1932

Abstract

Recently, dozens of virus structures have been solved to resolutions between 2.5 and 5.0 Å by means of electron cryomicroscopy. With these structures we are now firmly within the “atomic age” of electron cryomicroscopy, as these studies can reveal atomic details of protein and nucleic acid topology and interactions between specific residues. This improvement in resolution has been the result of direct electron detectors and image processing advances. Although enforcing symmetry facilitates reaching near-atomic resolution with fewer particle images, it unfortunately obscures some biologically interesting components of a virus. New approaches on relaxing symmetry and exploring structure dynamics and heterogeneity of viral assemblies have revealed important insights into genome packaging, virion assembly, cell entry, and other stages of the viral life cycle. In the future, novel methods will be required to reveal yet-unknown structural conformations of viruses, relevant to their biological activities. Ultimately, these results hold the promise of answering many unresolved questions linking structural diversity of viruses to their biological functions.

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2017-09-29
2024-12-05
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Literature Cited

  1. Krause F. 1.  1938. Aufnahmen von Viren mit dem Elektronenmikroskop. Naturwissenschaften 26:122 [Google Scholar]
  2. Stanley WM, Anderson TF. 2.  1941. A study of purified viruses with the electron microscope. J. Biol. Chem. 139:325–38 [Google Scholar]
  3. Horne RW, Wildy P. 3.  1961. Symmetry in virus architecture. Virology 15:348–73 [Google Scholar]
  4. Ackermann HW, Prangishvili D. 4.  2012. Prokaryote viruses studied by electron microscopy. Arch. Virol. 157:1843–49 [Google Scholar]
  5. Prangishvili D. 5.  2013. The wonderful world of archaeal viruses. Annu. Rev. Microbiol. 67:565–85 [Google Scholar]
  6. Adrian M, Dubochet J, Lepault J, McDowall A. 6.  1984. Cryo-electron microscopy of viruses. Nature 308:32–36 [Google Scholar]
  7. Dubochet J, Adrian M, Chang JJ, Homo JC, Lepault J. 7.  et al. 1988. Cryo-electron microscopy of vitrified specimens. Q. Rev. Biophys. 21:129–228 [Google Scholar]
  8. Bammes BE, Jakana J, Schmid MF, Chiu W. 8.  2010. Radiation damage effects at four specimen temperatures from 4 to 100 K. J. Struct. Biol. 169:331–41 [Google Scholar]
  9. De Rosier DJ, Klug A. 9.  1968. Reconstruction of three dimensional structures from electron micrographs. Nature 217:130–34 [Google Scholar]
  10. Ksiazek TG, Erdman D, Goldsmith CS, Zaki SR, Peret T. 10.  et al. 2003. A novel coronavirus associated with severe acute respiratory syndrome. N. Engl. J. Med. 348:1953–66 [Google Scholar]
  11. Brum JR, Steward GF. 11.  2010. Morphological characterization of viruses in the stratified water column of alkaline, hypersaline Mono Lake. Microb. Ecol. 60:636–43 [Google Scholar]
  12. Finch JT, Leberman R, Yu-Shang C, Klug A. 12.  1966. Rotational symmetry of the two turn disk aggregate of tobacco mosaic virus protein. Nature 212:349–50 [Google Scholar]
  13. Crowther RA, Amos LA, Finch JT, De Rosier DJ, Klug A. 13.  1970. Three dimensional reconstructions of spherical viruses by Fourier synthesis from electron micrographs. Nature 226:421–25 [Google Scholar]
  14. Frank J. 14.  1975. Averaging of low exposure electron micrographs of non-periodic objects. Ultramicroscopy 1:159–62 [Google Scholar]
