Irreversible Thermal Denaturation of Cytochrome c Studied by Electrospray Mass Spectrometry

Journal of the American Society for Mass Spectrometry

Volumn 20, Issue 5, 2009, Pages 819-828

  Liu, Jiangjiang ^a   Konermann, Lars ^a  

^a UNIVERSITY OF WESTERN ONTARIO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

AFTER HEATS; CHARGE STATE; CHARGE-STATE DISTRIBUTIONS; COVALENT MODIFICATIONS; CYTOCHROME C; DEGREE OF OXIDATIONS; DENATURED PROTEINS; ELECTROSPRAY MASS SPECTROMETRIES; ELECTROSPRAY-IONIZATION MASS SPECTROMETRIES; ELEVATED TEMPERATURES; HEAT EXPOSURES; HYDROGEN/DEUTERIUM EXCHANGES; INTERCONVERSION; IRREVERSIBLE DENATURATIONS; MODIFIED AMINO ACIDS; OPTICAL SPECTROSCOPIES; OXIDATION LEVELS; OXIDATIVE MODIFICATIONS; PEAK SHAPES; PHASE PROPERTIES; PROTEIN STRUCTURES; SOLUTION-PHASE CONFORMATIONS; TANDEM MASS SPECTROMETRIES; THERMAL DENATURATIONS; TRYPTIC DIGESTIONS;

AMINES; AMINO ACIDS; DENATURATION; ELECTROSPRAY IONIZATION; MASS SPECTROMETERS; MASS SPECTROMETRY; ORGANIC ACIDS; OXIDATION; OXYGEN; PYROLYSIS; SPECTRUM ANALYSIS;

HIGH PERFORMANCE LIQUID CHROMATOGRAPHY;

AMINO ACID DERIVATIVE; CYTOCHROME C; HYDROGEN; METHIONINE; OXYGEN; TRYPTOPHAN;

ARTICLE; DENATURATION; DEUTERIUM HYDROGEN EXCHANGE; ELECTROSPRAY MASS SPECTROMETRY; OXIDATION; PROTEIN MODIFICATION; PROTEIN STRUCTURE; TANDEM MASS SPECTROMETRY; TEMPERATURE MEASUREMENT;

ANIMALS; CATTLE; COMPUTER SIMULATION; CYTOCHROMES C; DEUTERIUM EXCHANGE MEASUREMENT; HOT TEMPERATURE; MYOCARDIUM; NORMAL DISTRIBUTION; OXIDATION-REDUCTION; PEPTIDE MAPPING; PROTEIN CONFORMATION; PROTEIN DENATURATION; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION; SPECTROPHOTOMETRY; TRYPSIN;

EID: 64049085647     PISSN: 10440305     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jasms.2008.12.016     Document Type: Article

References (81)

