Calcium-induced structural transitions of the calmodulin-melittin system studied by electrospray mass spectrometry: Conformational subpopulations and metal-unsaturated intermediates

Biochemistry

Volumn 49, Issue 16, 2010, Pages 3477-3486

  Pan, Jingxi ^a   Konermann, Lars ^a  

^a UNIVERSITY OF WESTERN ONTARIO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM CONCENTRATION; CELLULAR SIGNALING; CHARGE STATE; CHARGE STATE DISTRIBUTION; ELECTROSPRAY IONIZATION MASS SPECTROMETRY; ELECTROSPRAY MASS SPECTROMETRY; FOLDED PROTEINS; KINETIC PATHWAY; MELITTIN; METAL BINDING; METAL COMPLEXATION; METAL SOURCES; METALATIONS; PREMIXED; STRUCTURAL CHANGE; STRUCTURAL TRANSITIONS; TARGET BINDING; TIME-RESOLVED;

CALCIUM; CALCIUM ALLOYS; CALMODULIN; ELECTROSPRAY IONIZATION; EXPERIMENTS; MASS SPECTROMETRY; METALS; TARGETS; TITRATION;

CAMS;

CALCIUM; CALMODULIN; MELITTIN; TARTARIC ACID;

ARTICLE; ARTIFACT; CALCIUM BINDING; COMPLEX FORMATION; CONTROLLED STUDY; DISSOCIATION CONSTANT; ELECTROSPRAY MASS SPECTROMETRY; METAL BINDING; METALLATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE;

BINDING SITES; CALCIUM; CALMODULIN; KINETICS; MELITTEN; METALS; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN CONFORMATION; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION;

EID: 77951217255     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi100261c     Document Type: Article

References (88)

