Ion mobility measurements of nondenatured 12-150 kDa proteins and protein multimers by tandem differential mobility analysis-mass spectrometry (DMA-MS)

Journal of the American Society for Mass Spectrometry

Volumn 22, Issue 1, 2011, Pages 158-172

  Hogan Jr , Christopher J ^a,b,c   Fernández De La Mora, Juan ^b  

^a University of Minnesota   (United States)

^b Yale University   (United States)

^c SEADM SL   (Spain)

Author keywords

Charge reduction; Differential mobility analysis; Gas phase protein conformation; Ion mobility; Native state protein MS

Indexed keywords

CHARGE REDUCTION; DIFFERENTIAL MOBILITY ANALYSIS; GASPHASE; ION MOBILITY; NATIVE-STATE PROTEIN;

ATMOSPHERIC PRESSURE; ATMOSPHERIC STRUCTURE; CONFORMATIONS; DENSITY OF GASES; IONS; MASS SPECTROMETERS; MASS SPECTROMETRY; SURFACE ROUGHNESS;

PROTEINS;

ALBUMIN; CONCANAVALIN A; CYTOCHROME C; ION; LYSOZYME; MYOGLOBIN; OVALBUMIN; RIBONUCLEASE A; UBIQUITIN;

ANALYTIC METHOD; ANALYZER; ARTICLE; ATMOSPHERIC PRESSURE; CHEMICAL STRUCTURE; DIFFERENTIAL MOBILITY ANALYSIS; ELECTROSPRAY; GEOMETRY; MASS SPECTROMETER; MASS SPECTROMETRY; MOLECULAR WEIGHT; POLARIZATION; SIMULATION;

ANIMALS; CATTLE; PARTICLE SIZE; PLANT PROTEINS; PROTEIN MULTIMERIZATION; PROTEINS; QUATERNARY AMMONIUM COMPOUNDS; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION; TANDEM MASS SPECTROMETRY;

EID: 79952499886     PISSN: 10440305     EISSN: 18791123     Source Type: Journal    
DOI: 10.1007/s13361-010-0014-7     Document Type: Article

References (76)

