1932

Abstract

The preparation of extremely thin samples, which are required for high-resolution electron microscopy, poses extreme risk of damaging biological macromolecules due to interactions with the air-water interface. Although the rapid increase in the number of published structures initially gave little indication that this was a problem, the search for methods that substantially mitigate this hazard is now intensifying. The two main approaches under investigation are () immobilizing particles onto structure-friendly support films and () reducing the length of time during which such interactions may occur. While there is little possibility of outrunning diffusion to the interface, intentional passivation of the interface may slow the process of adsorption and denaturation. In addition, growing attention is being given to gaining more effective control of the thickness of the sample prior to vitrification.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-biochem-072020-020231
2021-06-20
2024-06-23
Loading full text...

Full text loading...

/deliver/fulltext/biochem/90/1/annurev-biochem-072020-020231.html?itemId=/content/journals/10.1146/annurev-biochem-072020-020231&mimeType=html&fmt=ahah

Literature Cited

  1. 1. 
    Glaeser RM. 2013. Stroboscopic imaging of macromolecular complexes. Nat. Methods 10:475–76
    [Google Scholar]
  2. 2. 
    Bai X-C, Fernandez IS, McMullan G, Scheres SHW 2013. Ribosome structures to near-atomic resolution from thirty thousand cryo-EM particles. eLife 2:e00461
    [Google Scholar]
  3. 3. 
    Li XM, 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]
  4. 4. 
    Nogales E, Scheres SHW. 2015. Cryo-EM: a unique tool for the visualization of macromolecular complexity. Mol. Cell 58:677–89
    [Google Scholar]
  5. 5. 
    Scheres SHW, Gao HX, Valle M, Herman GT, Eggermont PPB et al. 2007. Disentangling conformational states of macromolecules in 3D-EM through likelihood optimization. Nat. Methods 4:27–29
    [Google Scholar]
  6. 6. 
    Nogales E. 2016. The development of cryo-EM into a mainstream structural biology technique. Nat. Methods 13:24–27
    [Google Scholar]
  7. 7. 
    Zhou R, Yang GH, Guo XF, Zhou Q, Lei JL, Shi YG. 2019. Recognition of the amyloid precursor protein by human γ-secretase. Science 363:eaaw0930
    [Google Scholar]
  8. 8. 
    Rae CD, Gordiyenko Y, Ramakrishnan V. 2019. How a circularized tmRNA moves through the ribosome. Science 363:740–44
    [Google Scholar]
  9. 9. 
    Ehara H, Kujirai T, Fujino Y, Shirouzu M, Kurumizaka H, Sekine S. 2019. Structural insight into nucleosome transcription by RNA polymerase II with elongation factors. Science 363:744–47
    [Google Scholar]
  10. 10. 
    Fica SM, Oubridge C, Wilkinson ME, Newman AJ, Nagai K. 2019. A human postcatalytic spliceosome structure reveals essential roles of metazoan factors for exon ligation. Science 363:710–14
    [Google Scholar]
  11. 11. 
    Alam A, Kowal J, Broude E, Roninson I, Locher KP. 2019. Structural insight into substrate and inhibitor discrimination by human P-glycoprotein. Science 363:753–56
    [Google Scholar]
  12. 12. 
    Nakane T, Kotecha A, Sente A, McMullan G, Masiulis S et al. 2020. Single-particle cryo-EM at atomic resolution. Nature 587:152–56
    [Google Scholar]
  13. 13. 
    Yip KM, Fischer N, Paknia E, Chari A, Stark H. 2020. Atomic-resolution protein structure determination by cryo-EM. Nature 587:157–61
    [Google Scholar]
  14. 14. 
    Wu M, Lander GC. 2020. How low can we go? Structure determination of small biological complexes using single-particle cryo-EM. Curr. Opin. Struct. Biol. 64:9–16
    [Google Scholar]
  15. 15. 