1. Vetter, S. W. and Leclerc, E. (2003) Novel aspects of calmodulin target recognition and activation Eur. J. Biochem. 270, 404-414
2. Drakenberg, T., Finn, B., and Forsen, S. (2007) in Biological Inorganic Chemistry: Structure and Reactivity (Bertini, I., Gray, H. B., Stiefel, E. I., and Valentine, J. S., Eds.) pp 635 - 646, University Science Books, Sausalito, CA.
3. Kuboniwa, H., Tjandra, N., Grzesiek, S., Ren, H., Klee, C. B., and Bax, A. (1995) Solution structure of calcium-free calmodulin Nat. Struct. Biol. 2, 768-776
4. Zhang, M., Tanaka, T., and Ikura, M. (1995) Calcium-induced conformational transition revealed by the solution structure of apo calmodulin Nat. Struct. Biol. 2, 758-767
5. Chazin, W. J. (1995) Releasing the calcium trigger Nat. Struct. Biol. 2, 707-710
6. 2+ Curr. Top. Cell Regul. 27, 447-454
7. Nemirovskiy, O., Giblin, D. E., and Gross, M. L. (1999) Electrospray ionization mass spectrometry and hydrogen/deuterium exchange for probing the interaction of calmodulin with calcium J. Am. Soc. Mass Spectrom. 10, 711-718
8. Klee, C. B. (1988) in Calmodulin (Cohen, P. and Klee, C. B., Eds.) pp 35 - 56, Elsevier, New York.
9. Wintrode, P. L. and Privalov, P. L. (1997) Energetics of target peptide recognition by calmodulin: a calorimetric study J. Mol. Biol. 266, 1050-1062
10. 2+/calmodulin-dependent protein kinase II (CaMKII) is activated by calmodulin with two bound calciums Proc. Natl. Acad. Sci. U.S.A. 103, 13968-13973
11. 2+ binding studied with a microfluidic mixer Proc. Natl. Acad. Sci. U.S.A. 105, 542-547
12. 2+-induced conformational changes in porcine calmodulin by H/D exchange and ESI-MS: effect of cations and ionic strength Biochemistry 42, 15388-15397
13. Chattopadhyaya, R., Meador, W. E., Means, A. R., and Quiocho, F. A. (1992) Calmodulin structure refined at 1.7 ⋯ resolution J. Mol. Biol. 228, 1177-1192
14. Crivici, A. and Ikura, M. (1995) Molecular and structural basis of target recognition by calmodulin Annu. Rev. Biophys. Biomol. Struct. 24, 85-116
15. Frederick, K. K., Marlow, M. S., Valentine, K. G., and Wand, A. J. (2007) Conformational entropy in molecular recognition by proteins Nature 448, 325-330
16. Hill, T. J., Lafitte, D., Wallace, J. I., Cooper, H. J., Tsvetkov, P. O., and Derrick, P. J. (2000) Calmodulin-peptide interactions: apocalmodulin binding to the myosin light chain kinase target site Biochemistry 39, 7284-7290
17. Wong, J. W. H., Maleknia, S. D., and Downard, K. M. (2005) Hydroxyl radical probe of the calmodulin-melittin complex interface by electrospray ionization mass spectrometry J. Am. Soc. Mass Spectrom. 16, 225-233
18. Wall, M. E., Clarage, J. B., and Phillips, G. N., Jr. (1997) Motions of calmodulin characterized using both Bragg and diffuse X-ray scattering Structure 5, 1599-1612
19. 2+ to calmodulin for activation Proc. Natl. Acad. Sci. U.S.A. 78, 871-874
20. Maulet, Y. and Cox, J. A. (1983) Structural changes in melittin and calmodulin upon complex formation and their modulation by calcium Biochemistry 22, 5680-5686
21. 2+ channels Nature 411, 484-489
22. 2+ binding sites J. Biol. Chem. 268, 20096-20104
23. 2+ requirements for calmodulin interaction with and activation of protein phosphatase Proc. Natl. Acad. Sci. U.S.A. 83, 1193-1197
24. Zhu, M. M., Rempel, D. L., Du, Z., and Gross, M. L. (2003) Quantification of protein-ligand interactions by mass spectrometry, titration, and H/D exchange: PLIMSTEX J. Am. Chem. Soc. 125, 5252-5253
25. Powell, K. D., Ghaemmaghami, S., Wang, M. Z., Ma, L., Oas, T. G., and Fitzgerald, M. C. (2002) A general mass spectrometry-based assay for the quantitation of protein-ligand binding interactions in solution J. Am. Chem. Soc. 124, 10256-10257
26. Pan, J., Han, J., Borchers, C. H., and Konermann, L. (2009) Hydrogen/deuterium exchange mass spectrometry with top-down electron capture dissociation for characterizing structural transitions of a 17 kDa protein J. Am. Chem. Soc. 131, 12801-12808
27. Mendoza, V. L. and Vachet, R. W. (2009) Probing protein structure by amino acid-specific covalent labeling and mass spectrometry Mass Spectrom. Rev. 28, 785-815
28. Sinz, A. (2003) Chemical cross-linking and mass spectrometry for mapping three-dimensional structures of proteins and protein complexes J. Mass Spectrom. 38, 1225-1237
29. Ruotolo, B. T., Giles, K., Campuzano, I., Sandercock, A. M., Bateman, R. H., and Robinson, C. V. (2005) Evidence for macromolecular protein rings in the absence of bulk water Science 310, 1658-1661
30. Jurgensen, T. J. D., Roepstorff, P., and Heck, A. J. R. (1998) Direct determination of solution binding constants for noncovalent complexes between bacterial cell wall peptide analogues and vancomycin group antibiotics by electrospray ionization mass spectrometry Anal. Chem. 70, 4427-4432
31. Wang, W., Kitova, E. N., and Klassen, J. S. (2003) 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, 4945-4955
32. Jecklin, M. C., Touboul, D., Bovet, C., Wortmann, A., and Zenobi, R. (2008) Which electrospray-based ionization method best reflects protein-ligand interactions found in solution? A comparison of ESI, nanoESI, and ESSI for the determination of dissociation constants with mass spectrometry J. Am. Soc. Mass Spectrom. 19, 332-343
33. Frycak, P. and Schug, K. A. (2007) On-line dynamic titration: determination of dissociation constants for noncovalent complexes using Gaussian concentration profiles by electrospray ionization mass spectrometry Anal. Chem. 79, 5407-5413
34. Gabelica, V., Rosu, F., and De Pauw, E. (2009) A simple method to determine electrospray response factors of noncovalent complexes Anal. Chem. 81, 6708-6715
35. Robinson, C. V., Chung, E. W., Kragelund, B. B., Knudsen, J., Aplin, R. T., Poulsen, F. M., and Dobson, C. M. (1996) Probing the nature of noncovalent interactions by mass spectrometry. A study of protein-CoA ligand binding and assembly J. Am. Chem. Soc. 118, 8646-8653
36. Wang, W., Kitova, E. N., and Klassen, J. S. (2005) Nonspecific protein-carbohydrate complexes produced by nanoelectrospray ionization. Factors influencing their formation and stability Anal. Chem. 77, 3060-3071
37. Loo, J. A. (2005) in The Encyclopedia of Mass Spectrometry (Gross, M. L. and Caprioli, R. M., Eds.) pp 289 - 299, Elsevier, Amsterdam.
38. Benesch, J. L. P., Ruotolo, B. T., Simmons, D. A., and Robinson, C. V. (2007) Protein complexes in the gas phase: technology for structural genomics and proteomics Chem. Rev. 107, 3544-3567
39. Heck, A. J. R. (2008) Native mass spectrometry: a bridge between interactomics and structural biology Nat. Methods 5, 927-933
40. Konermann, L. (2007) A minimalist model for exploring conformational effects on the electrospray charge state distribution of proteins J. Phys. Chem. B 111, 6534-6543
41. Kaltashov, I. A. and Eyles, S. J. (2005) Mass Spectrometry in Biophysics, John Wiley and Sons, Hoboken, NJ.
42. Sogbein, O. O., Simmons, D. A., and Konermann, L. (2000) The effects of pH on the kinetic reaction mechanism of myoglobin unfolding studied by time-resolved electrospray ionization mass spectrometry J. Am. Soc. Mass Spectrom. 11, 312-319
43. Grandori, R. (2002) Detecting equilibrium cytochrome c folding intermediates by electrospray ionization mass spectrometry: two partially folded forms populate the molten globule state Protein Sci. 11, 453-458
44. Borysic, A. J. H., Radford, S. E., and Ashcroft, A. E. (2004) Co-populated conformational ensembles of I2-microglobulin uncovered quantitatively by electrospray ionization mass spectrometry J. Biol. Chem. 279, 27069-27077
45. Cai, X. and Dass, C. (2003) Conformational analysis of proteins and peptides Curr. Org. Chem. 7, 1841-8154
46. Frimpong, A. K., Abzatimov, R. R., Uversky, V. N., and Kaltashov, I. A. (2010) Characterization of intrinsically disordered proteins with electrospray ionization mass spectrometry: conformational heterogeneity of alpha-synuclein Proteins 78, 714-722
47. Katta, V. and Chait, B. T. (1991) Observation of the heme-globin complex in native myoglobin by electrospray-ionisation mass spectrometry J. Am. Chem. Soc. 113, 8534-8535
