2007. Aggresomes and pericentriolar sites of virus assembly: cellular defense or viral design? Annu. Rev. Microbiol. 61:149-67
30. Fontana J, López-Iglesias C, Tzeng WP, Frey TK, Fernández JJ, Risco C. 2010. Three-dimensional structure of Rubella virus factories. Virology 405:579-91
31. Wei T, Miyazaki N, Uehara-Ichiki T, Hibino H, Shimizu T, et al. 2011. Three-dimensional analysis of the association of viral particles with mitochondria during replication of Rice gall dwarf virus. J. Mol. Biol. 410:436-46
32. Fontana J, López-Montero N, Elliott RM, Fernández JJ, Risco C. 2008. The unique architecture of Bunyamwera virus factories around the Golgi complex. Cell. Microbiol. 10:2012-28
33. Ferraris P, Beaumont E, Uzbekov R, Brand D, Gaillard J, et al. 2013. Sequential biogenesis of host cell membrane rearrangements induced by hepatitis C virus infection. Cell. Mol. Life Sci. 70:1297-306
34. Risco C, Fernández de Castro I. 2013. Virus morphogenesis in the cell: methods and observations. In Structure and Physics of Viruses: An Integrated Textbook, ed. MG Mateu, pp. 417-40. Dordrecht: Springer SBM
35. Fernández de Castro I, Zamora PF, Ooms L, Fernández JJ, Lai CM-H, et al. 2014. Reovirus forms neo-organelles for progeny particle assembly within reorganized cell membranes. mBio 5:e00931-13
36. Hoenger A, McIntosh JR. 2008. Probing the macromolecular organization of cells by electron tomography. Curr. Opin. Cell Biol. 21:89-96
37. Lučić V, Rigort A, Baumeister W. 2013. Cryo-electron tomography: the challenge of doing structural biology in situ. J. Cell Biol. 202:407-19
38. Briggs JAG. 2013. Structural biology in situ-the potential of subtomogram averaging. Curr. Opin. Struct. Biol. 23:261-67
39. Erickson KD, Bouchet-Marquis C, Heiser K, Szomolanyi-Tsuda E, Mishra R, et al. 2013. Virion assembly factories in the nucleus of polyomavirus-infected cells. PLoS Pathog. 8:e1002630
40. Bernardi R, Pandolfi PP. 2007. Structure, dynamics and functions of promyelocytic leukaemia nuclear bodies. Nat. Rev. Mol. Cell Biol. 8:1006-16
41. Simon DN, Wilson KL. 2011. The nucleoskeleton as a genome-associated dynamic "network of networks." Nat. Rev. Mol. Cell Biol. 12:695-708
42. López-Iglesias C, Puvion-Dutilleul F. 1988. Ultrastructural localization of glycoproteins in rabbit fibroblasts altered by herpes simplex virus type 1 infection. Biol. Cell 62:47-56
43. Mettenleiter TC, Klupp BG, Granzow H. 2006. Herpesvirus assembly: a tale of two membranes. Curr. Opin. Microbiol. 9:423-29
44. Klupp BG, Granzow H, Fuchs W, Keil GM, Finke S, Mettenleiter TC. 2007. Vesicle formation from the nuclear membrane is induced by coexpression of two conserved herpesvirus proteins. Proc. Natl. Acad. Sci. USA 104:7241-46
45. Miller S, Krijnse-Locker J. 2008. Modification of intracellular membrane structures for virus replication. Nat. Rev. Microbiol. 6:363-74
46. den Boon JA, Ahlquist P. 2010. Organelle-like membrane compartmentalization of positive-strand virus replication factories. Annu. Rev. Microbiol. 64:241-56
47. Frolova EI, Gorchakov R, Pereboeva L, Atasheva S, Frolov I. 2010. Functional Sindbis virus replicative complexes are formed at the plasma membrane. J. Virol. 84:11679-95
48. Spuul P, Balistreri G, Kääriäinen L, Ahola T. 2010. Phosphatidylinositol 3-kinase-, actin-, and microtubule-dependent transport of Semliki Forest virus replication complexes from the plasma membrane to modified lysosomes. J. Virol. 84:7543-57
49. Risco C, Sanmartín-Conesa E, Tzeng WP, Frey TK, Seybold V, de Groot RJ. 2012. Specific, sensitive, high-resolution detection of protein molecules in eukaryotic cells using metal-tagging transmission electron microscopy. Structure 20:759-66