    Dashti A, Schwander P, Langlois R, Fung R, Li W et al. 2014. Trajectories of the ribosome as a Brownian nanomachine. PNAS 111:17492–97
    [Google Scholar]
  16. 16. 
    Frank J. 2017. Time-resolved cryo-electron microscopy: recent progress. J. Struct. Biol. 200:303–6
    [Google Scholar]
  17. 17. 
    Dandey VP, Budell WC, Wei H, Bobe D, Maruthi K et al. 2020. Time-resolved cryo-EM using Spotiton. Nature Methods 17:897–900
    [Google Scholar]
  18. 18. 
    Crowther RA. 2016. Preface. Methods Enzymol. 579:xiii–xx
    [Google Scholar]
  19. 19. 
    Danev R, Yanagisawa H, Kikkawa M. 2019. Cryo-electron microscopy methodology: current aspects and future directions. Trends Biochem. Sci. 44:837–48
    [Google Scholar]
  20. 20. 
    Fernandez-Leiro R, Scheres SHW. 2016. Unravelling biological macromolecules with cryo-electron microscopy. Nature 537:339–46
    [Google Scholar]
  21. 21. 
    Cheng Y, Grigorieff N, Penczek PA, Walz T. 2015. A primer to single-particle cryo-electron microscopy. Cell 161:438–49
    [Google Scholar]
  22. 22. 
    Milne JLS, Borgnia MJ, Bartesaghi A, Tran EEH, Earl LA et al. 2013. Cryo-electron microscopy—a primer for the non-microscopist. FEBS J 280:28–45
    [Google Scholar]
  23. 23. 
    Carragher B, Cheng Y, Frost A, Glaeser RM, Lander GC et al. 2019. Current outcomes when optimizing ‘standard’ sample preparation for single-particle cryo-EM. J. Microsc. 276:39–45
    [Google Scholar]
  24. 24. 
    Drulyte I, Johnson RM, Hesketh EL, Hurdiss DL, Scarff CA et al. 2018. Approaches to altering particle distributions in cryo-electron microscopy sample preparation. Acta Crystallogr. D74:560–71
    [Google Scholar]
  25. 25. 
    Klebl DP, Gravett MSC, Kontziampasis D, Wright DJ, Bon RS et al. 2020. Need for speed: examining protein behaviour during cryoEM grid preparation at different timescales. Structure 28:1238–48.e4
    [Google Scholar]
  26. 26. 
    Peet MJ, Henderson R, Russo CJ. 2019. The energy dependence of contrast and damage in electron cryomicroscopy of biological molecules. Ultramicroscopy 203:125–31
    [Google Scholar]
  27. 27. 
    Glaeser RM, Downing K, DeRosier D, Chiu W, Frank J. 2007. Electron Crystallography of Biological Macromolecules Oxford, UK: Oxford Univ. Press
    [Google Scholar]
  28. 28. 
    Taylor KA, Glaeser RM. 2008. Retrospective on the early development of cryoelectron microscopy of macromolecules and a prospective on opportunities for the future. J. Struct. Biol. 163:214–23
    [Google Scholar]
  29. 29. 
    Dubochet J, Adrian M, Chang JJ, Homo JC, Lepault J et al. 1988. Cryo-electron microscopy of vitrified specimens. Q. Rev. Biophys. 21:129–228
    [Google Scholar]
  30. 30. 
    Dobro MJ, Melanson LA, Jensen GJ, McDowall AW. 2010. Plunge freezing for electron cryomicroscopy. Methods Enzymol. 481:63–82
    [Google Scholar]
  31. 31. 
    Russo CJ, Passmore LA. 2016. Ultrastable gold substrates: properties of a support for high-resolution electron cryomicroscopy of biological specimens. J. Struct. Biol. 193:33–44
    [Google Scholar]
  32. 32. 
    Herzik MA Jr., Wu M, Lander GC. 2017. Achieving better-than-3-Å resolution by single-particle cryo-EM at 200 keV. Nat. Methods 14:1075–78
    [Google Scholar]
  33. 33. 
