Home LiteratureArticle Details
PMID: 21793131 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Review

Modern biomolecular mass spectrometry and its role in studying virus structure, dynamics, and assembly.

Angewandte Chemie (International ed. in English) ·Vol. 50 ·No. 36 ·2011-08-29 ·Pages 8248-62

Uetrecht C, Heck AJ

Abstract

Over a century since its development, the analytical technique of mass spectrometry is blooming more than ever, and applied in nearly all aspects of the natural and life sciences. In the last two decades mass spectrometry has also become amenable to the analysis of proteins and even intact protein complexes, and thus begun to make a significant impact in the field of structural biology. In this Review, we describe the emerging role of mass spectrometry, with its different technical facets, in structural biology, focusing especially on structural virology. We describe how mass spectrometry has evolved into a tool that can provide unique structural and functional information about viral-protein and protein-complex structure, conformation, assembly, and topology, extending to the direct analysis of intact virus capsids of several million Dalton in mass. Mass spectrometry is now used to address important questions in virology ranging from how viruses assemble to how they interact with their host.

MeSH Terms
Capsid/chemistry,metabolism Deuterium Exchange Measurement Proteomics Spectrometry, Mass, Electrospray Ionization Viral Proteins/chemistry,metabolism Viruses/metabolism
Chemicals
Viral Proteins
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Uetrecht Charlotte
Biomolecular Mass Spectrometry and Proteomics Group, Bijvoet Center for Biomolecular Research and Utrecht Institute for Pharmaceutical Sciences, University of Utrecht, Padualaan 8, 3584 CH Utrecht, The Netherlands.
Heck Albert J R
References (182)
182 references, click to expand
  1. Comparative multiplexed mass spectrometric analyses of endogenously expressed yeast nuclear and cytoplasmic exosomes.
    J Mol Biol. 2009 Jan 30;385(4):1300-13 PMID: 19046973
  2. Probing genuine strong interactions and post-translational modifications in the heterogeneous yeast exosome protein complex.
    Mol Cell Proteomics. 2006 Sep;5(9):1581-92 PMID: 16829593
  3. Proteomic analysis on structural proteins of Severe Acute Respiratory Syndrome coronavirus.
    Proteomics. 2004 Feb;4(2):492-504 PMID: 14760722
  4. Mass spectrometry of ribosomes and ribosomal subunits.
    Proc Natl Acad Sci U S A. 1998 Jun 23;95(13):7391-5 PMID: 9636159
  5. A visual approach to proteomics.
    Nat Rev Mol Cell Biol. 2006 Mar;7(3):225-30 PMID: 16482091
  6. Investigation of protein-ligand interactions by mass spectrometry.
    ChemMedChem. 2007 Apr;2(4):425-31 PMID: 17299828
  7. RNA-induced conformational changes in a viral coat protein studied by hydrogen/deuterium exchange mass spectrometry.
    Phys Chem Chem Phys. 2010 Nov 7;12(41):13468-75 PMID: 20877857
  8. Capsid structure and dynamics of a human rhinovirus probed by hydrogen exchange mass spectrometry.
    Protein Sci. 2005 Jun;14(6):1661-72 PMID: 15883190
  9. Advances in viral disease diagnostic and molecular epidemiological technologies.
    Expert Rev Mol Diagn. 2009 May;9(4):367-81 PMID: 19435457
  10. Ten reasons to exclude viruses from the tree of life.
    Nat Rev Microbiol. 2009 Apr;7(4):306-11 PMID: 19270719
  11. Determining the topology of virus assembly intermediates using ion mobility spectrometry-mass spectrometry.
    Rapid Commun Mass Spectrom. 2010 Oct 30;24(20):3033-3042 PMID: 20872636
  12. A theory for viral capsid assembly around electrostatic cores.
    J Chem Phys. 2009 Mar 21;130(11):114902 PMID: 19317561
  13. Disulfide bond configuration of human cytomegalovirus glycoprotein B.
    J Virol. 2002 Jun;76(12):6073-82 PMID: 12021340
  14. Filamentous phage structure, infection and assembly.
    Curr Opin Struct Biol. 1998 Apr;8(2):150-8 PMID: 9631287
  15. Interrogating viral capsid assembly with ion mobility-mass spectrometry.
    Nat Chem. 2011 Feb;3(2):126-32 PMID: 21258385
  16. Mass spectrometry of macromolecular assemblies: preservation and dissociation.
    Curr Opin Struct Biol. 2006 Apr;16(2):245-51 PMID: 16563743
  17. Investigation of protein-protein noncovalent interactions in soybean agglutinin by electrospray ionization time-of-flight mass spectrometry.
