Atomic Force Microscopy of Viruses

  • P. J. de PabloEmail author
  • I. A. T. Schaap
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 1215)


Atomic force microscopy employs a nanometric tip located at the end of a micro-cantilever to probe surface-mounted samples at nanometer resolution. Because the technique can also work in a liquid environment it offers unique possibilities to study individual viruses under conditions that mimic their natural milieu. Here, we review how AFM imaging can be used to study the surface structure of viruses including that of viruses lacking a well-defined symmetry. Beyond imaging, AFM enables the manipulation of single viruses by force spectroscopy experiments. Pulling experiments can provide information about the early events of virus–host interaction between the viral fibers and the cell membrane receptors. Pushing experiments measure the mechanical response of the viral capsid and its contents and can be used to show how virus maturation and exposure to different pH values change the mechanical response of the viruses and the interaction between the capsid and genome. Finally, we discuss how studying capsid rupture and self-healing events offers insight in virus uncoating pathways.


Protein Shell Cage Capsid Virus Atomic force microscopy Stiffness Spring constant Force curve Nano-indentation Tip Cantilever Topography Rupture Breaking Fatigue Elasticity 



Atomic Force Microscopy


Lateral Force


Normal Force


Force vs. Distance


human Adenovirus


Human Immunodeficiency Virus


Highly Oriented Pyrolytic Graphite


Jumping Mode






Total Internal Reflection Fluorescence Microscopy


Tobacco Mosaic Virus



We acknowledge our students, former students, collaborators, and projects FIS2014-59562-R, FIS2015-71108-REDT, FIS2017-89549-R. Fundación BBVA and “María de Maeztu” Program for Units of Excellence in R&D (MDM-2014-0377).