    Naydenova K, Russo CJ. 2017. Measuring the effects of particle orientation to improve the efficiency of electron cryomicroscopy. Nat. Commun. 8:629
    [Google Scholar]
  34. 34. 
    Wikipedia 2020. Affirming the consequent. Wikipedia https://en.wikipedia.org/wiki/Affirming_the_consequent
    [Google Scholar]
  35. 35. 
    Vinothkumar KR, Henderson R. 2016. Single particle electron cryomicroscopy: trends, issues and future perspective. Q. Rev. Biophys. 49:e13
    [Google Scholar]
  36. 36. 
    Bharat TAM, Scheres SHW. 2016. Resolving macromolecular structures from electron cryo-tomography data using subtomogram averaging in RELION. Nat. Protoc. 11:205465
    [Google Scholar]
  37. 37. 
    Noble AJ, Dandey VP, Wei H, Braschi J, Chase J et al. 2018. Routine single particle cryoEM sample and grid characterization by tomography. eLife 7:e34257
    [Google Scholar]
  38. 38. 
    D'Imprima E, Floris D, Joppe M, Sánchez R, Grininger M, Kühlbrandt W 2019. Protein denaturation at the air-water interface and how to prevent it. eLife 8:e42747
    [Google Scholar]
  39. 39. 
    Fan X, Wang J, Zhang X, Yang Z, Zhang J-C et al. 2019. Single particle cryo-EM reconstruction of 52kDa streptavidin at 3.2 Angstrom resolution. Nat. Commun. 10:2386
    [Google Scholar]
  40. 40. 
    Lum K, Chandler D, Weeks JD. 1999. Hydrophobicity at small and large length scales. J. Phys. Chem. B 103:4570–77
    [Google Scholar]
  41. 41. 
    Parker JL, Claesson PM, Attard P. 1994. Bubbles, cavities, and the long-ranged attraction between hydrophobic surfaces. J. Phys. Chem. 98:8468–80
    [Google Scholar]
  42. 42. 
    Glaeser RM, Han B-G. 2017. Hazards faced by macromolecules when confined to thin aqueous films. Biophys. Rep. 3:1–7
    [Google Scholar]
  43. 43. 
    Raffaini G, Ganazzoli F. 2010. Protein adsorption on a hydrophobic surface: a molecular dynamics study of lysozyme on graphite. Langmuir 26:5679–89
    [Google Scholar]
  44. 44. 
    Postel C, Abillon O, Desbat B. 2003. Structure and denaturation of adsorbed lysozyme at the air-water interface. J. Colloid Interface Sci. 266:74–81
    [Google Scholar]
  45. 45. 
    Gidalevitz D, Huang ZQ, Rice SA 1999. Protein folding at the air–water interface studied with x-ray reflectivity. PNAS 96:2608–11
    [Google Scholar]
  46. 46. 
    Yoshimura H, Scheybani T, Baumeister W, Nagayama K. 1994. Two-dimensional protein array growth in thin layers of protein solution on aqueous subphases. Langmuir 10:3290–95
    [Google Scholar]
  47. 47. 
    Glaeser RM. 2018. Proteins, interfaces, and cryo-EM grids. Curr. Opin. Colloid Interface Sci. 34:1–11
    [Google Scholar]
  48. 48. 
    Egelman EH. 2020. Cryo-EM: Ice is nice, but good ice can be hard to find. Biophys. J. 118:1238–39
    [Google Scholar]
  49. 49. 
    Galkin VE, Orlova A, Vos MR, Schroder GF, Egelman EH. 2015. Near-atomic resolution for one state of F-actin. Structure 23:173–82
    [Google Scholar]
  50. 50. 
    Jaspe J, Hagen SJ. 2006. Do protein molecules unfold in a simple shear flow?. Biophys. J. 91:3415–24
    [Google Scholar]
  51. 51. 
