Structure and organization of paramyxovirus particles

Current Opinion in Virology

Volumn 24, Issue , 2017, Pages 105-114

  Cox, Robert M ^a   Plemper, Richard K ^a  

^a GEORGIA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOPROTEIN; GUANINE NUCLEOTIDE BINDING PROTEIN; HYBRID PROTEIN; M PROTEIN; MATRIX PROTEIN; RIBONUCLEOPROTEIN; VIRUS FUSION PROTEIN;

NONHUMAN; PARAMYXOVIRIDAE; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; RECEPTOR BINDING; REVIEW; TRANSIENT EXPRESSION; VIRION; VIRUS INFECTION; VIRUS MORPHOLOGY; CHEMISTRY; CRYOELECTRON MICROSCOPY; ELECTRON TOMOGRAPHY; HUMAN; MEASLES VIRUS; METABOLISM; NEWCASTLE DISEASE VIRUS; NIPAH VIRUS; PHYSIOLOGY; ULTRASTRUCTURE; VIRUS ASSEMBLY; VIRUS GENOME; VIRUS RELEASE;

CRYOELECTRON MICROSCOPY; ELECTRON MICROSCOPE TOMOGRAPHY; GENOME, VIRAL; HUMANS; MEASLES VIRUS; NEWCASTLE DISEASE VIRUS; NIPAH VIRUS; PARAMYXOVIRIDAE; VIRAL FUSION PROTEINS; VIRAL MATRIX PROTEINS; VIRION; VIRUS ASSEMBLY; VIRUS RELEASE;

EID: 85020249829     PISSN: 18796257     EISSN: 18796265     Source Type: Journal    
DOI: 10.1016/j.coviro.2017.05.004     Document Type: Review

References (93)

1. Yanagi, Y., Takeda, M., Ohno, S., Seki, F., Measles virus receptors and tropism. Jpn. J. Infect. Dis. 59 (2006), 1–5.
2. Li, Z., Hung, C., Paterson, R.G., Michel, F., Fuentes, S., et al. Type II integral membrane protein, TM of J paramyxovirus promotes cell-to-cell fusion. Proc. Natl. Acad. Sci. U. S. A. 112 (2015), 12504–12509.
3. Pearce, L.A., Yu, M., Waddington, L.J., Barr, J.A., Scoble, J.A., et al. Structural characterization by transmission electron microscopy and immunoreactivity of recombinant Hendra virus nucleocapsid protein expressed and purified from Escherichia coli. Protein Expr. Purif. 116 (2015), 19–29.
4. 4• Gutsche, I., Desfosses, A., Effantin, G., Ling, W.L., Haupt, M., et al. Structural virology. Near-atomic cryo-EM structure of the helical measles virus nucleocapsid. Science 348 (2015), 704–707 High-resolution reconstruction of the measles virus genome assembly that provides important structural insight into the viral nucleoprotein–RNA interaction.
5. Gui, L., Jurgens, E.M., Ebner, J.L., Porotto, M., Moscona, A., et al. Electron tomography imaging of surface glycoproteins on human parainfluenza virus 3: association of receptor binding and fusion proteins before receptor engagement. mBio 6 (2015), e02393–02314.
6. 6•• Battisti, A.J., Meng, G., Winkler, D.C., McGinnes, L.W., Plevka, P., et al. Structure and assembly of a paramyxovirus matrix protein. Proc. Natl. Acad. Sci. U. S. A. 109 (2012), 13996–14000 First cryo-electron tomography reconstruction of Newcastle disease virus particles combined with X-ray crystallography of analysis of the viral matrix protein reveals pseudotetrameric matrix arrays that generate the membrane curvature required for virus budding.
7. Schoehn, G., Mavrakis, M., Albertini, A., Wade, R., Hoenger, A., et al. The 12 A structure of trypsin-treated measles virus N-RNA. J. Mol. Biol. 339 (2004), 301–312.
8. Bhella, D., Ralph, A., Yeo, R.P., Conformational flexibility in recombinant measles virus nucleocapsids visualised by cryo-negative stain electron microscopy and real-space helical reconstruction. J. Mol. Biol. 340 (2004), 319–331.
9. Chua, K.B., Bellini, W.J., Rota, P.A., Harcourt, B.H., Tamin, A., et al. Nipah virus: a recently emergent deadly paramyxovirus. Science 288 (2000), 1432–1435.