    Rapid Commun Mass Spectrom. 1994 Sep;8(9):750-4 PMID: 7949337
  18. Electron capture dissociation for structural characterization of multiply charged protein cations.
    Anal Chem. 2000 Feb 1;72(3):563-73 PMID: 10695143
  19. Analysis of protein-protein interaction surfaces using a combination of efficient lysine acetylation and nanoLC-MALDI-MS/MS applied to the E9:Im9 bacteriotoxin--immunity protein complex.
    J Am Soc Mass Spectrom. 2006 Jul;17(7):983-994 PMID: 16713291
  20. Quantitative analysis of severe acute respiratory syndrome (SARS)-associated coronavirus-infected cells using proteomic approaches: implications for cellular responses to virus infection.
    Mol Cell Proteomics. 2005 Jul;4(7):902-13 PMID: 15784933
  21. A small molecule inhibits and misdirects assembly of hepatitis B virus capsids.
    J Virol. 2002 May;76(10):4848-54 PMID: 11967301
  22. Probing native protein structures by chemical cross-linking, mass spectrometry, and bioinformatics.
    Mol Cell Proteomics. 2010 Aug;9(8):1634-49 PMID: 20360032
  23. Human rhinovirus capsid dynamics is controlled by canyon flexibility.
    Virology. 2003 Sep 15;314(1):34-44 PMID: 14517058
  24. Norwalk virus assembly and stability monitored by mass spectrometry.
    Mol Cell Proteomics. 2010 Aug;9(8):1742-51 PMID: 20418222
  25. Synthesis of a cross-linked branched polymer network in the interior of a protein cage.
    J Am Chem Soc. 2009 Apr 1;131(12):4346-54 PMID: 19317506
  26. Investigation of intact protein complexes by mass spectrometry.
    Mass Spectrom Rev. 2004 Sep-Oct;23(5):368-89 PMID: 15264235
  27. Understanding the concentration dependence of viral capsid assembly kinetics--the origin of the lag time and identifying the critical nucleus size.
    Biophys J. 2010 Mar 17;98(6):1065-74 PMID: 20303864
  28. Analysis of Rous sarcoma virus Gag protein by mass spectrometry indicates trimming by host exopeptidase.
    J Virol. 1996 May;70(5):3313-8 PMID: 8627817
  29. Holins: the protein clocks of bacteriophage infections.
    Annu Rev Microbiol. 2000;54:799-825 PMID: 11018145
  30. Virus entry by endocytosis.
    Annu Rev Biochem. 2010;79:803-33 PMID: 20196649
  31. Structural transitions in Cowpea chlorotic mottle virus (CCMV).
    Phys Biol. 2005 Nov 09;2(4):S166-72 PMID: 16280622
  32. Structure and energetics of encapsidated DNA in bacteriophage HK97 studied by scanning calorimetry and cryo-electron microscopy.
    J Mol Biol. 2009 Aug 14;391(2):471-83 PMID: 19540242
  33. Is phage DNA 'injected' into cells--biologists and physicists can agree.
    Curr Opin Microbiol. 2007 Aug;10(4):401-9 PMID: 17714979
  34. Quadrupole-time-of-flight mass spectrometer modified for higher-energy dissociation reduces protein assemblies to peptide fragments.
    Anal Chem. 2009 Feb 1;81(3):1270-4 PMID: 19105602
  35. Weak protein-protein interactions are sufficient to drive assembly of hepatitis B virus capsids.
    Biochemistry. 2002 Oct 1;41(39):11525-31 PMID: 12269796
  36. Stability and morphology comparisons of self-assembled virus-like particles from wild-type and mutant human hepatitis B virus capsid proteins.
