Pulsed hydrogen-deuterium exchange mass spectrometry probes conformational changes in amyloid beta (Aβ) peptide aggregation

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 36, 2013, Pages 14604-14609

  Zhang, Ying ^a   Rempel, Don L ^a   Zhang, Jun ^a   Sharma, Anuj K ^a   Mirica, Liviu M ^a   Gross, Michael L ^a  

^a WASHINGTON UNIVERSITY   (United States)

Author keywords

Amyloid beta peptide; Copper; Electrospray ionization; Finke Watsky mode; Soluble A oligomers

Indexed keywords

AMYLOID BETA PROTEIN[1-42]; CUPRIC ION; AMYLOID; AMYLOID BETA PROTEIN; AMYLOID BETA PROTEIN[1-40]; AMYLOID BETA-PROTEIN (1-42); COPPER; DEUTERIUM; HYDROGEN; PEPTIDE FRAGMENT;

ALZHEIMER DISEASE; AMINO TERMINAL SEQUENCE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BIOPHYSICS; CARBOXY TERMINAL SEQUENCE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; DEUTERIUM HYDROGEN EXCHANGE; FLUORESCENCE ANALYSIS; MASS SPECTROMETRY; MOLECULAR PROBE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; TEMPERATURE; CHEMISTRY; HUMAN; METABOLISM; PROCEDURES; PROTEIN CONFORMATION; TRANSMISSION ELECTRON MICROSCOPY; ULTRASTRUCTURE; WESTERN BLOTTING;

ALZHEIMER DISEASE; AMYLOID; AMYLOID BETA-PEPTIDES; BLOTTING, WESTERN; COPPER; DEUTERIUM; DEUTERIUM EXCHANGE MEASUREMENT; HUMANS; HYDROGEN; MASS SPECTROMETRY; MICROSCOPY, ELECTRON, TRANSMISSION; PEPTIDE FRAGMENTS; PROTEIN CONFORMATION; TEMPERATURE;

EID: 84883426127     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1309175110     Document Type: Article

References (68)