10. Chua, K.B., Wang, L.F., Lam, S.K., Crameri, G., Yu, M., et al. Tioman virus, a novel paramyxovirus isolated from fruit bats in Malaysia. Virology 283 (2001), 215–229.
11. Chua, K.B., Wang, L.F., Lam, S.K., Eaton, B.T., Full length genome sequence of Tioman virus, a novel paramyxovirus in the genus Rubulavirus isolated from fruit bats in Malaysia. Arch. Virol. 147 (2002), 1323–1348.
12. Curry, A., Appleton, H., Dowsett, B., Application of transmission electron microscopy to the clinical study of viral and bacterial infections: present and future. Micron 37 (2006), 91–106.
13. Goldsmith, C.S., Ksiazek, T.G., Rollin, P.E., Comer, J.A., Nicholson, W.L., et al. Cell culture and electron microscopy for identifying viruses in diseases of unknown cause. Emerg. Infect. Dis. 19 (2013), 886–891.
14. Goldsmith, C.S., Miller, S.E., Modern uses of electron microscopy for detection of viruses. Clin. Microbiol. Rev. 22 (2009), 552–563.
15. Hall, W.W., Martin, S.J., Purification and characterization of measles virus. J. Gen. Virol. 19 (1973), 175–188.
16. Halpin, K., Young, P.L., Field, H.E., Mackenzie, J.S., Isolation of Hendra virus from pteropid bats: a natural reservoir of Hendra virus. J. Gen. Virol. 81 (2000), 1927–1932.
17. Kvellestad, A., Dannevig, B.H., Falk, K., Isolation and partial characterization of a novel paramyxovirus from the gills of diseased seawater-reared Atlantic salmon (Salmo salar L.). J. Gen. Virol. 84 (2003), 2179–2189.
18. Li, Z., Yu, M., Zhang, H., Magoffin, D.E., Jack, P.J., et al. Beilong virus, a novel paramyxovirus with the largest genome of non-segmented negative-stranded RNA viruses. Virology 346 (2006), 219–228.
19. Mast, J., Demeestere, L., Electron tomography of negatively stained complex viruses: application in their diagnosis. Diagn. Pathol., 4, 2009, 5.
20. Philbey, A.W., Kirkland, P.D., Ross, A.D., Field, H.E., Srivastava, M., et al. Infection with Menangle virus in flying foxes (Pteropus spp.) in Australia. Aust. Vet. J. 86 (2008), 449–454.
21. Schmitt, A.P., Leser, G.P., Waning, D.L., Lamb, R.A., Requirements for budding of paramyxovirus simian virus 5 virus-like particles. J. Virol. 76 (2002), 3952–3964.
22. Terrier, O., Rolland, J.P., Rosa-Calatrava, M., Lina, B., Thomas, D., et al. Parainfluenza virus type 5 (PIV-5) morphology revealed by cryo-electron microscopy. Virus Res. 142 (2009), 200–203.
23. Ludwig, K., Schade, B., Bottcher, C., Korte, T., Ohlwein, N., et al. Electron cryomicroscopy reveals different F1 + F2 protein states in intact parainfluenza virions. J. Virol. 82 (2008), 3775–3781.
24. Wong, J.J., Paterson, R.G., Lamb, R.A., Jardetzky, T.S., Structure and stabilization of the Hendra virus F glycoprotein in its prefusion form. Proc. Natl. Acad. Sci. U. S. A. 113 (2016), 1056–1061.
25. 25•• Xu, K., Chan, Y.P., Bradel-Tretheway, B., Akyol-Ataman, Z., Zhu, Y., et al. Crystal structure of the pre-fusion Nipah virus fusion glycoprotein reveals a novel hexamer-of-trimers assembly. PLoS Pathog., 11, 2015, e1005322 First report that Nipah fusion protein trimers may exist in higher order oligomer assemblies on the surface of viral particles.
26. Guryanov, S.G., Liljeroos, L., Kasaragod, P., Kajander, T., Butcher, S.J., Crystal structure of the measles virus nucleoprotein core in complex with an N-terminal region of phosphoprotein. J. Virol. 90 (2015), 2849–2857.
27. Yabukarski, F., Lawrence, P., Tarbouriech, N., Bourhis, J.M., Delaforge, E., et al. Structure of Nipah virus unassembled nucleoprotein in complex with its viral chaperone. Nat. Struct. Mol. Biol. 21 (2014), 754–759.
