Twenty years of gas phase structural biology

Structure

Volumn 21, Issue 9, 2013, Pages 1541-1550

  Marcoux, Julien ^a   Robinson, Carol V ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATE; ADRENERGIC RECEPTOR; AQUAPORIN; BINDING PROTEIN; CAPSID PROTEIN; CARDIOLIPIN; CHAPERONIN; COLICIN; CYCLOSPORIN A; CYTOPLASM PROTEIN; DEUTERIUM; EPITOPE; LIPID; MEMBRANE PROTEIN; MONOMER; MULTIDRUG RESISTANCE PROTEIN; NUCLEOTIDE; OUTER MEMBRANE PROTEIN F; PEPTIDE; PHOSPHOPROTEIN PHOSPHATASE 2A; RADICAL; TRANSLOCON;

ALLOSTERISM; BINDING AFFINITY; BIOLOGY; CELL DEATH; DEPHOSPHORYLATION; DRUG BINDING; ELECTROSPRAY; ESCHERICHIA COLI; GAS; HINGE REGION; INTERACTIONS WITH NUCLEIC ACID; LASER; LIGAND BINDING; MASS SPECTROMETRY; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MEMBRANE; METABOLOMICS; MICELLE; MOLECULAR WEIGHT; MOLECULE; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN SECRETION; PROTEIN STRUCTURE; PROTEIN SUBUNIT; REVIEW; SEDIMENTATION; SEDIMENTATION RATE; STOICHIOMETRY; THERMUS THERMOPHILUS;

ANIMALS; DETERGENTS; GASES; HUMANS; LIPIDS; MEMBRANE PROTEINS; MICELLES; MOLECULAR BIOLOGY; MULTIPROTEIN COMPLEXES; PROTEIN BINDING; SOLUBILITY; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION;

EID: 84883466602     PISSN: 09692126     EISSN: 18784186     Source Type: Journal    
DOI: 10.1016/j.str.2013.08.002     Document Type: Review

References (62)

