The influence of vesicle size and composition on α-synuclein structure and stability

Biophysical Journal

Volumn 96, Issue 7, 2009, Pages 2857-2870

  Kjaer, Lars ^a   Giehm, Lise ^a,b   Heimburg, Thomas ^c   Otzen, Daniel ^a,b  

^a AALBORG UNIVERSITY   (Denmark)

^b AARHUS UNIVERSITY   (Denmark)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SYNUCLEIN; ANION; LIPID;

ALPHA HELIX; ARTICLE; CELL COMPOSITION; CELL SIZE; ELECTRICITY; ELECTRON SPIN RESONANCE; HUMAN; HUMAN CELL; IONIC STRENGTH; MEMBRANE VESICLE; PH; PHYSICAL CHEMISTRY; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN STABILITY; PROTEIN STRUCTURE; CHEMICAL STRUCTURE; CHEMISTRY; DRUG EFFECT; LIPID METABOLISM; METABOLISM; OSMOLARITY; PHASE TRANSITION; PROTEIN CONFORMATION; PROTEIN DENATURATION; TEMPERATURE; THERMODYNAMICS; TRANSITION TEMPERATURE;

ALPHA-SYNUCLEIN; LIPID METABOLISM; LIPIDS; MODELS, MOLECULAR; OSMOLAR CONCENTRATION; PHASE TRANSITION; PROTEIN CONFORMATION; PROTEIN DENATURATION; PROTEIN STABILITY; TEMPERATURE; THERMODYNAMICS; TRANSITION TEMPERATURE;

EID: 67649344732     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2008.12.3940     Document Type: Article

References (64)

1. Lashuel, H. A., B. M. Petre, J. Wall, M. Simon, R. J. Nowak, et al. 2002. alpha -synuclein, especially the Parkinson's Disease-associated mutants, forms pore-like annular and tubular protofibrils. J. Mol. Biol. 322:1089-1102.
2. Volles, M. J., S. -J. Lee, J. -C. Rochet, M. D. Shtilerman, T. T. Ding, et al. 2001. Vesicle permeabilization by protofibrillar α-synuclein: Implications for the pathogenesis and treatment of Parkinson's Disease. Biochemistry. 40:7812-7819.
3. Volles, M. J., and P. T. Lansbury. 2002. Vesicle permeabilization by protofibrillar α-synuclein is sensitive to Parkinson's disease-linked mutations and occurs by a pore-like mechanism. Biochemistry. 41:4595-4602.
4. Volles, M. J., and P. T. Lansbury. 2003. Zeroing in on the pathogenic form of alpha-synuclein and its mechanism of neurotoxicity in Parkinson's Disease. Biochemistry. 42:7871-7878.
5. Danzer, K. M., D. Haasen, A. R. Karow, S. Moussaud, M. Habeck, et al. 2007. Different species of a-synuclein oligomers induce calcium influx and seeding. J. Neurosci. 27:9220-9232.
6. Cabin, D. E., K. Shimazu, D. Murphy, N. B. Cole, W. Gottschalk, et al. 2002. Synaptic vesicle depletion correlates with attenuated synaptic responses to prolonged repetitive stimulation in mice lacking alpha-synuclein. J. Neurosci. 22:8787-8807.
7. Willingham, S., T. F. Outerio, M. J. DeVit, S. L. Lindquist, and P. J. Muchowski. 2003. Yeast genes that enhance the toxicity of a mutant Huntingtin fragment or α-synuclein. Science. 302:1769-1772.
8. Cooper, A. A., A. D. Gitler, A. Cashikar, C. M. Haynes, K. J. Hill, et al. 2006. alpha-synuclein blocks ER-Golgi traffic and Rab1 rescues neuron loss in Parkinson's models. Science. 313:234-238.
9. Zhu, M., and A. L. Fink. 2003. Lipid binding inhibits alpha-synuclein fibril formation. J. Biol. Chem. 278:16873-16877.
10. Jensen, P. H., M. S. Nielsen, R. Jakes, C. G. Dotti, and M. Goedert. 1998. Binding of alpha-synuclein to brain vesicles is abolished by familial Parkinson's disease mutation. J. Biol. Chem. 273:26292-26294.
11. Perrin, R. J., W. S. Woods, D. F. Clayton, and J. M. George. 2000. Interaction of human alpha-Synuclein and Parkinson's disease variants with phospholipids. Structural analysis using site-directed mutagenesis. J. Biol. Chem. 275:34393-34398.
12. Bussell, R., and D. Eliezer. 2004. Effects of Parkinson's disease-linked mutations on the structure of lipid-associated alpha-synuclein. Biochemistry. 43:4810-4818.
13. Stöckl, M., P. Fischer, E. Wanker, and A. Herrmann. 2008. Alpha-synuclein selectively binds to anionic phospholipids embedded in liquid-disordered domains. J. Mol. Biol. 375:1394-1404.
14. Bussell, R., and D. Eliezer. 2001. Residual structure and dynamics in Parkinson's disease-associated mutants of alpha-synuclein. J. Biol. Chem. 276:45996-46003.
15. Chandra, S., G. Gallardo, R. Fernández-Chacon, O. M. Schlüter, and T. C. Südhof. 2005. α-synuclein cooperates with CSP-α in preventing neurodegeneration. Cell. 123:383-396.
16. Kim, Y. S., E. Laurine, W. Woods, and S.-J. Lee. 2006. A novel mechanism of interaction between α-synuclein and biological membranes. J. Mol. Biol. 360:386-397.
17. Bertoncini, C. W., Y.-S. Jung, C. O. Fernandez, W. Hoyer, C. Griesinger, et al. 2005. Release of long-range tertiary interactions potentiates aggregation of natively unstructured a-synuclein. Proc. Natl. Acad. Sci. USA. 102:1430-1435.
18. Ulmer, T. S., A. Bax, N. B. Cole, and R. L. Nussbaum. 2005. Structure and dynamics of micelle-bound human alpha-synuclein. J. Biol. Chem. 280:9595-9603.
19. Kubo, S.-I., V. M. Nemani, R. J. Chalkley, M. D. Anthony, N. Hattori, et al. 2005. A combinatorial code for the interaction of a-synuclein with membranes. J. Biol. Chem. 280:31664-31672.
20. Zhu, M., J. Li, and A. L. Fink. 2003. The association of alpha-synuclein with membranes affects bilayer structure, stability and fibril formation. J. Biol. Chem. 278:40186-40197.
21. Jo, E., J. McLaurin, C. M. Yip, P. St. George-Hyslop, and P. E. Faser. 2000. alpha-synuclein membrane interactions and lipid specificity. J. Biol. Chem. 275:34328-34334.
22. Broersen, K., D. van den Brink, G. Fraser, M. Goedert, and B. Davletov. 2006. Alpha-synuclein adopts an alpha-helical conformation in the presence of polyunsaturated fatty acids to hinder micelle formation. Biochemistry. 45:15610-15616.
23. Georgieva, E. R., T. F. Ramlall, P. P. Borbat, J. H. Freed, and D. Eliezer. 2008. Membrane-bound alpha-synuclein forms an extended helix: long-distance pulsed ESR measurements using vesicles, bicelles, and rodlike micelles. J. Am. Chem. Soc. 130:12856-12857.
24. Jao, C. C., B. G. Hegde, J. Chen, I. S. Haworth, and R. Langen. 2008. Structure of membrane-bound alpha-synuclein from site-directed spin labeling and computational refinement. Proc. Natl. Acad. Sci. USA. 105:19666-19671.
25. Drescher, M., G. Veldhuis, B. D. van Rooijen, S. Milikisyants, V. Subramaniam, et al. 2008. Antiparallel arrangement of the helices of vesicle-bound alpha-synuclein. J. Am. Chem. Soc. 130:7796-7797.
26. Bortolus, M., F. Tombolato, I. Tessari, M. Bisaglia, S. Mammi, et al. 2008. Broken helix in vesicle and micelle-bound alpha-synuclein: insights from site-directed spin labeling-EPR experiments and MD simulations. J. Am. Chem. Soc. 130:6690-6691.
27. Sharon, R., M. S. Goldberg, I. Bar-Josef, R. A. Betensky, J. Shen, et al. 2001. alpha-Synuclein occurs in lipid-rich high molecular weight complexes, binds fatty acids, and shows homology to the fatty acid-binding proteins. Proc. Natl. Acad. Sci. USA. 98:9110-9115.
28. Sharon, R., I. Bar-Joseph, M. P. Frosch, D. M. Walsh, J. A. Hamilton, et al. 2003. The formation of highly soluble oligomers of alpha-synuclein is regulated by fatty acids and enhanced in Parkinson's disease. Neuron. 37:583-595.
29. Davidson, W. S., A. Jonas, D. F. Clayton, and J. M. George. 1998. Stabilization of alpha-synuclein secondary structure upon binding to synthetic membranes. J. Biol. Chem. 273:9443-9449.
30. Ramakrishnan, M., P. H. Jensen, and D. Marsh. 2003. Alpha-synuclein association with phosphatidylglycerol probed by lipid spin label. Biochemistry. 42:12919-12926.
31. Madine, J., J. Hughes, A. J. Doig, and D. A. Middleton. 2008. The effects of alpha-synuclein on phospholipid vesicle integrity: a study using 31P NMR and electron microscopy. Mol. Membr. Biol. 25:518-527.
32. Giannakis, E., J. Pacifico, D. P. Smith, L. W. Hung, C. L. Masters, et al. 2008. Dimeric structures of alpha-synuclein bind preferentially to lipid membranes. Biochim. Biophys. Acta. 1778:1112-1119.
33. Bussell, R., T. F. Ramlall, and D. Eliezer. 2005. Helix periodicity, topology, and dynamics of membrane-associated alpha-synuclein. Protein Sci. 14:862-872.
34. Bisaglia, M., I. Tessari, L. Pinato, M. Bellanda, S. Giraudo, et al. 2005. A topological model of the interaction between alpha-synuclein and sodium dodecyl sulfate micelles. Biochemistry. 44:329-339.
35. Nuscher, B., F. Kamp, T. Mehnert, S. Odoy, C. Haass, et al. 2004. alpha-synuclein has a high affinity for packing defects in a bilayer membrane: a thermodynamics study. J. Biol. Chem. 279:21966-21975.
36. Kamp, F., and K. Beyer. 2005. Binding of a-synuclein affects the lipid packing in bilayers of small vesicles. J. Biol. Chem. 281:9251-9259.
37. Zakharov, S. D., J. D. Hulleman, E. A. Dutseva, Y. N. Antonenko, J.-C. R. Ochet, et al. 2007. Helical α-synuclein forms highly conductive ion channels. Biochemistry. 46:14369-14379.
38. Lindersson, E., D. Lundvig, C. Petersen, P. Madsen, P. Højrup, et al. 2005. P25a is co-expressed with a-synuclein in a-synucleinopathies and stimulates its aggregation. J. Biol. Chem. 280:5703-5715.
39. Wimmer, R., K. Andersen, B. Vad, M. Davidsen, S. Mølgaard, et al. 2006. Versatile interactions of the antimicrobial peptide Novispirin with detergents and lipids. Biochemistry. 45:481-497.
40. Schneider, M. F., D. Marsh, W. Jahn, B. Kloesgen, and T. Heimburg. 1999. Network formation of lipid membranes: triggering structural transitions by chain melting. Proc. Natl. Acad. Sci. USA. 96:14312-14317.
41. Heimburg, T. 2007. Thermal Biophysics of Membranes Wiley-VCH, Berlin.
42. White, S. H., and W. C. Wimley. 1999. Membrane protein folding and stability: physical principles. Annu. Rev. Biophys. Biomol. Struct. 28:319-365.
43. Privalov, P. L. 1990. Cold denaturation of proteins. Crit. Rev. Biochem. Mol. Biol. 25:281-305.
44. Heimburg, T., and D. Marsh. 1995. Protein surface-distribution and protein-protein interactions in the binding of peripheral proteins to charged lipid membranes. Biophys. J. 68:536-546.
45. Privalov, P. L., and G. I. Makhatadze. 1990. Heat capacity of proteins II. Partial molar heat capacity of the unfolded polypeptide chains of proteins: protein unfolding effects. J. Mol. Biol. 213:385-391.
46. Ivanova, V. P., I. Makarov, T. E. Schäffer, and T. Heimburg. 2003. Analyzing heat capacity profiles of peptide-containing membranes: cluster formation of gramicidin A. Biophys. J. 84:2427-2439.
47. Zuckermann, M. J., and T. Heimburg. 2001. Insertion and pore formation driven by adsorption of proteins onto lipid bilayer membrane-water interfaces. Biophys. J. 81:2458-2472.
48. