1932

Abstract

The recent proliferation of cryo-electron tomography (cryo-ET) techniques has led to the cryo-ET resolution revolution. Meanwhile, significant efforts have been made to improve the identification of targets in the cellular context and the throughput of cryo-focused ion beam (FIB) milling. Together, these developments led to a surge of in situ discoveries on how enveloped viruses are assembled and how viruses interact with cells in infected hosts. In this article, we review the recent advances in cryo-ET, high-resolution insights into virus assembly, and the findings from inside infected eukaryotic and prokaryotic cells.

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2023-05-09
2024-04-24
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Literature Cited

  1. 1.
    Arnold J, Mahamid J, Lucic V, Marco AD, Fernandez JJ et al. 2016. Site-specific cryo-focused ion beam sample preparation guided by 3D correlative microscopy. Biophys. J. 110:860–69
    [Google Scholar]
  2. 2.
    Bepler T, Kelley K, Noble AJ, Berger B. 2020. Topaz-Denoise: general deep denoising models for cryoEM and cryoET. Nat. Commun. 11:5208
    [Google Scholar]
  3. 3.
    Bharat TAM, Davey NE, Ulbrich P, Riches JD, de Marco A et al. 2012. Structure of the immature retroviral capsid at 8 Å resolution by cryo-electron microscopy. Nature 487:385–89
    [Google Scholar]
  4. 4.
    Bharat TAM, Russo CJ, Lowe J, Passmore LA, Scheres SHW. 2015. Advances in single-particle electron cryomicroscopy structure determination applied to sub-tomogram averaging. Structure 23:1743–53
    [Google Scholar]
  5. 5.
    Bieber A, Capitanio C, Schiøtz O, Smeets M, Fenzke J et al. 2021. Precise 3D-correlative FIB-milling of biological samples using METEOR, an integrated cryo-CLEM imaging system. Microsc. Microanal. 27:3230–32
    [Google Scholar]
  6. 6.
    Bohning J, Bharat TAM, Collins SM. 2022. Compressed sensing for electron cryotomography and high-resolution subtomogram averaging of biological specimens. Structure 30:408–17.e4
    [Google Scholar]
  7. 7.
    Bouvette J, Liu H-F, Du X, Zhou Y, Sikkema AP et al. 2021. Beam image-shift accelerated data acquisition for near-atomic resolution single-particle cryo-electron tomography. Nat. Commun. 12:1957
    [Google Scholar]
  8. 8.
    Burt A, Gaifas L, Dendooven T, Gutsche I. 2021. A flexible framework for multi-particle refinement in cryo-electron tomography. PLOS Biol. 19:e3001319
    [Google Scholar]
  9. 9.
    Calder LJ, Rosenthal PB. 2016. Cryomicroscopy provides structural snapshots of influenza virus membrane fusion. Nat. Struct. Mol. Biol. 23:853–58
    [Google Scholar]
  10. 10.
    Castaño-Díez D, Kudryashev M, Arheit M, Stahlberg H. 2012. Dynamo: a flexible, user-friendly development tool for subtomogram averaging of cryo-EM data in high-performance computing environments. J. Struct. Biol. 178:139–51
    [Google Scholar]
  11. 11.
    Chaikeeratisak V, Khanna K, Nguyen KT, Egan ME, Enustun E et al. 2022. Subcellular organization of viral particles during maturation of nucleus-forming jumbo phage. Sci. Adv. 8:eabj9670
    [Google Scholar]
  12. 12.
    Chaikeeratisak V, Khanna K, Nguyen KT, Sugie J, Egan ME et al. 2019. Viral capsid trafficking along treadmilling tubulin filaments in bacteria. Cell 177:1771–80.e12
    [Google Scholar]
  13. 13.
    Chaikeeratisak V, Nguyen K, Khanna K, Brilot AF, Erb ML et al. 2017. Assembly of a nucleus-like structure during viral replication in bacteria. Science 355:194–97
    [Google Scholar]
  14. 14.
    Chen M, Bell JM, Shi X, Sun SY, Wang Z, Ludtke SJ 2019. A complete data processing workflow for cryo-ET and subtomogram averaging. Nat. Methods 16:1161–68
    [Google Scholar]
  15. 15.
    Chen M, Dai W, Sun SY, Jonasch D, He CY et al. 2017. Convolutional neural networks for automated annotation of cellular cryo-electron tomograms. Nat. Methods 14:983–85
    [Google Scholar]
  16. 16.
