Protein species-specific characterization of conformational change induced by multisite phosphorylation

Journal of Proteomics

Volumn 134, Issue , 2016, Pages 138-143

  Pan, Jingxi ^a   Zhang, Suping ^b   Borchers, Christoph H ^a,c  

^a UNIVERSITY OF VICTORIA   (Canada)

^b MRM Proteomics Inc   (Canada)

^c UNIVERSITY OF VICTORIA   (Canada)

Author keywords

Calmodulin; Electron transfer dissociation; Hydrogen deuterium exchange; Phosphorylation; Post translational modification; Top down

Indexed keywords

CALMODULIN; PHOSPHOPROTEIN; SERINE; THREONINE; RECOMBINANT PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; CONFORMATIONAL TRANSITION; DEUTERIUM HYDROGEN EXCHANGE; DISSOCIATION; ELECTRON TRANSFER DISSOCIATION; ELECTRON TRANSPORT; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CONFORMATION; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE; CHEMISTRY; HUMAN; PHOSPHORYLATION;

CALMODULIN; HUMANS; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTEIN CONFORMATION; RECOMBINANT PROTEINS;

EID: 84958181515     PISSN: 18743919     EISSN: 18767737     Source Type: Journal    
DOI: 10.1016/j.jprot.2015.12.002     Document Type: Article

References (40)