    Han B-G, Watson Z, Cate JHD, Glaeser RM. 2017. Monolayer-crystal streptavidin support films provide an internal standard of cryo-EM image quality. J. Struct. Biol. 200:307–13
    [Google Scholar]
  52. 52. 
    Rice WJ, Cheng AC, Noble AJ, Eng ET, Kim LY et al. 2018. Routine determination of ice thickness for cryo-EM grids. J. Struct. Biol. 204:38–44
    [Google Scholar]
  53. 53. 
    Pantelic RS, Meyer JC, Kaiser U, Baumeister W, Plitzko JM. 2010. Graphene oxide: a substrate for optimizing preparations of frozen-hydrated samples. J. Struct. Biol. 170:152–56
    [Google Scholar]
  54. 54. 
    Boland A, Martin TG, Zhang ZG, Yang J, Bai XC et al. 2017. Cryo-EM structure of a metazoan separase-securin complex at near-atomic resolution. Nat. Struct. Mol. Biol. 24:414–18
    [Google Scholar]
  55. 55. 
    Han Y, Fan X, Wang H, Zhao F, Tully CG et al. 2020. High-yield monolayer graphene grids for near-atomic resolution cryoelectron microscopy. PNAS 117:1009–14
    [Google Scholar]
  56. 56. 
    Naydenova K, Peet MJ, Russo CJ 2019. Multifunctional graphene supports for electron cryomicroscopy. PNAS 116:11718–24
    [Google Scholar]
  57. 57. 
    Rafiee J, Mi X, Gullapalli H, Thomas AV, Yavari F et al. 2012. Wetting transparency of graphene. Nat. Mater. 11:217–22
    [Google Scholar]
  58. 58. 
    Kim D, Pugno NM, Buehler MJ, Ryu S. 2015. Solving the controversy on the wetting transparency of graphene. Sci. Rep. 5:15526
    [Google Scholar]
  59. 59. 
    Ghoshal D, Jain R, Koratkar NA. 2019. Graphene's partial transparency to van der Waals and electrostatic interactions. Langmuir 35:12306–16
    [Google Scholar]
  60. 60. 
    Llaguno MC, Xu H, Shi L, Huang N, Zhang H et al. 2014. Chemically functionalized carbon films for single molecule imaging. J. Struct. Biol. 185:405–17
    [Google Scholar]
  61. 61. 
    Liu N, Zhang J, Chen Y, Liu C, Zhang X et al. 2019. Bioactive functionalized monolayer graphene for high-resolution cryo-electron microscopy. J. Am. Chem. Soc. 141:4016–25
    [Google Scholar]
  62. 62. 
    Zheng L, Chen Y, Li N, Zhang J, Liu N et al. 2020. Robust ultraclean atomically thin membranes for atomic-resolution electron microscopy. Nat. Commun. 11:541
    [Google Scholar]
  63. 63. 
    Benjamin CJ, Wright KJ, Bolton SC, Hyun SH, Krynski K et al. 2016. Selective capture of histidine-tagged proteins from cell lysates using TEM grids modified with NTA-graphene oxide. Sci. Rep. 6:32500
    [Google Scholar]
  64. 64. 
    Wang F, Liu Y, Yu Z, Li S, Cheng Y, Agard DA 2020. General and robust covalently linked graphene oxide affinity grids for high-resolution cryo-EM. PNAS 117:24269–73
    [Google Scholar]
  65. 65. 
    Schmitt L, Dietrich C, Tampe R. 1994. Synthesis and characterization of chelator-lipids for reversible immobilization of engineered proteins at self-assembled lipid interfaces. J. Am. Chem. Soc. 116:8485–91
    [Google Scholar]
  66. 66. 
    Kubalek EW, Legrice SFJ, Brown PO. 1994. Two-dimensional crystallization of histidine-tagged, HIV-1 reverse-transcriptase promoted by a novel nickel-chelating lipid. J. Struct. Biol. 113:117–23
    [Google Scholar]
  67. 67. 
