The interaction of amyloid Aβ(1-40) with lipid bilayers and ganglioside as studied by 31P solid-state NMR

Chemistry and Physics of Lipids

Volumn 158, Issue 1, 2009, Pages 54-60

  Nakazawa, Yasumoto ^a   Suzuki, Yu ^a   Williamson, Mike P ^b   Saitô, Hazime ^a   Asakura, Tetsuo ^a  

^a TOKYO UNIVERSITY OF AGRICULTURE AND TECHNOLOGY   (Japan)

^b UNIVERSITY OF SHEFFIELD   (United Kingdom)

Author keywords

Amyloid; Alzheimer's disease; GM1 ganglioside; Lipid bilayer; NMR

Indexed keywords

AMYLOID BETA PROTEIN[1-40]; DIMYRISTOYLPHOSPHATIDYLCHOLINE; GANGLIOSIDE GM1; AMYLOID BETA PROTEIN; PEPTIDE FRAGMENT;

ARTICLE; CONTROLLED STUDY; LIPID BILAYER; MICELLE; PHASE TRANSITION; PHOSPHORUS NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN LIPID INTERACTION; SOLID STATE; CHEMISTRY; METABOLISM; NUCLEAR MAGNETIC RESONANCE;

AMYLOID BETA-PROTEIN; DIMYRISTOYLPHOSPHATIDYLCHOLINE; G(M1) GANGLIOSIDE; LIPID BILAYERS; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PEPTIDE FRAGMENTS;

EID: 60249099854     PISSN: 00093084     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.chemphyslip.2008.12.001     Document Type: Article

References (48)

