Surface induced dissociation yields quaternary substructure of refractory noncovalent phosphorylase B and glutamate dehydrogenase complexes

Journal of the American Society for Mass Spectrometry

Volumn 25, Issue 3, 2014, Pages 368-379

  Ma, Xin ^a   Zhou, Mowei ^a   Wysocki, Vicki H ^a  

^a OHIO STATE UNIVERSITY   (United States)

Author keywords

Charge state; Ion mobility; Nanoelectrospray; Protein complex; Quaternary structure; Surface induced dissociation; Tandem mass spectrometry

Indexed keywords

ANIMALS; CATTLE; GLUTAMATE DEHYDROGENASE; MULTIPROTEIN COMPLEXES; PHOSPHORYLASE B; PROTEIN STRUCTURE, QUATERNARY; RABBITS; TANDEM MASS SPECTROMETRY;

EID: 84894432633     PISSN: 10440305     EISSN: 18791123     Source Type: Journal    
DOI: 10.1007/s13361-013-0790-y     Document Type: Article

References (74)

1. Loo, J.A.: Studying noncovalent protein complexes by electrospray ionization mass spectrometry. Mass Spectrom. Rev. 16, 1-23 (1997)
2. Hernandez, H.; Robinson, C.V.: Determining the stoichiometry and interactions of macromolecular assemblies from mass spectrometry. Nat. Protoc. 2, 715-726 (2007)
3. Benesch, J.L.; Ruotolo, B.T.; Simmons, D.A.; Robinson, C.V.: Protein complexes in the gas phase: technology for structural genomics and proteomics. Chem. Rev. 107, 3544-3567 (2007)
4. Kaddis, C.S.; Loo, J.A.: Native protein MS and ion mobility large flying proteins with ESI. Anal. Chem. 79, 1778-1784 (2007)
5. Heck, A.J.: Native mass spectrometry: a bridge between interactomics and structural biology. Nat. Methods 5, 927-933 (2008)
6. Heck, A.J.; Van Den Heuvel, R.H.: Investigation of intact protein complexes by mass spectrometry. Mass Spectrom. Rev. 23, 368-389 (2004)
7. Pace, C.N.; Trevino, S.; Prabhakaran, E.; Scholtz, J.M.: Protein structure, stability and solubility in water and other solvents. Philos. Trans. R. Soc. Lond. B Biol. Sci. 359, 1225-1235 (2004)
8. Hall, Z.; Robinson, C.V.: Do charge state signatures guarantee protein conformations? J. Am. Soc. Mass Spectrom. 23, 1161-1168 (2012)
9. Uetrecht, C.; Watts, N.R.; Stahl, S.J.; Wingfield, P.T.; Steven, A.C.; Heck, A.J.: Subunit exchange rates in Hepatitis B virus capsids are geometry- and temperature-dependent. Phys. Chem. Chem. Phys. 12, 13368-13371 (2010)
10. Shoemaker, G.K.; van Duijn, E.; Crawford, S.E.; Uetrecht, C.; Baclayon, M.; Roos, W.H.; Wuite, G.J.; Estes, M.K.; Prasad, B.V.; Heck, A.J.: Norwalk virus assembly and stability monitored by mass spectrometry. Mol. Cell. Proteomics 9, 1742-1751 (2010)
11. Uetrecht, C.; Barbu, I.M.; Shoemaker, G.K.; van Duijn, E.; Heck, A.J.: Interrogating viral capsid assembly with ion mobility-mass spectrometry. Nat. Chem. 3, 126-132 (2011)
12. Uetrecht, C.; Heck, A.J.: Modern biomolecular mass spectrometry and its role in studying virus structure, dynamics, and assembly. Angew. Chem. Int. Ed. 50, 8248-8262 (2011)
13. Ruotolo, B.T.; Benesch, J.L.; Sandercock, A.M.; Hyung, S.J.; Robinson, C.V.: Ion mobility-mass spectrometry analysis of large protein complexes. Nat. Protoc. 3, 1139-1152 (2008)
14. Uetrecht, C.; Rose, R.J.; van Duijn, E.; Lorenzen, K.; Heck, A.J.: Ion mobility mass spectrometry of proteins and protein assemblies. Chem. Soc. Rev. 39, 1633-1655 (2010)
15. Jurneczko, E.; Barran, P.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, 20-28 (2011)
16. Borsdorf, H.; Mayer, T.; Zarejousheghani, M.; Eiceman, G.A.: Recent developments in ion mobility spectrometry. Appl. Spectrosc. Rev. 46, 472-521 (2011)
17. Borsdorf, H.; Eiceman, G.A.: Ion mobility spectrometry: principles and applications. Appl. Spectrosc. Rev. 41, 323-375 (2006)
18. Politis, A.; Park, A.Y.; Hyung, S.J.; Barsky, D.; Ruotolo, B.T.; Robinson, C.V.: Integrating ion mobility mass spectrometry with molecular modeling to determine the architecture of multiprotein complexes. PLoS One 5, e12080 (2010)
19. Scarff, C.A.; Thalassinos, K.; Hilton, G.R.; Scrivens, J.H.: Traveling 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, 3297-3304 (2008)
20. Geels, R.B.J.; van der Vies, S.M.; Heck, A.J.R.; Heeren, R.M.A.: Electron capture dissociation as structural probe for noncovalent gas-phase protein assemblies. Anal. Chem. 78, 7191-7196 (2006)
21. Zhang, H.; Cui, W.; Wen, J.; Blankenship, R.E.; Gross, M.L.: Native electrospray and electron-capture dissociation FTICR mass spectrometry for top-down studies of protein assemblies. Anal. Chem. 83, 5598-5606 (2011)
22. Raspopov, S.A.; El-Faramawy, A.; Thomson, B.A.; Siu, K.W.M.: Infrared multiphoton dissociation in quadrupole time-of-flight mass spectrometry: top-down characterization of proteins. Anal. Chem. 78, 4572-4577 (2006)
23. Fernandez, F.M.; Wysocki, V.H.; Futrell, J.H.; Laskin, J.: Protein identification via surface-induced dissociation in an FT-ICR mass spectrometer and a patchwork sequencing approach. J. Am. Soc. Mass Spectrom. 17, 700-709 (2006)
24. Wysocki, V.H.; Joyce, K.E.; Jones, C.M.; Beardsley, R.L.: Surface-induced dissociation of small molecules, peptides, and noncovalent protein complexes. J. Am. Soc. Mass Spectrom. 19, 190-208 (2008)
25. Wysocki, V.H.; Jones, C.M.; Galhena, A.S.; Blackwell, A.E.: 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, 903-913 (2008)
26. Beardsley, R.L.; Jones, C.M.; Galhena, A.S.; Wysocki, V.H.: Noncovalent protein tetramers and pentamers with "n" charges yield monomers with n/4 and n/5 charges. Anal. Chem. 81, 1347-1356 (2009)
27. Felitsyn, N.; Kitova, E.N.; Klassen, J.S.: Thermal decomposition of a gaseous multiprotein complex studied by blackbody infrared radiative dissociation. Investigating the origin of the asymmetric dissociation behavior. Anal. Chem. 73, 4647-4661 (2001)
28. Jurchen, J.C.; Williams, E.R.: Origin of asymmetric charge partitioning in the dissociation of gas-phase protein homodimers. J. Am. Chem. Soc. 125, 2817-2826 (2003)
29. Boeri Erba, E.; Ruotolo, B.T.; Barsky, D.; Robinson, C.V.: Ion mobility-mass spectrometry reveals the influence of subunit packing and charge on the dissociation of multiprotein complexes. Anal. Chem. 82, 9702-9710 (2010)
30. Pagel, K.; Hyung, S.J.; Ruotolo, B.T.; Robinson, C.V.: Alternate dissociation pathways identified in charge-reduced protein complex ions. Anal. Chem. 82, 5363-5372 (2010)
