How far can we go with structural mass spectrometry of protein complexes?

Journal of the American Society for Mass Spectrometry

Volumn 21, Issue 4, 2010, Pages 487-500

  Sharon, Michal ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

ASYMMETRIC STRUCTURES; BIOLOGICAL FUNCTIONS; CRITICAL STEPS; FUTURE DIRECTIONS; HETEROGENEOUS COMPOSITION; LARGE SIZES; NON-COVALENT COMPLEXES; PHYSICAL INTERACTIONS; PROTEIN ASSEMBLY; PROTEIN COMPLEXES; STABLE COMPLEXES; STRUCTURAL INFORMATION; STRUCTURAL MASS; STRUCTURAL ORGANIZATION;

COMPLEXATION; MASS SPECTROMETRY; STOICHIOMETRY;

PROTEINS;

ALGORITHM; AMINO ACID SEQUENCE; ARTICLE; CELL LINE; CELL MEMBRANE; COLLISIONALLY ACTIVATED DISSOCIATION; COMPLEX FORMATION; CROSS LINKING; HYBRIDIZATION; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; NONHUMAN; PROTEIN ANALYSIS; PROTEIN ASSEMBLY; PROTEIN CONFORMATION; PROTEIN INTERACTION; PROTEIN STRUCTURE; STOICHIOMETRY; STRUCTURE ANALYSIS;

FORECASTING; MASS SPECTROMETRY; MICROCHEMISTRY; PEPTIDE MAPPING; PROTEINS;

EID: 77950339600     PISSN: 10440305     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jasms.2009.12.017     Document Type: Article

References (96)

1. Lander E.S., Linton L.M., Birren B., Nusbaum C., Zody M.C., Baldwin J., Devon K., Dewar K., Doyle M., FitzHugh W., Funke R., Gage D., Harris K., Heaford A., Howland J., Kann L., Lehoczky J., LeVine R., McEwan P., McKernan K., Meldrim J., Mesirov J.P., Miranda C., Morris W., Naylor J., Raymond C., Rosetti M., Santos R., Sheridan A., Sougnez C., Stange-Thomann N., Stojanovic N., Subramanian A., Wyman D., Rogers J., Sulston J., Ainscough R., Beck S., Bentley D., Burton J., Clee C., Carter N., Coulson A., Deadman R., Deloukas P., Dunham A., Dunham I., Durbin R., French L., Grafham D., Gregory S., Hubbard T., Humphray S., Hunt A., Jones M., Lloyd C., McMurray A., Matthews L., Mercer S., Milne S., Mullikin J.C., Mungall A., Plumb R., Ross M., Shownkeen R., Sims S., Waterston R.H., Wilson R.K., Hillier L.W., McPherson J.D., Marra M.A., Mardis E.R., Fulton L.A., Chinwalla A.T., Pepin K.H., Gish W.R., Chissoe S.L., Wendl M.C., Delehaunty K.D., Miner T.L., Delehaunty A., Kramer J.B., Cook L.L., Fulton R.S., Johnson D.L., Minx P.J., Clifton S.W., Hawkins T., Branscomb E., Predki P., Richardson P., Wenning S., Slezak T., Doggett N., Cheng J.F., Olsen A., Lucas S., Elkin C., Uberbacher E., Frazier M., Gibbs R.A., Muzny D.M., Scherer S.E., Bouck J.B., Sodergren E.J., Worley K.C., Rives C.M., Gorrell J.H., Metzker M.L., Naylor S.L., Kucherlapati R.S., Nelson D.L., Weinstock G.M., Sakaki Y., Fujiyama A., Hattori M., Yada T., Toyoda A., Itoh T., Kawagoe C., Watanabe H., Totoki Y., Taylor T., Weissenbach J., Heilig R., Saurin W., Artiguenave F., Brottier P., Bruls T., Pelletier E., Robert C., Wincker P., Smith D.R., Doucette-Stamm L., Rubenfield M., Weinstock K., Lee H.M., Dubois J., Rosenthal A., Platzer M., Nyakatura G., Taudien S., Rump