1. Ambroggio E.E., Kim D.H., Separovic F., Barrow C.J., Barnham K.J., Bagatolli L.A., and Fidelio G.D. Surface behavior and lipid interaction of Alzheimer β-amyloid peptide 1-42: a membrane-disrupting peptide. Biophys. J. 88 (2005) 2706-2713
2. Arispe N., Pollard H.B., and Rojas E. Giant multilevel cation channels formed by Alzheimer disease amyloid β-protein [Aβ P-(1-40)] in bilayer membranes. Proc. Natl. Acad. Sci. USA 90 (1993) 10573-10577
3. Bateman D.A., McLaurin J., and Chakrabartty A. Requirement of aggregation propensity of Alzheimer amyloid peptides for neuronal cell surface binding. BMC Neurosci. 8 (2007) 29
4. Bokvist M., Lindstrom F., Watts A., and Grobner G. Two types of Alzheimer's β-amyloid (1-40) peptide membrane interactions: aggregation preventing transmembrane anchoring versus accelerated surface fibril formation. J. Mol. Biol. 335 (2004) 1039-1049
5. Brender J.R., Durr U.H., Heyl D., Budarapu M.B., and Ramamoorthy A. Membrane fragmentation by an amyloidogenic fragment of human Islet Amyloid Polypeptide detected by solid-state NMR spectroscopy of membrane nanotubes. Biochim. Biophys. Acta 1768 (2007) 2026-2029
6. Brocca P., and Sonnino S. Dynamics and spatial organization of surface gangliosides. Trends Glycosci. Glycotechnol. 9 (1997) 433-445
7. Chi E.Y., Frey S.L., and Lee K.Y. Ganglioside GM1-mediated amyloid-β fibrillogenesis and membrane disruption. Biochemistry 46 (2007) 1913-1924
8. Choo-Smith L.P., and Surewicz W.K. The interaction between Alzheimer amyloid β(1-40) peptide and ganglioside GM1-containing membranes. FEBS Lett. 402 (1997) 95-98
9. Cornell B.A., and Separovic F. A model for gramicidin A'-phospholipid interactions in bilayers. Eur. Biophys. J. 16 (1988) 299-306
10. Cullis P.R., and de Kruijff B. Lipid polymorphism and the functional roles of lipids in biological membranes. Biochim. Biophys. Acta 559 (1979) 399-420
11. De Kruijff B., Van den Besselaar A.M., Cullis P.R., Van den Bosch H., and Van Deenen L.L. Evidence for isotropic motion of phospholipids in liver microsomal membranes. A phosphorus-31 NMR study. Biochim. Biophys. Acta 514 (1978) 1-8
12. de Planque M.R., Raussens V., Contera S.A., Rijkers D.T., Liskamp R.M., Ruysschaert J.M., Ryan J.F., Separovic F., and Watts A. β-Sheet structured β-amyloid(1-40) perturbs phosphatidylcholine model membranes. J. Mol. Biol. 368 (2007) 982-997
13. II phase formation in phosphatidylcholine model membranes. Biochim. Biophys. Acta 939 (1988) 79-88
14. Geula C., Wu C.K., Saroff D., Lorenzo A., Yuan M., and Yankner B.A. Aging renders the brain vulnerable to amyloid β-protein neurotoxicity. Nat. Med. 4 (1998) 827-831
15. Glenner G.G., and Wong C.W. Alzheimer's disease and Down's syndrome: sharing of a unique cerebrovascular amyloid fibril protein. Biochem. Biophys. Res. Commun. 122 (1984) 1131-1135
16. Iversen L.L., Mortishire-Smith R.J., Pollack S.J., and Shearman M.S. The toxicity in vitro of β-amyloid protein. Biochem. J. 311 (1995) 1-16
17. Kakio A., Nishimoto S., Yanagisawa K., Kozutsumi Y., and Matsuzaki K. 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 (2002) 7385-7390
18. Kakio A., Nishimoto S., Kozutsumi Y., and Matsuzaki K. Formation of a membrane-active form of amyloid β-protein in raft-like model membranes. Biochem. Biophys. Res. Commun. 303 (2003) 514-518
19. Kang J., Lemaire H.G., Unterbeck A., Salbaum J.M., Masters C.L., Grzeschik K.H., Multhaup G., Beyreuther K., and Muller-Hill B. The precursor of Alzheimer's disease amyloid A4 protein resembles a cell-surface receptor. Nature 325 (1987) 733-736
20. Kasahara K., and Sanai Y. Involvement of lipid raft signaling in ganglioside-mediated neural function. Trends Glycosci. Glycotechnol. 74 (2001) 587-594
21. Keller S.L., Gruner S.M., and Gawrisch K. Small concentrations of alamethicin induce a cubic phase in bulk phosphatidylethanolamine mixtures. Biochim. Biophys. Acta 1278 (1996) 241-246
22. II phase formation in dioleoylphosphatidylcholine model membranes. Biochemistry 24 (1985) 7890-7898
23. Kirschner D.A., Abraham C., and Selkoe D.J. X-ray diffraction from intraneuronal paired helical filaments and extraneuronal amyloid fibers in Alzheimer disease indicates cross-β conformation. Proc. Natl. Acad. Sci. USA 83 (1986) 503-507
24. Lambert M.P., Barlow A.K., Chromy B.A., Edwards C., Freed R., Liosatos M., Morgan T.E., Rozovsky I., Trommer B., Viola K.L., Wals P., Zhang C., Finch C.E., Krafft G.A., and Klein W.L. Diffusible, nonfibrillar ligands derived from Aβ1-42 are potent central nervous system neurotoxins. Proc. Natl. Acad. Sci. USA 95 (1998) 6448-6453
25. Lau T.L., Ambroggio E.E., Tew D.J., Cappai R., Masters C.L., Fidelio G.D., Barnham K.J., and Separovic F. Amyloid-β peptide disruption of lipid membranes and the effect of metal ions. J. Mol. Biol. 356 (2006) 759-770
26. 31P NMR spectroscopic study of the effect of transmembrane α-helical peptides on the lamellar-reversed hexagonal phase transition of phosphatidylethanolamine model membranes. Biochemistry 40 (2001) 760-768
27. Masters C.L., Multhaup G., Simms G., Pottgiesser J., Martins R.N., and Beyreuther K. Neuronal origin of a cerebral amyloid: neurofibrillary tangles of Alzheimer's disease contain the same protein as the amyloid of plaque cores and blood vessels. EMBO J. 4 (1985) 2757-2763
28. McLaurin J., and Chakrabartty A. Membrane disruption by Alzheimer β-amyloid peptides mediated through specific binding to either phospholipids or gangliosides. Implications for neurotoxicity. J. Biol. Chem. 271 (1996) 26482-26489
29. McLaurin J., Franklin T., Chakrabartty A., and Fraser P.E. Phosphatidylinositol and inositol involvement in Alzheimer amyloid-β fibril growth and arrest. J. Mol. Biol. 278 (1998) 183-194
30. McLaurin J., Franklin T., Fraser P.E., and Chakrabartty A. Structural transitions associated with the interaction of Alzheimer β-amyloid peptides with gangliosides. J. Biol. Chem. 273 (1998) 4506-4515
31. Moll III F., and Cross T.A. Optimizing and characterizing alignment of oriented lipid bilayers containing gramicidin D. Biophys. J. 57 (1990) 351-362
32. Muller W.E., Koch S., Eckert A., Hartmann H., and Scheuer K. β-Amyloid peptide decreases membrane fluidity. Brain Res. 674 (1995) 133-136
33. Nagai Y. Functional roles of gangliosides in bio-signaling. Behav. Brain Res. 66 (1995) 99-104
34. 15N NMR of oriented lipid bilayer bound gramicidin A'. Biochemistry 26 (1987) 6621-6626
35. Petkova A.T., Ishii Y., Balbach J.J., Antzutkin O.N., Leapman R.D., Delaglio F., and Tycko R. A structural model for Alzheimer's β-amyloid fibrils based on experimental constraints from solid-state NMR. Proc. Natl. Acad. Sci. USA 99 (2002) 16742-16747
36. Petkova A.T., Yau W.M., and Tycko R. Experimental constraints on quaternary structure in Alzheimer's β-amyloid fibrils. Biochemistry 45 (2006) 498-512
37. Ramamoorthy A., Thennarasu S., Lee D.K., Tan A.M., and Maloy L. Solid-state NMR investigation of the membrane-disrupting mechanism of antimicrobial peptides MSI-78 and MSI-594 derived from magainin 2 and melittin. Biophys. J. 91 (2006) 206-216
38. Ramamoorthy A., Thennarasu S., Tan A., Lee D.K., Clayberger C., and Krensky A.M. Cell selectivity correlates with membrane-specific interactions: a case study on the antimicrobial peptide G15 derived from granulysin. Biochim. Biophys. Acta 1758 (2006) 154-163
39. 13C NMR. Magn. Reson. Chem. 24 (1986) 835-852
40. Santos J.S., Lee D.K., and Ramamoorthy A. Effects of antidepressants on the conformation of phospholipid headgroups studied by solid-state NMR. Magn. Reson. Chem. 42 (2004) 105-114
41. II phase transitions. Biophys. J. 49 (1986) 1155-1170
42. Siegel D.P., and Epand R.M. The mechanism of lamellar-to-inverted hexagonal phase transitions in phosphatidylethanolamine: implications for membrane fusion mechanisms. Biophys. J. 73 (1997) 3089-3111
43. Smith I.C.P., and Ekiel I.H. Phosphorus-31 NMR (1984), Academic Press
44. 31P NMR study. FEBS Lett. 91 (1978) 109-112
45. Thayer A.M., and Kohler S.J. Phosphorus-31 nuclear magnetic resonance spectra characteristic of hexagonal and isotropic phospholipid phases generated from phosphatidylethanolamine in the bilayer phase. Biochemistry 20 (1981) 6831-6834
46. Williamson M.P., Suzuki Y., Bourne N.T., and Asakura T. Binding of amyloid β-peptide to ganglioside micelles is dependent on histidine-13. Biochem. J. 397 (2006) 483-490
47. Yanagisawa K., and Ihara Y. GM1 ganglioside-bound amyloid β-protein in Alzheimer's disease brain. Neurobiol. Aging 19 (1998) S65-67
48. Yanagisawa K., Odaka A., Suzuki N., and Ihara Y. GM1 ganglioside-bound amyloid β-protein (Aβ): a possible form of preamyloid in Alzheimer's disease. Nat. Med. 1 (1995) 1062-1066