Gas-phase structure of amyloid-β (12 - 28) peptide investigated by infrared spectroscopy, electron capture dissociation and ion mobility mass spectrometry

Journal of the American Society for Mass Spectrometry

Volumn 24, Issue 12, 2013, Pages 1937-1949

  Le, Thi Nga ^a   Poully, Jean Christophe ^a,d   Lecomte, Frédéric ^a   Nieuwjaer, Nicolas ^a   Manil, Bruno ^a   Desfrançois, Charles ^a   Chirot, Fabien ^b   Lemoine, Jerome ^b   Dugourd, Philippe ^b   Van Der Rest, Guillaume ^c   Grégoire, Gilles ^a  

^a UNIVERSITÉ PARIS 13   (France)

^b UNIVERSITÉ LYON 1   (France)

^c UNIVERSITÉ PARIS SUD   (France)

^d UNIVERSITÉ DE CAEN   (France)

Author keywords

Amyloid peptide; ECD; Gas phase structure; Ion Mobility; IRMPD

Indexed keywords

AMYLOID PEPTIDES; ECD; GAS-PHASE STRUCTURES; ION MOBILITY; IRMPD;

DISSOCIATION; EXPERIMENTS; GLYCOPROTEINS; INFRARED SPECTROSCOPY; MASS SPECTROMETRY; MOLECULAR DYNAMICS; PHASE STRUCTURE; PROTONATION;

PEPTIDES;

AMYLOID BETA PROTEIN; AMYLOID BETA PROTEIN[12-28]; CARBONYL DERIVATIVE; OXYGEN; UNCLASSIFIED DRUG;

ARTICLE; CHEMICAL BOND; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; ELECTRON CAPTURE DISSOCIATION MASS SPECTROMETRY; GAS PHASE STRUCTURE; INFRARED MULTIPHOTON DISSOCIATION SPECTROSCOPY; ION MOBILITY MASS SPECTROMETRY; MASS SPECTROMETRY; MOLECULAR DYNAMICS; PHYSICAL PARAMETERS; PHYSICAL PHASE; PRODUCT ION ABUNDANCE; PROTEIN CONFORMATION; PROTEIN MOTIF; PROTEIN SECONDARY STRUCTURE; PROTEIN STRUCTURE; PROTON TRANSPORT; QUANTUM MECHANICS; SPECTROSCOPY; STRUCTURE ANALYSIS; THEORETICAL MODEL;

AMYLOID BETA-PEPTIDES; HUMANS; IONS; MASS SPECTROMETRY; MODELS, MOLECULAR; PEPTIDE FRAGMENTS; PROTEIN STRUCTURE, SECONDARY; PROTONS; SPECTROPHOTOMETRY, INFRARED;

EID: 84890481109     PISSN: 10440305     EISSN: 18791123     Source Type: Journal    
DOI: 10.1007/s13361-013-0722-x     Document Type: Article

References (70)