A., Yang H., Yu J., Wang J., Huang G., Gu J., Hood L., Rowen L., Madan A., Qin S., Davis R.W., Federspiel N.A., Abola A.P., Proctor M.J., Myers R.M., Schmutz J., Dickson M., Grimwood J., Cox D.R., Olson M.V., Kaul R., Shimizu N., Kawasaki K., Minoshima S., Evans G.A., Athanasiou M., Schultz R., Roe B.A., Chen F., Pan H., Ramser J., Lehrach H., Reinhardt R., McCombie W.R., de la Bastide M., Dedhia N., Blocker H., Hornischer K., Nordsiek G., Agarwala R., Aravind L., Bailey J.A., Bateman A., Batzoglou S., Birney E., Bork P., Brown D.G., Burge C.B., Cerutti L., Chen H.C., Church D., Clamp M., Copley R.R., Doerks T., Eddy S.R., Eichler E.E., Furey T.S., Galagan J., Gilbert J.G., Harmon C., Hayashizaki Y., Haussler D., Hermjakob H., Hokamp K., Jang W., Johnson L.S., Jones T.A., Kasif S., Kaspryzk A., Kennedy S., Kent W.J., Kitts P., Koonin E.V., Korf I., Kulp D., Lancet D., Lowe T.M., McLysaght A., Mikkelsen T., Moran J.V., Mulder N., Pollara V.J., Ponting C.P., Schuler G., Schultz J., Slater G., Smit A.F., Stupka E., Szustakowski J., Thierry-Mieg D., Thierry-Mieg J., Wagner L., Wallis J., Wheeler R., Williams A., Wolf Y.I., Wolfe K.H., Yang S.P., Yeh R.F., Collins F., Guyer M.S., Peterson J., Felsenfeld A., Wetterstrand K.A., Patrinos A., Morgan M.J., de Jong P., Catanese J.J., Osoegawa K., Shizuya H., Choi S., Chen Y.J., et al. Initial Sequencing and Analysis of the Human Genome. Nature 2001, 409:860-921.
2. Venter J.C., Adams M.D., Myers E.W., Li P.W., Mural R.J., Sutton G.G., Smith H.O., Yandell M., Evans C.A., Holt R.A., Gocayne J.D., Amanatides P., Ballew R.M., Huson D.H., Wortman J.R., Zhang Q., Kodira C.D., Zheng X.H., Chen L., Skupski M., Subramanian G., Thomas P.D., Zhang J., Gabor Miklos G.L., Nelson C., Broder S., Clark A.G., Nadeau J., McKusick V.A., Zinder N., Levine A.J., Roberts R.J., Simon M., Slayman C., Hunkapiller M., Bolanos R., Delcher A., Dew I., Fasulo D., Flanigan M., Florea L., Halpern A., Hannenhalli S., Kravitz S., Levy S., Mobarry C., Reinert K., Remington K., Abu-Threideh J., Beasley E., Biddick K., Bonazzi V., Brandon R., Cargill M., Chandramouliswaran I., Charlab R., Chaturvedi K., Deng Z., Di Francesco V., Dunn P., Eilbeck K., Evangelista C., Gabrielian A.E., Gan W., Ge W., Gong F., Gu Z., Guan P., Heiman T.J., Higgins M.E., Ji R.R., Ke Z., Ketchum K.A., Lai Z., Lei Y., Li Z., Li J., Liang Y., Lin X., Lu F., Merkulov G.V., Milshina N., Moore H.M., Naik A.K., Narayan V.A., Neelam B., Nusskern D., Rusch D.B., Salzberg S., Shao W., Shue B., Sun J., Wang Z., Wang A., Wang X., Wang J., Wei M., Wides R., Xiao C., Yan C., Yao A., Ye J., Zhan M., Zhang W., Zhang H., Zhao Q., Zheng L., Zhong F., Zhong W., Zhu S., Zhao S., Gilbert D., Baumhueter S., Spier G., Carter C., Cravchik A., Woodage T., Ali F., An H., Awe A., Baldwin D., Baden H., Barnstead M., Barrow I., Beeson K., Busam D., Carver A., Center A., Cheng M.L., Curry L., Danaher S., Davenport L., Desilets