    Chlanda P, Mekhedov E, Waters H, Schwartz CL, Fischer ER et al. 2016. The hemifusion structure induced by influenza virus haemagglutinin is determined by physical properties of the target membranes. Nat. Microbiol. 1:16050
    [Google Scholar]
  17. 17.
    Chmielewski D, Schmid MF, Simmons G, Jin J, Chiu W 2022. Chikungunya virus assembly and budding visualized in situ using cryogenic electron tomography. Nat. Microbiol. 7:1270–79
    [Google Scholar]
  18. 18.
    Chreifi G, Chen S, Metskas LA, Kaplan M, Jensen GJ. 2019. Rapid tilt-series acquisition for electron cryotomography. J. Struct. Biol. 205:163–69
    [Google Scholar]
  19. 19.
    Dahlberg PD, Moerner WE. 2021. Cryogenic super-resolution fluorescence and electron microscopy correlated at the nanoscale. Annu. Rev. Phys. Chem. 72:253–78
    [Google Scholar]
  20. 20.
    Deng YC, Chen Y, Zhang Y, Wang SL, Zhang F, Sun F. 2016. ICON: 3D reconstruction with “missing-information” restoration in biological electron tomography. J. Struct. Biol. 195:100–12
    [Google Scholar]
  21. 21.
    Eibauer M, Hoffmann C, Plitzko JM, Baumeister W, Nickell S, Engelhardt H. 2012. Unraveling the structure of membrane proteins in situ by transfer function corrected cryo-electron tomography. J. Struct. Biol. 180:488–96
    [Google Scholar]
  22. 22.
    Eisenstein F, Danev R, Pilhofer M. 2019. Improved applicability and robustness of fast cryo-electron tomography data acquisition. J. Struct. Biol. 208:107–14
    [Google Scholar]
  23. 23.
    Eisenstein F, Yanagisawa H, Kashihara H, Kikkawa M, Tsukita S, Danev R. 2023. Parallel cryo electron tomography on in situ lamellae. Nat. Methods 20131–38
  24. 24.
    El Omari K, Li S, Kotecha A, Walter TS, Bignon EA et al. 2019. The structure of a prokaryotic viral envelope protein expands the landscape of membrane fusion proteins. Nat. Commun. 10:846
    [Google Scholar]
  25. 25.
    Engel L, Vasquez CG, Montabana EA, Sow BM, Walkiewicz MP et al. 2021. Lattice micropatterning for cryo-electron tomography studies of cell-cell contacts. J. Struct. Biol. 213:107791
    [Google Scholar]
  26. 26.
    Ertel KJ, Benefield D, Castaño-Diez D, Pennington JG, Horswill M et al. 2017. Cryo-electron tomography reveals novel features of a viral RNA replication compartment. eLife 6:e25940
    [Google Scholar]
  27. 27.
    Etibor TA, Yamauchi Y, Amorim MJ. 2021. Liquid biomolecular condensates and viral lifecycles: review and perspectives. Viruses 13:366
    [Google Scholar]
  28. 28.
    Farley MM, Tu J, Kearns DB, Molineux IJ, Liu J. 2017. Ultrastructural analysis of bacteriophage Φ29 during infection of Bacillus subtilis. J. Struct. Biol. 197:163–71
    [Google Scholar]
  29. 29.
    Fernandez JJ, Li S 2021. TomoAlign: a novel approach to correcting sample motion and 3D CTF in cryoET. J. Struct. Biol. 213:107778
    [Google Scholar]
  30. 30.
    Fernandez JJ, Li S, Agard DA. 2019. Consideration of sample motion in cryo-tomography based on alignment residual interpolation. J. Struct. Biol. 205:1–6
    [Google Scholar]
  31. 31.
    Fernandez JJ, Li S, Bharat TAM, Agard DA. 2018. Cryo-tomography tilt-series alignment with consideration of the beam-induced sample motion. J. Struct. Biol. 202:200–9
    [Google Scholar]
  32. 32.
    Fernandez JJ, Li S, Crowther RA. 2006. CTF determination and correction in electron cryotomography. Ultramicroscopy 106:587–96
    [Google Scholar]
  33. 33.
    Gui L, Ebner JL, Mileant A, Williams JA, Lee KK. 2016. Visualization and sequencing of membrane remodeling leading to influenza virus fusion. J. Virol. 90:6948–62
    [Google Scholar]
  34. 34.