1. Roychaudhuri, R.; Yang, M.; Hoshi, M.M.; Teplow, D.B.: Amyloid β-protein assembly and alzheimer disease. J. Biol. Chem. 284, 4749-4753 (2009)
2. Dyson, H.J.; Rance, M.; Houghten, R.A.; Wright, P.E.; Lerner, R.A.: Folding of immunogenic peptide-fragments of proteins in water solution. 2. The nascent helix. J. Mol. Biol 201, 201-217 (1988)
3. Roccatano, D.; Colombo, G.; Fioroni, M.; Mark, A.E.: Mechanism by which 2,2,2-trifluoroethanol/water mixtures stabilize secondary-structure formation in peptides: a molecular dynamics study. Proc. Natl. Acad. Sci. USA 99, 12179-12184 (2002)
4. Hou, L.M.; Shao, H.Y.; Zhang, Y.B.; Li, H.; Menon, N.K.; Neuhaus, E.B.; Brewer, J.M.; Byeon, I.J.L.; Ray, D.G.; Vitek, M.P.; Iwashita, T.; Makula, R.A.; Przybyla, A.B.; Zagorski, M.G.: Solution NMR studies of the A β(1-40) and A β(1-42) peptides establish that the met35 oxidation state affects the mechanism of amyloid formation. J. Am. Chem. Soc. 126, 1992-2005 (2004)
5. Barrow, C.J.; Zagorski, M.G.: Solution structures of Β peptide and its constituent fragments - relation to amyloid deposition. Science 253, 179-182 (1991)
6. Barrow, C.J.; Yasuda, A.; Kenny, P.T.M.; Zagorski, M.G.: Solution conformations and aggregational properties of synthetic amyloid β-peptides of Alzheimer's disease - analysis of circular-dichroism spectra. J. Mol. Biol. 225, 1075-1093 (1992)
7. Fraser, P.E.; Levesque, L.; McLachlan, D.R.: Alzheimer a-Β amyloid forms an inhibitory neuronal substrate. J. Neurochem. 62, 1227-1230 (1994)
8. Jarvet, J.; Damberg, P.; Bodell, K.; Eriksson, L.E.G.; Graslund, A.: Reversible random coil to β-sheet transition and the early stage of aggregation of the Aβ(12-28) fragment from the Alzheimer peptide. J. Am. Chem. Soc. 122, 4261-4268 (2000)
9. Danielsson, J.; Jarvet, J.; Damberg, P.; Graslund, A.: The Alzheimer β-peptide shows temperature-dependent transitions between left-handed 3(1)-helix, β-strand and random coil secondary structures. FEBS J. 272, 3938-3949 (2005)
10. Daidone, I.; Simona, F.; Roccatano, D.; Broglia, R.A.; Tiana, G.; Colombo, G.; Di Nola, A.: β-hairpin conformation of fibrillogenic peptides: Structure and α-β transition mechanism revealed by molecular dynamics simulations. Prot. Struct. Funct Bioinformatics 57, 198-204 (2004)
11. Simona, F.; Tiana, G.; Broglia, R.A.; Colombo, G.: Modeling the α-helix to β-hairpin transition mechanism and the formation of oligomeric aggregates of the fibrillogenic peptide A β(12-28): insights from all-atom molecular dynamics simulations. J. Mol. Graphics Modeling 23, 263-273 (2004)
12. Baumketner, A.; Shea, J.E.: Folding landscapes of the Alzheimer amyloid-β (12-28) peptide. J. Mol. Biol. 362, 567-579 (2006)
13. Ma, K.; Clancy, E.L.; Zhang, Y.B.; Ray, D.G.; Wollenberg, K.; Zagorski, M.G.: Residue-specific pK(a) measurements of the β-peptide and mechanism of pH-induced amyloid formation. J. Am. Chem. Soc. 121, 8698-8706 (1999)
14. Fraser, P.E.; Nguyen, J.T.; Surewicz, W.K.; Kirschner, D.A.: Ph-dependent structural transitions of Alzheimer amyloid peptides. Biophys. J. 60, 1190-1201 (1991)
15. Bernstein, S.L.; Wyttenbach, T.; Baumketner, A.; Shea, J.E.; Bitan, G.; Teplow, D.B.; Bowers, M.T.: Amyloid β-protein: monomer structure and early aggregation states of Amyloid-β 42 and its Pro(19) alloform. J. Am. Chem. Soc. 127, 2075-2084 (2005)