50. Kujala P, Ikäheimonen A, Ehsani N, Vihinen H, Auvinen P, Kääriänien L. 2001. Biogenesis of the Semliki Forest virus RNA replication complex. J. Virol. 75:3873-84
51. Prod'homme D, Le Panse S, Grugeon G, Jupin I. 2001. Detection and subcellular localization of the Turnip yellow mosaic virus 66K replication protein in infected cells. Virology 281:88-101
52. Nagy PD, Pogany J. 2011. The dependence of viral RNA replication on co-opted host factors. Nat. Rev. Microbiol. 10:137-48
53. Barajas D, Jiang Y, Nagy PD. 2009. A unique role for the host ESCRT proteins in replication of Tomato bushy stunt virus. PLoS Pathog. 5:e1000705
54. Diaz A, Wang X, Alhquist P. 2010. Membrane-shaping host reticulon proteins play crucial roles in viral RNA replication compartment formation and function. Proc. Natl. Acad. Sci. USA 107:16291-96
55. Liu ST, Sharon-Friling R, Ivanova P, Milne SB, Myers DS, et al. 2011. Synaptic vesicle-like lipidome of human cytomegalovirus virions reveals a role for SNARE machinery in virion egress. Proc. Natl. Acad. Sci. USA 108:12869-74
56. Nagy PD, Barajas D, Pogany J. 2012. Host factors with regulatory roles in tombusvirus replication. Curr. Opin. Virol. 2:691-98
57. Gillespie LK, Hoenen A, Morgan G, Mackenzie JM. 2010. The endoplasmic reticulum provides the membrane platform for biogenesis of the flavivirus replication complex. J. Virol. 84:10438-47
58. Welsch S, Miller S,Romero-Brey I, Merz A, Bleck CKE, et al. 2009. Composition and three-dimensional architecture of the dengue virus replication and assembly sites. Cell Host Microbe 6:81-90
59. Knoops K, KikkertM,WormSH, Zevenhoven-Dobbe JC, van der Meer Y, et al. 2008. SARS-coronavirus replication is supported by a reticulovesicular network of modified endoplasmic reticulum. PLoS Biol. 6:e226
60. Limpens RWAL, van der Schaar HM, Kumar D, Koster AJ, Snijder EJ, et al. 2011. The transformation of enterovirus replication structures: a three-dimensional study of single-and double-membrane compartments. mBio 2:e00166-11
61. Knoops K, Bárcena M, Limpens RW, Koster AJ, Mommaas AM, Snijder EJ. 2012. Ultrastructural characterization of arterivirus replication structures: reshaping the endoplasmic reticulum to accommodate viral RNA synthesis. J. Virol. 86:2474-87
62. Belov GA, Nair V, Hansen BT,Hoyt FH, Fischer ER, Ehrenfeld E. 2012. Complex dynamic development of poliovirus membranous replication complexes. J. Virol. 86:302-12
63. Romero-Brey I, Merz A, Chiramel A, Lee J-Y, Chlanda P, et al. 2012. Three-dimensional architecture and biogenesis of membrane structures associated with hepatitis C virus replication. PLoS Pathog. 8:e1003056
64. Griffiths G, Roos N, Schleich S, Locker JK. 2001. Structure and assembly of intracellular mature vaccinia virus: thin-section analysis. J. Virol. 75:11056-70
65. Risco C, Rodríguez JR, López-Iglesias C, Carrascosa JL, Esteban M, Rodríguez D. 2002. Endoplasmic reticulum-Golgi intermediate compartment membranes and vimentin filaments participate in vaccinia virus assembly. J. Virol. 76:1839-55
66. Pais-Correia A-M, Sachse M, Guadagnini S, Robbiati V, Lasserre R, et al. 2010. Biofilm-like extracellular viral assemblies mediate HTLV-1 cell-to-cell transmission at virological synapses. Nat. Med. 16:83-89
67. Miorin L, Romero-Brey I, Maiuri P, Hoppe S, Krijnse-Locker J, et al. 2013. Three-dimensional architecture of tick-borne encephalitis virus replication sites and trafficking of the replicated RNA. J. Virol. 87:6469-81
