Ion mobility-mass spectrometry for structural proteomics

Expert Review of Proteomics

Volumn 9, Issue 1, 2012, Pages 47-58

  Zhong, Yueyang ^a   Hyung, Suk Joon ^a   Ruotolo, Brandon T ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

Author keywords

High throughput; Macromolecular; Non covalent complexes; Protein network; Protein topology; Structural genomics

Indexed keywords

CRYSTALLIZATION; HIGH THROUGHPUT SCREENING; ION MOBILITY SPECTROMETRY; MEDICAL TECHNOLOGY; PHYSICAL CHEMISTRY; PROCESS OPTIMIZATION; PROTEIN ANALYSIS; PROTEIN ASSEMBLY; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; REVIEW; STRUCTURAL GENOMICS; STRUCTURAL PROTEOMICS;

CRYSTALLIZATION; MASS SPECTROMETRY; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEOMICS;

EID: 84856614421     PISSN: 14789450     EISSN: 17448387     Source Type: Journal    
DOI: 10.1586/epr.11.75     Document Type: Review

References (107)

1. Alberts B. The cell as a collection of protein machines: preparing the next generation of molecular biologists. Cell 92(3), 291-294 (1998). (Pubitemid 28093007)
2. Robinson CV, Sali A, Baumeister W. The molecular sociology of the cell. Nature 450(7172), 973-982 (2007). (Pubitemid 350273627)
3. Alber F, Kim MF, Sali A. Structural characterization of assemblies from overall shape and subcomplex compositions. Structure 13(3), 435-445 (2005). (Pubitemid 40342883)
4. Sali A, Glaeser R, Earnest T, Baumeister W. From words to literature in structural proteomics. Nature 422(6928), 216-225 (2003). (Pubitemid 36362759)
5. Von Heijne G. Membrane-protein topology. Nat. Rev. Mol. Cell Biol. 7(12), 909-918 (2006). (Pubitemid 44871417)
6. Pierce KL, Premont RT, Lefkowitz RJ. Seven-transmembrane receptors. Nat. Rev. Mol. Cell Biol. 3(9), 639-650 (2002). (Pubitemid 34987785)
7. Steven AC, Baumeister W. The future is hybrid. J. Struct. Biol. 163(3), 186-195 (2008).
8. Wyttenbach T, Bowers MT. Intermolecular interactions in biomolecular systems examined by mass spectrometry. Annu. Rev. Phys. Chem. 58511-58533 (2007).
9. Barran PE, Jurneczko E. How useful is ion mobility mass spectrometry for structural biology? The relationship between protein crystal structures and their collision cross sections in the gas phase. Analyst 136(1), 20-28 (2011).
10. Scrivens JH, Scarff CA, Thalassinos K, Hilton GR. 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).
11. Ruotolo BT, Giles K, Campuzano I et al. Evidence for macromolecular protein rings in the absence of bulk water. Science 310(5754), 1658-1661 (2005). (Pubitemid 41780783)
12. Benesch JLP, Ruotolo BT, Simmons DA, Robinson CV. Protein complexes in the gas phase: technology for structural genomics and proteomics. Chem. Rev. 107(8), 3544-3567 (2007). (Pubitemid 47322744)
13. Heck AJR. Native mass spectrometry: a bridge between interactomics and structural biology. Nat. Methods 5(11), 927-933 (2008).
14. Ruotolo BT, Robinson CV. Aspects of native proteins are retained in vacuum. Curr. Opin. Chem. Biol. 10(5), 402-408 (2006). (Pubitemid 44375072)
15. Politis A, Park AY, Hyung SJ et al. Integrating ion mobility mass spectrometry with molecular modelling to determine the architecture of multiprotein complexes. PLoS One 5(8), e12080 (2010).
16. Taverner T, Hernandez H, Sharon M et al. Subunit architecture of intact protein complexes from mass spectrometry and homology modeling. Acc. Chem. Res. 41(5), 617-627 (2008).
