The driving force of alpha-synuclein insertion and amyloid channel formation in the plasma membrane of neural cells: Key role of ganglioside-and cholesterol-binding domains

Advances in Experimental Medicine and Biology

Volumn 991, Issue , 2013, Pages 15-26

  Fantini, Jacques ^a   Yahi, Nouara ^a  

^a Aix Marseille University   (France)

Author keywords

Alpha synuclein; Calcium channel; Cholesterol; Ganglioside; Glycosphingolipid; GM1; GM3; Langmuir monolayer; Molecular modeling simulations; OH Pi bond; Parkinson's disease; Tilted peptide; Virus fusion; Weak hydrogen bond

Indexed keywords

ALPHA SYNUCLEIN; AMYLOID; GANGLIOSIDE; GANGLIOSIDE GM3;

ARTICLE; BINDING AFFINITY; COMPLEX FORMATION; HUMAN; HYDROGEN BOND; LIPID ANALYSIS; LIPID BILAYER; LIPID RAFT; NERVE CELL MEMBRANE; NONHUMAN; PHYSICAL CHEMISTRY; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN LIPID INTERACTION; STRUCTURE ANALYSIS; VIRUS ENTRY;

EID: 84885014584     PISSN: 00652598     EISSN: None     Source Type: Book Series    
DOI: 10.1007/978-94-007-6331-9_2     Document Type: Article

References (52)

