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Annual Review of Analytical Chemistry

Volume 7, 2014

Analytical Approaches for Size and Mass Analysis of Large Protein Assemblies

Abstract

Analysis of the size and mass of nanoparticles, whether they are natural biomacromolecular or synthetic supramolecular assemblies, is an important step in the characterization of such molecular species. In recent years, electrospray ionization (ESI) has emerged as a technology through which particles with masses up to 100 MDa can be ionized and transferred into the gas phase, preparing them for accurate mass analysis. Here we review currently used methodologies, with a clear focus on native mass spectrometry (MS). Additional complementary methodologies are also covered, including ion-mobility analysis, nanomechanical mass sensors, and charge-detection MS. The literature discussed clearly demonstrates the great potential of ESI-based methodologies for the size and mass analysis of nanoparticles, including very large naturally occurring protein assemblies. The analytical approaches discussed are powerful tools in not only structural biology, but also nanotechnology.

Keyword(s): electrospray ionization, native mass spectrometry, Orbitrap, protein complex, Time-of-Flight
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2014-06-12
2024-05-07
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Literature Cited

  1. Barabási A-L, Oltvai ZN. 1.  2004. Network biology: understanding the cell's functional organization. Nat. Rev. Genet. 5:101–13 [Google Scholar]
  2. Robinson CV, Sali A, Baumeister W. 2.  2007. Review article: The molecular sociology of the cell. Nature 450:973–82 [Google Scholar]
  3. Walzthoeni T, Leitner A, Stengel F, Aebersold R. 3.  2013. Mass spectrometry supported determination of protein complex structure. Curr. Opin. Struct. Biol. 23:252–60 [Google Scholar]
  4. Gingras AC, Gstaiger M, Raught B, Aebersold R. 4.  2007. Analysis of protein complexes using mass spectrometry. Nat. Rev. Mol. Cell Biol. 8:645–54 [Google Scholar]
  5. Gavin A-C, Bösche M, Krause R, Grandi P, Marzioch M. 5.  et al. 2002. Functional organization of the yeast proteome by systematic analysis of protein complexes. Nature 415:141–47 [Google Scholar]
  6. Gavin A-C, Aloy P, Grandi P, Krause R, Boesche M. 6.  et al. 2006. Proteome survey reveals modularity of the yeast cell machinery. Nature 440:631–36 [Google Scholar]
  7. Fenn JB, Mann M, Meng CK, Wong SF, Whitehouse CM. 7.  1989. Electrospray ionization for mass spectrometry of large biomolecules. Science 246:64–71 [Google Scholar]
  8. Fenn JB.8.  2003. Electrospray wings for molecular elephants (Nobel lecture). Angew. Chem. 42:3871–94 [Google Scholar]
  9. Dole M, Mack LL, Hines RL, Mobley RC, Ferguson LD, Alice MB. 9.  1968. Molecular beams of macroions. J. Chem. Phys. 49:2240–49 [Google Scholar]
  10. Wilm M.10.  2011. Principles of electrospray ionization. Mol. Cell. Proteomics 10:M111.009407 [Google Scholar]
  11. Wilm MS, Mann M. 11.  1994. Electrospray and Taylor-Cone theory, Dole's beam of macromolecules at last. Int. J. Mass Spectrom. Ion Process. 136:167–80 [Google Scholar]