  15. Kuo IA, Glaeser RM. 15.  1975. Development of methodology for low exposure, high resolution electron microscopy of biological specimens. Ultramicroscopy 1:53–66 [Google Scholar]
  16. Jeng TW, Crowther RA, Stubbs G, Chiu W. 16.  1989. Visualization of alpha-helices in tobacco mosaic virus by cryo-electron microscopy. J. Mol. Biol. 205:251–57 [Google Scholar]
  17. Ludtke SJ, Baker ML, Chen DH, Song JL, Chuang DT, Chiu W. 17.  2008. De novo backbone trace of GroEL from single particle electron cryomicroscopy. Structure 16:441–48 [Google Scholar]
  18. Jiang W, Baker ML, Jakana J, Weigele PR, King J, Chiu W. 18.  2008. Backbone structure of the infectious ε15 virus capsid revealed by electron cryomicroscopy. Nature 451:1130–34 [Google Scholar]
  19. Yu X, Jin L, Zhou ZH. 19.  2008. 3.88 Å structure of cytoplasmic polyhedrosis virus by cryo-electron microscopy. Nature 453:415–19 [Google Scholar]
  20. Zhang X, Settembre E, Xu C, Dormitzer PR, Bellamy R. 20.  et al. 2008. Near-atomic resolution using electron cryomicroscopy and single-particle reconstruction. PNAS 105:1867–72 [Google Scholar]
  21. Crowther RA. 21.  2016. The Resolution Revolution: Recent Advances in CryoEM Cambridge, MA: Academic Press [Google Scholar]
  22. Kuo J. 22.  2014. Electron Microscopy Totowa, NJ: Humana Press [Google Scholar]
  23. Liu Z, Gutierrez-Vargas C, Wei J, Grassucci RA, Sun M. 23.  et al. 2017. Determination of the ribosome structure to a resolution of 2.5 Å by single-particle cryo-EM. Protein Sci 26:82–92 [Google Scholar]
  24. Zhang X, Ge P, Yu X, Brannan JM, Bi G. 24.  et al. 2013. Cryo-EM structure of the mature dengue virus at 3.5-Å resolution. Nat. Struct. Mol. Biol. 20:105–10 [Google Scholar]
  25. Yu G, Li K, Huang P, Jiang X, Jiang W. 25.  2016. Antibody-based affinity cryoelectron microscopy at 2.6-Å resolution. Structure 24:1984–90 [Google Scholar]
  26. Wang Z, Hryc CF, Bammes B, Afonine P V, Jakana J. 26.  et al. 2014. An atomic model of brome mosaic virus using direct electron detection and real-space optimization. Nat. Commun. 5:4808 [Google Scholar]
  27. Fromm SA, Bharat TAM, Jakobi AJ, Hagen WJH, Sachse C. 27.  2015. Seeing tobacco mosaic virus through direct electron detectors. J. Struct. Biol. 189:87–97 [Google Scholar]
  28. DiMaio F, Yu X, Rensen E, Krupovic M, Prangishvili D, Egelman EH. 28.  2015. A virus that infects a hyperthermophile encapsidates A-form DNA. Science 348:914–17 [Google Scholar]
  29. Hryc CF, Chen DH, Afonine PV, Jakana J, Wang Z. 29.  et al. 2017. Accurate model annotation of a near-atomic resolution cryo-EM map. PNAS 114:3103–8 [Google Scholar]
  30. Liu H, Jin L, Koh SBS, Atanasov I, Schein S. 30.  et al. 2010. Atomic structure of human adenovirus by cryo-EM reveals interactions among protein networks. Science 329:1038–43 [Google Scholar]
  31. Li X, Zhou N, Chen W, Zhu B, Wang X. 31.  et al. 2017. Near-atomic resolution structure determination of a cypovirus capsid and polymerase complex using cryo-EM at 200 kV. J. Mol. Biol. 429:79–87 [Google Scholar]
  32. Liu Z, Guo F, Wang F, Li TC, Jiang W. 32.  2016. 2.9 Å resolution cryo-EM 3D reconstruction of close-packed virus particles. Structure 24:319–28 [Google Scholar]
  33. McMullan G, Chen S, Henderson R, Faruqi AR. 33.  2009. Detective quantum efficiency of electron area detectors in electron microscopy. Ultramicroscopy 109:1126–43 [Google Scholar]
  34. Bammes BE, Rochat RH, Jakana J, Chen DH, Chiu W. 34.  2012. Direct electron detection yields cryo-EM reconstructions at resolutions beyond 3/4 Nyquist frequency. J. Struct. Biol. 177:589–601 [Google Scholar]