  1. 1.
    Cheng S, Liu Y, Crowley CS, Yeates TO, Bobik TA (2008) Bacterial microcompartments: their properties and paradoxes. BioEssays 30:1084–1095PubMedPubMedCentralGoogle Scholar
  2. 2.
    Querol-Audí J, Casañas A, Usón I, Luque D, Castón JR, Fita I, Verdaguer N (2009) The mechanism of vault opening from the high resolution structure of the N-terminal repeats of MVP. EMBO J 28:3450PubMedPubMedCentralGoogle Scholar
  3. 3.
    Fotin A, Cheng Y, Sliz P, Grigorieff N, Harrison SC, Kirchhausen T, Walz T (2004) Molecular model for a complete clathrin lattice from electron cryomicroscopy. Nature 432:573PubMedPubMedCentralGoogle Scholar
  4. 4.
    Lai Y-T, Reading E, Hura GL, Tsai K-L, Laganowsky A, Asturias FJ, Tainer JA, Robinson CV, Yeates TO (2014) Structure of a designed protein cage that self-assembles into a highly porous cube. Nat Chem 6:1065–1071PubMedPubMedCentralGoogle Scholar
  5. 5.
    Wimmer E, Mueller S, Tumpey TM, Taubenberger JK (2009) Synthetic viruses: a new opportunity to understand and prevent viral disease. Nat Biotechnol 27:1163PubMedPubMedCentralGoogle Scholar
  6. 6.
    Wörsdörfer B, Woycechowsky KJ, Hilvert D (2011) Directed evolution of a protein container. Science 331:589Google Scholar
  7. 7.
    Flint SJ, Enquist LW, Racaniello VR, Skalka AM (2004) Principles of virology. ASM Press, Washington D.C.Google Scholar
  8. 8.
    Mateu MGE (2013) Structure and physics of viruses. Springer, DordrechtGoogle Scholar
  9. 9.
    Douglas T, Young M (1998) Host-guest encapsulation of materials by assembled virus protein cages. Nature 393:152–155Google Scholar
  10. 10.
    Agirre J, Aloria K, Arizmendi JM, Iloro I, Elortza F, Sánchez-Eugenia R, Marti GA, Neumann E, Rey FA, Guérin DMA (2011) Capsid protein identification and analysis of mature Triatoma virus (TrV) virions and naturally occurring empty particles. Virology 409:91–101PubMedPubMedCentralGoogle Scholar
  11. 11.
    Cordova A, Deserno M, Gelbart WM, Ben-Shaul A (2003) Osmotic shock and the strength of viral capsids. Biophys J 85:70–74PubMedPubMedCentralGoogle Scholar
  12. 12.
    Minton AP (2001) The influence of macromolecular crowding and macromolecular confinement on biochemical reactions in physiological media. J Biol Chem 276:10577–10580PubMedGoogle Scholar
  13. 13.
    Baker TS, Olson NH, Fuller SD (1999) Adding the third dimension to virus life cycles: three-dimensional reconstruction of icosahedral viruses from cryo-electron micrographs. Microbiol Mol Biol Rev 63:862–922PubMedPubMedCentralGoogle Scholar
  14. 14.
    Calder LJ, Wasilewski S, Berriman JA, Rosenthal PB (2010) Structural organization of a filamentous influenza A virus. Proc Natl Acad Sci 107:10685–10690PubMedGoogle Scholar
  15. 15.
    Hinterdorfer P, van Oijen A (2009) Handbook of single-molecule biophysics. Springer, DordrechtGoogle Scholar
  16. 16.
    Muller DJ, Amrein M, Engel A (1997) Adsorption of biological molecules to a solid support for scanning probe microscopy. J Struct Biol 119:172–188PubMedGoogle Scholar
  17. 17.
    Armanious A, Aeppli M, Jacak R, Refardt D, Sigstam T, Kohn T, Sander M (2016) Viruses at solid-water interfaces: a systematic assessment of interactions driving adsorption. Environ Sci Technol 50:732–743PubMedGoogle Scholar
  18. 18.
    Moreno-Madrid F, Martin-Gonzalez N, Llauro A, Ortega-Esteban A, Hernando-Perez M, Douglas T, Schaap IAT, de Pablo PJ (2017) Atomic force microscopy of virus shells. Biochem Soc Trans 45:499–511PubMedGoogle Scholar
