Supercharging protein complexes from aqueous solution disrupts their native conformations

Journal of the American Society for Mass Spectrometry

Volumn 23, Issue 2, 2012, Pages 191-200

  Sterling, Harry J ^a   Kintzer, Alexander F ^a   Feld, Geoffrey K ^a   Cassou, Catherine A ^a   Krantz, Bryan A ^a   Williams, Evan R ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Anthrax toxin; Charge enhancement; Concanavalin A; Electrospray ionization; Native mass spectrometry; Protein complex; Supercharging; Traveling wave ion mobility

Indexed keywords

ANTHRAX TOXINS; CHARGE ENHANCEMENT; CONCANAVALIN A; ELECTROSPRAYS; PROTEIN COMPLEX; SUPERCHARGING; TRAVELING WAVE;

DISEASES; DISSOCIATION; ELECTROSPRAY IONIZATION; GASES; IONS; MASS SPECTROMETRY; OLIGOMERS; PROTEINS; SOLUTIONS; TOXIC MATERIALS;

IONIZATION OF GASES;

3 NITROBENZYL ALCOHOL; ALCOHOL; ANTHRAX TOXIN; CONCANAVALIN A; DIMER; TETRAMER; UNCLASSIFIED DRUG;

AQUEOUS SOLUTION; ARTICLE; CHEMICAL PROCEDURES; COMPLEX FORMATION; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; DISSOCIATION; ELECTROSPRAY; EVAPORATION; FRAGMENTATION REACTION; IONIC STRENGTH; MASS SPECTROMETRY; PRESSURE; PROTEIN COMPLEX SUPERCHARGING; PROTEIN CONFORMATION; PROTEIN STABILITY; TRAVELING WAVE ION MOBILITY MASS SPECTROMETRY;

ACETATES; ANTIGENS, BACTERIAL; BACTERIAL TOXINS; BENZYL ALCOHOLS; CONCANAVALIN A; GASES; HYDROGEN-ION CONCENTRATION; IONS; MODELS, MOLECULAR; OSMOLAR CONCENTRATION; PROTEIN CONFORMATION; PROTEIN SUBUNITS; PROTEIN UNFOLDING; PROTEINS; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION; STATIC ELECTRICITY;

EID: 84856244569     PISSN: 10440305     EISSN: 18791123     Source Type: Journal    
DOI: 10.1007/s13361-011-0301-y     Document Type: Article

References (68)

