Mechanism of amyloid β-protein aggregation mediated by GM1 ganglioside clusters

Biochemistry

Volumn 50, Issue 29, 2011, Pages 6433-6440

  Ikeda, Keisuke ^a   Yamaguchi, Takahiro ^a   Fukunaga, Saori ^a   Hoshino, Masaru ^a   Matsuzaki, Katsumi ^a  

^a KYOTO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ALZHEIMERS DISEASE; AMYLOID FIBRIL; AQUEOUS PHASE; CIRCULAR DICHROISM DATA; FIBRILLIZATION; IN-VIVO; LIPID RAFT; MOLECULAR MECHANISM; PHYSICOCHEMICAL PROPERTY; PROTEIN AGGREGATION; PROTEIN DENSITY; SHEET STRUCTURE; SPHINGOMYELIN;

DICHROISM; LIPID BILAYERS; MONOMERS; PHOSPHOLIPIDS; PROTEINS;

GLYCOPROTEINS;

AMYLOID BETA PROTEIN; CHOLESTEROL; GANGLIOSIDE GM1;

ARTICLE; BETA SHEET; CIRCULAR DICHROISM; LIPID BILAYER; LIPID RAFT; PHYSICAL CHEMISTRY; PRIORITY JOURNAL; PROTEIN AGGREGATION;

AMYLOID BETA-PEPTIDES; ANIMALS; CATTLE; CIRCULAR DICHROISM; G(M1) GANGLIOSIDE; KINETICS; MODELS, BIOLOGICAL; PROTEIN BINDING; PROTEIN STABILITY; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, SECONDARY; TEMPERATURE; THIAZOLES;

EID: 79960506176     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi200771m     Document Type: Article

References (55)

