Gas-Phase H/D Exchange and Collision Cross Sections of Hemoglobin Monomers, Dimers, and Tetramers

Journal of the American Society for Mass Spectrometry

Volumn 20, Issue 3, 2009, Pages 484-495

  Wright, P John ^a   Douglas, D J ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CHARGE STATE; COLLISION CROSS SECTIONS; COMPACT STRUCTURES; CROSS SECTIONS; CROSS-SECTION MEASUREMENTS; EXCHANGE KINETICS; GAS-PHASE; GAS-PHASE IONS; H/D EXCHANGES; HEXAMERS; LOW LEVELS; MONOMER IONS; NATIVE CONFORMATIONS; OCTAMERS; TETRAMER; TETRAMERS;

DIMERS; HEMOGLOBIN; HYDROGEN; IONS; MONOMERS; SOLVATION;

CONFORMATIONS;

ANIMALS; CATTLE; HEMOGLOBINS; HYDROGEN; MASS SPECTROMETRY; PROTEIN MULTIMERIZATION; WATER;

EID: 60649117125     PISSN: 10440305     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jasms.2008.11.006     Document Type: Article

References (71)

1. Murphy, K. P. Noncovalent Forces Important to the Conformational Stability of Protein Structures. In: Protein Stability and Folding: Theory and Practice, Shirley, B. A., Ed.; Humana Press: New York; pp. 1-35.
2. Hoaglund-Hyzer C.S., Counterman A.E., and Clemmer D.E. Anhydrous Protein Ions. Chem. Rev. 99 (1999) 3037-3079
3. Jarrold M.F. Peptides and Proteins in the Vapor Phase. Annu. Rev. Phys. Chem. 51 (2000) 179-207
4. Jarrold M.F. Unfolding, Refolding, and Hydration of Proteins in the Gas Phase. Acc. Chem. Res. 32 (1999) 360-367
5. Clemmer D.E., and Jarrold M.F. Ion Mobility Measurements and Their Applications to Clusters and Biomolecules. J. Mass Spectrom. 32 (1997) 577-592
6. Collins D.C., and Lee M.L. Developments in Ion Mobility Spectrometry-Mass Spectrometry. Anal. Bioanal. Chem. 372 (2002) 66-73
7. Ruotolo B.T., and Robinson C.V. Aspects of Native Proteins are Retained in Vacuum. Curr. Opin. Chem. Biol. 10 (2006) 402-408
8. Loo J.A., Berhane B., Kaddis C.S., Wooding K.M., Xie Y.M., Kaufman S.L., and Chernushevich I.V. Electrospray Ionization Mass Spectrometry and Ion Mobility Analysis of the 20S Proteasome Complex. J. Am. Soc. Mass Spectrom. 16 (2005) 998-1008
9. Ruotolo B.T., Hyung S.J., Robinson P.M., Giles K., Bateman R.H., and Robinson C.V. Ion Mobility-Mass Spectrometry Reveals Long-Lived, Unfolded Intermediates in the Dissociation of Protein Complexes. Angew. Chem. 46 (2007) 8001-8004
10. Ruotolo B.T., Giles K., Campuzano I., Sandercock A.M., Bateman R.H., and Robinson C.V. Evidence for Macromolecular Protein Rings in the Absence of Bulk Water. Science 310 (2005) 1658-1661
11. Collings B.A., and Douglas D.J. Conformation of Gas-Phase Myoglobin Ions. J. Am. Chem. Soc. 118 (1996) 4488-4489
12. Douglas D.J. An Aerodynamic Drag Model for Protein Ions. J. Am. Soc. Mass Spectrom. 5 (1994) 17-18
13. Chen Y.L., Collings B.A., and Douglas D.J. Collision Cross Sections of Myoglobin and Cytochrome c Ions with Ne, Ar, and Kr. J. Am. Soc. Mass Spectrom. 8 (1997) 681-687
14. 5. J. Am. Soc. Mass Spectrom. 13 (2002) 59-71
15. Tesic M., Wicki J., Poon D.K.Y., Withers S.G., and Douglas D.J. Gas-Phase Noncovalent Protein Complexes That Retain Solution Binding Properties: Binding of Xylobiose Inhibitors to the β-1,4 Exoglucanase from Cellulomonas fimi. J. Am. Soc. Mass Spectrom. 18 (2007) 64-73