  12. Fernandez De La Mora J. 12.  2000. Electrospray ionization of large multiply charged species proceeds via Dole's charged residue mechanism. Anal. Chim. Acta 406:93–104 [Google Scholar]
  13. Breuker K, McLafferty FW. 13.  2008. Stepwise evolution of protein native structure with electrospray into the gas phase, 10−12 to 102 s. Proc. Natl. Acad. Sci. USA 105:18145–52 [Google Scholar]
  14. Ruotolo BT, Giles K, Campuzano I, Sandercock AM, Bateman RH, Robinson CV. 14.  2005. Evidence for macromolecular protein rings in the absence of bulk water. Science 310:1658–61 [Google Scholar]
  15. Hall Z, Politis A, Bush MF, Smith LJ, Robinson CV. 15.  2012. Charge-state dependent compaction and dissociation of protein complexes: insights from ion mobility and molecular dynamics. J. Am. Chem. Soc. 134:3429–38 [Google Scholar]
  16. Wilm M, Mann M. 16.  1996. Analytical properties of the nanoelectrospray ion source. Anal. Chem. 68:1–8 [Google Scholar]
  17. Hedges JB, Vahidi S, Yue X, Konermann L. 17.  2013. Effects of ammonium bicarbonate on the electrospray mass spectra of proteins: evidence for bubble-induced unfolding. Anal. Chem. 85:6469–76 [Google Scholar]
  18. Dyachenko A, Gruber R, Shimon L, Horovitz A, Sharon M. 18.  2013. Allosteric mechanisms can be distinguished using structural mass spectrometry. Proc. Natl. Acad. Sci. USA 110:7235–39 [Google Scholar]
  19. Kaltashov IA, Mohimen A. 19.  2005. Estimates of protein areas in solution by electrospray ionization mass spectrometry. Anal. Chem. 77:5370–79 [Google Scholar]
  20. Chowdhury SK, Katta V, Chait BT. 20.  1990. Probing conformational changes in proteins by mass spectrometry. J. Am. Chem. Soc. 112:9012–13 [Google Scholar]
  21. Kaltashov IA, Abzalimov RR. 21.  2008. Do ionic charges in ESI MS provide useful information on macromolecular structure?. J. Am. Soc. Mass Spectrom. 19:1239–46 [Google Scholar]
  22. Catalina MI, Van Den Heuvel RHH, Van Duijn E, Heck AJR. 22.  2005. Decharging of globular proteins and protein complexes in electrospray. Chem. Eur. J. 11:960–68 [Google Scholar]
  23. Flick TG, Williams ER. 23.  2012. Supercharging with trivalent metal ions in native mass spectrometry. J. Am. Soc. Mass Spectrom. 23:1885–95 [Google Scholar]
  24. Lomeli SH, Peng IX, Yin S, Ogorzalek Loo RR, Loo JA. 24.  2010. New reagents for increasing ESI multiple charging of proteins and protein complexes. J. Am. Soc. Mass Spectrom. 21:127–31 [Google Scholar]
  25. Lomeli SH, Yin S, Ogorzalek Loo RR, Loo JA. 25.  2009. Increasing charge while preserving noncovalent protein complexes for ESI-MS. J. Am. Soc. Mass Spectrom. 20:593–96 [Google Scholar]
  26. Van Duijn E, Barendregt A, Synowsky S, Versluis C, Heck AJR. 26.  2009. Chaperonin complexes monitored by ion mobility mass spectrometry. J. Am. Chem. Soc. 131:1452–59 [Google Scholar]
  27. Mann M, Meng CK, Fenn JB. 27.  1989. Interpreting mass spectra of multiply charged ions. Anal. Chem. 61:1702–8 [Google Scholar]
  28. Morgner N, Robinson CV. 28.  2012. Massign: an assignment strategy for maximizing information from the mass spectra of heterogeneous protein assemblies. Anal. Chem. 84:2939–48 [Google Scholar]
  29. Van Breukelen B, Barendregt A, Heck AJR, Van Den Heuvel RHH. 29.  2006. Resolving stoichiometries and oligomeric states of glutamate synthase protein complexes with curve fitting and simulation of electrospray mass spectra. Rapid Commun. Mass Spectrom. 20:2490–96 [Google Scholar]