1. Jarrett, J. T. and Lansbury, P. T., Jr. (1993) Seeding one-dimensional crystallization of amyloid: A pathogenic mechanism in Alzheimers disease and scrapie? Cell 73, 1055-1058 (Pubitemid 23180480)
2. Naiki, H., Hasegawa, K., Yamaguchi, I., Nakamura, H., Gejyo, F., and Nakakuki, K. (1998) Apolipoprotein E and antioxidants have different mechanisms of inhibiting Alzheimers β-amyloid fibril formation in vitro Biochemistry 37, 17882-17889 (Pubitemid 29023943)
3. Naiki, H. and Nakakuki, K. (1996) First-order kinetic model of Alzheimers β-amyloid fibril extension in vitro Lab. Invest. 74, 374-383 (Pubitemid 26072080)
4. Naiki, H. and Gejyo, F. (1999) Kinetic analysis of amyloid fibril formation Methods Enzymol. 309, 305-318 (Pubitemid 29446457)
5. Oosawa, F. and Asakura, S. (1975) Thermodynamics of the polymerizaiton of protein, Academic Press, London.
6. Murphy, R. M. (2007) Kinetics of amyloid formation and membrane interaction with amyloidogenic proteins Biochim. Biophys. Acta 1768, 1923-1934 (Pubitemid 47125847)
7. Gorbenko, G. P. and Kinnunen, P. K. (2006) The role of lipid-protein interactions in amyloid-type protein fibril formation Chem. Phys. Lipids 141, 72-82 (Pubitemid 43728804)
8. Sani, M. A., Gehman, J. D., and Separovic, F. (2011) Lipid matrix plays a role in Aβ fibril kinetics and morphology FEBS Lett. 585, 749-754
9. Selkoe, D. J. (1994) Cell biology of the amyloid β-protein precursor and the mechanism of Alzheimers disease Annu. Rev. Cell Biol. 10, 373-403 (Pubitemid 24372824)
10. Hardy, J. and Selkoe, D. J. (2002) The amyloid hypothesis of Alzheimers disease: Progress and problems on the road to therapeutics Science 297, 353-356 (Pubitemid 34790756)
11. Seubert, P., Vigo-Pelfrey, C., Esch, F., Lee, M., Dovey, H., Davis, D., Sinha, S., Schlossmacher, M., Whaley, J., Swindlehurst, C., McCormack, R., Wolfert, R., Selkoe, J., Lieberburg, I., and Schenk, D. (1992) Isolation and quantification of soluble Alzheimers β-peptide from biological fluids Nature 359, 325-327
12. ONuallain, B., Shivaprasad, S., Kheterpal, I., and Wetzel, R. (2005) Thermodynamics of Aβ(1-40) amyloid fibril elongation Biochemistry 44, 10709-12718
13. Matsuzaki, K. (2007) Physicochemical interactions of amyloid β-peptide with lipid bilayers Biochim. Biophys. Acta 1768, 1935-1942 (Pubitemid 47135568)
14. Matsuzaki, K., Kato, K., and Yanagisawa, K. (2010) Aβ polymerization through interaction with membrane gangliosides Biochim. Biophys. Acta 1801, 868-877
15. Kakio, A., Nishimoto, S., Yanagisawa, K., Kozutsumi, Y., and Matsuzaki, K. (2001) Cholesterol-dependent formation of GM1 ganglioside-bound amyloid β-protein, an endogenous seed for Alzheimer amyloid J. Biol. Chem. 276, 24985-24990
16. Yanagisawa, K. (2007) Role of gangliosides in Alzheimers disease Biochim. Biophys. Acta 1768, 1943-1951
17. Ariga, T., McDonald, M. P., and Yu, R. K. (2008) Role of ganglioside metabolism in the pathogenesis of Alzheimers disease: A review J. Lipid Res. 49, 1157-1175
18. Kakio, A., Nishimoto, S., Yanagisawa, K., Kozutsumi, Y., and Matsuzaki, K. (2002) Interactions of amyloid β-protein with various gangliosides in raft-like membranes: Importance of GM1 ganglioside-bound form as an endogenous seed for Alzheimer amyloid Biochemistry 41, 7385-7390 (Pubitemid 34602456)
19. Lee, E. K., Hwang, J. H., Shin, D. Y., Kim, D. I., and Yoo, Y. J. (2005) Production of recombinant amyloid-β a peptide 42 as an ubiquitin extension Protein Expression Purif. 40, 183-189 (Pubitemid 40240986)
20. Yamaguchi, T., Yagi, H., Goto, Y., Matsuzaki, K., and Hoshino, M. (2010) A disulfide-linked amyloid-β peptide dimer forms a protofibril-like oligomer through a distinct pathway from amyloid fibril formation Biochemistry 49, 7100-7107
21. Yang, J. T., Wu, C.-S. C., and Martinez, H. M. (1986) Calculation of protein conformation from circular dichroism Methods Enzymol. 130, 208-269
22. Okada, T., Wakabayashi, M., Ikeda, K., and Matsuzaki, K. (2007) Formation of toxic fibrils of Alzheimers amyloid β-protein-(1-40) by monosialoganglioside GM1, a neuronal membrane component J. Mol. Biol. 371, 481-489 (Pubitemid 47048280)
23. Svennerholm, L. (1957) Quantitative estimation of sialic acids. II. A colorimetric resorcinol-hydrochloric acid method Biochim. Biophys. Acta 24, 604-611
24. Bartlett, G. R. (1959) Phosphorus assay in column chromatography J. Biol. Chem. 234, 466-468
25. Matsuzaki, K., Noguch, T., Wakabayashi, M., Ikeda, K., Okada, T., Ohashi, Y., Hoshino, M., and Naiki, H. (2007) Inhibitors of amyloid β-protein aggregation mediated by GM1-containing raft-like membranes Biochim. Biophys. Acta 1768, 122-130 (Pubitemid 44909079)
26. Yamamoto, N., Matsuzaki, K., and Yanagisawa, K. (2005) Cross-seeding of wild-type and hereditary variant type amyloid β-proteins in the presence of gangliosides J. Neurochem. 95, 1167-1176 (Pubitemid 41713499)
27. Takakuwa, T., Konno, T., and Meguro, H. (1985) A new standard substance for calibration of circular dichroism: Ammonium d -10-camphorsulfonate Anal. Sci. 1, 215-218