16. Mao D.M., Ding C.F., and Douglas D.J. Hydrogen/Deuterium Exchange of Myoglobin Ions in a Linear Quadrupole Ion Trap. Rapid Commun. Mass Spectrom. 16 (2002) 1941-1945
17. Mao D.M., and Douglas D.J. H/D Exchange of Gas-Phase Bradykinin Ions in a Linear Quadrupole Ion Trap. J. Am. Soc. Mass Spectrom. 14 (2003) 85-94
18. Mao D.M., Babu K.R., Chen Y.L., and Douglas D.J. Conformations of Gas-Phase Lysozyme Ions Produced from Two Different Solution Conformations. Anal. Chem. 75 (2003) 1325-1330
19. Wright P.J., and Douglas D.J. Conformations of Gas-Phase Ions of Ubiquitin, Cytochrome c, Apomyoglobin, and β-Lactoglobulin Produced from Two Different Solution Conformations. J. Am. Soc. Mass Spectrom. 19 (2008) 1906-1913
20. Evans S.E., Lueck N., and Marzluff E.M. Gas-Phase Hydrogen/Deuterium Exchange of Proteins in an Ion Trap Mass Spectrometer. Int. J. Mass Spectrom. 222 (2003) 175-187
21. McLafferty F.W., Guan Z.Q., Haupts U., Wood T.D., and Kelleher N.L. Gaseous Conformational Structures of Cytochrome. c. J. Am. Chem. Soc. 120 (1998) 4732-4740
22. Wood T.D., Chorush R.A., Wampler F.M., Little D.P., O'Connor P.B., and McLafferty F.W. Gas-Phase Folding and Unfolding of Cytochrome c Cations. Proc. Natl. Acad. Sci. U.S.A. 92 (1995) 2451-2454
23. Freitas M.A., Hendrickson C.L., Emmett M.R., and Marshall A.G. High-Field Fourier Transform Ion Cyclotron Resonance Mass Spectrometry for Simultaneous Trapping and Gas-Phase Hydrogen/Deuterium Exchange of Peptide Ions. J. Am. Soc. Mass Spectrom. 9 (1998) 1012-1019
24. Freitas M.A., and Marshall A.G. Rate and Extent of Gas-Phase Hydrogen/Deuterium Exchange of Bradykinin: Evidence for Peptide Zwitterions in the Gas-Phase. Int. J. Mass Spectrom. 183 (1999) 221-231
25. Jurchen J.C., Garcia D.E., and Williams E.R. Further Studies on the Origins of Asymmetric Charge Partitioning in Protein Homodimers. J. Am. Soc. Mass Spectrom. 15 (2004) 1408-1415
26. Valentine S.J., and Clemmer D.E. H/D Exchange Levels of Shape-Resolved Cytochrome c Conformers in the Gas-Phase. J. Am. Chem. Soc. 119 (1997) 3558-3566
27. Valentine S.J., and Clemmer D.E. Temperature-Dependent H/D Exchange of Compact and Elongated Cytochrome c Ions in the Gas-Phase. J. Am. Soc. Mass Spectrom. 13 (2002) 506-517
28. Konermann L., Rosell F.I., Mauk A.G., and Douglas D.J. Acid-Induced Denaturation of Myoglobin Studied by Time-Resolved Electrospray Ionization Mass Spectrometry. Biochemistry 36 (1997) 6448-6454
29. Edelstein S.J., Rehmar M.J., Olson J.S., and Gibson Q.H. Functional Aspects of Subunit Association-Dissociation Equilibria of Hemoglobin. J. Biol. Chem. 245 (1970) 4372-4381
30. Vasudevan G., and McDonald M.J. Ordered Heme Binding Ensures the Assembly of Fully Functional Hemoglobin: A Hypothesis. Curr. Prot. Pept. Sci. 3 (2002) 461-466
31. Apostol I. Assessing the Relative Stabilities of Engineered Hemoglobins Using Electrospray Mass Spectrometry. Anal. Biochem. 272 (1999) 8-18
32. Simmons D.A., Wilson D.J., Lajoie G.A., Doherty-Kirby A., and Konermann L. Subunit Disassembly and Unfolding Kinetics of Hemoglobin Studied by Time-Resolved Electrospray Mass Spectrometry. Biochemistry 43 (2004) 14792-14801
33. Versluis C., and Heck A.J.R. Gas-Phase Dissociation of Hemoglobin. Int. J. Mass Spectrom. 210 (2001) 637-649