  19. 19.
    Ortega-Esteban A, Perez-Berna AJ, Menendez-Conejero R, Flint SJ, Martin CS, de Pablo PJ (2013) Monitoring dynamics of human adenovirus disassembly induced by mechanical fatigue. Sci Rep 3:1434PubMedPubMedCentralGoogle Scholar
  20. 20.
    Snijder J, Radtke K, Anderson F, Scholtes L, Corradini E, Baines J, Heck AJR, Wuite GJL, Sodeik B, Roos WH (2017) Vertex-specific proteins pUL17 and pUL25 mechanically reinforce herpes simplex virus capsids. J Virol 91:e00123–e00117PubMedPubMedCentralGoogle Scholar
  21. 21.
    Llauro A, Luque D, Edwards E, Trus BL, Avera J, Reguera D, Douglas T, Pablo PJ, Caston JR (2016b) Cargo-shell and cargo-cargo couplings govern the mechanics of artificially loaded virus-derived cages. Nanoscale 8:9328–9336PubMedPubMedCentralGoogle Scholar
  22. 22.
    Ramalho R, Rankovic S, Zhou J, Aiken C, Rousso I (2016) Analysis of the mechanical properties of wild type and hyperstable mutants of the HIV-1 capsid. Retrovirology 13:17PubMedPubMedCentralGoogle Scholar
  23. 23.
    Li S, Eghiaian F, Sieben C, Herrmann A, Schaap IAT (2011) Bending and puncturing the influenza lipid envelope. Biophys J 100:637–645PubMedPubMedCentralGoogle Scholar
  24. 24.
    Calo A, Eleta-Lopez A, Stoliar P, de Sancho D, Santos S, Verdaguer A, Bittner AM (2016) Multifrequency force microscopy of helical protein assembly on a virus. Sci Rep 6:21899PubMedPubMedCentralGoogle Scholar
  25. 25.
    Ares P, Garcia-Doval C, Llauro A, Gomez-Herrero J, van Raaij MJ, de Pablo PJ (2014) Interplay between the mechanics of bacteriophage fibers and the strength of virus-host links. Phys Rev E Stat Nonlinear Soft Matter Phys 89:052710Google Scholar
  26. 26.
    Kuznetsov YG, Xiao CA, Sun SY, Raoult D, Rossmann M, Mcpherson A (2010) Atomic force microscopy investigation of the giant mimivirus. Virology 404:127–137PubMedGoogle Scholar
  27. 27.
    de Pablo PJ (2017) Atomic force microscopy of virus shells. Semin Cell Dev Biol 73:199–208PubMedGoogle Scholar
  28. 28.
    Carpick RW, Ogletree DF, Salmeron M (1997) Lateral stiffness: a new nanomechanical measurement for the determination of shear strengths with friction force microscopy. Appl Phys Lett 70:1548–1550Google Scholar
  29. 29.
    Ohnesorge F, Binnig G (1993) True atomic-resolution by atomic force microscopy through repulsive and attractive forces. Science 260:1451–1456PubMedGoogle Scholar
  30. 30.
    Butt HJ, Prater CB, Hansma PK (1991) Imaging purple membranes dry and in water with the atomic force microscope. J Vac Sci Technol B 9:1193–1196Google Scholar
  31. 31.
    Moreno-Herrero F, Colchero J, Gomez-Herrero J, Baro AM (2004) Atomic force microscopy contact, tapping, and jumping modes for imaging biological samples in liquids. Phys Rev E Stat Nonlinear Soft Matter Phys 69:031915Google Scholar
  32. 32.
    Xiao C, Kuznetsov YG, Sun SY, Hafenstein SL, Kostyuchenko VA, Chipman PR, Suzan-Monti M, Raoult D, Mcpherson A, Rossmann MG (2009) Structural studies of the giant mimivirus. PLoS Biol 7:958–966Google Scholar
  33. 33.
    Carrasco C, Luque A, Hernando-Perez M, Miranda R, Carrascosa JL, Serena PA, de Ridder M, Raman A, Gomez-Herrero J, Schaap IAT, Reguera D, de Pablo PJ (2011) Built-in mechanical stress in viral shells. Biophys J 100:1100–1108PubMedPubMedCentralGoogle Scholar
  34. 34.
    Vinckier A, Heyvaert I, Dhoore A, Mckittrick T, Vanhaesendonck C, Engelborghs Y, Hellemans L (1995) Immobilizing and imaging microtubules by atomic-force microscopy. Ultramicroscopy 57:337–343PubMedGoogle Scholar