  30. Tseng Y, Uetrecht C, Heck AJR, Peng W. 30.  2011. Interpreting the charge state assignment in electrospray mass spectra of bioparticles. Anal. Chem. 83:1960–68 [Google Scholar]
  31. Sanglier S, Leize E, Dorsselaer A, Zal F. 31.  2003. Comparative ESI-MS study of approximately 2.2 MDa native hemocyanins from deep-sea and shore crabs: from protein oligomeric state to biotope. J. Am. Soc. Mass Spectrom. 14:419–29 [Google Scholar]
  32. Chen F, Gerber S, Heuser K, Korkhov VM, Lizak C. 32.  et al. 2013. High-mass matrix-assisted laser desorption ionization-mass spectrometry of integral membrane proteins and their complexes. Anal. Chem. 85:3483–88 [Google Scholar]
  33. Hoffmann J, Aslimovska L, Bamann C, Glaubitz C, Bamberg E, Brutschy B. 33.  2010. Studying the stoichiometries of membrane proteins by mass spectrometry: microbial rhodopsins and a potassium ion channel. Phys. Chem. Chem. Phys. 12:3480–85 [Google Scholar]
  34. Morgner N, Hoffmann J, Barth H, Meier T, Brutschy B. 34.  2008. LILBID-mass spectrometry applied to the mass analysis of RNA polymerase II and an F1Fo-ATP synthase. Int. J. Mass Spectrom. 277:309–13 [Google Scholar]
  35. Van Den Heuvel RHH, Heck AJR. 35.  2004. Native protein mass spectrometry: from intact oligomers to functional machineries. Curr. Opin. Chem. Biol. 8:519–26 [Google Scholar]
  36. Sharon M.36.  2013. Structural MS pulls its weight. Science 340:1059–60 [Google Scholar]
  37. Sobott F, Hernández H, McCammon MG, Tito MA, Robinson CV. 37.  2002. A tandem mass spectrometer for improved transmission and analysis of large macromolecular assemblies. Anal. Chem. 74:1402–7 [Google Scholar]
  38. Kozlovski VI, Donald LJ, Collado VM, Spicer V, Loboda AV. 38.  et al. 2011. A TOF mass spectrometer for the study of noncovalent complexes. Int. J. Mass Spectrom. 308:118–25 [Google Scholar]
  39. Van Den Heuvel RHH, Van Duijn E, Mazon H, Synowsky SA, Lorenzen K. 39.  et al. 2006. Improving the performance of a quadrupole time-of-flight instrument for macromolecular mass spectrometry. Anal. Chem. 78:7473–83 [Google Scholar]
  40. Tahallah N, Pinkse M, Maier CS, Heck AJR. 40.  2001. The effect of the source pressure on the abundance of ions of noncovalent protein assemblies in an electrospray ionization orthogonal time-of-flight instrument. Rapid Commun. Mass Spectrom. 15:596–601 [Google Scholar]
  41. Schmidt A, Bahr U, Karas M. 41.  2001. Influence of pressure in the first pumping stage on analyte desolvation and fragmentation in nano-ESI MS. Anal. Chem. 73:6040–46 [Google Scholar]
  42. Chernushevich IV, Thomson BA. 42.  2004. Collisional cooling of large ions in electrospray mass spectrometry. Anal. Chem. 76:1754–60 [Google Scholar]
  43. Benesch JLP.43.  2009. Collisional activation of protein complexes: picking up the pieces. J. Am. Soc. Mass Spectrom. 20:341–48 [Google Scholar]
  44. Benesch JLP, Aquilina JA, Ruotolo BT, Sobott F, Robinson CV. 44.  2006. Tandem mass spectrometry reveals the quaternary organization of macromolecular assemblies. Chem. Biol. 13:597–605 [Google Scholar]
