Solid-support electron paramagnetic resonance (EPR) studies of Aβ40 monomers reveal a structured state with three ordered segments

Journal of Biological Chemistry

Volumn 287, Issue 12, 2012, Pages 9081-9089

  Gu, Lei ^a   Ngo, Sam ^a   Guo, Zhefeng ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AGGREGATION PROCESS; ALZHEIMER DISEASE; BUILDING BLOCKES; CAUSATIVE AGENTS; DENATURING CONDITIONS; DISORDERED STATE; DISORDERED STRUCTURES; EPR SPECTRA; HIS-TAG; N-TERMINALS; SOLID SUPPORTS; SPIN LABEL; STRUCTURAL FEATURE;

AGGLOMERATION; ELECTRON SPIN RESONANCE SPECTROSCOPY; GLYCOPROTEINS; MAGNETIC RESONANCE; NEURODEGENERATIVE DISEASES; OLIGOMERIZATION; OLIGOMERS; PARAMAGNETISM;

MONOMERS;

AMYLOID BETA PROTEIN[1-40]; MONOMER;

ARTICLE; CONTROLLED STUDY; ELECTRON SPIN RESONANCE; MOLECULAR INTERACTION; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN DENATURATION; PROTEIN STRUCTURE; SPIN LABELING;

AMINO ACID MOTIFS; AMYLOID BETA-PEPTIDES; ELECTRON SPIN RESONANCE SPECTROSCOPY; HUMANS; PROTEIN STRUCTURE, SECONDARY;

EID: 84858612961     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.292086     Document Type: Article

References (52)