  35. 35.
    Roos WH, Bruinsma R, Wuite GJL (2010) Physical virology. Nat Phys 6:733–743Google Scholar
  36. 36.
    de Pablo PJ, Colchero J, Gomez-Herrero J, Baro AM (1998) Jumping mode scanning force microscopy. Appl Phys Lett 73:3300–3302Google Scholar
  37. 37.
    Miyatani T, Horii M, Rosa A, Fujihira M, Marti O (1997) Mapping of electrical double-layer force between tip and sample surfaces in water with pulsed-force-mode atomic force microscopy. Appl Phys Lett 71:2632–2634Google Scholar
  38. 38.
    Ortega-Esteban A, Horcas I, Hernando-Perez M, Ares P, Perez-Berna AJ, San Martin C, Carrascosa JL, de Pablo PJ, Gomez-Herrero J (2012) Minimizing tip-sample forces in jumping mode atomic force microscopy in liquid. Ultramicroscopy 114:56–61PubMedGoogle Scholar
  39. 39.
    de Pablo PJ (2013) Atomic force microscopy of viruses. Subcell Biochem 68:247–271PubMedGoogle Scholar
  40. 40.
    Schaap IAT, Carrasco C, de Pablo PJ, Mackintosh FC, Schmidt CF (2006) Elastic response, buckling, and instability of microtubules under radial indentation. Biophys J 91:1521–1531PubMedPubMedCentralGoogle Scholar
  41. 41.
    Legleiter J, Park M, Cusick B, Kowalewski T (2006) Scanning probe acceleration microscopy (SPAM) in fluids: mapping mechanical properties of surfaces at the nanoscale. Proc Natl Acad Sci USA 103:4813–4818PubMedGoogle Scholar
  42. 42.
    Muller DJ, Janovjak H, Lehto T, Kuerschner L, Anderson K (2002) Observing structure, function and assembly of single proteins by AFM. Prog Biophys Mol Biol 79:1–43PubMedGoogle Scholar
  43. 43.
    Sugimoto Y, Abe M, Hirayama S, Oyabu N, Custance O, Morita S (2005) Atom inlays performed at room temperature using atomic force microscopy. Nat Mater 4:156PubMedGoogle Scholar
  44. 44.
    Rief M, Gautel M, Oesterhelt F, Fernandez JM, Gaub HE (1997) Reversible unfolding of individual titin immunoglobulin domains by AFM. Science 276:1109–1112Google Scholar
  45. 45.
    Carrasco C, Carreira A, Schaap IAT, Serena PA, Gomez-Herrero J, Mateu MG, de Pablo PJ (2006) DNA-mediated anisotropic mechanical reinforcement of a virus. Proc Natl Acad Sci USA 103:13706–13711PubMedGoogle Scholar
  46. 46.
    Carrasco C, Castellanos M, de Pablo PJ, Mateu MG (2008) Manipulation of the mechanical properties of a virus by protein engineering. Proc Natl Acad Sci USA 105:4150–4155PubMedGoogle Scholar
  47. 47.
    Hernando-Perez M, Miranda R, Aznar M, Carrascosa JL, Schaap IAT, Reguera D, de Pablo PJ (2012) Direct measurement of phage phi29 stiffness provides evidence of internal pressure. Small 8:2366–2370PubMedGoogle Scholar
  48. 48.
    Roos WH, Radtke K, Kniesmeijer E, Geertsema H, Sodeik B, Wuite GJL (2009) Scaffold expulsion and genome packaging trigger stabilization of herpes simplex virus capsids. Proc Natl Acad Sci USA 106:9673–9678PubMedGoogle Scholar
  49. 49.
    Snijder J, Uetrecht C, Rose RJ, Sanchez-Eugenia R, Marti GA, Agirre J, Guerin DM, Wuite GJ, Heck AJ, Roos WH (2013) Probing the biophysical interplay between a viral genome and its capsid. Nat Chem 5:502–509PubMedGoogle Scholar
  50. 50.
    Zeng C, Moller-Tank S, Asokan A, Dragnea B (2017) Probing the link among genomic cargo, contact mechanics, and nanoindentation in recombinant Adeno-associated virus 2. J Phys Chem B 121:1843–1853PubMedPubMedCentralGoogle Scholar
  51. 51.
    Hernando-Perez M, Pascual E, Aznar M, Ionel A, Caston JR, Luque A, Carrascosa JL, Reguera D, de Pablo PJ (2014) The interplay between mechanics and stability of viral cages. Nanoscale 6:2702–2709PubMedGoogle Scholar