    Wilson-Kubalek EM, Chappie JS, Arthur CP. 2010. Helical crystallization of soluble and membrane binding proteins. Methods Enzymol 481:45–62
    [Google Scholar]
  68. 68. 
    Kelly DF, Abeyrathne PD, Dukovski D, Walz T. 2008. The affinity grid: a pre-fabricated EM grid for monolayer purification. J. Mol. Biol. 382:423–33
    [Google Scholar]
  69. 69. 
    Kelly DF, Dukovski D, Walz T. 2010. A practical guide to the use of monolayer purification and affinity grids. Methods Enzymol. 481:83–107
    [Google Scholar]
  70. 70. 
    Benjamin CJ, Wright KJ, Hyun S-H, Krynski K, Yu G et al. 2016. Nonfouling NTA-PEG-based TEM grid coatings for selective capture of histidine-tagged protein targets from cell lysates. Langmuir 32:551–59
    [Google Scholar]
  71. 71. 
    Yu G, Li K, Jiang W. 2016. Antibody-based affinity cryo-EM grid. Methods 100:16–24
    [Google Scholar]
  72. 72. 
    Darst SA, Kubalek EW, Edwards AM, Kornberg RD. 1991. Two-dimensional and epitaxial crystallization of a mutant form of yeast RNA polymerase II. J. Mol. Biol. 221:347–57
    [Google Scholar]
  73. 73. 
    Wang LG, Ounjai P, Sigworth FJ. 2008. Streptavidin crystals as nanostructured supports and image-calibration references for cryo-EM data collection. J. Struct. Biol. 164:190–98
    [Google Scholar]
  74. 74. 
    Wang LG, Sigworth FJ. 2010. Liposomes on a streptavidin crystal: a system to study membrane proteins by cryo-EM. Methods Enzymol. 481:147–64
    [Google Scholar]
  75. 75. 
    Crucifix C, Uhring M, Schultz P. 2004. Immobilization of biotinylated DNA on 2-D streptavidin crystals. J. Struct. Biol. 146:441–51
    [Google Scholar]
  76. 76. 
    Han BG, Walton RW, Song A, Hwu P, Stubbs MT et al. 2012. Electron microscopy of biotinylated protein complexes bound to streptavidin monolayer crystals. J. Struct. Biol. 180:249–53
    [Google Scholar]
  77. 77. 
    Han B-G, Watson Z, Kang H, Pulk A, Downing KH et al. 2016. Long shelf-life streptavidin support-films suitable for electron microscopy of biological macromolecules. J. Struct. Biol. 195:238–44
    [Google Scholar]
  78. 78. 
    Lahiri I, Xu J, Han BG, Oh J, Wang D et al. 2019. 3.1 Å structure of yeast RNA polymerase II elongation complex stalled at a cyclobutane pyrimidine dimer lesion solved using streptavidin affinity grids. J. Struct. Biol. 207:270–78
    [Google Scholar]
  79. 79. 
    Kasinath V, Beck C, Sauer P, Poepsel S, Kosmatka J et al. 2020. JARID2 and AEBP2 regulate PRC2 activity in the presence of H2A ubiquitination or other histone modifications. bioRxiv https://doi.org/10.1101/2020.04.20.049213
    [Crossref]
  80. 80. 
    Takizawa Y, Binshtein E, Erwin AL, Pyburn TM, Mittendorf KF, Ohi MD. 2017. While the revolution will not be crystallized, biochemistry reigns supreme. Protein Sci 26:69–81
    [Google Scholar]
  81. 81. 
    Joppe M, D'Imprima E, Salustros N, Paithankar KS, Vonck J et al. 2020. The resolution revolution in cryoEM requires high-quality sample preparation: a rapid pipeline to a high-resolution map of yeast fatty acid synthase. IUCrJ 7:220–27
    [Google Scholar]
  82. 82. 
    Chari A, Haselbach D, Kirves J-M, Ohmer J, Paknia E et al. 2015. ProteoPlex: stability optimization of macromolecular complexes by sparse-matrix screening of chemical space. Nat. Methods 12:859–65
    [Google Scholar]
  83. 83. 
