Solution dependence of the collisional activation of ubiquitin [M + 7H]7+ ions

Journal of the American Society for Mass Spectrometry

Volumn 25, Issue 12, 2014, Pages 2000-2008

  Shi, Huilin ^a   Atlasevich, Natalya ^a,b   Merenbloom, Samuel I ^a,c   Clemmer, David E ^a  

^a INDIANA UNIVERSITY   (United States)

^b METROPOLITAN MUSEUM OF ART   (United States)

^c MDS SCIEX   (Canada)

Author keywords

Gas phase activation; Ion mobility spectrometry; Solution populations; Ubiquitin

Indexed keywords

ION; METHANOL; UBIQUITIN; WATER; GAS;

ALPHA HELIX; AQUEOUS SOLUTION; ARTICLE; BETA SHEET; CHEMICAL COMPOSITION; CHEMICAL STRUCTURE; CIRCULAR DICHROISM; CRYSTAL STRUCTURE; ELECTRIC FIELD; ELECTRIC POTENTIAL; GAS; HEATING; ION MOBILITY SPECTROMETRY; MASS SPECTROMETRY; PROTEIN CONFORMATION; PROTEIN UNFOLDING; X RAY CRYSTALLOGRAPHY; CHEMISTRY; ELECTROSPRAY MASS SPECTROMETRY;

GASES; IONS; METHANOL; MODELS, MOLECULAR; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION; UBIQUITIN; WATER;

EID: 84919930201     PISSN: 10440305     EISSN: 18791123     Source Type: Journal    
DOI: 10.1007/s13361-014-0834-y     Document Type: Article

References (66)