  35. Brilot AF, Chen JZ, Cheng A, Pan J, Harrison SC. 35.  et al. 2012. Beam-induced motion of vitrified specimen on holey carbon film. J. Struct. Biol. 177:630–37 [Google Scholar]
  36. Jiang W, Chang J, Jakana J, Weigele P, King J, Chiu W. 36.  2006. Structure of ε15 bacteriophage reveals genome organization and DNA packaging/injection apparatus. Nature 439:612–16 [Google Scholar]
  37. Yu X, Ge P, Jiang J, Atanasov I, Zhou ZH. 37.  2011. Atomic model of CPV reveals the mechanism used by this single-shelled virus to economically carry out functions conserved in multishelled reoviruses. Structure 19:652–61 [Google Scholar]
  38. Chang J, Liu X, Rochat RH, Baker ML, Chiu W. 38.  2012. Reconstructing virus structures from nanometer to near-atomic resolutions with cryo-electron microscopy and tomography. Adv. Exp. Med. Biol 726:49–90 [Google Scholar]
  39. Henderson R, Sali A, Baker ML, Carragher B, Devkota B. 39.  et al. 2012. Outcome of the first electron microscopy validation task force meeting. Structure 20:205–14 [Google Scholar]
  40. Murray SC, Flanagan J, Popova OB, Chiu W, Ludtke SJ, Serysheva II. 40.  2013. Validation of cryo-EM structure of IP3R1 channel. Structure 21:900–9 [Google Scholar]
  41. Chen S, McMullan G, Faruqi AR, Murshudov GN, Short JM. 41.  et al. 2013. High-resolution noise substitution to measure overfitting and validate resolution in 3D structure determination by single particle electron cryomicroscopy. Ultramicroscopy 135:24–35 [Google Scholar]
  42. Hryc CF, Chen DH, Chiu W. 42.  2011. Near-atomic resolution cryo-EM for molecular virology. Curr. Opin. Virol. 1:110–17 [Google Scholar]
  43. Chen VB, Arendall WB, Headd JJ, Keedy DA, Immormino RM. 43.  et al. 2010. MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr. D 66:Pt. 112–21 [Google Scholar]
  44. Barad BA, Echols N, Wang RYR, Cheng Y, DiMaio F. 44.  et al. 2015. EMRinger: side chain-directed model and map validation for 3D cryo-electron microscopy. Nat. Methods 12:943–46 [Google Scholar]
  45. Jiang W, Li Z, Zhang Z, Baker ML, Prevelige PE, Chiu W. 45.  2003. Coat protein fold and maturation transition of bacteriophage P22 seen at subnanometer resolutions. Nat. Struct. Biol. 10:131–35 [Google Scholar]
  46. Baker ML, Jiang W, Rixon FJ, Chiu W. 46.  2005. Common ancestry of herpesviruses and tailed DNA bacteriophages. J. Virol. 79:14967–70 [Google Scholar]
  47. Grant T, Grigorieff N. 47.  2015. Measuring the optimal exposure for single particle cryo-EM using a 2.6 Å reconstruction of rotavirus VP6. eLife 4:e06980 [Google Scholar]
  48. Sirohi D, Chen Z, Sun L, Klose T, Pierson TC. 48.  et al. 2016. The 3.8 Å resolution cryo-EM structure of Zika virus. Science 352:467–70 [Google Scholar]
  49. Ge P, Zhou ZH. 49.  2011. Hydrogen-bonding networks and RNA bases revealed by cryo electron microscopy suggest a triggering mechanism for calcium switches. PNAS 108:9637–42 [Google Scholar]
  50. Yu X, Jiang J, Sun J, Zhou ZH. 50.  2015. A putative ATPase mediates RNA transcription and capping in a dsRNA virus. eLife 4:e07901 [Google Scholar]
  51. Hesketh EL, Meshcheriakova Y, Dent KC, Saxena P, Thompson RF. 51.  et al. 2015. Mechanisms of assembly and genome packaging in an RNA virus revealed by high-resolution cryo-EM. Nat. Commun. 6:10113 [Google Scholar]
  52. Bartesaghi A, Matthies D, Banerjee S, Merk A, Subramaniam S. 52.  2014. Structure of β-galactosidase at 3.2-Å resolution obtained by cryo-electron microscopy. PNAS 111:11709–14 [Google Scholar]
