The fusogenic tilted peptide (67-78) of α-synuclein is a cholesterol binding domain

Biochimica et Biophysica Acta - Biomembranes

Volumn 1808, Issue 10, 2011, Pages 2343-2351

  Fantini, Jacques ^a   Carlus, Denis ^a   Yahi, Nouara ^a  

^a University of Mediterranée   (France)

Author keywords

Amyloid protein; Cholesterol; Glycosphingolipid; Lipid raft; Tilted peptide; Virus fusion

Indexed keywords

ALPHA SYNUCLEIN; ALPHA SYNUCLEIN[34-45]; ALPHA SYNUCLEIN[67-78]; CHOLESTEROL; GLYCOSPHINGOLIPID; SPHINGOLIPID; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; ASTROCYTE; BINDING AFFINITY; BINDING SITE; CONSENSUS SEQUENCE; CYTOTOXICITY; EBOLA VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN T CELL LEUKEMIA VIRUS 1; LIPID MONOLAYER; LIPID RAFT; MOLECULAR MODEL; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN LIPID INTERACTION; PROTEIN MOTIF; RAT; SIGNAL TRANSDUCTION; VIRUS ATTACHMENT;

ALPHA-SYNUCLEIN; ANIMALS; BINDING SITES; CELLS, CULTURED; CHOLESTEROL; HUMANS; MOLECULAR DYNAMICS SIMULATION; RATS; RECOMBINANT PROTEINS;

HUMAN T-LYMPHOTROPIC VIRUS 1;

EID: 79960453030     PISSN: 00052736     EISSN: 18792642     Source Type: Journal    
DOI: 10.1016/j.bbamem.2011.06.017     Document Type: Article

References (53)