    J Virol. 2003 Dec;77(24):12950-60 PMID: 14645551
  37. Crystallographically identical virus capsids display different properties in solution.
    Nat Struct Biol. 1999 Feb;6(2):114-6 PMID: 10048920
  38. Straightforward ladder sequencing of peptides using a Lys-N metalloendopeptidase.
    Nat Methods. 2008 May;5(5):405-7 PMID: 18425140
  39. The adenovirus capsid: major progress in minor proteins.
    J Gen Virol. 2005 Jun;86(Pt 6):1581-1588 PMID: 15914835
  40. The molecular architecture of the nuclear pore complex.
    Nature. 2007 Nov 29;450(7170):695-701 PMID: 18046406
  41. Subunit architecture of intact protein complexes from mass spectrometry and homology modeling.
    Acc Chem Res. 2008 May;41(5):617-27 PMID: 18314965
  42. Theoretical aspects of virus capsid assembly.
    J Mol Recognit. 2005 Nov-Dec;18(6):479-90 PMID: 16193532
  43. Fast photochemical oxidation of protein footprints faster than protein unfolding.
    Anal Chem. 2009 Aug 15;81(16):6563-71 PMID: 20337372
  44. Separating and visualising protein assemblies by means of preparative mass spectrometry and microscopy.
    J Struct Biol. 2010 Nov;172(2):161-8 PMID: 20227505
  45. Detecting structural changes in viral capsids by hydrogen exchange and mass spectrometry.
    Protein Sci. 2001 Jun;10(6):1234-43 PMID: 11369862
  46. Controlled assembly of bifunctional chimeric protein cages and composition analysis using noncovalent mass spectrometry.
    J Am Chem Soc. 2008 Dec 10;130(49):16527-9 PMID: 19554690
  47. Mass spectrometry-based proteomics.
    Nature. 2003 Mar 13;422(6928):198-207 PMID: 12634793
  48. The role of mass spectrometry in structure elucidation of dynamic protein complexes.
    Annu Rev Biochem. 2007;76:167-93 PMID: 17328674
  49. Mycoviruses of filamentous fungi and their relevance to plant pathology.
    Mol Plant Pathol. 2009 Jan;10(1):115-28 PMID: 19161358
  50. Structural transitions during bacteriophage HK97 head assembly.
    J Mol Biol. 1995 Apr 7;247(4):618-35 PMID: 7723019
  51. Curated list of prokaryote viruses with fully sequenced genomes.
    Res Microbiol. 2007 Sep;158(7):555-66 PMID: 17889511
  52. Laser desorption ionization of proteins with molecular masses exceeding 10,000 daltons.
    Anal Chem. 1988 Oct 15;60(20):2299-301 PMID: 3239801
  53. Insights into virus capsid assembly from non-covalent mass spectrometry.
    Mass Spectrom Rev. 2008 Nov-Dec;27(6):575-95 PMID: 18498137
  54. Evidence for macromolecular protein rings in the absence of bulk water.
    Science. 2005 Dec 9;310(5754):1658-61 PMID: 16293722
  55. Phosphorylation of hepatitis B virus core C-terminally truncated protein (Cp149) by PKC increases capsid assembly and stability.
    Biochem J. 2008 Nov 15;416(1):47-54 PMID: 18605987
  56. Hepatitis B virus DNA replication is coordinated by core protein serine phosphorylation and HBx expression.
    J Virol. 2005 Aug;79(15):9810-20 PMID: 16014942
  57. Mapping of protein:protein contact surfaces by hydrogen/deuterium exchange, followed by on-line high-performance liquid chromatography-electrospray ionization Fourier-transform ion-cyclotron-resonance mass analysis.