1. A.E. Ashcroft Mass spectrometry and the amyloid problem - how far can we go in the gas phase? J. Am. Soc. Mass Spectrom. 21 2010 1087 1096
2. D. Bagal, E.N. Kitova, L. Liu, A. El-Hawiet, P.D. Schnier, and J.S. Klassen Gas phase stabilization of noncovalent protein complexes formed by electrospray ionization Anal. Chem. 81 2009 7801 7806
3. N.P. Barrera, N. Di Bartolo, P.J. Booth, and C.V. Robinson Micelles protect membrane complexes from solution to vacuum Science 321 2008 243 246
4. N.P. Barrera, S.C. Isaacson, M. Zhou, V.N. Bavro, A. Welch, T.A. Schaedler, M.A. Seeger, R.N. Miguel, V.M. Korkhov, and H.W. van Veen Mass spectrometry of membrane transporters reveals subunit stoichiometry and interactions Nat. Methods 6 2009 585 587
5. A.J. Borysik, and C.V. Robinson Formation and dissociation processes of gas-phase detergent micelles Langmuir 28 2012 7160 7167
6. A.J. Borysik, and C.V. Robinson The 'sticky business' of cleaning gas-phase membrane proteins: a detergent oriented perspective Phys. Chem. Chem. Phys. 14 2012 14439 14449
7. A.J. Borysik, D.J. Hewitt, and C.V. Robinson Detergent release prolongs the lifetime of native-like membrane protein conformations in the gas-phase J. Am. Chem. Soc. 135 2013 6078 6083
8. A.V. Botelho, T. Huber, T.P. Sakmar, and M.F. Brown Curvature and hydrophobic forces drive oligomerization and modulate activity of rhodopsin in membranes Biophys. J. 91 2006 4464 4477
9. M.F. Bush, Z. Hall, K. Giles, J. Hoyes, C.V. Robinson, and B.T. Ruotolo Collision cross sections of proteins and their complexes: a calibration framework and database for gas-phase structural biology Anal. Chem. 82 2010 9557 9565
10. J. Chen, D.L. Rempel, B.C. Gau, and M.L. Gross Fast photochemical oxidation of proteins and mass spectrometry follow submillisecond protein folding at the amino-acid level J. Am. Chem. Soc. 134 2012 18724 18731
11. K.Y. Chung, S.G. Rasmussen, T. Liu, S. Li, B.T. DeVree, P.S. Chae, D. Calinski, B.K. Kobilka, V.L. Woods Jr.; and R.K. Sunahara Conformational changes in the G protein Gs induced by the β2 adrenergic receptor Nature 477 2011 611 615
12. S.L. Cohen, and B.T. Chait Mass spectrometry as a tool for protein crystallography Annu. Rev. Biophys. Biomol. Struct. 30 2001 67 85
13. A. Dyachenko, R. Gruber, L. Shimon, A. Horovitz, and M. Sharon Allosteric mechanisms can be distinguished using structural mass spectrometry Proc. Natl. Acad. Sci. USA 110 2013 7235 7239
14. I.O. Ebong, N. Morgner, M. Zhou, M.A. Saraiva, S. Daturpalli, S.E. Jackson, and C.V. Robinson Heterogeneity and dynamics in the assembly of the heat shock protein 90 chaperone complexes Proc. Natl. Acad. Sci. USA 108 2011 17939 17944
15. S. Gupta, R. D'Mello, and M.R. Chance Structure and dynamics of protein waters revealed by radiolysis and mass spectrometry Proc. Natl. Acad. Sci. USA 109 2012 14882 14887
16. Z. Hall, A. Politis, and C.V. Robinson Structural modeling of heteromeric protein complexes from disassembly pathways and ion mobility-mass spectrometry Structure 20 2012 1596 1609
17. F. Herzog, A. Kahraman, D. Boehringer, R. Mak, A. Bracher, T. Walzthoeni, A. Leitner, M. Beck, F.U. Hartl, and N. Ban Structural probing of a protein phosphatase 2A network by chemical cross-linking and mass spectrometry Science 337 2012 1348 1352
18. P. Hong, S. Koza, and E.S. Bouvier Size-exclusion chromatography for the analysis of protein biotherapeutics and their aggregates J. Liquid Chromatogr. Relat. Technol. 35 2012 2923 2950
19. N.G. Housden, J.A. Wojdyla, J. Korczynska, I. Grishkovskaya, N. Kirkpatrick, A.M. Brzozowski, and C. Kleanthous Directed epitope delivery across the Escherichia coli outer membrane through the porin OmpF Proc. Natl. Acad. Sci. USA 107 2010 21412 21417
20. N.G. Housden, J.T. Hopper, N. Lukoyanova, D. Rodriguez-Larrea, J.A. Wojdyla, A. Klein, R. Kaminska, H. Bayley, H.R. Saibil, C.V. Robinson, and C. Kleanthous Intrinsically disordered protein threads through the bacterial outer-membrane porin OmpF Science 340 2013 1570 1574
21. G.J. Howlett, A.P. Minton, and G. Rivas Analytical ultracentrifugation for the study of protein association and assembly Curr. Opin. Chem. Biol. 10 2006 430 436