1. P.K. Auluck, G. Caraveo, and S. Lindquist α-Synuclein: membrane interactions and toxicity in Parkinson's disease Annu. Rev. Cell Dev. Biol. 26 2010 211 233
2. V.N. Uversky α-Synuclein aggregation and Parkinson's disease V.N. Uversky, A.L. Fink, Protein Misfolding, Aggregation, and Conformational Diseases, Part B: Molecular Mechanisms of Conformational Diseases 2007 Springer New York 61 110
3. H.J. Lee, S. Patel, and S.J. Lee Intravesicular localization and exocytosis of alpha-synuclein and its aggregates J. Neurosci. 25 2005 6016 6024 (Pubitemid 40911433)
4. R. Borghi, R. Marchese, A. Negro, L. Marinelli, G. Forloni, D. Zaccheo, G. Abbruzzese, and M. Tabaton Full length alpha-synuclein is present in cerebrospinal fluid from Parkinson's disease Neurosci. Lett. 287 2000 65 67 (Pubitemid 30332379)
5. J.Y. Sung, J. Kim, S.R. Paik, J.H. Park, Y.S. Ahn, and K.C. Chung Induction of neuronal cell death by Rab5A-dependent endocytosis of alpha-synuclein J. Biol. Chem. 276 2001 27441 27448
6. J.Y. Park, K.S. Kim, S.B. Lee, J.S. Ryu, K.C. Chung, Y.K. Choo, I. Jou, and S.M. Park On the mechanism of internalizationof α-synuclein into microglia: roles of ganglioside GM1 and lipid raft J. Neurochem. 110 2009 400 411
7. S. Park, H.Y. Jung, H.O. Kim, H. Rhim, S.R. Paik, K.C. Chung, J.H. Park, and J. Kim Evidence that alpha-synuclein functions as a negative regulator of Ca(++)-dependent alpha-granule release from human platelets Blood 100 2002 2506 2514
8. K.J. Ahn, S.R. Paik, K.C. Chung, and J. Kim Amino acid sequence motifs and mechanistic features of the membrane translocation of alpha-synuclein J. Neurochem. 97 2006 265 279
9. M.J. Volles, and P.T. Lansbury Jr. Vesicle permeabilization by protofibrillar alpha-synuclein is sensitive to Parkinson's disease-linked mutations and occurs by a pore-like mechanism Biochemistry 41 2002 4595 6402
10. D.L. Fortin, M.D. Troyer, K. Nakamura, S. Kubo, M.D. Anthony, and R.H. Edwards Lipid rafts mediate the synaptic localization of alpha-synuclein J. Neurosci. 24 2004 6623 6715
11. S. Kubo, V.M. Nemani, R.J. Chalkley, M.D. Anthony, N. Hattori, Y. Mizuno, R.H. Edwards, and D.L. Fortin A combinatorial code for the interaction of alpha-synuclein with membranes J. Biol. Chem. 280 2005 31664 31672 (Pubitemid 41291913)
12. P. Zabrocki, I. Bastiaens, C. Delay, T. Bammens, R. Ghillebert, K. Pellens, C. De Virgilio, F. Van Leuven, and J. Winderickx Phosphorylation, lipid raft interaction and traffic of alpha-synuclein in a yeast model for Parkinson Biochim. Biophys. Acta 1783 2008 1767 1780
13. Z. Martinez, M. Zhu, S. Han, and A.L. Fink GM1 specifically interacts with alpha-synuclein and inhibits fibrillation Biochemistry 46 2007 1868 1877
14. J. Fantini, and N. Yahi Molecular basis for the glycosphingolipid-binding specificity of α-synuclein: key role of tyrosine 39 in membrane insertion J. Mol. Biol. 408 2011 654 669
15. J. Fantini How sphingolipids bind and shape proteins: molecular basis of lipid-protein interactions in lipid shells, rafts and related biomembrane domains Cell. Mol. Life Sci. 60 2003 1027 1032 (Pubitemid 36791909)
16. E. Di Pasquale, J. Fantini, H. Chahinian, M. Maresca, N. Taïeb, and N. Yahi Altered ion channel formation by the Parkinson's-disease-linked E46K mutant of alpha-synuclein is corrected by GM3 but not by GM1 gangliosides J. Mol. Biol. 397 2010 202 218
17. H. Asou, S. Hirano, and K. Uyemura Ganglioside composition of astrocytes Cell Struct. Funct. 14 1989 561 568 (Pubitemid 20009133)
18. S.J. Lee Origins and effects of extracellular alpha-synuclein: implications in Parkinson's disease J. Mol. Neurosci. 34 2008 17 22
19. J. Fantini, N. Garmy, R. Mahfoud, and N. Yahi Lipid rafts: structure, function and role in HIV, Alzheimer's and prion diseases Expert Rev. Mol. Med. 4 2002 1 22
20. P. Bar-On, L. Crews, A.O. Koob, H. Mizuno, A. Adame, B. Spencer, and E. Masliah Statins reduce neuronal alpha-synuclein aggregation in in vitro models of Parkinson's disease J. Neurochem. 105 2008 1656 1667 (Pubitemid 351678486)
21. A.O. Koob, K. Ubhi, J.F. Paulsson, J. Kelly, E. Rockenstein, M. Mante, A. Adame, and E. Masliah Lovastatin ameliorates alpha-synuclein accumulation and oxidation in transgenic mouse models of alpha-synucleinopathies Exp. Neurol. 221 2010 267 274
22. J. Fantini, and N. Yahi Molecular insights into amyloid regulation by membrane cholesterol and sphingolipids: common mechanisms in neurodegenerative diseases Expert Rev. Mol. Med. 12 2010 e27
23. G. Thakur, M. Micic, and R.M. Leblanc Surface chemistry of Alzheimer's disease: a Langmuir monolayer approach Colloids Surf. B Biointerfaces 74 2009 436 456
24. J.M. Crowet, L. Lins, I. Dupiereux, B. Elmoualija, A. Lorin, B. Charloteaux, V. Stroobant, E. Heinen, and R. Brasseur Tilted properties of the 67-78 fragment of alpha-synuclein are responsible for membrane destabilization and neurotoxicity Proteins 68 2007 936 947 (Pubitemid 47434715)
25. N. Jamin, J.M. Neumann, M.A. Ostuni, T.K. Vu, Z.X. Yao, S. Murail, J.C. Robert, C. Giatzakis, V. Papadopoulos, and J.J. Lacapère Characterization of the cholesterol recognition amino acid consensus sequence of the peripheral-type benzodiazepine receptor Mol. Endocrinol. 19 2005 588 594 (Pubitemid 40349433)
