Evidence for two new solution states of ubiquitin by IMS-MS analysis

Journal of Physical Chemistry B

Volumn 118, Issue 13, 2014, Pages 3498-3506

  Shi, Huilin ^a   Clemmer, David E ^a  

^a INDIANA UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHARGE STATE; CHARGE STATE DISTRIBUTION; DENATURING CONDITIONS; ION MOBILITY; ION MOBILITY SPECTROMETRY; RELATIVE ABUNDANCE; SOLUTION STRUCTURES; SUBSTANTIAL VARIATIONS;

ION MOBILITY SPECTROMETERS; MASS SPECTROMETRY; PROTEINS; URANIUM;

METHANOL;

ION; METHANOL; SOLUTION AND SOLUBILITY; UBIQUITIN; WATER;

CHEMISTRY; ELECTROSPRAY MASS SPECTROMETRY; METABOLISM; SOLUTION AND SOLUBILITY;

IONS; METHANOL; SOLUTIONS; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION; UBIQUITIN; WATER;

EID: 84898072896     PISSN: 15206106     EISSN: 15205207     Source Type: Journal    
DOI: 10.1021/jp4097327     Document Type: Article

References (67)

1. Ishima, R.; Torchia, D. A. Protein Dynamics from NMR Nat. Struct. Biol. 2000, 7, 740-743
2. Bahar, I.; Lezon, T. R.; Yang, L.-W.; Eyal, E. Global Dynamics of Proteins: Bridging Between Structure and Function Annu. Rev. Biophys. 2010, 39, 23-42
3. Chowdhury, S. K.; Katta, V.; Chait, B. T. An Electrospray-Ionization Mass Spectrometer with New Features Rapid Commun. Mass Spectrom. 1990, 4, 81-87
4. Suckau, D.; Shi, Y.; Beu, S. C.; Senko, M. W.; Quinn, J. P.; Wampler, F. M.; McLafferty, F. W. Coexisting Stable Conformations of Gaseous Protein Ions Proc. Natl. Acad. Sci. U. S. A. 1993, 90, 790-793
5. Konermann, L.; Rosell, F. I.; Mauk, A. G.; Douglas, D. J. Acid-Induced Denaturation of Myoglobin Studied by Time-Resolved Electrospray Ionization Mass Spectrometry Biochemistry 1997, 36, 6448-6454
6. Frimpong, A. K.; Abzalimov, R. R.; Eyles, S. J.; Kaltashov, I. A. Gas-Phase Interference-Free Analysis of Protein Ion Charge-State Distributions: Detection of Small-Scale Conformational Transitions Accompanying Pepsin Inactivation Anal. Chem. 2007, 79, 4154-4161
7. Kaltashov, I. A.; Abzalimov, R. R. Do Ionic Charges in ESI MS Provide Useful Information on Macromolecular Structure? J. Am. Soc. Mass Spectrom. 2008, 19, 1239-1246
8. Konermann, L.; Ahadi, E.; Rodriguez, A. D.; Vahidi, S. Unraveling the Mechanism of Electrospray Ionization Anal. Chem. 2013, 85, 2-9
9. Stahl-Zeng, J.; Lange, V.; Ossola, R.; Eckhardt, K.; Krek, W.; Aebersold, R.; Domon, B. High Sensitivity Detection of Plasma Proteins by Multiple Reaction Monitoring of N-Glycosites Mol. Cell. Proteomics 2007, 6, 1809-1817
10. Heck, A. J. R. Native Mass Spectrometry: a Bridge Between Interactomics and Structural Biology Nat. Methods 2008, 5, 927-933
11. Clemmer, D. E.; Jarrold, M. F. Ion Mobility Measurements and their Applications to Clusters and Biomolecules J. Mass Spectrom. 1997, 32, 577-592
12. Clemmer, D. E.; Hudgins, R. R.; Jarrold, M. F. Naked Protein Conformations: Cytochrome c in the Gas Phase J. Am. Chem. Soc. 1995, 117, 10141-10142
13. Bohrer, B. C.; Merenbloom, S. I.; Koeniger, S. L.; Hilderbrand, A. E.; Clemmer, D. E. Biomolecule Analysis by Ion Mobility Spectrometry Annu. Rev. Anal. Chem. 2008, 1, 293-327
