Binding, Conformational Transition and Dimerization of Amyloid-β Peptide on GM1-Containing Ternary Membrane: Insights from Molecular Dynamics Simulation

PLoS ONE

Volumn 8, Issue 8, 2013, Pages

  Manna, Moutusi ^a,b   Mukhopadhyay, Chaitali ^a  

^a UNIVERSITY OF CALCUTTA   (India)

^b TAMPERE UNIVERSITY OF TECHNOLOGY   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID BETA PROTEIN[1-42]; GANGLIOSIDE GM1;

ALZHEIMER DISEASE; ARTICLE; BETA SHEET; BINDING AFFINITY; BINDING SITE; CELL MEMBRANE; DIMERIZATION; HYDROGEN BOND; LIPID BILAYER; LIPID COMPOSITION; MOLECULAR DYNAMICS; OLIGOMERIZATION; PROTEIN AGGREGATION; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN LIPID INTERACTION; PROTEIN PROTEIN INTERACTION; PROTEIN SECONDARY STRUCTURE;

EID: 84881230154     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0071308     Document Type: Article

References (74)

1. Iwatsubo T, Odaka A, Suzuki N, Mizusawa H, Nukina N, et al. (1994) Visualization of Aβ42(43) and Aβ40 in senile plaques with end-specific Aβ monoclonals: evidence that an initially deposited species is Aβ42(43). Neuron 13: 45-53.
2. Jarrett JT, Berger EP, Lansbury PT Jr, (1993) The carboxy terminus of the β amyloid protein is critical for the seeding of amyloid formation: implications for the pathogenesis of Alzheimer's disease. Biochemistry 32: 4693-4697.
3. Kirkitadze MD, Bitan G, Teplow DB, (2002) Paradigm shifts in Alzheimer's disease and other neurodegenerative disorders: the emerging role of oligomeric assemblies. J Neurosci Res 69: 567-577.
4. Walsh DM, Klyubin I, Fadeeva JV, Cullen WK, Anwyl R, et al. (2002) Naturally secreted oligomers of amyloid β protein potently inhibit hippocampal long-term potentiation in vivo. Nature 416: 535-539.
5. Ahmed M, Davis J, Aucoin D, Sato T, Ahuja S, et al. (2010) Structural conversion of neurotoxic amyloid-β1-42 oligomers to fibrils. Nat Struct Mol Biol 17: 561-567.
6. Luhrs T, Ritter C, Adrian M, Riek-Loher D, Bohrmann B, et al. (2005) 3D structure of Alzheimer's amyloid-β(1-42) fibrils. Proc Natl Acad Sci U S A 102: 17342-17347.
7. Laganowsky A, Liu C, Sawaya MR, Whitelegge JP, Park J, et al. (2012) Atomic view of a toxic amyloid small oligomer. Science 335: 1228-1231.
8. Zhu X, Bora RP, Barman A, Singh R, Prabhakar R, (2012) Dimerization of the full-length Alzheimer amyloid β-peptide (Aβ42) in explicit aqueous solution: a molecular dynamics study. J Phys Chem B 116: 4405-4416.
9. Rushworth JV, Hooper NM (2011) Lipid rafts: linking Alzheimer's amyloid-β production, aggregation, and toxicity at neuronal membranes. International J Alzheimer's Disease, volume 2011, Article ID 603052, 14 pages, doi:10.4061/2011/603052.
10. Matsuzaki K, (2007) Physicochemical interactions of amyloid β-peptide with lipid bilayers. Biochim Biophys Acta 1768: 1935-1942.
11. Sciacca MF, Kotler SA, Brender JR, Chen J, Lee DK, et al. (2012) Two-step mechanism of membrane disruption by Aβ through membrane fragmentation and pore formation. Biophys J 103: 702-710.
12. Kagan BL, Thundimadathil J, (2010) Amyloid peptide pores and the beta sheet conformation. Adv Exp Med Biol 677: 150-167.
13. Jang H, Zheng J, Nussinov R, (2007) Models of β-Amyloid ion channels in the membrane suggest that channel formation in the bilayer is a dynamic process. Biophys J 93: 1938-1949.
