Endoplasmic reticulum: The favorite intracellular niche for viral replication and assembly

Viruses

Volumn 8, Issue 6, 2016, Pages

  Romero Brey, Inés ^a   Bartenschlager, Ralf ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

Cell membranes; Electron microscopy; Intracellular organelles; Membrane rearrangements; Nuclear envelope; Peripheral endoplasmic reticulum (ER); Vesicles; Viral replication; Virion assembly; Virus host interactions

Indexed keywords

CELL NUCLEUS MEMBRANE; ELECTRON MICROSCOPY; ENDOPLASMIC RETICULUM MEMBRANE; GENE AMPLIFICATION; MORPHOLOGY; POSITIVE-STRAND RNA VIRUS; PROGENY; VIRION; VIRUS CELL INTERACTION; VIRUS REPLICATION; ANIMAL; ENDOPLASMIC RETICULUM; HOST PATHOGEN INTERACTION; HUMAN; PHYSIOLOGY; RNA VIRUS; VIROLOGY; VIRUS ASSEMBLY;

ANIMALS; ENDOPLASMIC RETICULUM; HOST-PATHOGEN INTERACTIONS; HUMANS; RNA VIRUSES; VIRUS ASSEMBLY; VIRUS REPLICATION;

EID: 84973369331     PISSN: None     EISSN: 19994915     Source Type: Journal    
DOI: 10.3390/v8060160     Document Type: Review

References (214)

1. Schuldiner, M.; Schwappach, B. From rags to riches—The history of the endoplasmic reticulum. Biochim. Biophys. Acta 2013, 1833, 2389–2391. [CrossRef] [PubMed]
2. Veratti, E. Investigations on the fine structure of striated muscle fiber read before the reale istituto lombardo, 13 March 1902. J. Biophys. Biochem. Cytol. 1961, 10, 1–59. [CrossRef] [PubMed]
3. Porter, K.R. Observations on a submicroscopic basophilic component of cytoplasm. J. Exp. Med. 1953, 97, 727–750. [CrossRef] [PubMed]
4. Palade, G.E.; Porter, K.R. Studies on the endoplasmic reticulum. I. Its identification in cells in situ. J. Exp. Med. 1954, 100, 641–656. [CrossRef] [PubMed]
5. Porter, K.R.; Palade, G.E. Studies on the endoplasmic reticulum. III. Its form and distribution in striated muscle cells. J. Biophys. Biochem. Cytol. 1957, 3, 269–300. [CrossRef] [PubMed]
6. Westrate, L.M.; Lee, J.E.; Prinz, W.A.; Voeltz, G.K. Form follows function: The importance of endoplasmic reticulum shape. Annu. Rev. Biochem. 2015, 84, 791–811. [CrossRef] [PubMed]
7. Terasaki, M.; Shemesh, T.; Kasthuri, N.; Klemm, R.W.; Schalek, R.; Hayworth, K.J.; Hand, A.R.; Yankova, M.; Huber, G.; Lichtman, J.W.; et al. Stacked endoplasmic reticulum sheets are connected by helicoidal membrane motifs. Cell 2013, 154, 285–296. [CrossRef] [PubMed]
8. Shibata, Y.; Shemesh, T.; Prinz, W.A.; Palazzo, A.F.; Kozlov, M.M.; Rapoport, T.A. Mechanisms determining the morphology of the peripheral ER. Cell 2010, 143, 774–788. [CrossRef] [PubMed]
9. Lin, S.; Sun, S.; Hu, J. Molecular basis for sculpting the endoplasmic reticulum membrane. Int. J. Biochem. Cell Biol. 2012, 44, 1436–1443. [CrossRef] [PubMed]
10. Razafsky, D.; Hodzic, D. Nuclear envelope: Positioning nuclei and organizing synapses. Curr. Opin. Cell Biol. 2015, 34, 84–93. [CrossRef] [PubMed]
11. Meinke, P.; Schirmer, E.C. Linc’ing form and function at the nuclear envelope. FEBS Lett. 2015, 589, 2514–2521.[CrossRef] [PubMed]
12. Burke, B.; Ellenberg, J. Remodelling the walls of the nucleus. Nat. Rev. Mol. Cell Biol. 2002, 3, 487–497.[CrossRef] [PubMed]
13. Hetzer, M.W.; Walther, T.C.; Mattaj, I.W. Pushing the envelope: Structure, function, and dynamics of the nuclear periphery. Annu. Rev. Cell Dev. Biol. 2005, 21, 347–380. [CrossRef] [PubMed]
14. D’Angelo, M.A.; Hetzer, M.W. The role of the nuclear envelope in cellular organization. Cell. Mol. Life Sci. 2006, 63, 316–332. [CrossRef] [PubMed]
15. Yamauchi, Y.; Helenius, A. Virus entry at a glance. J. Cell Sci. 2013, 126, 1289–1295. [CrossRef] [PubMed]
16. Pante, N.; Kann, M. Nuclear pore complex is able to transport macromolecules with diameters of about 39 nm. Mol. Biol. Cell 2002, 13, 425–434. [CrossRef] [PubMed]
17. Kiseleva, E.; Morozova, K.N.; Voeltz, G.K.; Allen, T.D.; Goldberg, M.W. Reticulon 4a/NogoA locates to regions of high membrane curvature and may have a role in nuclear envelope growth. J. Struct. Biol. 2007, 160, 224–235. [CrossRef] [PubMed]
18. Sparkes, I.; Tolley, N.; Aller, I.; Svozil, J.; Osterrieder, A.; Botchway, S.; Mueller, C.; Frigerio, L.; Hawes, C. Five arabidopsis reticulon isoforms share endoplasmic reticulum location, topology, and membrane-shaping properties. Plant Cell 2010, 22, 1333–1343. [CrossRef] [PubMed]
19. Shibata, Y.; Voeltz, G.K.; Rapoport, T.A. Rough sheets and smooth tubules. Cell 2006, 126, 435–439. [CrossRef] [PubMed]
20. West, M.; Zurek, N.; Hoenger, A.; Voeltz, G.K. A 3D analysis of yeast ER structure reveals how ER domains are organized by membrane curvature. J. Cell Biol. 2011, 193, 333–346. [CrossRef] [PubMed]
21. Schweizer, A.; Ericsson, M.; Bachi, T.; Griffiths, G.; Hauri, H.P. Characterization of a novel 63 kDa membrane protein. Implications for the organization of the ER-to-Golgi pathway. J. Cell Sci. 1993, 104, 671–683.[PubMed]
22. Schweizer, A.; Rohrer, J.; Slot, J.W.; Geuze, H.J.; Kornfeld, S. Reassessment of the subcellular localization of p63. J. Cell Sci. 1995, 108, 2477–2485. [PubMed]
23. Klopfenstein, D.R.; Klumperman, J.; Lustig, A.; Kammerer, R.A.; Oorschot, V.; Hauri, H.P. Subdomain-specific localization of climp-63 (p63) in the endoplasmic reticulum is mediated by its luminal alpha-helical segment. J. Cell Biol. 2001, 153, 1287–1300. [CrossRef] [PubMed]
24. Klopfenstein, D.R.; Kappeler, F.; Hauri, H.P. A novel direct interaction of endoplasmic reticulum with microtubules. EMBO J. 1998, 17, 6168–6177. [CrossRef] [PubMed]
25. Nikonov, A.V.; Snapp, E.; Lippincott-Schwartz, J.; Kreibich, G. Active translocon complexes labeled with GFP-Dad1 diffuse slowly as large polysome arrays in the endoplasmic reticulum. J. Cell Biol. 2002, 158, 497–506. [CrossRef] [PubMed]
26. Nikonov, A.V.; Hauri, H.P.; Lauring, B.; Kreibich, G. Climp-63-mediated binding of microtubules to the ER affects the lateral mobility of translocon complexes. J. Cell Sci. 2007, 120, 2248–2258. [CrossRef] [PubMed]
