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Atomic Force Microscopy Study on the Mechanics of Influenza Viruses and Liposomes

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Atomic Force Microscopy Study on the Mechanics of Influenza Viruses and Liposomes Atomic force microscopy study on the mechanics of influenza viruses and liposomes Dissertation for the award of the degree “Doctor rerum naturalium” In the program of Physics of Biological and Complex Systems Göttingen Graduate School for Neurosciences, Biophysics, and Molecular Biosciences of the Georg-August-Universität Göttingen submitted by Sai Li from Hubei, China Göttingen, 2012 Members of the Thesis Committee Dr. Iwan A.T. Schaap (Reviewer, Examination board) Atomic Force Microscopy group at the III. Physikalisches Institut Faculty of Physics Prof. Dr. Andreas Janshoff (Reviewer, Examination board) Institute for Physical Chemistry Faculty of Chemistry Prof. Dr. Christoph F. Schmidt (Examination board) III. Physikalisches Institut Faculty of Physics Prof. Dr. Jörg Enderlein (Examination board) III. Physikalisches Institut Faculty of Physics Prof. Dr. Sarah Köster (Examination board) Institute for X-Ray Physics Faculty of Physics Prof. Dr. Bert de Groot (Examination board) Computational Biomolecular Dynamics Group Max Planck Institute for Biophysical Chemistry Date of oral examination: November, 2012 II I, Sai Li, hereby certify that my doctoral thesis entitled “Atomic force microscopy study on the mechanics of influenza viruses and liposomes” has been written independently and with no other sources and aids than quoted. Signature: III IV Table of contents Abbreviations ........................................................................................................ 1 Abstract ................................................................................................................. 3 1. introduction ..................................................................................................... 5 1.1. Viruses ........................................................................................................................................... 5 1.1.1. The structure, activity and mechanics of viruses .................................................................. 5 1.1.2. Influenza A virus .................................................................................................................. 13 1.2. Small unilamellar vesicles ........................................................................................................... 24 1.2.1. Lipid bilayers and liposomes ............................................................................................... 24 1.2.2. Mechanics of lipid bilayers .................................................................................................. 25 1.2.3. Parameters that influence the mechanics of lipid bilayer .................................................. 28 1.3. Atomic force microscopy ............................................................................................................ 31 1.3.1. General introduction ........................................................................................................... 31 1.3.2. AFM cantilever calibration .................................................................................................. 33 1.3.3. Application of the AFM: imaging ........................................................................................ 37 1.3.4. Application of the AFM: Mechanics .................................................................................... 39 1.3.5. Tip shape characterization and tip-induced image artifacts ............................................... 41 1.3.6. Outlook of novel AFM methods .......................................................................................... 43 2. Mechanics of liposomes .................................................................................45 2.1. Introduction to the experiments ................................................................................................ 45 2.2. Materials and methods ............................................................................................................... 47 2.3. Results ......................................................................................................................................... 54 2.3.1. Mechanics of liposomes made from pure lipids ................................................................. 54 2.3.2. Mechanics of liposomes made from myelin lipids .............................................................. 55 2.3.3. Mechanics of liposomes made from influenza viral lipid ................................................... 57 2.4. Discussion .................................................................................................................................... 70 3. Mechanics of the influenza A virus .................................................................73 3.1. Introduction to the experiments ................................................................................................ 73 3.2. Materials and methods ............................................................................................................... 74 3.3. Results ......................................................................................................................................... 76 3.3.1. Morphology of influenza viruses......................................................................................... 76 3.3.2. pH-controlled unpacking of Influenza virus ........................................................................ 77 V 3.3.3. Both softening steps are required for complete virus disassembly ................................... 83 3.4. Discussion .................................................................................................................................... 87 4. Appendices .....................................................................................................91 4.1. Nano-particle size determination ............................................................................................... 91 4.1.1. Dynamic light scattering ..................................................................................................... 91 4.1.2. Viral particle size determination by single virus tracking ................................................... 92 4.2. Characterization of AFM tip induced image artifacts ............................................................... 101 4.2.1. Tip shape characterization ................................................................................................ 101 4.2.2. Shape dilation function calculation................................................................................... 103 4.3. Low force mechanical measurements with AFM and optical tweezers ................................... 105 4.3.1. Mechanics of the cell membrane by AFM pulling experiments ....................................... 105 4.3.2. Mechanics of cells by optical tweezers pushing ............................................................... 108 References .......................................................................................................... 113 Curriculum Vitae ................................................................................................. 125 Acknowledgements ............................................................................................ 129 VI ABBREVIATIONS AFM: Atomic force microscopy CCMV: Cowpea chlorotic mottle virus CCPs: Clathrin coated pits Cm1: Cellular export factor CME: Clathrin-mediated endocytosis cRNA: Complimentary RNA DAPI: 4',6-diamidino-2-phenylindole DETA: 3-[2-(2-Aminoethylamino)ethylamino] propyltrimethoxysilane DMPC: 1,2-dimyristoyl(d54)-sn-glycero-3-phosphocholine DOPC: 1,2-dioleoyl-sn-glycero-3-phosphocholine DSC: Differential scanning calorimetry EE: Early endosome EM: Electron microscopy FDQ: Fluorescence dequenching FEM: Finite element methods FZ: Force-distance GUV: Giant unilamellar vesicle HA: Hemagglutinin HIV: Human immunodeficiency virus HOPG: Highly ordered pyrolytic graphite HSV: Herpes simplex virus LE: Late endosome MDCK: Madin-darby canine kidney mRNA: Messenger RNA 1 MSD: Mean square displacement MVM: Minute virus of mice N.A.: Numerical aperture NA: Neuraminidase NP: Nucleoprotein PA: Polymerase acidic protein PB: Polymerase basic protein PBS: Phosphate buffered saline PSD: Power spectral density PTA: Phosphotungstic acid RES: Reticuloendothelial system RNP: Ribonucleoprotein SDE: Stochastic differential equation SEM: Scanning electron microscopy SFV: Semliki forest virus SHO: simple harmonic oscillator STED: Stimulated emission depletion microscopy SUV: Small unilamellar vesicle TMV: Tobacco mosaic virus tRNA: transfer RNA vRNA: Viral RNA VSV: Vesicular stomatitis virus WT: Wild-type 2 ABSTRACT Physics exists wherever there is matter: measures such as energy, mass, temperature, speed, dimension and stiffness are all examples of the physical properties. Such quantities are important characterizations for biological organisms: they are changing all the time during the life cycle. For a bio-mechanist, stiffness is an important measure to understand biological design. Because biological building blocks can be as small as 1 nm (protein/DNA/lipid), special techniques are required to study their stiffness. Both atomic force microscopy (AFM) and optical tweezers can be used to actively deform the objects at pN- nN forces and measure the deformation on nanometer length scales. In this thesis AFM is applied to study the mechanics of influenza viruses, liposomes and living cells. The genome of viruses is packed by a protein shell
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