    J Chromatogr A. 2002 Dec 20;982(1):85-95 PMID: 12489858
  58. Conformational equilibria and rates of localized motion within hepatitis B virus capsids.
    J Mol Biol. 2008 Jan 11;375(2):581-94 PMID: 18022640
  59. Kinetic and mass spectrometry-based investigation of human immunodeficiency virus type 1 assembly and maturation.
    Adv Virus Res. 2005;64:285-309 PMID: 16139598
  60. Distinguishing reversible from irreversible virus capsid assembly.
    J Mol Biol. 2007 Feb 9;366(1):14-8 PMID: 17157314
  61. Mass spectrometry reveals the missing links in the assembly pathway of the bacterial 20 S proteasome.
    J Biol Chem. 2007 Jun 22;282(25):18448-18457 PMID: 17430901
  62. Glycoproteomics: past, present and future.
    FEBS Lett. 2009 Jun 5;583(11):1728-35 PMID: 19328791
  63. The impact of viral RNA on assembly pathway selection.
    J Mol Biol. 2010 Aug 13;401(2):298-308 PMID: 20621589
  64. Mass spectrometry and viral analysis.
    Chem Biol. 1996 Jan;3(1):45-8 PMID: 8807827
  65. Large-scale database searching using tandem mass spectra: looking up the answer in the back of the book.
    Nat Methods. 2004 Dec;1(3):195-202 PMID: 15789030
  66. International Committee on Taxonomy of Viruses and the 3,142 unassigned species.
    Virol J. 2005 Aug 16;2:64 PMID: 16105179
  67. Detection and selective dissociation of intact ribosomes in a mass spectrometer.
    Proc Natl Acad Sci U S A. 2000 May 9;97(10):5185-90 PMID: 10805779
  68. Host-cell-specific glycosylation of HIV-2 envelope glycoprotein.
    Glycoconj J. 1997 Nov;14(7):785-93 PMID: 9511983
  69. Quantitative proteomics analysis reveals BAG3 as a potential target to suppress severe acute respiratory syndrome coronavirus replication.
    J Virol. 2010 Jun;84(12):6050-9 PMID: 20392858
  70. Improving the performance of a quadrupole time-of-flight instrument for macromolecular mass spectrometry.
    Anal Chem. 2006 Nov 1;78(21):7473-83 PMID: 17073415
  71. The origin of viruses.
    Res Microbiol. 2009 Sep;160(7):466-72 PMID: 19647075
  72. Tandem mass spectrometry reveals the quaternary organization of macromolecular assemblies.
    Chem Biol. 2006 Jun;13(6):597-605 PMID: 16793517
  73. Structures and mechanisms of viral membrane fusion proteins: multiple variations on a common theme.
    Crit Rev Biochem Mol Biol. 2008 May-Jun;43(3):189-219 PMID: 18568847
  74. Sizing large proteins and protein complexes by electrospray ionization mass spectrometry and ion mobility.
    J Am Soc Mass Spectrom. 2007 Jul;18(7):1206-16 PMID: 17434746
  75. Detection of intact megaDalton protein assemblies of vanillyl-alcohol oxidase by mass spectrometry.
    Protein Sci. 2000 Mar;9(3):435-9 PMID: 10752605
  76. Structural proteomics of the SARS coronavirus: a model response to emerging infectious diseases.
    J Struct Funct Genomics. 2007 Sep;8(2-3):85-97 PMID: 17680348
  77. Mechanisms of capsid assembly around a polymer.
    Biophys J. 2010 Jul 21;99(2):619-28 PMID: 20643082
  78. Viral genomic single-stranded RNA directs the pathway toward a T=3 capsid.
    J Mol Biol. 2010 Feb 5;395(5):924-36 PMID: 19913556
  79. cGMP-binding prepares PKG for substrate binding by disclosing the C-terminal domain.