17. Hernandez H, Robinson CV. Determining the stoichiometry and interactions of macromolecular assemblies from mass spectrometry. Nat. Protoc. 2(3), 715-726 (2007). (Pubitemid 47040033)
18. Sharon M, Robinson CV. The role of mass spectrometry in structure elucidation of dynamic protein complexes. Annu. Rev. Biochem. 76167-76193 (2007).
19. Zhou M, Robinson CV. When proteomics meets structural biology. Trends Biochem. Sci. 35(9), 522-529 (2010).
20. Hernandez H, Dziembowski A, Taverner T, Seraphin B, Robinson CV. Subunit architecture of multimeric complexes isolated directly from cells. EMBO Rep. 7(6), 605-610 (2006). (Pubitemid 43827327)
21. Leary JA, Schenauer MR, Stefanescu R et al. 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(9), 1699-1706 (2009).
22. Ruotolo BT, Hyung SJ, Robinson PM et al. Ion mobility-mass spectrometry reveals long-lived, unfolded intermediates in the dissociation of protein complexes. Angew. Chem. Int. Ed. 46(42), 8001-8004 (2007). (Pubitemid 350033476)
23. Benesch JLP. Collisional activation of protein complexes: picking up the pieces. J. Am. Soc. Mass Spectrom. 20(3), 341-348 (2009).
24. Pukala TL, Ruotolo BT, Zhou M et al. Subunit architecture of multiprotein assemblies determined using restraints from gas-phase measurements. Structure 17(9), 1235-1243 (2009).
25. Mason EA, Mcdaniel EW. Transport Properties of Ions in Gases. John Wiley & Sons, NY, USA (1988).
26. Harvey SR, Macphee CE, Barran PE. Ion mobility mass spectrometry for peptide analysis. Methods 54(4), 454-461 (2011).
27. Kanu AB, Dwivedi P, Tam M, Matz L, Hill HH. Ion mobility-mass spectrometry. J. Mass Spectrom. 43(1), 1-22 (2008). (Pubitemid 351251969)
28. Eiceman GA, Karpas Z. Ion Mobility Spectrometry. CRC Press, FL, USA (2005).
29. Shvartsburg AA. Differential Ion Mobility Spectrometry: Nonlinear Ion Transport and Fundamentals of FAIMS. CRC Press, FL, USA (2008).
30. Kolakowski BM, Mester Z. Review of applications of high-field asymmetric waveform ion mobility spectrometry (FAIMS) and differential mobility spectrometry (DMS). Analyst 132(9), 842-864 (2007). (Pubitemid 47283703)
31. Kurulugama R, Nachtigall F, Lee S, Valentine S, Clemmer D. Overtone mobility spectrometry: part 1. Experimental observations. J. Am. Soc. Mass Spectrom. 20(5), 729-737 (2009).
32. Valentine S, Stokes S, Kurulugama R, Nachtigall F, Clemmer D. Overtone mobility spectrometry: part 2. Theoretical considerations of resolving power. J. Am. Soc. Mass Spectrom. 20(5), 738-750 (2009).
33. Merenbloom SI, Glaskin RS, Henson ZB, Clemmer DE. High-resolution ion cyclotron mobility spectrometry. Anal. Chem. 81(4), 1482-1487 (2009).
34. Clemmer DE, Jarrold MF. Ion mobility measurements and their applications to clusters and biomolecules. J. Mass Spectrom. 32(6), 577-592 (1997). (Pubitemid 27273948)
35. Gillig KJ, Ruotolo B, Stone EG et al. Coupling high-pressure MALDI with ion mobility/orthogonal time-of flight mass spectrometry. Anal. Chem. 72(17), 3965-3971 (2000).
36. Gillig KJ, Ruotolo BT, Stone EG, Russell DH. An electrostatic focusing ion guide for ion mobility-mass spectrometry. Int. J. Mass Spectrom. 239(1), 43-49 (2004).
37. Valentine SJ, Koeniger SL, Clemmer DE. A split-field drift tube for separation and efficient fragmentation of biomolecular ions. Anal. Chem. 75(22), 6202-6208 (2003). (Pubitemid 37424009)