28. 28• Cox, R., Pickar, A., Qiu, S., Tsao, J., Rodenburg, C., et al. Structural studies on the authentic mumps virus nucleocapsid showing uncoiling by the phosphoprotein. Proc. Natl. Acad. Sci. U. S. A. 111 (2014), 15208–15213 Study presents evidence that the viral phosphoprotein may mediate local de-encapsidation of the mumps virus RNP genome.
29. Welch, B.D., Yuan, P., Bose, S., Kors, C.A., Lamb, R.A., et al. Structure of the parainfluenza virus 5 (PIV5) hemagglutinin-neuraminidase (HN) ectodomain. PLoS Pathog., 9, 2013, e1003534.
30. Yuan, P., Paterson, R.G., Leser, G.P., Lamb, R.A., Jardetzky, T.S., Structure of the ulster strain newcastle disease virus hemagglutinin–neuraminidase reveals auto-inhibitory interactions associated with low virulence. PLoS Pathog., 8, 2012, e1002855.
31. Welch, B.D., Liu, Y., Kors, C.A., Leser, G.P., Jardetzky, T.S., et al. Structure of the cleavage-activated prefusion form of the parainfluenza virus 5 fusion protein. Proc. Natl. Acad. Sci. U. S. A. 109 (2012), 16672–16677.
32. Yuan, P., Swanson, K.A., Leser, G.P., Paterson, R.G., Lamb, R.A., et al. Structure of the Newcastle disease virus hemagglutinin–neuraminidase (HN) ectodomain reveals a four-helix bundle stalk. Proc. Natl. Acad. Sci. U. S. A. 108 (2011), 14920–14925.
33. Bose, S., Welch, B.D., Kors, C.A., Yuan, P., Jardetzky, T.S., et al. Structure and mutagenesis of the parainfluenza virus 5 hemagglutinin–neuraminidase stalk domain reveals a four-helix bundle and the role of the stalk in fusion promotion. J. Virol. 1285 (2011), 5–12866.
34. Swanson, K., Wen, X., Leser, G.P., Paterson, R.G., Lamb, R.A., et al. Structure of the Newcastle disease virus F protein in the post-fusion conformation. Virology 402 (2010), 372–379.
35. Santiago, C., Celma, M.L., Stehle, T., Casasnovas, J.M., Structure of the measles virus hemagglutinin bound to the CD46 receptor. Nat. Struct. Mol. Biol. 17 (2010), 124–129.
36. Bowden, T.A., Crispin, M., Harvey, D.J., Aricescu, A.R., Grimes, J.M., et al. Crystal structure and carbohydrate analysis of Nipah virus attachment glycoprotein: a template for antiviral and vaccine design. J. Virol. 82 (2008), 11628–11636.
37. 37• Yin, H.S., Wen, X., Paterson, R.G., Lamb, R.A., Jardetzky, T.S., Structure of the parainfluenza virus 5 F protein in its metastable, prefusion conformation. Nature 439 (2006), 38–44 First high-resolution structure of a paramyxovirus fusion protein in a prefusion conformation.
38. Li, T., Chen, X., Garbutt, K.C., Zhou, P., Zheng, N., Structure of DDB1 in complex with a paramyxovirus V protein: viral hijack of a propeller cluster in ubiquitin ligase. Cell 124 (2006), 105–117.
39. Yuan, P., Thompson, T.B., Wurzburg, B.A., Paterson, R.G., Lamb, R.A., et al. Structural studies of the parainfluenza virus 5 hemagglutinin–neuraminidase tetramer in complex with its receptor, sialyllactose. Structure 13 (2005), 803–815.
40. Yin, H.S., Paterson, R.G., Wen, X., Lamb, R.A., Jardetzky, T.S., Structure of the uncleaved ectodomain of the paramyxovirus (hPIV3) fusion protein. Proc. Natl. Acad. Sci. U. S. A. 102 (2005), 9288–9293.
41. Crennell, S., Takimoto, T., Portner, A., Taylor, G., Crystal structure of the multifunctional paramyxovirus hemagglutinin–neuraminidase. Nat. Struct. Biol. 7 (2000), 1068–1074.
42. Baker, K.A., Dutch, R.E., Lamb, R.A., Jardetzky, T.S., Structural basis for paramyxovirus-mediated membrane fusion. Mol. Cell 3 (1999), 309–319.
43. 43•• Liljeroos, L., Huiskonen, J.T., Ora, A., Susi, P., Butcher, S.J., Electron cryotomography of measles virus reveals how matrix protein coats the ribonucleocapsid within intact virions. Proc. Natl. Acad. Sci. U. S. A. 108 (2011), 18085–18090 First reconstruction of measles virus particles, revealing unexpected tubular matrix protein assemblies around the viral RNPs.
44. 44•• Loney, C., Mottet-Osman, G., Roux, L., Bhella, D., Paramyxovirus ultrastructure and genome packaging: cryo-electron tomography of sendai virus. J. Virol. 83 (2009), 8191–8197 First cryo-electron tomography-based reconstruction of Sendai virus particles.
45. Liljeroos, L., Krzyzaniak, M.A., Helenius, A., Butcher, S.J., Architecture of respiratory syncytial virus revealed by electron cryotomography. Proc. Natl. Acad. Sci. U. S. A. 110 (2013), 11133–11138.
46. Lamb, R.A., Parks, G.D., Paramyxoviridae: the viruses and their replication. Knipe, D.M., Howley, P.M., (eds.) Fields Virology, 5th ed., 2007, Wolters Kluwer/Lippincott Williams & Wilkins, Philadelphia, 1449–1496.
47. Bhella, D., Ralph, A., Murphy, L.B., Yeo, R.P., Significant differences in nucleocapsid morphology within the Paramyxoviridae. J. Gen. Virol. 83 (2002), 1831–1839.
48. Egelman, E.H., Wu, S.S., Amrein, M., Portner, A., Murti, G., The Sendai virus nucleocapsid exists in at least four different helical states. J. Virol. 63 (1989), 2233–2243.
49. Rager, M., Vongpunsawad, S., Duprex, W.P., Cattaneo, R., Polyploid measles virus with hexameric genome length. EMBO J. 21 (2002), 2364–2372.
50. 50• Brindley, M.A., Suter, R., Schestak, I., Kiss, G., Wright, E.R., et al. A stabilized headless measles virus attachment protein stalk efficiently triggers membrane fusion. J. Virol. 87 (2013), 11693–11703 First demonstration that induced tetramerization of morbillivirus attachment protein stalk domains restores intracellular transport competence and fusion triggering activity in the absence of the head domains.
51. El Najjar, F., Schmitt, A.P., Dutch, R.E., Paramyxovirus glycoprotein incorporation, assembly and budding: a three way dance for infectious particle production. Viruses 6 (2014), 3019–3054.
52. Harrison, M.S., Sakaguchi, T., Schmitt, A.P., Paramyxovirus assembly and budding: building particles that transmit infections. Int. J. Biochem. Cell Biol. 42 (2010), 1416–1429.
53. Riedl, P., Moll, M., Klenk, H.D., Maisner, A., Measles virus matrix protein is not cotransported with the viral glycoproteins but requires virus infection for efficient surface targeting. Virus Res. 83 (2002), 1–12.
54. Pohl, C., Duprex, W.P., Krohne, G., Rima, B.K., Schneider-Schaulies, S., Measles virus M and F proteins associate with detergent-resistant membrane fractions and promote formation of virus-like particles. J. Gen. Virol. 88 (2007), 1243–1250.
55. Sugahara, F., Uchiyama, T., Watanabe, H., Shimazu, Y., Kuwayama, M., et al. Paramyxovirus Sendai virus-like particle formation by expression of multiple viral proteins and acceleration of its release by C protein. Virology 325 (2004), 1–10.
56. Takimoto, T., Murti, K.G., Bousse, T., Scroggs, R.A., Portner, A., Role of matrix and fusion proteins in budding of Sendai virus. J. Virol. 75 (2001), 11384–11391.
57. Runkler, N., Pohl, C., Schneider-Schaulies, S., Klenk, H.D., Maisner, A., Measles virus nucleocapsid transport to the plasma membrane requires stable expression and surface accumulation of the viral matrix protein. Cell Microbiol. 9 (2007), 1203–1214.
58. Ciancanelli, M.J., Basler, C.F., Mutation of YMYL in the Nipah virus matrix protein abrogates budding and alters subcellular localization. J. Virol. 80 (2006), 12070–12078.
59. Patch, J.R., Crameri, G., Wang, L.F., Eaton, B.T., Broder, C.C., Quantitative analysis of Nipah virus proteins released as virus-like particles reveals central role for the matrix protein. Virol. J., 4, 2007, 1.