    J Mol Biol. 2008 Feb 1;375(5):1380-93 PMID: 18082764
  80. Critical salt bridges guide capsid assembly, stability, and maturation behavior in bacteriophage HK97.
    Mol Cell Proteomics. 2010 Aug;9(8):1752-63 PMID: 20332083
  81. Plant viruses. Invaders of cells and pirates of cellular pathways.
    Plant Physiol. 2005 Aug;138(4):1809-14 PMID: 16172093
  82. Investigating protein structure and dynamics by hydrogen exchange MS.
    Anal Chem. 2001 May 1;73(9):256A-265A PMID: 11354508
  83. Physical principles in the construction of regular viruses.
    Cold Spring Harb Symp Quant Biol. 1962;27:1-24 PMID: 14019094
  84. Coupling of rotavirus genome replication and capsid assembly.
    Adv Virus Res. 2007;69:167-201 PMID: 17222694
  85. Phages and the evolution of bacterial pathogens: from genomic rearrangements to lysogenic conversion.
    Microbiol Mol Biol Rev. 2004 Sep;68(3):560-602, table of contents PMID: 15353570
  86. Phosphoproteomics for the masses.
    ACS Chem Biol. 2010 Jan 15;5(1):105-19 PMID: 20047291
  87. Identification of novel interactions in HIV-1 capsid protein assembly by high-resolution mass spectrometry.
    J Mol Biol. 2003 Jan 24;325(4):759-72 PMID: 12507478
  88. Electrospray ionization for mass spectrometry of large biomolecules.
    Science. 1989 Oct 6;246(4926):64-71 PMID: 2675315
  89. Post-translational modifications differentially affect IgG1 conformation and receptor binding.
    Mol Cell Proteomics. 2010 Aug;9(8):1716-28 PMID: 20103567
  90. Kinetics and thermodynamics of amyloid fibril assembly.
    Acc Chem Res. 2006 Sep;39(9):671-9 PMID: 16981684
  91. Determinants of bacteriophage phi29 head morphology.
    Structure. 2006 Nov;14(11):1723-7 PMID: 17098197
  92. Membrane-containing viruses with icosahedrally symmetric capsids.
    Curr Opin Struct Biol. 2007 Apr;17(2):229-36 PMID: 17387010
  93. Protein-folding kinetics and mechanisms studied by pulse-labeling and mass spectrometry.
    Mass Spectrom Rev. 2003 Jan-Feb;22(1):1-26 PMID: 12768602
  94. Key interactions in HIV-1 maturation identified by hydrogen-deuterium exchange.
    Nat Struct Mol Biol. 2004 Jul;11(7):676-7 PMID: 15208693
  95. Native protein mass spectrometry: from intact oligomers to functional machineries.
    Curr Opin Chem Biol. 2004 Oct;8(5):519-26 PMID: 15450495
  96. An unexpected twist in viral capsid maturation.
    Nature. 2009 Apr 2;458(7238):646-50 PMID: 19204733
  97. Virus maturation: dynamics and mechanism of a stabilizing structural transition that leads to infectivity.
    Curr Opin Struct Biol. 2005 Apr;15(2):227-36 PMID: 15837183
  98. Freedom and restraint: themes in virus capsid assembly.
    Structure. 2000 Aug 15;8(8):R157-62 PMID: 10997898
  99. Tandem mass spectrometry of intact GroEL-substrate complexes reveals substrate-specific conformational changes in the trans ring.
    J Am Chem Soc. 2006 Apr 12;128(14):4694-702 PMID: 16594706
  100. The tobacco mosaic virus particle: structure and assembly.
    Philos Trans R Soc Lond B Biol Sci. 1999 Mar 29;354(1383):531-5 PMID: 10212932
  101. A guide to viral inclusions, membrane rearrangements, factories, and viroplasm produced during virus replication.
    Adv Virus Res. 2007;70:101-82 PMID: 17765705
  102. Hydroxyl radical-mediated modification of proteins as probes for structural proteomics.
    Chem Rev. 2007 Aug;107(8):3514-43 PMID: 17683160
  103. Mimivirus and its virophage.
    Annu Rev Genet. 2009;43:49-66 PMID: 19653859
  104. Hydrogen exchange mass spectrometry for the analysis of protein dynamics.
    Mass Spectrom Rev. 2006 Jan-Feb;25(1):158-70 PMID: 16208684
  105. Optical methods in the study of protein-protein interactions.
    Adv Exp Med Biol. 2010;674:33-42 PMID: 20549938
  106. Ion mobility mass spectrometry of proteins and protein assemblies.
    Chem Soc Rev. 2010 May;39(5):1633-55 PMID: 20419213
  107. 3.3 A cryo-EM structure of a nonenveloped virus reveals a priming mechanism for cell entry.
    Cell. 2010 Apr 30;141(3):472-82 PMID: 20398923
  108. Mass spectrometry-based metabolomics.
    Mass Spectrom Rev. 2007 Jan-Feb;26(1):51-78 PMID: 16921475
  109. Mass Spectrometry of an Intact Virus.
    Angew Chem Int Ed Engl. 2001 Feb 2;40(3):541-544 PMID: 29712014
  110. On the origin of cells and viruses: primordial virus world scenario.
    Ann N Y Acad Sci. 2009 Oct;1178:47-64 PMID: 19845627
  111. Structure-based engineering of an icosahedral virus for nanomedicine and nanotechnology.
    Curr Top Microbiol Immunol. 2009;327:23-58 PMID: 19198569
  112. Core protein phosphorylation modulates pregenomic RNA encapsidation to different extents in human and duck hepatitis B viruses.
