Small amphipathic molecules modulate secondary structure and amyloid fibril-forming kinetics of Alzheimer disease peptide Aβ1-42

Journal of Biological Chemistry

Volumn 287, Issue 20, 2012, Pages 16947-16954

  Ryan, Timothy M ^a   Friedhuber, Anna ^a   Lind, Monica ^a   Howlett, Geoffrey J ^b   Masters, Colin ^a   Roberts, Blaine R ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

AGGREGATION PROCESS; ALZHEIMER DISEASE; AMPHIPATHIC MOLECULES; AMYLOID FIBRIL FORMATION; ANALYTICAL ULTRACENTRIFUGATION; END-PRODUCTS; FIBRIL FORMATION; HELICAL STRUCTURES; LARGE AGGREGATES; NEURONAL LOSS; SECONDARY STRUCTURES; SELF-ASSOCIATIONS; SHEET STRUCTURE; SMALL-MOLECULE BINDINGS; THERAPEUTIC STRATEGY; THIOFLAVIN T;

AGGLOMERATION; CENTRIFUGATION; DICHROISM; ELECTRON MICROSCOPY; MOLECULES; NEURODEGENERATIVE DISEASES; OLIGOMERS; PEPTIDES; STOICHIOMETRY;

POLYPEPTIDES;

AMYLOID; AMYLOID BETA PROTEIN[1-42];

ALPHA HELIX; ALZHEIMER DISEASE; ARTICLE; BETA SHEET; BINDING SITE; CIRCULAR DICHROISM; CONFORMATION; ELECTRON MICROSCOPY; FLUORESCENCE MICROSCOPY; HUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN SECONDARY STRUCTURE; SOLUBILIZATION; STOICHIOMETRY; ULTRACENTRIFUGATION;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; HUMANS; KINETICS; PEPTIDE FRAGMENTS; PEPTIDE LIBRARY; PROTEIN MULTIMERIZATION; PROTEIN STABILITY; PROTEIN STRUCTURE, SECONDARY;

EID: 84860849103     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.321778     Document Type: Article

References (51)