14. Liu, X.; Valentine, S. J.; Plasencia, M. D.; Trimpin, S.; Naylor, S.; Clemmer, D. E. Mapping the Human Plasma Proteome by SCX-LC-IMS-MS J. Am. Soc. Mass Spectrom. 2007, 18, 1249-1264
15. Gaye, M. M.; Valentine, S. J.; Hu, Y.; Mirjankar, N.; Hammoud, Z. T.; Mechref, Y.; Lavine, B. K.; Clemmer, D. E. Ion Mobility-Mass Spectrometry Analysis of Serum N-Linked Glycans from Esophageal Adenocarcinoma Phenotypes J. Proteome. Res. 2012, 11, 6102-6110
16. 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
17. Uetrecht, C.; Barbu, I. M.; Shoemaker, G. K.; van Duijn, E.; Heck, A. J. R. Interrogating Viral Capsid Assembly with Ion Mobility-Mass Spectrometry Nat. Chem. 2011, 3, 126-132
18. Zhang, Z.; Smith, D. L. Determination of Amide Hydrogen Exchange by Mass Spectrometry: a New Tool for Protein Structure Elucidation Protein Sci. 1993, 2, 522-531
19. Konermann, L.; Pan, J.; Liu, Y.-H. Hydrogen Exchange Mass Spectrometry for Studying Protein Structure and Dynamics Chem. Soc. Rev. 2011, 40, 1224-1234
20. Breuker, K.; Oh, H. B.; Horn, D. M.; Cerda, B. A.; McLafferty, F. W. Detailed Unfolding and Folding of Gaseous Ubiquitin Ions Characterized by Electron Capture Dissociation J. Am. Chem. Soc. 2002, 124, 6407-6420
21. Robinson, E. W.; Leib, R. D.; Williams, E. R. the Role of Conformation on Electron Capture Dissociation of Ubiquitin J. Am. Soc. Mass Spectrom. 2006, 17, 1469-1479
22. Skinner, O. S.; McLafferty, F. W.; Breuker, K. How Ubiquitin Unfolds after Transfer into the Gas Phase J. Am. Soc. Mass Spectrom. 2012, 23, 1011-1014
23. Gau, B. C.; Sharp, J. S.; Rempel, D. L.; Gross, M. L. Fast Photochemical Oxidation of Protein Footprints Faster than Protein Unfolding Anal. Chem. 2009, 81, 6563-6571
24. Chen, J.; Rempel, D. L.; Gau, B. C.; Gross, M. L. Fast Photochemical Oxidation of Proteins and Mass Spectrometry Follow Submillisecond Protein Folding at the Amino-Acid Level J. Am. Soc. Chem. 2012, 134, 18724-18731
25. Bleiholder, C.; Dupuis, N. F.; Wyttenbach, T.; Bowers, M. T. Ion Mobility-Mass Spectrometry Reveals a Conformational Conversion from Random Assembly to β-Sheet in Amyloid Fibril Formation Nat. Chem. 2011, 2, 172-177
26. Wilson, D. J.; Rafferty, S. P.; Konermann, L. Kinetic Unfolding Mechanism of the Inducible Nitric Oxide Synthase Oxygenase Domain Determined by Time-Resolved Electrospray Mass Spectrometry Biochemistry 2005, 44, 2276-2283
27. Pan, J.; Han, J.; Borchers, C. H.; Konermann, L. Characterizing Short-Lived Protein Folding Intermediates by Top-Down Hydrogen Exchange Mass Spectrometry Anal. Chem. 2010, 82, 8591-8597
28. Mason, E. A.; McDaniel, E. W. Transport Properties of Ions in Gases; Wiley: New York, 1988.
29. Mesleh, M. F.; Hunter, J. M.; Shvartsburg, A. A.; Schatz, G. C.; Jarrold, M. F. Structural Information from Ion Mobility Measurements: Effects of the Long-Range Potential J. Phys. Chem. 1996, 100, 16082-16086
30. Wyttenbach, T.; von Helden, G.; Batka, J. J.; Carlat, D.; Bowers, M. T. Effect of the Long-Range Potential on Ion Mobility Measurements J. Am. Soc. Mass Spectrom. 1997, 8, 275-282
31. Politis, A.; Park, A. Y.; Hyung, S.-J.; Barsky, D.; Ruotolo, B. T.; Robinson, C. V. Integrating Ion Mobility Mass Spectrometry with Molecular Modeling to Determine the Architecture of Multiprotein Complexes PLoS ONE 2010, 5, e12080