16. Teplow, D.B.; Lazo, N.D.; Bitan, G.; Bernstein, S.; Wyttenbach, T.; Bowers, M.T.; Baumketner, A.; Shea, J.E.; Urbanc, B.; Cruz, L.; Borreguero, J.; Stanley, H.E.: Elucidating amyloid β-protein folding and assembly: a multidisciplinary approach. Acc. Chem. Res. 39, 635-645 (2006)
17. Bernstein, S.L.; Dupuis, N.F.; Lazo, N.D.; Wyttenbach, T.; Condron, M.M.; Bitan, G.; Teplow, D.B.; Shea, J.E.; Ruotolo, B.T.; Robinson, C.V.; Bowers, M.T.: Amyloid-β protein oligomerization and the importance of tetramers and dodecamers in the etiology of Alzheimer's disease. Nat. Chem. 1, 326-331 (2009)
18. Drayss, M.K.; Blunk, D.; Oomens, J.; Polfer, N.; Schmuck, C.; Gao, B.; Wyttenbach, T.; Bowers, M.T.; Schafer, M.: Gas-phase structures of solution-phase zwitterions: charge solvation or salt bridge? Int. J. Mass Spectrom. 281, 97-100 (2009)
19. Joly, L.; Antoine, R.; Albrieux, F.; Ballivian, R.; Broyer, M.; Chirot, F.; Lemoine, J.; Dugourd, P.; Greco, C.; Mitric, R.; Bonacic-Koutecky, V.: Optical and structural properties of copper-oxytocin dications in the gas phase. J Phys Chem B 113, 11293-11300 (2009)
20. Poully, J.C.; Lecomte, F.; Nieuwjaer, N.; Manil, B.; Schermann, J.P.; Desfrancois, C.; Gregoire, G.; Ballivian, R.; Chirot, F.; Lemoine, J.; Calvo, F.; Antoine, R.; Dugourd, P.: Combining ion mobility mass spectrometry and infrared multiphoton dissociation spectroscopy to probe the structure of gas-phase vancomycin-Ac(2)(L)K(D)A(D)A non-covalent complex. Int. J. Mass Spectrom. 297, 28-35 (2010)
21. Poully, J.C.; Gregoire, G.; Ballivian, R.; Dugourd, P.; Schermann, J.P.: Coupling infrared multiphoton dissociation spectroscopy, mass-spectrometry and ion mobility spectrometry for the determination of structures of angiotensin II cations. Vibrational Spectrosc. 56, 105-109 (2011)
22. Papadopoulos, G.; Svendsen, A.; Boyarkin, O.V.; Rizzo, T.R.: Spectroscopy of mobility-selected biomolecular ions. Faraday Discuss. 150, 243-255 (2011)
23. Papadopoulos, G.; Svendsen, A.; Boyarkin, O.V.; Rizzo, T.R.: Conformational distribution of bradykinin bk + 2 H (2+) revealed by cold ion spectroscopy coupled with FAIMS. J. Am. Soc. Mass Spectrom. 23, 1173-1181 (2012)
24. Oomens, J.; Sartakov, B.G.; Meijer, G.; von Helden, G.: Gas-phase infrared multiple photon dissociation spectroscopy of mass-selected molecular ions. Int. J. Mass Spectrom. 254, 1-19 (2006)
25. Gregoire, G.; Gaigeot, M.P.; Marinica, D.C.; Lemaire, J.; Schermann, J.P.; Desfrançois, C.: Resonant infrared multiphoton dissociation spectroscopy of gas-phase protonated peptides. Experiments and Car-Parrinello dynamis at 300 K. Phys. Chem.; Chem. Phys. 9, 3082-3097 (2007)
26. Eyler, J.R.: Infrared multiple photon dissociation spectroscopy of ions in penning traps. Mass Spectrom. Rev. 28, 448-467 (2009)
27. Polfer, N.C.; Oomens, J.: Vibrational spectroscopy of bare and solvated ionic complexes of biological relevance. Mass Spectrom. Rev. 28, 468-494 (2009)
28. Vaden, T.D.; Gowers, S.A.N.; de Boer, T.; Steill, J.D.; Oomens, J.; Snoek, L.C.: Conformational preferences of an amyloidogenic peptide: IR spectroscopy of Ac-VQIVYK-NHMe. J. Am. Chem. Soc. 130, 14640-14650 (2008)