1. Dobson, C.M.: Protein folding and misfolding. Nature 426, 884-890 (2003)
2. Brockwell, D.J.; Radford, S.E.: Intermediates: ubiquitous species on folding energy landscapes? Curr. Opin. Struct. Biol. 17, 30-37 (2007)
3. Dill, K.A.; Ozkan, S.B.; Shell, M.S.; Weikl, T.R.: The protein folding problem. Annu. Rev. Biophys. 37, 289-316 (2008)
4. Freddolino, P.L.; Harrison, C.B.; Liu, Y.; Schulten, K.: Challenges in protein-folding simulations. Nat. Phys. 6, 751-758 (2010)
5. Roder, H.; Maki, K.; Cheng, H.: Early events in protein folding explored by rapid mixing methods. Chem. Rev. 106, 1836-1861 (2006)
6. Bartlett, A.I.; Radford, S.E.: An expanding arsenal of experimental methods yields and explosion of insights into protein folding mechanisms. Nat. Struct. Mol. Biol. 16, 582-588 (2009)
7. Schuler, B.; Eaton, W.A.: Protein folding studied by single-molecule FRET. Curr. Opin. Struct. Biol. 18, 16-26 (2008)
8. Korzhnev, D.M.; Religa, T.L.; Banachewicz, W.; Fersht, A.R.; Kay, L.E.: A transient and low-populated protein-folding intermediate at atomic resolution. Science 329, 1312-1316 (2010)
9. Gianni, S.; Ivarsson, Y.; De Simone, A.; Travaglini-Allocatelli, C.; Brunori, M.; Vendruscolo, M.: Structural characterization of a misfolded intermediate populated during the folding process of a PDZ domain. Nat. Struct. Mol. Biol. 17, 1431-1438 (2010)
10. Rennella, E.; Cutuil, T.; Schanda, P.; Ayala, I.; Forge, V.; Brutscher, B.: Real-time NMR characterization of structure and dynamics in a transiently populated protein folding intermediate. J. Am. Chem. Soc. 134, 8066-8069 (2012)
11. Konermann, L.; Pan, J.; Liu, Y.-H.: Hydrogen exchange mass spectrometry for studying protein structure and dynamics. Chem. Soc. Rev. 40, 1224-1234 (2011)
12. Skinner, O.S.; McLafferty, F.W.; Breuker, K.: How ubiquitin unfolds after transfer into the gas phase. J. Am. Soc. Mass Spectrom. 23, 1011-1014 (2012)
13. Zhang, H.; Cui, W.; Gross, M.L.: Native electrospray ionization and electron-capture dissociation for comparison of protein structure in solution and the gas phase. Int. J. Mass Spectrom. 354/355, 288-291 (2013)
14. Chen, J.; Rempel, D.L.; Gross, M.L.: Temperature jump and fast photochemical oxidation probe submillisecond protein folding. J. Am. Chem. Soc. 132, 15502-15504 (2010)
15. Hoaglund-Hyzer, C.S.; Counterman, A.E.; Clemmer, D.E.: Anhydrous protein ions. Chem. Rev. 99, 3037-3079 (1999)
16. 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. 1, 293-327 (2008)
17. Lenkinski, R.E.; Chen, D.M.; Glickson, J.D.; Goldstein, G.: Nuclear magnetic resonance studies of the denaturation of ubiquitin. Biochim. Biophys. Acta 494, 126-130 (1977)
18. Wilkinson, K.D.; Mayer, A.N.: Alcohol-induced conformational changes of ubiquitin. Arch. Biochem. Biophys. 250, 390-399 (1986)
19. 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 30, 3120-3128 (1991)
20. Vijay-Kumar, S.; Bugg, C.E.; Cook, W.J.: Structure of ubiquitin refined at 1.8 Å resolution. J. Mol. Biol. 194, 531-544 (1987)
21. 15N nuclear magnetic resonance spectroscopy. Biochemistry 36, 13043-13053 (1997)
22. Pan, Y.; Briggs, M.S.: Hydrogen exchange in native and alcohol forms of ubiquitin. Biochemistry 31, 11405-11412 (1992)
23. 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. 3, 285-296 (1993)
24. 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. 234, 483-492 (1993)
25. Cordier, F.; Grzesiek, S.: Quantitative comparison of the hydrogen bond network of A-State and native ubiquitin by hydrogen bond scalar couplings. Biochemistry 43, 11295-11301 (2004)
26. 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. 16, 1101-1118 (2007)
27. Clemmer, D.E.; Jarrold, M.F.: Ion mobility measurements and their applications to clusters and biomolecules. J. Mass Spectrom. 32, 577-592 (1997)
28. 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. 100, 16082-16086 (1996)
29. 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. 8, 275-282 (1997)
30. Shvartsburg, A.A.; Jarrold, M.F.: An exact hard-spheres scattering model for the mobilities of polyatomic ions. Chem. Phys. Lett. 261, 86-91 (1996)
31. Wyttenbach, T.; Bowers, M.T.: Gas-phase conformations: the ion mobility/ion chromatography method. Top. Curr. Chem. 225, 207-232 (2003)
32. Loo, J.A.: Studying noncovalent protein complexes by electrospray ionization mass spectrometry. Mass Spectrom. Rev. 16, 1-23 (1997)
33. Loo, J.A.; He, J.X.; Cody, W.L.: Higher order structure in the gas phase reflects solution structure. J. Am. Chem. Soc. 120, 4542-4543 (1998)
34. 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 310, 1658-1661 (2005)
35. Ruotolo, B.T.; Robinson, C.V.: Aspects of native proteins are retained in vacuum. Curr. Opin. Chem. Biol. 10, 402-408 (2006)