R., Dietz S., Dodson K., Doup L., Ferriera S., Garg N., Gluecksmann A., Hart B., Haynes J., Haynes C., Heiner C., Hladun S., Hostin D., Houck J., Howland T., Ibegwam C., Johnson J., Kalush F., Kline L., Koduru S., Love A., Mann F., May D., McCawley S., McIntosh T., McMullen I., Moy M., Moy L., Murphy B., Nelson K., Pfannkoch C., Pratts E., Puri V., Qureshi H., Reardon M., Rodriguez R., Rogers Y.H., Romblad D., Ruhfel B., Scott R., Sitter C., Smallwood M., Stewart E., Strong R., Suh E., Thomas R., Tint N.N., Tse S., Vech C., Wang G., Wetter J., Williams S., Williams M., Windsor S., Winn-Deen E., Wolfe K., Zaveri J., Zaveri K., Abril J.F., Guigo R., Campbell M.J., Sjolander K.V., Karlak B., Kejariwal A., Mi H., Lazareva B., Hatton T., Narechania A., Diemer K., Muruganujan A., Guo N., Sato S., Bafna V., Istrail S., Lippert R., Schwartz R., Walenz B., Yooseph S., Allen D., Basu A., Baxendale J., Blick L., Caminha M., Carnes-Stine J., Caulk P., Chiang Y.H., Coyne M., Dahlke C., Mays A., Dombroski M., Donnelly M., Ely D., Esparham S., Fosler C., Gire H., Glanowski S., Glasser K., Glodek A., Gorokhov M., Graham K., Gropman B., Harris M., Heil J., Henderson S., Hoover J., Jennings D., Jordan C., Jordan J., Kasha J., Kagan L., Kraft C., Levitsky A., Lewis M., Liu X., Lopez J., Ma D., Majoros W., McDaniel J., Murphy S., Newman M., Nguyen T., Nguyen N., Nodell M., Pan S., Peck J., Peterson M., Rowe W., Sanders R., Scott J., Simpson M., Smith T., Sprague A., Stockwell T., Turner R., Venter E., Wang M., Wen M., Wu D., Wu M., Xia A., Zandieh A., Zhu X. The Sequence of the Human Genome. Science 2001, 291:1304-1351.
3. Hart G.T., Ramani A.K., Marcotte E.M. How Complete are Current Yeast and Human Protein-Interaction Networks?. Genome Biol. 2006, 7:120.
4. Reguly T., Breitkreutz A., Boucher L., Breitkreutz B.J., Hon G.C., Myers C.L., Parsons A., Friesen H., Oughtred R., Tong A., Stark C., Ho Y., Botstein D., Andrews B., Boone C., Troyanskya O.G., Ideker T., Dolinski K., Batada N.N., Tyers M. Comprehensive Curation and Analysis of Global Interaction Networks in Saccharomyces cerevisiae. J. Biol. 2006, 5:11.
5. Stumpf M.P., Thorne T., de Silva E., Stewart R., An H.J., Lappe M., Wiuf C. Estimating the Size of the Human Interactome. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:6959-6964.
6. Sharon M., Mao H., Boeri Erba E., Stephens E., Zheng N., Robinson C.V. Symmetrical Modularity of the COP9 Signalosome Complex Suggests Its Multifunctionality. Structure 2009, 17:31-40.
7. Robinson C.V., Sali A., Baumeister W. The Molecular Sociology of the Cell. Nature 2007, 450:973-982.
8. Sali A., Glaeser R., Earnest T., Baumeister W. From Words to Literature in Structural Proteomics. Nature 2003, 422:216-225.
9. 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. 2007, 107:3544-3567.
10. Heck A.J. Native Mass Spectrometry: A Bridge Between Interactomics and Structural biology. Nat. Methods 2008, 5:927-933.