1. Breteler, M. M., Claus, J. J., van Duijn, C. M., Launer, L. J., and Hofman, A. (1992) Epidemiology of Alzheimer's disease. Epidemiol. Rev. 14, 59-82 (Pubitemid 23024554)
2. Chai, C. K. (2007) The genetics of Alzheimer's disease. Am. J. Alzheimers Dis. Other Demen. 22, 37-41
3. Götz, J., and Ittner, L. M. (2008) Animal models of Alzheimer's disease and frontotemporal dementia. Nat. Rev. Neurosci. 9, 532-544 (Pubitemid 351873467)
4. Lorenzo, A., and Yankner, B. A. (1994) β-Amyloid neurotoxicity requires fibril formation and is inhibited by Congo Red. Proc. Natl. Acad. Sci. U.S.A. 91, 12243-12247 (Pubitemid 24368641)
5. Lorenzo, A., and Yankner, B. A. (1996) Amyloid fibril toxicity in Alzheimer's disease and diabetes. Ann. N.Y. Acad. Sci. 777, 89-95 (Pubitemid 26149175)
6. McLean, C. A., Cherny, R. A., Fraser, F. W., Fuller, S. J., Smith, M. J., Beyreuther, K., Bush, A. I., and Masters, C. L. (1999) Soluble pool of Aßamyloid as a determinant of severity of neurodegeneration in Alzheimer's disease. Ann. Neurol. 46, 860-866
7. Haass, C., and Selkoe, D. J. (2007) Soluble protein oligomers in neurodegeneration: lessons from the Alzheimer's amyloid-β peptide. Nat. Rev. Mol. Cell Biol. 8, 101-112 (Pubitemid 46432529)
8. Marchesi, V. T. (2005) An alternative interpretation of the amyloid Aßhypothesis with regard to the pathogenesis of Alzheimer's disease. Proc. Natl. Acad. Sci. U.S.A. 102, 9093-9098
9. Kokubo, H., Saido, T. C., Iwata, N., Helms, J. B., Shinohara, R., and Yamaguchi, H. (2005) Part of membrane-bound Aβ exists in rafts within senile plaques in Tg2576 mouse brain. Neurobiol. Aging 26, 409-418 (Pubitemid 40093924)
10. Widenbrant, M. J., Rajadas, J., Sutardja, C., and Fuller, G. G. (2006) Lipid-induced β-amyloid peptide assemblage fragmentation. Biophys. J. 91, 4071-4080 (Pubitemid 44887267)
11. Wong, P. T., Schauerte, J. A., Wisser, K. C., Ding, H., Lee, E. L., Steel, D. G., and Gafni, A. (2009) Amyloid-β membrane binding and permeabilization are distinct processes influenced separately by membrane charge and fluidity. J. Mol. Biol. 386, 81-96
12. Yoda, M., Miura, T., and Takeuchi, H. (2008) Non-electrostatic binding and self-association of amyloid-β peptide on the surface of tightly packed phosphatidylcholine membranes. Biochem. Biophys. Res. Commun. 376, 56-59
13. Ikeda, K., and Matsuzaki, K. (2008) Driving force of binding of amyloid-βprotein to lipid bilayers. Biochem. Biophys. Res. Commun. 370, 525-529
14. M1-mediated amyloid-β fibrillogenesis and membrane disruption. Biochemistry 46, 1913-1924
15. Ryan, T. M., Howlett, G. J., and Bailey, M. F. (2008) Fluorescence detection of a lipid-induced tetrameric intermediate in amyloid fibril formation by apolipoprotein C-II. J. Biol. Chem. 283, 35118-35128
16. Ryan, T. M., Teoh, C. L., Griffin, M. D., Bailey, M. F., Schuck, P., and Howlett, G. J. (2010) Phospholipids enhance nucleation but not elongation of apolipoprotein C-II amyloid fibrils. J. Mol. Biol. 399, 731-740
17. Ryan, T. M., Griffin, M. D., Teoh, C. L., Ooi, J., and Howlett, G. J. (2011) High-affinity amphipathic modulators of amyloid fibril nucleation and elongation. J. Mol. Biol. 406, 416-429
18. 3-42. J. Biol. Chem. 284, 22697-22702
19. Schuck, P. (2000) Size distribution analysis of macromolecules by sedimentation velocity ultracentrifugation and lamm equation modeling. Biophys. J. 78, 1606-1619
20. Schuck, P. (2003) On the analysis of protein self-association by sedimentation velocity analytical ultracentrifugation. Anal. Biochem. 320, 104-124