1. Roher AE, et al. (1993) beta-Amyloid-(1-42) is a major component of cerebrovascular amyloid deposits: Implications for the pathology of Alzheimer disease. Proc Natl Acad Sci USA 90(22):10836-10840.
2. Jarrett JT, Berger EP, Lansbury PT, Jr. (1993) The carboxy terminus of the beta amyloid protein is critical for the seeding of amyloid formation: Implications for the pathogenesis of Alzheimer's disease. Biochemistry 32(18):4693-4697. (Pubitemid 23162022)
3. Fagan AM, Holtzman DM (2010) Cerebrospinal fluid biomarkers of Alzheimer's disease. Biomarkers Med 4(1):51-63.
4. Kim J, et al. (2011) Haploinsufficiency of human APOE reduces amyloid deposition in a mouse model of amyloid-β amyloidosis. J Neurosci 31(49):18007-18012.
5. McGowan E, et al. (2005) Abeta42 is essential for parenchymal and vascular amyloid deposition in mice. Neuron 47(2):191-199. (Pubitemid 41019251)
6. Kim J, et al. (2007) Abeta40 inhibits amyloid deposition in vivo. J Neurosci 27(3):627-633. (Pubitemid 46143766)
7. Pauwels K, et al. (2012) Structural basis for increased toxicity of pathological aβ42: aβ40 ratios in Alzheimer disease. J Biol Chem 287(8):5650-5660.
8. Klein WL, Stine WB, Jr., Teplow DB (2004) Small assemblies of unmodified amyloid beta-protein are the proximate neurotoxin in Alzheimer's disease. Neurobiol Aging 25(5):569-580. (Pubitemid 38686476)
9. Cleary JP, et al. (2005) Natural oligomers of the amyloid-beta protein specifically disrupt cognitive function. Nat Neurosci 8(1):79-84. (Pubitemid 41236735)
10. Lesné S, et al. (2006) A specific amyloid-beta protein assembly in the brain impairs memory. Nature 440(7082):352-357.
11. Bharadwaj PR, Dubey AK, Masters CL, Martins RN, Macreadie IG (2009) Abeta aggregation and possible implications in Alzheimer 's disease pathogenesis. J Cell Mol Med 13(3):412-421.
12. Masuda Y, et al. (2009) Identification of physiological and toxic conformations in Abeta42 aggregates. ChemBioChem 10(2):287-295.
13. Upadhaya AR, Lungrin I, Yamaguchi H, Fändrich M, Thal DR (2012) High-molecular weight Aβ oligomers and protofibrils are the predominant Aβ species in the native soluble protein fraction of the AD brain. J Cell Mol Med 16(2):287-295.
14. Atwood CS, et al. (1998) Dramatic aggregation of Alzheimer abeta by Cu(II) is induced by conditions representing physiological acidosis. J Biol Chem 273(21):12817-12826. (Pubitemid 28246837)
15. Atwood CS, et al. (2004) Copper mediates dityrosine cross-linking of Alzheimer's amyloid-beta. Biochemistry 43(2):560-568. (Pubitemid 38082580)
16. Tõugu V, et al. (2009) Zn(II)- and Cu(II)-induced non-fibrillar aggregates of amyloid-beta (1-42) peptide are transformed to amyloid fibrils, both spontaneously and under the influence of metal chelators. J Neurochem 110(6):1784-1795.
17. Alí-Torres J, Maréchal JD, Rodríguez-Santiago L, Sodupe M (2011) Three dimensional models of Cu(2+)-Aβ(1-16) complexes from computational approaches. J Am Chem Soc 133(38):15008-15014.
18. 2+ ions on the aggregation and degradation of soluble Aβ oligomers and protofibrils investigated by fluorescence spectroscopy and AFM. J Inorg Biochem 116:26-36.
19. Sharma AK, et al. (2012) Bifunctional compounds for controlling metal-mediated aggregation of the aβ42 peptide. J Am Chem Soc 134(15):6625-6636.
20. Gong Y, et al. (2003) Alzheimer' s disease-affected brain: Presence of oligomeric A beta ligands (ADDLs) suggests a molecular basis for reversible memory loss. Proc Natl Acad Sci USA 100(18):10417-10422. (Pubitemid 37071893)
21. Prohaska JR, Gybina AA (2004) Intracellular copper transport in mammals. J Nutr 134(5):1003-1006. (Pubitemid 38619931)
22. Sawaya MR, et al. (2007) Atomic structures of amyloid cross-beta spines reveal varied steric zippers. Nature 447(7143):453-457. (Pubitemid 46816731)
23. Laganowsky A, et al. (2012) Atomic view of a toxic amyloid small oligomer. Science 335(6073):1228-1231.
24. Stroud JC, Liu C, Teng PK, Eisenberg D (2012) Toxic fibrillar oligomers of amyloid-β have cross-β structure. Proc Natl Acad Sci USA 109(20):7717-7722.