  53. Yonekura K, Kato K, Ogasawara M, Tomita M, Toyoshima C. 53.  2015. Electron crystallography of ultrathin 3D protein crystals: atomic model with charges. PNAS 112:3368–73 [Google Scholar]
  54. Wang J, Moore PB. 54.  2017. On the interpretation of electron microscopic maps of biological macromolecules. Protein Sci 26:122–29 [Google Scholar]
  55. Zhong S, Dadarlat VM, Glaeser RM, Head-Gordon T, Downing KH. 55.  2002. Modeling chemical bonding effects for protein electron crystallography: the transferable fragmental electrostatic potential (TFESP) method. Acta Crystallogr. A. 58:Pt. 2162–70 [Google Scholar]
  56. Xie Q, Spilman M, Meyer NL, Lerch TF, Stagg SM, Chapman MS. 56.  2013. Electron microscopy analysis of a disaccharide analog complex reveals receptor interactions of adeno-associated virus. J. Struct. Biol. 184:129–35 [Google Scholar]
  57. Lerch TF, O'Donnell JK, Meyer NL, Xie Q, Taylor KA. 57.  et al. 2012. Structure of AAV-DJ, a retargeted gene therapy vector: cryo-electron microscopy at 4.5 Å resolution. Structure 20:1310–20 [Google Scholar]
  58. Baker ML, Hryc CF, Zhang Q, Wu W, Jakana J. 58.  et al. 2013. Validated near-atomic resolution structure of bacteriophage ε15 derived from cryo-EM and modeling. PNAS 110:12301–6 [Google Scholar]
  59. Gipson P, Baker ML, Raytcheva D, Haase-Pettingell C, Piret J. 59.  et al. 2014. Protruding knob-like proteins violate local symmetries in an icosahedral marine virus. Nat. Commun. 5:4278 [Google Scholar]
  60. Auguste AJ, Kaelber JT, Fokam EB, Guzman H, Carrington CVF. 60.  et al. 2015. A newly isolated reovirus has the simplest genomic and structural organization of any reovirus. J. Virol. 89:676–87 [Google Scholar]
  61. Reinisch K, Nibert M, Harrison S. 61.  2000. Structure of the reovirus core at 3.6 Å resolution. Nature 404:960–67 [Google Scholar]
  62. Guan J, Bywaters SM, Brendle SA, Ashley RE, Makhov AM. 62.  et al. 2017. Cryoelectron microscopy maps of human papillomavirus 16 reveal L2 densities and heparin binding site. Structure 25:253–63 [Google Scholar]
  63. Hurdiss DL, Morgan EL, Thompson RF, Prescott EL, Panou MM. 63.  et al. 2016. New structural insights into the genome and minor capsid proteins of BK polyomavirus using cryo-electron microscopy. Structure 24:528–36 [Google Scholar]
  64. Liu X, Zhang Q, Murata K, Baker ML, Sullivan MB. 64.  et al. 2010. Structural changes in a marine podovirus associated with release of its genome into Prochlorococcus. Nat. Struct. Mol. Biol. 17:830–36 [Google Scholar]
  65. Hendrix RW. 65.  1978. Symmetry mismatch and DNA packaging in large bacteriophages. PNAS 75:4779–83 [Google Scholar]
  66. Tang J, Olson N, Jardine PJ, Grimes S, Anderson DL, Baker TS. 66.  2008. DNA poised for release in bacteriophage φ29. Structure 16:935–43 [Google Scholar]
  67. Sun L, Zhang X, Gao S, Rao PA, Padilla-Sanchez V. 67.  et al. 2015. Cryo-EM structure of the bacteriophage T4 portal protein assembly at near-atomic resolution. Nat. Commun. 6:7548 [Google Scholar]
  68. Rao VB, Feiss M. 68.  2015. Mechanisms of DNA packaging by large double-stranded DNA viruses. Annu. Rev. Virol. 2:351–78 [Google Scholar]
  69. Black LW. 69.  2015. Old, new, and widely true: the bacteriophage T4 DNA packaging mechanism. Virology 479:650–56 [Google Scholar]
  70. Tang L, Marion WR, Cingolani G, Prevelige PE, Johnson JE. 70.  2005. Three-dimensional structure of the bacteriophage P22 tail machine. EMBO J 24:2087–95 [Google Scholar]