68. Kukulski W, Schorb M, Welsch S, Picco A, Kaksonen M, Briggs JAG. 2011. Correlated fluorescence and 3D electron microscopy with high sensitivity and spatial precision. J. Cell Biol. 192:111-19
69. McDonald KL. 2007. Cryopreparation methods for electron microscopy of selected model systems. Methods Cell Biol. 79:23-56
70. Sosinsky GE, Crum J, Jones YZ, Lanman J, Smarr B, et al. 2008. The combination of chemical fixation procedures with high pressure freezing and freeze substitution preserves highly labile tissue ultrastructure for electron tomography applications. J. Struct. Biol. 161:359-71
71. Mercogliano CP, DeRosier DJ. 2007. Concatenated metallothionein as a clonable gold label for electron microscopy. J. Struct. Biol. 160:70-82
72. Diestra E, Fontana J, Guichard P, Marco S, Risco C. 2009. Visualization of proteins in intact cells with a clonable tag for electron microscopy. J. Struct. Biol. 165:157-68
73. Shu X, Lev-Ram V, Deerinck TJ, Qi Y, Ramko EB, et al. 2011. A genetically encoded tag for correlated light and electron microscopy of intact cells, tissues and organisms. PLoS Biol. 9:e1001041
74. Bouchet-Marquis C, Pagratis M, Kirmse R, Hoenger A. 2012. Metallothionein as a clonable high-density marker for cryo-electron microscopy. J. Struct. Biol. 177:119-27
75. Martell JD, Deerinck TJ, Sancak Y, Poulos TL, Mootha VK, et al. 2012. Engineered ascorbate peroxidase as a genetically encoded reporter for electron microscopy. Nat. Biotechnol. 30:1143-48
76. Barajas D, Martín I, Pogany J, Risco C, Nagy PD. 2014. Noncanonical role for the host Vps4 AAA+ ATPase ESCRT protein in the formation of Tomato bushy stunt virus replicase. PLoS Pathog. 10:e1004087
77. Fernández JJ. 2012. Computational methods for electron tomography. Micron 43:1010-30
78. Schur FKM, Hagen WJH, de Marco A, Briggs JAG. 2013. Determination of protein structure at 8.5A resolution using cryo-electron tomography and sub-tomogram averaging. J. Struct. Biol. 184:394-400
79. Chlanda P, Carbajal MA, Cyrklaff M, Griffiths G, Krijnse-Locker J. 2009. Membrane rupture generates single open membrane sheets during vaccinia virus assembly. Cell Host Microbe 6:81-90
80. Mutsafi Y, Shimoni E, Shimon A, Minsky A. 2013. Membrane assembly during the infection cycle of the giant Mimivirus. PLoS Pathog. 9:e1003367
81. Suárez C, Welsch S, Chlanda P, Hagen W, Hoppe S, et al. 2013. Open membranes are the precursors for assembly of large DNA viruses. Cell. Microbiol. 15:1883-95
82. Suzan-Monti M, La Scola B, Barrassi L, Espinosa L, Raoult D. 2007. Ultrastructural characterization of the giant volcano-like virus factory of Acanthamoeba polyphaga Mimivirus. PLoS ONE 2:e328
83. Aoyama K, Takagi T, Hirase A, Miyazawa A. 2008. STEM tomography for thick biological specimens. Ultramicroscopy 109:70-80
84. Krijnse-Locker J, Schleich S, Rodríguez D, Goud B, Snijder EJ, Griffiths G. 1996. The role of a 21-kDa viral membrane protein in the assembly of vaccinia virus from the intermediate compartment. J. Biol. Chem. 271:14950-58
85. Rodríguez JR, Risco C, Carrascosa JL, Esteban M, Rodríguez D. 1998. Vaccinia virus 15-kilodalton (A14L) protein is essential for assembly and attachment of viral crescents to virosomes. J. Virol. 72:1287-96
86. Grünewald K, Cyrklaff M. 2006. Structure of complex viruses and virus-infected cells by electron cryo tomography. Curr. Opin. Microbiol. 9:437-42
87. Ibiricu I, Huiskonen JT,Döhner K, Bradke F, Sodeik B, Grünewald K. 2011. Cryo electron tomography of herpes simplex virus during axonal transport and secondary envelopment in primary neurons. PLoS Pathog. 7:e1002406