32. Hoaglund, C. S.; Valentine, S. J.; Sporleder, C. R.; Reilly, J. P.; Clemmer, D. E. Three-Dimensional Ion Mobility/TOFMS Analysis of Electrosprayed Biomolecules Anal. Chem. 1998, 70, 2236-2242
33. Loo, J. A. Studying Noncovalent Protein Complexes by Electrospray Ionization Mass Spectrometry Mass Spectrom. Rev. 1997, 16, 1-23
34. Loo, J. A.; He, J. X.; Cody, W. L. Higher Order Structure in the Gas Phase Reflects Solution Structure J. Am. Chem. Soc. 1998, 120, 4542-4543
35. Ruotolo, B. T.; Robinson, C. V. Aspects of Native Proteins are Retained in Vacuum Curr. Opin. Chem. Biol. 2006, 10, 402-408
36. Koeniger, S. L.; Merenbloom, S. I.; Sevugarajan, S.; Clemmer, D. E. Transfer of Structural Elements from Compact to Extended States in Unsolvated Ubiquitin J. Am. Chem. Soc. 2006, 128, 11713-11719
37. 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
38. Wyttenbach, T.; Bowers, M. T. 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 2011, 115, 12266-12275
39. Valentine, S. J.; Anderson, J. G.; Ellington, A. D.; Clemmer, D. E. Disulfide-Intact and -Reduced Lysozyme in the Gas Phase: Conformations and Pathways of Folding and Unfolding J. Phys. Chem. B 1997, 101, 3891-3900
40. Valentine, S. J.; Counterman, A. E.; Clemmer, D. E. Conformer-Dependent Proton-Transfer Reactions of Ubiquitin Ions J. Am. Soc. Mass. Spectrom. 1997, 8, 954-961
41. Goldstein, G.; Scheid, M.; Hammerling, U.; Boyse, E. A.; Schlesinger, D. H.; Niall, H. D. Isolation of a Polypeptide that Has Lymphocyte-Differentiating Properties and is Probably Represented Universally in Living Cells Proc. Natl. Acad. Sci. U. S. A. 1975, 72, 11-15
42. Rechsteiner, M. Ubiquitin; Plenum Press: New York, 1988.
43. Wilkinson, K. D.; Cox, M. J.; O'Connor, L. B.; Shapira, R. Structure and Activities of a Variant Ubiquitin Sequence from Bakers' Yeast Biochemistry 1986, 25, 4999-5004
44. Vijay-Kumar, S.; Bugg, C. E.; Wilkinson, K. D.; Vierstra, R. D.; Hatfield, P. M.; Cook, W. J. Comparison of the Three-Dimensional Structures of Human, Yeast, and Oat Ubiquitin J. Biol. Chem. 1987, 262, 6396-6399
45. Jentsch, S. The Ubiquitin-Conjugation System Annu. Rev. Genet. 1992, 26, 179-207
46. Lenkinski, R. E.; Chen, D. M.; Glickson, J. D.; Goldstein, G. Nuclear Magnetic Resonance Studies of Denaturation of Ubiquitin Biochim. Biophys. Acta 1977, 494, 126-130
47. Wilkinson, K. D.; Mayer, A. N. Alcohol-Induced Conformational Changes of Ubiquitin Arch. Biochem. Biophys. 1986, 250, 390-399
48. Harding, M. M.; Williams, D. H.; Woolfson, D. N. Characterization of a Partially Denatured State of a Protein by Two-Dimensional NMR: Reduction of the Hydrophobic Interactions in Ubiquitin Biochemistry 1991, 30, 3120-3128
49. Vijay-Kumar, S.; Bugg, C. E.; Cook, W. J. Structure of Ubiquitin Refined at 1.8 Å Resolution J. Mol. Biol. 1987, 194, 531-544
50. Pan, Y.; Briggs, M. S. Hydrogen Exchange in Native and Alcohol Forms of Ubiquitin Biochemistry 1992, 31, 11405-11412
51. Stockman, B. J.; Euvrard, A.; Scahill, T. A. Heteronuclear Three-Dimensional NMR Spectroscopy of a Partially Denatured Protein: the A-state of Human Ubiquitin J. Biomol. NMR 1993, 3, 285-296