60. Sun, W., McCrory, T.S., Khaw, W.Y., Petzing, S., Myers, T., et al. Matrix proteins of Nipah and Hendra viruses interact with beta subunits of AP-3 complexes. J. Virol. 88 (2014), 13099–13110.
61. Pantua, H.D., McGinnes, L.W., Peeples, M.E., Morrison, T.G., Requirements for the assembly and release of Newcastle disease virus-like particles. J. Virol. 80 (2006), 11062–11073.
62. Coronel, E.C., Murti, K.G., Takimoto, T., Portner, A., Human parainfluenza virus type 1 matrix and nucleoprotein genes transiently expressed in mammalian cells induce the release of virus-like particles containing nucleocapsid-like structures. J. Virol. 73 (1999), 7035–7038.
63. Li, M., Schmitt, P.T., Li, Z., McCrory, T.S., He, B., et al. Mumps virus matrix, fusion, and nucleocapsid proteins cooperate for efficient production of virus-like particles. J. Virol. 83 (2009), 7261–7272.
64. Johnston, G.P., Contreras, E.M., Dabundo, J., Henderson, B.A., Matz, K.M., et al. Cytoplasmic motifs in the Nipah virus fusion protein modulate virus particle assembly and egress. J. Virol., 91, 2017.
65. Cathomen, T., Mrkic, B., Spehner, D., Drillien, R., Naef, R., et al. A matrix-less measles virus is infectious and elicits extensive cell fusion: consequences for propagation in the brain. EMBO J. 17 (1998), 3899–3908.
66. Cathomen, T., Naim, H.Y., Cattaneo, R., Measles viruses with altered envelope protein cytoplasmic tails gain cell fusion competence. J. Virol. 72 (1998), 1224–1234.
67. Sawatsky, B., Bente, D.A., Czub, M., von Messling, V., Morbillivirus and henipavirus attachment protein cytoplasmic domains differently affect protein expression, fusion support and particle assembly. J. Gen. Virol. 97 (2016), 1066–1076.
68. Plemper, R.K., Cell entry of enveloped viruses. Curr. Opin. Virol. 1 (2011), 92–100.
69. Sourimant, J., Plemper, R.K., Organization, function, and therapeutic targeting of the morbillivirus RNA-dependent RNA polymerase complex. Viruses, 8, 2016.
70. Longhi, S., Nucleocapsid structure and function. Curr. Top. Microbiol. Immunol. 329 (2009), 103–128.
71. 71• Iwasaki, M., Takeda, M., Shirogane, Y., Nakatsu, Y., Nakamura, T., et al. The matrix protein of measles virus regulates viral RNA synthesis and assembly by interacting with the nucleocapsid protein. J. Virol. 83 (2009), 10374–10383 First mapping of a measles virus matrix protein binding domain near the carboxy-terminus of the nucleocapsid protein tail domain.
72. 72• Cox, R.M., Krumm, S.A., Thakkar, V.D., Sohn, M., Plemper, R.K., The structurally disordered paramyxovirus nucleocapsid protein tail domain is a regulator of the mRNA transcription gradient. Sci. Adv., 3, 2017, e1602350 First demonstration that productive interaction of the viral polymerase complex with the RNP genome does not require a previously postulated fly-casting mechanism mediated by the intrinsically unstructured paramyxovirus nucleoprotein tail domain.
73. Griffin, D.E., Measles virus. Knipe, D.M., Howley, P.M., (eds.) Fields Virology, 5th ed., 2007, Wolters Kluwer/Lippincott Williams & Wilkins, Philadelphia, 1551–1585.
74. McChesney, M.B., Miller, C.J., Rota, P.A., Zhu, Y.D., Antipa, L., et al. Experimental measles. I. Pathogenesis in the normal and the immunized host. Virology 233 (1997), 74–84.
75. 75• Suryanarayana, K., Baczko, K., ter Meulen, V., Wagner, R.R., Transcription inhibition and other properties of matrix proteins expressed by M genes cloned from measles viruses and diseased human brain tissue. J. Virol. 68 (1994), 1532–1543 Early demonstration that the measles virus matrix protein suppresses transcription of the viral genome.
76. Mottet-Osman, G., Iseni, F., Pelet, T., Wiznerowicz, M., Garcin, D., et al. Suppression of the Sendai virus M protein through a novel short interfering RNA approach inhibits viral particle production but does not affect viral RNA synthesis. J. Virol. 81 (2007), 2861–2868.