14. Chang Z, Luo Y, Zhang Y, Wei G, (2011) Interactions of Aβ25-35 β-barrel-like oligomers with anionic lipid bilayer and resulting membrane leakage: an all-atom molecular dynamics study. J Phys Chem B 115: 1165-1174.
15. Nikolic A, Baud S, Rauscher S, Pomès R, (2011) Molecular mechanism of β-sheet self-organization at water-hydrophobic interfaces. Proteins 79: 1-22.
16. Nagai Y, (1995) Functional role of gangliosides in bio-signaling. Behav Brain Res 66: 99-104.
17. Yanagisawa K, Odaka A, Suzuki N, Ihara Y, (1995) GM1 ganglioside-bound amyloidβ-protein (Aβ): a possible form of preamyloid in Alzheimer's disease. Nat Med 1: 1062-1066.
18. Yagi-Utsumi M, Matsuo K, Yanagisawa K, Gekko K, Kato K (2011) Spectroscopic characterization of inter-molecular interaction of amyloid β promoted on GM1 micelles. Int J Alzheimer's Disease 2011, 8 pages (doi:10.4061/2011/925073).
19. Mikhalyov I, Olofsson A, Gröbner G, Johansson LBA, (2010) Designed flurescent probes reveals interactions between amyloid-β(1-40) peptides and GM1 ganglioside in micelles and lipids vesicles. Biophys J 99: 1510-1519.
20. Kakio A, Nishimoto S, Yanagisawa K, Kozutsumi Y, 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.
21. Matsuzaki K, Horikiri C, (1999) Interactions of amyloid β-Peptide (1-40) with ganglioside-containing membranes. Biochemistry 38: 4137-4142.
22. Chi EY, Frey SL, Lee KYC, (2007) Ganglioside GM1-mediated amyloid-beta fibrillogenesis and membrane disruption. Biochemistry 46: 1913-1924.
23. Lemkul JA, Bevan DR, (2011) Lipid composition influences the release of Alzheimer's amyloid β-peptide from membranes. Protein Sci 20: 1530-1545.
24. Fukunaga S, Ueno H, Yamaguchi T, Yano Y, Hoshino M, (2012) GM1 cluster mediates formation of toxic Aβ fibrils by providing hydrophobic environments. Biochemistry 51: 8125-8131.
25. Manna M, Mukhopadhyay C, (2009) Cause and effect of melittin-induced pore formation: a computational approach. Langmuir 25: 12235-12242.
26. Niemelä PS, Ollila S, Hyvönen MT, Karttunen M, Vattulainen I, (2007) Assessing the nature of lipid raft membranes. PLoS Comput Biol 3: e34 doi:10.1371/journal. pcbi.0030034.
27. Wei G, Jewett AI, Shea JE, (2011) Structural diversity of dimers of Alzheimer amyloid-β(25-35) peptide and polymorphism of resulting fibrils. Phys Chem Chem Phys 12: 3622-3629.
28. Jang S, Shin S, (2006) Amyloid β-peptide oligomerization in silico: dimers and trimers. J Phys Chem B Lett 110: 1955-1958.
29. Kittner M, Knecht V, (2010) Disordered versus fibril-like amyloid β (25-35) dimers in water: structure and thermodynamics. J Phys Chem B 114: 15288-15295.
30. Barz B, Urbanc B, (2012) Dimer formation enhances structural differences between amyloid β-protein (1-40) and (1-42): an explicit-solvent molecular dynamics study. PLoS One 7: e34345 Doi:10.1371/journal.pone.0034345.
31. Baftizadeh F, Biarnes X, Pietrucci F, Affinito F, Laio A, (2012) Multidimensional view of amyloid fibril nucleation in atomistic details. J Am Chem Soc 134: 3886-3894.
32. Davis CH, Berkowitz ML, (2010) A molecular dynamics study of the early stages of amyloid-β(1-42) oligomerization: the role of lipid membranes. Proteins 78: 2533-2545.
33. Zhao LN, Chiu S-W, Benoit J, Chew LY, Mu Y, (2011) Amyloid β peptides aggregation in a mixed membrane bilayer: a molecular dynamics study. J Phys Chem B 115: 12247-12256.
34. Strodel B, Lee JWL, Whittleston CS, Wales DJ, (2010) Transmembrane structures for Alzheimer's Aβ1-42 oligomers. J Am Chem Soc 132: 13300-13312.