1. Kaltashov I.A., and Eyles S.J. Studies of Biomolecular Conformations and Conformational Dynamics by Mass Spectrometry. Mass Spectrom. Rev. 21 (2002) 37-71
2. de la Mora F.J. Electrospray Ionization of Large Multiply Charged Species Proceeds via Dole's Charged Residue Mechanism. Anal. Chim. Acta 406 (2000) 93-104
3. Felitsyn N., Peschke M., and Kebarle P. Origin and Number of Charges Observed on Multiply-Protonated Native Proteins Produced by ESI. Int. J. Mass Spectrom. Ion Process. 219 (2002) 39-62
4. Nesatyy V.J., and Suter M.J.-F. On the Conformation-Dependent Neutralization Theory and Charging of Individual Proteins and Their Non-covalent Complexes in the Gas Phase. J. Mass Spectrom. 39 (2004) 93-97
5. Iavarone A.T., and Williams E.R. Mechanism of Charging and Supercharging Molecules in Electrospray Ionization. J. Am. Chem. Soc. 125 (2003) 2319-2327
6. Heck A.J.R., and Van den Heuvel R.H.H. Investigation of Intact Protein Complexes by Mass Spectrometry. Mass Spectrom. Rev. 23 (2004) 368-389
7. Hogan C.J., Carroll J.A., Rohrs H.W., Biswas P., and Gross M.L. Charge Carrier Field Emission Determines the Number of Charges on Native State Proteins in Electrospray Ionization. J. Am. Chem. Soc. 130 (2008) 6929-6927
8. Samalikova M., and Grandori R. Protein Charge-State Distributions in Electrospray-Ionization Mass Spectrometry Do Not Appear To Be Limited by the Surface Tension of the Solvent. J. Am. Chem. Soc. 125 (2003) 13352-13353
9. Nguyen S., and Fenn J.B. Gas-Phase Ions of Solute Species from Charged Droplets of Solutions. Proc. Natl. Acad. Sci. U. S. A. 104 (2007) 1111-1117
10. Chowdhury S.K., Katta V., and Chait B.T. Probing Conformational Changes in Proteins by Mass Spectrometry. J. Am. Chem. Soc. 112 (1990) 9012-9013
11. Konermann L., and Douglas D.J. Acid-Induced Unfolding of Cytochrome c at Different Methanol Concentrations: Electrospray Ionization Mass Spectrometry Specifically Monitors Changes in the Tertiary Structure. Biochemistry 36 (1997) 12296-12302
12. Grandori R., Matecko I., and Muller N. Uncoupled Analysis of Secondary and Tertiary Protein Structure by Circular Dichroism and Electrospray Ionization Mass Spectrometry. J. Mass Spectrom. 37 (2002) 191-196
13. Loo J.A., Edmonds C.G., Udseh H.R., and Smith R.D. Effect of Reducing Disulfide-Containing Proteins on Electrospray Ionisation Mass Spectra. Anal. Chem. 62 (1990) 693-698
14. Lin H., and Dass C. Conformational Changes in β-Endorphin as Studied by Electrospray Ionization Mass Spectrometry. Rapid Commun. Mass Spectrom. 15 (2001) 2341-2346
15. Kaltashov I.A., and Abzalimov R.R. Do Ionic Charges in ESI MS Provide Useful Information on Macromolecular Structure?. J. Am. Soc. Mass Spectrom. 19 (2008) 1239-1246
16. Cai X., and Dass C. Conformational Analysis of Proteins and Peptides. Curr. Org. Chem. 7 (2003) 1841-8154
17. Katta V., and Chait B.T. Observation of the Heme-Globin Complex in Native Myoglobin by Electrospray-Ionisation Mass Spectrometry. J. Am. Chem. Soc. 113 (1991) 8534-8535
18. Grandori R. Origin of the Conformation Dependence of Protein Charge-State Distributions in Electrospray Ionization Mass Spectrometry. J. Mass Spectrom. 38 (2003) 11-15
19. Wu J., and Lebrilla C.B. Intrinsic Basicity of Oligomeric Peptides that Contain Glycine, Alanine, and Valine: The Effects of the Alkyl Side Chain on Proton Transfer Reactions. J. Am. Soc. Mass Spectrom. 6 (1995) 91-101
20. Abzalimov R.R., Frimpong A.K., and Kaltashov I.A. Gas-Phase Processes and Measurements of Macromolecular Properties in Solution: On the Possibility of False Positive and False Negative Signals of Protein Unfolding. Int. J. Mass Spectrom. 253 (2006) 207-216
21. Schnier P.D., Gross D.S., and Williams E.R. On the Maximum Charge State and Proton Transfer Reactivity of Peptide and Protein Ions Formed by Electrospray Ionization. J. Am. Soc. Mass Spectrom. 6 (1995) 1086-1097
