Defining the Interacting Regions between Apomyoglobin and Lipid Membrane by Hydrogen/Deuterium Exchange Coupled to Mass Spectrometry

Journal of Molecular Biology

Volumn 368, Issue 2, 2007, Pages 464-472

  Man, Petr ^a   Montagner, Caroline ^b   Vernier, Grégory ^b   Dublet, Bernard ^a   Chenal, Alexandre ^b   Forest, Eric ^a   Forge, Vincent ^b  

^a INSTITUT DE BIOLOGIE STRUCTURALE   (France)

^b CEA GRENOBLE   (France)

Author keywords

amphitropic proteins; apomyoglobin; H D exchange; mass spectrometry; protein membrane interactions

Indexed keywords

APOMYOGLOBIN; BACTERIAL TOXIN; DEUTERIUM; HYDROGEN;

ALPHA HELIX; ARTICLE; CHANNEL GATING; DEUTERIUM HYDROGEN EXCHANGE; FEASIBILITY STUDY; HYDROPHOBICITY; LIPID BILAYER; LIPID MEMBRANE; MASS SPECTROMETRY; MOLECULE; PH; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN INTERACTION; PROTEIN STABILITY;

BACTERIA (MICROORGANISMS); PHYSETERIDAE;

EID: 33947599164     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2007.02.014     Document Type: Article

References (40)