88. Offerdahl DK, Dorward DW, Hansen BT, Bloom ME. 2012. A three-dimensional comparison of tickborne flavivirus infection in mammalian and tick cell lines. PLoS ONE 7:e47912
89. Miyazaki N, Nakagawa A, Iwasaki K. 2013. Life cycle of phytoreoviruses visualized by electron microscopy and tomography. Front. Microbiol. 4:1-9
90. Carlson LA, Briggs JA, Glass B, Riches JD, Simon MN, et al. 2008. Three-dimensional analysis of budding sites and released virus suggests a revised model for HIV-1 morphogenesis. Cell Host Microbe 4:592-99
91. Carlson LA, de Marco A, Oberwinkler H, Habermann, Briggs JAG, et al. 2010. Cryo electron tomography of native HIV-1 budding sites. PLoS Pathog. 6:e1001173
92. Briggs JAG, Kräusslich H-G. 2011. The molecular architecture of HIV. J. Mol. Biol. 410:491-500
93. Noda T, Sagara H, Yen A, Takada A, Kida H, et al. 2006. Architecture of ribonucleoprotein complexes in influenza A virus particles. Nature 439:490-92
94. Vijayakrishnan S, Loney C, Jackson D, Suphamungmee W, Rixon FJ, Bhella D. 2013. Cryotomography of budding influenza A virus reveals filaments with diverse morphologies that mostly do not bear a genome at their distal end. PLoS Pathog. 9:e1003413
95. Welsch S, Kolesnikova L, Krähling V, Riches JD, Becker S, Briggs JAG. 2010. Electron tomography reveals the steps in filovirus budding. PLoS Pathog. 6:e1000875
96. Bharat TAM, Riches JD, Kolesnikova L, Welsch S, Krähling V, et al. 2011. Cryo-electron tomography of Marburg virus particles and their morphogenesis within infected cells. PLoS Biol. 9:e1001196
97. Noda T, Ebihara H, Muramoto Y, Fuji K, Takada A, et al. 2006. Assembly and budding of Ebolavirus. PLoS Pathog. 2:e99
98. Welsch S,Müller B, Kräusslich H-G. 2007. More than one door-budding of enveloped viruses through cellular membranes. FEBS Lett. 581:2089-97
99. Votteler J, Sundquist WI. 2013. Virus budding and the ESCRT pathway. Cell Host Microbe 14:232-41
100. Schauflinger M, Fischer D, Schreiber A, Chevillotte M, Walther P, et al. 2011. The tegument protein UL71 of human cytomegalovirus is involved in late envelopment and affects multivesicular bodies. J. Virol. 85:3821-32
101. Schauflinger M, Villinger C, Mertens T, Walther P, von Einem J. 2013. Analysis of human cytomegalovirus secondary envelopment by advanced electron microscopy. Cell. Microbiol. 15:305-14
102. Mettenleiter TC. 2004. Budding events in herpesvirus morphogenesis. Virus Res. 106:167-80
103. Lescar J, Roussel A, WienMW,Navaza J, Fuller SD, et al. 2001. The fusion glycoprotein shell of Semliki Forest virus: an icosahedral assembly primed for fusogenic activation at endosomal pH. Cell 105:137-48
104. Soonsawad P, Xing L, Milla E, Espinoza JM, Kawano M, et al. 2010. Structural evidence of glycoprotein assembly in cellular membrane compartments prior to alphavirus budding. J. Virol. 84:11145-51
105. von Schwedler UK, Stuchell M, Müller B, Ward DM, Chung H-Y, et al. 2003. The protein network of HIV budding. Cell 114:701-13
106. Jolly C, Mitar I, Sattentau QJ. 2007. Adhesion molecule interactions facilitate human immunodeficiency virus type 1-induced virological synapse formation between T cells. J. Virol. 81:13916-21
107. Piguet V, Sattentau Q. 2004. Dangerous liaisons at the virological synapse. J. Clin. Investig. 114:605-10
108. Groot F, Welsch S, Sattentau QJ. 2008. Efficient HIV-1 transmission from macrophages to T cells across transient virological synapses. Blood 111:4660-63
109. Waki K, Freed EO. 2010. Macrophages and cell-cell spread of HIV-1. Viruses 2:1603-20