  71. Cerritelli ME, Trus BL, Smith CS, Cheng N, Conway JF, Steven AC. 71.  2003. A second symmetry mismatch at the portal vertex of bacteriophage T7: 8-fold symmetry in the procapsid core. J. Mol. Biol. 327:1–6 [Google Scholar]
  72. Guo F, Liu Z, Vago F, Ren Y, Wu W. 72.  et al. 2013. Visualization of uncorrelated, tandem symmetry mismatches in the internal genome packaging apparatus of bacteriophage T7. PNAS 110:6811–16 [Google Scholar]
  73. Trus BL, Cheng N, Newcomb WW, Homa FL, Brown JC, Steven AC. 73.  2004. Structure and polymorphism of the UL6 portal protein of herpes simplex virus type 1. J. Virol. 78:12668–71 [Google Scholar]
  74. Schmid MF, Hecksel CW, Rochat RH, Bhella D, Chiu W. 74.  et al. 2012. A tail-like assembly at the portal vertex in intact herpes simplex type-1 virions. PLOS Pathog 8:e1002961 [Google Scholar]
  75. Bamford DH, Grimes JM, Stuart DI. 75.  2005. What does structure tell us about virus evolution?. Curr. Opin. Struct. Biol. 15:655–63 [Google Scholar]
  76. Cherrier MV, Kostyuchenko VA, Xiao C, Bowman VD, Battisti AJ. 76.  et al. 2009. An icosahedral algal virus has a complex unique vertex decorated by a spike. PNAS 106:11085–89 [Google Scholar]
  77. Christensen JB, Byrd SA, Walker AK, Strahler JR, Andrews PC, Imperiale MJ. 77.  2008. Presence of the adenovirus IVa2 protein at a single vertex of the mature virion. J. Virol. 82:9086–93 [Google Scholar]
  78. Schmid MF. 78.  2011. Single-particle electron cryotomography (cryoET). Adv. Protein Chem. Struct. Biol. 82:37–65 [Google Scholar]
  79. Dai W, Fu C, Raytcheva D, Flanagan J, Khant HA. 79.  et al. 2013. Visualizing virus assembly intermediates inside marine cyanobacteria. Nature 502:707–10 [Google Scholar]
  80. Daum B, Quax TEF, Sachse M, Mills DJ, Reimann J. 80.  et al. 2014. Self-assembly of the general membrane-remodeling protein PVAP into sevenfold virus-associated pyramids. PNAS 111:3829–34 [Google Scholar]
  81. Guerrero-Ferreira RC, Viollier PH, Ely B, Poindexter JS, Georgieva M. 81.  et al. 2011. Alternative mechanism for bacteriophage adsorption to the motile bacterium Caulobacter crescentus. PNAS 108:9963–68 [Google Scholar]
  82. Maurer UE, Sodeik B, Grünewald K. 82.  2008. Native 3D intermediates of membrane fusion in herpes simplex virus 1 entry. PNAS 105:10559–64 [Google Scholar]
  83. Zauberman N, Mutsafi Y, Ben Halevy D, Shimoni E, Klein E. 83.  et al. 2008. Distinct DNA exit and packaging portals in the virus Acanthamoeba polyphaga mimivirus. PLOS Biol. 6:e114 [Google Scholar]
  84. Marko M, Hsieh C, Schalek R, Frank J, Mannella C. 84.  2007. Focused-ion-beam thinning of frozen-hydrated biological specimens for cryo-electron microscopy. Nat. Methods 4:215–17 [Google Scholar]
  85. Rigort A, Bäuerlein FJB, Villa E, Eibauer M, Laugks T. 85.  et al. 2012. Focused ion beam micromachining of eukaryotic cells for cryoelectron tomography. PNAS 109:4449–54 [Google Scholar]
  86. Dai W, Fu C, Khant HA, Ludtke SJ, Schmid MF, Chiu W. 86.  2014. Zernike phase-contrast electron cryotomography applied to marine cyanobacteria infected with cyanophages. Nat. Protoc. 9:2630–42 [Google Scholar]
  87. Guerrero-Ferreira RC, Wright ER. 87.  2014. Zernike phase contrast cryo-electron tomography of whole bacterial cells. J. Struct. Biol. 185:129–33 [Google Scholar]
  88. Cerritelli ME, Cheng N, Rosenberg AH, McPherson CE, Booy FP, Steven AC. 88.  1997. Encapsidated conformation of bacteriophage T7 DNA. Cell 91:271–80 [Google Scholar]