21. Olofsson, A., Borowik, T., Gröbner, G., and Sauer-Eriksson, A. E. (2007) Negatively charged phospholipid membranes induce amyloid formation of medin via an α-helical intermediate. J. Mol. Biol. 374, 186-194 (Pubitemid 47600226)
22. Andreola, A., Bellotti, V., Giorgetti, S., Mangione, P., Obici, L., Stoppini, M., Torres, J., Monzani, E., Merlini, G., and Sunde, M. (2003) Conformational switching and fibrillogenesis in the amyloidogenic fragment of apolipoprotein A-I. J. Biol. Chem. 278, 2444-2451 (Pubitemid 36801320)
23. Stöckl, M., Fischer, P., Wanker, E., and Herrmann, A. (2008) α-Synuclein selectively binds to anionic phospholipids embedded in liquid-disordered domains. J. Mol. Biol. 375, 1394-1404
24. Knight, J. D., and Miranker, A. D. (2004) Phospholipid catalysis of diabetic amyloid assembly. J. Mol. Biol. 341, 1175-1187 (Pubitemid 39099208)
25. 2-microglobulin in vitro under physiological conditions. Biochemistry 48, 5689-5699
26. Deleault, N. R., Harris, B. T., Rees, J. R., and Supattapone, S. (2007) Formation of native prions from minimal components in vitro. Proc. Natl. Acad. Sci. U.S.A. 104, 9741-9746 (Pubitemid 47175337)
27. Näsström, T., Fagerqvist, T., Barbu, M., Karlsson, M., Nikolajeff, F., Kasrayan, A., Ekberg, M., Lannfelt, L., Ingelsson, M., and Bergström, J. (2011) The lipid peroxidation products 4-oxo-2-nonenal and 4-hydroxy-2-nonenal promote the formation of α-synuclein oligomers with distinct biochemical, morphological, and functional properties. Free Radic. Biol. Med. 50, 428-437
28. Siegel, S. J., Bieschke, J., Powers, E. T., and Kelly, J. W. (2007) The oxidative stress metabolite 4-hydroxynonenal promotes Alzheimer protofibril formation. Biochemistry 46, 1503-1510
29. 1-40 peptide membrane interactions: aggregation preventing transmembrane anchoring versus accelerated surface fibril formation. J. Mol. Biol. 335, 1039-1049
30. Wood, S. J., MacKenzie, L., Maleeff, B., Hurle, M. R., and Wetzel, R. (1996) Selective inhibition of Aβ fibril formation. J. Biol. Chem. 271, 4086-4092
31. Arispe, N., and Doh, M. (2002) Plasma membrane cholesterol controls the cytotoxicity of Alzheimer's disease AßP1-40 and 1-42 peptides. FASEB J. 16, 1526-1536 (Pubitemid 35154635)
32. Avdulov, N. A., Chochina, S. V., Igbavboa, U., Warden, C. S., Vassiliev, A. V., and Wood, W. G. (1997) Lipid binding to amyloid-β peptide aggregates: preferential binding of cholesterol as compared with phosphatidylcholine and fatty acids. J. Neurochem. 69, 1746-1752 (Pubitemid 27406976)
33. Yip, C. M., Elton, E. A., Darabie, A. A., Morrison, M. R., and McLaurin, J. (2001) Cholesterol, a modulator of membrane-associated Aβ- fibrillogenesis and neurotoxicity. J. Mol. Biol. 311, 723-734 (Pubitemid 32803731)
34. Gibson Wood, W., Eckert, G. P., Igbavboa, U., and Muller, W. E. (2003) Amyloid-βprotein interactions with membranes and cholesterol: causes or casualties of Alzheimer's disease. Biochim. Biophys. Acta 1610, 281-290 (Pubitemid 36324471)
35. Hane, F., and Drolle, E., and Leonenko, Z. (2010) Effect of cholesterol and amyloid-β peptide on structure and function of mixed lipid films and pulmonary surfactant BLES: an atomic force microscopy study. Nanomedicine 6, 808-814
36. Panchal, M., Loeper, J., Cossec, J. C., Perruchini, C., Lazar, A., Pompon, D., and Duyckaerts, C. (2010) Enrichment of cholesterol in microdissected Alzheimer's disease senile plaques as assessed by mass spectrometry. J. Lipid Res. 51, 598-605
37. Rojo, L., Sjöberg, M. K., Hernández, P., Zambrano, C., and Maccioni, R. B. (2006) Roles of cholesterol and lipids in the etiopathogenesis of Alzheimer's disease. J. Biomed. Biotechnol. 2006, 73976