110. Spearman P. 2006. Cellular cofactors involved in HIV assembly and budding. Curr. Opin. HIV AIDS 1:200-7
111. Raposo G, Moore M, Innes D, Leijendekker R, Leigh-Brown A, et al. 2002. Human macrophages accumulate HIV-1 particles in MHC II compartments. Traffic 3:718-29
112. Yu HJ, Reuter MA, McDonald D. 2008. HIV traffics through a specialized, surface-accessible intracellular compartment during trans-infection of T cells by mature dendritic cells. PLoS Pathog. 4:e1000134
113. Marsh M, Theusner K, Pelchen-Matthews A. 2009. HIV assembly and budding in macrophages. Biochem. Soc. Trans. 37:185-89
114. Welsch S, Groot F, Kräusslich H-G, Keppler OT, Sattentau QJ. 2011. Architecture and regulation of the HIV-1 assembly and holding compartment in macrophages. J. Virol. 85:7922-27
115. Bennett AE, Narayan K, Shi D, Hartnell LM, Gousset K, et al. 2009. Ion-abrasion scanning electron microscopy reveals surface-connected tubular conduits in HIV-infected macrophages. PLoS Pathog. 5:e1000591
116. Usami Y, Popov S, Popova E, Inoue M, Weissenhorn W, Göttlinger HG. 2009. The ESCRT pathway and HIV-1 budding. Biochem. Soc. Trans. 37:181-84
117. Sundquist WI, Kräusslich HG. 2012. HIV-1 assembly, budding, and maturation. Cold Spring Harb. Perspect. Med. 2:a006924
118. Majorovits E, Nejmeddine M, Tanaka Y, Taylor GP, Fuller SD, Bangham CRM. 2008. Human Tlymphotropic virus-1 visualized at the virological synapse by electron tomography. PLoS ONE 3:e2251
119. Martin N, Welsch S, Jolly C, Briggs JAG, Vaux D, Sattentau QJ. 2010. Virological synapse-mediated spread of human immunodeficiency virus type 1 between T cells is sensitive to entry inhibition. J. Virol. 84:3516-27
120. Zhong P, Agosto LM, Munro JB, Mothes W. 2013. Cell-to-cell transmission of viruses. Curr. Opin. Virol. 3:44-50
121. Kahn JS, Schnell MJ, Buonocore L, Rose JK. 1999. Recombinant vesicular stomatitis virus expressing respiratory syncytial virus (RSV) glycoproteins: RSV fusion protein can mediate infection and cell fusion. Virology 254:81-91
122. Paloheimo O, Ihalainen TO, Tauriainen S, Välilehto O, Kirjavainen S, et al. 2011. Coxsackievirus B3-induced cellular protrusions: structural characteristics and functional competence. J. Virol. 85:6714-24
123. Iwasaki Y, Clark HF. 1975. Cell to cell transmission of virus in the central nervous system. II. Experimental rabies in mouse. Lab. Investig. 33:391-99
124. Dingwell KS, Johnson DC. 1998. The herpes simplex virus gE-gI complex facilitates cell-to-cell spread and binds to components of cell junctions. J. Virol. 72:8933-42
125. van LeeuwenH, Elliott G, O'Hare P. 2002. Evidence of a role for nonmuscle myosin II in herpes simplex virus type 1 egress. J. Virol. 76:3471-81
126. Rudnicka D, Feldmann J, Porrot F, Wietgrefe S, Guadagnini S, et al. 2009. Simultaneous cell-tocell transmission of human immunodeficiency virus to multiple targets through polysynapses. J. Virol. 83:6234-46
127. Jolly C, Mitar I, Sattentau QJ. 2007. Requirement for an intact T-cell actin and tubulin cytoskeleton for efficient assembly and spread of human immunodeficiency virus type 1. J. Virol. 81:5547-60
128. Kupfer A, Swain SL, Singer SJ. 1987. The specific direct interaction of helper T cells and antigenpresenting B cells. II. Reorientation of the microtubule organizing center and reorganization of the membrane-associated cytoskeleton inside the bound helper T cells. J. Exp. Med. 165:1565-80
129. Stinchcombe JC, Majorovits E, Bossi G, Fuller S, Griffiths GM. 2006. Centrosome polarization delivers secretory granules to the immunological synapse. Nature 443:462-65