27. Ogawa-Goto, K.; Tanaka, K.; Ueno, T.; Tanaka, K.; Kurata, T.; Sata, T.; Irie, S. P180 is involved in the interaction between the endoplasmic reticulum and microtubules through a novel microtubule-binding and bundling domain. Mol. Biol. Cell 2007, 18, 3741–3751. [CrossRef] [PubMed]
28. Benyamini, P.; Webster, P.; Meyer, D.I. Knockdown of p180 eliminates the terminal differentiation of a secretory cell line. Mol. Biol. Cell 2009, 20, 732–744. [CrossRef] [PubMed]
29. Ueno, T.; Tanaka, K.; Kaneko, K.; Taga, Y.; Sata, T.; Irie, S.; Hattori, S.; Ogawa-Goto, K. Enhancement of procollagen biosynthesis by p180 through augmented ribosome association on the endoplasmic reticulum in response to stimulated secretion. J. Biol. Chem. 2010, 285, 29941–29950. [CrossRef] [PubMed]
30. Short, B.; Haas, A.; Barr, F.A. Golgins and GTPases, giving identity and structure to the Golgi apparatus. Biochim. Biophys. Acta 2005, 1744, 383–395. [CrossRef] [PubMed]
31. Friedman, J.R.; Voeltz, G.K. The ER in 3D: A multifunctional dynamic membrane network. Trends Cell Biol. 2011, 21, 709–717. [CrossRef] [PubMed]
32. Oertle, T.; Klinger, M.; Stuermer, C.A.; Schwab, M.E. A reticular rhapsody: Phylogenic evolution and nomenclature of the RNT/Nogo gene family. FASEB J. 2003, 17, 1238–1247. [CrossRef] [PubMed]
33. Voeltz, G.K.; Prinz, W.A.; Shibata, Y.; Rist, J.M.; Rapoport, T.A. A class of membrane proteins shaping the tubular endoplasmic reticulum. Cell 2006, 124, 573–586. [CrossRef] [PubMed]
34. Hu, J.; Shibata, Y.; Voss, C.; Shemesh, T.; Li, Z.; Coughlin, M.; Kozlov, M.M.; Rapoport, T.A.; Prinz, W.A. Membrane proteins of the endoplasmic reticulum induce high-curvature tubules. Science 2008, 319, 1247–1250. [CrossRef] [PubMed]
35. Shibata, Y.; Voss, C.; Rist, J.M.; Hu, J.; Rapoport, T.A.; Prinz, W.A.; Voeltz, G.K. The reticulon and DP1/Yop1p proteins form immobile oligomers in the tubular endoplasmic reticulum. J. Biol. Chem. 2008, 283, 18892–18904.[CrossRef] [PubMed]
36. Tolley, N.; Sparkes, I.; Craddock, C.P.; Eastmond, P.J.; Runions, J.; Hawes, C.; Frigerio, L. Transmembrane domain length is responsible for the ability of a plant reticulon to shape endoplasmic reticulum tubules in vivo. Plant J. 2010, 64, 411–418. [CrossRef] [PubMed]
37. Di Sano, F.; Bernardoni, P.; Piacentini, M. The reticulons: Guardians of the structure and function of the endoplasmic reticulum. Exp. Cell Res. 2012, 318, 1201–1207. [CrossRef] [PubMed]
38. Tolley, N.; Sparkes, I.A.; Hunter, P.R.; Craddock, C.P.; Nuttall, J.; Roberts, L.M.; Hawes, C.; Pedrazzini, E.; Frigerio, L. Overexpression of a plant reticulon remodels the lumen of the cortical endoplasmic reticulum but does not perturb protein transport. Traffic 2008, 9, 94–102. [CrossRef] [PubMed]
39. Yang, Y.S.; Strittmatter, S.M. The reticulons: A family of proteins with diverse functions. Genome Biol. 2007, 8, 234. [CrossRef] [PubMed]
40. Roebroek, A.J.; van de Velde, H.J.; van Bokhoven, A.; Broers, J.L.; Ramaekers, F.C.; van de Ven, W.J. Cloning and expression of alternative transcripts of a novel neuroendocrine-specific gene and identification of its 135-kDa translational product. J. Biol. Chem. 1993, 268, 13439–13447. [PubMed]
41. Roebroek, A.J.; Ayoubi, T.A.; van de Velde, H.J.; Schoenmakers, E.F.; Pauli, I.G.; van de Ven, W.J. Genomic organization of the human NSP gene, prototype of a novel gene family encoding reticulons. Genomics 1996, 32, 191–199. [CrossRef] [PubMed]
42. Roebroek, A.J.; Contreras, B.; Pauli, I.G.; van de Ven, W.J. Cdna cloning, genomic organization, and expression of the human rtn2 gene, a member of a gene family encoding reticulons. Genomics 1998, 51, 98–106. [CrossRef] [PubMed]
43. Moreira, E.F.; Jaworski, C.J.; Rodriguez, I.R. Cloning of a novel member of the reticulon gene family (rtn3): Gene structure and chromosomal localization to 11q13. Genomics 1999, 58, 73–81. [CrossRef] [PubMed]
44. GrandPre, T.; Nakamura, F.; Vartanian, T.; Strittmatter, S.M. Identification of the nogo inhibitor of axon regeneration as a reticulon protein. Nature 2000, 403, 439–444. [PubMed]
45. Oertle, T.; Huber, C.; van der Putten, H.; Schwab, M.E. Genomic structure and functional characterisation of the promoters of human and mouse nogo/rtn4. J. Mol. Biol. 2003, 325, 299–323. [CrossRef]
46. Hu, J.; Shibata, Y.; Zhu, P.P.; Voss, C.; Rismanchi, N.; Prinz, W.A.; Rapoport, T.A.; Blackstone, C. A class of dynamin-like GTPases involved in the generation of the tubular ER network. Cell 2009, 138, 549–561.[CrossRef] [PubMed]
47. Anwar, K.; Klemm, R.W.; Condon, A.; Severin, K.N.; Zhang, M.; Ghirlando, R.; Hu, J.; Rapoport, T.A.; Prinz, W.A. The dynamin-like gtpase sey1p mediates homotypic ER fusion in s. Cerevisiae. J. Cell Biol. 2012, 197, 209–217. [CrossRef] [PubMed]
48. Zhu, P.P.; Patterson, A.; Lavoie, B.; Stadler, J.; Shoeb, M.; Patel, R.; Blackstone, C. Cellular localization, oligomerization, and membrane association of the hereditary spastic paraplegia 3a (spg3a) protein atlastin. J. Biol. Chem. 2003, 278, 49063–49071. [CrossRef] [PubMed]
49. Chan, D.C. Mitochondrial fusion and fission in mammals. Annu. Rev. Cell Dev. Biol. 2006, 22, 79–99.[CrossRef] [PubMed]
50. Byrnes, L.J.; Sondermann, H. Structural basis for the nucleotide-dependent dimerization of the large g protein atlastin-1/spg3a. Proc. Natl. Acad. Sci. USA 2011, 108, 2216–2221. [CrossRef] [PubMed]
51. Bian, X.; Klemm, R.W.; Liu, T.Y.; Zhang, M.; Sun, S.; Sui, X.; Liu, X.; Rapoport, T.A.; Hu, J. Structures of the atlastin gtpase provide insight into homotypic fusion of endoplasmic reticulum membranes. Proc. Natl. Acad. Sci. USA 2011, 108, 3976–3981. [CrossRef] [PubMed]
52. English, A.R.; Voeltz, G.K. Endoplasmic reticulum structure and interconnections with other organelles. Cold Spring Harb. Perspect. Biol. 2013, 5, a013227. [CrossRef] [PubMed]
53. Gerondopoulos, A.; Bastos, R.N.; Yoshimura, S.; Anderson, R.; Carpanini, S.; Aligianis, I.; Handley, M.T.; Barr, F.A. Rab18 and a rab18 gef complex are required for normal ER structure. J. Cell Biol. 2014, 205, 707–720.[CrossRef] [PubMed]