    Hagen C, Dent KC, Zeev-Ben-Mordehai T, Grange M, Bosse JB et al. 2015. Structural basis of vesicle formation at the inner nuclear membrane. Cell 163:1692–701
    [Google Scholar]
  35. 35.
    Hagen WJH, Wan W, Briggs JAG. 2017. Implementation of a cryo-electron tomography tilt-scheme optimized for high resolution subtomogram averaging. J. Struct. Biol. 197:191–98
    [Google Scholar]
  36. 36.
    Halldorsson S, Li S, Li M, Harlos K, Bowden TA, Huiskonen JT. 2018. Shielding and activation of a viral membrane fusion protein. Nat. Commun. 9:349
    [Google Scholar]
  37. 37.
    Harastani M, Eltsov M, Leforestier A, Jonic S. 2021. HEMNMA-3D: cryo electron tomography method based on normal mode analysis to study continuous conformational variability of macromolecular complexes. Front. Mol. Biosci. 8:663121
    [Google Scholar]
  38. 38.
    Harastani M, Eltsov M, Leforestier A, Jonic S. 2022. TomoFlow: analysis of continuous conformational variability of macromolecules in cryogenic subtomograms based on 3D dense optical flow. J. Mol. Biol. 434:167381
    [Google Scholar]
  39. 39.
    Hart RG. 1968. Electron microscopy of unstained biological material: the polytropic montage. Science 159:1464–67
    [Google Scholar]
  40. 40.
    Hauser M, Wojcik M, Kim D, Mahmoudi M, Li W, Xu K. 2017. Correlative super-resolution microscopy: new dimensions and new opportunities. Chem. Rev. 117:7428–56
    [Google Scholar]
  41. 41.
    Heinrich BS, Maliga Z, Stein DA, Hyman AA, Whelan SPJ. 2018. Phase transitions drive the formation of vesicular stomatitis virus replication compartments. mBio 9:e02290–17
    [Google Scholar]
  42. 42.
    Herrmann T, Torres R, Salgado EN, Berciu C, Stoddard D et al. 2021. Functional refolding of the penetration protein on a non-enveloped virus. Nature 590:666–70
    [Google Scholar]
  43. 43.
    Himes BA, Zhang P. 2018. emClarity: software for high-resolution cryo-electron tomography and subtomogram averaging. Nat. Methods 15:955–61
    [Google Scholar]
  44. 44.
    Hu B, Margolin W, Molineux IJ, Liu J. 2013. The bacteriophage T7 virion undergoes extensive structural remodeling during infection. Science 339:576–79
    [Google Scholar]
  45. 45.
    Hu B, Margolin W, Molineux IJ, Liu J. 2015. Structural remodeling of bacteriophage T4 and host membranes during infection initiation. PNAS 112:E4919–28
    [Google Scholar]
  46. 46.
    Jensen GJ, Kornberg RD. 2000. Defocus-gradient corrected back-projection. Ultramicroscopy 84:57–64
    [Google Scholar]
  47. 47.
    Jiang Z, Jin X, Li Y, Liu S, Liu XM et al. 2020. Genetically encoded tags for direct synthesis of EM-visible gold nanoparticles in cells. Nat. Methods 17:937–46
    [Google Scholar]
  48. 48.
    Jiménez de la Morena J, Conesa P, Fonseca YC, de Isidro-Gómez FP, Herreros D et al. 2022. ScipionTomo: towards cryo-electron tomography software integration, reproducibility, and validation. J. Struct. Biol. 214:107872
    [Google Scholar]
  49. 49.
    Jin J, Liss NM, Chen DH, Liao M, Fox JM et al. 2015. Neutralizing monoclonal antibodies block chikungunya virus entry and release by targeting an epitope critical to viral pathogenesis. Cell Rep. 13:2553–64
    [Google Scholar]
  50. 50.
    Jonker C, Boltje D, Hoogenboom J, Jakobi A, Jensen G et al. 2021. Fluorescence-guided lamella fabrication with ENZEL, an integrated cryogenic CLEM solution for the cryo-electron tomography workflow. Microsc. Microanal. 27:3234–35
    [Google Scholar]
  51. 51.
    Ke Z, Oton J, Qu K, Cortese M, Zila V et al. 2020. Structures and distributions of SARS-CoV-2 spike proteins on intact virions. Nature 588:498–502
    [Google Scholar]
  52. 52.
    Ke Z, Strauss JD, Hampton CM, Brindley MA, Dillard RS et al. 2018. Promotion of virus assembly and organization by the measles virus matrix protein. Nat. Commun. 9:1736
    [Google Scholar]
  53. 53.