38. Tang K, Shvartsburg AA, Lee HN et al. High-sensitivity ion mobility spectrometry/ mass spectrometry using electrodynamic ion funnel interfaces. Anal. Chem. 77(10), 3330-3339 (2005). (Pubitemid 40695493)
39. Koeniger SL, Merenbloom SI, Valentine SJ et al. An IMS-IMS analogue of MS-MS. Anal. Chem. 78(12), 4161-4174 (2006). (Pubitemid 43927412)
40. Koeniger SL, Merenbloom SI, Clemmer DE. Evidence for many resolvable structures within conformation types of electrosprayed ubiquitin ions. J. Phys. Chem. B. 110(13), 7017-7021 (2006). (Pubitemid 43672175)
41. Laschober C, Kaddis CS, Reischl GP et al. Comparison of various nano-differential mobility analysers (nDMAs) applying globular proteins. J. Exp. Nanosci. 2(4), 291-301 (2007). (Pubitemid 350176921)
42. Hogan CJ Jr, Ruotolo BT, Robinson CV, Fernandez De La Mora J. Tandem differential mobility analysis-mass spectrometry reveals partial gas-phase collapse of the GroEL complex. J. Phys. Chem. B. 115(13), 3614-3621 (2011).
43. De La Mora JF, De Juan L, Eichler T, Rosell J. Differential mobility analysis of molecular ions and nanometer particles. Trends Anal. Chem. 17(6), 328-339 (1998). (Pubitemid 28298674)
44. Hogan CJ, Jr., De La Mora JF. Ion mobility measurements of nondenatured 12-150 kDa proteins and protein multimers by tandem differential mobility analysismass spectrometry (DMA-MS). J. Am. Soc. Mass Spectrom. 22(1), 158-172 (2011).
45. Kaufman SL, Kuchumov AR, Kazakevich M, Vinogradov SN. Analysis of a 3.6 MDa hexagonal bilayer hemoglobin from lumbricus terrestris using a gas-phase electrophoretic mobility molecular analyzer. Anal. Biochem. 259(2), 195-202 (1998). (Pubitemid 28265578)
46. John JT, Brian B, Joe T, Benner WH, Gary S. Electrospray ion mobility spectrometry of intact viruses. Spectroscopy 18(1), 31-36 (2004). (Pubitemid 38223376)
47. Loo J, Berhane B, Kaddis C et al. Electrospray ionization mass spectrometry and ion mobility analysis of the 20S proteasome complex. J. Am. Soc. Mass Spectrom. 16(7), 998-1008 (2005). (Pubitemid 40828781)
48. Giles K, Pringle SD, Worthington KR et al. Applications of a travelling wave-based radio-frequency only stacked ring ion guide. Rapid Commun. Mass Spectrom. 18(20), 2401-2414 (2004). (Pubitemid 39361780)
49. Pringle SD, Giles K, Wildgoose JL et al. An investigation of the mobility separation of some peptide and protein ions using a new hybrid quadrupole/travelling wave IMS/oa-ToF instrument. Int. J. Mass Spectrom. 261(1), 1-12 (2007).
50. Shvartsburg AA, Smith RD. Fundamentals of traveling wave ion mobility spectrometry. Anal. Chem. 80(24), 9689-9699 (2008).
51. Ruotolo BT, Benesch JLP, Sandercock AM, Hyung SJ, Robinson CV. Ion mobility-mass spectrometry analysis of large protein complexes. Nat. Protoc. 3(7), 1139-1152 (2008).
52. Giles K, Wildgoose JL, Langridge DJ, Campuzano I. A method for direct measurement of ion mobilities using a travelling wave ion guide. Int. J. Mass Spectrom. 298(1-3), 10-16 (2010).
53. Zhong Y, Hyung SJ, Ruotolo BT. Characterizing the resolution and accuracy of a second-generation traveling-wave ion mobility separator for biomolecular ions. Analyst 136(17), 3534-3541 (2011).
54. Giles K, Williams JP, Campuzano I. Enhancements in travelling wave ion mobility resolution. Rapid Commun. Mass Spectrom. 25(11), 1559-1566 (2011).