1. A Dobo IA Kaltashov 2001 Detection of Multiple Protein Conformational Ensembles in Solution Via Deconvolution of Charge-State Distributions in ESI MS Anal. Chem. 73 4763 4773 10.1021/ac010713f 1:CAS:528:DC%2BD3MXmslOhtbw%3D (Pubitemid 32980095)
2. SK Chowdhury V Katta BT Chait 1990 Probing Conformational Changes in Proteins by Mass Spectrometry J. Am. Chem. Soc. 112 9012 9013 10.1021/ja00180a074 1:CAS:528:DyaK3cXmtVOktb0%3D
3. JA Loo RRO Loo HR Udseth CG Edmonds RD Smith 1991 Solvent-Induced Conformational Changes of Polypeptides Probed by Electrospray-Ionization Mass-Spectrometry Rapid Commun. Mass Spectrom. 5 101 105 10.1002/rcm.1290050303 1:CAS:528:DyaK3MXhvVWmurs%3D
4. AT Iavarone JC Jurchen ER Williams 2000 Effects of Solvent on the Maximum Charge State and Charge State Distribution of Protein Ions Produced by Electrospray Ionization J. Am. Soc. Mass Spectrom. 11 976 985 10.1016/S1044-0305(00)00169-0 1:CAS:528:DC%2BD3cXotlCit7k%3D (Pubitemid 34546668)
5. RRO Loo RD Smith 1995 Proton-Transfer Reactions of Multiply-Charged Peptide and Protein Cations and Anions J. Mass Spectrom. 30 339 347 10.1002/jms.1190300217
6. ER Williams 1996 Proton Transfer Reactivity of Large Multiply Charged Ions J. Mass Spectrom. 31 831 842 10.1002/(SICI)1096-9888(199608)31:8<831:: AID-JMS392>3.0.CO;2-7 1:CAS:528:DyaK28XkvFSgt78%3D (Pubitemid 26258960)
7. AT Iavarone JC Jurchen ER Williams 2001 Supercharged Protein and Peptide Ions Formed by Electrospray Ionization Anal. Chem. 73 1455 1460 10.1021/ac001251t 1:CAS:528:DC%2BD3MXhsFKht7o%3D (Pubitemid 32896200)
8. AT Iavarone ER Williams 2002 Supercharging in Electrospray Ionization: Effects on Signal and Charge Int. J. Mass Spectrom. 219 63 72 10.1016/S1387-3806(02)00587-0 1:CAS:528:DC%2BD38XmtVWlu7c%3D
9. AT Iavarone ER Williams 2003 Mechanism of Charging and Supercharging Molecules in Electrospray Ionization J. Am. Chem. Soc. 125 2319 2327 10.1021/ja021202t 1:CAS:528:DC%2BD3sXovFyksw%3D%3D (Pubitemid 36245725)
10. K Benkestock G Sundqvist PO Edlund J Roeraade 2004 Influence of Droplet Size, Capillary-Cone Distance and Selected Instrumental Parameters for the Analysis of Noncovalent Protein-Ligand Complexes by Nano-Electrospray Ionization Mass Spectrometry J. Mass Spectrom. 39 1059 1067 10.1002/jms.685 1:CAS:528:DC%2BD2cXnvVGqu7c%3D (Pubitemid 39242977)
11. JS Page RT Kelly K Tang RD Smith 2007 Ionization and Transmission Efficiency in an Electrospray Ionization-Mass Spectrometry Interface J. Am. Soc. Mass Spectrom. 18 1582 1590 10.1016/j.jasms.2007.05.018 1:CAS:528: DC%2BD2sXps1Glu7o%3D (Pubitemid 47302317)
12. BA Thomson 1997 Declustering and Fragmentation of Protein Ions from an Electrospray Ion Source J. Am. Soc. Mass Spectrom. 8 1053 1058 10.1016/S1044-0305(97)00129-3 1:CAS:528:DyaK2sXmtlOksr4%3D (Pubitemid 27514578)
13. PX Yang RG Cooks Z Ouyang AM Hawkridge DC Muddiman 2005 Gentle Protein Ionization Assisted by High-Velocity Gas Flow Anal. Chem. 77 6174 6183 10.1021/ac050711l 1:CAS:528:DC%2BD2MXpsVSksLY%3D (Pubitemid 41439691)
14. M Scalf MS Westphall LM Smith 2000 Charge Reduction Electrospray Mass Spectrometry Anal. Chem. 72 52 60 10.1021/ac990878c 1:CAS:528:DyaK1MXnslSlsb8%3D (Pubitemid 30027737)