52. Cox, J. P. L.; Evans, P. A.; Packman, L. C.; Williams, D. H.; Woolfson, D. N. Dissecting the Structure of a Partially Folded Protein Circular Dichroism and Nuclear Magnetic Resonance Studies of Peptides from Ubiquitin J. Mol. Biol. 1993, 234, 483-492
53. Brutscher, B.; Brüschweiler, R.; Ernst, R. R. Backbone Dynamics and Structural Characterization of the Partially Folded A State of Ubiquitin by 1H, 13C, and 15N Nuclear Magnetic Resonance Spectroscopy Biochemistry 1997, 36, 13043-13053
54. Cordier, F.; Grzesiek, S. Quantitative Comparison of the Hydrogen Bond Network of A-State and Native Ubiquitin by Hydrogen Bond Scalar Couplings Biochemistry 2004, 43, 11295-11301
55. Kony, D. B.; Hünenberger, P. H.; van Gunsteren, W. F. Molecular Dynamics Simulations of the Native and Partially Folded States of Ubiquitin: Influence of Methanol Cosolvent, pH and Temperature on the protein Structure and Dynamics Protein Sci. 2007, 16, 1101-1118
56. Pierson, N. A.; Chen, L.; Valentine, S. J.; Russell, D. H.; Clemmer, D. E. Number of Solution States of Bradykinin from Ion Mobility and Mass Spectrometry Measurements J. Am. Chem. Soc. 2011, 133, 13810-13813
57. Silveira, J. A.; Fort, K. L; Kim, D. Y.; Servage, K. A.; Pierson, N. A.; Clemmer, D. E.; Russell, D. H. From Solution to the Gas Phase: Stepwise Dehydration and Kinetic Trapping of Substance P Reveals the Origin of Peptide Conformations J. Am. Chem. Soc. 2013, 135, 19147-19153
58. 8+ Ions from Water:Methanol Solutions: Evidence for the N and A States in Aqueous Solution J. Phys. Chem. B 2012, 116, 3344-3352
59. Shi, H.; Gu, L.; Clemmer, D. E.; Robinson, R. A. S. Effects of Fe(II)/H2O2 Oxidation on Ubiquitin Conformers Measured by Ion Mobility-Mass Spectrometry J. Phys. Chem. B 2013, 117, 164-173
60. Revercomb, H. E.; Mason, E. A. Theory of Plasma Chromatography/Gaseous Electrophoresis-A Review Anal. Chem. 1975, 47, 970-983
61. Shvartsburg, A. A.; Jarrold, M. F. An Exact Hard-Spheres Scattering Model for the Mobilities of Polyatomic Ions Chem. Phys. Lett. 1996, 261, 86-91
62. Dugourd, Ph.; Hudgins, R. R.; Clemmer, D. E.; Jarrold, M. F. High-Resolution Ion Mobility Measurements Rev. Sci. Instrum. 1997, 68, 1122-1129
63. Hoaglund-Hyzer, C. S.; Clemmer, D. E. Ion Trap/Ion Mobility/Quadrupole/ Time-of-Flight Mass Spectrometry for Peptide Mixture Analysis Anal. Chem. 2001, 73, 177-184
64. Tang, K.; Shvartsburg, A. A.; Lee, H.-N.; Prior, D. C.; Buschbach, M. A.; Li, F.; Tolmachev, A. V.; Anderson, G. A.; Smith, R. D. High-Sensitivity Ion Mobility Spectrometry/Mass Spectrometry Using Electrodynamic Ion Funnel Interfaces Anal. Chem. 2005, 77, 3330-3339
65. Koeniger, S. L.; Merenbloom, S. I.; Valentine, S. J.; Jarrold, M. F.; Udseth, H. R.; Smith, R. D.; Clemmer, D. E. An IMS-IMS Analogue of MS-MS Anal. Chem. 2006, 78, 4161-4174
66. Katta, V.; Chait, B. T. Hydrogen/Deuterium Exchange Electrospray Ionization Mass Spectrometry: a Method for Probing Protein Conformational Changes in Solution J. Am. Chem. Soc. 1993, 115, 6317-6321
67. Koeniger, S. L.; Clemmer, D. E. Resolution and Structural Transitions of Elongated States of Ubiquitin J. Am. Soc. Mass Spectrom. 2007, 18, 322-331