11. Loo J.A. Studying Noncovalent Protein Complexes by Electrospray Ionization Mass Spectrometry. Mass Spectrom. Rev. 1997, 16:1-23.
12. Sharon M., Robinson C.V. The Role of Mass Spectrometry in Structure Elucidation of Dynamic Protein Complexes. Annu. Rev. Biochem. 2007, 76:167-193.
13. van den Heuvel R.H., Heck A.J. Native Protein Mass Spectrometry: From Intact Oligomers to Functional Machineries. Curr. Opin. Chem. Biol. 2004, 8:519-526.
14. Ganem B., Li Y.T., Henion J.D. Detection of Noncovalent Receptor-Ligand Complexes by Mass Spectrometry. J Am. Chem. Soc. 1991, 113:6294-6296.
15. Ganem B., Li Y.T., Henion J.D. Observation of Noncovalent Enzyme-Substrate and Enzyme-Product Complexes by Ion-Spray Mass Spectrometry. J. Am. Chem. Soc. 1991, 113:7818-7819.
16. Karasa M., Bahra U., Ingendoha A., Nordhoffa E., Stahla B., Strupata K., Hillenkamp F. Principles and Applications of Matrix-Assisted UV-Laser Desorption/Ionization Mass Spectrometry. Anal. Chim. Acta 1990, 241:175-185.
17. Videler H., Ilag L.L., McKay A.R., Hanson C.L., Robinson C.V. Mass Spectrometry of Intact Ribosomes. FEBS Lett. 2005, 579:943-947.
18. Uetrecht C., Versluis C., Watts N.R., Roos W.H., Wuite G.J., Wingfield P.T., Steven A.C., Heck A.J. High-Resolution Mass Spectrometry of Viral Assemblies: Molecular Composition and Stability of Dimorphic Hepatitis B Virus Capsids. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:9216-9220.
19. Uetrecht C., Versluis C., Watts N.R., Wingfield P.T., Steven A.C., Heck A.J. Stability and Shape of Hepatitis B Virus Capsids In Vacuo. Angew. Chem. Int. Ed. Engl. 2008, 47:6247-6251.
20. Morton V.L., Stockley P.G., Stonehouse N.J., Ashcroft A.E. Insights into Virus Capsid Assembly from Noncovalent Mass Spectrometry. Mass Spectrom. Rev. 2008, 27:575-595.
21. van Duijn E., Simmons D.A., van den Heuvel R.H., Bakkes P.J., van Heerikhuizen H., Heeren R.M., Robinson C.V., van der Vies S.M., Heck A.J. Tandem Mass Spectrometry of Intact GroEL-Substrate Complexes Reveals Substrate-Specific Conformational Changes in the trans Ring. J Am. Chem. Soc. 2006, 128:4694-4702.
22. van Duijn E., Heck A.J., van der Vies S.M. Inter-Ring Communication Allows the GroEL Chaperonin Complex to Distinguish Between Different Substrates. Protein Sci. 2007, 16:956-965.
23. Sharon M., Witt S., Felderer K., Rockel B., Baumeister W., Robinson C.V. 20S Proteasomes Have the Potential to Keep Substrates in Store for Continual Degradation. J. Biol. Chem. 2006, 281:9569-9575.
24. Aquilina J.A., Benesch J.L., Bateman O.A., Slingsby C., Robinson C.V. Polydispersity of a Mammalian Chaperone: Mass Spectrometry Reveals the Population of Oligomers in αB-crystallin. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:10611-10616.
25. Bich C., Zenobi R. Mass Spectrometry of Large Complexes. Curr. Opin. Struct. Biol. 2009, 19:632-639.
26. Charvat A., Abel B. How to Make Big Molecules Fly Out of Liquid Water: Applications, Features, and Physics of Laser Assisted Liquid Phase Dispersion Mass Spectrometry. Phys. Chem., Chem. Phys. 2007, 9:3335-3360.