26. R.P. Singh, B.R. Brooks, and J.B. Klauda Binding and release of cholesterol in the Osh4 protein of yeast Proteins 75 2009 468 477
27. R. Thomsen, and M.H. Christensen MolDock: a new technique for high-accuracy molecular docking J. Med. Chem. 49 2006 3315 3321 (Pubitemid 43830529)
28. N. Yahi, A. Aulas, and J. Fantini How cholesterol constrains glycolipid conformation for optimal recognition of Alzheimer's beta amyloid peptide (Abeta1-40) PLoS One 5 2010 e9079
29. A. Seelig Local anesthetics and pressure: a comparison of dibucaine binding to lipid monolayers and bilayers Biochim. Biophys. Acta 899 1987 196 204 (Pubitemid 17086618)
30. L. Lins, M. Decaffmeyer, A. Thomas, and R. Brasseur Relationships between the orientation and the structural properties of peptides and their membrane interactions Biochim. Biophys. Acta 1778 2008 1537 1544
31. T.S. Ulmer, A. Bax, N.B. Cole, and R.L. Nussbaum Structure and dynamics of micelle-bound human alpha-synuclein J. Biol. Chem. 280 2005 9595 9603 (Pubitemid 40409655)
32. A.J. Trexler, and E. Rhoades Alpha-synuclein binds large unilamellar vesicles as an extended helix Biochemistry 48 2009 2304 2306
33. B. Ramstedt, and J.P. Slotte Interaction of cholesterol with sphingomyelins and acyl-chain-matched phosphatidylcholines: a comparative study of the effect of the chain length Biophys. J. 76 1999 908 915 (Pubitemid 29264570)
34. S.D. Zakharov, J.D. Hulleman, E.A. Dutseva, Y.N. Antonenko, J.C. Rochet, and W.A. Cramer Helical alpha-synuclein forms highly conductive ion channels Biochemistry 46 2007 14369 71439
35. A.M. Bodles, D.J. Guthrie, B. Greer, and G.B. Irvine Identification of the region of non-Abeta component (NAC) of Alzheimer's disease amyloid responsible for its aggregation and toxicity J. Neurochem. 78 2001 384 395 (Pubitemid 32664420)
36. B.L. Kagan, R. Azimov, and R. Azimova Amyloid peptide channels J. Membr. Biol. 202 2004 1 10 (Pubitemid 40298660)
37. D. Lingwood, B. Binnington, T. Róg, L. Vattulainen, M. Grzybek, U. Coskun, C.A. Lingwood, and K. Simons Cholesterol modulates glycolipid conformation and receptor activity Nat. Chem. Biol. 7 2011 260 262
38. R.M. Epand, A. Thomas, R. Brasseur, and R.F. Epand Cholesterol interaction with proteins that partition into membrane domains: an overview Subcell. Biochem. 51 2010 253 728
39. R. Brasseur, T. Pillot, L. Lins, J. Vandekerckhove, and M. Rosseneu Peptides in membranes: tipping the balance of membrane stability Trends Biochem. Sci. 22 1997 167 171 (Pubitemid 27199317)
40. B. Charloteaux, A. Lorin, R. Brasseur, and L. Lins The "Tilted Peptide Theory" links membrane insertion properties and fusogenicity of viral fusion peptides Protein Pept. Lett. 16 2009 718 725
41. C. Schroeder Cholesterol-binding viral proteins in virus entry and morphogenesis Subcell. Biochem. 51 2010 77 108
42. S.S. Rawat, M. Viard, S.A. Gallo, A. Rein, R. Blumenthal, and A. Puri Modulation of entry of enveloped viruses by cholesterol and sphingolipids (Review) Mol. Membr. Biol. 20 2003 243 254 (Pubitemid 37046249)
43. A.A. Waheed, and E.O. Freed The role of lipids in retrovirus replication Viruses 2 2010 1146 1180
44. R. Mahfoud, N. Garmy, M. Maresca, N. Yahi, A. Puigserver, and J. Fantini Identification of a common sphingolipid-binding domain in Alzheimer, prion, and HIV-1 proteins J. Biol. Chem. 2002 277 2002 11292 11296 (Pubitemid 34952893)
45. T. Pillot, M. Goethals, B. Vanloo, C. Talussot, R. Brasseur, J. Vandekerckhove, M. Rosseneu, and L. Lins Fusogenic properties of the C-terminal domain of the Alzheimer beta-amyloid peptide J. Biol. Chem. 271 1996 28757 28765 (Pubitemid 26382570)
46. T. Pillot, L. Lins, M. Goethals, B. Vanloo, J. Baert, J. Vandekerckhove, M. Rosseneu, and R. Brasseur The 118-135 peptide of the human prion protein forms amyloid fibrils and induces liposome fusion J. Mol. Biol. 274 1997 381 393 (Pubitemid 27520626)
47. W. Popik, T.M. Alce, and W.C. Au Human immunodeficiency virus type 1 uses lipid raft-colocalized CD4 and chemokine receptors for productive entry into CD4(+) T cells J. Virol. 76 2002 4709 4722 (Pubitemid 34441677)
48. M.M. Wielgosz, D.A. Rauch, K.S. Jones, F.W. Ruscetti, and L. Ratner Cholesterol dependence of HTLV-I infection AIDS Res. Hum. Retroviruses 21 2005 43 50 (Pubitemid 40179800)
49. S. Bavari, C.M. Bosio, E. Wiegand, G. Ruthel, A.B. Will, T.W. Geisbert, M. Hevey, C. Schmaljohn, A. Schmaljohn, and M.J. Aman Lipid raft microdomains: a gateway for compartmentalized trafficking of Ebola and Marburg viruses J. Exp. Med. 195 2002 593 602 (Pubitemid 34461504)
50. P.K. Chatterjee, C.H. Eng, and M. Kielian Novel mutations that control the sphingolipid and cholesterol dependence of the Semliki Forest virus fusion protein J. Virol. 2002 12712 12722 (Pubitemid 35386956)
51. N. Vincent, C. Genin, and E. Malvoisin Identification of a conserved domain of the HIV-1 transmembrane protein gp41 which interacts with cholesteryl groups Biochim. Biophys. Acta 1567 2002 157 164 (Pubitemid 35454057)
52. J. Fantini, and F. Barrantes Sphingolipid/cholesterol regulation of neurotransmitter receptor conformation and function Biochim. Biophys. Acta 1788 2009 2345 2361
53. A.S. Desplanques, H.J. Nauwynck, D. Vercauteren, T. Geens, and H.W. Favoreel Plasma membrane cholesterol is required for efficient pseudorabies virus entry Virology 376 2008 339 345