22. L.L. Ilag, I. Ubarretxena-Belandia, C.G. Tate, and C.V. Robinson Drug binding revealed by tandem mass spectrometry of a protein-micelle complex J. Am. Chem. Soc. 126 2004 14362 14363
23. S. Inagaki, R. Ghirlando, and R. Grisshammer Biophysical characterization of membrane proteins in nanodiscs Methods 59 2013 287 300
24. M.F. Jarrold Helices and sheets in vacuo Phys. Chem. Chem. Phys. 9 2007 1659 1671
25. E.N. Kitova, A. El-Hawiet, P.D. Schnier, and J.S. Klassen Reliable determinations of protein-ligand interactions by direct ESI-MS measurements. Are we there yet? J. Am. Soc. Mass Spectrom. 23 2012 431 441
26. L. Konermann, and Y. Pan Exploring membrane protein structural features by oxidative labeling and mass spectrometry Expert Rev. Proteomics 9 2012 497 504
27. A. Laganowsky, E. Reading, J.T. Hopper, and C.V. Robinson Mass spectrometry of intact membrane protein complexes Nat. Protoc. 8 2013 639 651
28. M. Landreh, J. Astorga-Wells, J. Johansson, T. Bergman, and H. Jörnvall New developments in protein structure-function analysis by MS and use of hydrogen-deuterium exchange microfluidics FEBS J. 278 2011 3815 3821
29. M. le Maire, B. Arnou, C. Olesen, D. Georgin, C. Ebel, and J.V. Møller Gel chromatography and analytical ultracentrifugation to determine the extent of detergent binding and aggregation, and Stokes radius of membrane proteins using sarcoplasmic reticulum Ca2+-ATPase as an example Nat. Protoc. 3 2008 1782 1795
30. J.A. Leary, M.R. Schenauer, R. Stefanescu, A. Andaya, B.T. Ruotolo, C.V. Robinson, K. Thalassinos, J.H. Scrivens, M. Sokabe, and J.W. Hershey Methodology for measuring conformation of solvent-disrupted protein subunits using T-WAVE ion mobility MS: an investigation into eukaryotic initiation factors J. Am. Soc. Mass Spectrom. 20 2009 1699 1706
31. A. Leitner, T. Walzthoeni, A. Kahraman, F. Herzog, O. Rinner, M. Beck, and R. Aebersold Probing native protein structures by chemical cross-linking, mass spectrometry, and bioinformatics Mol. Cell. Proteomics 9 2010 1634 1649
32. A.C. Leney, L.M. McMorran, S.E. Radford, and A.E. Ashcroft Amphipathic polymers enable the study of functional membrane proteins in the gas phase Anal. Chem. 84 2012 9841 9847
33. J. Lengqvist, R. Svensson, E. Evergren, R. Morgenstern, and W.J. Griffiths Observation of an intact noncovalent homotrimer of detergent-solubilized rat microsomal glutathione transferase-1 by electrospray mass spectrometry J. Biol. Chem. 279 2004 13311 13316
34. H.T. Lin, V.N. Bavro, N.P. Barrera, H.M. Frankish, S. Velamakanni, H.W. van Veen, C.V. Robinson, M.I. Borges-Walmsley, and A.R. Walmsley MacB ABC transporter is a dimer whose ATPase activity and macrolide-binding capacity are regulated by the membrane fusion protein MacA J. Biol. Chem. 284 2009 1145 1154
35. L. Liu, E.N. Kitova, and J.S. Klassen Quantifying protein-fatty acid interactions using electrospray ionization mass spectrometry J. Am. Soc. Mass Spectrom. 22 2011 310 318
36. J.A. Loo Studying noncovalent protein complexes by electrospray ionization mass spectrometry Mass Spectrom. Rev. 16 1997 1 23
37. J. Marcoux, S.C. Wang, A. Politis, E. Reading, J. Ma, P.C. Biggin, M. Zhou, H. Tao, Q. Zhang, and G. Chang Mass spectrometry reveals synergistic effects of nucleotides, lipids, and drugs binding to a multidrug resistance efflux pump Proc. Natl. Acad. Sci. USA 110 2013 9704 9709
38. M.T. Marty, A. Das, and S.G. Sligar Ultra-thin layer MALDI mass spectrometry of membrane proteins in nanodiscs Anal. Bioanal. Chem. 402 2012 721 729
39. M.T. Marty, H. Zhang, W. Cui, R.E. Blankenship, M.L. Gross, and S.G. Sligar Native mass spectrometry characterization of intact nanodisc lipoprotein complexes Anal. Chem. 84 2012 8957 8960
40. N. Morgner, and C.V. Robinson Massign: an assignment strategy for maximizing information from the mass spectra of heterogeneous protein assemblies Anal. Chem. 84 2012 2939 2948
41. J.L. Norris, and R.M. Caprioli Analysis of tissue specimens by matrix-assisted laser desorption/ionization imaging mass spectrometry in biological and clinical research Chem. Rev. 113 2013 2309 2342
