Current limitations in native mass spectrometry based structural biology

Journal of the American Society for Mass Spectrometry

Volumn 21, Issue 6, 2010, Pages 971-978

  van Duijn, Esther ^a  

^a UTRECHT UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL ASSEMBLY; COMPLEX COMPOSITIONS; CURRENT LIMITATION; DETAILED MODELS; DISSOCIATION EFFICIENCY; INTACT PROTEINS; ION MOBILITY-MASS SPECTROMETRY; PROTEIN COMPLEXES; PROTEOMICS; STRUCTURAL BIOLOGY; TANDEM MASS SPECTROMETRIC ANALYSIS;

MOLECULAR BIOLOGY; PROTEINS;

MASS SPECTROMETRY;

ARTICLE; DISSOCIATION; ION MOBILITY SPECTROMETRY; MASS SPECTROMETRY; MOLECULAR BIOLOGY; MOLECULAR MODEL; PROTEIN DETERMINATION; PROTEIN MODIFICATION; PROTEIN STRUCTURE; PROTEOMICS; STRUCTURE ANALYSIS;

BIOCHEMISTRY; CHAPERONIN 60; ESCHERICHIA COLI PROTEINS; PROTEIN CONFORMATION; PROTEOMICS; TANDEM MASS SPECTROMETRY;

EID: 77952879872     PISSN: 10440305     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jasms.2009.12.010     Document Type: Article

References (73)