    J Virol. 2000 May;74(10):4721-8 PMID: 10775610
  113. Quantitative proteomic analysis of A549 cells infected with human respiratory syncytial virus.
    Mol Cell Proteomics. 2010 Nov;9(11):2438-59 PMID: 20647383
  114. Pandemic influenza as a current threat.
    Curr Top Microbiol Immunol. 2009;333:3-24 PMID: 19768398
  115. Chlorella viruses.
    Adv Virus Res. 2006;66:293-336 PMID: 16877063
  116. Seeking membranes: positive-strand RNA virus replication complexes.
    PLoS Biol. 2008 Oct 28;6(10):e270 PMID: 18959488
  117. Identification of subunit-subunit interactions in bacteriophage P22 procapsids by chemical cross-linking and mass spectrometry.
    J Proteome Res. 2006 Feb;5(2):370-7 PMID: 16457603
  118. Comparative genomics and evolution of the tailed-bacteriophages.
    Curr Opin Microbiol. 2005 Aug;8(4):451-8 PMID: 16019256
  119. Glycosylation site-specific analysis of clade C HIV-1 envelope proteins.
    J Proteome Res. 2009 Sep;8(9):4231-42 PMID: 19610667
  120. HK97 maturation studied by crystallography and H/2H exchange reveals the structural basis for exothermic particle transitions.
    J Mol Biol. 2010 Mar 26;397(2):560-74 PMID: 20093122
  121. Switches in bacteriophage lambda development.
    Annu Rev Genet. 2005;39:409-29 PMID: 16285866
  122. Characterization of glycopeptides from HIV-I(SF2) gp120 by liquid chromatography mass spectrometry.
    J Am Soc Mass Spectrom. 2004 Nov;15(11):1545-55 PMID: 15519221
  123. Subunit architecture of multiprotein assemblies determined using restraints from gas-phase measurements.
    Structure. 2009 Sep 9;17(9):1235-43 PMID: 19748344
  124. Micelles protect membrane complexes from solution to vacuum.
    Science. 2008 Jul 11;321(5886):243-6 PMID: 18556516
  125. Native mass spectrometry: a bridge between interactomics and structural biology.
    Nat Methods. 2008 Nov;5(11):927-33 PMID: 18974734
  126. Protein surface topology-probing by selective chemical modification and mass spectrometric peptide mapping.
    Proc Natl Acad Sci U S A. 1992 Jun 15;89(12):5630-4 PMID: 1608973
  127. Biochemical characterization of a smaller form of recombinant Norwalk virus capsids assembled in insect cells.
    J Virol. 1997 Oct;71(10):8066-72 PMID: 9311906
  128. Probing the oligomeric structure of an enzyme by electrospray ionization time-of-flight mass spectrometry.
    Proc Natl Acad Sci U S A. 1996 Jul 9;93(14):6851-6 PMID: 8692908
  129. Physical approaches to biomaterial design.
    Nat Mater. 2009 Jan;8(1):15-23 PMID: 19096389
  130. Chemical cross-linking and mass spectrometry to map three-dimensional protein structures and protein-protein interactions.
    Mass Spectrom Rev. 2006 Jul-Aug;25(4):663-82 PMID: 16477643
  131. Collisionally activated dissociation and tandem mass spectrometry of intact hemoglobin beta-chain variant proteins with electrospray ionization.