36. Bernstein, S.L.; Dupuis, N.F.; Lazo, N.D.; Wyttenbach, T.; Condron, M.M.; Bitan, G.; Teplow, D.B.; Shea, J.-E.; Ruotolo, B.T.; Robinson, C.V.; Bowers, M.T.: Amyloid-β protein oligomerization and the importance of tetramers and dodecamers in the aetiology of alzheimer's disease. Nat. Chem. 1, 326-331 (2009)
37. 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 115, 12266-12275 (2011)
38. 2 oxidation on ubiquitin conformers measured by ion mobility-mass spectrometry. J. Phys. Chem. B 117, 164-173 (2013)
39. 8+ ions from water:methanol solutions: evidence for the N and A states in aqueous solution. J. Phys. Chem. B 116, 3344-3352 (2012)
40. Valentine, S.J.; Counterman, A.E.; Clemmer, D.E.: Conformer-dependent proton-transfer reactions of ubiquitin ions. J. Am. Soc. Mass Spectrom. 8, 954-961 (1997)
41. Shelimov, K.B.; Clemmer, D.E.; Hudgins, R.R.; Jarrold, M.F.: Protein Structure in vacuo: gas-phase conformations of BPTI and cytochrome c. J. Am. Chem. Soc. 119, 2240-2248 (1997)
42. 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. 133, 13810-13813 (2011)
43. Shi, H.; Clemmer, D.E.: Evidence for two new solution states of ubiquitin by IMS-MS analysis. Submitted
44. Li, J.; Taraszka, J.A.; Counterman, A.E.; Clemmer, D.E.: Influence of solvent composition and capillary temperature on the conformations of electrosprayed ions: unfolding of compact ubiquitin conformers from pseudonative and denatured solutions. Int. J. Mass Spectrom. 185/186/187, 37-47 (1999)
45. Badman, E.R.; Hoaglund-Hyzer, C.S.; Clemmer, D.E.: Dissociation of different conformations of ubiquitin ions. J. Am. Soc. Mass Spectrom. 13, 719-723 (2002)
46. Myung, S.; Badman, E.R.; Lee, Y.J.; Clemmer, D.E.: Structural transitions of electrosprayed ubiquitin ions stored in an ion trap over ~10 ms to 30 s. J. Phys. Chem. A 106, 9976-9982 (2002)
47. Koeniger, S.L.; Merenbloom, S.I.; Clemmer, D.E.: Evidence for many resolvable structures within conformation types of electrosprayed ubiquitin ions. J. Phys. Chem. B 110, 7017-7021 (2006)
48. 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. 128, 11713-11719 (2006)
49. Koeniger, S.L.; Clemmer, D.E.: Resolution and structural transitions of elongated states of ubiquitin. J. Am. Soc. Mass Spectrom. 18, 322-331 (2007)
50. Lee, S.; Ewing, M.A.; Nachtigall, F.M.; Kurulugama, R.T.; Valentine, S.J.; Clemmer, D.E.: Determination of cross sections by overtone mobility spectrometry: evidence for loss of unstable structures at higher overtones. J. Phys. Chem. B 114, 12406-12415 (2010)
51. 11+ enhance hydrogen/deuterium exchange. J. Phys. Chem. B 115, 4509-4515 (2011)
52. Mack, E.: Average cross-sectional areas of molecules by gaseous diffusion methods. J. Am. Chem. Soc. 47, 2468-2482 (1925)
53. Revercomb, H.E.; Mason, E.A.: Theory of plasma chromatography/gaseous electrophoresis - a review. Anal. Chem. 47, 970-983 (1975)
54. Mason, E.A.; McDaniel, E.W.: Transport properties of ions in gases. Wiley, New York (1988)
55. Merenbloom, S.I.; Koeniger, S.L.; Valentine, S.J.; Plasencia, M.D.; Clemmer, D.E.: IMS-IMS and IMS-IMS-IMS/MS for separating peptide and protein fragment ions. Anal. Chem. 78, 2802-2809 (2006)
56. Koeniger, S.L.; Merenbloom, S.I.; Valentine, S.J.; Jarrold, M.F.; Udseth, H.; Smith, R.D.; Clemmer, D.E.: An IMS-IMS analogue of MS-MS. Anal. Chem. 78, 4161-4174 (2006)
57. 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. 70, 2236-2242 (1998)
58. Mohimen, A.; Dobo, A.; Hoerner, J.K.; Kaltashov, I.A.: A chemometric approach to detection and characterization of multiple protein conformers in solution using electrospray ionization mass spectrometry. Anal. Chem. 75, 4139-4147 (2003)
59. Zubarev, R.A.; Kelleher, N.L.; McLafferty, F.W.: Electron capture dissociation of multiply charged protein cations. A nonergodic process. J. Am. Chem. Soc. 120, 3265-3266 (1998)
60. 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. 124, 6407-6420 (2002)
61. Robinson, E.: The role of conformation on electron capture dissociation of ubiquitin. J. Am. Soc. Mass Spectrom. 2006(17), 1469-1479 (2006)
62. Reilly, J.P.: Ultraviolet photofragmentation of biomolecular ions. Mass Spectrom. Rev. 28, 425-447 (2009)
63. Lee, S.; Li, Z.; Valentine, S.J.; Zucker, S.M.; Webber, N.; Reilly, J.P.; Clemmer, D.E.: Extracted fragment ion mobility distributions: a new method for complex mixture analysis. Int. J. Mass Spectrom. 309, 154-160 (2012)
64. 2+ revealed by cold ion spectroscopy coupled with FAIMS. J. Am. Soc. Mass Spectrom. 23, 1173-1181 (2012)
65. Nagornova, N.S.; Rizzo, T.R.; Boyarkin, O.V.: Exploring the mechanism of IR-UV double-resonance for quantitative spectroscopy of protonated polypeptides and proteins. Angew. Chem.; Int. Ed. 52, 6002-6005 (2013)
66. Breuker, K.; Brüschweiler, S.; Tollinger, M.: Electrostatic stabilization of a native protein structure in the gas phase. Angew. Chem.; Int. Ed. 50, 873-877 (2011)