Characterizationof intrinsically disordered proteins with electrospray inization mass spectrometry: Conformationl heterogeneity of α-synuciein

Proteins: Structure, Function and Bioinformatics

Volumn 78, Issue 3, 2010, Pages 714-722

  Frimpong, Agya K ^a   Abzalimov, Rinat R ^a   Uversky, Vladimir N ^b,c   Kaltashov, Igor A ^a  

^a UNIVERSITY OF MASSACHUSETTS   (United States)

^b INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c INSTITUTE FOR BIOLOGICAL INSTRUMENTATION   (Russian Federation)

Author keywords

Aggregation; Amyloidosis; Charge state distribution; Electrospray ionization; Intrinsic disorder; Mass spectrometry; Protein conformation; synuclein

Indexed keywords

ALPHA SYNUCLEIN; DIMER; GLOBULAR PROTEIN; OLIGOMER; ALCOHOL;

ACIDITY; ANALYTIC METHOD; ARTICLE; BETA SHEET; ELECTROSPRAY MASS SPECTROMETRY; PH; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN STABILITY; PROTEIN STRUCTURE; CHEMISTRY; HUMAN; PROTEIN MULTIMERIZATION;

ALPHA-SYNUCLEIN; ETHANOL; HUMANS; HYDROGEN-ION CONCENTRATION; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION;

EID: 77949885897     PISSN: 08873585     EISSN: 10970134     Source Type: Journal    
DOI: 10.1002/prot.22604     Document Type: Article

References (68)