1. Johnson J.E., and Cornell R.B. Amphitropic proteins: regulation by reversible membrane interactions. Mol. Membr. Biol. 16 (1999) 217-235
2. Holm L., and Sander C. Globin fold in a bacterial toxin. Nature 361 (1993) 309
3. Parker M.W., and Feil S.C. Pore-forming protein toxins: from structure to function. Prog. Biophys. Mol. Biol. 88 (2005) 91-142
4. Choe S., Bennett M.J., Fujii G., Curmi P.M., Kantardjieff K.A., Collier R.J., and Eisenberg D. The crystal structure of diphtheria toxin. Nature 357 (1992) 216-222
5. Bennett M.J., Choe S., and Eisenberg D. Refined structure of dimeric diphtheria toxin at 2.0 Å resolution. Protein Sci. 3 (1994) 1444-1463
6. Parker M.W., Pattus F., Tucker A.D., and Tsernoglou D. Structure of the membrane-pore-forming fragment of colicin A. Nature 337 (1989) 93-96
7. Fesik S.W. Insights into programmed cell death through structural biology. Cell 103 (2000) 273-282
8. Tsujimoto Y. Bcl-2 family of proteins: life-or-death switch in mitochondria. Biosci. Rep. 22 (2002) 47-58
9. Thuduppathy G.R., Craig J.W., Kholodenko V., Schon A., and Hill R.B. Evidence that membrane insertion of the cytosolic domain of Bcl-xL is governed by an electrostatic mechanism. J. Mol. Biol. 359 (2006) 1045-1058
10. Chenal A., Savarin P., Nizard P., Guillain F., Gillet D., and Forge V. Membrane protein insertion regulated by bringing electrostatic and hydrophobic interactions into play. A case study with the translocation domain of diphtheria toxin. J. Biol. Chem. 277 (2002) 43425-43432
11. Petros A.M., Olejniczak E.T., and Fesik S.W. Structural biology of the Bcl-2 family of proteins. Biochim. Biophys. Acta 1644 (2004) 83-94
12. van der Goot F.G., Gonzalez-Manas J.M., Lakey J.H., and Pattus F. A 'molten-globule' membrane-insertion intermediate of the pore-forming domain of colicin A. Nature 354 (1991) 408-410
13. Griko Y.V., Privalov P.L., Venyaminov S.Y., and Kutyshenko V.P. Thermodynamic study of the apomyoglobin structure. J. Mol. Biol. 202 (1988) 127-138
14. Hughson F.M., Wright P.E., and Baldwin R.L. Structural characterization of a partly folded apomyoglobin intermediate. Science 249 (1990) 1544-1548
15. Barrick D., and Baldwin R.L. Three-state analysis of sperm whale apomyoglobin folding. Biochemistry 32 (1993) 3790-3796
16. Kataoka M., Nishii I., Fujisawa T., Ueki T., Tokunaga F., and Goto Y. Structural characterization of the molten globule and native states of apomyoglobin by solution X-ray scattering. J. Mol. Biol. 249 (1995) 215-228
17. Gulotta M., Rogatsky E., Callender R.H., and Dyer R.B. Primary folding dynamics of sperm whale apomyoglobin: core formation. Biophys. J. 84 (2003) 1909-1918
18. Jamin M. The folding process of apomyoglobin. Protein Pept. Letters 3 (2005) 229-234
19. Nishimura C., Dyson H.J., and Wright P.E. Identification of native and non-native structure in kinetic folding intermediates of apomyoglobin. J. Mol. Biol. 355 (2006) 139-156
20. Eliezer D., Chung J., Dyson H.J., and Wright P.E. Native and non-native secondary structure and dynamics in the pH 4 intermediate of apomyoglobin. Biochemistry 39 (2000) 2894-2901
21. Bertagna A.M., and Barrick D. Nonspecific hydrophobic interactions stabilize an equilibrium intermediate of apomyoglobin at a key position within the electrodes AGH region. Proc. Natl Acad. Sci. USA 101 (2004) 12514-12519
22. Basova L.V., Tiktopulo E.I., Kashparov I.A., and Bychkova V.E. Conformational state of apomyoglobin in the presence of phospholipid vesicles at neutral pH. Mol. Biol. (Mosk) 38 (2004) 323-332
23. Lee J.W., and Kim H. Fragmentation of dimyristoylphosphatidylcholine vesicles by apomyoglobin. Arch. Biochem. Biophys. 297 (1992) 354-361
24. Vernier, G., Chenal, A., Vitrac, H., Barumandzadhe, R., Montagner, C. & Forge, V. (2007). Interactions of apomyoglobin with membranes: mechanisms and effects on the heme uptake. Protein Sci. In the press.
25. Redfield C. Using nuclear magnetic resonance spectroscopy to study molten globule states of proteins. Methods 34 (2004) 121-132
26. Eyles S.J., and Kaltashov I.A. Methods to study protein dynamics and folding by mass spectrometry. Methods 34 (2004) 88-99
27. Krishna M.M., Hoang L., Lin Y., and Englander S.W. Hydrogen exchange methods to study protein folding. Methods 34 (2004) 51-64
28. Miranker A., Robinson C.V., Radford S.E., and Dobson C.M. Investigation of protein folding by mass spectrometry. FASEB J. 10 (1996) 93-101
29. Dyson H.J., and Wright P.E. Equilibrium NMR studies of unfolded and partially folded proteins. Nature Struct. Biol. 5 (1998) 499-503
30. Konermann L., and Simmons D.A. Protein-folding kinetics and mechanisms studied by pulse-labeling and mass spectrometry. Mass Spectrom Rev. 22 (2003) 1-26
31. Chenal A., Vernier G., Savarin P., Bushmarina N.A., Geze A., Guillain F., et al. Conformational states and thermodynamics of alpha-lactalbumin bound to membranes: a case study of the effects of pH, calcium, lipid membrane curvature and charge. J. Mol. Biol. 349 (2005) 890-905
32. Pinheiro T.J., Cheng H., Seeholzer S.H., and Roder H. Direct evidence for the cooperative unfolding of cytochrome c in lipid membranes from H-(2)H exchange kinetics. J. Mol. Biol. 303 (2000) 617-626
33. Halskau O., Froystein N.A., Muga A., and Martinez A. The membrane-bound conformation of α-lactalbumin studied by NMR-monitored 1H exchange. J. Mol. Biol. 321 (2002) 99-110
34. Cravello L., Lascoux D., and Forest E. Use of different proteases working in acidic conditions to improve sequence coverage and resolution in hydrogen/deuterium exchange of large proteins. Rapid Commun. Mass Spectrom. 17 (2003) 2387-2393
35. Brier S., Lemaire D., DeBonis S., Kozielski F., and Forest E. Use of hydrogen/deuterium exchange mass spectrometry and mutagenesis as a tool to identify the binding region of inhibitors targeting the human mitotic kinesin Eg5. Rapid Commun. Mass Spectrom. 20 (2006) 456-462
36. Mandell J.G., Falick A.M., and Komives E.A. Identification of protein-protein interfaces by decreased amide proton solvent accessibility. Proc. Natl Acad. Sci. USA 95 (1998) 14705-14710
37. Wang L., Lane L.C., and Smith D.L. Detecting structural changes in viral capsids by hydrogen exchange and mass spectrometry. Protein Sci. 10 (2001) 1234-1243
38. Bai Y., Milne J.S., Mayne L., and Englander S.W. Primary structure effects on peptide group hydrogen exchange. Proteins: Struct. Funct. Genet. 17 (1993) 75-86
39. Weisbuch S., Gerard F., Pasdeloup M., Cappadoro J., Dupont Y., and Jamin M. Cooperative sub-millisecond folding kinetics of apomyoglobin pH 4 intermediate. Biochemistry 18 (2005) 7013-7023
40. Glasoe P.K., and Long F.A. Use of glass electrodes to measure acidities in deuterium oxide. J. Phys. Chem. 64 (1960) 188-189