1. Bohrer, B.C., Merenbloom, S.I., Koeniger, S.L., Hilderbrand, A.E., Clemmer, D.E.: Biomolecule analysis by ion mobility spectrometry. Ann. Rev. Anal. Chem. 1, 293-327 (2008)
2. Counterman, A.E., Valentine, S.J., Srebalus, C.A., Henderson, S.C., Hoaglund, C.S., Clemmer, D.E.: High-order structure and dissociation of gaseous peptide aggregates that are hidden in mass spectra. J. Am. Soc. Mass Spectrom. 9(8), 743-759 (1998)
3. Bernstein, S.L., Liu, D.F., Wyttenbach, T., Bowers, M.T., Lee, J.C., Gray, H.B., Winkler, J.R.: Alpha-synuclein: stable compact and extended monomeric structures and pH dependence of dimer formation. J. Am. Soc. Mass Spectrom. 15(10), 1435-1443 (2004)
4. Shelimov, K.B., Clemmer, D.E., Hudgins, R.R., Jarrold, M.F.: Protein structure in vacuo: gas-phase confirmations of BPTI and cytochrome c. J. Am. Chem. Soc. 119(9), 2240-2248 (1997)
5. Myung, S., Badman, E.R., Lee, Y.J., Clemmer, D.E.: Structural transitions of electrosprayed ubiquitin ions stored in an ion trap over similar to 10 ms to 30 s. J. Phys. Chem. A 106(42), 9976-9982 (2002)
6. Shelimov, K.B., Jarrold, M.F.: Conformations, unfolding, and refolding of apomyoglobin in vacuum: an activation barrier for gas-phase protein folding. J. Am. Chem. Soc. 119(13), 2987-2994 (1997)
7. Hudgins, R.R., Woenckhaus, J., Jarrold, M.F.: High resolution ion mobility measurements for gas phase proteins: correlation between solution phase and gas phase conformations. Int. J. Mass Spectrom. 165, 497-507 (1997)
8. Ruotolo, B.T., Benesch, J.L.P., Sandercock, A.M., Hyung, S.J., Robinson, C.V.: Ion mobility-mass spectrometry analysis of large protein complexes. Nat. Protoc. 3(7), 1139-1152 (2008)
9. 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)
10. Faull, P.A., Korkeila, K.E., Kalapothakis, J.M., Gray, A., McCullough, B.J., Barran, P.E.: Gas-phase metalloprotein complexes interrogated by ion mobility-mass spectrometry. Int. J. Mass Spectrom. 283(1-3), 140-148 (2009)
11. Scarff, C.A., Patel, V.J., Thalassinos, K., Scrivens, J.H.: Probing hemoglobin structure by means of traveling-wave ion mobility mass spectrometry. J. Am. Soc. Mass Spectrom. 20(4), 625-631 (2009)
12. van Duijn, E., Barendregt, A., Synowsky, S., Versluis, C., Heck, A.J.R.: Chaperonin complexes monitored by ion mobility mass spectrometry. J. Am. Chem. Soc. 131(4), 1452-1459 (2009)
13. Fernandez-Lima, F.A., Blase, R.C., Russell, D.H.: A study of ion-neutral collision cross-section value for low charge states of peptides, proteins, and peptide/protein complexes. Int. J. Mass Spectrom. 298(1-3), 111-118 (2010)
14. Zhao, Q., Schieffer, G.M., Soyk, M.W., Anderson, T.J., Houk, R.S., Badman, E.R.: Effects of ion/ion proton transfer reactions of conformation of gas-phase cytochrome c ions. 21, 1208-1217, J. Am. Soc. Mass Spectrom. (2010)
15. Bush, M.F., Hall, Z., Giles, K., Hoyes, J., Robinson, C.V., Ruotolo, B. T.: Collision cross sections of proteins and their complexes: a calibration framework and database for gas-phase structural biology. Anal. Chem. 82(22), 9557-9565 (2010)
16. Ruotolo, B.T., Robinson, C.V.: Aspects of native proteins are retained in vacuum. Curr. Opin. Chem. Biol. 10, 402-408 (2006)
17. Breuker, K., McLafferty, F.W.: Stepwise evolution of protein native structure with electrospray into the gas phase, 10(-12) to 10(2) S. Proc. Natl Acad. Sci. USA 105(47), 18145-18152 (2008)
18. Thomson, B.A.: Declustering and fragmentation of protein ions from an electrospray ion source. J. Am. Soc. Mass Spectrom. 8, 1053-1058 (1997)