54. Wagner, W.; Brenowitz, S.D.; Hammer, J.A., 3rd. Myosin-va transports the endoplasmic reticulum into the dendritic spines of purkinje neurons. Nat. Cell Biol. 2011, 13, 40–48. [CrossRef] [PubMed]
55. Schwarz, D.S.; Blower, M.D. The endoplasmic reticulum: Structure, function and response to cellular signaling. Cell. Mol. Life Sci. 2016, 73, 79–94. [CrossRef] [PubMed]
56. Friedman, J.R.; Lackner, L.L.; West, M.; DiBenedetto, J.R.; Nunnari, J.; Voeltz, G.K. ER tubules mark sites of mitochondrial division. Science 2011, 334, 358–362. [CrossRef] [PubMed]
57. Friedman, J.R.; Dibenedetto, J.R.; West, M.; Rowland, A.A.; Voeltz, G.K. Endoplasmic reticulum-endosome contact increases as endosomes traffic and mature. Mol. Biol. Cell 2013, 24, 1030–1040. [CrossRef] [PubMed]
58. Rowland, A.A.; Chitwood, P.J.; Phillips, M.J.; Voeltz, G.K. ER contact sites define the position and timing of endosome fission. Cell 2014, 159, 1027–1041. [CrossRef] [PubMed]
59. Shai, N.; Schuldiner, M.; Zalckvar, E. No peroxisome is an island—Peroxisome contact sites. Biochim. Biophys. Acta 2016, 1863, 1061–1069. [CrossRef] [PubMed]
60. Goodman, J.M. The gregarious lipid droplet. J. Biol. Chem. 2008, 283, 28005–28009. [CrossRef] [PubMed]
61. Murphy, S.; Martin, S.; Parton, R.G. Lipid droplet-organelle interactions; sharing the fats. Biochim. Biophys. Acta 2009, 1791, 441–447. [CrossRef] [PubMed]
62. Yla-Anttila, P.; Vihinen, H.; Jokitalo, E.; Eskelinen, E.L. 3D tomography reveals connections between the phagophore and endoplasmic reticulum. Autophagy 2009, 5, 1180–1185. [CrossRef] [PubMed]
63. Schneider, M.F. Control of calcium release in functioning skeletal muscle fibers. Annu. Rev. Physiol. 1994, 56, 463–484. [CrossRef] [PubMed]
64. Takeshima, H.; Komazaki, S.; Nishi, M.; Iino, M.; Kangawa, K. Junctophilins: A novel family of junctional membrane complex proteins. Mol. Cell 2000, 6, 11–22. [CrossRef]
65. Zhang, D.; Vjestica, A.; Oliferenko, S. Plasma membrane tethering of the cortical ER necessitates its finely reticulated architecture. Curr. Biol. 2012, 22, 2048–2052. [CrossRef] [PubMed]
66. Stefan, C.J.; Manford, A.G.; Emr, S.D. ER-PM connections: Sites of information transfer and inter-organelle communication. Curr. Opin. Cell Biol. 2013, 25, 434–442. [CrossRef] [PubMed]
67. Vance, J.E. Phospholipid synthesis and transport in mammalian cells. Traffic 2015, 16, 1–18. [CrossRef] [PubMed]
68. Puhka, M.; Vihinen, H.; Joensuu, M.; Jokitalo, E. Endoplasmic reticulum remains continuous and undergoes sheet-to-tubule transformation during cell division in mammalian cells. J. Cell Biol. 2007, 179, 895–909.[CrossRef] [PubMed]
69. Puhka, M.; Joensuu, M.; Vihinen, H.; Belevich, I.; Jokitalo, E. Progressive sheet-to-tubule transformation is a general mechanism for endoplasmic reticulum partitioning in dividing mammalian cells. Mol. Biol. Cell 2012, 23, 2424–2432. [CrossRef] [PubMed]
70. Baumann, O.; Walz, B. Endoplasmic reticulum of animal cells and its organization into structural and functional domains. Int. Rev. Cytol. 2001, 205, 149–214. [PubMed]
71. Husain, M.; Weisberg, A.S.; Moss, B. Existence of an operative pathway from the endoplasmic reticulum to the immature poxvirus membrane. Proc. Natl. Acad. Sci. USA 2006, 103, 19506–19511. [CrossRef] [PubMed]
72. Chlanda, P.; Carbajal, M.A.; Cyrklaff, M.; Griffiths, G.; Krijnse-Locker, J. Membrane rupture generates single open membrane sheets during vaccinia virus assembly. Cell Host Microbe 2009, 6, 81–90. [CrossRef] [PubMed]
73. Maruri-Avidal, L.; Weisberg, A.S.; Bisht, H.; Moss, B. Analysis of viral membranes formed in cells infected by a vaccinia virus l2-deletion mutant suggests their origin from the endoplasmic reticulum. J. Virol. 2013, 87, 1861–1871. [CrossRef] [PubMed]
74. Maruri-Avidal, L.; Weisberg, A.S.; Moss, B. Association of the vaccinia virus A11 protein with the endoplasmic reticulum and crescent precursors of immature virions. J. Virol. 2013, 87, 10195–10206.[CrossRef] [PubMed]
75. Maruri-Avidal, L.; Weisberg, A.S.; Moss, B. Direct formation of vaccinia virus membranes from the endoplasmic reticulum in the absence of the newly characterized l2-interacting protein a30.5. J. Virol. 2013, 87, 12313–12326. [CrossRef] [PubMed]
76. Mutsafi, Y.; Shimoni, E.; Shimon, A.; Minsky, A. Membrane assembly during the infection cycle of the giant mimivirus. PLoS Pathog. 2013, 9, e1003367. [CrossRef] [PubMed]
77. Suarez, C.; Andres, G.; Kolovou, A.; Hoppe, S.; Salas, M.L.; Walther, P.; Krijnse Locker, J. African swine fever virus assembles a single membrane derived from rupture of the endoplasmic reticulum. Cell. Microbiol. 2015, 17, 1683–1698. [CrossRef] [PubMed]
78. Liu, Y.; Tran, B.N.; Wang, F.; Ounjai, P.; Wu, J.; Hew, C.L. Visualization of assembly intermediates and budding vacuoles of singapore grouper iridovirus in grouper embryonic cells. Sci. Rep. 2016, 6, 18696.[CrossRef] [PubMed]
79. Milrot, E.; Mutsafi, Y.; Fridmann-Sirkis, Y.; Shimoni, E.; Rechav, K.; Gurnon, J.R.; van Etten, J.L.; Minsky, A. Virus-host interactions: Insights from the replication cycle of the large paramecium bursaria chlorella virus. Cell. Microbiol. 2016, 18, 3–16. [CrossRef] [PubMed]
80. Fernandez de Castro, I.; Zamora, P.F.; Ooms, L.; Fernandez, J.J.; Lai, C.M.; Mainou, B.A.; Dermody, T.S.; Risco, C. Reovirus forms neo-organelles for progeny particle assembly within reorganized cell membranes. MBIO 2014, 5, e00931–e00913. [CrossRef] [PubMed]
81. Kim, K.S. An ultrastructural study of inclusions and disease development in plant cells infected by cowpea chlorotic mottle virus. J. Gen. Virol. 1977, 35, 535–543. [CrossRef]
82. Restrepo-Hartwig, M.A.; Ahlquist, P. Brome mosaic virus helicase- and polymerase-like proteins colocalize on the endoplasmic reticulum at sites of viral RNA synthesis. J. Virol. 1996, 70, 8908–8916. [PubMed]