  45. Zhou M, Sandercock AM, Fraser CS, Ridlova G, Stephens E. 45.  et al. 2008. Mass spectrometry reveals modularity and a complete subunit interaction map of the eukaryotic translation factor eIF3. Proc. Natl. Acad. Sci. USA 105:18139–44 [Google Scholar]
  46. Zhang Z, Zheng Y, Mazon H, Milgrom E, Kitagawa N. 46.  et al. 2008. Structure of the yeast vacuolar ATPase. J. Biol. Chem. 283:35983–95 [Google Scholar]
  47. Lorenzen K, Vannini A, Cramer P, Heck AJR. 47.  2007. Structural biology of RNA polymerase III: mass spectrometry elucidates subcomplex architecture. Structure 15:1237–45 [Google Scholar]
  48. Hall Z, Politis A, Robinson CV. 48.  2012. Structural modeling of heteromeric protein complexes from disassembly pathways and ion mobility-mass spectrometry. Structure 20:1596–609 [Google Scholar]
  49. Benesch JLP, Ruotolo BT, Sobott F, Wildgoose J, Gilbert A. 49.  et al. 2009. Quadrupole-time-of-flight mass spectrometer modified for higher-energy dissociation reduces protein assemblies to peptide fragments. Anal. Chem. 81:1270–74 [Google Scholar]
  50. Lee J, Reilly PTA. 50.  2011. Limitation of time-of-flight resolution in the ultra high mass range. Anal. Chem. 83:5831–33 [Google Scholar]
  51. Snijder J, Rose RJ, Veesler D, Johnson JE, Heck AJ. 51.  2013. Studying 18 MDa virus assemblies with native mass spectrometry. Angew. Chem. 52:4020–23 [Google Scholar]
  52. Lössl P, Snijder J, Heck AJR. 52.  2014. Boundaries of mass resolution in native mass spectrometry. J. Am. Soc. Mass Spectrom. 25906–17
  53. Kitova EN, Bundle DR, Klassen JS. 53.  2002. Thermal dissociation of protein-oligosaccharide complexes in the gas phase: mapping the intrinsic intermolecular interactions. J. Am. Chem. Soc. 124:5902–13 [Google Scholar]
  54. Felitsyn N, Kitova EN, Klassen JS. 54.  2001. Thermal decomposition of a gaseous multiprotein complex studied by blackbody infrared radiative dissociation. Investigating the origin of the asymmetric dissociation behavior. Anal. Chem. 73:4647–61 [Google Scholar]
  55. Zhang H, Cui W, Wen J, Blankenship RE, Gross ML. 55.  2010. Native electrospray and electron-capture dissociation in FTICR mass spectrometry provide top-down sequencing of a protein component in an intact protein assembly. J. Am. Soc. Mass Spectrom. 21:1966–68 [Google Scholar]
  56. Zhang H, Cui W, Wen J, Blankenship RE, Gross ML. 56.  2011. Native electrospray and electron-capture dissociation FTICR mass spectrometry for top-down studies of protein assemblies. Anal. Chem. 83:5598–606 [Google Scholar]
  57. Yin S, Loo JA. 57.  2011. Top-down mass spectrometry of supercharged native protein-ligand complexes. Int. J. Mass Spectrom. 300:118–22 [Google Scholar]
  58. Rose RJ, Damoc E, Denisov E, Makarov A, Heck AJR. 58.  2012. High-sensitivity Orbitrap mass analysis of intact macromolecular assemblies. Nat. Methods 9:1084–86 [Google Scholar]
  59. Perry RH, Cooks RG, Noll RJ. 59.  2008. Orbitrap mass spectrometry: instrumentation, ion motion and applications. Mass Spectrom. Rev. 27:661–99 [Google Scholar]
  60. Makarov A.60.  2000. Electrostatic axially harmonic orbital trapping: a high-performance technique of mass analysis.. Anal. Chem. 72:1156–62 [Google Scholar]
  61. Rosati S, Rose RJ, Thompson NJ, van Duijn E, Damoc E. 61.  et al. 2012. Exploring an orbitrap analyzer for the characterization of intact antibodies by native mass spectrometry. Angew. Chem. 51:12992–96 [Google Scholar]