1. Romero P, Obradovic Z, Kissinger CR, Villafranca JE, Garner E, Guilliot S Dunker AK. Thousands of proteins likely to have long disordered regions. Pac Symp Biocomput 1998;3:437-448.
2. Wright PE Dyson HJ. Intrinsically unstructured proteins: re-assessing the protein structure-function paradigm. J Mol Biol 1999;293:321-331.
3. Uversky VN, Gillespie JR Fink AL. Why are "natively unfolded." proteins unstructured under physiologic conditions? Proteins Struct Func Genet 2000;41:415-427.
4. Tompa P. Intrinsically unstructured proteins. Trends Biochem. Sci 2002;27:527-533.
5. Dyson HJ Wright PE. Intrinsically unstructured proteins and their functions. Nat Rev Mol Cell Biol 2005;6:197-208.
6. Xie H, Vucetic S, Iakoucheva LM, Oldfield CJ, Dunker AK, Uversky VN Obradovic Z. Functional anthology of intrinsic disorder. 1, Biological processes and functions of proteins with long disordered regions. J Proteome Res 2007;6:1882-1898.
7. Uversky VN Dunker AK. Biochemistry: controlled chaos. Science 2008;322:1340-1341,
8. Dunker AK, Oldfield C, Meng J, Romero P, Yang J, Chen J, Vacie V, Obradovic Z Uversky V. The unfoldomics decade: an update on intrinsically disordered proteins. BMC Genomics 2008;9:S1.
9. Bright JN, Woolf TB Hoh JH. Predicting properties of intrinsically unstructured proteins. Progr Biophys Mol Biol 2001;76:131-173.
10. Shortle D. The denatured state (the other half of the folding equation) and its role in protein stability. FASEB J 1996;10:27-34.
11. Smith LJ, Fiebig KM, Schwalbe H, Dobson CM, The concept of a random coil. Residual structure in peptides and denatured proteins. Fold Des 1996;1:R95-R106.
12. Blanco FJ, Serrano L, Forman-Kay JD. High populations of nonnative structures in the denatured state are compatible with the formation of the native folded state. J Mol Biol 1998;284:1153-1164.
13. Hammarstrom P, Carlsson U. Is the unfolded state the Rosetta Stone of the protein folding problem? Biochem Biophys Res Comm 2000;276:393-398.
14. Shortle D. The expanded denatured, state; an ensemble of conformations trapped in a locally encoded topological space. Adv Protein Chem 2002;62:1-23.
15. Eliezer D. Biophysical characterization of intrinsically disordered proteins. Curr Opin Struct Biol 2009;19:23-30.
16. Receveur-Bréchot V, Bourhis, J-M, Uversky VN, Canard B Longhi S. Assessing protein disorder and induced folding. Proteins 2006;62:24-115
17. Kaltashov IA, Eyles SJ. Studies of biomolecuiar conformations and conformational dynamics by mass spectrometry. Mass Spectrom Rev 2002;21:37-71.
18. Konermann L, Douglas DJ. Acid-induced unfolding of cytochrome c at different methanol concentrations: electrospray ionization mass spectrometry specifically monitors changes in the tertiary structure. Biochemistry 1997;36:12296-12302.
19. Kaltashov IA, Abzalimov RR. Do ionic charges in ESI MS provide useful information on macromolecuiar structure? J Am Soc Mass Spectrom 2008;19:1239-1246.
20. Konermann L, Douglas DJ. Equilibrium unfolding of proteins monitored by electrospray ionization mass spectrometry: distinguishing two-state from multi-state transitions. Rapid Commun Mass Spectrom 1998;12:435-442. (Pubitemid 28181283)
21. Grandori R. Detecting equilibrium cytochrome c folding intermediates by electrospray ionisation mass spectrometry: two partially folded forms populate the molten-globule state. Protein Sci 2002; 11:453-458.
22. Borysik AJ, Radford SE, Ashcroft AE. Co-populated conformational ensembles of β2-microglobulin uncovered quantitatively by electrospray ionization mass spectrometry. J Biol Chem 2004;279:27069-27077.
23. Bobst CE, Abzalimov RR, Houde D, Kloczewiak M, Mhatre R, Berkowitz SA, Kaltashov IA. Detection and characterization of altered conformations of protein pharmaceuticals using complementary mass spectrometry-based approaches. Anal Chem 2008;80:7473-7481.
24. Yu X, Wojciechowski M, Fenselau C. Assessment of metals in reconstituted metaliothioneins by electrospray mass spectrometry. Anal Chem 1993;65:1355-1359.
25. Gumerov DR, Kaltashov IA. Dynamics of iron release from transferrin N-lobe studied by electrospray ionization mass spectrometry. Anal Chem 2001;73:2565-2570.
26. van den Bremer ET, Jiskoot W, James R, Moore GR, Kleanthous C, Heck AJ, Maier CS. Probing metal ion binding and conformational properties of the colicin E9 endonuclease by electrospray ionization time-of-flight mass spectrometry. Protein Sci. 2002;11:1738-1752.
27. Low LY, Hernandez H, Robinson CV, O'Brien. R, Grossmann JG, Ladbury JE, Luisi B. Metal-dependent folding and stability of nuclear hormone receptor DNA-binding domains. J Mol Biol 2002;319:87-106.
28. Griffith WP, Kaltashov IA. Highly asymmetric interactions between globin chains during hemoglobin assembly revealed by electrospray ionization mass spectrometry. Biochemistry 2003;42: 10024-10033.
29. Simmons DA, Wilson DJ, Lajoie GA, Doherty-Kirby A, Konermann L. Subunit disassembly and unfolding kinetics of hemoglobin studied by time-resolved electrospray mass spectrometry. Biochemistry 2004;43:14792-14801.
30. Griffith WP, Kaltashov IA. Protein conformational heterogeneity as a binding catalyst: ESI-MS study of hemoglobin. H formation. Biochemistry 2007;46:2020-2026.
31. Kamadurai HB, Subramaniam S, Jones RB, Green-Church KB, Foster MP. Protein folding coupled to DNA binding in the catalytic domain of bacteriophage lambda integrase detected by mass spectrometry. Protein Sci 2003;12:620-626.
32. Abzalimov RR, Dubin PL, Kaltashov IA. Glycosaminoglycans as naturally occurring combinatorial libraries: developing a mass spectrometry-based strategy for characterization of anti-thrombin interaction with low molecular weight heparin and heparin oligomers. Anal Chem. 2007;79:6055-6063.