31. Hall, Z.; Politis, A.; Bush, M.F.; Smith, L.J.; Robinson, C.V.: Charge-state dependent compaction and dissociation of protein complexes: insights from ion mobility and molecular dynamics. J. Am. Soc. Mass Spectrom. 134, 3429-3438 (2012)
32. Hall, Z.; Hernández, H.; Marsh, J.A.; Teichmann, S.A.; Robinson, C.V.: The role of salt bridges, charge density, and subunit flexibility in determining disassembly routes of protein complexes. Structure 21, 1325-1337 (2013)
33. Erba, E.B.; Ruotolo, B.T.; Barsky, D.; Robinson, C.V.: Ion mobility-mass spectrometry reveals the influence of subunit packing and charge on the dissociation of multiprotein complexes. Anal. Chem. 82, 9702-9710 (2010)
34. Jones, C.M.; Beardsley, R.L.; Galhena, A.S.; Dagan, S.; Cheng, G.; Wysocki, V.H.: Symmetrical gas-phase dissociation of noncovalent protein complexes via surface collisions. J. Am. Chem. Soc. 128, 15044-15045 (2006)
35. Blackwell, A.E.; Dodds, E.D.; Bandarian, V.; Wysocki, V.H.: Revealing the quaternary structure of a heterogeneous noncovalent protein complex through surface-induced dissociation. Anal. Chem. 83, 2862-2865 (2011)
36. Dodds, E.D.; Blackwell, A.E.; Jones, C.M.; Holso, K.L.; O'Brien, D.J.; Cordes, M.H.J.; Wysocki, V.H.: Determinants of gas-phase disassembly behavior in homodimeric protein complexes with related yet divergent structures. Anal. Chem. 83, 3881-3889 (2011)
37. Zhou, M.; Huang, C.; Wysocki, V.H.: Surface-induced dissociation of ion mobility-separated noncovalent complexes in a quadrupole/time-of-flight mass spectrometer. Anal. Chem. 84, 6016-6023 (2012)
38. Zhou, M.; Dagan, S.; Wysocki, V.H.: Protein subunits released by surface collisions of noncovalent complexes: nativelike compact structures revealed by ion mobility mass spectrometry. Angew. Chem. Int. Ed. 51, 4336-4339 (2012)
39. Zhou, M.; Dagan, S.; Wysocki, V.H.: Impact of charge state on gas-phase behaviors of noncovalent protein complexes in collision induced dissociation and surface induced dissociation. Analyst 138, 1353-1362 (2013)
40. Zhou, M.; Jones, C.M.; Wysocki, V.H.: Dissecting the large noncovalent protein complex GroEL with surface-induced dissociation and ion mobility-mass spectrometry. Anal. Chem. 85, 8262-8267 (2013)
41. Ruotolo, B.T.; Giles, K.; Campuzano, I.; Sandercock, A.M.; Bateman, R.H.; Robinson, C.V.: Evidence for macromolecular protein rings in the absence of bulk water. Science 310, 1658-1661 (2005)
42. Fernandez-Lima, F.A.; Blase, R.C.; Russell, D.H.: A study of ion-neutral collision cross-section values for low charge states of peptides, proteins, and peptide/protein complexes. Int. J. Mass Spectrom. 298, 111-118 (2010)
43. Shelimov, K.B.; Jarrold, M.F.: Conformations, unfolding, and refolding of apomyoglobin in vacuum: an activation barrier for gas-phase protein folding. J. Am. Chem. Soc. 119, 2987-2994 (1997)
44. Badman, E.R.; Hoaglund-Hyzer, C.S.; Clemmer, D.E.: Monitoring structural changes of proteins in an ion trap over approximately 10-200 ms: unfolding transitions in cytochrome c ions. Anal. Chem. 73, 6000-6007 (2001)