29. Gabelica, V.; Rosu, F.; De Pauw, E.; Lemaire, J.; Gillet, J.C.; Poully, J.C.; Lecomte, F.; Gregoire, G.; Schermann, J.P.; Desfrancois, C.: Infrared signature of DNA G-quadruplexes in the gas phase. J. Am. Chem. Soc. 130, 1810-1811 (2008)
30. Rosu, F.; Gabelica, V.; Joly, L.; Gregoire, G.; De Pauw, E.: Zwitterionic i-motif structures are preserved in DNA negatively charged ions produced by electrospray mass spectrometry. Phys. Chem.; Chem. Phys. 12, 13448-13454 (2010)
31. Oomens, J.; Polfer, N.; Moore, D.T.; van der Meer, L.; Marshall, A.G.; Eyler, J.R.; Meijer, G.; von Helden, G.: Charge-state resolved mid-infrared spectroscopy of a gas-phase protein. Phys. Chem. Chem. Phys. 7, 1345-1348 (2005)
32. Poully, J.C.; Lecomte, F.; Nieuwjaer, N.; Manil, B.; Schermann, J.P.; Desfrancois, C.; Calvo, F.; Gregoire, G.: Probing the specific interactions and structures of gas-phase vancomycin antibiotics with cell-wall precursor through IRMPD spectroscopy. Phys. Chem. Chem. Phys. 12, 3606-3615 (2010)
33. Breuker, K.; Oh, H.B.; Horn, D.M.; Cerda, B.A.; McLafferty, F.W.: Detailed unfolding and folding of gaseous ubiquitin ions characterized by electron capture dissociation. J. Am. Chem. Soc. 124, 6407-6420 (2002)
34. Budnik, B.A.; Nielsen, M.L.; Olsen, J.V.; Haselmann, K.F.; Horth, P.; Haehnel, W.; Zubarev, R.A.: Can relative cleavage frequencies in peptides provide additional sequence information? Int. J. Mass Spectrom. 219, 283-294 (2002)
35. Leymarie, N.; Costello, C.E.; O'Connor, P.B.: Electron capture dissociation initiates a free radical reaction cascade. J. Am. Chem. Soc. 125, 8949-8958 (2003)
36. Breuker, K.; Oh, H.B.; Lin, C.; Carpenter, B.K.; McLafferty, F.W.: Nonergodic and conformational control of the electron capture dissociation of protein cations. Proc. Natl. Acad. Sci. USA 101, 14011-14016 (2004)
37. Polfer, N.C.; Haselmann, K.F.; Langridge-Smith, P.R.R.; Barran, P.E.: Structural investigation of naturally occurring peptides by electron capture dissociation and AMBER force field modelling. Mol. Phys. 103, 1481-1489 (2005)
38. O'Connor, P.B.; Lin, C.; Cournoyer, J.J.; Pittman, J.L.; Belyayev, M.; Budnik, B.A.: Long-lived electron capture dissociation product ions experience radical migration via hydrogen abstraction. J. Am. Soc. Mass Spectrom. 17, 576-585 (2006)
39. Ben-Hamidane, H.; He, H.; Tsybin, O.Y.; Emmett, M.R.; Hendrickson, C.L.; Marshall, A.G.; Tsybin, Y.O.: Periodic sequence distribution of product ion abundances in electron capture dissociation of amphipathic peptides and proteins. J. Am. Soc. Mass Spectrom. 20, 1182-1192 (2009)
40. Haag, N.; Holm, A.I.S.; Johansson, H.A.B.; Zettergren, H.; Schmidt, H.T.; Nielsen, S.B.; Hvelplund, P.; Cederquist, H.: Electron capture induced dissociation of doubly protonated pentapeptides: dependence on molecular structure and charge separation. J. Chem. Phys. 134, 035102 (2011)
41. Turecek, F.: N-C-α bond dissociation energies and kinetics in amide and peptide radicals. Is the dissociation a nonergodic process? J. Am. Chem. Soc. 125, 5954-5963 (2003)