    Kelley K, Raczkowski AM, Klykov O, Jaroenlak P, Bobe D et al. 2022. Waffle method: a general and flexible approach for improving throughput in FIB-milling. Nat. Commun. 13:1857
    [Google Scholar]
  54. 54.
    Khavnekar S, Wan W, Majumder P, Wietrzynski W, Erdmann PS, Plitzko JM. 2023. Multishot tomography for high-resolution in situ subtomogram averaging. J. Struct. Biol 215107911
  55. 55.
    Kimanius D, Dong L, Sharov G, Nakane T, Scheres SHW. 2021. New tools for automated cryo-EM single-particle analysis in RELION-4.0. Biochem. J. 478:4169–85
    [Google Scholar]
  56. 56.
    Klein S, Cortese M, Winter SL, Wachsmuth-Melm M, Neufeldt CJ et al. 2020. SARS-CoV-2 structure and replication characterized by in situ cryo-electron tomography. Nat. Commun. 11:5885
    [Google Scholar]
  57. 57.
    Knoops K, Kikkert M, van den Worm SHE, Zevenhoven-Dobbe JC, van der Meer Y et al. 2008. SARS-coronavirus replication is supported by a reticulovesicular network of modified endoplasmic reticulum. PLOS Biol. 6:e226
    [Google Scholar]
  58. 58.
    Kopek BG, Perkins G, Miller DJ, Ellisman MH, Ahlquist P. 2007. Three-dimensional analysis of a viral RNA replication complex reveals a virus-induced mini-organelle. PLOS Biol. 5:e220
    [Google Scholar]
  59. 59.
    Laughlin TG, Deep A, Prichard AM, Seitz C, Gu Y et al. 2022. Architecture and self-assembly of the jumbo bacteriophage nuclear shell. Nature 608:429–35
    [Google Scholar]
  60. 60.
    Laurent T, Kumar P, Liese S, Zare F, Jonasson M et al. 2022. Architecture of the chikungunya virus replication organelle. eLife 11e83042
  61. 61.
    Lee KK. 2010. Architecture of a nascent viral fusion pore. EMBO J. 29:1299–311
    [Google Scholar]
  62. 62.
    Leiman PG, Chipman PR, Kostyuchenko VA, Mesyanzhinov VV, Rossmann MG. 2004. Three-dimensional rearrangement of proteins in the tail of bacteriophage T4 on infection of its host. Cell 118:419–29
    [Google Scholar]
  63. 63.
    Li S. 2022. Cryo-electron tomography of enveloped viruses. Trends Biochem. Sci. 47:173–86
    [Google Scholar]
  64. 64.
    Li S, Sun Z, Pryce R, Parsy ML, Fehling SK et al. 2016. Acidic pH-induced conformations and LAMP1 binding of the Lassa virus glycoprotein spike. PLOS Pathog. 12:e1005418
    [Google Scholar]
  65. 65.
    Li X, Mooney P, Zheng S, Booth CR, Braunfeld MB et al. 2013. Electron counting and beam-induced motion correction enable near-atomic-resolution single-particle cryo-EM. Nat. Methods 10:584–90
    [Google Scholar]
  66. 66.
    Li Z, Li W, Lu M, Bess J Jr., Chao CW et al. 2020. Subnanometer structures of HIV-1 envelope trimers on aldrithiol-2-inactivated virus particles. Nat. Struct. Mol. Biol. 27:726–34
    [Google Scholar]
  67. 67.
    Liu J, Bartesaghi A, Borgnia MJ, Sapiro G, Subramaniam S. 2008. Molecular architecture of native HIV-1 gp120 trimers. Nature 455:109–13
    [Google Scholar]
  68. 68.
    Liu Y-T, Zhang H, Wang H, Tao C-L, Bi G-Q, Zhou ZH. 2022. Isotropic reconstruction for electron tomography with deep learning. Nat. Commun 136482
  69. 69.
    Mangala Prasad V, Blijleven JS, Smit JM, Lee KK 2022. Visualization of conformational changes and membrane remodeling leading to genome delivery by viral class-II fusion machinery. Nat. Commun 134772
  70. 70.
    Mangala Prasad V, Leaman DP, Lovendahl KN, Croft JT, Benhaim MA et al. 2022. Cryo-ET of Env on intact HIV virions reveals structural variation and positioning on the Gag lattice. Cell 185:641–53.e17
    [Google Scholar]
  71. 71.