  62. Barrera NP, Di Bartolo N, Booth PJ, Robinson CV. 62.  2008. Micelles protect membrane complexes from solution to vacuum. Science 321:243–46 [Google Scholar]
  63. Zhou M, Morgner N, Barrera NP, Politis A, Isaacson SC. 63.  et al. 2011. Mass spectrometry of intact V-type ATPases reveals bound lipids and the effects of nucleotide binding. Science 334:380–85 [Google Scholar]
  64. Laganowsky A, Reading E, Hopper JTS, Robinson CV. 64.  2013. Mass spectrometry of intact membrane protein complexes. Nat. Protoc. 8:639–51 [Google Scholar]
  65. Rose RJ, Verger D, Daviter T, Remaut H, Paci E. 65.  et al. 2008. Unraveling the molecular basis of subunit specificity in P pilus assembly by mass spectrometry. Proc. Natl. Acad. Sci. USA 105:12873–78 [Google Scholar]
  66. Uetrecht C, Barbu IM, Shoemaker GK, Van Duijn E, Heck AJR. 66.  2011. Interrogating viral capsid assembly with ion mobility-mass spectrometry. Nat. Chem. 3:126–32 [Google Scholar]
  67. Smith DP, Woods LA, Radford SE, Ashcroft AE. 67.  2011. Structure and dynamics of oligomeric intermediates in β2-microglobulin self-assembly. Biophys. J. 101:1238–47 [Google Scholar]
  68. Bernstein SL, Dupuis NF, Lazo ND, Wyttenbach T, Condron MM. 68.  et al. 2009. Amyloid-β protein oligomerization and the importance of tetramers and dodecamers in the aetiology of Alzheimer's disease. Nat. Chem. 1:326–31 [Google Scholar]
  69. Jurchen JC, Williams ER. 69.  2003. Origin of asymmetric charge partitioning in the dissociation of gas-phase protein homodimers. J. Am. Chem. Soc. 125:2817–26 [Google Scholar]
  70. Zhou M, Dagan S, Wysocki VH. 70.  2012. Protein subunits released by surface collisions of noncovalent complexes: nativelike compact structures revealed by ion mobility mass spectrometry. Angew. Chem. 51:4336–39 [Google Scholar]
  71. Wysocki VH, Jones CM, Galhena AS, Blackwell AE. 71.  2008. Surface-induced dissociation shows potential to be more informative than collision-induced dissociation for structural studies of large systems. J. Am. Soc. Mass Spectrom. 19:903–13 [Google Scholar]
  72. Blackwell AE, Dodds ED, Bandarian V, Wysocki VH. 72.  2011. Revealing the quaternary structure of a heterogeneous noncovalent protein complex through surface-induced dissociation. Anal. Chem. 83:2862–65 [Google Scholar]
  73. Uetrecht C, Rose RJ, Van Duijn E, Lorenzen K, Heck AJR. 73.  2010. Ion mobility mass spectrometry of proteins and protein assemblies. Chem. Soc. Rev. 39:1633–55 [Google Scholar]
  74. Bush MF, Hall Z, Giles K, Hoyes J, Robinson CV, Ruotolo BT. 74.  2010. Collision cross sections of proteins and their complexes: a calibration framework and database for gas-phase structural biology. Anal. Chem. 82:9557–65 [Google Scholar]
  75. Pringle SD, Giles K, Wildgoose JL, Williams JP, Slade SE. 75.  et al. 2007. An investigation of the mobility separation of some peptide and protein ions using a new hybrid quadrupole/travelling wave IMS/oa-ToF instrument. Int. J. Mass Spectrom. 261:1–12 [Google Scholar]
  76. Clemmer DE, Jarrold MF. 76.  1997. Ion mobility measurements and their applications to clusters and biomolecules. J. Mass Spectrom. 32:577–92 [Google Scholar]