27. Bolbach G. Matrix-Assisted Laser Desorption/Ionization Analysis of Noncovalent Complexes: Fundamentals and Applications. Curr. Pharm. Des. 2005, 11:2535-2557.
28. Smith D.L., Zhang Z. Probing Noncovalent Structural Interactions in Soybean Agglutinin by Electrofeatures of Proteins by Mass Spectrometry. Mass Spectrom. Rev. 1994, 13:411-429.
29. Smith V.F., Schwartz B.L., Randall L.L., Smith R.D. Electrospray Mass Spectrometric Investigation of the Chaperone SecB. Protein Sci. 1996, 5:488-494.
30. Mcluckey S.A. Principles of Collisional Activation in Analytical Mass Spectrometry. J Am. Soc. Mass Spectrom. 1992, 3:599-614.
31. Benesch J.L., Aquilina J.A., Ruotolo B.T., Sobott F., Robinson C.V. Tandem Mass Spectrometry Reveals the Quaternary Organization of Macromolecular Assemblies. Chem. Biol. 2006, 13:597-605.
32. Chernushevich I.V., Thomson B.A. Collisional Cooling of Large Ions in Electrospray Mass Spectrometry. Anal. Chem. 2004, 76:1754-1760.
33. Sobott F., Hernandez H., McCammon M.G., Tito M.A., Robinson C.V. A Tandem Mass Spectrometer for Improved Transmission and Analysis of Large Macromolecular Assemblies. Anal. Chem. 2002, 74:1402-1407.
34. Hernandez H., Dziembowski A., Taverner T., Seraphin B., Robinson C.V. Subunit Architecture of Multimeric Complexes Isolated Directly from cells. EMBO Rep. 2006, 7:605-610.
35. Sharon M., Taverner T., Ambroggio X.I., Deshaies R.J., Robinson C.V. Structural Organization of the 19S Oroteasome Lid: Insights from MS of Intact Complexes. PLoS Biol 2006, 4:e267.
36. 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. 2004, 18:2401-2414.
37. Thalassinos K., Slade S.E., Jennings K.R., Scrivens J.H., Giles K., Wildgoose J., Hoyes J., Bateman R.H., Bowers M.T. Ion Mobility Mass Spectrometry of Proteins in a Modified Commercial Mass Spectrometer. Int. J. Mass Spectrom. 2004, 236:55-63.
38. Zhou M., Sandercock A.M., Fraser C.S., Ridlova G., Stephens E., Schenauer M.R., Yokoi-Fong T., Barsky D., Leary J.A., Hershey J.W., Doudna J.A., Robinson C.V. Mass Spectrometry Reveals Modularity and a Complete Subunit Interaction Map of the Eukaryotic Translation Factor eIF3. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:18139-18144.
39. Ferrige A.G., Seddon M.J., Green B.N., Jarvis S.A., Skilling J., Staunton J. Disentangling Electrospray Spectra with Maximum Entropy. Rapid Commun. Mass Spectrom. 1992, 6:707-711.
40. Ferrige A.G., Seddon M.J., Skilling J., Ordsmith N. The Application of MaxEnt to High Resolution Mass Spectrometry. Mass Spectrom. 1992, 6:765-770.
41. Taverner T., Hernandez H., Sharon M., Ruotolo B.T., Matak-Vinkovic D., Devos D., Russell R.B., Robinson C.V. Subunit Architecture of Intact Protein Complexes from Mass Spectrometry and Homology Modeling. Acc. Chem. Res. 2008, 41:617-627.
42. van Breukelen B., Barendregt A., Heck A.J., van den Heuvel R.H. Resolving Stoichiometries and Oligomeric States of Glutamate Synthase Protein Complexes with Curve Fitting and Simulation of Electrospray Mass Spectra. Rapid Commun. Mass Spectrom. 2006, 20:2490-2496.
43. McKay A.R., Ruotolo B.T., Ilag L.L., Robinson C.V. Mass Measurements of Increased Accuracy Resolve Heterogeneous Populations of Intact Ribosomes. J. Am. Chem. Soc. 2006, 128:11433-11442.