1. Gygi S.P., Rist B., Gerber S.A., Turecek F., Gelb M.H., Aebersold R. Quantitative Analysis of Complex Protein Mixtures using Isotope-Coded Affinity Tags. Nat. Biotechnol 1999, 17:994-999.
2. Heck A.J., Krijgsveld J. Mass Spectrometry-Based Quantitative Proteomics. Expert Rev. Proteom 2004, 1:317-326.
3. Hu Q., Noll R.J., Li H., Makarov A., Hardman M., Graham Cooks R. The Orbitrap: A New Mass Spectrometer. J. Mass Spectrom 2005, 40:430-443.
4. Makarov A. Electrostatic Axially Harmonic Orbital Trapping: A High-Performance Technique of Mass Analysis. Anal. Chem 2000, 72:1156-1162.
5. Ong S.E., Blagoev B., Kratchmarova I., Kristensen D.B., Steen H., Pandey A., Mann M. Stable Isotope Labeling by Amino Acids in Cell Culture, SILAC, as a Simple and Accurate Approach to Expression Proteomics. Mol. Cell. Proteom 2002, 1:376-386.
6. Syka J.E., Marto J.A., Bai D.L., Horning S., Senko M.W., Schwartz J.C., Ueberheide B., Garcia B., Busby S., Muratore T., Shabanowitz J., Hunt D.F. Novel Linear Quadrupole Ion trap/FT Mass Spectrometer: Performance Characterization and use in the Comparative Analysis of Histone H3 Post-Translational Modifications. J. Proteome Res 2004, 3:621-626.
7. Boersema P.J., Raijmakers R., Lemeer S., Mohammed S., Heck A.J. Multiplex Peptide Stable Isotope Dimethyl Labeling for Quantitative Proteomics. Nat. Protoc 2009, 4:484-494.
8. van den Heuvel R.H., Heck A.J. Native Protein Mass Spectrometry: From Intact Oligomers to Functional Machineries. Curr. Opin. Chem. Biol 2004, 8:519-526.
9. Kaddis C.S., Loo J.A. Native Protein MS and Ion Mobility Large Flying Proteins with ESI. Anal. Chem 2007, 79:1778-1784.
10. Ganem B., Li Y.T., Henion J.D. Detection of Noncovalent Receptor-Ligand Complexes by Mass Spectrometry. J. Am. Chem. Soc 1991, 113:6294-6296.
11. Videler H., Ilag L.L., McKay A.R., Hanson C.L., Robinson C.V. Mass Spectrometry of Intact Ribosomes. FEBS Lett 2005, 579:943-947.
12. Uetrecht C., Versluis C., Watts N.R., Roos G.J.L., Wingfield P.T., Steven A.C., Heck A.J. 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, 105:9216-9220.
13. van Duijn, E.; Barendregt, A.; Uetrecht, C.; Lorenzen, K.; Rose, R. J.; Shoemaker, G.; Heck, A. J. Investigation of Intact Protein Complexes and Protein-Protein Interactions by Native Ion Mobility and Tandem Mass Spectrometry. Proceedings of the 57th ASMS Conference; Philadelphia, May 31-June 4, 2009.
14. Hartl F.U., Hayer-Hartl M. Molecular Chaperones in the Cytosol: From Nascent Chain to Folded Protein. Science 2002, 295:1852-1858.
15. Hartl F.U., Hayer-Hartl M. Converging Concepts of Protein Folding In Vitro and In Vivo. Nat. Struct. Mol. Biol 2009, 16:574-581.
16. Ross C.A., Poirier M.A. Protein Aggregation and Neurodegenerative Disease. Nat. Med 2004, 10(Suppl.):10-17.
17. Benesch J.L., Ruotolo B.T., Simmons D.A., Robinson C.V. Protein Complexes in the Gas Phase: Technology for Structural Genomics and Proteomics. Chem. Rev 2007, 107:3544-3567.
18. Heck A.J., van Den Heuvel R.H. Investigation of Intact Protein Complexes by Mass Spectrometry. Mass Spectrom Rev 2004, 23:368-389.
19. Heck A.J. Native Mass Spectrometry: A Bridge Between Interactomics and Structural Biology. Nat. Methods 2008, 5:927-933.
20. Lorenzen K., Vannini A., Cramer P., Heck A.J. Structural Biology of RNA Polymerase III: Mass Spectrometry Elucidates Subcomplex Architecture. Structure 2007, 15:1237-1245.
21. Ruotolo B.T., Benesch J.L., Sandercock A.M., Hyung S.J., Robinson C.V. Ion Mobility-Mass Spectrometry Analysis of Large Protein Complexes. Nat. Protoc. 2008, 3:1139-1152.