33. Lundvig D, Lindersson E, Jensen PH. Pathogenic effects of a-synuclein aggregation. Mol Brain Res 2005;134:3-17.
34. Bennett MC. The role of α-synuclein in neurodegenerative diseases. Pharmacol Ther 2005;105:311-331.
35. Cookson MR. The biochemistry of Parkinson's disease. Annu Rev Biochem 2005;74:29-52.
36. Moore DJ, West AB, Dawson VL, Dawson TM. Molecular pathophysiology of Parkinson's disease. Annu Rev Neurosci 2005;28:57-87.
37. Bonini NM, Giasson BI. Snaring the function of α-synuclein. Cell. 2005;123:359-361.
38. Uversky VN. A protein-chameleon: conformational plasticity of αsynuclein, a disordered protein involved in neurodegenerative disorders. J Biomol Struct Dyn 2003;21:211-234.
39. Uversky VN, Yamin G, Souiliac PO, Goers J, Glaser CB, Fink AL. Methionine oxidation inhibits fibrillation of human a-synuclein in vitro. FEBS Lett 2002;517:239-244.
40. Mohimen A, Dobo A, Hoerner JK, Kaltashov IA. A chemometric approach to detection and characterization of multiple protein conformers in solution using electrospray ionization mass spectrometry. Anal Chem 2003;75:4139-4147.
41. Konermann L. A minimalist model for exploring conformational effects on the electrospray charge state distribution of proteins. J Phys Chem B 2007;111:6534-6543.
42. Kaltashov IA, Mohimen A, Estimates of protein surface areas in solution by electrospray ionization mass spectrometry. Anal Chem 2005;77:5370-5379.
43. Felitsyn N, Kitova EN, Klassen JS. Thermal dissociation of the protein homodimer ecotin in the gas phase. J Am Soc Mass Spectrom 2002;13:1432-1442.
44. Abzalimov RR, Frimpong AK, Kaltashov IA, Gas-phase processes and measurements of macromolecuiar properties in solution: on the possibility of false positive and false negative signals of protein unfolding. Int. J Mass Spectrom 2006;253:207-216.
45. Le Gall T, Romero PR, Cortese MS, Uversky VN, Dunker AK. Intrinsic disorder in the Protein Data Bank. J Biomol Struct Dyn 2007;24:325-342.
46. Koo EH, Lansbury PT, Jr, Kelly JW. Amyloid diseases: abnormal protein aggregation in neurodegeneration. Proc Natl Acad Sci U S A 1999;96:9989-9990.
47. Thompson AJ, Barrow CJ. Protein conformational misfolding and amyloid formation: characteristics of a new class of disorders that include Alzheimer's and Prion diseases. Curr Med Chem. 2002;9:1751-1762.
48. Dobson CM. Protein aggregation and its consequences for human disease. Protein Pept Lett 2006;13:219-227.
49. Uversky VN, Oldfield. CJ, Dunker AK, Intrinsically disordered proteins in human diseases: introducing the D2 concept. Ann Rev Biophys 2008;37:215-246.
50. Johnson WG. Late-onset neurodegenerative diseases-the role of protein insolubility. J Anat 2000;196:609-616.
51. Trojanowski JQ, Lee VM-Y. Parkinson's disease and related synucleinopathies are a new class of nervous system amyloidoses. Neuro Toxicol. 2002;23:457-460.
52. Lee JC, Lai BT, Kozak JJ, Gray HB, Winkler JR. α-Synuclein tertiary contact dynamics. J Phys Chem B 2007;111:2107-2112.
53. Ly T, Julian RR. Protein-metal interactions of calmodulin and asynuclein monitored by selective noncovalent adduct protein probing mass spectrometry. J Am Soc Mass Spectrom 2008;19:1663-1672.
54. Ulmer TS, Bax A, Cole NB, Nussbaum RL. Structure and dynamics of micelle-bound human a-synuclein. J Biol Chem 2005;280:9595-9603.
55. Ferreon ACM, Deniz AA. α-Synuclein multistate folding thermodynamics: implications for protein misfolding and aggregation. Biochemistry 2007;46:4499-4509.
56. Kuprowski MC, Konermann. L. Signal, response of coexisting protein conformers in electrospray mass spectrometry. Anal Chem 2007;79:2499-2506.
57. Dobo A, Kaltashov IA. Detection of multiple protein conformational ensembles in solution via deconvolution of charge state distributions in ESI MS. Anal Chem. 2001;73:4763-4773.
58. Frimpong AK, Abzalimov RR, Eyles SJ, Kaltashov IA. Gas-phase interference-free analysis of protein ion charge-state distributions: detection of small-scale conformational transitions accompanying pepsin inactivation. Anal Chem 2007;79:4154-4161.
59. Grabenauer M, Bernstein SL, Lee JC, Wyttenbach T, Dupuis NF, Gray HB, Winkler JR, Bowers MT, Spermine binding to Parkinson's protein a-synuclein and its disease-related A30P and A53T mutants. J Phys Chem. B 2008;112:11147-11154.
60. Bernstein SL, Liu D, Wyttenbach T, Bowers MT, Lee JC, Gray HB, Winkler JR. α-Synuclein: stable compact and extended monomeric structures and pH dependence of dimer formation. J Am Soc Mass Spectrom 2004;15:1435-1443.
61. Sharon M, Robinson CV. The role of mass spectrometry in structure elucidation of dynamic protein complexes. Annu Rev Biochem 2007;76:167-193.
62. Maiti NC, Apetri MM, Zagorski MG, Carey PR, Anderson VE. Raman spectroscopic characterization of secondary structure in natively unfolded proteins: α-synuclein. J Am Chem Soc 2004;126:2399-2408.
63. Del Mar C, Greenbaum EA, Mayne L, Englander SW, Woods VL, Jr. Structure and properties of α-synuclein and other amyloids determined, at the amino acid level. Proc Natl Acad Sei U S A. 2005;102:15477-15482.
64. Jurchen JC, Garcia DE, Williams ER. Further studies on the origins of asymmetric charge partitioning in protein homodimers. J Am Soc Mass Spectrom 2004;15:1408-1415.
65. Fink AL. The aggregation and fibrillation of α-synuclein. Ace Chem Res 2006;39:628-634.
66. Apetri. MM, Maiti NC, Zagorski MG, Carey PR, Anderson VE. Secondary structure of α-synuclein oligomers: characterization by Raman and atomic force microscopy. J Mol Biol 2006;355:63-71.
67. Dusa A, Kaylor J, Edridge S, Bodner N, Hong, D-P, Fink AL. Characterization of oligomers during α-synuclein aggregation using intrinsic tryptophan fluorescence. Biochemistry 2006;45:2752-2760.
68. Heck AJR. Native mass spectrometry: a bridge between interactomics and structural biology. Nat Meth 2008;5:927-933.