1. Aebersold R., Mann M. Mass spectrometry-based proteomics. Nature 2003, 422:198-207.
2. Cravatt B.F., Simon G.M., Yates J.R. The biological impact of mass-spectrometry-based proteomics. Nature 2007, 450:991-1000.
3. Mann M., Jensen O.N. Proteomic analysis of post-translational modifications. Nat. Biotechnol. 2003, 21:255-261.
4. Krueger K.E., Srivastava S. Posttranslational protein modifications - current implications for cancer detection, prevention, and therapeutics. Mol. Cell. Proteomics 2006, 5:1799-1810.
5. Grimsrud P.A., Swaney D.L., Wenger C.D., Beauchene N.A., Coon J.J. Phosphoproteomics for the masses. ACS Chem. Biol. 2010, 5:105-119.
6. Johnson L.N., Barford D. The effects of phosphorylation on the structure and function of proteins. Annu. Rev. Biophys. Biomol. Struct. 1993, 22:199-232.
7. Han L., Talwar S., Wang Q., Shan Q., Lynch J.W. Phosphorylation of alpha 3 glycine receptors induces a conformational change in the glycine-binding site. ACS Chem. Neurosci. 2013, 4:1361-1370.
8. Yamada T., Bhate M.P., Strange K. Regulatory phosphorylation induces extracellular conformational changes in a CLC anion channel. Biophys. J. 2013, 104:1893-1904.
9. Hsieh L.S., Su W.M., Han G.S., Carman G.M. Phosphorylation regulates the ubiquitin-independent degradation of yeast Pah1 phosphatidate phosphatase by the 20S proteasome. J. Biol. Chem. 2015, 290:11467-11478.
10. Zhai B., Villen J., Beausoleil S.A., Mintseris J., Gygi S.P. Phosphoproteome analysis of drosophila metanogaster embryos. J. Proteome Res. 2008, 7:1675-1682.
11. Wisniewski J.R., Zougman A., Nagaraj N., Mann M. Universal sample preparation method for proteome analysis. Nat. Methods 2009, 6:359-362.
12. Tran J.C., Zamdborg L., Ahlf D.R., Lee J.E., Catherman A.D., Durbin K.R., et al. Mapping intact protein isoforms in discovery mode using top-down proteomics. Nature 2011, 480:254-258.
13. Schlueter H., Apweiler R., Holzhuetter H.-G., Jungblut P.R. Finding one's way in proteomics: a protein species nomenclature. Chem. Cent. J. 2009, 3:11.
14. Jungblut P.R., Schlüter H. Towards the analysis of protein species: an overview about strategies and methods 2011, 41:219-222. (PMID: 21594639).
15. Schlüter H., Jungblut P.R. Special issue on protein species 2011, 41:217-218.
16. Jungblut P.R. Back to the future-the value of single protein species investigations. Proteomics 2014, 13:3103-3105.
17. Jungblut P.R. The proteomics quantification dilemma 2014, 107:98-102.
18. Yee A.A., Savchenko A., Ignachenko A., Lukin J., Xu X.H., Skarina T., et al. NMR and x-ray crystallography, complementary tools in structural proteomics of small proteins. J. Am. Chem. Soc. 2005, 127:16512-16517.
19. Wales T.E., Engen J.R. Hydrogen exchange mass spectrometry for the analysis of protein dynamics. Mass Spectrom. Rev. 2006, 25:158-170.
20. Konermann L., Pan J., Liu Y. Hydrogen exchange mass spectrometry for studying protein structure and dynamics. Chem. Soc. Rev. 2011, 40:1224-1234.
21. Kaltashov I.A., Eyles S.J. Studies of biomolecular conformations and conformational dynamics by mass spectrometry. Mass Spectrom. Rev. 2002, 21:37-71.
22. Pan J., Han J., Borchers C.H., Konermann L. Electron capture dissociation of electrosprayed protein ions for spatially-resolved hydrogen exchange measurements. J. Am. Chem. Soc. 2008, 130:11574-11575.
23. Pan J., Han J., Borchers C.H., Konermann L. Hydrogen/deuterium exchange mass spectrometry with top-down electron capture dissociation for characterizing structural transitions of a 17 kDa protein. J. Am. Chem. Soc. 2009, 131:12801-12808.
24. Wang G., Kaltashov I.A. Approach to characterization of the higher order structure of disulfide-containing proteins using hydrogen/deuterium exchange and top-down mass spectrometry. Anal. Chem. 2014, 86:7293.
25. Wang G.B., Abzalimov R.R., Bobst C.E., Kaltashov I.A. Conformer-specific characterization of nonnative protein states using hydrogen exchange and top-down mass spectrometry. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:20087-20092.
26. Pan J., Zhang S., Parker C.E., Borchers C.H. Subzero temperature chromatography and top-down mass spectrometry for protein higher-order structure characterization: method validation and application to therapeutic antibodies. J. Am. Chem. Soc. 2014, 136:13065-13071.
27. Zehl M., Rand K.D., Jensen O.N., Jørgensen T.J.D. Electron transfer dissociation facilitates the measurement of deuterium incorporation into selectively labeled peptides with single residue resolution. J. Am. Chem. Soc. 2008, 130:17453-17459.
28. Abzalimov R.R., Kaplan D.A., Easterling M.L., Kaltashov I.A. Protein conformations can be probed in top-down HDX MS experiments utilizing electron transfer dissociation of protein ions without hydrogen scrambling. J. Am. Soc. Mass Spectrom. 2009, 20:1514-1517.
29. Sterling H.J., Williams E.R. Real-time hydrogen/deuterium exchange kinetics via supercharged electrospray ionization tandem mass spectrometry. Anal. Chem. 2010, 82:9050-9057.
30. Amon S., Trelle M.B., Jensen O.N., Jørgensen T.J.D. Spatially resolved protein hydrogen exchange measured by subzero-cooled chip-based nanoelectrospray ionization tandem mass spectrometry. Anal. Chem. 2012, 84:4467-4473.
31. Pan J., Zhang S., Chou A., Hardie D.B., Borchers C.H. Fast comparative structural characterization of intact therapeutic antibodies using hydrogen-deuterium exchange and electron transfer dissociation. Anal. Chem. 2015, 87:5884-5890.
32. Pan J., Han J., Borchers C.H., Konermann L. Structure and dynamics of small soluble a beta(1-40) oligomers studied by top-down hydrogen exchange mass spectrometry. Biochemistry 2012, 51:3694-3703.
33. Pan J., Borchers C.H. Top-down structural analysis of posttranslationally modified proteins by Fourier transform ion cyclotron resonance-MS with hydrogen/deuterium exchange and electron capture dissociation. Proteomics 2013, 13:974-981.
34. Drakenberg T., Finn B., Forsen S. Calcium in mammalian cells. Biological Inorganic Chemistry: Structure and Reactivity 2007, 635-646. University Science Books, Sausalito, CA. I. Bertini, H.B. Gray, E.I. Stiefel, J.S. Valentine (Eds.).
35. Park H.Y., Kim S.A., Korlach J., Rhoades E., Kwok L.W., Zipfel W.R., et al. Conformational changes of calmodulin upon Ca2+ binding studied with a microfluidic mixer. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:542-547.
36. Benaim G., Villalobo A. Phosphorylation of calmodulin - functional implications. Eur. J. Biochem. 2002, 269:3619-3631.
37. Quadroni M., James P., Carafoli E. Isolation of phosphorylated calmodulin from rat-liver and identification of the in-vivo phosphorylation sites. J. Biol. Chem. 1994, 269:16116-16122.
38. Quadroni M., L'Hostis E.L., Corti C., Myagkikh I., Durussel I., Cox J., et al. Phosphorylation of calmodulin alters its potency as an activator of target enzymes. Biochemistry 1998, 37:6523-6532.
39. Greif D.M., Sacks D.B., Michel T. Calmodulin phosphorylation and modulation of endothelial nitric oxide synthase catalysis. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:1165-1170.
40. Kuboniwa H., Tjandra N., Grzesiek S., Ren H., Klee C.B., Bax A. Solution structure of calcium-free calmodulin. Nat. Struct. Biol. 1995, 2:768-776.