19. Fernandez de la Mora, J., de Juan, L., Eichler, T., Rosell, J.: Differential mobility analysis of molecular ions and nanometer particles. Trends Anal. Chem. 17(6), 328-339 (1998)
20. Knutson, E.O., Whitby, K.T.: Aerosol classification by electric mobility: apparatus, theory, and applications. J. Aerosol Sci. 6, 443-451 (1975)
21. Fernandez de la Mora, J., Ude, S., Thomson, B.A.: The potential of differential mobility analysis coupled to MS for the study of very large singly and multiply charged proteins and protein complexes in the gas phase. Biotechnol. J. 1, 988-997 (2006)
22. Rus, J., Moro, D., Sillero, J.A., Royuela, J., Casado, A., Estevez-Molinero, F., Fernandez de la Mora, J.: IMS-MS studies based on coupling a differential mobility analyzer (DMA) to commercial API-MS systems. Int. J. Mass Spectrom. 298, 30-40 (2010)
23. Hogan, C.J., Fernandez de la Mora, J.: Tandem ion mobility-mass spectrometry (IMS-MS) study of ion evaporation from ionic liquid-acetonitrile nanodrops. Phys. Chem. Chem. Phys. 11, 8079-8090 (2009)
24. Kaufman, S.L., Skogen, J.W., Dorman, F.D., Zarrin, F., Lewis, K.C.: Macromolecule analysis based on electrophoretic mobility in air: globular proteins. Anal. Chem. 68(11), 1895-1904 (1996)
25. Scalf, M., Westphall, M.S., Krause, J., Kaufman, S.L., Smith, L.M.: Controlling charge states of large ions. Science 283(5399), 194-197 (1999)
26. Scalf, M., Westphall, M.S., Smith, L.M.: Charge reduction electrospray mass spectrometry. Anal. Chem. 72(1), 52-60 (2000)
27. Chen, D.R., Pui, D.Y.H., Kaufman, S.L.: Electrospraying of conducting liquids for monodisperse aerosol generation in the 4 nm to 1.8 μm diameter range. J. Aerosol Sci. 26(6), 963-977 (1995)
28. Kousaka, Y., Okuyama, K., Adachi, M., Mimura, T.: Effect of Brownian diffusion on electrical classification of ultrafine aerosol-particles in differential mobility analyzer. J. Chem. Eng. Jpn 19(5), 401-407 (1986)
29. Stolzenburg, M.R., Mcmurry, P.H.: An ultrafine aerosol condensation nucleus counter. Aerosol Sci. Technol. 14(1), 48-65 (1991)
30. Kaufman, S.L., Skogen, J.W., Dorman, F.D., Zarrin, F., Lewis, K.C.: Macromolecule analysis based on electrophoretic mobility in air: globular proteins. (Vol 68, pg 1895, 1996). Anal. Chem. 68(20), 3703 (1996)
31. Rupley, J.A., Gratton, E., Careri, G.: Water and globular-proteins. Trends Biochem. Sci. 8(1), 18-22 (1983)
32. Fernandez de la Mora, J.: Electrospray ionization of large multiply charged species proceeds via Dole's charged residue mechanism. Anal. Chim. Acta 406(1), 93-104 (2000)
33. Bacher, G., Szymanski, W.W., Kaufman, S.L., Zollner, P., Blaas, D., Allmaier, G.: Charge-reduced nano electrospray ionization combined with differential mobility analysis of peptides, proteins, glycoproteins, noncovalent protein complexes and viruses. J. Mass Spectrom. 36(9), 1038-1052 (2001)
34. Kaddis, C.S., Lomeli, S.H., Yin, S., Berhane, B., Apostol, M.I., Kickhoefer, V.A., Rome, L.H., Loo, J.A.: Sizing large proteins and protein complexes by electrospray ionization mass spectrometry and ion mobility. J. Am. Soc. Mass Spectrom. 18(7), 1206-1216 (2007)
35. Chen, D.R., Pui, D.Y.H., Hummes, D., Fissan, H., Quant, F.R., Sem, G. J.: Design and evaluation of a nanometer aerosol differential mobility analyzer (Nano-DMA). J. Aerosol Sci. 29(5-6), 497-509 (1998)
36. Laschober, C., Kaddis, C.S., Reischl, G.P., Loo, J.A., Allmaier, G., Szymanski, W.W.: Comparison of various nano-differential mobility analysers (nDMAs) applying globular proteins. J. Exp. Nanosci. 2(4), 291-301 (2007)