25. Castaño EM, et al. (1986) In vitro formation of amyloid fibrils from two synthetic peptides of different lengths homologous to Alzheimer's disease beta-protein. Biochem Biophys Res Commun 141(2):782-789. (Pubitemid 17001925)
26. Miller Y, Ma B, Tsai CJ, Nussinov R (2010) Hollow core of Alzheimer's Abeta42 amyloid observed by cryoEM is relevant at physiological pH. Proc Natl Acad Sci USA 107(32):14128-14133.
27. LeVine H, 3rd (1999) Quantification of beta-sheet amyloid fibril structures with thioflavin T. Methods Enzymol 309:274-284.
28. Lührs T, et al. (2005) 3D structure of Alzheimer's amyloid-beta(1-42) fibrils. Proc Natl Acad Sci USA 102(48):17342-17347.
29. Fawzi NL, Ying J, Ghirlando R, Torchia DA, Clore GM (2011) Atomic-resolution dynamics on the surface of amyloid-β protofibrils probed by solution NMR. Nature 480(7376):268-272.
30. Parthasarathy S, et al. (2011) Molecular-level examination of Cu2+ binding structure for amyloid fibrils of 40-residue Alzheimer's β by solid-state NMR spectroscopy. J Am Chem Soc 133(10):3390-3400.
31. Kheterpal I, Zhou S, Cook KD, Wetzel R (2000) Abeta amyloid fibrils possess a core structure highly resistant to hydrogen exchange. Proc Natl Acad Sci USA 97(25):13597-13601.
32. Kheterpal I, et al. (2003) Abeta protofibrils possess a stable core structure resistant to hydrogen exchange. Biochemistry 42(48):14092-14098. (Pubitemid 37499405)
33. Carulla N, Zhou M, Giralt E, Robinson CV, Dobson CM (2010) Structure and intermolecular dynamics of aggregates populated during amyloid fibril formation studied by hydrogen/deuterium exchange. Acc Chem Res 43(8):1072-1079.
34. Bernstein SL, et al. (2009) Amyloid-β protein oligomerization and the importance of tetramers and dodecamers in the aetiology of Alzheimer's disease. Nat Chem 1(4):326-331.
35. Zheng X, et al. (2012) Z-Phe-Ala-diazomethylketone (PADK) disrupts and remodels early oligomer states of the Alzheimer disease Aβ42 protein. J Biol Chem 287(9):6084-6088.
36. Gessel MM, et al. (2012) Aβ(39-42) modulates Aβ oligomerization but not fibril formation. Biochemistry 51(1):108-117.
37. Chalmers MJ, et al. (2006) Probing protein ligand interactions by automated hydrogen/deuterium exchange mass spectrometry. Anal Chem 78(4):1005-1014. (Pubitemid 43271829)
38. Kaltashov IA, Bobst CE, Abzalimov RR (2009) H/D exchange and mass spectrometry in the studies of protein conformation and dynamics: Is there a need for a top-down approach? Anal Chem 81(19):7892-7899.
39. Zhang J, et al. (2010) Hydrogen/deuterium exchange reveals distinct agonist/partial agonist receptor dynamics within vitamin D receptor/retinoid X receptor heterodimer. Structure 18(10):1332-1341.
40. Chalmers MJ, Busby SA, Pascal BD, West GM, Griffin PR (2011) Differential hydrogen/deuterium exchange mass spectrometry analysis of protein-ligand interactions. Expert Rev Proteomics 8(1):43-59.
41. Zhang Z, Smith DL (1993) Determination of amide hydrogen exchange by mass spectrometry: a new tool for protein structure elucidation. Protein Sci 2(4):522-531. (Pubitemid 23119303)
42. Wales TE, Engen JR (2006) Hydrogen exchange mass spectrometry for the analysis of protein dynamics. Mass Spectrom Rev 25(1):158-170.
43. Pan J, Han J, Borchers CH, Konermann L (2011) Conformer-specific hydrogen exchange analysis of Aβ(1-42) oligomers by top-down electron capture dissociation mass spectrometry. Anal Chem 83(13):5386-5393.
44. Pan J, Han J, Borchers CH, Konermann L (2012) Structure and dynamics of small soluble A β(1-40) oligomers studied by top-down hydrogen exchange mass spectrometry. Biochemistry 51(17):3694-3703.
45. Sánchez L, et al. (2011) Aβ40 and Aβ42 amyloid fibrils exhibit distinct molecular recycling properties. J Am Chem Soc 133(17):6505-6508.
46. Roder H, Elöve GA, Englander SW (1988) Structural characterization of folding intermediates in cytochrome c by H-exchange labelling and proton NMR. Nature 335(6192):700-704.