130. Sowinski S, Jolly C, Berninghausen O, Purbhoo MA, Chauveau A, et al. 2008. Membrane nanotubes physically connect T cells over long distances presenting a novel route for HIV-1 transmission. Nat. Cell Biol. 10:211-19
131. Hübner W, McNerney GP, Chen P, Dale BM, Gordon RE, et al. 2009. Quantitative 3D video microscopy of HIV transfer across T cell virological synapses. Science 323:1743-47
132. Gan L, Jensen GJ. 2012. Electron tomography of cells. Q. Rev. Biophys. 45:27-56
133. Medalia O, Beck M, Ecke M, Weber I, Neujahr R, et al. 2007. Organization of actin networks in intact filopodia. Curr. Biol. 17:79-84
134. Wang K, Strunk K, Zhao G, Gray JL, Zhang P. 2012. 3D structure determination of native mammalian cells using cryo-FIB and cryo-electron tomography. J. Struct. Biol. 180:318-26
135. Rigort A, Villa E, Bäuerlein FJ, Engel BD, Plitzko JM. 2012. Integrative approaches for cellular cryoelectron tomography: correlative imaging and focused ion beam micromachining. Methods Cell Biol. 111:259-81
136. Felts RL, Narayan K, Estes JD, Shi D, Trubey CM, et al. 2010. 3D visualization of HIV transfer at the virological synapse between dendritic cells and T cells. Proc. Natl. Acad. Sci. USA 107:13336-41
137. Lim JP, Gleeson PA. 2011. Macropinocytosis: an endocytic pathway for internalising large gulps. Immunol. Cell Biol. 89:836-43
138. Garcia E, Nikolic DS, Piguet V. 2008. HIV-1 replication in dendritic cells occurs through a tetraspanincontaining compartment enriched in AP-3. Traffic 9:200-14
139. Al-Amoudi A, Studer D, Dubochet J. 2005. Cutting artefacts and cutting process in vitreous sections for cryo-electron microscopy. J. Struct. Biol. 150:109-21
140. Chlanda P, Sachse M. 2014. Cryo-electron microscopy of vitreous sections. Methods Mol. Biol. 1117:193-214
141. van Weering JRT, Brown E, Sharp TH, Mantell J, Cullen PJ, Verkade P. 2010. Intracellular membrane traffic at high resolution. Methods Cell Biol. 96:619-48
142. Jouvenet N, Zhadina M, Bieniasz PD, Simon SM. 2011. Dynamics of ESCRT protein recruitment during retroviral assembly. Nat. Cell Biol. 13:394-401
143. Fogarty KH, Zhang W, Grigsby IF, Johnson JL, Chen Y, et al. 2011. New insights intoHTLV-1 particle structure, assembly, and Gag-Gag interactions in living cells. Viruses 3:770-93
144. Chojnacki J, Staudt T, Glass B, Bingen P, Engelhardt J, et al. 2012. Maturation-dependent HIV-1 surface protein redistribution revealed by fluorescence nanoscopy. Science 26:524-28
145. Lelek M, Di Nunzio F, Henriques R, Charneau P, Arhel N, Zimmer C. 2012. Superresolution imaging of HIV in infected cells with FlAsH-PALM. Proc. Natl. Acad. Sci. USA 109:8564-69
146. Goto T, Nakai M, Ikuta K. 1998. The life-cycle of human immunodeficiency virus type 1. Micron 29:123-38
147. Pelchen-Matthews A, Marsh M. 2007. Electron microscopy analysis of viral morphogenesis. Methods Cell Biol. 79:515-42
148. Szakal C, Narayan K, Fu J, Lefman J, Subramaniam S. 2011. Compositional mapping of the surface and interior of mammalian cells at submicrometer resolution. Anal. Chem. 83:1207-13
149. Narayan K, Prosa TJ, Fu J, Kelly TF, Subramaniam S. 2012. Chemical mapping of mammalian cells by atom probe tomography. J. Struct. Biol. 178:98-107
150. Hagen C, Guttmann P, Klupp B, Werner S, Rehbein S, et al. 2012. Correlative VIS-fluorescence and soft X-ray cryo-microscopy/tomography of adherent cells. J. Struct. Biol. 177:193-201
151. Carzaniga R, Domart M-C, Collinson LM, Duke E. 2014. Cryo-soft X-ray tomography: a journey into the world of the native-state cell. Protoplasma 251:449-58