35. Tofoleanu F, Buchete N-V, (2012) Molecular interactions of Alzheimer's Aβ protofilaments with lipid membranes. J Mol Biol 421: 572-586.
36. Jang H, Connelly L, Arce FT, Ramachandran S, Kagan BL, et al. (2013) Mechanisms for the insertion of toxic, fibril-like β-amyloid oligomers into the membrane. J Chem Theory Comput 9: 822-833.
37. Wang Q, Zhao C, Zhao J, Wang J, Yang J-C, et al. (2010) Comparative molecular dynamics study of Aβ adsorption on the self-assembled monolayers. Langmuir 26: 3308-3316.
38. Manna M, Mukhopadhyay C, (2011) Cholesterol driven alteration of the conformation and dynamics of phospholamban in model membranes. Phys Chem Chem Phys 13: 20188-20198.
39. Alberts B, Johnson A, Lewis J, Raff M, Roberts K, et al. (2002) Molecular biology of the cell, 4th ed., Garland Science, Taylor & Francis Group, New York, NY.
40. Mondal S, Mukhopadhyay C, (2008) Molecular level investigation of organization in ternary lipid bilayer: a computational approach. Langmuir 24: 10298-10305.
41. Tomaselli S, Esposito V, Vangone P, van Nuland NAJ, Bonvin AMJJ, et al. (2006) The α-to-β conformational transition of Alzheimer's Aβ-(1-42) peptide in aqueous media is reversible: a step by step conformational analysis suggests the location of beta conformation seeding. Chem Bio Chem 7: 257-267.
42. Ma B, Nussinov R, (2002) Stabilities and conformations of Alzheimer's β-amyloid peptide oligomers (Aβ16-22, Aβ16-35, and Aβ10-35): sequence effects. Proc Natl Acad Sci U S A 99: 14126-14131.
43. Lindahl E, Hess B, van der Spoel D, (2001) GROMACS 3.0: a package for molecular simulation and trajectory analysis. J Mol Model 7: 306-317.
44. Berendsen HJC, van der Spoel D, van Drunen R, (1995) GROMACS: A message-passing parallel molecular dynamics implementation. Comput Phys Commun 91: 43-56.
45. Van Gunsteren WF, Berendsen HJC (1987) Gromos-87 manual; Biomos BV: Nijenborgh 4, 9747 AG Groningen, The Netherlands.
46. Berger O, Edholm O, Jähnig F, (1997) Molecular dynamics simulations of a fluid bilayer of dipalmitoylphosphatidylcholine at full hydration, constant pressure, and constant temperature. Biophys J 72: 2002-2013.
47. Manna M, Mukhopadhyay C, (2011) Molecular dynamics simulations of the interactions of kinin peptides with an anionic POPG bilayer. Langmuir 27: 3713-3722.
48. Polyansky AA, Volynsky PE, Nolde DE, Arseniev AS, Efremov RG, (2005) Role of lipid charge in organization of water/lipid bilayer interface: insights via computer simulations. J Phys Chem B 109: 15052-15059.
49. Höltje M, Förster T, Brandt B, Engels T, von Rybinski W, et al. (2001) Molecular dynamics simulations of stratum corneum lipid models: fatty acids and cholesterol. Biochim Biophys Acta 1511: 156-167.
50. Olsen BN, Schlesinger PH, Baker NA, (2009) Perturbations of membrane structure by cholesterol and cholesterol derivatives are determined by sterol orientation. J Am Chem Soc 131: 4854-4865.
51. Jedlovszky P, Sega M, Vallauri R, (2009) GM1 ganglioside embedded in a hydrated DOPC membrane: a molecular dynamics simulation study. J Phys Chem B 113: 4876-4886.
52. Ryckaert JP, Bellemans A, (1975) Molecular dynamics of liquid n-butane near its boiling point. Chem Phys Lett 30: 123-125.
53. Berendsen HJC, Postma JPM, van Gunsteren WF, Hermans J (1981) Interaction models for water in relation to protein hydration. Intermolecular Forces, B. Pullman, Ed., Reidel, Dordrecht, The Netherlands 331-342.