47. Pan J, Wilson DJ, Konermann L (2005) Pulsed hydrogen exchange and electrospray charge-state distribution as complementary probes of protein structure in kinetic experiments: implications for ubiquitin folding. Biochemistry 44(24):8627-8633. (Pubitemid 40840428)
48. Khanal A, Pan Y, Brown LS, Konermann L (2012) Pulsed hydrogen/deuterium exchange mass spectrometry for time-resolved membrane protein folding studies. J Mass Spectrom 47(12):1620-1626.
49. Dahlgren KN, et al. (2002) Oligomeric and fibrillar species of amyloid-beta peptides differentially affect neuronal viability. J Biol Chem 277(35):32046-32053. (Pubitemid 34969015)
50. Zhang Z, Marshall AG (1998) A universal algorithm for fast and automated charge state deconvolution of electrospray mass-to-charge ratio spectra. J Am Soc Mass Spectrom 9(3):225-233. (Pubitemid 128370213)
51. Morris AM, Watzky MA, Agar JN, Finke RG (2008) Fitting neurological protein aggregation kinetic data via a 2-step, minimal/"Ockham's razor" model: The Finke-Watzky mechanism of nucleation followed by autocatalytic surface growth. Biochemistry 47(8):2413-2427. (Pubitemid 351304547)
52. Caceci MS (1989) Estimating error limits in parametric curve fitting. Anal Chem 61(20):2324-2327.
53. Efron B (1979) 1977 Rietz Lecture - Bootstrap methods - Another look at the jackknife. Ann Stat 7 (1):1-26.
54. Efron B, Tibshirani R (1993) An Introduction to the Bootstrap (Chapman & Hall, New York), p xvi.
55. Murray MM, et al. (2009) Amyloid beta protein: Abeta40 inhibits Abeta42 oligomerization. J Am Chem Soc 131(18):6316-6317.
56. Yan Y, Wang C (2007) Abeta40 protects non-toxic Abeta42 monomer from aggregation. J Mol Biol 369(4):909-916. (Pubitemid 46754070)
57. Garai K, Frieden C (2013) Quantitative analysis of the time course of Aβ oligomerization and subsequent growth steps using tetramethylrhodamine- labeled Aβ. Proc Natl Acad Sci USA 110(9):3321-3326.
58. Urbanc B, Betnel M, Cruz L, Bitan G, Teplow DB (2010) Elucidation of amyloid beta-protein oligomerization mechanisms: Discrete molecular dynamics study. J Am Chem Soc 132(12):4266-4280.
59. Cruz L, Rao JS, Teplow DB, Urbanc B (2012) Dynamics of metastable β-hairpin structures in the folding nucleus of amyloid β-protein. J Phys Chem B 116(22):6311-6325.
60. Roychaudhuri R, Yang M, Condron MM, Teplow DB (2012) Structural dynamics of the amyloid β-protein monomer folding nucleus. Biochemistry 51(19):3957-3959.
61. Kumar-Singh S, et al. (2002) In vitro studies of Flemish, Dutch, and wild-type beta-amyloid provide evidence for two-staged neurotoxicity. Neurobiol Dis 11(2):330-340. (Pubitemid 36135696)
62. Nilsberth C, et al. (2001) The 'Arctic' APP mutation (E693G) causes Alzheimer's disease by enhanced Abeta protofibril formation. Nat Neurosci 4(9):887-893. (Pubitemid 32801591)
63. Levy E, et al. (1990) Mutation of the Alzheimer's disease amyloid gene in hereditary cerebral hemorrhage, Dutch type. Science 248(4959):1124-1126.
64. Grabowski TJ, Cho HS, Vonsattel JP, Rebeck GW, Greenberg SM (2001) Novel amyloid precursor protein mutation in an Iowa family with dementia and severe cerebral amyloid angiopathy. Ann Neurol 49(6):697-705. (Pubitemid 32530235)
65. Murakami K, et al. (2002) Synthesis, aggregation, neurotoxicity, and secondary structure of various A beta 1-42 mutants of familial Alzheimer's disease at positions 21-23. Biochem Biophys Res Commun 294(1):5-10. (Pubitemid 34687206)
66. Zhang J, Ramachandran P, Kumar R, Gross ML (2013) H/D exchange centroid monitoring is insufficient to show differences in the behavior of protein states. J Am Soc Mass Spectrom 24(3):450-453.
67. Huang RY, Garai K, Frieden C, Gross ML (2011) Hydrogen/deuterium exchange and electron-transfer dissociation mass spectrometry determine the interface and dynamics of apolipoprotein E oligomerization. Biochemistry 50(43):9273-9282.
68. Stine WB, Jr., Dahlgren KN, Krafft GA, LaDu MJ (2003) In vitro characterization of conditions for amyloid-beta peptide oligomerization and fibrillogenesis. J Biol Chem 278(13):11612-11622. (Pubitemid 36792723)