  77. Ruotolo BT, Benesch JLP, Sandercock AM, Hyung S, Robinson CV. 77.  2008. Ion mobility-mass spectrometry analysis of large protein complexes. Nat. Protoc. 3:1139–52 [Google Scholar]
  78. Politis A, Park AY, Hyung S, Barsky D, Ruotolo BT, Robinson CV. 78.  2010. Integrating ion mobility mass spectrometry with molecular modelling to determine the architecture of multiprotein complexes. PLoS ONE 5:e12080 [Google Scholar]
  79. Barrera NP, Isaacson SC, Zhou M, Bavro VN, Welch A. 79.  et al. 2009. Mass spectrometry of membrane transporters reveals subunit stoichiometry and interactions. Nat. Methods 6:585–87 [Google Scholar]
  80. Schmidt C, Zhou M, Marriott H, Morgner N, Politis A, Robinson CV. 80.  2013. Comparative cross-linking and mass spectrometry of an intact F-type ATPase suggest a role for phosphorylation. Nat. Commun. 4:1985 [Google Scholar]
  81. Van Duijn E, Barbu IM, Barendregt A, Jore MM, Wiedenheft B. 81.  et al. 2012. Native tandem and ion mobility mass spectrometry highlight structural and modular similarities in clustered-regularly-interspaced shot-palindromic-repeats (CRISPR)-associated protein complexes from Escherichia coli and Pseudomonas aeruginosa. Mol. Cell. Proteomics 11:1430–41 [Google Scholar]
  82. Wiedenheft B, Van Duijn E, Bultema J, Waghmare S, Zhou K. 82.  et al. 2011. RNA-guided complex from a bacterial immune system enhances target recognition through seed sequence interactions. Proc. Natl. Acad. Sci. USA 108:10092–97 [Google Scholar]
  83. Jore MM, Lundgren M, Van Duijn E, Bultema JB, Westra ER. 83.  et al. 2011. Structural basis for CRISPR RNA-guided DNA recognition by Cascade. Nat. Struct. Mol. Biol. 18:529–36 [Google Scholar]
  84. Hall Z, Hernández H, Marsh J, Teichmann S, Robinson C. 84.  2013. The role of salt bridges, charge density, and subunit flexibility in determining disassembly routes of protein complexes. Structure 21:1325–37 [Google Scholar]
  85. Marsh JA, Hernández H, Hall Z, Ahnert SE, Perica T. 85.  et al. 2013. Protein complexes are under evolutionary selection to assemble via ordered pathways. Cell 153:461–70 [Google Scholar]
  86. Kitova EN, El-Hawiet A, Schnier PD, Klassen JS. 86.  2012. Reliable determinations of protein-ligand interactions by direct ESI-MS measurements. Are we there yet?. J. Am. Soc. Mass Spectrom. 23:431–41 [Google Scholar]
  87. Boeri Erba E, Barylyuk K, Yang Y, Zenobi R. 87.  2011. Quantifying protein-protein interactions within noncovalent complexes using electrospray ionization mass spectrometry. Anal. Chem. 83:9251–59 [Google Scholar]
  88. El-Hawiet A, Kitova EN, Arutyunov D, Simpson DJ, Szymanski CM, Klassen JS. 88.  2012. Quantifying ligand binding to large protein complexes using electrospray ionization mass spectrometry. Anal. Chem. 84:3867–70 [Google Scholar]
  89. Rose RJ, Labrijn AF, Van Den Bremer ETJ, Loverix S, Lasters I. 89.  et al. 2011. Quantitative analysis of the interaction strength and dynamics of human IgG4 half molecules by native mass spectrometry. Structure 19:1274–82 [Google Scholar]
  90. Deroo S, Hyung S, Marcoux J, Gordiyenko Y, Koripella RK. 90.  et al. 2012. Mechanism and rates of exchange of L7/L12 between ribosomes and the effects of binding EF-G. ACS Chem. Biol. 7:1120–27 [Google Scholar]