  52. 52.
    Roos WH, Gertsman I, May ER, Brooks CL, Johnson JE, Wuite GJL (2012) Mechanics of bacteriophage maturation. Proc Natl Acad Sci USA 109:2342–2347PubMedGoogle Scholar
  53. 53.
    Llauro A, Schwarz B, Koliyatt R, de Pablo PJ, Douglas T (2016c) Tuning viral capsid nanoparticle stability with symmetrical morphogenesis. ACS Nano 10:8465–8473PubMedGoogle Scholar
  54. 54.
    Purohit PK, Kondev J, Phillips R (2003) Mechanics of DNA packaging in viruses. Proc Natl Acad Sci USA 100:3173–3178PubMedGoogle Scholar
  55. 55.
    Gonzalez-Huici V, Salas M, Hermoso JM (2004) The push-pull mechanism of bacteriophage O29 DNA injection. Mol Microbiol 52:529–540PubMedGoogle Scholar
  56. 56.
    Smith DE, Tans SJ, Smith SB, Grimes S, Anderson DL, Bustamante C (2001) The bacteriophage phi 29 portal motor can package DNA against a large internal force. Nature 413:748–752Google Scholar
  57. 57.
    Llauró A, Guerra P, Irigoyen N, Rodríguez JF, Verdaguer N, de Pablo PJ (2014) Mechanical stability and reversible fracture of vault particles. Biophys J 106:687–695PubMedPubMedCentralGoogle Scholar
  58. 58.
    Snijder J, Kononova O, Barbu IM, Uetrecht C, Rurup WF, Burnley RJ, Koay MS, Cornelissen JJ, Roos WH, Barsegov V, Wuite GJ, Heck AJ (2016) Assembly and mechanical properties of the cargo-free and cargo-loaded bacterial nanocompartment encapsulin. Biomacromolecules 17:2522–2529PubMedGoogle Scholar
  59. 59.
    Ortega-Esteban A, Condezo GN, Perez-Berna AJ, Chillon M, Flint SJ, Reguera D, San Martin C, de Pablo PJ (2015b) Mechanics of viral chromatin reveals the pressurization of human adenovirus. ACS Nano 9:10826–10833PubMedGoogle Scholar
  60. 60.
    Snijder J, Ivanovska IL, Baclayon M, Roos WH, Wuite GJ (2012) Probing the impact of loading rate on the mechanical properties of viral nanoparticles. Micron 43:1343–1350Google Scholar
  61. 61.
    Klug WS, Bruinsma RF, Michel JP, Knobler CM, Ivanovska IL, Schmidt CF, Wuite GJL (2006) Failure of viral shells. Phys Rev Lett 97:228101PubMedGoogle Scholar
  62. 62.
    Landau LD, Lifshizt E (1986) Theory of elasticity. Pergamon, LondonGoogle Scholar
  63. 63.
    Falvo MR, Washburn S, Superfine R, Finch M, Brooks FP, Chi V, Taylor RM (1997) Manipulation of individual viruses: friction and mechanical properties. Biophys J 72:1396–1403PubMedPubMedCentralGoogle Scholar
  64. 64.
    Ivanovska IL, de Pablo PJ, Ibarra B, Sgalari G, Mackintosh FC, Carrascosa JL, Schmidt CF, Wuite GJL (2004) Bacteriophage capsids: tough nanoshells with complex elastic properties. Proc Natl Acad Sci USA 101:7600–7605PubMedGoogle Scholar
  65. 65.
    San Martín C (2012) Latest insights on adenovirus structure and assembly. Viruses 4:847–877PubMedPubMedCentralGoogle Scholar
  66. 66.
    Dimitriadis EK, Horkay F, Maresca J, Kachar B, Chadwick RS (2002) Determination of elastic moduli of thin layers of soft material using the atomic force microscope. Biophys J 82:2798–2810PubMedPubMedCentralGoogle Scholar
  67. 67.
    Ivanovska IL, Miranda R, Carrascosa JL, Wuite GJL, Schmidt CF (2011) Discrete fracture patterns of virus shells reveal mechanical building blocks. Proc Natl Acad Sci USA 108:12611–12616PubMedGoogle Scholar
  68. 68.
    Llauro A, Guerra P, Irigoyen N, Rodriguez JF, Verdaguer N, de Pablo PJ (2014) Mechanical stability and reversible fracture of vault particles. Biophys J 106:687–695PubMedPubMedCentralGoogle Scholar