37. Lemaire, D., Marie, G., Serani, L., Laprevote, O.: Stabilization of gas-phase noncovalent macromolecular complexes in electrospray mass spectrometry using aqueous triethylammonium bicarbonate buffer. Anal. Chem. 73, 1699-1706 (2001)
38. Badman, E.R., Hoaglund-Hyzer, C.S., Clemmer, D.E.: Monitoring structural changes of proteins in an ion trap over similar to 10-200 ms: unfolding transitions in cytochrome c ions. Anal. Chem. 73(24), 6000-6007 (2001)
39. Hogan, C.J., Biswas, P.: Monte Carlo simulation of macromolecular nanoelectrospray ionization. J. Am. Soc. Mass Spectrom. 19, 1098-1107 (2008)
40. Ude, S., Fernandez de la Mora, J.: Molecular monodisperse mobility and mass standards from electrosprays of tetra-alkyl ammonium halides. J. Aerosol Sci. 36(10), 1224-1237 (2005)
41. Ku, B.K., Fernandez de la Mora, J.: Relation between electrical mobility, mass, and size for nanodrops 1-6.5 nm in diameter in air. Aerosol Sci. Technol. 43(3), 241-249 (2009)
42. Fernandez de la Mora, J.: The differential mobility analyzer (DMA): adding a true mobility dimension to a preexisting API-MS. Chap. 5 in: Wilkins, C., Trimpin, S. (eds.) Ion mobility spectroscopy-mass spectrometry: theory and applications. Taylor and Francis, New York (2010)
43. Thomson, B.A., Iribarne, J.V.: Field induced ion evaporation from liquid surfaces at atmospheric pressure. J. Chem. Phys. 71(11), 4451-4463 (1979)
44. Benesch, J.L.P.: Collisional activation of protein complexes: picking up the pieces. J. Am. Soc. Mass Spectrom. 20(3), 341-348 (2009)
45. Hogan, C.J., Ruotolo, B.T., Robinson, C.V., Fernandez de la Mora, J.: Tandem differential mobility analysis-mass spectrometry reveals partial collapse of the GroEL complex. Submitted to: J. Phys. Chem. B (2010)
46. Millikan, R.A.: The general law of fall of a small spherical body through a gas, and its bearing upon the nature of molecular reflection from surfaces. Phys. Rev. 22, 1-23 (1923)
47. Kim, J.H., Mulholland, G.W., Kukuck, S.R., Pui, D.Y.H.: Slip correction measurements of certified PSL nanoparticles using a nanometer differential mobility analyzer (nano-DMA) for Knudsen number from 0.5 to 83. J. Res. Nat. Inst. Stand. Technol. 110(1), 31-54 (2005)
48. Davies, C.N.: Definitive equations for the fluid resistance of spheres. Proc. Phys. Soc. 57, 259-270 (1945)
49. Epstein, P.S.: On the resistance experienced by spheres in their motion through gases. Phys. Rev. 23, 710-733 (1924)
50. Chen, Y.L., Collings, B.A., Douglas, D.J.: Collision cross sections of myoglobin and cytochrome c ions with Ne, Ar, and Kr. J. Am. Soc. Mass Spectrom. 8(7), 681-687 (1997)
51. Shvartsburg, A.A., Jarrold, M.F.: An exact hard-spheres scattering model for the mobilities of polyatomic ions. Chem. Phys. Lett. 261(1-2), 86-91 (1996)
52. Shvartsburg, A.A., Mashkevich, S.V., Baker, E.S., Smith, R.D.: Optimization of algorithms for ion mobility calculations. J. Phys. Chem. A 111(10), 2002-2010 (2007)
53. Tammet, H.: Size and mobility of nanometer particles, clusters and ions. J. Aerosol Sci. 26(3), 459-475 (1995)
54. Eglin, J.M.: The coefficients of viscosity and slip of carbon dioxide by the oil drop method and the law of motion of an oil drop in carbon dioxide, oxygen, and helium, at low pressures. Phys. Rev. 22, 161-170 (1923)
55. Rader, D.G.: Momentum slip correction factor for small particles in 9 common gases. J. Aerosol Sci. 21, 161-168 (1990)
56. Allen, M.D., Raabe, O.G.: Slip correction measurements of spherical solid aerosol-particles in an improved Millikan apparatus. Aerosol Sci. Technol. 4, 269-286 (1985)