45. Giles, K.; Pringle, S.D.; Worthington, K.R.; Little, D.; Wildgoose, J.L.; Bateman, R.H.: Applications of a traveling wave-based radio-frequency-only stacked ring ion guide. Rapid Commun. Mass Spectrom. 18, 2401-2414 (2004)
46. Giles, K.; Williams, J.P.; Campuzano, I.: Enhancements in traveling wave ion mobility resolution. Rapid Commun. Mass Spectrom. 25, 1559-1566 (2011)
47. Zhong, Y.; Hyung, S.J.; Ruotolo, B.T.: Characterizing the resolution and accuracy of a second-generation traveling-wave ion mobility separator for biomolecular ions. Analyst 136, 3534-3541 (2011)
48. Atmanene, C.; Petiot-Becard, S.; Zeyer, D.; Van Dorsselaer, A.; Vivat Hannah, V.; Sanglier-Cianferani, S.: Exploring key parameters to detect subtle ligand-induced protein conformational changes using traveling wave ion mobility mass spectrometry. Anal. Chem. 84, 4703-4710 (2012)
49. Bush, M.F.; Hall, Z.; Giles, K.; Hoyes, J.; Robinson, C.V.; Ruotolo, B.T.: Collision cross sections of proteins and their complexes: a calibration framework and database for gas-phase structural biology. Anal. Chem. 82, 9557-9565 (2010)
50. Salbo, R.; Bush, M.F.; Naver, H.; Campuzano, I.; Robinson, C.V.; Pettersson, I.; Jorgensen, T.J.; Haselmann, K.F.: Traveling-wave ion mobility mass spectrometry of protein complexes: accurate calibrated collision cross-sections of human insulin oligomers. Rapid Commun. Mass Spectrom. 26, 1181-1193 (2012)
51. Shvartsburg, A.A.; Jarrold, M.F.: An exact hard-spheres scattering model for the mobilities of polyatomic ions. Chem. Phys. Lett. 261, 86-91 (1996)
52. Mesleh, M.F.; Hunter, J.M.; Shvartsburg, A.A.; Schatz, G.C.; Jarrold, M.F.: Structural information from ion mobility measurements: effects of the long-range potential. J. Phys. Chem. 100, 16082-16086 (1996)
53. Benesch, J.L.; Ruotolo, B.T.: Mass spectrometry: come of age for structural and dynamical biology. Curr. Opin. Struct. Biol. 21, 641-649 (2011)
54. Barford, D.; Hu, S.H.; Johnson, L.N.: Structural mechanism for glycogen phosphorylase control by phosphorylation and AMP. J. Mol. Biol. 218, 233-260 (1991)
55. Bailey, J.; Powell, L.; Sinanan, L.; Neal, J.; Li, M.; Smith, T.; Bell, E.: A novel mechanism of V-type zinc inhibition of glutamate dehydrogenase results from disruption of subunit interactions necessary for efficient catalysis. FEBS J. 278, 3140-3151 (2011)
56. Titani, K.; Koide, A.; Hermann, J.; Ericsson, L.H.; Kumar, S.; Wade, R.D.; Walsh, K.A.; Neurath, H.; Fischer, E.H.: Complete amino acid sequence of rabbit muscle glycogen phosphorylase. Proc. Natl. Acad. Sci. U. S. A. 74, 4762-4766 (1977)
57. Nakano, K.; Hwang, P.K.; Fletterick, R.J.: Complete cDNA sequence for rabbit muscle glycogen phosphorylase. FEBS Lett. 204, 283-287 (1986)
58. Fletterick, R.J.; Madsen, N.B.: The structures and related functions of phosphorylase a. Annu. Rev. Biochem. 49, 31-61 (1980)
59. Sprang, S.R.; Withers, S.G.; Goldsmith, E.J.; Fletterick, R.J.; Madsen, N.B.: Structural basis for the activation of glycogen phosphorylase b by adenosine monophosphate. Science 254, 1367-1371 (1991)