    Stark H. 2010. GraFix: stabilization of fragile macromolecular complexes for single particle cryo-EM. Methods Enzymol. 481:109–26
    [Google Scholar]
  84. 84. 
    Yan L, Zheng YB, Zhao F, Li SJ, Gao XF et al. 2012. Chemistry and physics of a single atomic layer: strategies and challenges for functionalization of graphene and graphene-based materials. Chem. Soc. Rev. 41:97–114
    [Google Scholar]
  85. 85. 
    Mali KS, Greenwood J, Adisoejoso J, Phillipson R, De Feyter S. 2015. Nanostructuring graphene for controlled and reproducible functionalization. Nanoscale 7:1566–85
    [Google Scholar]
  86. 86. 
    Touze E, Gohier F, Daffos B, Taberna PL, Cougnon C. 2018. Improvement of electrochemical performances of catechol-based supercapacitor electrodes by tuning the redox potential via different-sized O-protected catechol diazonium salts. Electrochim. Acta 265:121–30
    [Google Scholar]
  87. 87. 
    Kaplan A, Yuan Z, Benck JD, Rajan AG, Chu XS et al. 2017. Current and future directions in electron transfer chemistry of graphene. Chem. Soc. Rev. 46:4530–71
    [Google Scholar]
  88. 88. 
    ElSohly AM, Francis MB. 2015. Development of oxidative coupling strategies for site-selective protein modification. Acc. Chem. Res. 48:1971–78
    [Google Scholar]
  89. 89. 
    Armstrong M, Han BG, Gomez S, Turner J, Fletcher DA, Glaeser RM. 2020. Microscale fluid behavior during cryo-EM sample blotting. Biophys. J. 118:708–19
    [Google Scholar]
  90. 90. 
    Wei H, Dandey VP, Zhang ZN, Raczkowski A, Rice WJ et al. 2018. Optimizing “self-wicking” nanowire grids. J. Struct. Biol. 202:170–74
    [Google Scholar]
  91. 91. 
    Dandey VP, Wei H, Zhang ZN, Tan YZ, Acharya P et al. 2018. Spotiton: new features and applications. J. Struct. Biol. 202:161–69
    [Google Scholar]
  92. 92. 
    Ashtiani D, Venugopal H, Belousoff M, Spicer B, Mak J et al. 2018. Delivery of femtolitre droplets using surface acoustic wave based atomisation for cryo-EM grid preparation. J. Struct. Biol. 203:94–101
    [Google Scholar]
  93. 93. 
    Liu Y, Zhou K, Zhang N, Wei H, Tan YZ et al. 2020. FACT caught in the act of manipulating the nucleosome. Nature 577:426–31
    [Google Scholar]
  94. 94. 
    Scapin G, Dandey VP, Zhang Z, Prosise W, Hruza A et al. 2018. Structure of the insulin receptor-insulin complex by single-particle cryo-EM analysis. Nature 556:122–25
    [Google Scholar]
  95. 95. 
    Han H, Fulcher JM, Dandey VP, Iwasa JH, Sundquist WI et al. 2019. Structure of Vps4 with circular peptides and implications for translocation of two polypeptide chains by AAA+ ATPases. eLife 8:e44071
    [Google Scholar]
  96. 96. 
    Feng X, Fu Z, Kaledhonkar S, Jia Y, Shah B et al. 2017. A fast and effective microfluidic spraying-plunging method for high-resolution single-particle cryo-EM. Structure 25:663–70.e3
    [Google Scholar]
  97. 97. 
    Kontziampasis D, Klebl DP, Iadanza MG, Scarff CA, Kopf F et al. 2019. A cryo-EM grid preparation device for time-resolved structural studies. IUCrJ 6:1024–31
    [Google Scholar]
  98. 98. 