22. Samalikova M., and Grandori R. Role of Opposite Charge in Protein Electrospray Ionization Mass Spectrometry. J. Mass Spectrom. 38 (2003) 941-947
23. Konermann L. A Minimalist Model for Exploring Conformational Effects on the Electrospray Charge State Distribution of Proteins. J. Phys. Chem. B 111 (2007) 6534-6543
24. Kaltashov I.A., and Mohimen A. Estimates of Protein Surface Area in Solution by Electrospray Ionization Mass Spectrometry. Anal. Chem. 77 (2005) 5370-5379
25. Grandori R. Detecting Equilibrium Cytochrome c Folding Intermediates by Electrospray Ionization Mass Spectrometry: Two Partially Folded Forms Populate the Molten Globule State. Protein Sci. 11 (2002) 453-458
26. Mohimen A., Dobo A., Hoerner J.K., and Kaltashov I.A. A Chemometric Approach to Detection and Characterization of Multiple Protein Conformers in Solution Using Electrospray Ionization Mass Spectrometry. Anal. Chem. 75 (2003) 4139-4147
27. Yin S., Xie Y., and Loo J.A. Mass Spectrometry of Protein-Ligand Complexes: Enhanced Gas-Phase Stability of Ribonuclease-Nucleotide Complexes. J. Am. Soc. Mass Spectrom. 19 (2008) 1199-1208
28. Benesch J.L.P., Ruotolo B.T., Simmons D.A., and Robinson C.V. Protein Complexes in the Gas Phase: Technology for Structural Genomics and Proteomics. Chem. Rev. 107 (2007) 3544-3567
29. Wang W., Kitova E.N., and Klassen J.S. Influence of Solution and Gas Phase Processes on Protein-Carbohydrate Binding Affinities Determined by Nanoelectrospray Fourier Transform Ion Cyclotron Resonance Mass Spectrometry. Anal. Chem. 75 (2003) 4945-4955
30. Feng R., and Konishi Y. Stepwise Refolding of Acid-Denatured Myoglobin: Evidence from Electrospray Mass Spectrometry. J. Am. Soc. Mass Spectrom. 4 (1993) 638-645
31. Vis H., Heinemann U., Dobson C.M., and Robinson C.V. Detection of a Monomeric Intermediate Associated with Dimerization of Protein Hu by Mass Spectrometry. J. Am. Chem. Soc. 120 (1998) 6427-6428
32. Wilson D.J., Rafferty S.P., and Konermann L. Kinetic Unfolding Mechanism of the Inducible Nitric Oxide Synthase Oxygenase Domain Determined by Time-Resolved Electrospray Mass Spectrometry. Biochemistry 44 (2005) 2276-2283
33. Nabuchi Y., Murao N., Asoh Y., and Takayama M. Probing the Unfolding and Refolding Processes of Carbonic Anhydrase 2 Using Electrospray Ionization Mass Spectrometry Combined with pH Jump. Anal. Chem. 79 (2007) 8342-8349
34. Smith A.M., Jahn T.R., Ashcroft A.E., and Radford S.E. Direct Observation of Oligomeric Species Formed in the Early Stages of Amyloid Formation Using Electrospray Ionization Mass Spectrometry. J. Mol. Biol. 364 (2006) 9-19
35. Nemirovskiy O.V., Ramanathan R., and Gross M.L. Investigation of Calcium-Induced, Noncovalent Association of Calmodulin with Melittin by Electrospray Ionization Mass Spectrometry. J. Am. Soc. Mass Spectrom. 8 (1997) 809-812
36. Invernizzi G., Samalikova M., Brocca S., Lotti M., Molinari H., and Grandori R. Comparison of Bovine and Porcine β-Lactoglobulin: A Mass Spectrometric Analysis. J. Mass Spectrom. 41 (2006) 717-727
37. Borysik A.J.H., Read P., Little D.R., Bateman R.H., Radford S.E., and Ashcroft A.E. Separation of β2-Microglobulin Conformers by High-Field Asymmetric Waveform Ion Mobility Spectrometry (FAIMS) Coupled to Electrospray Ionisation Mass Spectrometry. Rapid Commun. Mass Spectrom. 18 (2004) 2229-2234
38. Smith D.P., Giles K., Bateman R.H., Radford S.E., and Ashcroft A.E. Monitoring Copopulated Conformational States During Protein Folding Events Using Electrospray Ionization-Ion Mobility Spectrometry-Mass Spectrometry. J. Am. Soc. Mass Spectrom. 18 (2007) 2180-2190
39. Katta V., and Chait B.T. Hydrogen/Deuterium Exchange Electrospray Ionisation Mass Spectrometry: A Method for Probing Protein Conformational Changes in Solution. J. Am. Chem. Soc. 115 (1993) 6317-6321
40. Anderegg R.J., and Wagner D.S. Mass Spectrometric Characterization of a Protein-Ligand Interaction. J. Am. Chem. Soc. 117 (1995) 1374-1377
