One of the possible mechanisms of amyloid fibrils formation based on the sizes of primary and secondary folding nuclei of Aβ40 and Aβ42

Journal of Structural Biology

Volumn 194, Issue 3, 2016, Pages 404-414

  Dovidchenko, Nikita V ^a   Glyakina, Anna V ^a,b   Selivanova, Olga M ^a   Grigorashvili, Elizaveta I ^a   Suvorina, Mariya Yu ^a   Dzhus, Ulyana F ^a   Mikhailina, Alisa O ^a   Shiliaev, Nikita G ^a   Marchenkov, Victor V ^a   Surin, Alexey K ^a,c   Galzitskaya, Oxana V ^a  

^a INSTITUTE OF PROTEIN RESEARCH   (Russian Federation)

^b INSTITUTE OF MATHEMATICAL PROBLEMS OF BIOLOGY   (Russian Federation)

^c STATE RESEARCH CENTER FOR APPLIED MICROBIOLOGY AND BIOTECHNOLOGY   (Russian Federation)

Author keywords

Alzheimer's disease; Amyloid fibril; A 40 peptide; A 42 peptide; Electron microscopy; Oligomer; Secondary nucleation; Size of nucleus

Indexed keywords

AMYLOID BETA PROTEIN[1-40]; AMYLOID BETA PROTEIN[1-42]; MONOMER; OLIGOMER; AMYLOID; AMYLOID BETA PROTEIN; AMYLOID BETA-PROTEIN (1-42); PEPTIDE FRAGMENT;

ALZHEIMER DISEASE; ARTICLE; CONTROLLED STUDY; ELECTRON MICROSCOPY; MOLECULAR BIOLOGY; NONHUMAN; NUCLEAR SIZE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FOLDING; PROTEIN PURIFICATION; PROTEIN SYNTHESIS; QUANTITATIVE ANALYSIS; X RAY DIFFRACTION; BIOSYNTHESIS; CHEMISTRY; ESCHERICHIA COLI; MOLECULAR MODEL;

AMYLOID; AMYLOID BETA-PEPTIDES; ESCHERICHIA COLI; MODELS, MOLECULAR; PEPTIDE FRAGMENTS; PROTEIN FOLDING;

EID: 84963812107     PISSN: 10478477     EISSN: 10958657     Source Type: Journal    
DOI: 10.1016/j.jsb.2016.03.020     Document Type: Article

References (55)