44. Waugh D.S. Making the Most of Affinity Tags. Trends Biotechnol. 2005, 23:316-320.
45. Brizzard B. Epitope Yagging. Biotechniques 2008, 44:693-695.
46. Benesch J.L.P., Aquilina J.A., Ruotolo B.T., Sobott F., Robinson C.V. Tandem Mass Spectrometry Reveals the Quaternary Organization of Macromolecular Assemblies. Chem. Biol. 2006, 13:597-605.
47. Fandrich M., Tito M.A., Leroux M.R., Rostom A.A., Hartl F.U., Dobson C.M., Robinson C.V. Observation of the Noncovalent Assembly and Disassembly Pathways of the Chaperone Complex MtGimC by Mass Spectrometry. Proc. Natl. Acad. Sci. U.S.A. 2000, 97:14151-14155.
48. Ilag L.L., Videler H., McKay A.R., Sobott F., Fucini P., Nierhaus K.H., Robinson C.V. Heptameric (L12)6/L10 Rather Than Canonical Pentameric Complexes are Found by Tandem MS of Intact Ribosomes from Thermophilic Bacteria. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:8192-8197.
49. Zhang Z., Zheng Y., Mazon H., Milgrom E., Kitagawa N., Kish-Trier E., Heck A.J., Kane P.M., Wilkens S. Structure of the Yeast Vacuolar ATPase. J. Biol. Chem. 2008, 283:35983-35995.
50. Loo J.A., Berhane B., Kaddis C.S., Wooding K.M., Xie Y., Kaufman S.L., Chernushevich I.V. Electrospray Ionization Mass Spectrometry and Ion Mobility Analysis of the 20S Proteasome Complex. J. Am. Soc. Mass Spectrom. 2005, 16:998-1008.
51. Benesch J.L., 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. 2009, 81:1270-1274.
52. 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. 2009, 20:593-596.
53. Kaltashov I.A., Abzalimov R.R. Do Ionic Charges in ESI-MS Provide Useful Information on Macromolecular Structure?. J. Am. Soc. Mass Spectrom. 2008, 19:1239-1246.
54. 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. 2009, 81:1347-1356.
55. Galhena A.S., Dagan S., Jones C.M., Beardsley R.L., Wysocki V.H. Surface-Induced Dissociation of Peptides and Protein Complexes in a Quadrupole/Time-of-Flight Mass Spectrometer. Anal. Chem. 2008, 80:1425-1436.
56. 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. 2008, 19:903-913.
57. 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. 2008, 19:190-208.
58. Hernandez H., Robinson C.V. Determining the Stoichiometry and Interactions of Macromolecular Assemblies from Mass Spectrometry. Nat. Protoc. 2007, 2:715-726.
59. Mason E.R., McDaniel E.W. Transport Properties of Ions in Gases 1988, John Wiley and Sons, New York.
60. 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. 2008, 3:1139-1152.
61. 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 2005, 310:1658-1661.
62. van Duijn E., Barendregt A., Synowsky S., Versluis C., Heck A.J. Chaperonin Complexes Monitored by Ion Mobility Mass Spectrometry. J. Am. Chem. Soc. 2009, 131:1452-1459.
63. Remaut H., Rose R.J., Hannan T.J., Hultgren S.J., Radford S.E., Ashcroft A.E., Waksman G. Donor-Strand Exchange in Chaperone-Assisted Pilus Assembly Proceeds Through a Concerted β Strand Displacement Mechanism. Mol. Cell. 2006, 22:831-842.
64. Sharon M., Witt S., Glasmacher E., Baumeister W., Robinson C.V. Mass Spectrometry Reveals the Missing Links in the Assembly Pathway of the Bacterial 20 S Proteasome. J. Biol. Chem. 2007, 282:18448-18457.
65. Levy E.D., Boeri Erba E., Robinson C.V., Teichmann S.A. Assembly Reflects Evolution of Protein Complexes. Nature 2008, 453:1262-1265.