    Biol Mass Spectrom. 1993 Feb;22(2):112-20 PMID: 8448219
  132. RNA polymerase I contains a TFIIF-related DNA-binding subcomplex.
    Mol Cell. 2010 Aug 27;39(4):583-94 PMID: 20797630
  133. A docking model based on mass spectrometric and biochemical data describes phage packaging motor incorporation.
    Mol Cell Proteomics. 2010 Aug;9(8):1764-73 PMID: 20124351
  134. Geometry of phage head construction.
    J Mol Biol. 1999 Oct 22;293(2):401-33 PMID: 10529353
  135. The virophage as a unique parasite of the giant mimivirus.
    Nature. 2008 Sep 4;455(7209):100-4 PMID: 18690211
  136. Protein conformations, interactions, and H/D exchange.
    Methods Enzymol. 2005;402:312-60 PMID: 16401514
  137. Mass spectrometry sampling under ambient conditions with desorption electrospray ionization.
    Science. 2004 Oct 15;306(5695):471-3 PMID: 15486296
  138. Peptide and protein sequence analysis by electron transfer dissociation mass spectrometry.
    Proc Natl Acad Sci U S A. 2004 Jun 29;101(26):9528-33 PMID: 15210983
  139. A simple, RNA-mediated allosteric switch controls the pathway to formation of a T=3 viral capsid.
    J Mol Biol. 2007 Jun 1;369(2):541-52 PMID: 17434527
  140. A library of protein cage architectures as nanomaterials.
    Curr Top Microbiol Immunol. 2009;327:71-93 PMID: 19198571
  141. Noroviruses everywhere: has something changed?
    Curr Opin Infect Dis. 2006 Oct;19(5):467-74 PMID: 16940871
  142. Evidence of viral capsid dynamics using limited proteolysis and mass spectrometry.
    J Biol Chem. 1998 Jan 9;273(2):673-6 PMID: 9422714
  143. Morphogenesis of hepatitis B virus and its subviral envelope particles.
    Cell Microbiol. 2009 Nov;11(11):1561-70 PMID: 19673892
  144. The Phage Proteomic Tree: a genome-based taxonomy for phage.
    J Bacteriol. 2002 Aug;184(16):4529-35 PMID: 12142423
  145. Virus glycosylation: role in virulence and immune interactions.
    Trends Microbiol. 2007 May;15(5):211-8 PMID: 17398101
  146. Fluorescence spectroscopic investigations of the dynamic properties of proteins, membranes and nucleic acids.
    J Biochem Biophys Methods. 1980 Jan-Feb;2(1):91-119 PMID: 6158533
  147. Phage P22 procapsids equilibrate with free coat protein subunits.
    J Mol Biol. 2007 Jan 12;365(2):513-22 PMID: 17067636
  148. Mass spectrometry combined with oxidative labeling for exploring protein structure and folding.
    Mass Spectrom Rev. 2010 Jul-Aug;29(4):651-67 PMID: 19672951
  149. Electrospray ionization mass spectrometric peptide mapping: a rapid, sensitive technique for protein structure analysis.
    Biochem Biophys Res Commun. 1990 Mar 16;167(2):686-92 PMID: 2108669
  150. Studying noncovalent protein complexes by electrospray ionization mass spectrometry.
    Mass Spectrom Rev. 1997 Jan-Feb;16(1):1-23 PMID: 9414489
  151. Mechanisms for enveloped virus budding: can some viruses do without an ESCRT?
    Virology. 2008 Mar 15;372(2):221-32 PMID: 18063004
  152. Mass spectrometric imaging for biomedical tissue analysis.
    Chem Rev. 2010 May 12;110(5):3237-77 PMID: 20423155
  153. Potential for biomolecular imaging with femtosecond X-ray pulses.
    Nature. 2000 Aug 17;406(6797):752-7 PMID: 10963603
  154. Electrospray ionization mass spectrometry and ion mobility analysis of the 20S proteasome complex.
    J Am Soc Mass Spectrom. 2005 Jul;16(7):998-1008 PMID: 15914020
  155. High-resolution mass spectrometry of viral assemblies: molecular composition and stability of dimorphic hepatitis B virus capsids.
    Proc Natl Acad Sci U S A. 2008 Jul 8;105(27):9216-20 PMID: 18587050
  156. From metal binding to nanoparticle formation: monitoring biomimetic iron oxide synthesis within protein cages using mass spectrometry.