42. Zubarev, R.A.; Haselmann, K.F.; Budnik, B.; Kjeldsen, F.; Jensen, F.: Towards an understanding of the mechanism of electron-capture dissociation: a historical perspective and modern ideas. Eur. J. Mass Spectrom. 8, 337-349 (2002)
43. Cooper, H.J.; Hudgins, R.R.; Hakansson, K.; Marshall, A.G.: Characterization of amino acid side chain losses in electron capture dissociation. J. Am. Soc. Mass Spectrom. 13, 241-249 (2002)
44. Turecek, F.; Syrstad, E.A.: Mechanism and energetics of intramolecular hydrogen transfer in amide and peptide radicals and cation-radicals. J. Am. Chem. Soc. 125, 3353-3369 (2003)
45. Chamot-Rooke, J.; Malosse, C.; Frison, G.; Turecek, F.: Electron capture in charge-tagged peptides. Evidence for the role of excited electronic states. J. Am. Soc. Mass Spectrom. 18, 2146-2161 (2007)
46. Holm, A.I.S.; Larsen, M.K.; Panja, S.; Hvelplund, P.; Nielsen, S.B.; Leib, R.D.; Donald, W.A.; Williams, E.R.; Hao, C.T.; Turecek, F.: Electron capture, femtosecond electron transfer and theory: a study of noncovalent crown ether 1, n-diammonium alkane complexes. Int. J. Mass Spectrom. 276, 116-126 (2008)
47. Simons, J.: Mechanisms for S-S and N-C-α bond cleavage in peptide ECD and ETD mass spectrometry. Chem. Phys. Lett. 484, 81-95 (2010)
48. Sobczyk, M.; Anusiewicz, W.; Berdys-Kochanska, J.; Sawicka, A.; Skurski, P.; Simons, J.: Coulomb-assisted dissociative electron attachment: application to a model peptide. J. Phys. Chem. A 109, 250-258 (2005)
49. Neff, D.; Smuczynska, S.; Simons, J.: Electron shuttling in electron transfer dissociation. Int. J. Mass Spectrom. 283, 122-134 (2009)
50. Mac Aleese, L.; Simon, A.; McMahon, T.B.; Ortega, J.M.; Scuderi, D.; Lemaire, J.; Maitre, P.: Mid-IR spectroscopy of protonated leucine methyl ester performed with an FTICR or a Paul type ion-trap. Int. J. Mass Spectrom. 249, 14-20 (2006)
51. Albrieux, F.; Calvo, F.; Chirot, F.; Vorobyev, A.; Tsybin, Y.O.; Lepere, V.; Antoine, R.; Lemoine, J.; Dugourd, P.: Conformation of polyalanine and polyglycine dications in the gas phase: insight from ion mobility spectrometry and replica-exchange molecular dynamics. J. Phys. Chem. A 114, 6888-6896 (2010)
52. Caravatti, P.; Allemann, M.: The infinity cell - a new trapped-ion cell with radiofrequency covered trapping electrodes for Fourier-transform ion-cyclotron resonance mass-spectrometry. Org. Mass Spectrom. 26, 514-518 (1991)
53. Pearlman, D.A.; Case, D.A.; Caldwell, J.W.; Ross, W.S.; Cheatham, T.E.; Debolt, S.; Ferguson, D.; Seibel, G.; Kollman, P.: Amber, a package of computer-programs for applying molecular mechanics, normal-mode analysis, molecular-dynamics and free-energy calculations to simulate the structural and energetic properties of molecules. Computer Phys. Commun. 91, 1-41 (1995)
54. Sugita, Y.; Okamoto, Y.: Replica-exchange molecular dynamics method for protein folding. Chem. Phys. Lett. 314, 141-151 (1999)
55. 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)
56. Poully, J.C.; Gregoire, G.; Schermann, J.P.: Evaluation of the ONIOM Method for interpretation of infrared spectra of gas-phase molecules of biological interest. J. Phys. Chem. A 113, 8020-8026 (2009)