41. Jaquinod M., Guy P., Halgand F., Caffrey M., Fitch J., Cusanovich M., and Forest E. Stability Study of Rhodobacter capsulatus Ferrocytochrome c2 Wild-Type and Site-Directed Mutants Using Hydrogen/Deuterium Exchange Monitored by Electrospray Ionization Mass Spectrometry. FEBS Lett. 380 (1996) 44-48
42. Nemirovskiy O., Giblin D.E., and Gross M.L. Electrospray Ionization Mass Spectrometry and Hydrogen/Deuterium Exchange for Probing the Interaction of Calmodulin with Calcium. J. Am. Soc. Mass Spectrom. 10 (1999) 711-718
43. Krishna M.M.G., Hoang L., Lin Y., and Englander S.W. Hydrogen Exchange Methods to Study Protein Folding. Methods 34 (2004) 51-64
44. Maier C.S., Schimerlik M.I., and Deinzer M.L. Thermal Denaturation of Escherichia coli Thioredoxin Studied by Hydrogen/Deuterium Exchange and Electrospray Ionization Mass Spectrometry: Monitoring a Two-State Protein Unfolding Transition. Biochemistry 38 (1999) 1136-1143
45. Kim M.-Y., Maier C.S., Reed D.J., and Deinzer M.L. Conformational Changes in Chemically Modified Escherichia coli Thioredoxin Monitored by H/D Exchange and Electrospray Mass Spectrometry. Protein Sci. 11 (2002) 1320-1329
46. Eyles S.J., Dresch T., Gierasch L.M., and Kaltashov I.A. Unfolding Dynamics of a β-Sheet Protein Studied by Mass Spectrometry. J. Mass Spectrom. 34 (1999) 1289-1295
47. Simmons D.A., Dunn S.D., and Konermann L. Conformational Dynamics of Partially Denatured Myoglobin Studied by Time-Resolved Electrospray Mass Spectrometry with Online Hydrogen-Deuterium Exchange. Biochemistry 42 (2003) 5896-5905
48. Pan J.X., Wilson D.J., and Konermann L. Pulsed Hydrogen Exchange and Electrospray Charge-State Distribution as Complementary Probes of Protein Structure in Kinetic Experiments: Implications for Ubiquitin Folding. Biochemistry 44 (2005) 8627-8633
49. Babu K.R., and Douglas D.J. Methanol-Induced Conformations of Myoglobin at pH 4.0. Biochemistry 39 (2000) 14702-14710
50. Babu K.R., Moradian A., and Douglas D.J. The Methanol-Induced Conformational Transitions of β-Lactoglobulin, Cytochrome c, and Ubiquitin at Low pH: A Study by Electrospray Ionization Mass Spectrometry. J. Am. Soc. Mass Spectrom. 12 (2001) 317-328
51. Wang F., and Tang X. Conformational Heterogeneity and Stability of Apomyoglobin Studied by Hydrogen/Deuterium Exchange and Electrospray Ionization Mass Spectrometry. Biochemistry 35 (1996) 4069-4078
52. Bai Y., Sosnick T.R., Mayne L., and Englander S.W. Protein Folding Intermediates: Native State Hydrogen Exchange. Science 269 (1995) 192-197
53. Wagner D.S., and Anderegg R.J. Conformation of Cytochrome c Studied by Deuterium Exchange-Electrospray Ionization Mass Spectrometry. Anal. Chem. 66 (1994) 706-711
54. Anfinsen C.B. Principles That Govern the Folding of Protein Chains. Science 181 (1973) 223-230
55. Mirza U.A., Cohen S.L., and Chait B.T. Heat-Induced Conformational Changes in Proteins Studied by Electrospray Ionisation Mass Spectrometry. Anal. Chem. 65 (1993) 1-6
56. Potekhin S.A., and Kovrigin E.L. Folding under Inequilibrium Conditions as Possible Reason for Partial Irreversibility of Heat-Denatured Proteins: Computer Simulation Study. Biophys. Chem. 73 (1998) 241-248
57. Kreimer D.I., Shnyrov V.L., Villar E., Silman I., and Weiner L. Irreversible Thermal Denaturation of Torpedo californica Acetylcholinesterase. Protein Sci. 4 (1995) 2349-2357
58. Miller S., Schuler B., and Seckler R. Phage P22 Tailspike Protein: Removal of Head-Binding Domain Unmasks Effects of Folding Mutations on Native-State Thermal Stability. Protein Sci. 7 (1998) 2223-2232
59. Tani F., Shirai N., Onishi T., Venelle F., Kyoden Y., and Doi E. Temperature Control for Kinetic Refolding of Heat-Denatured Ovalbumin. Protein Sci. 6 (1997) 1491-1502
60. Boys B.L., and Konermann L. A Temperature-Jump Stopped-Flow System of Monitoring Chemical Kinetics Triggered by Rapid Cooling. Talanta 71 (2007) 1276-1281