    Angew Chem Int Ed Engl. 2009;48(26):4772-6 PMID: 19455534
  157. Hot spots--a review of the protein-protein interface determinant amino-acid residues.
    Proteins. 2007 Sep 1;68(4):803-12 PMID: 17546660
  158. Mass spectrometric characterization of proteins from the SARS virus: a preliminary report.
    Mol Cell Proteomics. 2003 May;2(5):346-56 PMID: 12775768
  159. Structural biology of RNA polymerase III: mass spectrometry elucidates subcomplex architecture.
    Structure. 2007 Oct;15(10):1237-45 PMID: 17937913
  160. Stability and shape of hepatitis B virus capsids in vacuo.
    Angew Chem Int Ed Engl. 2008;47(33):6247-51 PMID: 18642251
  161. Viruses in the sea.
    Nature. 2005 Sep 15;437(7057):356-61 PMID: 16163346
  162. Structural and functional studies of archaeal viruses.
    J Biol Chem. 2009 May 8;284(19):12599-603 PMID: 19158076
  163. Determination of stoichiometry and conformational changes in the first step of the P22 tail assembly.
    J Mol Biol. 2008 May 30;379(2):385-96 PMID: 18448123
  164. Targeted large-scale analysis of protein acetylation.
    Proteomics. 2011 Feb;11(4):571-89 PMID: 21246731
  165. Viral entry into the nucleus.
    Annu Rev Cell Dev Biol. 2000;16:627-51 PMID: 11031249
  166. Electrospray wings for molecular elephants (Nobel lecture).
    Angew Chem Int Ed Engl. 2003 Aug 25;42(33):3871-94 PMID: 12949861
  167. Assembly properties of the human immunodeficiency virus type 1 CA protein.
    J Virol. 2004 Mar;78(5):2545-52 PMID: 14963157
  168. Proteomic analysis of SARS associated coronavirus using two-dimensional liquid chromatography mass spectrometry and one-dimensional sodium dodecyl sulfate-polyacrylamide gel electrophoresis followed by mass spectroemtric analysis.
    J Proteome Res. 2004 May-Jun;3(3):549-55 PMID: 15253436
  169. Subunit exchange rates in Hepatitis B virus capsids are geometry- and temperature-dependent.
    Phys Chem Chem Phys. 2010 Nov 7;12(41):13368-71 PMID: 20676421
  170. Plus- and minus-end directed microtubule motors bind simultaneously to herpes simplex virus capsids using different inner tegument structures.
    PLoS Pathog. 2010 Jul 08;6(7):e1000991 PMID: 20628567
  171. Genome-wide analysis of retroviral DNA integration.
    Nat Rev Microbiol. 2005 Nov;3(11):848-58 PMID: 16175173
  172. Phosphorylation of hepatitis B virus Cp at Ser87 facilitates core assembly.
    Biochem J. 2006 Sep 1;398(2):311-7 PMID: 16740137
  173. DNA packaging and delivery machines in tailed bacteriophages.
    Curr Opin Struct Biol. 2007 Apr;17(2):237-43 PMID: 17395453
  174. Probing protein structure by amino acid-specific covalent labeling and mass spectrometry.
    Mass Spectrom Rev. 2009 Sep-Oct;28(5):785-815 PMID: 19016300
  175. Mass spectrometric characterization of the glycosylation pattern of HIV-gp120 expressed in CHO cells.
    Biochemistry. 2000 Sep 19;39(37):11194-204 PMID: 10985765
  176. Classical nucleation theory of virus capsids.
    Biophys J. 2006 Mar 15;90(6):1939-48 PMID: 16387781
  177. Structure, assembly, and antigenicity of hepatitis B virus capsid proteins.
    Adv Virus Res. 2005;64:125-64 PMID: 16139594
  178. Genome packaging in viruses.
    Curr Opin Struct Biol. 2010 Feb;20(1):114-20 PMID: 20060706
  179. Physical regulation of the self-assembly of tobacco mosaic virus coat protein.
    Biophys J. 2006 Aug 15;91(4):1501-12 PMID: 16731551
  180. Emerging issues in virus taxonomy.
    Emerg Infect Dis. 2004 Jan;10(1):8-13 PMID: 15078590
  181. Synthesis of biotin-tagged chemical cross-linkers and their applications for mass spectrometry.
    Rapid Commun Mass Spectrom. 2009 Jun;23(11):1719-26 PMID: 19412923
  182. Observed hysteresis of virus capsid disassembly is implicit in kinetic models of assembly.
    J Biol Chem. 2003 May 16;278(20):18249-55 PMID: 12639968
Article Info
Journal
Angewandte Chemie (International ed. in English)
Abbr.
Angew Chem Int Ed Engl
ISSN
1521-3773
DOI
10.1002/anie.201008120
Published
2011-08-29
Epub
2011-00-26
Pages
8248-62
Language
English
Region
Germany
NLM ID
0370543
PMCID
PMC7159578
Subset
IM
External Links
PubMed source DOI: 10.1002/anie.201008120 PMC Full Text View journal details
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2