    Marko M, Hsieh C, Schalek R, Frank J, Mannella C. 2007. Focused-ion-beam thinning of frozen-hydrated biological specimens for cryo-electron microscopy. Nat. Methods 4:215–17
    [Google Scholar]
  72. 72.
    Martell JD, Deerinck TJ, Sancak Y, Poulos TL, Mootha VK et al. 2012. Engineered ascorbate peroxidase as a genetically encoded reporter for electron microscopy. Nat. Biotechnol. 30:1143–48
    [Google Scholar]
  73. 73.
    Mastronarde DN, Held SR. 2017. Automated tilt series alignment and tomographic reconstruction in IMOD. J. Struct. Biol. 197:102–13
    [Google Scholar]
  74. 74.
    Mattei S, Glass B, Hagen WJH, Kräusslich H-G, Briggs JAG. 2016. The structure and flexibility of conical HIV-1 capsids determined within intact virions. Science 354:1434–37
    [Google Scholar]
  75. 75.
    Mattei S, Tan A, Glass B, Müller B, Kräusslich H-G, Briggs JAG. 2018. High-resolution structures of HIV-1 Gag cleavage mutants determine structural switch for virus maturation. PNAS 115:E9401–10
    [Google Scholar]
  76. 76.
    Mendonça L, Howe A, Gilchrist JB, Sheng Y, Sun D et al. 2021. Correlative multi-scale cryo-imaging unveils SARS-CoV-2 assembly and egress. Nat. Commun. 12:4629
    [Google Scholar]
  77. 77.
    Mendonça L, Sun D, Ning J, Liu J, Kotecha A et al. 2021. CryoET structures of immature HIV Gag reveal six-helix bundle. Commun. Biol. 4:481
    [Google Scholar]
  78. 78.
    Miller S, Krijnse-Locker J. 2008. Modification of intracellular membrane structures for virus replication. Nat. Rev. Microbiol. 6:363–74
    [Google Scholar]
  79. 79.
    Mindell JA, Grigorieff N. 2003. Accurate determination of local defocus and specimen tilt in electron microscopy. J. Struct. Biol. 142:334–47
    [Google Scholar]
  80. 80.
    Moebel E, Martinez-Sanchez A, Lamm L, Righetto RD, Wietrzynski W et al. 2021. Deep learning improves macromolecule identification in 3D cellular cryo-electron tomograms. Nat. Methods 18:1386–94
    [Google Scholar]
  81. 81.
    Nguyen N, Bohak C, Engel D, Mindek P, Strnad O et al. 2022. Finding nano-Ötzi: cryo-electron tomography visualization guided by learned segmentation. IEEE Trans. Vis. Comput. Graph. In press
    [Google Scholar]
  82. 82.
    Ni T, Zhu Y, Yang Z, Xu C, Chaban Y et al. 2021. Structure of native HIV-1 cores and their interactions with IP6 and CypA. Sci. Adv. 7:eabj5715
    [Google Scholar]
  83. 83.
    Obr M, Hagen WJH, Dick RA, Yu L, Kotecha A, Schur FKM. 2022. Exploring high-resolution cryo-ET and subtomogram averaging capabilities of contemporary DEDs. J. Struct. Biol. 214:107852
    [Google Scholar]
  84. 84.
    Peck A, Carter SD, Mai H, Chen S, Burt A, Jensen GJ. 2022. Montage electron tomography of vitrified specimens. J. Struct. Biol. 214:107860
    [Google Scholar]
  85. 85.
    Peukes J, Xiong X, Erlendsson S, Qu K, Wan W et al. 2020. The native structure of the assembled matrix protein 1 of influenza A virus. Nature 587:495–98
    [Google Scholar]
  86. 86.
    Qu K, Ke Z, Zila V, Anders-Össwein M, Glass B et al. 2021. Maturation of the matrix and viral membrane of HIV-1. Science 373:700–4
    [Google Scholar]
  87. 87.
    Quemin ERJ, Machala EA, Vollmer B, Prazak V, Vasishtan D et al. 2020. Cellular electron cryo-tomography to study virus-host interactions. Annu. Rev. Virol. 7:239–62
    [Google Scholar]
  88. 88.
    Rice G, Wagner T, Stabrin M, Raunser S. 2022. TomoTwin: generalized 3D localization of macromolecules in cryo-electron tomograms with structural data mining. bioRxiv 2022.06.24.497279. https://doi.org/10.1101/2022.06.24.497279
  89. 89.