1. Li J, Uversky V, Fink AL (2001) Effect of familial Parkinson's disease point mutations A30P and A53T on the structural properties, aggregation, and fibrillation of human alpha-synuclein. Biochemistry 40:11604-11613
2. Stöckl M, Fischer P, Wanker E et al (2008) Alphasynuclein selectively binds to anionic phospholipids embedded in liquid-disordered domains. J Mol Biol 375:1394-1404
3. Kubo S, Nemani VM, Chalkley RJ et al (2005) A combinatorial code for the interaction of alpha-synuclein with membranes. J Biol Chem 280:31664-31672
4. Davidson WS, Jonas A, Clayton DF et al (1998) Stabilization of alpha-synuclein secondary structure upon binding to synthetic membranes. J Biol Chem 273:9443-9449
5. Ramakrishnan M, Jensen PH, Marsh D (2003) Alphasynuclein association with phosphatidylglycerol probed by lipid spin labels. Biochemistry 42:12919-12926
6. Martinez Z, Zhu M, Han S et al (2007) GM1 specifically interacts with alpha-synuclein and inhibitsfibrillation. Biochemistry 46:1868-1877
7. Di Pasquale E, Fantini J, Chahinian H et al (2010) 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 397:202-218
8. Fantini J, Yahi N (2011) Molecular basis for the glycosphingolipid- binding specificity of a -synuclein: key role of tyrosine 39 in membrane insertion. J Mol Biol 408:654-669
9. Fantini J, Yahi N (2010) Molecular insights into amyloid regulation by membrane cholesterol and sphingolipids: common mechanisms in neurodegenerative diseases. Expert Rev Mol Med 12:e27
10. Butterfield SM, Lashuel HA (2010) Amyloidogenic protein-membrane interactions: mechanistic insight from model systems. Angew Chem Int Ed Engl 49: 5628-5654
11. Aisenbrey C, Borowik T, Byström R et al (2008) How is protein aggregation in amyloidogenic diseases modulated by biological membranes? Eur Biophys J 37:247-255
12. Fantini J (2003) How sphingolipids bind and shape proteins: molecular basis of lipid-protein interactions in lipid shells, rafts and related biomembrane domains. Cell Mol Life Sci 60:1027-1032
13. Sarnataro D, Campana V, Paladino S et al (2004) PrP(C) association with lipid rafts in the early secretory pathway stabilizes its cellular conformation. Mol Cell Biol 15:4031-4042
14. Yanagisawa K, Odaka A, Suzuki N et al (1995) GM1 ganglioside-bound amyloid beta-protein (A beta): a possible form of preamyloid in Alzheimer's disease. Nat Med 1:1062-1066
15. Choo-Smith LP, Garzon-Rodriguez GCC et al (1997) Acceleration of amyloidfibril formation by specific binding of Abeta-(1-40) peptide to ganglioside-containing membrane vesicles. J Biol Chem 272:22987-22990
16. Okada T, Wakabayashi M, Ikeda K (2007) Formation of toxicfibrils of Alzheimer's amyloid beta-protein-(1-40) by monosialoganglioside GM1, a neuronal membrane component. J Mol Biol 371:481-489
17. Rochet JC, Lansbury PT Jr (2000) Amyloid fibrillo-genesis: themes and variations. Curr Opin Struct Biol 10:60-68
18. Quist A, Doudevski I, Lin H et al (2005) Amyloid ion channels: a common structural link for proteinmisfolding disease. Proc Natl Acad Sci USA 102: 10427-10432
19. Arispe N, Rojas E, Pollard HB (1993) Alzheimer disease amyloid beta protein forms calcium channels in bilayer membranes: blockade by tromethamine and aluminum. Proc Natl Acad Sci USA 90:567-571
20. Zakharov SD, Hulleman JD, Dutseva EA et al (2007) Helical alpha-synuclein forms highly conductive ion channels. Biochemistry 46:14369-14379
21. Arispe N, Pollard HB, Rojas E (1994) beta-Amyloid Ca(2+)-channel hypothesis for neuronal death in Alzheimer disease. Mol Cell Biochem 140:119-125
22. Stroud RM, Reiling K, Wiener M (1998) Ion-channelforming colicins. Curr Opin Struct Biol 8:525-533
23. Fantini J, Carlus D, Yahi N (2011) The fusogenic tilted peptide (67-78) of a -synuclein is a cholesterol binding domain. Biochim Biophys Acta 1808: 2343-2351
24. Waheed AA, Freed EO (2010) The role of lipids in retrovirus replication. Viruses 2:1146-1180
25. Snook CF, Jones JA, Hannun YA (2006) Sphingolipidbinding proteins. Biochim Biophys Acta 1761:927-946
26. Taïeb N, Yahi N, Fantini J (2004) Rafts and related glycosphingolipid-enriched microdomains in the intestinal epithelium: bacterial targets linked to nutrient absorption. Adv Drug Deliv Rev 56:779-794
27. Yahi N, Aulas A, Fantini J (2010) How cholesterol constrains glycolipid conformation for optimal recognition of Alzheimer's beta amyloid peptide (Abeta1-40). PLoS One 5:e9079
28. Mahfoud R, Garmy N, Maresca M et al (2002) Identification of a common sphingolipid-binding domain in Alzheimer, prion, and HIV-1 proteins. J Biol Chem 277:11292-11296