55. Dugourd P, Hudgins RR, Clemmer DE, Jarrold MF. High-resolution ion mobility measurements. Rev. Sci. Instrum. 68(2), 1122-1129 (1997).
56. Kemper PR, Dupuis NF, Bowers MT. A new, higher resolution, ion mobility mass spectrometer. Int. J. Mass Spectrom. 287(1-3), 46-57 (2009).
57. Roscioli KM, Davis E, Siems WF et al. Modular ion mobility spectrometer for explosives detection using corona ionization. Anal. Chem. 83(15), 5965-5971 (2011).
58. Loo JA, Kaddis CS, Lomeli SH et al. Sizing large proteins and protein complexes by electrospray ionization mass spectrometry and ion mobility. J. Am. Soc. Mass Spectrom. 18(7), 1206-1216 (2007). (Pubitemid 46963586)
59. Mckay AR, Ruotolo BT, Ilag LL, Robinson CV. Mass measurements of increased accuracy resolve heterogeneous populations of intact ribosomes. J. Am. Chem. Soc. 128(35), 11433-11442 (2006). (Pubitemid 44338835)
60. Han L, Hyung SJ, Mayers JJ, Ruotolo BT. Bound anions differentially stabilize multiprotein complexes in the absence of bulk solvent. J. Am. Chem. Soc. 133(29), 11358-11367 (2011).
61. Freeke J, Robinson CV, Ruotolo BT. Residual counter ions can stabilise a large protein complex in the gas phase. Int. J. Mass Spectrom. 298(1-3), 91-98 (2010).
62. Liepold L, Oltrogge L, Suci P, Young M, Douglas T. Correct charge state assignment of native electrospray spectra of protein complexes. J. Am. Soc. Mass Spectrom. 20(3), 435-442 (2009).
63. Tseng YH, Uetrecht C, Heck AJR, Peng WP. Interpreting the charge state assignment in electrospray mass spectra of bioparticles. Anal. Chem. 83(6), 1960-1968 (2011).
64. Van Breukelen B, Barendregt A, Heck AJR, Van Den Heuvel RHH. Resolving stoichiometries and oligomeric states of glutamate synthase protein complexes with curve fitting and simulation of electrospray mass spectra. Rapid Commun. Mass Spectrom. 20(16), 2490-2496 (2006). (Pubitemid 44258455)
65. Hernandez H, Makarova OV, Makarov EM et al. Isoforms of U1-70k control subunit dynamics in the human spliceosomal U1 snRNP. PLoS One 4(9), e7202 (2009).
66. Bush MF, Hall Z, Giles K et al. 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).
67. Sharon M, Michaelevski I, Eisenstein M. Gas-phase compaction and unfolding of protein structures. Anal. Chem. 82(22), 9484-9491 (2010).
68. Morsa D, Gabelica V, De Pauw E. Effective temperature of ions in traveling wave ion mobility spectrometry. Anal. Chem. 83(14), 5775-5782 (2011).
69. Benesch JLP, Ruotolo BT. Mass spectrometry: come of age for structural biology. Curr. Opin. Struct. Biol. 21(5), 641-649 (2011).
70. Ruotolo BT, Mclean JA, Gillig KJ, Russell DH. The influence and utility of varying field strength for the separation of tryptic peptides by ion mobility-mass spectrometry. J. Am. Soc. Mass Spectrom. 16(2), 158-165 (2005). (Pubitemid 40203139)
71. Bleiholder C, Wyttenbach T, Bowers MT. A novel projection approximation algorithm for the fast and accurate computation of molecular collision cross sections (I). Method. Int. J. Mass Spectrom. 308(1), 1-10 (2011).
72. Felitsyn N, Kitova EN, Klassen JS. Thermal decomposition of a gaseous multiprotein complex studied by blackbody infrared radiative dissociation. Investigating the origin of the asymmetric dissociation behavior. Anal. Chem. 73(19), 4647-4661 (2001). (Pubitemid 32953190)
73. Jurchen JC, Williams ER. Origin of asymmetric charge partitioning in the dissociation of gas-phase protein homodimers. J. Am. Chem. Soc. 125(9), 2817-2826 (2003). (Pubitemid 36512268)