    Ruska H, von Borries B, Ruska E. 1939. Die Bedeutung der Übermikroskopie für die Virusforschung. Arch. Gesamte Virusforsch. 1:155–69
    [Google Scholar]
  90. 90.
    Saibil HR. 2022. Cryo-EM in molecular and cellular biology. Mol. Cell 82:274–84
    [Google Scholar]
  91. 91.
    Sanchez RM, Zhang Y, Chen W, Dietrich L, Kudryashev M. 2020. Subnanometer-resolution structure determination in situ by hybrid subtomogram averaging—single particle cryo-EM. Nat. Commun. 11:3709
    [Google Scholar]
  92. 92.
    Scaramuzza S, Castaño-Díez D. 2021. Step-by-step guide to efficient subtomogram averaging of virus-like particles with Dynamo. PLOS Biol. 19:e3001318
    [Google Scholar]
  93. 93.
    Schaffer M, Pfeffer S, Mahamid J, Kleindiek S, Laugks T et al. 2019. A cryo-FIB lift-out technique enables molecular-resolution cryo-ET within native Caenorhabditis elegans tissue. Nat. Methods 16:757–62
    [Google Scholar]
  94. 94.
    Schorb M, Haberbosch I, Hagen WJH, Schwab Y, Mastronarde DN. 2019. Software tools for automated transmission electron microscopy. Nat. Methods 16:471–77
    [Google Scholar]
  95. 95.
    Schur FKM, Obr M, Hagen WJH, Wan W, Jakobi AJ et al. 2016. An atomic model of HIV-1 capsid-SP1 reveals structures regulating assembly and maturation. Science 353:506–8
    [Google Scholar]
  96. 96.
    Schur FKM, Hagen WJH, de Marco A, Briggs JAG. 2013. Determination of protein structure at 8.5 Å resolution using cryo-electron tomography and sub-tomogram averaging. J. Struct. Biol. 184:394–400
    [Google Scholar]
  97. 97.
    Schur FKM, Hagen WJH, Rumlová M, Ruml T, Müller B et al. 2015. Structure of the immature HIV-1 capsid in intact virus particles at 8.8 Å resolution. Nature 517:505–8
    [Google Scholar]
  98. 98.
    Si Z, Zhou K, Tsao J, Luo M, Zhou ZH. 2022. Locations and in situ structure of the polymerase complex inside the virion of vesicular stomatitis virus. PNAS 119:e2111948119
    [Google Scholar]
  99. 99.
    Sibert BS, Kim JY, Yang JE, Wright ER. 2021. Whole-cell cryo-electron tomography of cultured and primary eukaryotic cells on micropatterned TEM grids. bioRxiv 2021.06.06.447251. https://doi.org/10.1101/2021.06.06.447251
  100. 100.
    Silvester E, Vollmer B, Prazak V, Vasishtan D, Machala EA et al. 2021. DNA origami signposts for identifying proteins on cell membranes by electron cryotomography. Cell 184:1110–21.e16
    [Google Scholar]
  101. 101.
    Singla J, White KL, Stevens RC, Alber F. 2021. Assessment of scoring functions to rank the quality of 3D subtomogram clusters from cryo-electron tomography. J. Struct. Biol. 213:107727
    [Google Scholar]
  102. 102.
    Song K, Shang Z, Fu X, Lou X, Grigorieff N, Nicastro D. 2020. In situ structure determination at nanometer resolution using TYGRESS. Nat. Methods 17:201–8
    [Google Scholar]
  103. 103.
    Song Y, Yao H, Wu N, Xu J, Zhang Z et al. 2022. In situ architecture and membrane fusion of SARS-CoV-2 Delta variant. bioRxiv 2022.05.13.491759. https://doi.org/10.1101/2022.05.13.491759
  104. 104.
    Su JM, Wilson MZ, Samuel CE, Ma D. 2021. Formation and function of liquid-like viral factories in negative-sense single-stranded RNA virus infections. Viruses 13:126
    [Google Scholar]
  105. 105.
    Sutton G, Sun DP, Fu XF, Kotecha A, Hecksel CW et al. 2020. Assembly intermediates of orthoreovirus captured in the cell. Nat. Commun. 11:4445
    [Google Scholar]
  106. 106.
    Tacke S, Erdmann P, Wang Z, Klumpe S, Grange M et al. 2021. A streamlined workflow for automated cryo focused ion beam milling. J. Struct. Biol. 213:107743
    [Google Scholar]
  107. 107.