57. Larriba, C., Hogan, C.J., Attoui, M., Borrajo, R., Fernandez-Garcia, J., Fernandez de la Mora, J.: The mobility-volume relationship below 3.0 nm examined by tandem mobility-mass measurement. Aerosol Sci. Techn. In press (2010)
58. Scarff, C.A., Thalassinos, K., Hilton, G.R., Scrivens, J.H.: Travelling wave ion mobility mass spectrometry studies of protein structure: biological significance and comparison with X-ray crystallography and nuclear magnetic resonance spectroscopy measurements. Rapid Commun. Mass Spectrom. 22(20), 3297-3304 (2008)
59. Kinnear, B.S., Kaleta, D.T., Kohtani, M., Hudgins, R.R., Jarrold, M.F.: Conformations of unsolvated valine-based peptides. J. Am. Chem. Soc. 122(38), 9243-9256 (2000)
60. Breaux, G.A., Jarrold, M.F.: Probing helix formation in unsolvated peptides. J. Am. Chem. Soc. 125(35), 10740-10747 (2003)
61. Jarrold, M.F.: Helices and sheets in vacuo. Phys. Chem. Chem. Phys. 9 (14), 1659-1671 (2007)
62. Friedlander, S.K.: Smoke, dust, and haze. Oxford University Press, New York (2000)
63. 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 101(19), 3891-3900 (1997)
64. Asbury, G.R., Hill, H.H.: Using different drift gases to change separation factors (α) in ion mobility spectrometry. Anal. Chem. 72, 580-584 (2000)
65. Lane, L.A., Ruotolo, B.T., Robinson, C.V., Favrin, G., Benesch, J.L.P.: A Monte Carlo approach for assessing the specificity of protein oligomers observed in nanoelectrospray mass spectra. Int. J. Mass Spectrom. 282, 169-177 (2009)
66. Lewis, K.C., Dohmeier, D.M., Jorgenson, J.W., Kaufman, S.L., Zarrin, F., Dorman, F.D.: Electrospray-condensation particle counter - a molecule-counting LC-detector for macromolecules. Anal. Chem. 66(14), 2285-2292 (1994)
67. Hogan, C.J., Carroll, J.A., Rohrs, H.W., Biswas, P., Gross, M.L.: Charge carrier field emission determines the number of charges on native state proteins in electrospray ionization. J. Am. Chem. Soc. 130, 6926-6927 (2008)
68. Hogan, C.J., Carroll, J.A., Rohrs, H.W., Biswas, P., Gross, M.L.: Combined charged residue-field emission model of macromolecular electrospray ionization. Anal. Chem. 81(1), 369-377 (2009)
69. Iribarne, J.V., Thomson, B.A.: On the evaporation of small ions from charged droplets. J. Chem. Phys. 64(6), 2287-2294 (1976)
70. Gamero-Castano, M., Fernandez de la Mora, J.: Kinetics of small ion evaporation from the charge and mass distribution of multiply charged clusters in electrosprays. J. Mass Spectrom. 35(7), 790-803 (2000)
71. Labowsky, M., Fenn, J.B., Fernandez de la Mora, J.: A continuum model for ion evaporation from a drop: effect of curvature and charge on ion solvation energy. Anal. Chim. Acta 406(1), 105-118 (2000)
72. Ku, B.K., Fernandez de la Mora, J.: Evaporation kinetics of tetraalkylammonium ions from charged formamide drops. J. Phys. Chem. B 109 (22), 11173-11179 (2005)
73. Gamero-Castano, M., Fernandez de la Mora, J.: Mechanisms of electrospray ionization of singly and multiply charged salt clusters. Anal. Chim. Acta 406(1), 67-91 (2000)
74. Hautreux, M., Hue, N., de Kerdaniel, A.D.F., Zahir, A., Malec, V., Laprevote, O.: Under non-denaturing solvent conditions, the mean charge state of a multiply charged protein ion formed by electrospray is linearly correlated with the macromolecular surface. Int. J. Mass Spectrom. 231, 131-137 (2004)
75. Castro, S.: PhD dissertation. Yale University, New Haven (2008)
76. Krusemark, C.J., Frey, B.L., Belshaw, P.J., Smith, L.M.: Modifying the charge state distribution of proteins in electrospray ionization mass spectrometry by chemical derivatization. J. Am. Soc. Mass Spectrom. 20 (9), 1617-1625 (2009)