34. Light-Wahl K.J., Schwartz B.L., and Smith R.D. Observation of the Noncovalent Quaternary Associations of Proteins by Electrospray-Ionization Mass-Spectrometry. J. Am. Chem. Soc. 116 (1994) 5271-5278
35. Boys B.L., Kuprowski M.C., and Konermann L. Symmetric Behavior of Hemoglobin α- and β-Subunits During Acid-Induced Denaturation Observed by Electrospray Mass Spectrometry. Biochemistry 46 (2007) 10675-10684
36. Babu K.R., and Douglas D.J. Methanol-Induced Conformations of Myoglobin at pH 4.0. Biochemistry 39 (2000) 14702-14710
37. Campbell J.M., Collings B.A., and Douglas D.J. A New Linear Ion Trap Time-of-Flight System with Tandem Mass Spectrometry Capabilities. Rapid Commun. Mass Spectrom. 12 (1998) 1463-1474
38. n Capabilities. Rapid Commun. Mass Spectrom. 15 (2001) 1777-1795
39. Mark K.J., and Douglas D.J. Coulomb Effects in Binding of Heme in Gas-Phase Ions of Myoglobin. Rapid Commun. Mass Spectrom. 20 (2006) 111-117
40. Covey T., and Douglas D.J. Collision Cross-Sections for Protein Ions. J. Am. Soc. Mass Spectrom. 4 (1993) 616-623
41. Mrabet N.T., Shaeffer J.R., McDonald M.J., and Bunn H.F. Dissociation of Dimers of Human Hemoglobin-A and Hemoglobin-F into Monomers. J. Biol. Chem. 261 (1986) 1111-1115
42. Boys B.L., and Konermann L. Folding and Assembly of Hemoglobin Monitored by Electrospray Mass Spectrometry Using an On-Line Dialysis System. J. Am. Soc. Mass Spectrom. 18 (2007) 8-16
43. Griffith W.P., and Kaltashov I.A. Highly Asymmetric Interactions between Globin Chains During Hemoglobin Assembly Revealed by Electrospray Ionization Mass Spectrometry. Biochemistry 42 (2003) 10024-10033
44. Hossain B.M., and Konermann L. Pulsed Hydrogen/Deuterium Exchange MS/MS for Studying the Relationship Between Noncovalent Protein Complexes in Solution and in the Gas-Phase after Electrospray Ionization. Anal. Chem. 78 (2006) 1613-1619
45. Abzalimov R.R., Frinpong 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 in Protein Unfolding. Int. J. Mass Spectrom. 253 (2006) 207-216
46. Chernushevich I.V., and Thomson B.A. Collisional Cooling of Large Ions in Electrospray Mass Spectrometry. Anal. Chem. 76 (2004) 1754-1760
47. Van Berkel W.J.H., van den Heuvel R.H.H., Versluis C., and Heck A.J.R. Detection of Intact Megadalton Protein Assemblies of Vanillyl-Alcohol Oxidase by Mass Spectrometry. Protein Sci. 9 (2000) 435-439
48. Griffon N., Baudin V., Dieryck W., Dumoulin A., Pagbier J., Poyart C., and Marden M.C. Tetramer-Dimer Equilibrium of Oxyhemoglobin Mutants Determined from Auto-Oxidation Rates. Protein Sci. 7 (1998) 673-680
49. Ackers G.K., and Thompson T.E. Determination of Stoichiometry and Equilibrium Constants for Reversibly Associating Systems by Molecular Sieve Chromatography. Proc. Natl. Acad. Sci. U.S.A. 53 (1965) 342-349
50. Chiancone E., Gilbert L.M., Gilbert G.A., and Kellet G.L. Dissociation of Hemoglobin into Subunits, I. Human Oxyhemoglobin: Gel Filtration Studies. J. Biol. Chem. 243 (1968) 1212-1219
51. Kuprowski M.C., Boys B.L., and Konermann L. Analysis of Protein Mixtures by Electrospray Mass Spectrometry: Effects of Conformation and Desolvation Behavior on the Signal Intensities of Hemoglobin Subunits. J. Am. Soc. Mass Spectrom. 18 (2007) 1279-1285