60. Johnson, L.N.; Snape, P.; Martin, J.L.; Acharya, K.R.; Barford, D.; Oikonomakos, N.G.: Crystallographic binding studies on the allosteric inhibitor glucose-6-phosphate to T state glycogen phosphorylase b. J. Mol. Biol. 232, 253-267 (1993)
61. Newgard, C.B.; Hwang, P.K.; Fletterick, R.J.: The family of glycogen phosphorylases: structure and function. Crit. Rev. Biochem. Mol. Biol. 24, 69-99 (1989)
62. Fegan, S.K.; Thachuk, M.: A charge moving algorithm for molecular dynamics simulations of gas-phase proteins. J. Chem. Theory Comput. 9, 2531-2539 (2013)
63. Wanasundara, S.; Thachuk, M.: Theoretical investigations of the dissociation of charged protein complexes in the gas phase. J. Am. Soc. Spectrom. 18, 2242-2253 (2007)
64. Wanasundara, S.N.; Thachuk, M.: Free energy barrier estimation for the dissociation of charged protein complexes in the gas phase. J. Phys. Chem. A 113, 3814-3821 (2009)
65. Wanasundara, S.N.; Thachuk, M.: Toward an improved understanding of the dissociation mechanism of gas phase protein complexes. J. Phys. Chem. B 114, 11646-11653 (2010)
66. Benesch, J.L.P.; Ruotolo, B.T.; Sobott, F.; Wildgoose, J.; Gilbert, A.; Bateman, R.; Robinson, C.V.: Quadrupole-time-of-flight mass spectrometer modified for higher-energy dissociation reduces protein assemblies to peptide fragments. Anal. Chem. 81, 1270-1274 (2008)
67. Lomeli, S.H.; Yin, S.; Ogorzalek Loo, R.R.; Loo, J.A.: Increasing charge while preserving noncovalent protein complexes for ESI-MS. J. Am. Soc. Mass Spectrom. 20, 593-596 (2009)
68. Lomeli, S.H.; Peng, I.X.; Yin, S.; Ogorzalek Loo, R.R.; Loo, J.A.: New reagents for increasing ESI multiple charging of proteins and protein complexes. J. Am. Soc. Mass Spectrom. 21, 127-131 (2010)
69. Sterling, H.J.; Williams, E.R.: Origin of supercharging in electrospray ionization of noncovalent complexes from aqueous solution. J. Am. Soc. Mass Spectrom. 20, 1933-1943 (2009)
70. Sterling, H.J.; Daly, M.P.; Feld, G.K.; Thoren, K.L.; Kintzer, A.F.; Krantz, B.A.; Williams, E.R.: Effects of supercharging reagents on noncovalent complex structure in electrospray ionization from aqueous solutions. J. Am. Soc. Mass Spectrom. 21, 1762-1774 (2010)
71. Sterling, H.J.; Cassou, C.A.; Trnka, M.J.; Burlingame, A.L.; Krantz, B.A.; Williams, E.R.: The role of conformational flexibility on protein supercharging in native electrospray ionization. Phys. Chem. Chem. Phys. 13, 18288-18296 (2011)
72. Sterling, H.; Kintzer, A.; Feld, G.; Cassou, C.; Krantz, B.; Williams, E.: Supercharging protein complexes from aqueous solution disrupts their native conformations. J. Am. Soc. Mass Spectrom. 23, 191-200 (2012)
73. Peterson, P.E.; Smith, T.J.: The structure of bovine glutamate dehydrogenase provides insights into the mechanism of allostery. Structure 7, 769-782 (1999)
74. Smith, T.J.; Peterson, P.E.; Schmidt, T.; Fang, J.; Stanley, C.A.: Structures of bovine glutamate dehydrogenase complexes elucidate the mechanism of purine regulation. J. Mol. Biol. 307, 707-720 (2001)