  91. Sobott F, Benesch JLP, Vierling E, Robinson CV. 91.  2002. Subunit exchange of multimeric protein complexes. Real-time monitoring of subunit exchange between small heat shock proteins by using electrospray mass spectrometry. J. Biol. Chem. 277:38921–29 [Google Scholar]
  92. Uetrecht C, Watts NR, Stahl SJ, Wingfield PT, Steven AC, Heck AJR. 92.  2010. Subunit exchange rates in Hepatitis B virus capsids are geometry- and temperature-dependent. Phys. Chem. Chem. Phys. 12:13368–71 [Google Scholar]
  93. Bruce JE, Cheng X, Bakhtiar R, Wu Q, Hofstadler SA. 93.  et al. 1994. Trapping, detection, and mass measurement of individual ions in a Fourier transform ion cyclotron resonance mass spectrometer. J. Am. Chem. Soc. 116:7839–47 [Google Scholar]
  94. Cheng X, Bakhtlar R, Van Orden S, Smith RD. 94.  1994. Charge-state shifting of individual multiply-charged ions of bovine albumin dimer and molecular weight determination using an individual-ion approach. Anal. Chem. 66:2084–87 [Google Scholar]
  95. Cheng X, Camp DG II, Wu Q, Bakhtiar R, Springer DL. 95.  et al. 1996. Molecular weight determination of plasmid DNA using electrospray ionization mass spectrometry. Nucleic Acids Res. 24:2183–89 [Google Scholar]
  96. Makarov A, Denisov E. 96.  2009. Dynamics of ions of intact proteins in the Orbitrap mass analyzer. J. Am. Soc. Mass Spectrom. 20:1486–95 [Google Scholar]
  97. Fuerstenau SD, Benner WH. 97.  1995. Molecular weight determination of megadalton DNA electrospray ions using charge detection time-of-flight mass spectrometry. Rapid Commun. Mass Spectrom. 9:1528–38 [Google Scholar]
  98. Fuerstenau SD, Benner WH, Thomas JJ, Brugidou C, Bothner B, Siuzdak G. 98.  2001. Mass spectrometry of an intact virus. Angew. Chem. 40:542–44 [Google Scholar]
  99. Gamero-Castão M.99.  2007. Induction charge detector with multiple sensing stages. Rev. Sci. Instrum. 78:043301 [Google Scholar]
  100. Smith JW, Siegel EE, Maze JT, Jarrold MF. 100.  2011. Image charge detection mass spectrometry: pushing the envelope with sensitivity and accuracy. Anal. Chem. 83:950–56 [Google Scholar]
  101. Contino NC, Pierson EE, Keifer DZ, Jarrold MF. 101.  2013. Charge detection mass spectrometry with resolved charge states. J. Am. Soc. Mass Spectrom. 24:101–8 [Google Scholar]
  102. Pierson EE, Keifer DZ, Selzer L, Lee LS, Contino NC. 102.  et al. 2014. Detection of late intermediates in virus capsid assembly by charge detection mass spectrometry. J. Am. Chem. Soc. 136:3536–41 [Google Scholar]
  103. Keifer DZ, Pierson EE, Hogan JA, Bedwell GJ, Prevelige PE, Jarrold MF. 103.  2014. Charge detection mass spectrometry of bacteriophage P22 procapsid distributions above 20 MDa. Rapid Commun. Mass Spectrom. 28:483–88 [Google Scholar]
  104. Chen GY, Thundat T, Wachter EA, Warmack RJ. 104.  1995. Adsorption-induced surface stress and its effects on resonance frequency of microcantilevers. J. Appl. Phys. 77:3618–22 [Google Scholar]
  105. Chaste J, Eichler A, Moser J, Ceballos G, Rurali R, Bachtold A. 105.  2012. A nanomechanical mass sensor with yoctogram resolution. Nat. Nanotechnol. 7:301–4 [Google Scholar]
  106. Jiang C, Chen B, Li J, Zhu K. 106.  2011. Mass spectrometry based on a coupled Cooper-pair box and nanomechanical resonator system. Nanoscale Res. Lett. 6:570 [Google Scholar]