1. Ahmed M., Davis J., Aucoin D., Sato T., Ahuja S., Aimoto S., Elliott J.I., Van Nostrand W.E., Smith S.O. Structural conversion of neurotoxic amyloid-beta(1-42) oligomers to fibrils. Nat. Struct. Mol. Biol. 2010, 17:561-567. 10.1038/nsmb.1799.
2. Bieschke J., Zhang Q., Powers E.T., Lerner R.A., Kelly J.W. Oxidative metabolites accelerate Alzheimer's amyloidogenesis by a two-step mechanism, eliminating the requirement for nucleation. Biochemistry (Mosc.) 2005, 44:4977-4983. 10.1021/bi0501030.
3. Brender J.R., Krishnamoorthy J., Messina G.M.L., Deb A., Vivekanandan S., La Rosa C., Penner-Hahn J.E., Ramamoorthy A. Zinc stabilization of prefibrillar oligomers of human islet amyloid polypeptide. Chem. Commun. Camb. Engl. 2013, 49:3339-3341. 10.1039/c3cc40383a.
4. Brender J.R., Krishnamoorthy J., Sciacca M.F.M., Vivekanandan S., D'Urso L., Chen J., La Rosa C., Ramamoorthy A. Probing the sources of the apparent irreproducibility of amyloid formation: drastic changes in kinetics and a switch in mechanism due to micellelike oligomer formation at critical concentrations of IAPP. J. Phys. Chem. B 2015, 119:2886-2896. 10.1021/jp511758w.
5. Chiti F., Dobson C.M. Protein misfolding, functional amyloid, and human disease. Annu. Rev. Biochem. 2006, 75:333-366. 10.1146/annurev.biochem.75.101304.123901.
6. Cho K.R., Huang Y., Yu S., Yin S., Plomp M., Qiu S.R., Lakshminarayanan R., Moradian-Oldak J., Sy M.-S., De Yoreo J.J. A multistage pathway for human prion protein aggregation in vitro: from multimeric seeds to β-oligomers and nonfibrillar structures. J. Am. Chem. Soc. 2011, 133:8586-8593. 10.1021/ja1117446.
7. Cohen S.I.A., Linse S., Luheshi L.M., Hellstrand E., White D.A., Rajah L., Otzen D.E., Vendruscolo M., Dobson C.M., Knowles T.P.J. Proliferation of amyloid-β42 aggregates occurs through a secondary nucleation mechanism. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:9758-9763. 10.1073/pnas.1218402110.
8. Derrick J.S., Lim M.H. Tools of the trade: investigations into design strategies of small molecules to target components in Alzheimer's disease. ChemBioChem 2015, 16:887-898. 10.1002/cbic.201402718.
9. Dobson C.M. Principles of protein folding, misfolding and aggregation. Semin. Cell Dev. Biol. 2004, 15:3-16. 10.1016/j.semcdb.2003.12.008.
10. Dovidchenko N.V., Finkelstein A.V., Galzitskaya O.V. How to determine the size of folding nuclei of protofibrils from the concentration dependence of the rate and lag-time of aggregation. I. Modeling the amyloid protofibril formation. J. Phys. Chem. B 2014, 118:1189-1197. 10.1021/jp4083294.
11. Fändrich M., Meinhardt J., Grigorieff N. Structural polymorphism of Alzheimer Abeta and other amyloid fibrils. Prion 2009, 3:89-93.
12. Ferrone F.A. Assembly of Aβ proceeds via monomeric nuclei. J. Mol. Biol. 2015, 427:287-290. 10.1016/j.jmb.2014.10.028.
13. Finder V.H., Glockshuber R. Amyloid-beta aggregation. Neurodegener. Dis. 2007, 4:13-27. 10.1159/000100355.
14. Hellstrand E., Boland B., Walsh D.M., Linse S. Amyloid β-protein aggregation produces highly reproducible kinetic data and occurs by a two-phase process. ACS Chem. Neurosci. 2010, 1:13-18. 10.1021/cn900015v.
15. Jansen R., Dzwolak W., Winter R. Amyloidogenic self-assembly of insulin aggregates probed by high resolution atomic force microscopy. Biophys. J. 2005, 88:1344-1353. 10.1529/biophysj.104.048843.
16. Kheterpal I., Lashuel H.A., Hartley D.M., Walz T., Lansbury P.T., Wetzel R. Abeta protofibrils possess a stable core structure resistant to hydrogen exchange. Biochemistry (Mosc.) 2003, 42:14092-14098. 10.1021/bi0357816.
17. Knowles T.P.J., Vendruscolo M., Dobson C.M. The amyloid state and its association with protein misfolding diseases. Nat. Rev. Mol. Cell Biol. 2014, 15:384-396. 10.1038/nrm3810.
18. Knowles T.P.J., Waudby C.A., Devlin G.L., Cohen S.I.A., Aguzzi A., Vendruscolo M., Terentjev E.M., Welland M.E., Dobson C.M. An analytical solution to the kinetics of breakable filament assembly. Science 2009, 326:1533-1537. 10.1126/science.1178250.
19. Kooistra J., Milojevic J., Melacini G., Ortega J. A new function of human HtrA2 as an amyloid-beta oligomerization inhibitor. J. Alzheimers Dis. JAD 2009, 17:281-294. 10.3233/JAD-2009-1037.