  69. 69.
    Llauro A, Coppari E, Imperatori F, Bizzarri AR, Caston JR, Santi L, Cannistraro S, de Pablo PJ (2015) Calcium ions modulate the mechanics of tomato bushy stunt virus. Biophys J 109:390–397PubMedPubMedCentralGoogle Scholar
  70. 70.
    Valbuena A, Mateu MG (2015) Quantification and modification of the equilibrium dynamics and mechanics of a viral capsid lattice self-assembled as a protein nanocoating. Nanoscale 7:14953–14964PubMedGoogle Scholar
  71. 71.
    Voros Z, Csik G, Herenyi L, Kellermayer MSZ (2017) Stepwise reversible nanomechanical buckling in a viral capsid. Nanoscale 9:1136–1143PubMedGoogle Scholar
  72. 72.
    Uchida M, Douglas T (2013) Biophysical chemistry: unravelling capsid transformations. Nat Chem 5:444–445PubMedGoogle Scholar
  73. 73.
    Tang L, Gilcrease EB, Casjens SR, Johnson JE (2006) Highly discriminatory binding of capsid-cementing proteins in bacteriophage L. Structure 14:837–845PubMedGoogle Scholar
  74. 74.
    Carrillo PJ, Medrano M, Valbuena A, Rodriguez-Huete A, Castellanos M, Perez R, Mateu MG (2017) Amino acid side chains buried along intersubunit interfaces in a viral capsid preserve low mechanical stiffness associated with virus infectivity. ACS Nano 11:2194–2208PubMedGoogle Scholar
  75. 75.
    Castellanos M, Perez R, Carrasco C, Hernando-Perez M, Gomez-Herrero J, de Pablo PJ, Mateu MG (2012) Mechanical elasticity as a physical signature of conformational dynamics in a virus particle. Proc Natl Acad Sci USA 109:12028–12033PubMedGoogle Scholar
  76. 76.
    Greber UF, Willetts M, Webster P, Helenius A (1993) Stepwise dismantling of Adenovirus-2 during entry into cells. Cell 75:477–486PubMedGoogle Scholar
  77. 77.
    Zhou HX, Rivas G, Minton AP (2008) Macromolecular crowding and confinement: biochemical, biophysical, and potential physiological consequences. Annu Rev Biophys 37:375–397PubMedPubMedCentralGoogle Scholar
  78. 78.
    Hernando-Pérez M, Lambert S, Nakatani-Webster E, Catalano CE, de Pablo PJ (2014) Cementing proteins provide extra mechanical stabilization to viral cages. Nat Commun 5:4520PubMedGoogle Scholar
  79. 79.
    Medina E, Nakatani E, Kruse S, Catalano CE (2012) Thermodynamic characterization of viral procapsid expansion into a functional capsid shell. J Mol Biol 418:167–180PubMedGoogle Scholar
  80. 80.
    Valbuena A, Mateu MG (2017) Kinetics of surface-driven self-assembly and fatigue-induced disassembly of a virus-based nanocoating. Biophys J 112:663–673PubMedPubMedCentralGoogle Scholar
  81. 81.
    Mertens J, Casado S, Mata CP, Hernando-Perez M, de Pablo PJ, Carrascosa JL, Caston JR (2015) A protein with simultaneous capsid scaffolding and dsRNA-binding activities enhances the birnavirus capsid mechanical stability. Sci Rep 5:13486PubMedPubMedCentralGoogle Scholar
  82. 82.
    Ortega-Esteban A, Bodensiek K, San Martin C, Suomalainen M, Greber UF, de Pablo PJ, Schaap IAT (2015a) Fluorescence tracking of genome release during mechanical unpacking of single viruses. ACS Nano 9:10571–10579PubMedGoogle Scholar
  83. 83.
    Gaiduk A, Kuhnemuth R, Antonik M, Seidel CA (2005) Optical characteristics of atomic force microscopy tips for single-molecule fluorescence applications. ChemPhysChem 6:976–983PubMedGoogle Scholar
  84. 84.
    Fontana J, Cardone G, Heymann JB, Winkler DC, Steven AC (2012) Structural changes in influenza virus at low pH characterized by cryo-electron tomography. J Virol 86:2919–2929PubMedPubMedCentralGoogle Scholar
  85. 85.