48. Vis, H., Heinemann, U., Dobson, C. M., and Robinson, C. V. (1998) Detection of a monomeric intermediate associated with dimerization of protein Hu by mass spectrometry J. Am. Chem. Soc. 120, 6427-6428
49. Wilson, D. J., Rafferty, S. P., and Konermann, L. (2005) Kinetic unfolding mechanism of the inducible nitric oxide synthase oxygenase domain determined by time-resolved electrospray mass spectrometry Biochemistry 44, 2276-2283
50. Gumerov, D. R., Mason, A. B., and Kaltashov, I. A. (2003) Interlobe communication in human serum transferrin: metal binding and conformational dynamics investigated by electrospray ionization mass spectrometry Biochemistry 42, 5421-5428
51. Nemirovskiy, O. V., Ramanathan, R., and Gross, M. L. (1997) Investigation of calcium-induced, noncovalent association of calmodulin with melittin by electrospray ionization mass spectrometry J. Am. Soc. Mass Spectrom. 8, 809-812
52. Hu, P. and Loo, J. A. (1995) Determining calcium-binding stoichiometry and cooperativity of parvalbumin and calmodulin by mass spectrometry J. Mass Spectrom. 30, 1076-1082
53. Shirran, S. L. and Barran, P. E. (2009) The use of ESI-MS to probe the binding of divalent cations to calmodulin J. Am. Soc. Mass Spectrom. 20, 1159-1171
54. 2+ calmodulin, using negative ion electrospray ionisation mass spectrometry Rapid Commun. Mass Spectrom. 22, 3501-3509
55. Mathur, S., Badertscher, M., Scott, M., and Zenobi, R. (2007) Critical evaluation of mass spectrometric measurement of dissociation constants: accuracy and cross-validation against surface plasmon resonance and circular dichroism for the calmodulin-melittin system Phys. Chem. Chem. Phys. 9, 6187-6198
56. Watt, S. J., Oakley, A., Sheil, M. M., and Beck, J. L. (2005) Comparison of negative and positive ion electrospray ionization mass spectra of calmodulin and its complex with trifluoperazine Rapid Commun. Mass Spectrom. 19, 2123-2130
57. Ly, T. and Julian, R. R. (2008) Protein-metal interactions of calmodulin and α-synuclein monitored by selective noncovalent adduct protein probing mass spectrometry J. Am. Soc. Mass Spectrom. 19, 1663-1672
58. Wyttenbach, T., Grabenauer, M., Thalassinos, K., Scrivens, J. H., and Bowers, M. T. (2010) The effect of calcium ions and peptide ligands on the relative stabilities of the calmodulin dumbbell and compact structures J. Phys. Chem. B 114, 437-447
59. Lafitte, D., Capony, J. P., Grassy, G., Haiech, J., and Calas, B. (1995) Analysis of ion binding sites of calmodulin by electrospray ionization mass spectrometry Biochemistry 34, 13825-13832
60. Verkerk, U. H. and Kebarle, P. (2005) Ion-ion and ion-molecule reactions at the surface of proteins produced by nanospray. Information on the number of acidic residues and control of the number of ionized acidic and basic residues J. Am. Soc. Mass Spectrom. 16, 1325-1341
61. Turner, K. B., Monti, S. A., and Fabris, D. (2008) Like polarity ion/ion reactions enable the investigation of specific metal interactions in nucleic acids and their noncovalent assemblies J. Am. Chem. Soc. 130, 13353-13363
62. Deng, L., Sun, N., Kitova, E. N., and Klassen, J. S. (2010) Direct quantification of protein-metal ion affinities by electrospray ionization mass spectrometry Anal. Chem. 82, 2170-2174
63. Hu, P., Ye, Q.-Z., and Loo, J. A. (1994) Calcium stoichiometry determination for calcium binding proteins by electrospray ionization mass spectrometry Anal. Chem. 66, 4190-4194
64. Watt, S. J., Oakley, A., Sheil, M. M., and Beck, J. L. (2006) Comparison of negative and positive ion electrospray ionization mass spectra of calmodulin and its complex with trifluoperazine Rapid Commun. Mass Spectrom. 19, 2123-2130
65. Pan, J., Xu, K., Yang, X., Choy, W. Y., and Konermann, L. (2009) Solution-phase chelators for suppressing nonspecific protein-metal interactions in electrospray mass spectrometry Anal. Chem. 81, 5008-5015
66. Cannan, R. K. and Kibrik, A. (1938) Complex formation between carboxylic acids and divalent cations J. Am. Chem. Soc. 60, 2314-2320