1. Walsh, D. M., and Selkoe, D. J. (2007) Aβ oligomers, a decade of discovery. J. Neurochem. 101, 1172-1184
2. Younkin, S. G. (1995) Evidence that Aβ 42 is the real culprit in Alzheimer disease. Ann. Neurol. 37, 287-288
3. Irie, K., Murakami, K., Masuda, Y., Morimoto, A., Ohigashi, H., Ohashi, R., Takegoshi, K., Nagao, M., Shimizu, T., and Shirasawa, T. (2005) Structure of β-amyloid fibrils and its relevance to their neurotoxicity: implications for the pathogenesis of Alzheimer disease. J. Biosci. Bioeng. 99, 437-447 (Pubitemid 40874521)
4. Walsh, D. M., Klyubin, I., Fadeeva, J. V., Cullen, W. K., Anwyl, R., Wolfe, M. S., Rowan, M. J., and Selkoe, D. J. (2002) Naturally secreted oligomers of amyloid β protein potently inhibit hippocampal long-term potentiation in vivo. Nature 416, 535-539 (Pubitemid 34288854)
5. Cleary, J. P., Walsh, D. M., Hofmeister, J. J., Shankar, G. M., Kuskowski, M. A., Selkoe, D. J., and Ashe, K. H. (2005) Natural oligomers of the amyloid-β protein specifically disrupt cognitive function. Nat. Neurosci. 8, 79-84 (Pubitemid 41236735)
6. Shankar, G. M., Li, S., Mehta, T. H., Garcia-Munoz, A., Shepardson, N. E., Smith, I., Brett, F. M., Farrell, M. A., Rowan, M. J., Lemere, C. A., Regan, C. M., Walsh, D. M., Sabatini, B. L., and Selkoe, D. J. (2008) Amyloid-β protein dimers isolated directly from Alzheimer's brains impair synaptic plasticity and memory. Nat. Med. 14, 837-842
7. Hou, L., Shao, H., Zhang, Y., Li, H., Menon, N. K., Neuhaus, E. B., Brewer, J. M., Byeon, I. J., Ray, D. G., Vitek, M. P., Iwashita, T., Makula, R. A., Przybyla, A. B., and Zagorski, M. G. (2004) Solution NMR studies of the Aβ (1-40) and Aβ (1-42) peptides establish that the Met35 oxidation state affects the mechanism of amyloid formation. J. Am. Chem. Soc. 126, 1992-2005 (Pubitemid 38228879)
8. Riek, R., Güntert, P., Döbeli, H., Wipf, B., and Wüthrich, K. (2001) NMR studies in aqueous solution fail to identify significant conformational differences between the monomeric forms of two Alzheimer peptides with widely different plaque-competence, Aβ (1-40)(ox) and Aβ (1-42)(ox). Eur. J. Biochem. 268, 5930-5936 (Pubitemid 33079329)
9. Lim, K. H., Collver, H. H., Le, Y. T., Nagchowdhuri, P., and Kenney, J. M. (2007) Characterizations of distinct amyloidogenic conformations of the Aβ (1-40) and (1-42) peptides. Biochem. Biophys. Res. Commun. 353, 443-449 (Pubitemid 46014583)
10. Lim, K. H., Henderson, G. L., Jha, A., and Louhivuori, M. (2007) Structural, dynamic properties of key residues in Aβ amyloidogenesis: implications of an important role of nanosecond timescale dynamics. ChemBioChem 8, 1251-1254 (Pubitemid 47171991)
11. Zhang, S., Iwata, K., Lachenmann, M. J., Peng, J. W., Li, S., Stimson, E. R., Lu, Y., Felix, A. M., Maggio, J. E., and Lee, J. P. (2000) The Alzheimer peptide Aβ adopts a collapsed coil structure in water. J. Struct. Biol. 130, 130-141
12. Danielsson, J., Andersson, A., Jarvet, J., and Gräslund, A. (2006) 15N relaxation study of the amyloid β-peptide: structural propensities and persistence length. Magn Reson Chem 44, S114-121 (Pubitemid 44090397)
13. Yan, Y., Liu, J., McCallum, S. A., Yang, D., and Wang, C. (2007) Methyl dynamics of the amyloid-β peptides Aβ42. Biochem. Biophys. Res. Commun. 362, 410-414
14. Yan, Y., and Wang, C. (2006) Aβ42 is more rigid than Aβ40 at the C terminus: implications for Aβ aggregation and toxicity. J. Mol. Biol. 364, 853-862 (Pubitemid 44765041)
15. Lazo, N. D., Grant, M. A., Condron, M. C., Rigby, A. C., and Teplow, D. B. (2005) On the nucleation of amyloid β-protein monomer folding. Protein Sci. 14, 1581-1596 (Pubitemid 41007920)