    Tan A, Pak AJ, Morado DR, Voth GA, Briggs JAG. 2021. Immature HIV-1 assembles from Gag dimers leaving partial hexamers at lattice edges as potential substrates for proteolytic maturation. PNAS 118:e2020054118
    [Google Scholar]
  108. 108.
    Tan YB, Chmielewski D, Law MCY, Zhang K, He Y et al. 2022. Molecular architecture of the chikungunya virus replication complex. Sci. Adv 8eadd2536
  109. 109.
    Tegunov D, Cramer P. 2019. Real-time cryo-electron microscopy data preprocessing with Warp. Nat. Methods 16:1146–52
    [Google Scholar]
  110. 110.
    Tegunov D, Xue L, Dienemann C, Cramer P, Mahamid J. 2021. Multi-particle cryo-EM refinement with M visualizes ribosome-antibiotic complex at 3.5 Å in cells. Nat. Methods 18:186–93
    [Google Scholar]
  111. 111.
    Toro-Nahuelpan M, Zagoriy I, Senger F, Blanchoin L, Thery M, Mahamid J. 2020. Tailoring cryo-electron microscopy grids by photo-micropatterning for in-cell structural studies. Nat. Methods 17:50–54
    [Google Scholar]
  112. 112.
    Turoňová B, Hagen WJH, Obr M, Mosalaganti S, Beugelink JW et al. 2020. Benchmarking tomographic acquisition schemes for high-resolution structural biology. Nat. Commun. 11:876
    [Google Scholar]
  113. 113.
    Turoňová B, Marsalek L, Slusallek P. 2016. On geometric artifacts in cryo electron tomography. Ultramicroscopy 163:48–61
    [Google Scholar]
  114. 114.
    Turoňová B, Schur FKM, Wan W, Briggs JAG. 2017. Efficient 3D-CTF correction for cryo-electron tomography using NovaCTF improves subtomogram averaging resolution to 3.4 Å. J. Struct. Biol. 199:187–95
    [Google Scholar]
  115. 115.
    Turoňová B, Sikora M, Christoph S, Hagen WJH, Welsch S et al. 2020. In situ structural analysis of SARS-CoV-2 spike reveals flexibility mediated by three hinges. Science 370:203–8
    [Google Scholar]
  116. 116.
    Unchwaniwala N, Zhan H, Pennington J, Horswill M, den Boon JA, Ahlquist P. 2020. Subdomain cryo-EM structure of nodaviral replication protein A crown complex provides mechanistic insights into RNA genome replication. PNAS 117:18680–91
    [Google Scholar]
  117. 117.
    Vijayakrishnan S, McElwee M, Loney C, Rixon F, Bhella D. 2020. In situ structure of virus capsids within cell nuclei by correlative light and cryo-electron tomography. Sci. Rep. 10:17596
    [Google Scholar]
  118. 118.
    Wan W, Kolesnikova L, Clarke M, Koehler A, Noda T et al. 2017. Structure and assembly of the Ebola virus nucleocapsid. Nature 551:394–97
    [Google Scholar]
  119. 119.
    Wang C, Tu J, Liu J, Molineux IJ. 2019. Structural dynamics of bacteriophage P22 infection initiation revealed by cryo-electron tomography. Nat. Microbiol. 4:1049–56
    [Google Scholar]
  120. 120.
    Ward AE, Kiessling V, Pornillos O, White JM, Ganser-Pornillos BK, Tamm LK 2020. HIV-cell membrane fusion intermediates are restricted by Serincs as revealed by cryo-electron and TIRF microscopy. J. Biol. Chem. 295:15183–95
    [Google Scholar]
  121. 121.
    Wieland J, Frey S, Rupp U, Essbauer S, Groß R et al. 2021. Zika virus replication in glioblastoma cells: Electron microscopic tomography shows 3D arrangement of endoplasmic reticulum, replication organelles, and viral ribonucleoproteins. Histochem. Cell Biol. 156:527–38
    [Google Scholar]
  122. 122.
    Winter SL, Chlanda P. 2021. Dual-axis volta phase plate cryo-electron tomography of Ebola virus-like particles reveals actin-VP40 interactions. J. Struct. Biol. 213:107742
    [Google Scholar]
  123. 123.
    Wolff G, Limpens RWAL, Zevenhoven-Dobbe JC, Laugks U, Zheng S et al. 2020. A molecular pore spans the double membrane of the coronavirus replication organelle. Science 369:1395–98
    [Google Scholar]
  124. 124.