  107. Hanay MS, Kelber S, Naik AK, Chi D, Hentz S. 107.  et al. 2012. Single-protein nanomechanical mass spectrometry in real time. Nat. Nanotechnol. 7:602–8 [Google Scholar]
  108. Naik AK, Hanay MS, Hiebert WK, Feng XL, Roukes ML. 108.  2009. Towards single-molecule nanomechanical mass spectrometry. Nat. Nanotechnol. 4:445–50 [Google Scholar]
  109. Gil-Santos E, Ramos D, Martínez J, Fernández-Regúlez M, García R. 109.  et al. 2010. Nanomechanical mass sensing and stiffness spectrometry based on two-dimensional vibrations of resonant nanowires. Nat. Nanotechnol. 5:641–45 [Google Scholar]
  110. Kaufman SL.110.  1998. Analysis of biomolecules using electrospray and nanoparticle methods: the gas-phase electrophoretic mobility molecular analyzer (GEMMA). J. Aerosol. Sci. 29:537–52 [Google Scholar]
  111. Bacher G, Szymanski WW, Kaufman SL, Zllner P, Blaas D, Allmaier G. 111.  2001. Charge-reduced nano electrospray ionization combined with differential mobility analysis of peptides, proteins, glycoproteins, noncovalent protein complexes and viruses. J. Mass Spectrom. 36:1038–52 [Google Scholar]
  112. Snijder J, Uetrecht C, Rose RJ, Sanchez-Eugenia R, Marti GA. 112.  et al. 2013. Probing the biophysical interplay between a viral genome and its capsid. Nat. Chem. 5:502–9 [Google Scholar]
  113. Mouradian S, Skogen J, Dorman FD, Zarrin F, Kaufman SL, Smith LM. 113.  1997. DNA analysis using an electrospray scanning mobility particle sizer. Anal. Chem. 69:5919–25 [Google Scholar]
  114. Loo JA, Berhane B, Kaddis CS, Wooding KM, Xie Y. 114.  et al. 2005. Electrospray ionization mass spectrometry and ion mobility analysis of the 20S proteasome complex. J. Am. Soc. Mass Spectrom. 16:998–1008 [Google Scholar]
  115. Kemptner J, Marchetti Deschmann M, Siekmann J, Turecek PL, Schwarz HP, Allmaier G. 115.  2010. GEMMA and MALDI-TOF MS of reactive PEGs for pharmaceutical applications. J. Pharm. Biomed. Anal. 52:432–37 [Google Scholar]
  116. Kaddis CS, Lomeli SH, Yin S, Berhane B, Apostol MI. 116.  et al. 2007. Sizing large proteins and protein complexes by electrospray ionization mass spectrometry and ion mobility. J. Am. Soc. Mass Spectrom. 18:1206–16 [Google Scholar]
  117. Allmaier G, Laschober C, Szymanski WW. 117.  2008. Nano ES GEMMA and PDMA, new tools for the analysis of nanobioparticles-protein complexes, lipoparticles, and viruses. J. Am. Soc. Mass Spectrom. 19:1062–68 [Google Scholar]
  118. Chapman HN, Fromme P, Barty A, White TA, Kirian RA. 118.  et al. 2011. Femtosecond X-ray protein nanocrystallography. Nature 470:73–78 [Google Scholar]
  119. Benesch JLP, Ruotolo BT, Simmons DA, Barrera NP, Morgner N. 119.  et al. 2010. Separating and visualising protein assemblies by means of preparative mass spectrometry and microscopy. J. Struct. Biol. 172:161–68 [Google Scholar]
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Analytical Approaches for Size and Mass Analysis of Large Protein Assemblies
Annual Review of Analytical Chemistry 7, 43 (2014); https://doi.org/10.1146/annurev-anchem-071213-020015
/content/journals/10.1146/annurev-anchem-071213-020015
/content/journals/10.1146/annurev-anchem-071213-020015
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