15. JL Stephenson SA McLuckey 1998 Charge Manipulation for Improved Mass Determination of High-Mass Species and Mixture Components by Electrospray Mass Spectrometry J. Mass Spectrom. 33 664 672 10.1002/(SICI)1096-9888(199807)33: 7<664::AID-JMS663>3.0.CO;2-P 1:CAS:528:DyaK1cXkvVOlurs%3D (Pubitemid 28343383)
16. MI Catalina RHH van den Heuvel E van Duijn AJR Heck 2005 Decharging of Globular Proteins and Protein Complexes in Electrospray Chem. Eur. J. 11 960 968 10.1002/chem.200400395 1:CAS:528:DC%2BD2MXhtVWrt7g%3D (Pubitemid 40188534)
17. AT Iavarone ER Williams 2003 Collisionally Activated Dissociation of Supercharged Proteins Formed by Electrospray Ionization Anal. Chem. 75 4525 4533 10.1021/ac034144i 1:CAS:528:DC%2BD3sXlsFOgsrc%3D (Pubitemid 37082244)
18. SH Lomeli S Yin RRO Loo JA Loo 2009 Increasing Charge While Preserving Noncovalent Protein Complexes for ESI-MS J. Am. Soc. Mass Spectrom. 20 593 596 10.1016/j.jasms.2008.11.013 1:CAS:528:DC%2BD1MXjs1ansb4%3D
19. HJ Sterling ER Williams 2009 Origin of Supercharging in Electrospray Ionization of Noncovalent Complexes from Aqueous Solution J. Am. Soc. Mass Spectrom. 20 1933 1943 10.1016/j.jasms.2009.06.012 1:CAS:528:DC%2BD1MXhtFGkurrM
20. HJ Sterling CA Cassou MJ Trnka AL Burlingame BA Krantz ER Williams 2011 The Role of Conformational Flexibility on Protein Supercharging in Native Electrospray Ionization Phys. Chem. Chem. Phys. 13 18288 18296 10.1039/c1cp20277d 1:CAS:528:DC%2BC3MXht12gt7%2FE
21. HJ Sterling MP Daly GK Feld KL Thoren AF Kintzer BA Krantz ER Williams 2010 Effects of Supercharging Reagents on Noncovalent Complex Structure in Electrospray Ionization from Aqueous Solutions J. Am. Soc. Mass Spectrom. 21 1762 1774 10.1016/j.jasms.2010.06.012 1:CAS:528:DC%2BC3cXht1Wmt7fM
22. HJ Sterling JS Prell CA Cassou ER Williams 2011 Protein Conformation and Supercharing with DMSO from Aqueous Solution J. Am. Soc. Mass Spectrom. 22 1178 1186 10.1007/s13361-011-0116-x 1:CAS:528:DC%2BC3MXnt1Ohsb8%3D
23. HJ Sterling ER Williams 2010 Real-Time Hydrogen/Deuterium Exchange Kinetics Via Supercharged Electrospray Ionization Tandem Mass Spectrometry Anal. Chem. 82 9050 9057 10.1021/ac101957x 1:CAS:528:DC%2BC3cXht12jtbbL
24. SH Lomeli IX Peng S Yin RRO Loo JA Loo 2010 New Reagents for Increasing ESI Multiple Charging of Proteins and Protein Complexes J. Am. Soc. Mass Spectrom. 21 127 131 10.1016/j.jasms.2009.09.014 1:CAS:528: DC%2BC3cXjslyltQ%3D%3D
25. NW Davies MD Wiese SGA Browne 2004 Characterization of Major Peptides in 'Jack Jumper' Ant Venom by Mass Spectrometry Toxicon 43 173 183 10.1016/j.toxicon.2003.11.021 1:CAS:528:DC%2BD2cXhs1Crs74%3D (Pubitemid 38281233)
26. F Kjeldsen AMB Giessing CR Ingrell ON Jensen 2007 Peptide Sequencing and Characterization of Post-Translational Modifications by Enhanced Ion-Charging and Liquid Chromatography Electron-Transfer Dissociation Tandem Mass Spectrometry Anal. Chem. 79 9243 9252 10.1021/ac701700g 1:CAS:528: DC%2BD2sXhtlWisrrF (Pubitemid 350276301)
27. JA Madsen JS Brodbelt 2009 Comparison of Infrared Multiphoton Dissociation and Collision-Induced Dissociation of Supercharged Peptides in Ion Traps J. Am. Soc. Mass Spectrom. 20 349 358 10.1016/j.jasms.2008.10.018 1:CAS:528:DC%2BD1MXisFaitL4%3D