42. A. Oliva, M. Llabrés, and J.B. Fariña Applications of multi-angle laser light-scattering detection in the analysis of peptides and proteins Curr. Drug Discov. Technol. 1 2004 229 242
43. A.Y. Park, and C.V. Robinson Protein-nucleic acid complexes and the role of mass spectrometry in their structure determination Crit. Rev. Biochem. Mol. Biol. 46 2011 152 164
44. A. Politis, A.Y. Park, Z. Hall, B.T. Ruotolo, and C.V. Robinson Integrative modelling coupled with ion mobility mass spectrometry reveals structural features of the clamp loader in complex with single-stranded DNA binding protein J. Mol. Biol. 2013
45. T.L. Pukala, B.T. Ruotolo, M. Zhou, A. Politis, R. Stefanescu, J.A. Leary, and C.V. Robinson Subunit architecture of multiprotein assemblies determined using restraints from gas-phase measurements Structure 17 2009 1235 1243
46. J.H. Ringrose, H.W. van den Toorn, M. Eitel, H. Post, P. Neerincx, B. Schierwater, A.F. Altelaar, and A.J. Heck Deep proteome profiling of Trichoplax adhaerens reveals remarkable features at the origin of metazoan multicellularity Nat. Commun. 4 2013 1408
47. C.V. Robinson, and S.E. Radford Weighing the evidence for structure: electrospray ionization mass spectrometry of proteins Structure 3 1995 861 865
48. C.V. Robinson, A. Sali, and W. Baumeister The molecular sociology of the cell Nature 450 2007 973 982
49. R.J. Rose, E. Damoc, E. Denisov, A. Makarov, and A.J. Heck High-sensitivity Orbitrap mass analysis of intact macromolecular assemblies Nat. Methods 9 2012 1084 1086
50. C. Schmidt, M. Zhou, H. Marriott, N. Morgner, A. Politis, and C.V. Robinson Comparative cross-linking and mass spectrometry of an intact F-type ATPase suggest a role for phosphorylation Nat. Commun. 4 2013 1985
51. A. Shevchenko, O.N. Jensen, A.V. Podtelejnikov, F. Sagliocco, M. Wilm, O. Vorm, P. Mortensen, A. Shevchenko, H. Boucherie, and M. Mann Linking genome and proteome by mass spectrometry: large-scale identification of yeast proteins from two dimensional gels Proc. Natl. Acad. Sci. USA 93 1996 14440 14445
52. A. Sinz Chemical cross-linking and mass spectrometry to map three-dimensional protein structures and protein-protein interactions Mass Spectrom. Rev. 25 2006 663 682
53. O.S. Skinner, K. Breuker, and F.W. McLafferty Charge site mass spectra: conformation-sensitive components of the electron capture dissociation spectrum of a protein J. Am. Soc. Mass Spectrom. 24 2013 807 810
54. J. Snijder, C. Uetrecht, R.J. Rose, R. Sanchez-Eugenia, G.A. Marti, J. Agirre, D.M. Guérin, G.J. Wuite, A.J. Heck, and W.H. Roos Probing the biophysical interplay between a viral genome and its capsid Nat. Chem. 5 2013 502 509
55. D. van der Spoel, E.G. Marklund, D.S. Larsson, and C. Caleman Proteins, lipids, and water in the gas phase Macromol. Biosci. 11 2011 50 59
56. S. Velamakanni, C.H. Lau, D.A. Gutmann, H. Venter, N.P. Barrera, M.A. Seeger, B. Woebking, D. Matak-Vinkovic, L. Balakrishnan, and Y. Yao A multidrug ABC transporter with a taste for salt PLoS ONE 4 2009 e6137
57. T.E. Wales, M.J. Eggertson, and J.R. Engen Considerations in the analysis of hydrogen exchange mass spectrometry data Methods Mol. Biol. 1007 2013 263 288
58. L. Wang, and M.R. Chance Structural mass spectrometry of proteins using hydroxyl radical based protein footprinting Anal. Chem. 83 2011 7234 7241
59. Z.Y. Wang, Y. Muraoka, M. Nagao, M. Shibayama, M. Kobayashi, and T. Nozawa Determination of the B820 subunit size of a bacterial core light-harvesting complex by small-angle neutron scattering Biochemistry 42 2003 11555 11560
60. P.G. Wolynes Biomolecular folding in vacuo!!!(?) Proc. Natl. Acad. Sci. USA 92 1995 2426 2427
61. T. Wyttenbach, and M.T. Bowers Structural stability from solution to the gas phase: native solution structure of ubiquitin survives analysis in a solvent-free ion mobility-mass spectrometry environment J. Phys. Chem. B 115 2011 12266 12275
62. M. Zhou, N. Morgner, N.P. Barrera, A. Politis, S.C. Isaacson, D. Matak-Vinković, T. Murata, R.A. Bernal, D. Stock, and C.V. Robinson Mass spectrometry of intact V-type ATPases reveals bound lipids and the effects of nucleotide binding Science 334 2011 380 385