54. Berendsen HJC, Postma JPM, van Gunsteren WF, DiNola A, Haak JR, (1984) Molecular dynamics with coupling to an external bath. J Chem Phys 81: 3684-3690.
55. Essmann U, Perera L, Berkowitz ML, Darden T, Lee H, et al. (1995) A smooth particle mesh Ewald method. J Chem Phys 103: 8577-8593.
56. Hess B, Bekker H, Berendsen HJC, Fraaije JGE, (1997) LINCS: a linear constraint solver for molecular simulations. J Comput Chem 18: 1463-1472.
57. Humphrey W, Dalke A, Schulten K, (1996) VMD: visual molecular dynamics. J Mol Graphics 14: 33-38.
58. DeLano WL (2002) The PyMOL molecular graphics system. DeLano Scientific, San Carlos, CA.
59. Yagi-Utsumi M, Kameda T, Yamaguchi Y, Kato K, (2010) NMR characterization of the interactions between lyso-GM1 aqueous micelles. FEBS Letts 584: 831-836.
60. Lemkul JA, Bevan DR, (2009) Perturbation of membranes by the amyloid β-peptide- a molecular dynamics study. FEBS J 276: 3060-3075.
61. Fantini J, Yahi N, (2010) Molecular insights into amyloid regulation by membrane cholesterol and sphingolipids: common mechanisms in neurodegenerative diseases. Expert Rev Mol Medicine 12: e27.
62. Williamson MP, Suzuki Y, Bourne NT, Asakura T, (2006) Binding of amyloid β-peptide to ganglioside micelles is dependent on histidine-13. Biochem J 397: 483-490.
63. Yahi N, Aulas A, Fantini J, (2010) How cholesterol constrains glycolipid conformation for optimal recognition of Alzheimer's β amyloid peptide (Aβ1-40). PLoS One 5: e9079.
64. Yu X, Zheng J, (2012) Cholesterol promotes the interaction of Alzheimer β-amyloid monomer with lipid bilayer. J Mol Biol 421: 561-571.
65. Qiu L, Buie C, Reay A, Vaughn MW, Cheng KH, (2011) Molecular dynamics simulations reveal the protective role of cholesterol in β-amyloid protein-induced membrane disruptions in neuronal membrane mimics. J Phys Chem B 115: 9795-9812.
66. Davis CH, Berkowitz ML, (2009) Structure of the amyloid-β (1-42) monomer absorbed to model phospholipid bilayers: a molecular dynamics study. J Phys Chem B 113: 14480-14486.
67. Kabsch W, Sander C, (1983) Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers 22: 2577-2637.
68. Choo-Smith L-P, Surewicz WK, (1997) The interaction between Alzheimer amyloid β(l-40) peptide and ganglioside GM1-containing membranes. FEBS Letts 402: 95-98.
69. Kirkitadze MD, Condron MM, Teplow DB, (2001) Identification and characterization of key kinetic intermediates in amyloid β-protein fibrillogenesis. J Mol Biol 312: 1103-1119.
70. Xue WF, Homans SW, Radfoed SE, (2008) Systematic analysis of nucleation-dependent polymerization reveals new insights into the mechanism of amyloid self-assembly. Proc Natl Acad Sci U S A 105: 8926-8931.
71. Walsh DM, Hartley DM, Kusumoto Y, Fezoui Y, Condron MM, et al. (1999) Amyloid β-protein fibrillogenesis. Structure and biological activity of protofibrillar intermediates. J Biol Chem 274: 25945-25952.
72. Tarus B, Straub JE, Thirumalai D, (2008) Structures and free-energy landscape of the wild type and mutants of the Aβ21-30 peptide are determined by an interplay between intrapeptide electrostatic and hydrophobic interactions. J Mol Biol 379: 815-829.
73. Thirumalai D, Reddy G, Straub JE, (2012) Role of water in protein aggregation and amyloid polymerization. Acc Chem Res 45: 83-92.
74. Sciarretta KL, Gordon DJ, Petkova AT, Tycko R, Meredith SC, (2005) Aβ40-Lactam (D23/K28) models a conformation highly favorable for nucleation of amyloid. Biochemistry 44: 6003-6014.