28. SK Sze Y Ge H Oh FW McLafferty 2002 Top-Down Mass Spectrometry of a 29-kDa Protein for Characterization of Any Posttranslational Modification to within One Residue Proc. Natl. Acad. Sci. U.S.A. 99 1774 1779 10.1073/pnas.251691898 1:CAS:528:DC%2BD38XitVSkurk%3D (Pubitemid 34168966)
29. SG Valeja JD Tipton MR Emmett AG Marshall 2010 New Reagents for Enhanced Liquid Chromatographic Separation and Charging of Intact Protein Ions for Electrospray Ionization Mass Spectrometry Anal. Chem. 82 7515 7519 10.1021/ac1016858 1:CAS:528:DC%2BC3cXhtVWqtLbK
30. EB Erba BT Ruotolo D Barsky CV Robinson 2010 Ion Mobility-Mass Spectrometry Reveals the Influence of Subunit Packing and Charge on the Dissociation of Multiprotein Complexes Anal. Chem. 82 9702 9710 10.1021/ac101778e 1:CAS:528:DC%2BC3cXhtlyks7vI
31. AA Enyenihi H Yang AJ Ytterberg Y Lyutvinskiy RA Zubarev 2011 Heme Binding in Gas-Phase Holo-Myoglobin Cations: Distal Becomes Proximal? J. Am. Soc. Mass Spectrom. 22 1763 1770 10.1007/s13361-011-0182-0 1:CAS:528: DC%2BC3MXhtlWitLjN
32. S Yin JA Loo 2011 Top-Down Mass Spectrometry of Supercharged Native Protein-Ligand Complexes Int. J. Mass Spectrom. 300 118 122 10.1016/j.ijms.2010. 06.032 1:CAS:528:DC%2BC3MXjsFart7o%3D
33. L Regazzoni L Bertoletti G Vistoli R Colombo G Aldini M Serra M Carini G Caccialanza E De Lorenzi 2010 A Combined High-Resolution Mass Spectrometric and in Silico Approach for the Characterization of Small Ligands of β(2)-Microglobulin Chem. Med. Chem. 5 1015 1025 1:CAS:528: DC%2BC3cXotVOmtbY%3D
34. CJ Hogan RRO Loo JA Loo JF de la Mora 2010 Ion Mobility-Mass Spectrometry of Phosphorylase B Ions Generated with Supercharging Reagents but in Charge-Reducing Buffer Phys. Chem. Chem. Phys. 12 13476 13483 10.1039/c0cp01208d 1:CAS:528:DC%2BC3cXht1ykurrO
35. RL Grimm JL Beauchamp 2010 Evaporation and Discharge Dynamics of Highly Charged Multicomponent Droplets Generated by Electrospray Ionization J. Phys. Chem. A 114 1411 1419 10.1021/jp907162w 1:CAS:528:DC%2BD1MXhtlSiu73K
36. E Ahadi L Konermann 2011 Ejection of Solvated Ions from Electrosprayed Methanol/Water Nanodroplets Studied by Molecular Dynamics Simulations J. Am. Chem. Soc. 133 9354 9363 10.1021/ja111492s 1:CAS:528:DC%2BC3MXmslGmsbc%3D
37. SL Zhou KD Cook 2000 Probing Solvent Fractionation in Electrospray Droplets with Laser-Induced Fluorescence of a Solvatochromic Dye Anal. Chem. 72 963 969 10.1021/ac990912n 1:CAS:528:DC%2BD3cXnsV2itQ%3D%3D (Pubitemid 30127402)
38. CRC Handbook of Chemistry and Physics. In [Online] 89th ed.; D. R. Lide, Ed. 2008-2009.
39. JM Goodman PD Kirby LO Haustedt 2000 Some Calculations for Organic Chemists: Boiling Point Variation, Boltzmann Factors and the Eyring Equation Tetrahedron Lett. 41 9879 9882 10.1016/S0040-4039(00)01754-8 1:CAS:528:DC%2BD3cXosFGjsLw%3D
40. Lord Rayleigh Phils. Mag. 1882, 14, 184-186.
41. R Scherrenberg B Coussens P van Vliet G Edouard J Brackman E de Brabander K Mortensen 1998 The Molecular Characteristics of Poly(Propyleneimine) Dendrimers as Studied with Small-Angle Neutron Scattering, Viscosimetry, and Molecular Dynamics Macromolecules 31 456 461 10.1021/ma9618181 1:CAS:528:DyaK1cXit1SltQ%3D%3D (Pubitemid 128559871)