28. LeVine, H., III (1993) Thioflavine T interaction with synthetic Alzheimers disease β-amyloid peptides: Detection of amyloid aggregation in solution Protein Sci. 2, 404-410
29. Kojima, M., Tanokura, M., Maeda, M., Kimura, K., Amemiya, Y., Kihara, H., and Takahashi, K. (2000) pH-dependent unfolding of aspergillopepsin II studied by small-angle X-ray scattering Biochemistry 39, 1364-1372 (Pubitemid 30090705)
30. Henry, E. R. and Hofrichter, J. (1992) Singular value decomposition: Application to analysis of experimental data Methods Enzymol. 210, 129-192
31. Roy, R. S., Gopi, H. N., Raghothama, S., Gilardi, R. D., Karle, I. L., and Balaram, P. (2005) Peptide hairpins with strand segments containing α- and β-amino acid residues: Cross-strand aromatic interactions of facing Phe residues Biopolymers 80, 787-799 (Pubitemid 43266585)
32. Kirkitadze, M. D., Condron, M. M., and Teplow, D. B. (2001) Identification and characterization of key kinetic intermediates in amyloid β-protein fibrillogenesis J. Mol. Biol. 312, 1103-1119 (Pubitemid 32980329)
33. Fezoui, Y. and Teplow, D. B. (2002) Kinetic studies of amyloid β-protein fibril assembly. Differential effects of α-helix stabilization J. Biol. Chem. 277, 36948-36954
34. Mandal, P. K. and Pettegrew, J. W. (2004) Alzheimers disease: Soluble oligomeric Aβ(1-40) peptide in membrane mimic environment from solution NMR and circular dichroism studies Neurochem. Res. 29, 2267-2272 (Pubitemid 40036899)
35. Jayasinghe, S. A. and Langen, R. (2005) Lipid membranes modulate the structure of islet amyloid polypeptide Biochemistry 44, 12113-12119 (Pubitemid 41285709)
36. Knight, J. D., Hebda, J. A., and Miranker, A. D. (2006) Conserved and cooperative assembly of membrane-bound α-helical states of islet amyloid polypeptide Biochemistry 45, 9496-9508 (Pubitemid 44223253)
37. 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)
38. Abedini, A. and Raleigh, D. P. (2009) A critical assessment of the role of helical intermediates in amyloid formation by natively unfolded proteins and polypeptides Protein Eng., Des. Sel. 22, 453-459
39. Lee, C.-C., Sun, Y., and Huang, H. W. (2010) Membrane-mediated peptide conformation change from α-monomers to β-aggregates Biophys. J. 98, 2236-2245
40. Sun, Y., Lee, C.-C., Chen, T.-H., and Huang, H. W. (2010) Kinetic process of β-amyloid formation via membrane binding Biophys. J. 99, 544-552
41. Butterfield, S. M. and Lashuel, H. A. (2010) Amyloidogenic protein-membrane interactions: Mechanistic insight from model systems Angew. Chem., Int. Ed. 49, 5628-5654
42. Choi, J.-S., Braymer, J. J., Nanga, R. P. R., 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. Hindo, S. S., Mancino, A. M., Braymer, J. J., Liu, Y., Vivekanandan, S., Ramamoorthy, A., and Lim, M. H. (2009) Small molecule modulators of copper-induced Aβ aggregation J. Am. Chem. Soc. 131, 16663-16665
44. Yoo, S. I., Yang, M., Brender, J. R., Subramanian, V., Sun, K., Joo, N. E., Jeong, S. H., Ramamoorthy, A., and Kotov, N. A. (2011) Inhibition of amyloid peptide fibrillation by inorganic nanoparticles: Functional similarities with proteins Angew. Chem., Int. Ed. 50, 5110-5115
45. Wieprecht, T., Beyermann, M., and Seelig, J. (1999) Binding of antibacterial magainin peptides to electrically neutral membranes: Thermodynamics and structure Biochemistry 38, 10377-10387
46. Meier, M. and Seelig, J. (2007) Thermodynamics of the coil-β-sheet transition in a membrane environment J. Mol. Biol. 369, 277-289 (Pubitemid 46635428)
47. Mikhalyov, I., Olofsson, A., Gröbner, G., and Johansson, L. B. (2010) Designed fluorescent probes reveal interactions between amyloid-β(1-40) peptides and GM1 gangliosides in micelles and lipid vesicles Biophys. J. 99, 1510-1519
48. Konno, T. (1998) Conformational diversity of acid-denatured cytochrome c studied by a matrix analysis of far-UV CD spectra Protein Sci. 7, 975-982 (Pubitemid 28216539)
49. Kamiyoshihara, T., Kojima, M., Uéda, K., Tashiro, M., and Shimotakahara, S. (2007) Observation of multiple intermediates in α-synuclein fibril formation by singular value decomposition analysis Biochem. Biophys. Res. Commun. 355, 398-403 (Pubitemid 46282641)
50. Chen, Y.-H., Yang, J. T., and Martinez, H. M. (1972) Determination of the secondary structures of proteins by circular dichroism and optical rotatory dispersion Biochemistry 11, 4120-4131
51. Utsumi, M., Yamaguchi, Y., Sasakawa, H., Yamamoto, N., Yanagisawa, K., and Kato, K. (2008) Up-and-down topological mode of amyloid β-peptide lying on hydrophilic/hydrophobic interface of ganglioside clusters Glycoconjugate J. 26, 999-1006
52. Terzi, E., Hölzemann, G., and Seelig, J. (1997) Interaction of Alzheimer β-amyloid peptide(1-40) with lipid membranes Biochemistry 36, 14845-14852 (Pubitemid 27524407)
53. 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
54. Daune, M. (1999) Hydrophobic and hydrophilic molecules. In Molecular biophysics, Chapter 12, Oxford University Press, New York.
55. Terzi, E., Hölzmann, G., and Seelig, J. (1995) Self-association of β-amyloid peptide (1-40) in solution and binding to lipid membranes J. Mol. Biol. 252, 633-642