83. Schwartz, M.; Chen, J.; Janda, M.; Sullivan, M.; den Boon, J.; Ahlquist, P. A positive-strand RNA virus replication complex parallels form and function of retrovirus capsids. Mol. Cell 2002, 9, 505–514. [CrossRef]
84. Turner, K.A.; Sit, T.L.; Callaway, A.S.; Allen, N.S.; Lommel, S.A. Red clover necrotic mosaic virus replication proteins accumulate at the endoplasmic reticulum. Virology 2004, 320, 276–290. [CrossRef] [PubMed]
85. Cao, X.; Jin, X.; Zhang, X.; Li, Y.; Wang, C.; Wang, X.; Hong, J.; Wang, X.; Li, D.; Zhang, Y. Morphogenesis of endoplasmic reticulum membrane-invaginated vesicles during beet black scorch virus infection: Role of auxiliary replication protein and new implications of three-dimensional architecture. J. Virol. 2015, 89, 6184–6195. [CrossRef] [PubMed]
86. McGavran, M.H.; White, J.D. Electron microscopic and immunofluorescent observations on monkey liver and tissue culture cells infected with the asibi strain of yellow fever virus. Am. J. Pathol. 1964, 45, 501–517.[PubMed]
87. Mackenzie, J.M.; Westaway, E.G. Assembly and maturation of the flavivirus kunjin virus appear to occur in the rough endoplasmic reticulum and along the secretory pathway, respectively. J. Virol. 2001, 75, 10787–10799. [CrossRef] [PubMed]
88. Gillespie, L.K.; Hoenen, A.; Morgan, G.; Mackenzie, J.M. The endoplasmic reticulum provides the membrane platform for biogenesis of the flavivirus replication complex. J. Virol. 2010, 84, 10438–10447. [CrossRef] [PubMed]
89. Hase, T.; Summers, P.L.; Dubois, D.R. Ultrastructural changes of mouse brain neurons infected with japanese encephalitis virus. Int. J. Exp. Pathol. 1990, 71, 493–505. [PubMed]
90. Mackenzie, J.M.; Jones, M.K.; Young, P.R. Improved membrane preservation of flavivirus-infected cells with cryosectioning. J. Virol. Methods 1996, 56, 67–75. [CrossRef]
91. Grief, C.; Galler, R.; Cortes, L.M.; Barth, O.M. Intracellular localisation of dengue-2 RNA in mosquito cell culture using electron microscopic in situ hybridisation. Arch. Virol. 1997, 142, 2347–2357. [CrossRef] [PubMed]
92. Welsch, S.; Miller, S.; Romero-Brey, I.; Merz, A.; Bleck, C.K.; Walther, P.; Fuller, S.D.; Antony, C.; Krijnse-Locker, J.; Bartenschlager, R. Composition and three-dimensional architecture of the dengue virus replication and assembly sites. Cell Host Microbe 2009, 5, 365–375. [CrossRef] [PubMed]
93. Matthews, V.; Robertson, T.; Kendrick, T.; Abdo, M.; Papadimitriou, J.; McMinn, P. Morphological features of murray valley encephalitis virus infection in the central nervous system of swiss mice. Int. J. Exp. Pathol. 2000, 81, 31–40. [CrossRef] [PubMed]
94. Overby, A.K.; Popov, V.L.; Niedrig, M.; Weber, F. Tick-borne encephalitis virus delays interferon induction and hides its double-stranded RNA in intracellular membrane vesicles. J. Virol. 2010, 84, 8470–8483.[CrossRef] [PubMed]
95. Miorin, L.; Romero-Brey, I.; Maiuri, P.; Hoppe, S.; Krijnse-Locker, J.; Bartenschlager, R.; Marcello, A. Three-dimensional architecture of tick-borne encephalitis virus replication sites and trafficking of the replicated RNA. J. Virol. 2013, 87, 6469–6481. [CrossRef] [PubMed]
96. Offerdahl, D.K.; Dorward, D.W.; Hansen, B.T.; Bloom, M.E. A three-dimensional comparison of tick-borne flavivirus infection in mammalian and tick cell lines. PLoS ONE 2012, 7, e47912. [CrossRef] [PubMed]
97. Bienz, K.; Egger, D.; Pasamontes, L. Association of polioviral proteins of the P2 genomic region with the viral replication complex and virus-induced membrane synthesis as visualized by electron microscopic immunocytochemistry and autoradiography. Virology 1987, 160, 220–226. [CrossRef]
98. Schlegel, A.; Giddings, T.H., Jr.; Ladinsky, M.S.; Kirkegaard, K. Cellular origin and ultrastructure of membranes induced during poliovirus infection. J. Virol. 1996, 70, 6576–6588. [PubMed]
99. Suhy, D.A.; Giddings, T.H., Jr.; Kirkegaard, K. Remodeling the endoplasmic reticulum by poliovirus infection and by individual viral proteins: An autophagy-like origin for virus-induced vesicles. J. Virol. 2000, 74, 8953–8965. [CrossRef] [PubMed]
100. Pedersen, K.W.; van der Meer, Y.; Roos, N.; Snijder, E.J. Open reading frame 1A-encoded subunits of the arterivirus replicase induce endoplasmic reticulum-derived double-membrane vesicles which carry the viral replication complex. J. Virol. 1999, 73, 2016–2026. [PubMed]
101. Knoops, K.; Barcena, M.; Limpens, R.W.; Koster, A.J.; Mommaas, A.M.; Snijder, E.J. Ultrastructural characterization of arterivirus replication structures: Reshaping the endoplasmic reticulum to accommodate viral RNA synthesis. J. Virol. 2012, 86, 2474–2487. [CrossRef] [PubMed]
102. Snijder, E.J.; van der Meer, Y.; Zevenhoven-Dobbe, J.; Onderwater, J.J.; van der Meulen, J.; Koerten, H.K.; Mommaas, A.M. Ultrastructure and origin of membrane vesicles associated with the severe acute respiratory syndrome coronavirus replication complex. J. Virol. 2006, 80, 5927–5940. [CrossRef] [PubMed]
103. Knoops, K.; Kikkert, M.; Worm, S.H.; Zevenhoven-Dobbe, J.C.; van der Meer, Y.; Koster, A.J.; Mommaas, A.M.; Snijder, E.J. Sars-coronavirus replication is supported by a reticulovesicular network of modified endoplasmic reticulum. PLoS Biol. 2008, 6, e226. [CrossRef] [PubMed]
104. Ferraris, P.; Blanchard, E.; Roingeard, P. Ultrastructural and biochemical analyses of hepatitis C virus-associated host cell membranes. J. Gen. Virol. 2010, 91, 2230–2237. [CrossRef] [PubMed]
105. Romero-Brey, I.; Merz, A.; Chiramel, A.; Lee, J.Y.; Chlanda, P.; Haselman, U.; Santarella-Mellwig, R.; Habermann, A.; Hoppe, S.; Kallis, S.; et al. Three-dimensional architecture and biogenesis of membrane structures associated with hepatitis C virus replication. PLoS Pathog. 2012, 8, e1003056. [CrossRef] [PubMed]
106. Ferraris, P.; Beaumont, E.; Uzbekov, R.; Brand, D.; Gaillard, J.; Blanchard, E.; Roingeard, P. Sequential biogenesis of host cell membrane rearrangements induced by hepatitis C virus infection. Cell. Mol. Life Sci. 2013, 70, 1297–1306. [CrossRef] [PubMed]