20. Korshavn K.J., Bhunia A., Lim M.H., Ramamoorthy A. Amyloid-β adopts a conserved, partially folded structure upon binding to zwitterionic lipid bilayers prior to amyloid formation. Chem Commun 2016, 10.1039/C5CC08634E.
21. Kotler S.A., Brender J.R., Vivekanandan S., Suzuki Y., Yamamoto K., Monette M., Krishnamoorthy J., Walsh P., Cauble M., Holl M.M.B., Marsh E.N.G., Ramamoorthy A. High-resolution NMR characterization of low abundance oligomers of amyloid-β without purification. Sci. Rep. 2015, 5:11811. 10.1038/srep11811.
22. Krieger E., Koraimann G., Vriend G. Increasing the precision of comparative models with YASARA NOVA - a self-parameterizing force field. Proteins 2002, 47:393-402.
23. Lashuel H.A., Hartley D.M., Petre B.M., Wall J.S., Simon M.N., Walz T., Lansbury P.T. Mixtures of wild-type and a pathogenic (E22G) form of Abeta40 in vitro accumulate protofibrils, including amyloid pores. J. Mol. Biol. 2003, 332:795-808.
24. Lührs T., Ritter C., Adrian M., Riek-Loher D., Bohrmann B., Döbeli H., Schubert D., Riek R. 3D structure of Alzheimer's amyloid-beta(1-42) fibrils. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:17342-17347. 10.1073/pnas.0506723102.
25. Lu J.-X., Qiang W., Yau W.-M., Schwieters C.D., Meredith S.C., Tycko R. Molecular structure of β-amyloid fibrils in Alzheimer's disease brain tissue. Cell 2013, 154:1257-1268. 10.1016/j.cell.2013.08.035.
26. Maltsev A.V., Bystryak S., Galzitskaya O.V. The role of β-amyloid peptide in neurodegenerative diseases. Ageing Res. Rev. 2011, 10:440-452. 10.1016/j.arr.2011.03.002.
27. McDonald M., Box H., Bian W., Kendall A., Tycko R., Stubbs G. Fiber diffraction data indicate a hollow core for the Alzheimer's aβ 3-fold symmetric fibril. J. Mol. Biol. 2012, 423:454-461. 10.1016/j.jmb.2012.08.004.
28. Meisl G., Yang X., Hellstrand E., Frohm B., Kirkegaard J.B., Cohen S.I.A., Dobson C.M., Linse S., Knowles T.P.J. Differences in nucleation behavior underlie the contrasting aggregation kinetics of the Aβ40 and Aβ42 peptides. Proc. Natl. Acad. Sci. U. S. A. 2014, 111:9384-9389. 10.1073/pnas.1401564111.
29. Milojevic J., Melacini G. Stoichiometry and affinity of the human serum albumin-Alzheimer's Aβ peptide interactions. Biophys. J. 2011, 100:183-192. 10.1016/j.bpj.2010.11.037.
30. Nielsen E.H., Nybo M., Svehag S.E. Electron microscopy of prefibrillar structures and amyloid fibrils. Methods Enzymol. 1999, 309:491-496.
31. Ono K., Condron M.M., Teplow D.B. Structure-neurotoxicity relationships of amyloid beta-protein oligomers. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:14745-14750. 10.1073/pnas.0905127106.
32. Paravastu A.K., Leapman R.D., Yau W.-M., Tycko R. Molecular structural basis for polymorphism in Alzheimer's beta-amyloid fibrils. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:18349-18354. 10.1073/pnas.0806270105.
33. Paravastu A.K., Qahwash I., Leapman R.D., Meredith S.C., Tycko R. Seeded growth of beta-amyloid fibrils from Alzheimer's brain-derived fibrils produces a distinct fibril structure. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:7443-7448. 10.1073/pnas.0812033106.
34. Pauwels K., Williams T.L., Morris K.L., Jonckheere W., Vandersteen A., Kelly G., Schymkowitz J., Rousseau F., Pastore A., Serpell L.C., Broersen K. Structural basis for increased toxicity of pathological aβ42:aβ40 ratios in Alzheimer disease. J. Biol. Chem. 2012, 287:5650-5660. 10.1074/jbc.M111.264473.
35. Perutz M.F., Finch J.T., Berriman J., Lesk A. Amyloid fibers are water-filled nanotubes. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:5591-5595. 10.1073/pnas.042681399.
36. Petkova A.T., Leapman R.D., Guo Z., Yau W.-M., Mattson M.P., Tycko R. Self-propagating, molecular-level polymorphism in Alzheimer's beta-amyloid fibrils. Science 2005, 307:262-265. 10.1126/science.1105850.
37. Qiang W., Kelley K., Tycko R. Polymorph-specific kinetics and thermodynamics of β-amyloid fibril growth. J. Am. Chem. Soc. 2013, 135:6860-6871. 10.1021/ja311963f.
38. Quist A., Doudevski I., Lin H., Azimova R., Ng D., Frangione B., Kagan B., Ghiso J., Lal R. Amyloid ion channels: a common structural link for protein-misfolding disease. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:10427-10432. 10.1073/pnas.0502066102.