16. Grant, M. A., Lazo, N. D., Lomakin, A., Condron, M. M., Arai, H., Yamin, G., Rigby, A. C., and Teplow, D. B. (2007) Familial Alzheimer disease mutations alter the stability of the amyloid β-protein monomer folding nucleus. Proc. Natl. Acad. Sci. U.S.A. 104, 16522-16527 (Pubitemid 350211051)
17. Baumketner, A., Bernstein, S. L., Wyttenbach, T., Bitan, G., Teplow, D. B., Bowers, M. T., and Shea, J. E. (2006) Amyloid β-protein monomer structure: a computational and experimental study. Protein Sci. 15, 420-428
18. Sgourakis, N. G., Yan, Y., McCallum, S. A., Wang, C., and Garcia, A. E. (2007) The Alzheimer peptides Aβ40 and 42 adopt distinct conformations in water: a combined MD / NMR study. J. Mol. Biol. 368, 1448-1457 (Pubitemid 46617600)
19. Vivekanandan, S., Brender, J. R., Lee, S. Y., and Ramamoorthy, A. (2011) A partially folded structure of amyloid-β (1-40) in an aqueous environment. Biochem. Biophys. Res. Commun. 411, 312-316
20. Bitan, G., Kirkitadze, M. D., Lomakin, A., Vollers, S. S., Benedek, G. B., and Teplow, D. B. (2003) Amyloid β-protein (Aβ) assembly: Aβ40 and Aβ42 oligomerize through distinct pathways. Proc. Natl. Acad. Sci. U.S.A. 100, 330-335
21. Pallitto, M. M., and Murphy, R. M. (2001) A mathematical model of the kinetics of β-amyloid fibril growth from the denatured state. Biophys. J. 81, 1805-1822 (Pubitemid 32783616)
22. Teplow, D. B. (2006) Preparation of amyloid β-protein for structural and functional studies. Methods Enzymol. 413, 20-33
23. Amirgoulova, E. V., Groll, J., Heyes, C. D., Ameringer, T., Röcker, C., Möller, M., and Nienhaus, G. U. (2004) Biofunctionalized polymer surfaces exhibiting minimal interaction towards immobilized proteins. ChemPhysChem 5, 552-555
24. Zhuang, X., Bartley, L. E., Babcock, H. P., Russell, R., Ha, T., Herschlag, D., and Chu, S. (2000) A single-molecule study of RNA catalysis and folding. Science 288, 2048-2051 (Pubitemid 30397686)
25. Guo, Z. (2003) Correlation of spin label side-chain Dynamics with protein structure: studies of T4 lysozyme with site-directed mutagenesis and X-ray crystallography. Ph.D. Dissertation. University of California, Los Angeles.
26. López, C. J., Fleissner, M. R., Guo, Z., Kusnetzow, A. K., and Hubbell, W. L. (2009) Osmolyte perturbation reveals conformational equilibria in spinlabeled proteins. Protein Sci. 18, 1637-1652
27. Columbus, L., and Hubbell, W. L. (2002) A new spin on protein dynamics. Trends Biochem. Sci. 27, 288-295 (Pubitemid 34628668)
28. Fanucci, G. E., and Cafiso, D. S. (2006) Recent advances and applications of site-directed spin labeling. Curr. Opin. Struct. Biol. 16, 644-653 (Pubitemid 44466409)
29. Klug, C. S., and Feix, J. B. (2008) Methods and applications of site-directed spin labeling EPR spectroscopy. Methods Cell Biol. 84, 617-658
30. Ionu Iuracu, M., Cozma, C., Tomczyk, N., Rontree, J., Desor, M., Drescher, M., and Przybylski, M. (2009) Structural characterization of β-amyloid oligomer-aggregates by ion mobility mass spectrometry and electron spin resonance spectroscopy. Anal. Bioanal. Chem. 395, 2509-2519
31. Török, M., Milton, S., Kayed, R., Wu, P., McIntire, T., Glabe, C. G., and Langen, R. (2002) Structural and dynamic features of Alzheimer Aβ peptide in amyloid fibrils studied by site-directed spin labeling. J. Biol. Chem. 277, 40810-40815 (Pubitemid 35215666)
32. Murakami, K., Hara, H., Masuda, Y., Ohigashi, H., and Irie, K. (2007) Distance measurement between Tyr-10 and Met-35 in amyloid β by site-directed spin-labeling ESR spectroscopy: implications for the stronger neurotoxicity of Aβ42 than Aβ40. ChemBioChem 8, 2308-2314
33. Sepkhanova, I., Drescher, M., Meeuwenoord, N. J., Limpens, R. W., Koning, R. I., Filippov, D. V., and Huber, M. (2009) Monitoring Alzheimer amyloid peptide aggregation by EPR. Appl. Magn. Reson. 36, 209-222