66. Painter A.J., Jaya N., Basha E., Vierling E., Robinson C.V., Benesch J.L. Real-Time Monitoring of Protein Complexes Reveals Their Quaternary Organization and Dynamics. Chem. Biol. 2008, 15:246-253.
67. Sun Y., MacRae T.H. The Small Heat Shock Proteins and Their Role in Human Disease. FEBS J. 2005, 272:2613-2627.
68. Bova M.P., Ding L.L., Horwitz J., Fung B.K. Subunit Exchange of αA-Crystallin. J. Biol. Chem. 1997, 272:29511-29517.
69. van den Oetelaar P.J., van Someren P.F., Thomson J.A., Siezen R.J., Hoenders H.J. A Dynamic Quaternary Structure of Bovine α-Crystallin as Indicated from Intermolecular Exchange of Subunits. Biochemistry 1990, 29:3488-3493.
70. Schneider F., Hammarstrom P., Kelly J.W. Transthyretin Slowly Exchanges Subunits Under Physiologic Conditions: A Convenient Chromatographic Method to Study Subunit Exchange in Oligomeric Proteins. Protein Sci. 2001, 10:1606-1613.
71. Keetch C.A., Bromley E.H., McCammon M.G., Wang N., Christodoulou J., Robinson C.V.L. 55P Transthyretin Accelerates Subunit Exchange and Leads to Rapid Formation of Hybrid Tetramers. J. Biol. Chem. 2005, 280:41667-41674.
72. Back J.W., de Jong L., Muijsers A.O., de Koster C.G. Chemical Cross-Linking and Mass Spectrometry for Protein Structural Modeling. J. Mol. Biol. 2003, 331:303-313.
73. Sinz A. Chemical Cross-Linking and Mass Spectrometry to Map Three-Dimensional Protein Structures and Protein-Protein Interactions. Mass Spectrom. Rev. 2006, 25:663-682.
74. Kolstoe S.E., Ridha B.H., Bellotti V., Wang N., Robinson C.V., Crutch S.J., Keir G., Kukkastenvehmas R., Gallimore J.R., Hutchinson W.L., Hawkins P.N., Wood S.P., Rossor M.N., Pepys M.B. Molecular Dissection of Alzheimer's Disease Neuropathology by Depletion of Serum Amyloid P Component. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:7619-7623.
75. Jensen O.N., Barofsky D.F., Young M.C., von Hippel P.H., Swenson S., Seifried S.E. Direct Observation of UV-Crosslinked Protein-Nucleic Acid Complexes by Matrix-Assisted Laser Desorption Ionization Mass Spectrometry. Rapid Commun. Mass Spectrom. 1993, 7:496-501.
76. Nazabal A., Wenzel R.J., Zenobi R. Immunoassays with Direct Mass Spectrometric Detection. Anal. Chem. 2006, 78:3562-3570.
77. Farmer T.B., Caprioli R.M. Determination of Protein-Protein Interactions by Matrix-Assisted Laser Desorption/Ionization Mass Spectrometry. J. Mass Spectrom. 1998, 33:697-704.
78. Back J.W., Hartog A.F., Dekker H.L., Muijsers A.O., de Koning L.J., de Jong L. A New Crosslinker for Mass Spectrometric Analysis of the Quaternary Structure of Protein Complexes. J. Am. Soc. Mass Spectrom. 2001, 12:222-227.
79. Sinz A. Chemical Cross-Linking and Mass Spectrometry for Mapping Three-Dimensional Structures of Proteins and Protein Complexes. J. Mass Spectrom. 2003, 38:1225-1237.
80. Young M.M., Tang N., Hempel J.C., Oshiro C.M., Taylor E.W., Kuntz I.D., Gibson B.W., Dollinger G. High Throughput Protein Fold Identification by Using Experimental Constraints Derived from Intramolecular Cross-Links and Mass Spectrometry. Proc. Natl. Acad. Sci. U.S.A. 2000, 97:5802-5806.