74. Benesch JLP, Aquilina JA, Ruotolo BT, Sobott F, Robinson CV. Tandem mass spectrometry reveals the quaternary organization of macromolecular assemblies. Chem. Biol. 13(6), 597-605 (2006).
75. Pagel K, Hyung SJ, Ruotolo BT, Robinson CV. Alternate dissociation pathways identified in charge-reduced protein complex ions. Anal. Chem. 82(12), 5363-5372 (2010).
76. Boeri Erba E, Ruotolo BT, Barsky D, Robinson CV. Ion mobility-mass spectrometry reveals the influence of subunit packing and charge on the dissociation of multiprotein complexes. Anal. Chem. 82(23), 9702-9710 (2010).
77. Zhang H, Cui WD, Wen JZ, Blankenship RE, Gross ML. Native electrospray and electron-capture dissociation FTICR mass spectrometry for top-down studies of protein assemblies. Anal. Chem. 83(14), 5598-5606 (2011).
78. Wysocki VH, Jones CM, Galhena AS, Blackwell AE. Surface-induced dissociation shows potential to be more informative than collision-induced dissociation for structural studies of large systems. J. Am. Soc. Mass Spectrom. 19(7), 903-913 (2008). (Pubitemid 351885472)
79. Zhou M, Sandercock AM, Fraser CS et al. Mass spectrometry reveals modularity and a complete subunit interaction map of the eukaryotic translation factor eIF3. Proc. Natl Acad. Sci. USA 105(47), 18139-18144 (2008).
80. Sharon M, Taverner T, Ambroggio XI, Deshaies RJ, Robinson CV. Structural organization of the 19S proteasome lid: insights from MS of intact complexes. PLoS Biol. 4(8), 1314-1323 (2006).
81. Levy ED, Boeri Erba E, Robinson CV, Teichmann SA. Assembly reflects evolution of protein complexes. Nature 453(7199), 1262-1265 (2008). (Pubitemid 351913589)
82. Nooren IM, Thornton JM. Diversity of protein-protein interactions. EMBO J. 22(14), 3486-3492 (2003). (Pubitemid 36898326)
83. Uetrecht C, Barbu IM, Shoemaker GK, Van Duijn E, Heck AJR. Interrogating viral capsid assembly with ion mobility-mass spectrometry. Nat. Chem. 3(2), 126-132 (2011).
84. Knapman TW, Morton VL, Stonehouse NJ, Stockley PG, Ashcroft AE. Determining the topology of virus assembly intermediates using ion mobility spectrometry-mass spectrometry. Rapid Commun. Mass Spectrom. 24(20), 3033-3042 (2010).
85. Bornschein RE, Hyung SJ, Ruotolo BT. Ion mobility-mass spectrometry reveals conformational changes in charge reduced multiprotein complexes. J. Am. Soc. Mass Spectrom. 22(10), 1690-1698 (2011).
86. Bagal D, Kitova EN, Liu L et al. Gas phase stabilization of noncovalent protein complexes formed by electrospray ionization. Anal. Chem. 81(18), 7801-7806 (2009).
87. Flick TG, Merenbloom SI, Williams ER. A simple and robust method for determining the number of basic sites in peptides and proteins using electrospray ionization mass spectrometry. Anal. Chem. 83(6), 2210-2214 (2011).
88. Bohrer BC, Mererbloom SI, Koeniger SL, Hilderbrand AE, Clemmer DE. Biomolecule analysis by ion mobility spectrometry. Annu. Rev. Anal. Chem. 293-327 (2008).
89. Valentine SJ, Plasencia MD, Liu XY et al. Toward plasma proteome profiling with ion mobility-mass spectrometry. J. Proteome Res. 5(11), 2977-2984 (2006). (Pubitemid 44749216)
90. Ruotolo BT, Gillig KJ, Stone EG, Russell DH. Peak capacity of ion mobility mass spectrometry: separation of peptides in helium buffer gas. J. Chromatogr. B. 782(1-2), 385-392 (2002). (Pubitemid 35402040)