34. Santoro, M. M., and Bolen, D. W. (1988) Unfolding free energy changes determined by the linear extrapolation method. 1. Unfolding of phenylmethanesulfonyl α-chymotrypsin using different denaturants. Biochemistry 27, 8063-8068
35. Ngo, S., and Guo, Z. (2011) Key residues for the oligomerization of Aβ42 protein in Alzheimer disease. Biochem. Biophys. Res. Commun. 414, 512-516
36. McCoy, J., and Hubbell, W. L. (2011) High-pressure EPR reveals conformational equilibria and volumetric properties of spin-labeled proteins. Proc. Natl. Acad. Sci. U.S.A. 108, 1331-1336
37. Schneider, D. J., and Freed, J. H. (1989) in Spin Labeling: Theory and Applications (Berliner, L. J., and Reuben, J., eds), pp. 1-76, Plenum Press, New York
38. Budil, D. E., Lee, S., Saxena, S., and Freed, J. H. (1996) J. Magn. Reson., Ser A 120, 155-189
39. Columbus, L., Kálai, T., Jekö, J., Hideg, K., and Hubbell, W. L. (2001) Molecular motion of spin-labeled side chains in α-helices: analysis by variation of side chain structure. Biochemistry 40, 3828-3846 (Pubitemid 32280420)
40. Wilchek, M., and Miron, T. (1999) React. Funct. Polym. 41, 263-268
41. Carson, M., Johnson, D. H., McDonald, H., Brouillette, C., and Delucas, L. J. (2007) His tag impact on structure. Acta Crystallogr. D 63, 295-301
42. Wilchek, M., and Miron, T. (2003) Oriented versus random protein immobilization. J. Biochem. Biophys. Methods 55, 67-70 (Pubitemid 36135958)
43. Kohn, J. E., Millett, I. S., Jacob, J., Zagrovic, B., Dillon, T. M., Cingel, N., Dothager, R. S., Seifert, S., Thiyagarajan, P., Sosnick, T. R., Hasan, M. Z., Pande, V. S., Ruczinski, I., Doniach, S., and Plaxco, K. W. (2004) Randomcoil behavior and the dimensions of chemically unfolded proteins. Proc. Natl. Acad. Sci. U.S.A. 101, 12491-12496 (Pubitemid 39122051)
44. Kawahara, K., and Tanford, C. (1966) Viscosity and density of aqueous solutions of urea and guanidine hydrochloride. J. Biol. Chem. 241, 3228-3232
45. Guo, Z., Cascio, D., Hideg, K., and Hubbell, W. L. (2008) Structural determinants of nitroxide motion in spin-labeled proteins: solvent-exposed sites in helix B of T4 lysozyme. Protein Sci. 17, 228-239 (Pubitemid 351171835)
46. Guo, Z., Cascio, D., Hideg, K., Kálái, T., and Hubbell, W. L. (2007) Structural determinants of nitroxide motion in spin-labeled proteins: tertiary contact and solvent-inaccessible sites in helix G of T4 lysozyme. Protein Sci. 16, 1069-1086 (Pubitemid 46849217)
47. Bora, R. P., and Prabhakar, R. J. (2009) J. Chem. Phys. 131, 155103
48. Wang, S. S., Tobler, S. A., Good, T. A., and Fernandez, E. J. (2003) Hydrogen exchange-mass spectrometry analysis of β-amyloid peptide structure. Biochemistry 42, 9507-9514 (Pubitemid 36959259)
49. Sgourakis, N. G., Merced-Serrano, M., Boutsidis, C., Drineas, P., Du, Z., Wang, C., and Garcia, A. E. (2011) Atomic-level characterization of the ensemble of the Aβ(1-42) monomer in water using unbiased molecular dynamics simulations and spectral algorithms. J. Mol. Biol. 405, 570-583
50. Cote, S., Derreumaux, P., and Mousseau, N. (2011) J. Chem. Theory Comput. 7, 2584-2592
51. Yang, M., and Teplow, D. B. (2008) Amyloid β-protein monomer folding: free-energy surfaces reveal alloform-specific differences. J. Mol. Biol. 384, 450-464
52. Murakami, K., Irie, K., Morimoto, A., Ohigashi, H., Shindo, M., Nagao, M., Shimizu, T., and Shirasawa, T. (2003) Neurotoxicity and physicochemical properties of Aβ mutant peptides from cerebral amyloid angiopathy: implication for the pathogenesis of cerebral amyloid angiopathy and Alzheimer disease. J. Biol. Chem. 278, 46179-46187 (Pubitemid 37432769)