22. Sharon M., Robinson C.V. The Role of Mass Spectrometry in Structure Elucidation of Dynamic Protein Complexes. Annu. Rev. Biochem 2007, 76:167-193.
23. Sharon M., Mao H., Boeri Erba E., Stephens E., Zheng N., Robinson C.V. Symmetrical Modularity of the COP9 Signalosome Complex Suggests Its Multifunctionality. Structure 2009, 17:31-40.
24. Taverner T., Hernandez H., Sharon M., Ruotolo B.T., Matak-Vinkovic D., Devos D., Russell R.B., Robinson C.V. Subunit Architecture of Intact Protein Complexes from Mass Spectrometry and Homology Modeling. Acc. Chem. Res. 2008, 41:617-627.
25. van Duijn E., Barendregt A., Synowsky S., Versluis C., Heck A.J. Chaperonin Complexes Monitored by Ion Mobility Mass Spectrometry. J. Am. Chem. Soc. 2009, 131:1452-1459.
26. Robinson C.V., Sali A., Baumeister W. The Molecular Sociology of the Cell. Nature 2007, 450:973-982.
27. Mohammed S., Lorenzen K., Kerkhoven R., van Breukelen B., Vannini A., Cramer P., Heck A.J. Multiplexed Proteomics Mapping of Yeast RNA Polymerase II and III Allows Near-Complete Sequence Coverage and Reveals several Novel Phosphorylation Sites. Anal. Chem. 2008, 80:3584-3592.
28. Sobott F., Hernandez H., McCammon M.G., Tito M.A., Robinson C.V. A Tandem Mass Spectrometer for Improved Transmission and Analysis of Large Macromolecular Assemblies. Anal. Chem. 2002, 74:1402-1407.
29. Ruotolo B.T., Giles K., Campuzano I., Sandercock A.M., Bateman R.H., Robinson C.V. Evidence for Macromolecular Protein Rings in the Absence of Bulk Water. Science 2005, 310:1658-1661.
30. Pringle S.D., Giles K., Wildgoose J.L., Williams J.P., Slade S.E., Thalassinos K., Bateman R.H., Bowers M.T., Scrivens J.H. An Investigation of the Mobility Separation of Some Peptide and Protein Ions using a New Hybrid Quadrupole/Traveling Wave IMS/oa-TOF Instrument. Int. J. Mass Spectrom. 2007, 261:1-12.
31. Lorenzen K., Olia A.S., Uetrecht C., Cingolani G., Heck A.J. Determination of Stoichiometry and Conformational Changes in the First Step of the P22 Tail Assembly. J. Mol. Biol. 2008, 379:385-396.
32. Benesch J.L., Aquilina J.A., Ruotolo B.T., Sobott F., Robinson C.V. Tandem Mass Spectrometry Reveals the Quaternary Organization of Macromolecular Assemblies. Chem. Biol. 2006, 13:597-605.
33. Benesch J.L. Collisional Activation of Protein Complexes: Picking Up the Pieces. J. Am. Soc. Mass Spectrom. 2009, 20:341-348.
34. Benesch J.L., Ayoub M., Robinson C.V., Aquilina J.A. Small Heat Shock Protein Activity is Regulated by Variable Oligomeric Substructure. J. Biol. Chem. 2008, 283:28513-28517.
35. McCammon M.G., Scott D.J., Keetch C.A., Greene L.H., Purkey H.E., Petrassi H.M., Kelly J.W., Robinson C.V. Screening Transthyretin Amyloid Fibril Inhibitors: Characterization of Novel Multiprotein, Multiligand Complexes by Mass Spectrometry. Structure 2002, 10:851-863.
36. Poliakov A., van Duijn E., Lander G., Fu C.Y., Johnson J.E., Prevelige P.E., Heck A.J. Macromolecular Mass Spectrometry and Electron Microscopy as Complementary Tools for Investigation of the Heterogeneity of Bacteriophage Portal Assemblies. J. Struct. Biol 2007, 157:371-383.
37. de Geus D.C., Thomassen E.A., Hagedoorn P.L., Pannu N.S., van Duijn E., Abrahams J.P. Crystal Structure of Chlorite Dismutase, a Detoxifying Enzyme Producing Molecular Oxygen. J. Mol. Biol. 2009, 387:192-206.