91. Ruotolo BT, Mclean JA, Gillig KJ, Russell DH. Peak capacity of ion mobility mass spectrometry: the utility of varying drift gas polarizability for the separation of tryptic peptides. J. Mass Spectrom. 39(4), 361-367 (2004). (Pubitemid 38515349)
92. Valentine SJ, Kulchania M, Barnes CAS, Clemmer DE. Multidimensional separations of complex peptide mixtures: a combined high-performance liquid chromatography/ion mobility/time-offlight mass spectrometry approach. Int. J. Mass Spectrom. 212(1-3), 97-109 (2001).
93. Hoadlund-Hyzer CS, Li JW, Clemmer DE. Mobility labeling for parallel CID of ion mixtures. Anal. Chem. 72(13), 2737-2740 (2000). (Pubitemid 30452237)
94. Stone E, Gillig KJ, Ruotolo B et al. Surface-induced dissociation on a MALDI-ion mobility-orthogonal time-of-flight mass spectrometer: sequencing peptides from an 'in-solution' protein digest. Anal. Chem. 73(10), 2233-2238 (2001). (Pubitemid 32880688)
95. Mclean JA, Fenn LS. Structural resolution of carbohydrate positional and structural isomers based on gas-phase ion mobility-mass spectrometry. Phys. Chem. Chem. Phys. 13(6), 2196-2205 (2011).
96. Woods AS, Ugarov M, Egan T et al. Lipid/peptide/nucleotide separation with MALDI-ion mobility-TOF MS. Anal. Chem. 76(8), 2187-2195 (2004). (Pubitemid 38496058)
97. Bernstein SL, Dupuis NF, Lazo ND et al. Amyloid-beta protein oligomerization and the importance of tetramers and dodecamers in the aetiology of Alzheimer's disease. Nat. Chem. 1(4), 326-331 (2009).
98. Ashcroft AE. Mass spectrometry and the amyloid problem -how far can we go in the gas phase? J. Am. Soc. Mass. Spectrom. 21(7), 1087-1096 (2010).
99. Radford SE, Smith DP, Ashcroft AE. Elongated oligomers in beta(2)-microglobulin amyloid assembly revealed by ion mobility spectrometry-mass spectrometry. Proc. Natl Acad. Sci. USA 107(15), 6794-6798 (2010).
100. Van Duijn E, Barendregt A, Synowsky S, Versluis C, Heck AJR. Chaperonin complexes monitored by ion mobility mass spectrometry. J. Am. Chem. Soc. 131(4), 1452-1459 (2009).
101. Heck AJR, Uetrecht C, Rose RJ, Van Duijn E, Lorenzen K. Ion mobility mass spectrometry of proteins and protein assemblies. Chem. Soc. Rev. 39(5), 1633-1655 (2010).
102. Barrera NP, Wang SC, Politis A et al. Ion mobility mass spectrometry of two tetrameric membrane protein complexes reveals compact structures and differences in stability and packing. J. Am. Chem. Soc. 132(44), 15468-15470 (2010).
103. Ashcroft AE, Morton VL, Stockley PG, Stonehouse NJ. Insights into virus capsid assembly from non-covalent mass spectrometry. Mass Spectrom. Rev. 27(6), 575-595 (2008).
104. Heck AJR, Uetrecht C, Versluis C et al. Stability and shape of hepatitis B virus capsids in vacuo. Angew. Chem. Int. Ed. 47(33), 6247-6251 (2008).
105. Benesch JLP, Ruotolo BT, Sobott F et al. Quadrupole-time-of-flight mass spectrometer modified for higher-energy dissociation reduces protein assemblies to peptide fragments. Anal. Chem. 81(3), 1270-1274 (2009).
106. Dodds ED, Blackwell AE, Jones CM et al. Determinants of gas-phase disassembly behavior in homodimeric protein complexes with related yet divergent structures. Anal. Chem. 83(10), 3881-3889 (2011).
107. Blackwell AE, Dodds ED, Bandarian V, Wysocki VH. Revealing the quaternary structure of a heterogeneous noncovalent protein complex through surface-induced dissociation. Anal. Chem. 83(8), 2862-2865 (2011).