    Wu G-H, Mitchell PG, Galaz-Montoya JG, Hecksel CW, Sontag EM et al. 2020. Multi-scale 3D cryo-correlative microscopy for vitrified cells. Structure 28:1231–37.e3
    [Google Scholar]
  125. 125.
    Xia X, Wu W, Cui Y, Roy P, Zhou ZH 2021. Bluetongue virus capsid protein VP5 perforates membranes at low endosomal pH during viral entry. Nat. Microbiol. 6:1424–32
    [Google Scholar]
  126. 126.
    Xiong Q, Morphew MK, Schwartz CL, Hoenger AH, Mastronarde DN. 2009. CTF determination and correction for low dose tomographic tilt series. J. Struct. Biol. 168:378–87
    [Google Scholar]
  127. 127.
    Yan R, Venkatakrishnan SV, Liu J, Bouman CA, Jiang W. 2019. MBIR: a cryo-ET 3D reconstruction method that effectively minimizes missing wedge artifacts and restores missing information. J. Struct. Biol. 206:183–92
    [Google Scholar]
  128. 128.
    Yang JE, Larson MR, Sibert BS, Kim JY, Parrell D et al. 2022. Correlative cryogenic montage electron tomography for comprehensive in-situ whole-cell structural studies. bioRxiv 2021.12.31.474669. https://doi.org/10.1101/2021.12.31.474669
  129. 129.
    Yao H, Song Y, Chen Y, Wu N, Xu J et al. 2020. Molecular architecture of the SARS-CoV-2 virus. Cell 183:730–38.e13
    [Google Scholar]
  130. 130.
    Zanetti G, Briggs JAG, Grünewald KS, Quentin J, Fuller SD 2006. Cryo-electron tomographic structure of an immunodeficiency virus envelope complex in situ. PLOS Pathog. 2:e83
    [Google Scholar]
  131. 131.
    Zanetti G, Riches JD, Fuller SD, Briggs JAG. 2009. Contrast transfer function correction applied to cryo-electron tomography and sub-tomogram averaging. J. Struct. Biol. 168:305–12
    [Google Scholar]
  132. 132.
    Zhang X, Sridharan S, Zagoriy I, Oegema CE, Ching C et al. 2022. Molecular mechanisms of stress-induced reactivation in mumps virus condensates. bioRxiv 2021.07.10.451879. https://doi.org/10.1101/2021.07.10.451879
  133. 133.
    Zhang Y, Li S, Zeng C, Huang G, Zhu X et al. 2020. Molecular architecture of the luminal ring of the Xenopus laevis nuclear pore complex. Cell Res. 30:532–40
    [Google Scholar]
  134. 134.
    Zhao G, Perilla JR, Yufenyuy EL, Meng X, Chen B et al. 2013. Mature HIV-1 capsid structure by cryo-electron microscopy and all-atom molecular dynamics. Nature 497:643–46
    [Google Scholar]
  135. 135.
    Zheng S, Wolff G, Greenan G, Chen Z, Faas FGA et al. 2022. AreTomo: an integrated software package for automated marker-free, motion-corrected cryo-electron tomographic alignment and reconstruction. J. Struct. Biol. X 6:100068
    [Google Scholar]
  136. 136.
    Zheng SQ, Palovcak E, Armache JP, Verba KA, Cheng Y, Agard DA. 2017. MotionCor2: anisotropic correction of beam-induced motion for improved cryo-electron microscopy. Nat. Methods 14:331–32
    [Google Scholar]
  137. 137.
    Zhou Y, Su JM, Samuel CE, Ma D. 2019. Measles virus forms inclusion bodies with properties of liquid organelles. J. Virol. 93:e00948–19
    [Google Scholar]
  138. 138.
    Zhu H, Li M, Zhao R, Li M, Chai Y et al. 2022. In situ structure of intestinal apical surface reveals nanobristles on microvilli. PNAS 119:e2122249119
    [Google Scholar]
  139. 139.
    Zila V, Margiotta E, Turoňová B, Müller TG, Zimmerli CE et al. 2021. Cone-shaped HIV-1 capsids are transported through intact nuclear pores. Cell 184:1032–46.e18
    [Google Scholar]
  140. 140.
    Zivanov J, Otón J, Ke Z, von Kügelgen A, Pyle E et al. 2022. A Bayesian approach to single-particle electron cryo-tomography in RELION-4.0. eLife 11e83724
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