39. Raditsis A.V., Milojevic J., Melacini G. Aβ association inhibition by transferrin. Biophys. J. 2013, 105:473-480. 10.1016/j.bpj.2013.03.065.
40. Roychaudhuri R., Yang M., Deshpande A., Cole G.M., Frautschy S., Lomakin A., Benedek G.B., Teplow D.B. C-terminal turn stability determines assembly differences between Aβ40 and Aβ42. J. Mol. Biol. 2013, 425:292-308. 10.1016/j.jmb.2012.11.006.
41. Sambasivam D., Sivanesan S., Ashok B.S., Rajadas J. Structural preferences of Aβ fragments in different micellar environments. Neuropeptides 2011, 45:369-376. 10.1016/j.npep.2011.09.001.
42. Selivanova O.M., Suvorina M.Y., Dovidchenko N.V., Eliseeva I.A., Surin A.K., Finkelstein A.V., Schmatchenko V.V., Galzitskaya O.V. How to determine the size of folding nuclei of protofibrils from the concentration dependence of the rate and lag-time of aggregation. II. Experimental application for insulin and LysPro insulin: aggregation morphology, kinetics, and sizes of nuclei. J. Phys. Chem. B 2014, 118:1198-1206. 10.1021/jp4083568.
43. 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., Selkoe D.J. Amyloid-β protein dimers isolated directly from Alzheimer's brains impair synaptic plasticity and memory. Nat. Med. 2008, 14:837-842. 10.1038/nm1782.
44. Smaoui M.R., Poitevin F., Delarue M., Koehl P., Orland H., Waldispühl J. Computational assembly of polymorphic amyloid fibrils reveals stable aggregates. Biophys. J. 2013, 104:683-693. 10.1016/j.bpj.2012.12.037.
45. Soong R., Brender J.R., Macdonald P.M., Ramamoorthy A. Association of highly compact type II diabetes related islet amyloid polypeptide intermediate species at physiological temperature revealed by diffusion NMR spectroscopy. J. Am. Chem. Soc. 2009, 131:7079-7085. 10.1021/ja900285z.
46. Stroud J.C., Liu C., Teng P.K., Eisenberg D. Toxic fibrillar oligomers of amyloid-β have cross-β structure. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:7717-7722. 10.1073/pnas.1203193109.
47. Suvorina M.Y., Selivanova O.M., Grigorashvili E.I., Nikulin A.D., Marchenkov V.V., Surin A.K., Galzitskaya O.V. Studies of polymorphism of amyloid-β 42 peptide from different suppliers. J. Alzheimers Dis. 2015, 47:583-593. 10.3233/JAD-150147.
48. Toyama B.H., Weissman J.S. Amyloid structure: conformational diversity and consequences. Annu. Rev. Biochem. 2011, 80:557-585. 10.1146/annurev-biochem-090908-120656.
49. Van Gool D., David G., Lammens M., Baro F., Dom R. Heparan sulfate expression patterns in the amyloid deposits of patients with Alzheimer's and Lewy body type dementia. Dement. Basel Switz. 1993, 4:308-314.
50. Vivekanandan S., Brender J.R., Lee S.Y., Ramamoorthy A. A partially folded structure of amyloid-beta(1-40) in an aqueous environment. Biochem. Biophys. Res. Commun. 2011, 411:312-316. 10.1016/j.bbrc.2011.06.133.
51. Volpatti L.R., Vendruscolo M., Dobson C.M., Knowles T.P.J. A clear view of polymorphism, twist, and chirality in amyloid fibril formation. ACS Nano 2013, 7:10443-10448. 10.1021/nn406121w.
52. Xiao Y., Ma B., McElheny D., Parthasarathy S., Long F., Hoshi M., Nussinov R., Ishii Y. Aβ(1-42) fibril structure illuminates self-recognition and replication of amyloid in Alzheimer's disease. Nat. Struct. Mol. Biol. 2015, 22:499-505. 10.1038/nsmb.2991.
53. Zhang R., Hu X., Khant H., Ludtke S.J., Chiu W., Schmid M.F., Frieden C., Lee J.-M. Interprotofilament interactions between Alzheimer's Abeta1-42 peptides in amyloid fibrils revealed by cryoEM. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:4653-4658. 10.1073/pnas.0901085106.
54. Zhang Y., Rempel D.L., Zhang J., Sharma A.K., Mirica L.M., Gross M.L. Pulsed hydrogen-deuterium exchange mass spectrometry probes conformational changes in amyloid beta (Aβ) peptide aggregation. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:14604-14609. 10.1073/pnas.1309175110.
55. Zivanovic Y., Confalonieri F., Ponchon L., Lurz R., Chami M., Flayhan A., Renouard M., Huet A., Decottignies P., Davidson A.R., Breyton C., Boulanger P. Insights into bacteriophage T5 structure from analysis of its morphogenesis genes and protein components. J. Virol. 2014, 88:1162-1174. 10.1128/JVI.02262-13.