61. Benjwal S., Verma S., Röhm K.-H., and Gursky O. Monitoring Protein Aggregation during Thermal Unfolding in Circular Dichroism Experiments. Protein Sci. 15 (2006) 635-639
62. Mirkin N., Jaconcic J., Stojanoff V., and Moreno A. High Resolution X-ray Crystallographic Structure of Bovine Heart Cytochrome c and Its Application to the Design of an Electron Transfer Biosensor. Proteins Struct. Funct. Genet. 70 (2008) 83-92
63. Babul J., and Stellwagen W. Participation of the Protein Ligands in the Folding of Cytochrome c. Biochemistry 7 (1972) 1195-1200
64. Ferguson P.L., Pan J., Wilson D.J., Dempsey B., Lajoie G., Shilton B., and Konermann L. Hydrogen/Deuterium Scrambling During Quadrupole-Time-of-Flight MS/MS Analysis of a Zinc-Binding Protein Domain. Anal. Chem. 79 (2007) 153-160
65. Bychkova V.E., Dujsekina A.E., Klenin S.I., Tiktopulo E.I., Uversky V.N., and Ptitsyn O.B. Molten Globule-Like State of Cytochrome c under Conditions Simulating Those Near the Membrane Surface. Biochemistry 35 (1996) 6058-6063
66. March R., and Todd J.F.J. Quadrupole Ion Trap Mass Spectrometry. 2nd ed. (2005), Wiley, New York
67. Brahms S., and Brahms J. Determination of Protein Secondary Structure in Solution by Vacuum Ultraviolet Circular Dichroism. J. Mol. Biol. 138 (1980) 149-178
68. Sosnick T.R., Mayne L., and Englander S.W. Molecular Collapse: The Rate-Limiting Step in Two-State Cytochrome c Folding. Proteins Struct. Biol. Genet. 24 (1996) 413-426
69. Xu G., and Chance M.R. Hydroxyl Radical-Mediated Modification of Proteins as Probes for Structural Proteomics. Chem. Rev. 107 (2007) 3514-3543
70. Tong X., Wren J.C., and Konermann L. γ-Ray-Mediated Oxidative Labeling for Detecting Protein Conformational Changes by Electrospray Mass Spectrometry. Anal. Chem. 80 (2008) 2222-2231
71. Sharp J.S., and Tomer K.B. Analysis of the Oxidative Damage-Induced Conformational Changes of Apo- and Holocalmodulin by Dose-Dependent Protein Oxidative Surface Mapping. Biophys. J. 92 (2007) 1682-1692
72. Shum W.-K., Maleknia S.D., and Downard K.M. Onset of Oxidative Damage in α-Crystallin by Radical Probe Mass Spectrometry. Anal. Biochem. 344 (2005) 247-256
73. Chao C.-C., Ma Y.-S., and Stadtman E.R. Modification of Protein Surface Hydrophobicity and Methionine Oxidation by Oxidative Systems. Proc. Natl. Acad. Sci. U. S. A. 94 (1997) 2969-2974
74. Li Y.-T., Hsieh Y.-L., Henion J.D., and Ganem B. Studies on Heme Binding in Myoglobin, Hemoglobin, and Cytochrome c by Ion Spray Mass Spectrometry. J. Am. Soc. Mass Spectrom. 4 (1993) 631-637
75. Sugiyama K., Highet R.J., Woods A., Cotter R.J., and Osawa Y. Hydrogen Peroxide-Mediated Alteration of the Heme Prosthetic Group of Metmyoglobin to an Iron Chlorin Product: Evidence for a Novel Oxidative Pathway. Proc. Natl. Acad. Sci. U. S. A. 94 (1997) 796-801
76. Xiao H., Hoerner J.K., Eyles S.J., Dobo A., Voigtman E., Melcuk A.I., and Kaltashov I.A. Mapping Protein Energy Landscapes with Amide Hydrogen Exchange and Mass Spectrometry: I. A Generalized Model for a Two-State Protein and Comparison with Experiment. Protein Sci. 14 (2005) 543-557
77. Zabrouskov V., Han X., Welker E., Zhai H., Lin C., van Wijk K.J., Scheraga H.A., and McLafferty F.W. Stepwise Deamidation of Ribonuclease A at Five Sites Determined by Top Down Mass Spectrometry. Biochemistry 45 (2006) 987-992
78. Englander S.W., Sosnick T.R., Mayne L.C., Shtilterman M., Qi P.X., and Bai Y. Fast and Slow Folding in Cytochrome c. Acc. Chem. Res. 31 (1998) 737-744
79. Houry W.A., and Scheraga H.A. Nature of the Unfolded State of Ribonuclease A: Effect of cis-trans X-Pro Peptide Bond Isomerisation. Biochemistry 35 (1996) 11719-11733
80. Dobson C.M. Protein Folding and Misfolding. Nature 426 (2003) 884-890
81. Tong X., Wren J.C., and Konermann L. Effects of Protein Concentration on the Extent of γ-Ray-Mediated Oxidative Labeling Studied by Electrospray Mass Spectrometry. Anal. Chem. 79 (2007) 6376-6382