107. Maier, H.J.; Hawes, P.C.; Cottam, E.M.; Mantell, J.; Verkade, P.; Monaghan, P.; Wileman, T.; Britton, P. Infectious bronchitis virus generates spherules from zippered endoplasmic reticulum membranes. MBIO 2013, 4, e00801–e00813. [CrossRef] [PubMed]
108. Mettenleiter, T.C. Breaching the barrier-the nuclear envelope in virus infection. J. Mol. Biol. 2015, 10, 1949–1961. [CrossRef] [PubMed]
109. Hennig, T.; O’Hare, P. Viruses and the nuclear envelope. Curr. Opin. Cell Biol. 2015, 34, 113–121. [CrossRef] [PubMed]
110. Fay, N.; Pante, N. Nuclear entry of DNA viruses. Front. Microbiol. 2015, 6, 467. [CrossRef] [PubMed]
111. Fay, N.; Pante, N. Old foes, new understandings: Nuclear entry of small non-enveloped DNA viruses. Curr. Opin. Virol. 2015, 12, 59–65. [CrossRef] [PubMed]
112. Flatt, J.W.; Greber, U.F. Misdelivery at the nuclear pore complex-stopping a virus dead in its tracks. Cells 2015, 4, 277–296. [CrossRef] [PubMed]
113. Au, S.; Pante, N. Nuclear transport of baculovirus: Revealing the nuclear pore complex passage. J. Struct. Biol. 2012, 177, 90–98. [CrossRef] [PubMed]
114. Strunze, S.; Engelke, M.F.; Wang, I.H.; Puntener, D.; Boucke, K.; Schleich, S.; Way, M.; Schoenenberger, P.; Burckhardt, C.J.; Greber, U.F. Kinesin-1-mediated capsid disassembly and disruption of the nuclear pore complex promote virus infection. Cell Host Microbe 2011, 10, 210–223. [CrossRef] [PubMed]
115. Cohen, S.; Behzad, A.R.; Carroll, J.B.; Pante, N. Parvoviral nuclear import: Bypassing the host nuclear-transport machinery. J. Gen. Virol. 2006, 87, 3209–3213. [CrossRef] [PubMed]
116. Cohen, S.; Marr, A.K.; Garcin, P.; Pante, N. Nuclear envelope disruption involving host caspases plays a role in the parvovirus replication cycle. J. Virol. 2011, 85, 4863–4874. [CrossRef] [PubMed]
117. Goff, S.P. Host factors exploited by retroviruses. Nat. Rev. Microbiol. 2007, 5, 253–263. [CrossRef] [PubMed]
118. Aydin, I.; Weber, S.; Snijder, B.; Samperio Ventayol, P.; Kuhbacher, A.; Becker, M.; Day, P.M.; Schiller, J.T.; Kann, M.; Pelkmans, L.; et al. Large scale RNAi reveals the requirement of nuclear envelope breakdown for nuclear import of human papillomaviruses. PLoS Pathog. 2014, 10, e1004162. [CrossRef] [PubMed]
119. Butin-Israeli, V.; Ben-nun-Shaul, O.; Kopatz, I.; Adam, S.A.; Shimi, T.; Goldman, R.D.; Oppenheim, A. Simian virus 40 induces lamin A/C fluctuations and nuclear envelope deformation during cell entry. Nucleus 2011, 2, 320–330. [CrossRef] [PubMed]
120. Skepper, J.N.; Whiteley, A.; Browne, H.; Minson, A. Herpes simplex virus nucleocapsids mature to progeny virions by an envelopment –> deenvelopment –> reenvelopment pathway. J. Virol. 2001, 75, 5697–5702.[CrossRef] [PubMed]
121. Baines, J.D.; Hsieh, C.E.; Wills, E.; Mannella, C.; Marko, M. Electron tomography of nascent herpes simplex virus virions. J. Virol. 2007, 81, 2726–2735. [CrossRef] [PubMed]
122. Peng, L.; Ryazantsev, S.; Sun, R.; Zhou, Z.H. Three-dimensional visualization of gammaherpesvirus life cycle in host cells by electron tomography. Structure 2010, 18, 47–58. [CrossRef] [PubMed]
123. Hagen, C.; Dent, K.C.; Zeev-Ben-Mordehai, T.; Grange, M.; Bosse, J.B.; Whittle, C.; Klupp, B.G.; Siebert, C.A.; Vasishtan, D.; Bauerlein, F.J.; et al. Structural basis of vesicle formation at the inner nuclear membrane. Cell 2015, 163, 1692–1701. [CrossRef] [PubMed]
124. Johnson, D.C.; Baines, J.D. Herpesviruses remodel host membranes for virus egress. Nat. Rev. Microbiol. 2011, 9, 382–394. [CrossRef] [PubMed]
125. Mettenleiter, T.C.; Muller, F.; Granzow, H.; Klupp, B.G. The way out: What we know and do not know about herpesvirus nuclear egress. Cell. Microbiol. 2013, 15, 170–178. [CrossRef] [PubMed]
126. Williams, G.V.; Faulkner, P. Cytological changes and viral morphogenesis during baculovirus infection. In The Baculoviruses; Miller, L.K., Ed.; Plenum Press, Inc.: New York, NY, USA, 1997; pp. 61–107.
127. Shen, H.; Chen, K. Bm61 of bombyx mori nucleopolyhedrovirus: Its involvement in the egress of nucleocapsids from the nucleus. FEBS Lett. 2012, 586, 990–995. [CrossRef] [PubMed]
128. Yuan, M.; Huang, Z.; Wei, D.; Hu, Z.; Yang, K.; Pang, Y. Identification of autographa californica nucleopolyhedrovirus ac93 as a core gene and its requirement for intranuclear microvesicle formation and nuclear egress of nucleocapsids. J. Virol. 2011, 85, 11664–11674. [CrossRef] [PubMed]
129. Raghava, S.; Giorda, K.M.; Romano, F.B.; Heuck, A.P.; Hebert, D.N. Sv40 late protein VP4 forms toroidal pores to disrupt membranes for viral release. Biochemistry 2013, 52, 3939–3948. [CrossRef] [PubMed]
130. McIntosh, P.B.; Laskey, P.; Sullivan, K.; Davy, C.; Wang, Q.; Jackson, D.J.; Griffin, H.M.; Doorbar, J. E1-e4-mediated keratin phosphorylation and ubiquitylation: A mechanism for keratin depletion in HPV16-infected epithelium. J. Cell Sci. 2010, 123, 2810–2822. [CrossRef] [PubMed]
131. Wang, Q.; Griffin, H.; Southern, S.; Jackson, D.; Martin, A.; McIntosh, P.; Davy, C.; Masterson, P.J.; Walker, P.A.; Laskey, P.; et al. Functional analysis of the human papillomavirus type 16 E1ˆE4 protein provides a mechanism for in vivo and in vitro keratin filament reorganization. J. Virol. 2004, 78, 821–833. [CrossRef] [PubMed]
132. Iyer, L.M.; Balaji, S.; Koonin, E.V.; Aravind, L. Evolutionary genomics of nucleo-cytoplasmic large DNA viruses. Virus Res. 2006, 117, 156–184. [CrossRef] [PubMed]
133. Dales, S.; Mosbach, E.H. Vaccinia as a model for membrane biogenesis. Virology 1968, 35, 564–583. [CrossRef]
134. Risco, C.; Rodriguez, J.R.; Lopez-Iglesias, C.; Carrascosa, J.L.; Esteban, M.; Rodriguez, D. Endoplasmic reticulum-golgi intermediate compartment membranes and vimentin filaments participate in vaccinia virus assembly. J. Virol. 2002, 76, 1839–1855. [CrossRef] [PubMed]