42. AF Kintzer HJ Sterling II Tang A Abdul-Gader AJ Miles BA Wallace ER Williams BA Krantz 2010 Role of the Protective Antigen Octamer in the Molecular Mechanism of Anthrax Lethal Toxin Stabilization in Plasma J. Mol. Biol. 399 741 758 10.1016/j.jmb.2010.04.041 1:CAS:528:DC%2BC3cXntlagsbg%3D
43. MF Bush Z Hall K Giles J Hoyes CV Robinson BT Ruotolo 2010 Collision Cross Sections of Proteins and Their Complexes: A Calibration Framework and Database for Gas-Phase Structural Biology Anal. Chem. 82 9557 9565 10.1021/ac1022953 1:CAS:528:DC%2BC3cXhtlCltbjO
44. MF Mesleh JM Hunter AA Shvartsburg GC Schatz MF Jarrold 1996 Structural Information from Ion Mobility Measurements: Effects of the Long-Range Potential J. Phys. Chem. 100 16082 16086 10.1021/jp961623v 1:CAS:528:DyaK28XlsFCqu7w%3D (Pubitemid 126799343)
45. GK Feld KL Thoren AF Kintzer HJ Sterling II Tang SG Greenberg ER Williams BA Krantz 2010 Structural Basis for the Unfolding of Anthrax Lethal Factor by Protective Antigen Oligomers Nat. Struct. Mol. Biol. 17 1383 1390 10.1038/nsmb.1923 1:CAS:528:DC%2BC3cXhtlGrsb7L
46. P Emsley K Cowtan 2004 Coot: Model-Building Tools for Molecular Graphics Acta Crystallogr. D: Biol. Crystallogr. 60 2126 2132 10.1107/S0907444904019158 (Pubitemid 41742764)
47. DB Lacy DJ Wigelsworth RA Melnyk SC Harrison RJ Collier 2004 Structure of Heptameric Protective Antigen Bound to an Anthrax Toxin Receptor: A Role for Receptor in pH-Dependent Pore Formation Proc. Natl. Acad. Sci. U.S.A. 101 13147 13151 10.1073/pnas.0405405101 1:CAS:528:DC%2BD2cXnvFenurs%3D (Pubitemid 39209633)
48. M Huet JM Claverie 1978 Sedimentation Studies of Reversible Dimer-Tetramer Transition Kinetics of Concanavalin-A Biochemistry 17 236 241 10.1021/bi00595a007 1:CAS:528:DyaE1cXosVymsg%3D%3D (Pubitemid 8270207)
49. DF Senear DC Teller 1981 Thermodynamics of Concanavalin a Dimer-Tetramer Self-Association: Sedimentation Equilibrium Studies Biochemistry 20 3076 3083 10.1021/bi00514a014 1:CAS:528:DyaL3MXkt1alurY%3D
50. TT Herskovits R Jacobs K Nag 1983 The Effects of Salts and Ureas on the Subunit Dissociation of Concanavalin-A Biochim. Biophys. Acta 742 142 154 10.1016/0167-4838(83)90370-9 1:CAS:528:DyaL3sXoslChsg%3D%3D (Pubitemid 13184801)
51. JC Jurchen DE Garcia ER Williams 2004 Further Studies on the Origins of Asymmetric Charge Partitioning in Protein Homodimers J. Am. Soc. Mass Spectrom. 15 1408 1415 10.1016/j.jasms.2004.06.006 1:CAS:528:DC%2BD2cXotFGlsL4%3D (Pubitemid 39311691)
52. JC Jurchen ER Williams 2003 Origin of Asymmetric Charge Partitioning in the Dissociation of Gas-Phase Protein Homodimers J. Am. Chem. Soc. 125 2817 2826 10.1021/ja0211508 1:CAS:528:DC%2BD3sXpvVWqsw%3D%3D (Pubitemid 36512268)
53. CJ Hogan Jr. JA Carroll HW Rohrs P Biswas ML Gross 2008 Charge Carrier Field Emission Determines the Number of Charges on Native State Proteins in Electrospray Ionization J. Am. Chem. Soc. 130 6926 6927 10.1021/ja801280c 1:CAS:528:DC%2BD1cXlslamt7k%3D (Pubitemid 351770124)
54. CJ Hogan JA Carroll HW Rohrs P Biswas ML Gross 2009 Combined Charged Residue-Field Emission Model of Macromolecular Electrospray Ionization Anal. Chem. 81 369 377 10.1021/ac8016532 1:CAS:528:DC%2BD1cXhsVCgu7vF
55. GN Reeke JW Becker GM Edelman 1975 Covalent and Three-Dimensional Structure of Concanavalin A IV. Atomic Coordinates, Hydrogen Bonding, and Quaternary Structure J. Biol. Chem. 250 1525 1547 1:CAS:528:DyaE2MXht1Snsrc%3D