81. Krauth F., Ihling C.H., Ruttinger H.H., Sinz A. Heterobifunctional Isotope-Labeled Amine-Reactive Photo-Cross-Linker for Structural Investigation of Proteins by Matrix-Assisted Laser Desorption/Ionization Tandem Time-of-Flight and Electrospray Ionization LTQ-Orbitrap Mass Spectrometry. Rapid Commun. Mass Spectrom. 2009, 23:2811-2818.
82. Baca M., Kent S.B.H. Direct Observation of a Ternary Complex Between the Dimeric Enzyme HIV-1 Protease and a Substrate-Based Inhibitor. J. Am. Chem. Soc. 1992, 114:3992.
83. Barrera N.P., Di Bartolo N., Booth P.J., Robinson C.V. Micelles Protect Membrane Complexes from Solution to Vacuum. Science 2008, 321:243-246.
84. Barrera N.P., Isaacson S.C., Zhou M., Bavro V.N., Welch A., Schaedler T.A., Seeger M.A., Miguel R.N., Korkhov V.M., van Veen H.W., Venter H., Walmsley A.R., Tate C.G., Robinson C.V. Mass Spectrometry of Membrane Transporters Reveals Subunit Stoichiometry and Interactions. Nat. Methods 2009, 6:585-587.
85. Lin H.T., Bavro V.N., Barrera N.P., Frankish H.M., Velamakanni S., van Veen H.W., Robinson C.V., Borges-Walmsley M.I., Walmsley A.R. MacB ABC Transporter is a Dimer Whose ATPase Activity and Macrolide-Binding Capacity are Regulated by the Membrane Fusion Protein MacA. J Biol. Chem. 2009, 284:1145-1154.
86. Morgner N., Kleinschroth T., Barth H.D., Ludwig B., Brutschy B. A Novel Approach to Analyze Membrane Proteins by Laser Mass Spectrometry: From Protein Subunits to the Integral Complex. J. Am. Soc. Mass Spectrom. 2007, 18:1429-1438.
87. Hanna J., Finley D. A Proteasome for All Occasions. FEBS Lett. 2007, 581:2854-2861.
88. Hartwell L.H., Hopfield J.J., Leibler S., Murray A.W. From Molecular to Modular Cell Biology. Nature 1999, 402:C47-C52.
89. Alberts B. The Cell as a Collection of Protein Machines: Preparing the Next Generation of Molecular Biologists. Cell 1998, 92:291-294.
90. Glickman M.H., Raveh D. Proteasome Plasticity. FEBS Lett. 2005, 579:3214-3223.
91. Wei N., Serino G., Deng X.W. The COP9 Signalosome: More Than a Protease. Trends Biochem. Sci. 2008, 33:592-600.
92. Gonzalez C.M., Griffey S.M., Naydan D.K., Flores E., Cepeda R., Cattaneo G., Madewell B.R. Canine Transmissible Venereal Tumor: A Morphological and Immunohistochemical Study of 11 Tumors in Growth Phase and During Regression After Chemotherapy. J. Comp. Pathol. 2000, 122:241-248.
93. Kitova E.N., Kitov P.I., Bundle D.R., Klassen J.S. The Observation of Multivalent Complexes of Shiga-Like Toxin with Globotriaoside and the Determination of Their Stoichiometry by Nanoelectrospray Fourier-Transform Ion Cyclotron Resonance Mass Spectrometry. Glycobiology 2001, 11:605-611.
94. Robinson C.V., Chung E.W., Kragelund B.B., Knudsen J., Aplin R.T., Poulsen F.M., Dobson C.M. Probing the Nature of Noncovalent Interactions by Mass Spectrometry. A Study of Protein-CoA Ligand Binding and Assembly. J. Am. Chem. Soc. 1996, 118:8646-8653.
95. Rupp B. High-Throughput Crystallography at an Affordable Cost: The TB Structural Genomics Consortium Crystallization Facility. Acc. Chem. Res. 2003, 36:173-181.
96. Service R.F. Structural Biology. Robots Enter the Race to Analyze Proteins. Science 2001, 292:187-188.