77. 77• Brindley, M.A., Chaudhury, S., Plemper, R.K., Measles virus glycoprotein complexes preassemble intracellularly and relax during transport to the cell surface in preparation for fusion. J. Virol. 89 (2015), 1230–1241 Comprehensive assessment of the maturation cascade of the measles virus glycoprotein oligomers, demonstrating tight intracellular pre-assembly of the fusion and attachment proteins before surface expression and incorporation into viral particles.
78. Paal, T., Brindley, M.A., St Clair, C., Prussia, A., Gaus, D., et al. Probing the spatial organization of measles virus fusion complexes. J. Virol. 83 (2009), 10480–10493.
79. Bose, S., Song, A.S., Jardetzky, T.S., Lamb, R.A., Fusion activation through attachment protein stalk domains indicates a conserved core mechanism of paramyxovirus entry into cells. J. Virol. 88 (2014), 3925–3941.
80. 80• Bose, S., Zokarkar, A., Welch, B.D., Leser, G.P., Jardetzky, T.S., et al. Fusion activation by a headless parainfluenza virus 5 hemagglutinin–neuraminidase stalk suggests a modular mechanism for triggering. Proc. Natl. Acad. Sci. U. S. A. 109 (2012), E2625–E2634 First report demonstrating efficient triggering of a paramyxovirus fusion protein complex by an attachment protein mutant lacking the receptor binding head domains.
81. Liu, Q., Bradel-Tretheway, B., Monreal, A.I., Saludes, J.P., Lu, X., et al. Nipah virus attachment glycoprotein stalk C-terminal region links receptor binding to fusion triggering. J. Virol. 89 (2015), 1838–1850.
82. Liu, Q., Stone, J.A., Bradel-Tretheway, B., Dabundo, J., Benavides Montano, J.A., et al. Unraveling a three-step spatiotemporal mechanism of triggering of receptor-induced Nipah virus fusion and cell entry. PLoS Pathog., 9, 2013, e1003770.
83. Brindley, M.A., Takeda, M., Plattet, P., Plemper, R.K., Triggering the measles virus membrane fusion machinery. Proc. Natl. Acad. Sci. U. S. A. 109 (2012), E3018–3027.
84. 84• Brindley, M.A., Plemper, R.K., Blue native PAGE and biomolecular complementation reveal a tetrameric or higher-order oligomer organization of the physiological measles virus attachment protein H. J. Virol. 84 (2010), 12174–12184 First biochemical conformation that receptor binding-induced structural changes in the measles virus attachment protein lead to fusion triggering.
85. Danieli, T., Pelletier, S.L., Henis, Y.I., White, J.M., Membrane fusion mediated by the influenza virus hemagglutinin requires the concerted action of at least three hemagglutinin trimers. J. Cell Biol. 133 (1996), 559–569.
86. Floyd, D.L., Ragains, J.R., Skehel, J.J., Harrison, S.C., van Oijen, A.M., Single-particle kinetics of influenza virus membrane fusion. Proc. Natl. Acad. Sci. U. S. A. 105 (2008), 15382–15387.
87. Freed, E.O., Delwart, E.L., Buchschacher, G.L. Jr, Panganiban, A.T., A mutation in the human immunodeficiency virus type 1 transmembrane glycoprotein gp41 dominantly interferes with fusion and infectivity. Proc. Natl. Acad. Sci. U. S. A. 89 (1992), 70–74.
88. Brown, J.C., Newcomb, W.W., Lawrenz-Smith, S., pH-dependent accumulation of the vesicular stomatitis virus glycoprotein at the ends of intact virions. Virology 167 (1988), 625–629.
89. Lee, K.K., Architecture of a nascent viral fusion pore. EMBO J. 29 (2010), 1299–1311.
90. Gui, L., Ebner, J.L., Mileant, A., Williams, J.A., Lee, K.K., Visualization and sequencing of membrane remodeling leading to influenza virus fusion. J. Virol. 90 (2016), 6948–6962.
91. Calder, L.J., Rosenthal, P.B., Cryomicroscopy provides structural snapshots of influenza virus membrane fusion. Nat. Struct. Mol. Biol. 23 (2016), 853–858.
92. Pettersen, E.F., Goddard, T.D., Huang, C.C., Couch, G.S., Greenblatt, D.M., et al. UCSF Chimera—a visualization system for exploratory research and analysis. J. Comput. Chem. 25 (2004), 1605–1612.
93. The PyMOL Molecular Graphics System, Version 1.8. 2010, Schrödinger, LLC.