135. Sodeik, B.; Doms, R.W.; Ericsson, M.; Hiller, G.; Machamer, C.E.; van ’t Hof, W.; van Meer, G.; Moss, B.; Griffiths, G. Assembly of vaccinia virus: Role of the intermediate compartment between the endoplasmic reticulum and the Golgi stacks. J. Cell Biol. 1993, 121, 521–541. [CrossRef] [PubMed]
136. Alzhanova, D.; Hruby, D.E. A trans-golgi network resident protein, Golgin-97, accumulates in viral factories and incorporates into virions during poxvirus infection. J. Virol. 2006, 80, 11520–11527. [CrossRef] [PubMed]
137. Sodeik, B.; Krijnse-Locker, J. Assembly of vaccinia virus revisited: De novo membrane synthesis or acquisition from the host? Trends Microbiol. 2002, 10, 15–24. [CrossRef]
138. Moss, B. Poxvirus membrane biogenesis. Virology 2015, 479–480, 619–626. [CrossRef] [PubMed]
139. Tolonen, N.; Doglio, L.; Schleich, S.; Krijnse Locker, J. Vaccinia virus DNA replication occurs in endoplasmic reticulum-enclosed cytoplasmic mini-nuclei. Mol. Biol. Cell 2001, 12, 2031–2046. [CrossRef] [PubMed]
140. Chinchar, V.G.; Yu, K.H.; Jancovich, J.K. The molecular biology of frog virus 3 and other iridoviruses infecting cold-blooded vertebrates. Viruses 2011, 3, 1959–1985. [CrossRef] [PubMed]
141. Ma, J.; Zeng, L.; Zhou, Y.; Jiang, N.; Zhang, H.; Fan, Y.; Meng, Y.; Xu, J. Ultrastructural morphogenesis of an amphibian iridovirus isolated from chinese giant salamander (andrias davidianus). J. Comp. Pathol. 2014, 150, 325–331. [CrossRef] [PubMed]
142. Garcia-Beato, R.; Salas, M.L.; Vinuela, E.; Salas, J. Role of the host cell nucleus in the replication of african swine fever virus DNA. Virology 1992, 188, 637–649. [CrossRef]
143. Meints, R.H.; Lee, K.; van Etten, J.L. Assembly site of the virus PBCV-1 in a chlorella-like green alga: Ultrastructural studies. Virology 1986, 154, 240–245. [CrossRef]
144. Van Etten, J.L. Unusual life style of giant chlorella viruses. Annu. Rev. Genet. 2003, 37, 153–195. [CrossRef] [PubMed]
145. Yamada, T.; Onimatsu, H.; van Etten, J.L. Chlorella viruses. Adv. Virus Res. 2006, 66, 293–336. [PubMed]
146. Romero-Brey, I.; Bartenschlager, R. Membranous replication factories induced by plus-strand RNA viruses. Viruses 2014, 6, 2826–2857. [CrossRef] [PubMed]
147. Mackenzie, J.M.; Jones, M.K.; Young, P.R. Immunolocalization of the dengue virus nonstructural glycoprotein NS1 suggests a role in viral RNA replication. Virology 1996, 220, 232–240. [CrossRef] [PubMed]
148. Hase, T.; Summers, P.L.; Ray, P. Entry and replication of japanese encephalitis virus in cultured neurogenic cells. J. Virol. Methods 1990, 30, 205–214. [CrossRef]
149. Murphy, F.A.; Harrison, A.K.; Gary, G.W., Jr.; Whitfield, S.G.; Forrester, F.T. St. Louis encephalitis virus infection in mice. Electron microscopic studies of central nervous system. Lab. Investig. 1968, 19, 652–662.[PubMed]
150. Lee, W.M.; Ahlquist, P. Membrane synthesis, specific lipid requirements, and localized lipid composition changes associated with a positive-strand RNA virus RNA replication protein. J. Virol. 2003, 77, 12819–12828.[CrossRef] [PubMed]
151. Westaway, E.G.; Mackenzie, J.M.; Kenney, M.T.; Jones, M.K.; Khromykh, A.A. Ultrastructure of kunjin virus-infected cells: Colocalization of NS1 and NS3 with double-stranded RNA, and of NS2B with NS3, in virus-induced membrane structures. J. Virol. 1997, 71, 6650–6661. [PubMed]
152. Junjhon, J.; Pennington, J.G.; Edwards, T.J.; Perera, R.; Lanman, J.; Kuhn, R.J. Ultrastructural characterization and three-dimensional architecture of replication sites in dengue virus-infected mosquito cells. J. Virol. 2014, 88, 4687–4697. [CrossRef] [PubMed]
153. Chasey, D.; Roeder, P.L. Virus-like particles in bovine turbinate cells infected with bovine virus diarrhoea/mucosal disease virus. Arch. Virol. 1981, 67, 325–332. [CrossRef] [PubMed]
154. Gray, E.W.; Nettleton, P.F. The ultrastructure of cell cultures infected with border disease and bovine virus diarrhoea viruses. J. Gen. Virol. 1987, 68, 2339–2346. [CrossRef] [PubMed]
155. Kubovicova, E.; Makarevich, A.V.; Pivko, J.; Chrenek, P.; Grafenau, P.; Riha, L.; Sirotkin, A.V.; Louda, F. Alteration in ultrastructural morphology of bovine embryos following subzonal microinjection of bovine viral diarrhea virus (bvdv). Zygote 2008, 16, 187–193. [CrossRef] [PubMed]
156. Birk, A.V.; Dubovi, E.J.; Cohen-Gould, L.; Donis, R.; Szeto, H.H. Cytoplasmic vacuolization responses to cytopathic bovine viral diarrhoea virus. Virus Res. 2008, 132, 76–85. [CrossRef] [PubMed]
157. Schmeiser, S.; Mast, J.; Thiel, H.J.; Konig, M. Morphogenesis of pestiviruses: New insights from ultrastructural studies of strain giraffe-1. J. Virol. 2014, 88, 2717–2724. [CrossRef] [PubMed]
158. Weiskircher, E.; Aligo, J.; Ning, G.; Konan, K.V. Bovine viral diarrhea virus ns4b protein is an integral membrane protein associated with Golgi markers and rearranged host membranes. Virol. J. 2009, 6, 185.[CrossRef] [PubMed]
159. Kopek, B.G.; Perkins, G.; Miller, D.J.; Ellisman, M.H.; Ahlquist, P. Three-dimensional analysis of a viral RNA replication complex reveals a virus-induced mini-organelle. PLoS Biol. 2007, 5, e220. [CrossRef] [PubMed]
160. Weber-Lotfi, F.; Dietrich, A.; Russo, M.; Rubino, L. Mitochondrial targeting and membrane anchoring of a viral replicase in plant and yeast cells. J. Virol. 2002, 76, 10485–10496. [CrossRef] [PubMed]
161. Magliano, D.; Marshall, J.A.; Bowden, D.S.; Vardaxis, N.; Meanger, J.; Lee, J.Y. Rubella virus replication complexes are virus-modified lysosomes. Virology 1998, 240, 57–63. [CrossRef] [PubMed]
162. Fontana, J.; Lopez-Iglesias, C.; Tzeng, W.P.; Frey, T.K.; Fernandez, J.J.; Risco, C. Three-dimensional structure of rubella virus factories. Virology 2010, 405, 579–591. [CrossRef] [PubMed]
163. Hrsel, I.; Brcak, J. Ultrastructural changes in chloroplasts and cytoplasm caused by local infection of tobacco with tobacco mosaic virus and cucumber virus 4. Virology 1964, 23, 252–258. [CrossRef]