67. Kebarle, P. and Verkerk, U. H. (2009) Electrospray: from ions in solutions to ions in the gas phase, what we know now Mass Spectrom. Rev. 28, 898-917
68. Schulz, D. M., Ihling, C., Clore, G. M., and Sinz, A. (2004) Mapping the topology and determination of a low-resolution three-dimensional structure of the calmodulin-melittin complex by chemical cross-linking and high-resolution FTICRMS: direct demonstration of multiple binding modes Biochemistry 43, 4703-4715
69. Kataoka, M., Head, J. F., Seaton, B. A., and Engelman, D. M. (1989) Melittin binding causes a large calcium-dependent conformational change in calmodulin Proc. Natl. Acad. Sci. U.S.A. 86, 6944-6948
70. Brokx, R. D., Lopez, M. M., Vogel, H. J., and Makhatadze, G. I. (2001) Energetics of target peptide binding by calmodulin reveals different modes of binding J. Biol. Chem. 276, 14083-14091
71. Konermann, L., Rosell, F. I., Mauk, A. G., and Douglas, D. J. (1997) Acid-induced denaturation of myoglobin studied by time-resolved electrospray ionization mass spectrometry Biochemistry 36, 6448-6454 (Pubitemid 27231402)
72. 3+ to calmodulin and its effects on the interaction between calmodulin and calmodulin binding peptide, polistes mastoparan Biochemistry 43, 2688-2698
73. Putkey, J. A., Tsui, K. F., Tanaka, T., Lagacé, L., Stein, J. P., Lai, E. C., and Means, A. R. (1983) Chicken calmodulin genes. A species comparison of cDNA sequences and isolation of a genomic clone J. Biol. Chem. 258, 11864-11870
74. Pan, J. X., Rintala-Dempsey, A., Li, Y., Shaw, G. S., and Konermann, L. (2006) Folding kinetics of the S100A11 protein dimer studied by time-resolved electrospray mass spectrometry and pulsed hydrogen-deuterium exchange Biochemistry 45, 3005-3013
75. Wilson, D. J. and Konermann, L. (2003) A capillary mixer with adjustable reaction chamber volume for millisecond time resolved studies by electrospray mass spectrometry Anal. Chem. 75, 6408-6414
76. Wang, G. and Cole, R. B. (1997) in Electrospray Ionization Mass Spectroscopy (Cole, R. B., Ed.) pp 137 - 174, John Wiley & Sons, Hoboken, NJ.
77. Konermann, L. and Douglas, D. J. (1998) Unfolding of proteins monitored by electrospray ionization mass spectrometry: a comparison of positive and negative ion modes J. Am. Soc. Mass Spectrom. 9, 1248-1254
78. Burger, D., Cox, J. A., Comte, M., and Stein, E. A. (1984) Sequential conformational changes in calmodulin upon binding of calcium Biochemistry 23, 1966-1971
79. Gau, B. C., Sharp, J. S., Rempel, D. L., and Gross, M. L. (2009) Fast photochemical oxidation of protein footprints faster than protein unfolding Anal. Chem. 81, 6563-6571
80. Tripathi, S. and Portman, J. J. (2009) Inherent flexibility determines the transition mechanisms of the EF-hands of calmodulin Proc. Natl. Acad. Sci. U.S.A. 106, 2104-2109
81. Kuprowski, M. C. and Konermann, L. (2007) Signal response of co-existing protein conformers in electrospray mass spectrometry Anal. Chem. 79, 2499-2506
82. Scaloni, A., Miraglia, N., Orrui, S., Amodeo, P., Motta, A., Marino, G., and Pucci, P. (1998) Topology of the calmodulin-melittin complex J. Mol. Biol. 277, 945-958 (Pubitemid 28195992)
83. Llinás, R., Sugimori, M., and Silver, R. B. (1995) The concept of calcium concentration microdomains in synaptic transmission Neuropharmacology 34, 1443-1451
84. 2+ indicators in frog skeletal muscle fibers Biophys. J. 70, 896-916 (Pubitemid 26028304)
85. Konermann, L., Pan, J., Simmons, D. A., and Wilson, D. J. (2007) in The Encyclopedia of Mass Spectrometry (Gross, M. L. and Caprioli, R. M., Eds.) pp 802 - 810, Elsevier, Amsterdam.
86. Alberty, R. A. and Silbey, R. J. (1996) Physical Chemistry, John Wiley & Sons, New York.
87. Kiefhaber, T., Quaas, R., Hahn, U., and Schmid, F. X. (1990) Folding of ribonuclease T1. 1. Existence of multiple unfolded states created by proline isomerisation Biochemistry 29, 3053-3061 (Pubitemid 20119303)
88. Cheung, M. S., Klimov, D., and Thirumalai, D. (2005) Molecular crowding enhances native state stability and refolding rates of globular proteins Proc. Natl. Acad. Sci. U.S.A. 102, 4753-4758 (Pubitemid 40471526)