    Tan YZ, Rubinstein JL. 2020. Through-grid wicking enables high-speed cryoEM specimen preparation. bioRxiv https://doi.org/10.1101/2020.05.03.075366
    [Crossref]
  99. 99. 
    Schmidli C, Albiez S, Rima L, Righetto R, Mohammed I et al. 2019. Microfluidic protein isolation and sample preparation for high-resolution cryo-EM. PNAS 116:15007–12
    [Google Scholar]
  100. 100. 
    Arnold SA, Albiez S, Bieri A, Syntychaki A, Adaixo R et al. 2017. Blotting-free and lossless cryo-electron microscopy grid preparation from nanoliter-sized protein samples and single-cell extracts. J. Struct. Biol. 197:220–26
    [Google Scholar]
  101. 101. 
    Ravelli RBG, Nijpels FJT, Henderikx RJM, Weissenberger G, Thewessem S et al. 2020. Cryo-EM structures from sub-nl volumes using pin-printing and jet vitrification. Nat. Commun. 11:2563
    [Google Scholar]
  102. 102. 
    Trurnit HJ. 1960. A theory and method for the spreading of protein monolayers. J. Colloid Sci. 15:1–13
    [Google Scholar]
  103. 103. 
    Kistler J, Kellenberger E. 1977. Collapse phenomena in freeze-drying. J. Ultrastruct. Res. 59:70–75
    [Google Scholar]
  104. 104. 
    Lepault J, Booy FP, Dubochet J. 1983. Electron-microscopy of frozen biological suspensions. J. Microsc. 129:89–102
    [Google Scholar]
  105. 105. 
    McMillan PF, Clary DC, Sobott F, McCammon MG, Hernández H, Robinson CV. 2005. The flight of macromolecular complexes in a mass spectrometer. Philos. Trans. R. Soc. A 363:379–91
    [Google Scholar]
  106. 106. 
    Robinson CV. 2019. Mass spectrometry: from plasma proteins to mitochondrial membranes. PNAS 116:2814–20
    [Google Scholar]
  107. 107. 
    Wagner FR, Watanabe R, Schampers R, Singh D, Persoon H et al. 2020. Preparing samples from whole cells using focused-ion-beam milling for cryo-electron tomography. Nat. Protoc. 15:2041–70
    [Google Scholar]
  108. 108. 
    Dearnaley WJ, Schleupner B, Varano AC, Alden NA, Gonzalez F et al. 2019. Liquid-cell electron tomography of biological systems. Nano Lett 19:6734–41
    [Google Scholar]
  109. 109. 
    Frederik PM, Stuart MCA, Bomans PHH, Busing WM. 1989. Phospholipid, nature's own slide and cover slip for cryo-electron microscopy. J. Microsc. 153:81–92
    [Google Scholar]
  110. 110. 
    Chen J, Noble AJ, Kang JY, Darst SA. 2019. Eliminating effects of particle adsorption to the air/water interface in single-particle cryo-electron microscopy: bacterial RNA polymerase and CHAPSO. J. Struct. Biol. X 1:100005
    [Google Scholar]
  111. 111. 
    Ruckenstein E, Jain RK. 1974. Spontaneous rupture of thin liquid films. J. Chem. Soc., Faraday Trans. 2 70:132–47
    [Google Scholar]
  112. 112. 
    Jones MN, Mysels KJ, Scholten PC. 1966. Stability and some properties of 2nd black film. Trans. Faraday Soc. 62:1336–48
    [Google Scholar]
  113. 113. 
    Parsegian VA, Zemb T. 2011. Hydration forces: observations, explanations, expectations, questions. Curr. Opin. Colloid Interface Sci. 16:618–24
    [Google Scholar]
  114. 114. 
    Mysels KJ, Jones MN. 1966. Direct measurement of variation of double-layer repulsion with distance. Discuss. Faraday Soc. 42:42–50
    [Google Scholar]
/content/journals/10.1146/annurev-biochem-072020-020231
Loading
/content/journals/10.1146/annurev-biochem-072020-020231
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error