164. Panavas, T.; Hawkins, C.M.; Panaviene, Z.; Nagy, P.D. The role of the p33:P33/p92 interaction domain in RNA replication and intracellular localization of p33 and p92 proteins of cucumber necrosis tombusvirus. Virology 2005, 338, 81–95. [CrossRef] [PubMed]
165. Jonczyk, M.; Pathak, K.B.; Sharma, M.; Nagy, P.D. Exploiting alternative subcellular location for replication: Tombusvirus replication switches to the endoplasmic reticulum in the absence of peroxisomes. Virology 2007, 362, 320–330. [CrossRef] [PubMed]
166. Wei, T.; Huang, T.S.; McNeil, J.; Laliberte, J.F.; Hong, J.; Nelson, R.S.; Wang, A. Sequential recruitment of the endoplasmic reticulum and chloroplasts for plant potyvirus replication. J. Virol. 2010, 84, 799–809. [CrossRef] [PubMed]
167. Kallman, F.; Williams, R.C.; Dulbecco, R.; Vogt, M. Fine structure of changes produced in cultured cells sampled at specified intervals during a single growth cycle of polio virus. J. Biophys. Biochem. Cytol. 1958, 4, 301–308. [CrossRef] [PubMed]
168. Egger, D.; Bienz, K. Intracellular location and translocation of silent and active poliovirus replication complexes. J. Gen. Virol. 2005, 86, 707–718. [CrossRef] [PubMed]
169. Belov, G.A.; Nair, V.; Hansen, B.T.; Hoyt, F.H.; Fischer, E.R.; Ehrenfeld, E. Complex dynamic development of poliovirus membranous replication complexes. J. Virol. 2012, 86, 302–312. [CrossRef] [PubMed]
170. Limpens, R.W.; van der Schaar, H.M.; Kumar, D.; Koster, A.J.; Snijder, E.J.; van Kuppeveld, F.J.; Barcena, M. The transformation of enterovirus replication structures: A three-dimensional study of single- and double-membrane compartments. MBIO 2011, 2, e00166–e00111. [CrossRef] [PubMed]
171. Monaghan, P.; Cook, H.; Jackson, T.; Ryan, M.; Wileman, T. The ultrastructure of the developing replication site in foot-and-mouth disease virus-infected bhk-38 cells. J. Gen. Virol. 2004, 85, 933–946. [CrossRef] [PubMed]
172. Bienz, K.; Egger, D.; Rasser, Y.; Bossart, W. Intracellular distribution of poliovirus proteins and the induction of virus-specific cytoplasmic structures. Virology 1983, 131, 39–48. [CrossRef]
173. Hsu, N.Y.; Ilnytska, O.; Belov, G.; Santiana, M.; Chen, Y.H.; Takvorian, P.M.; Pau, C.; van der Schaar, H.; Kaushik-Basu, N.; Balla, T.; et al. Viral reorganization of the secretory pathway generates distinct organelles for RNA replication. Cell 2010, 141, 799–811. [CrossRef] [PubMed]
174. Rust, R.C.; Landmann, L.; Gosert, R.; Tang, B.L.; Hong, W.; Hauri, H.P.; Egger, D.; Bienz, K. Cellular COPII proteins are involved in production of the vesicles that form the poliovirus replication complex. J. Virol. 2001, 75, 9808–9818. [CrossRef] [PubMed]
175. Doedens, J.R.; Kirkegaard, K. Inhibition of cellular protein secretion by poliovirus proteins 2B and 3A. EMBO J. 1995, 14, 894–907. [PubMed]
176. Wessels, E.; Duijsings, D.; Notebaart, R.A.; Melchers, W.J.; van Kuppeveld, F.J. A proline-rich region in the coxsackievirus 3A protein is required for the protein to inhibit endoplasmic reticulum-to-Golgi transport. J. Virol. 2005, 79, 5163–5173. [CrossRef] [PubMed]
177. Irurzun, A.; Perez, L.; Carrasco, L. Involvement of membrane traffic in the replication of poliovirus genomes: Effects of brefeldin a. Virology 1992, 191, 166–175. [CrossRef]
178. Maynell, L.A.; Kirkegaard, K.; Klymkowsky, M.W. Inhibition of poliovirus RNA synthesis by brefeldin a. J. Virol. 1992, 66, 1985–1994. [PubMed]
179. Trahey, M.; Oh, H.S.; Cameron, C.E.; Hay, J.C. Poliovirus infection transiently increases COPII vesicle budding. J. Virol. 2012, 86, 9675–9682. [CrossRef] [PubMed]
180. Gazina, E.V.; Mackenzie, J.M.; Gorrell, R.J.; Anderson, D.A. Differential requirements for copi coats in formation of replication complexes among three genera of picornaviridae. J. Virol. 2002, 76, 11113–11122.[CrossRef] [PubMed]
181. Belov, G.A.; Altan-Bonnet, N.; Kovtunovych, G.; Jackson, C.L.; Lippincott-Schwartz, J.; Ehrenfeld, E. Hijacking components of the cellular secretory pathway for replication of poliovirus RNA. J. Virol. 2007, 81, 558–567. [CrossRef] [PubMed]
182. Belov, G.A.; Feng, Q.; Nikovics, K.; Jackson, C.L.; Ehrenfeld, E. A critical role of a cellular membrane traffic protein in poliovirus RNA replication. PLoS Pathog. 2008, 4, e1000216. [CrossRef] [PubMed]
183. Belov, G.A.; Habbersett, C.; Franco, D.; Ehrenfeld, E. Activation of cellular arf GTPases by poliovirus protein 3cd correlates with virus replication. J. Virol. 2007, 81, 9259–9267. [CrossRef] [PubMed]
184. Midgley, R.; Moffat, K.; Berryman, S.; Hawes, P.; Simpson, J.; Fullen, D.; Stephens, D.J.; Burman, A.; Jackson, T. A role for endoplasmic reticulum exit sites in foot-and-mouth disease virus infection. J. Gen. Virol. 2013, 94, 2636–2646. [CrossRef] [PubMed]
185. Gosert, R.; Kanjanahaluethai, A.; Egger, D.; Bienz, K.; Baker, S.C. RNA replication of mouse hepatitis virus takes place at double-membrane vesicles. J. Virol. 2002, 76, 3697–3708. [CrossRef] [PubMed]
186. Ulasli, M.; Verheije, M.H.; de Haan, C.A.; Reggiori, F. Qualitative and quantitative ultrastructural analysis of the membrane rearrangements induced by coronavirus. Cell. Microbiol. 2010, 12, 844–861. [CrossRef] [PubMed]
187. De Wilde, A.H.; Raj, V.S.; Oudshoorn, D.; Bestebroer, T.M.; van Nieuwkoop, S.; Limpens, R.W.; Posthuma, C.C.; van der Meer, Y.; Barcena, M.; Haagmans, B.L.; et al. MERS-coronavirus replication induces severe in vitro cytopathology and is strongly inhibited by cyclosporin A or interferon-alpha treatment. J. Gen. Virol. 2013, 94, 1749–1760. [CrossRef] [PubMed]
188. Paul, D.; Hoppe, S.; Saher, G.; Krijnse-Locker, J.; Bartenschlager, R. Morphological and biochemical characterization of the membranous hepatitis C virus replication compartment. J. Virol. 2013, 87, 10612–10627.[CrossRef] [PubMed]
189. Maier, H.J.; Hawes, P.C.; Keep, S.M.; Britton, P. Spherules and ibv. Bioengineered 2014, 5, 288–292. [CrossRef] [PubMed]
190. Westaway, E.G.; Khromykh, A.A.; Kenney, M.T.; Mackenzie, J.M.; Jones, M.K. Proteins C and NS4B of the flavivirus kunjin translocate independently into the nucleus. Virology 1997, 234, 31–41. [CrossRef] [PubMed]