29. Fantini J, Garmy N, Yahi N (2006) Prediction of glycolipid-binding domains from the amino acid sequence of lipid raft-associated proteins: application to HpaA, a protein involved in the adhesion of Helicobacter pylori to gastrointestinal cells. Biochemistry 45:10957-10962
30. Levy M, Garmy N, Gazit E et al (2006) The minimal amyloid-forming fragment of the islet amyloid polypeptide is a glycolipid-binding domain. FEBS J 273: 5724-5735
31. Fantini J (2007) Interaction of proteins with lipid rafts through glycolipid-binding domains: biochemical background and potential therapeutic applications. Curr Med Chem 14:2911-2917
32. Chakrabandhu K, Huault S, Garmy N et al (2008) The extracellular glycosphingolipid-binding motif of Fas defines its internalization route, mode and outcome of signals upon activation by ligand. Cell Death Differ 15:1824-1837
33. Taïeb N, Maresca M, Guo XJ et al (2009) Thefirst extracellular domain of the tumour stem cell marker CD133 contains an antigenic ganglioside-binding motif. Cancer Lett 278:164-173
34. Nishio M, Umezawa Y, Hirota M et al (1995) The CH/ pi interaction: significance in molecular recognition. Tetrahedron 51:8665-8701
35. Ulmer TS, Bax A, Cole NB et al (2005) Structure and dynamics of micelle-bound human alpha-synuclein. J Biol Chem 280:9595-9603
36. Desiraju GR, Steiner T (1999) The weak hydrogen bond in structural chemistry and biology. Oxford University Press, Oxford
37. Steiner T, Koellner G (2001) Hydrogen bonds with pi-acceptors in proteins: frequencies and role in stabilizing local 3D structures. J Mol Biol 305:535-557
38. Malone JF, Murray CM, Charlton MH et al (1997) X-H [pi ] (phenyl) interactions. Theoretical and crystallographic observations. J Chem Soc Faraday Trans 93:3429-3436
39. Thakur G, Micic M, Leblanc RM (2009) Surface chemistry of Alzheimer's disease: a Langmuir monolayer approach. Colloids Surf B Biointerfaces 74:436-456
40. Williamson MP, Suzuki Y, Bourne NT et al (2006) Binding of amyloid beta-peptide to ganglioside micelles is dependent on histidine-13. Biochem J 397:483-490
41. Crowet JM, Lins L, Dupiereux I et al (2007) Tilted properties of the 67-78 fragment of alpha-synuclein are responsible for membrane destabilization and neurotoxicity. Proteins 68:936-947
42. Brasseur R, Pillot T, Lins L et al (1997) Peptides in membranes: tipping the balance of membrane stability. Trends Biochem Sci 22:167-171
43. Charloteaux B, Lorin A, Brasseur R et al (2009) The "Tilted Peptide Theory" links membrane insertion properties and fusogenicity of viral fusion peptides. Protein Pept Lett 16:718-725
44. Uversky VN, Li J, Souilac P et al (2002) Biophysical properties of the synucleins and their propensities tofibrillate. Inhibition of a -synuclein assembly by b -and g -synucleins. J Biol Chem 277:11970-11978
45. Uversky VN, Dunker AK (2010) Understanding protein non-folding. Biochim Biophys Acta 1804: 1231-1264
46. Yahi N, Sabatier JM, Baghdiguian S et al (1995) Synthetic multimeric peptides derived from the principal neutralization domain (V3 loop) of human immunodeficiency virus type 1 (HIV-1) gp120 bind to galactosylceramide and block HIV-1 infection in a human CD4-negative mucosal epithelial cell line. J Virol 69:320-325
47. Yahi N, Fantini J, Baghdiguian S et al (1995) SPC3, a synthetic peptide derived from the V3 domain of human immunodeficiency virus type 1 (HIV-1) gp120, inhibits HIV-1 entry into CD4+ and CD4-cells by two distinct mechanisms. Proc Natl Acad Sci USA 92:4867-4871
48. Hammache D, Yahi N, Maresca M et al (1999) Human erythrocyte glycosphingolipids as alternative cofactors for human immunodeficiency virus type 1 (HIV-1) entry: evidence for CD4-induced interactions between HIV-1 gp120 and reconstituted membrane microdomains of glycosphingolipids (Gb3 and GM3). J Virol 73:5244-5528
49. Fantini J, Garmy N, Mahfoud R et al (2002) Lipid rafts: structure, function and role in HIV, Alzheimer's and prion diseases. Expert Rev Mol Med 4:1-22
50. El-Agnaf OM, Salem SA, Paleologou KE et al (2003) Alpha-synuclein implicated in Parkinson's disease is present in extracellular biological fl uids, including human plasma. FASEB J 17:1945-1947
51. Park JY, Kim KS, Lee SB et al (2009) On the mechanism of internalization of alpha-synuclein into microglia: roles of ganglioside GM1 and lipid raft. J Neurochem 110:400-411
52. Gagne JJ, Power MC (2010) Anti-in fl ammatory drugs and risk of Parkinson disease: a meta-analysis. Neurology 74:995-1002