38. Loo J.A., Berhane B., Kaddis C.S., Wooding K.M., Xie Y., Kaufman S.L., Chernushevich I.V. Electrospray Ionization Mass Spectrometry and Ion Mobility Analysis of the 20S Proteasome Complex. J. Am. Soc. Mass Spectrom. 2005, 16:998-1008.
39. van Duijn E., Bakkes P.J., Heeren R.M., van den Heuvel R.H., van Heerikhuizen H., van der Vies S.M., Heck A.J. Monitoring Macromolecular Complexes Involved in the Chaperonin-Assisted Protein Folding Cycle by Mass Spectrometry. Nat. Methods 2005, 2:371-376.
40. Zhou M., Sandercock A.M., Fraser C.S., Ridlova G., Stephens E., Schenauer M.R., Yokoi-Fong T., Barsky D., Leary J.A., Hershey J.W., Doudna J.A., Robinson C.V. Mass Spectrometry Reveals Modularity and a Complete Subunit Interaction Map of the Eukaryotic Translation Factor eIF3. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:18139-18144.
41. Black L.W. DNA Packaging in dsDNA Bacteriophages. Annual Review of Microbiology. 1989, 43:267-292.
42. Mitchell M.S., Rao V.B. Functional Analysis of the Bacteriophage T4 DNA-Packaging ATPase Motor. The J. Biol. Chem. 2006, 281:518-527.
43. Williams R.S., Williams G.J., Tainer J.A. A Charged Performance by gp17 in Viral Packaging. Cell 2008, 135:1169-1171.
44. Lin H., Simon M.N., Black L.W. Purification and Characterization of the Small Subunit of Phage T4 Terminase, gp16, Required for DNA Packaging. J. Biol. Chem. 1997, 272:3495-3501.
45. van Breukelen B., Barendregt A., Heck A.J., van den Heuvel R.H. Resolving Stoichiometries and Oligomeric States of Glutamate Synthase Protein Complexes with Curve Fitting and Simulation of Electrospray Mass Spectra. Rapid Commun. Mass Spectrom. 2006, 20:2490-2496.
46. Sun S., Kondabagil K., Draper B., Alam T.I., Bowman V.D., Zhang Z., Hegde S., Fokine A., Rossmann M.G., Rao V.B. The Structure of the Phage T4 DNA Packaging Motor Suggests a Mechanism Dependent on Electrostatic Forces. Cell 2008, 135:1251-1262.
47. Hernandez H., Robinson C.V. Determining the Stoichiometry and Interactions of Macromolecular Assemblies from Mass Spectrometry. Nat. Protoc. 2007, 2:715-726.
48. Lorenzen, K.; van Duijn, E. Native Mass Spectrometry as a Tool in Structural Biology. Curr. Protoc. Protein Sci. accepted.
49. Bartesaghi A., Subramaniam S. Membrane Protein Structure Determination using Cryo-Electron Tomography and 3D Image Averaging. Curr. Opin. Struct. Biol. 2009, 19:402-407.
50. Raunser S., Walz T. Electron Crystallography as a Technique to Study the Structure on Membrane Proteins in a Lipidic Environment. Annu. Rev. Biophys. 2009, 38:89-105.
51. Barrera N.P., Isaacson S.C., Zhou M., Bavro V.N., Welch A., Schaedler T.A., Seeger M.A., Miguel R.N., Korkhov V.M., van Veen H.W., Venter H., Walmsley A.R., Tate C.G., Robinson C.V. Mass Spectrometry of Membrane Transporters Reveals Subunit Stoichiometry and Interactions. Nat. Methods 2009, 6:585-587.
52. Barrera N.P., Di Bartolo N., Booth P.J., Robinson C.V. Micelles Protect Membrane Complexes from Solution to Vacuum. Science 2008, 321:243-246.
53. van den Heuvel R.H., van Duijn E., Mazon H., Synowsky S.A., Lorenzen K., Versluis C., Brouns S.J., Langridge D., van der Oost J., Hoyes J., Heck A.J. Improving the Performance of a Quadrupole Time-of-Flight Instrument for Macromolecular Mass Spectrometry. Anal. Chem. 2006, 78:7473-7483.
54. van Duijn E., Simmons D.A., van den Heuvel R.H., Bakkes P.J., van Heerikhuizen H., Heeren R.M., Robinson C.V., van der Vies S.M., Heck A.J. Tandem Mass Spectrometry of Intact GroEL-Substrate Complexes Reveals Substrate-Specific Conformational Changes in the Trans Ring. J. Am. Chem. Soc. 2006, 128:4694-4702.