191. Roosendaal, J.; Westaway, E.G.; Khromykh, A.; Mackenzie, J.M. Regulated cleavages at the west nile virus NS4A-2k-NS4B junctions play a major role in rearranging cytoplasmic membranes and Golgi trafficking of the NS4A protein. J. Virol. 2006, 80, 4623–4632. [CrossRef] [PubMed]
192. Miller, S.; Kastner, S.; Krijnse-Locker, J.; Buhler, S.; Bartenschlager, R. The non-structural protein 4A of dengue virus is an integral membrane protein inducing membrane alterations in a 2K-regulated manner. J. Biol. Chem. 2007, 282, 8873–8882. [CrossRef] [PubMed]
193. Rawson, R.B. The srebp pathway—Insights from insigs and insects. Nat. Rev. Mol. Cell Biol. 2003, 4, 631–640.[CrossRef] [PubMed]
194. Eichwald, C.; Arnoldi, F.; Laimbacher, A.S.; Schraner, E.M.; Fraefel, C.; Wild, P.; Burrone, O.R.; Ackermann, M. Rotavirus viroplasm fusion and perinuclear localization are dynamic processes requiring stabilized microtubules. PLoS ONE 2012, 7, e47947. [CrossRef] [PubMed]
195. Poruchynsky, M.S.; Maass, D.R.; Atkinson, P.H. Calcium depletion blocks the maturation of rotavirus by altering the oligomerization of virus-encoded proteins in the er. J. Cell Biol. 1991, 114, 651–656. [CrossRef] [PubMed]
196. Diaz, A.; Ahlquist, P. Role of host reticulon proteins in rearranging membranes for positive-strand RNA virus replication. Curr. Opin. Microbiol. 2012, 15, 519–524. [CrossRef] [PubMed]
197. Diaz, A.; Wang, X.; Ahlquist, P. Membrane-shaping host reticulon proteins play crucial roles in viral RNA replication compartment formation and function. Proc. Natl. Acad. Sci. USA 2010, 107, 16291–16296.[CrossRef] [PubMed]
198. Tang, W.F.; Yang, S.Y.; Wu, B.W.; Jheng, J.R.; Chen, Y.L.; Shih, C.H.; Lin, K.H.; Lai, H.C.; Tang, P.; Horng, J.T. Reticulon 3 binds the 2C protein of enterovirus 71 and is required for viral replication. J. Biol. Chem. 2007, 282, 5888–5898. [CrossRef] [PubMed]
199. Wu, M.J.; Ke, P.Y.; Hsu, J.T.; Yeh, C.T.; Horng, J.T. Reticulon 3 interacts with NS4B of the hepatitis C virus and negatively regulates viral replication by disrupting NS4B self-interaction. Cell. Microbiol. 2014, 16, 1603–1618.[CrossRef] [PubMed]
200. Ozeki, S.; Cheng, J.; Tauchi-Sato, K.; Hatano, N.; Taniguchi, H.; Fujimoto, T. Rab18 localizes to lipid droplets and induces their close apposition to the endoplasmic reticulum-derived membrane. J. Cell Sci. 2005, 118, 2601–2611. [CrossRef] [PubMed]
201. Martin, S.; Driessen, K.; Nixon, S.J.; Zerial, M.; Parton, R.G. Regulated localization of rab18 to lipid droplets: Effects of lipolytic stimulation and inhibition of lipid droplet catabolism. J. Biol. Chem. 2005, 280, 42325–42335. [CrossRef] [PubMed]
202. Salloum, S.; Wang, H.; Ferguson, C.; Parton, R.G.; Tai, A.W. Rab18 binds to hepatitis C virus NS5A and promotes interaction between sites of viral replication and lipid droplets. PLoS Pathog. 2013, 9, e1003513. [CrossRef] [PubMed]
203. Miyanari, Y.; Atsuzawa, K.; Usuda, N.; Watashi, K.; Hishiki, T.; Zayas, M.; Bartenschlager, R.; Wakita, T.; Hijikata, M.; Shimotohno, K. The lipid droplet is an important organelle for hepatitis C virus production. Nat. Cell Biol. 2007, 9, 1089–1097. [CrossRef] [PubMed]
204. Dansako, H.; Hiramoto, H.; Ikeda, M.; Wakita, T.; Kato, N. Rab18 is required for viral assembly of hepatitis C virus through trafficking of the core protein to lipid droplets. Virology 2014, 462, 166–174. [CrossRef] [PubMed]
205. Tang, W.C.; Lin, R.J.; Liao, C.L.; Lin, Y.L. Rab18 facilitates dengue virus infection by targeting fatty acid synthase to sites of viral replication. J. Virol. 2014, 88, 6793–6804. [CrossRef] [PubMed]
206. Barajas, D.; Xu, K.; de Castro Martin, I.F.; Sasvari, Z.; Brandizzi, F.; Risco, C.; Nagy, P.D. Co-opted oxysterol-binding ORP and VAP proteins channel sterols to RNA virus replication sites via membrane contact sites. PLoS Pathog. 2014, 10, e1004388. [CrossRef] [PubMed]
207. Roulin, P.S.; Lotzerich, M.; Torta, F.; Tanner, L.B.; van Kuppeveld, F.J.;Wenk, M.R.; Greber, U.F. Rhinovirus uses a phosphatidylinositol 4-phosphate/cholesterol counter-current for the formation of replication compartments at the ER-Golgi interface. Cell Host Microbe 2014, 16, 677–690. [CrossRef] [PubMed]
208. Strating, J.R.; van der Linden, L.; Albulescu, L.; Bigay, J.; Arita, M.; Delang, L.; Leyssen, P.; van der Schaar, H.M.; Lanke, K.H.; Thibaut, H.J.; et al. Itraconazole inhibits enterovirus replication by targeting the oxysterol-binding protein. Cell Rep. 2015, 10, 600–615. [CrossRef] [PubMed]
209. Wang, H.; Perry, J.W.; Lauring, A.S.; Neddermann, P.; de Francesco, R.; Tai, A.W. Oxysterol-binding protein is a phosphatidylinositol 4-kinase effector required for HCV replication membrane integrity and cholesterol trafficking. Gastroenterology 2014, 146, e1371–e1311. [CrossRef] [PubMed]
210. Romero-Brey, I.; Bartenschlager, R. Viral infection at high magnification: 3D electron microscopy methods to analyze the architecture of infected cells. Viruses 2015, 7, 6316–6345. [CrossRef] [PubMed]
211. Pinali, C.; Bennett, H.; Davenport, J.B.; Trafford, A.W.; Kitmitto, A. Three-dimensional reconstruction of cardiac sarcoplasmic reticulum reveals a continuous network linking transverse-tubules: This organization is perturbed in heart failure. Circ. Res. 2013, 113, 1219–1230. [CrossRef] [PubMed]
212. Joensuu, M.; Belevich, I.; Ramo, O.; Nevzorov, I.; Vihinen, H.; Puhka, M.; Witkos, T.M.; Lowe, M.; Vartiainen, M.K.; Jokitalo, E. ER sheet persistence is coupled to myosin 1c-regulated dynamic actin filament arrays. Mol. Biol. Cell 2014, 25, 1111–1126. [CrossRef] [PubMed]
213. Wang, L.; James Ou, J.H. Hepatitis C virus and autophagy. Biol. Chem. 2015, 396, 1215–1222. [CrossRef] [PubMed]
214. Bykov, Y.S.; Cortese, M.; Briggs, J.A.; Bartenschlager, R. Correlative light and electron microscopy methods for the study of virus-cell interactions. FEBS Lett. 2016. [CrossRef] [PubMed]