    Suomalainen M, Greber UF (2013) Uncoating of non-enveloped viruses. Curr Opin Virol 3:27–33PubMedGoogle Scholar
  86. 86.
    Wetz K, Kucinski T (1991) Influence of different ionic and pH environments on structural alterations of poliovirus and their possible relation to virus uncoating. J Gen Virol 72:2541–2544PubMedGoogle Scholar
  87. 87.
    Li S, Sieben C, Ludwig K, Höfer CT, Chiantia S, Herrmann A, Eghiaian F, Schaap IAT (2014) pH-controlled two-step uncoating of influenza virus. Biophys J 106:1447–1456PubMedPubMedCentralGoogle Scholar
  88. 88.
    Llauro A, Guerra P, Kant R, Bothner B, Verdaguer N, de Pablo PJ (2016a) Decrease in pH destabilizes individual vault nanocages by weakening the inter-protein lateral interaction. Sci Rep 6:34143PubMedPubMedCentralGoogle Scholar
  89. 89.
    Harris A, Cardone G, Winkler DC, Heymann JB, Brecher M, White JM, Steven AC (2006) Influenza virus pleiomorphy characterized by cryoelectron tomography. Proc Natl Acad Sci 103:19123–19127PubMedGoogle Scholar
  90. 90.
    Schaap IAT, Eghiaian F, Des Georges A, Veigel C (2012) Effect of envelope proteins on the mechanical properties of influenza virus. J Biol Chem 287:41078–41088PubMedPubMedCentralGoogle Scholar
  91. 91.
    Wilts BD, Schaap IA, Schmidt CF (2015) Swelling and softening of the cowpea chlorotic mottle virus in response to pH shifts. Biophys J 108:2541–2549PubMedPubMedCentralGoogle Scholar
  92. 92.
    Goldsmith LE, Yu M, Rome LH, Monbouquette HG (2007) Vault nanocapsule dissociation into halves triggered at low pH. Biochemistry 46:2865–2875PubMedGoogle Scholar
  93. 93.
    Alsteens D, Newton R, Schubert R, Martinez-Martin D, Delguste M, Roska B, Muller DJ (2017) Nanomechanical mapping of first binding steps of a virus to animal cells. Nat Nanotechnol 12:177–183PubMedGoogle Scholar
  94. 94.
    Gladnikoff M, Rousso I (2008) Directly monitoring individual retrovirus budding events using atomic force microscopy. Biophys J 94:320–326PubMedGoogle Scholar
  95. 95.
    Sieben C, Kappel C, Zhu R, Wozniak A, Rankl C, Hinterdorfer P, Grubmüller H, Herrmann A (2012) Influenza virus binds its host cell using multiple dynamic interactions. Proc Natl Acad Sci USA 109:13626–13631PubMedGoogle Scholar
  96. 96.
    Kuznetsov YG, Datta S, Kothari NH, Greenwood A, Fan H, Mcpherson A (2002) Atomic force microscopy investigation of fibroblasts infected with wild-type and Mutant Murine Leukemia Virus (MuLV). Biophys J 83:3665–3674PubMedPubMedCentralGoogle Scholar
  97. 97.
    Gladnikoff M, Shimoni E, Gov NS, Rousso I (2009) Retroviral assembly and budding occur through an actin-driven mechanism. Biophys J 97:2419–2428PubMedPubMedCentralGoogle Scholar
  98. 98.
    Cartagena A, Hernando-Perez M, Carrascosa JL, de Pablo PJ, Raman A (2013) Mapping in vitro local material properties of intact and disrupted virions at high resolution using multi-harmonic atomic force microscopy. Nanoscale 5:4729–4736PubMedGoogle Scholar
  99. 99.
    Ando T, Kodera N, Naito Y, Kinoshita T, Furuta K, Toyoshima YY (2003) A high-speed atomic force microscope for studying biological macromolecules in action. ChemPhysChem 4:1196–1202PubMedGoogle Scholar

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© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Department of Condensed Matter Physics and Solid Condensed Matter Institute IFIMACUniversidad Autónoma de MadridMadridSpain
  2. 2.SmarAct GmbHOldenburgGermany

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