  89. Bauer DW, Li D, Huffman J, Homa FL, Wilson K. 89.  et al. 2015. Exploring the balance between DNA pressure and capsid stability in herpesviruses and phages. J. Virol. 89:9288–98 [Google Scholar]
  90. Speir JA, Munshi S, Wang G, Baker TS, Johnson JE. 90.  1995. Structures of the native and swollen forms of cowpea chlorotic mottle virus determined by X-ray crystallography and cryo-electron microscopy. Structure 3:63–78 [Google Scholar]
  91. Gopal A, Zhou ZH, Knobler CM, Gelbart WM. 91.  2012. Visualizing large RNA molecules in solution. RNA 18:284–99 [Google Scholar]
  92. Irobalieva RN, Fogg JM, Catanese DJ, Sutthibutpong T, Chen M. 92.  et al. 2015. Structural diversity of supercoiled DNA. Nat. Commun. 6:8440 [Google Scholar]
  93. Gorzelnik KV, Cui Z, Reed CA, Jakana J, Young R, Zhang J. 93.  2016. Asymmetric cryo-EM structure of the canonical Allolevivirus Qβ reveals a single maturation protein and the genomic ssRNA in situ. PNAS 113:11519–24 [Google Scholar]
  94. Koning RI, Gomez-Blanco J, Akopjana I, Vargas J, Kazaks A. 94.  et al. 2016. Asymmetric cryo-EM reconstruction of phage MS2 reveals genome structure in situ. Nat. Commun. 7:12524 [Google Scholar]
  95. Dai X, Li Z, Lai M, Shu S, Du Y. 95.  et al. 2016. In situ structures of the genome and genome-delivery apparatus in a single-stranded RNA virus. Nature 541:112–16 [Google Scholar]
  96. Speir JA, Johnson JE. 96.  2012. Nucleic acid packaging in viruses. Curr. Opin. Struct. Biol. 22:65–71 [Google Scholar]
  97. Miyazaki Y, Irobalieva RN, Tolbert BS, Smalls-Mantey A, Iyalla K. 97.  et al. 2010. Structure of a conserved retroviral RNA packaging element by NMR spectroscopy and cryo-electron tomography. J. Mol. Biol. 404:751–72 [Google Scholar]
  98. Siridechadilok B, Fraser CS, Hall RJ, Doudna JA, Nogales E. 98.  2005. Structural roles for human translation factor eIF3 in initiation of protein synthesis. Science 310:1513–15 [Google Scholar]
  99. Tawar RG, Duquerroy S, Vonrhein C, Varela PF, Damier-Piolle L. 99.  et al. 2009. Crystal structure of a nucleocapsid-like nucleoprotein-RNA complex of respiratory syncytial virus. Science 326:1279–83 [Google Scholar]
  100. Gutsche I, Desfosses A, Effantin G, Ling WL, Haupt M. 100.  et al. 2015. Near-atomic cryo-EM structure of the helical measles virus nucleocapsid. Science 348:704–7 [Google Scholar]
  101. Raymond DD, Piper ME, Gerrard SR, Skiniotis G, Smith JL. 101.  2012. Phleboviruses encapsidate their genomes by sequestering RNA bases. PNAS 109:19208–13 [Google Scholar]
  102. Belnap DM, Filman DJ, Trus BL, Cheng N, Booy FP. 102.  et al. 2000. Molecular tectonic model of virus structural transitions: the putative cell entry states of poliovirus. J. Virol. 74:1342–54 [Google Scholar]
  103. He Y, Mueller S, Chipman PR, Bator CM, Peng X. 103.  et al. 2003. Complexes of poliovirus serotypes with their common cellular receptor, CD155. J. Virol. 77:4827–35 [Google Scholar]
  104. Zhang P, Mueller S, Morais MC, Bator CM, Bowman VD. 104.  et al. 2008. Crystal structure of CD155 and electron microscopic studies of its complexes with polioviruses. PNAS 105:18284–89 [Google Scholar]
  105. Tuthill TJ, Bubeck D, Rowlands DJ, Hogle JM. 105.  2006. Characterization of early steps in the poliovirus infection process: Receptor-decorated liposomes induce conversion of the virus to membrane-anchored entry-intermediate particles. J. Virol. 80:172–80 [Google Scholar]