57. Frisch, M.J.; Trucks, G.W.; Schlegel, H.B.; Scuseria, G.E.; Robb, M.A.; Cheeseman, J.R.; Scalmani, G.; Barone, V.; Mennucci, B.; Petersson, G.A.; Nakatsuji, H.; Caricato, M.; Li, X.; Hratchian, H.P.; Izmaylov, A.F.; Bloino, J.; Zheng, G.; Sonnenberg, J.L.; Hada, M.; Ehara, M.; Toyota, K.; Fukuda, R.; Hasegawa, J.; Ishida, M.; Nakajima, T.; Honda, Y.; Kitao, O.; Nakai, H.; Vreven, T.; Montgomery, J.A. Jr.; Peralta, J.E.; Ogliaro, F.; Bearpark, M.; Heyd, J.J.; Brothers, E.; Kudin, K.N.; Staroverov, V.N.; Kobayashi, R.; Normand, J.; Raghavachari, K.; Rendell, A.; Burant, J.C.; Iyengar, S.S.; Tomasi, J.; Cossi, M.; Rega, N.; Millam, N.J.; Klene, M.; Knox, J.E.; Cross, J.B.; Bakken, V.; Adamo,C.; Jaramillo, J.; Gomperts, R.; Stratmann, R.E.; Yazyev, O.; Austin, A.J.; Cammi, R.; Pomelli, C.; Ochterski, J.W.; Martin, R.L.; Morokuma, K.; Zakrzewski, V.G.; Voth, G.A.; Salvador, P.; Dannenberg, J.J.; Dapprich, S.; Daniels, A.D.; Farkas, Ö.; Foresman, J.B.; Ortiz, J.V.; Cioslowski, J.; Fox, D. Gaussian 09, Rev A.2, Wallingford, CT (2009)
58. NIST available at: http://cccbdb.nist.gov/vibscalejust.asp. Accessed June 2013
59. Parneix, P.; Basire, M.; Calvo, F.: Accurate modeling of infrared multiple photon dissociation spectra: the dynamical role of anharmonicities. J. Phys. Chem. A 117, 3954-3959 (2013)
60. Revercomb, H.E.; Mason, E.A.: Theory of plasma chromatography gaseous electrophoresis - review. Anal. Chem. 47, 970-983 (1975)
61. Gill, A.C.; Jennings, K.R.; Wyttenbach, T.; Bowers, M.T.: Conformations of biopolymers in the gas phase: a new mass spectrometric method. Int. J. Mass Spectrom. 195, 685-697 (2000)
62. Rossi, M.; Blum, V.; Kupser, P.; von Helden, G.; Bierau, F.; Pagel, K.; Meijer, G.; Scheffler, M.: Secondary structure of Ac-Ala(n)-LysH(+) polyalanine peptides (n =5, 10, 15) in vacuo: helical or not? J. Phys. Chem. Lett. 1, 3465-3470 (2010)
63. Lin, C.; O'Connor, P.B.; Cournoyer, J.J.: Use of a double resonance electron capture dissociation experiment to probe fragment intermediate lifetimes. J. Am. Soc. Mass Spectrom. 17, 1605-1615 (2006)
64. Lin, C.; Cournoyer, J.J.; O'Connor, P.B.: Probing the gas-phase folding kinetics of peptide ions by IR activated DR-ECD. J. Am. Soc. Mass Spectrom. 19, 780-789 (2008)
65. Mihalca, R.; Kleinnijenhuis, A.J.; McDonnell, L.A.; Heck, A.J.R.; Heeren, R.M.A.: Electron capture dissociation at low temperatures reveals selective dissociations. J. Am. Soc. Mass Spectrom. 15, 1869-1873 (2004)
66. Lynn, D.G.; Meredith, S.C.: Review: model peptides and the physicochemical approach to β-amyloids. J. Struct. Biol. 130, 153-173 (2000)
67. Klimov, D.K.; Thirumalai, D.: Dissecting the assembly of A β(16-22) amyloid peptides into antiparallel β sheets. Structure 11, 295-307 (2003)
68. Jarvet, J.; Damberg, P.; Danielsson, J.; Johansson, I.; Eriksson, L.E.G.; Graslund, A.: A left-handed 3(1) helical conformation in the Alzheimer A β(12-28) peptide. FEBS Lett. 555, 371-374 (2003)
69. Stearns, J.A.; Seaiby, C.; Boyarkin, O.V.; Rizzo, T.R.: Spectroscopy and conformational preferences of gas-phase helices. Phys. Chem.; Chem. Phys. 11, 125-132 (2009)
70. Pagel, K.; Kupser, P.; Bierau, F.; Polfer, N.C.; Steill, J.D.; Oomens, J.; Meijer, G.; Koksch, B.; von Helden, G.: Gas-phase IR spectra of intact [alpha]-helical coiled coil protein complexes. Int. J. Mass Spectrom. 283, 161-168 (2009)