56. JC Milne D Furlong PC Hanna JS Wall RJ Collier 1994 Anthrax Protective Antigen Forms Oligomers During Intoxication of Mammalian Cells J. Biol. Chem. 269 20607 20612 1:CAS:528:DyaK2cXlt1Oms7Y%3D (Pubitemid 24260471)
57. AF Kintzer KL Thoren HJ Sterling KC Dong GK Feld II Tang TT Zhang ER Williams JM Berger BA Krantz 2009 The Protective Antigen Component of Anthrax Toxin Forms Functional Octameric Complexes J. Mol. Biol. 392 614 629 10.1016/j.jmb.2009.07.037 1:CAS:528:DC%2BD1MXhtV2ku73K
58. C Petosa RJ Collier KR Klimpel SH Leppla RC Liddington 1997 Crystal Structure of the Anthrax Toxin Protective Antigen Nature 385 833 838 10.1038/385833a0 1:CAS:528:DyaK2sXhsFarsrg%3D (Pubitemid 27106075)
59. RO Blaustein TM Koehler RJ Collier A Finkelstein 1989 Anthrax Toxin-Channel-Forming Activity of Protective Antigen in Planar Phospholipid-Bilayers Proc Natl. Acad. Sci. U.S.A. 86 2209 2213 10.1073/pnas.86.7.2209 1:CAS:528:DyaL1MXitVOmtrg%3D (Pubitemid 19102481)
60. BA Krantz A Finkelstein RJ Collier 2006 Protein Translocation through the Anthrax Toxin Transmembrane Pore Is Driven by a Proton Gradient J. Mol. Biol. 355 968 979 10.1016/j.jmb.2005.11.030 1:CAS:528:DC%2BD2MXhtlGlsLrP (Pubitemid 43012140)
61. DB Lacy M Mourez A Fouassier RJ Collier 2002 Mapping the Anthrax Protective Antigen Binding Site on the Lethal and Edema Factors J. Biol. Chem. 277 3006 3010 10.1074/jbc.M109997200 1:CAS:528:DC%2BD38XhtVSgtbw%3D (Pubitemid 34953337)
62. K Giles JP Williams I Campuzano 2011 Enhancements in Traveling Wave Ion Mobility Resolution Rapid Commun. Mass Spectrom. 25 1559 1566 10.1002/rcm.5013 1:CAS:528:DC%2BC3MXmtlaisbw%3D
63. BT Ruotolo K Giles I Campuzano AM Sandercock RH Bateman CV Robinson 2005 Evidence for Macromolecular Protein Rings in the Absence of Bulk Water Science 310 1658 1661 10.1126/science.1120177 1:CAS:528:DC%2BD2MXhtlSntLfE (Pubitemid 41780783)
64. H Katayama J Wang F Tama L Chollet EP Gogol RJ Collier MT Fisher 2010 Three-Dimensional Structure of the Anthrax Toxin Pore Inserted into Lipid Nanodiscs and Lipid Vesicles Proc. Natl. Acad. Sci. U.S.A. 107 3453 3457 10.1073/pnas.1000100107 1:CAS:528:DC%2BC3cXjtFymuro%3D
65. G Vernier J Wang LD Jennings J Sun A Fischer LK Song RJ Collier 2009 Solubilization and Characterization of the Anthrax Toxin Pore in Detergent Micelles Prot. Sci. 18 1882 1895 10.1002/pro.199 1:CAS:528:DC%2BD1MXhtVKnt73N
66. H Katayama BE Janowiak M Brzozowski J Juryck S Falke EP Gogol RJ Collier MT Fisher 2008 GroEL as a Molecular Scaffold for Structural Analysis of the Anthrax Toxin Pore Nat. Struct. Mol. Biol. 15 754 760 10.1038/nsmb.1442 1:CAS:528:DC%2BD1cXotVeqtr8%3D (Pubitemid 351932002)
67. GD Wang RB Cole 1994 Effect of Solution Ionic-Strength on Analyte Charge-State Distributions in Positive and Negative-Ion Electrospray Mass-Spectrometry Anal. Chem. 66 3702 3708 10.1021/ac00093a026 1:CAS:528:DyaK2cXmtVSju70%3D
68. A Kharlamova BM Prentice TY Huang SA McLuckey 2010 Electrospray Droplet Exposure to Gaseous Acids for the Manipulation of Protein Charge State Distributions Anal. Chem. 82 7422 7429 10.1021/ac101578q 1:CAS:528: DC%2BC3cXhtVeiu7bL