55. Lomeli S.H., Yin S., Ogorzalek Loo R.R., Loo J.A. Increasing Charge While Preserving Noncovalent Protein Complexes for ESI-MS. J. Am. Soc. Mass Spectrom. 2009, 20:593-596.
56. Lomeli S.H., Peng I.X., Yin S., Loo R.R.O., Loo J.A. New Reagents for Increasing ESI Multiple Charging of Proteins and Protein Complexes. J. Am. Soc. Mass Spectrom 2010, 21:126-131.
57. Pukala T.L., Ruotolo B.T., Zhou M., Politis A., Stefanescu R., Leary J.A., Robinson C.V. Subunit Architecture of Multiprotein Assemblies Determined Using Restraints from Gas-Phase Measurements. Structure 2009, 17:1235-1243.
58. Smith L.M. Is Charge Reduction in ESI really Necessary?. J. Am. Soc. Mass Spectrom. 2008, 19:629-631.
59. Frey B.L., Krusemark C.J., Ledvina A.R., Coon J.J., Belshaw P.J., Smith L.M. Ion-Ion Reactions with Fixed-Charge Modified Proteins to Produce Ions in a Single, Very High Charge State. Int. J. Mass Spectrom. 2008, 276:136-143.
60. Pitteri S.J., McLuckey S.A. Recent Developments in the Ion/Ion Chemistry of High-Mass Multiply Charged Ions. Mass Spectrom. Rev. 2005, 24:931-958.
61. Xie Y., Zhang J., Yin S., Loo J.A. Top-Down ESI-ECD-FT-ICR Mass Spectrometry Localizes Noncovalent Protein-Ligand Binding Sites. J. Am. Chem. Soc. 2006, 128:14432-14433.
62. Breuker K., Jin M., Han X., Jiang H., McLafferty F.W. Top-Down Identification and Characterization of Biomolecules by Mass Spectrometry. J. Am. Soc. Mass Spectrom. 2008, 19:1045-1053.
63. Uetrecht, C., Rose, R. J., van Duijn, E., Lorenzen, K., Heck, A. J. Ion Mobility Mass Spectrometry of Proteins and Protein Assemblies. Chem. Soc. Rev. in press.
64. Liu L., Bagal D., Kitova E.N., Schnier P.D., Klassen J.S. Hydrophobic Protein-Ligand Interactions Preserved in the Gas Phase. J. Am. Chem. Soc. 2009, 131:15980-15981.
65. Ruotolo B.T., Hyung S.J., Robinson P.M., Giles K., Bateman R.H., Robinson C.V. Ion Mobility-Mass Spectrometry Reveals Long-Lived, Unfolded Intermediates in the Dissociation of Protein Complexes. Angew. Chem. Int 2007, 46:8001-8004.
66. Uetrecht C., Versluis C., Watts N.R., Wingfield P.T., Steven A.C., Heck A.J. Stability and Shape of Hepatitis B Virus Capsids In Vacuo. Angew. Chem. Int. Ed. Engl. 2008, 47:6247-6251.
67. Catalina M.I., van den Heuvel R.H., van Duijn E., Heck A.J. Decharging of Globular Proteins and Protein Complexes in Electrospray. Chemistry 2005, 11:960-968.
68. Sun J., Kitova E.N., Klassen J.S. Method for Stabilizing Protein-Ligand Complexes in Nanoelectrospray Ionization Mass Spectrometry. Anal. Chem. 2007, 79:416-425.
69. Ebeling D.D., Westphall M.S., Scalf M., Smith L.M. Corona Discharge in Charge Reduction Electrospray Mass Spectrometry. Anal. Chem. 2000, 72:5158-5161.
70. Chen X., Westphall M.S., Smith L.M. Mass Spectrometric Analysis of DNA Mixtures: Instrumental Effects Responsible for Decreased Sensitivity with Increasing Mass. Anal. Chem. 2003, 75:5944-5952.
71. Giles K., Pringle S.D., Worthington K.R., Little D., Wildgoose J.L., Bateman R.H. Applications of a Traveling Wave-Based Radio-Frequency-Only Stacked Ring Ion Guide. Rapid Commun. Mass Spectrom. 2004, 18:2401-2414.
72. Clemmer Cross Section Database. http://Http://www.Indiana.edu/~clemmer.
73. Bakkes P.J., Faber B.W., van Heerikhuizen H., van der Vies S.M. The T4-Encoded Cochaperonin, gp31, Has Unique Properties that Explain Its Requirement for the Folding of the T4 Major Capsid Protein. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:8144-8149.