  106. Levy HC, Bostina M, Filman DJ, Hogle JM. 106.  2010. Catching a virus in the act of RNA release: a novel poliovirus uncoating intermediate characterized by cryo-electron microscopy. J. Virol. 84:4426–41 [Google Scholar]
  107. Bostina M, Levy H, Filman DJ, Hogle JM. 107.  2011. Poliovirus RNA is released from the capsid near a twofold symmetry axis. J. Virol. 85:776–83 [Google Scholar]
  108. Lin J, Cheng N, Chow M, Filman DJ, Steven AC. 108.  et al. 2011. An externalized polypeptide partitions between two distinct sites on genome-released poliovirus particles. J. Virol. 85:9974–83 [Google Scholar]
  109. Nasr ML, Baptista D, Strauss M, Sun ZYJ, Grigoriu S. 109.  et al. 2016. Covalently circularized nanodiscs for studying membrane proteins and viral entry. Nat. Methods 14:49–52 [Google Scholar]
  110. Lee H, Shingler KL, Organtini LJ, Ashley RE, Makhov AM. 110.  et al. 2016. The novel asymmetric entry intermediate of a picornavirus captured with nanodiscs. Sci. Adv. 2:e1501929 [Google Scholar]
  111. Butan C, Filman DJ, Hogle JM. 111.  2014. Cryo-electron microscopy reconstruction shows poliovirus 135S particles poised for membrane interaction and RNA release. J. Virol. 88:1758–70 [Google Scholar]
  112. Kalynych S, Füzik T, Přidal A, de Miranda J, Plevka P. 112.  2017. Cryo-EM study of slow bee paralysis virus at low pH reveals iflavirus genome release mechanism. PNAS 114:598–603 [Google Scholar]
  113. Yang Z, Fang J, Chittuluru J, Asturias FJ, Penczek PA. 113.  2012. Iterative stable alignment and clustering of 2D transmission electron microscope images. Structure 20:237–47 [Google Scholar]
  114. Ludtke SJ. 114.  2016. Single-particle refinement and variability analysis in EMAN2.1. Methods Enzymol 579:159–89 [Google Scholar]
  115. Scheres SHW. 115.  2012. A Bayesian view on cryo-EM structure determination. J. Mol. Biol. 415:406–18 [Google Scholar]
  116. Bai X, Rajendra E, Yang G, Shi Y, Scheres SHW. 116.  2015. Sampling the conformational space of the catalytic subunit of human γ-secretase. eLife 4:e11182 [Google Scholar]
  117. Wang Z, Fan G, Hryc CF, Blaza JN, Serysheva II. 117.  et al. 2017. An allosteric transport mechanism for the AcrAB-TolC multidrug efflux pump. eLife 6:e24905 [Google Scholar]
  118. Scheres SHW. 118.  2016. Processing of structurally heterogeneous cryo-EM data in RELION. Methods Enzymol 579:125–57 [Google Scholar]
  119. Gui M, Song W, Zhou H, Xu J, Chen S. 119.  et al. 2017. Cryo-electron microscopy structures of the SARS-CoV spike glycoprotein reveal a prerequisite conformational state for receptor binding. Cell Res 27:119–29 [Google Scholar]
  120. Walls AC, Tortorici MA, Frenz B, Snijder J, Li W. 120.  et al. 2016. Glycan shield and epitope masking of a coronavirus spike protein observed by cryo-electron microscopy. Nat. Struct. Mol. Biol. 23:899–905 [Google Scholar]
  121. Walls AC, Tortorici MA, Bosch BJ, Frenz B, Rottier PJM. 121.  et al. 2016. Cryo-electron microscopy structure of a coronavirus spike glycoprotein trimer. Nature 531:114–17 [Google Scholar]
  122. Lee JH, Ozorowski G, Ward AB. 122.  2016. Cryo-EM structure of a native, fully glycosylated, cleaved HIV-1 envelope trimer. Science 351:1043–48 [Google Scholar]
  123. Ward AB, Wilson IA. 123.  2017. The HIV-1 envelope glycoprotein structure: nailing down a moving target. Immunol. Rev. 275:21–32 [Google Scholar]
  124. Ward AB, Wilson IA. 124.  2015. Insights into the trimeric HIV-1 envelope glycoprotein structure. Trends Biochem. Sci. 40:101–7 [Google Scholar]
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