38. Gervais, F., Paquette, J., Morissette, C., Krzywkowski, P., Yu, M., Azzi, M., Lacombe, D., Kong, X., Aman, A., Laurin, J., Szarek, W. A., and Tremblay, P. (2007) Targeting soluble Aβ peptide with Tramiprosate for the treatment of brain amyloidosis. Neurobiol. Aging 28, 537-547 (Pubitemid 46282205)
39. Schaefer, E. J., Bongard, V., Beiser, A. S., Lamon-Fava, S., Robins, S. J., Au, R., Tucker, K. L., Kyle, D. J., Wilson, P. W., and Wolf, P. A. (2006) Plasma phosphatidylcholine docosahexaenoic acid content and risk of dementia and Alzheimer disease: the Framingham Heart Study. Arch. Neurol. 63, 1545-1550 (Pubitemid 44748796)
40. Liu, Y., Yang, L., Conde-Knape, K., Beher, D., Shearman, M. S., and Shachter, N. S. (2004) Fatty acids increase presenilin-1 levels and γ-secretase activity in PSwt-1 cells. J. Lipid Res. 45, 2368-2376 (Pubitemid 39602985)
41. Calon, F., and Cole, G. (2007) Neuroprotective action of ω-3 polyunsaturated fatty acids against neurodegenerative diseases: evidence from animal studies. Prostaglandins Leukot. Essent. Fatty Acids 77, 287-293 (Pubitemid 350198857)
42. Choi, J. S., Braymer, J. J., Nanga, R. P., Ramamoorthy, A., and Lim, M. H. (2010) Design of small molecules that target metal-Aβ species and regulate metal-induced Aβ aggregation and neurotoxicity. Proc. Natl. Acad. Sci. U.S.A. 107, 21990-21995
43. Bazoti, F. N., Bergquist, J., Markides, K., and Tsarbopoulos, A. (2008) Localization of the noncovalent binding site between amyloid-β peptide and oleuropein using electrospray ionization FT-ICR mass spectrometry. J. Am. Soc. Mass Spectrom. 19, 1078-1085
44. 1-40 and antioxidant compounds by NMR spectroscopy. Biopolymers 96, 316-327
45. Nerelius, C., Sandegren, A., Sargsyan, H., Raunak, R., Leijonmarck, H., Chatterjee, U., Fisahn, A., Imarisio, S., Lomas, D. A., Crowther, D. C., Strömberg, R., and Johansson, J. (2009) α-Helix targeting reduces amyloid-βpeptide toxicity. Proc. Natl. Acad. Sci. U.S.A. 106, 9191-9196
46. Kinghorn, K. J., Crowther, D. C., Sharp, L. K., Nerelius, C., Davis, R. L., Chang, H. T., Green, C., Gubb, D. C., Johansson, J., and Lomas, D. A. (2006) Neuroserpin binds Aβ and is a neuroprotective component of amyloid plaques in Alzheimer disease. J. Biol. Chem. 281, 29268-29277 (Pubitemid 44507070)
47. Narayanan, S., Kamps, B., Boelens, W. C., and Reif, B. (2006) αB-crystallin competes with Alzheimer's disease β-amyloid peptide for peptide-peptide interactions and induces oxidation of Aβ-Met35. FEBS Lett. 580, 5941-5946 (Pubitemid 44584297)
48. Mandal, P. K., Williams, J. P., and Mandal, R. (2007) Molecular understanding of Aβ peptide interaction with isoflurane, propofol, and thiopental: NMR spectroscopic study. Biochemistry 46, 762-771 (Pubitemid 46133592)
49. Mandal, P. K., Pettegrew, J. W., McKeag, D. W., and Mandal, R. (2006) Alzheimer's disease: halothane induces Aβ peptide to oligomeric form: solution NMR studies. Neurochem. Res. 31, 883-890 (Pubitemid 44134241)
50. 1-40 peptide in a membrane mimic environment. Neurochem. Res. 29, 447-453
51. Bieschke, J., Herbst, M., Wiglenda, T., Friedrich, R. P., Boeddrich, A., Schiele, F., Kleckers, D., Lopez del Amo, J. M., Grüning, B. A., Wang, Q., Schmidt, M. R., Lurz, R., Anwyl, R., Schnoegl, S., Fändrich, M., Frank, R. F., Reif, B., Günther, S., Walsh, D. M., and Wanker, E. E. (2012) Small-molecule conversion of toxic oligomers to nontoxic β-sheet-rich amyloid fibrils. Nat. Chem. Biol. 8, 93-101