52. Green B.N., and Vinogradov S.N. An Electrospray Ionization Mass Spectrometric Study of the Subunit Structure of the Giant Hemoglobin from the Leech Nephelopsis obscura. J. Am. Soc. Mass Spectrom. 15 (2004) 22-27
53. 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
54. McKay A.R., Ruotolo B.T., Ilag L.L., and Robinson C.V. Mass Measurements of Increased Accuracy Resolve Heterogeneous Populations of Intact Ribosomes. J. Am. Chem. Soc. 128 (2006) 11433-11442
55. Sharon M., and Robinson C.V. The Role of Mass Spectrometry in Structure Elucidation of Dynamic Protein Complexes. Annu. Rev. Biochem. 76 (2007) 167-193
56. Adachi K., Zhao Yi., and Surrey S. Effects of Heme Addition on Formation of Stable Human Globin Chains and Hemoglobin Subunit Assembly in a Cell-Free System. Arch. Biochem. Biophys. 413 (2003) 99-106
57. Doster W., Bachleitner A., Dunau R., Hiebl M., and Luscher E. Thermal Properties of Water in Myoglobin Crystals and Solutions at Subzero Temperatures. Biophys. J. 50 (1986) 213-219
58. Steinbach P.J., and Brooks B.R. Protein Hydration Elucidated by Molecular-Dynamics Simulation. Proc. Natl. Acad. Sci. U.S.A. 90 (1993) 9135-9139
59. Phillips Jr. G.N., and Pettitt B.M. Structure and Dynamics of the Water around Myoglobin. Protein Sci. 4 (1995) 149-158
60. Chothia C., Wodak S., and Janin J. Role of Subunit Interfaces in Allosteric Mechanism of Hemoglobin. Proc. Natl. Acad. Sci. U.S.A. 73 (1976) 3793-3797
61. Wanasundara S.N., and Thachuk M. Theoretical Investigations of the Dissociation of Charged Protein Complexes in the Gas Phase. J. Am. Soc. Mass Spectrom. 18 (2007) 2242-2253
62. Nishii I., Kataoka M., Tokunaga F., and Goto Y. Cold Denaturation of the Molten Globule States of Apomyoglobin and a Profile for Protein Folding. Biochemistry 33 (1994) 4903-4909
63. Goto Y., Calciano L.J., and Fink A.L. Acid Induced Folding of Proteins. Proc. Natl. Acad. Sci. U.S.A. 87 (1990) 573-577
64. Fish W.W., Reynolds J.A., and Tanford C. Gel Chromatography of Proteins in Denaturing Solvents-Comparison between Sodium Dodecyl Sulfate and Guanidine Hydrochloride as Denaturants. J. Biol. Chem. 245 (1970) 5166-5168
65. Fischetti R.F., Rodi D.J., Mirza A., Irving T.C., Kondrashkina E., and Makowski L. High-Resolution Wide-Angle X-Ray Scattering of Protein Solutions: Effect of Beam Dose on Protein Integrity. J. Synchrotron. Rad. 10 (2003) 398-404
66. Ogasawar N., Yoshino M., and Asai J.P. Amp Nucleosidase from Azotobacter vinelandii. II. Association and Dissociation. J. Biochem. 68 (1970) 331-340
67. Winzor D.J., and Wills P.R. Allowance for Thermodynamic Non-Ideality in the Characterization of Protein Self-Association by Frontal Exclusion Chromatography: Hemoglobin Revisited. Biophys. Chem. 104 (2003) 345-359
68. Glatter O., and Kratzky O. Small Angle X-Ray Scattering (1982), Academic Press, New York 156
69. Shelimov K.B., and Jarrold M.F. Conformations, Unfolding, and Refolding of Apomyoglobin in Vacuum: An Activation Barrier for Gas-Phase Protein Folding. J. Am. Chem. Soc. 119 (1997) 2987-2994
70. 3: Exchange Kinetics Do Not Reflect Parent Ion Structures. J. Am. Chem. Soc. 126 (2004) 6485-6490
71. Jurchen J.C., Cooper R.E., and Williams E.R. The Role of Acidic Residues and of Sodium Ion Adduction on the Gas-Phase H/D Exchange of Peptides and Peptide Dimers. J. Am. Soc. Mass Spectrom. 14 (2003) 1477-1487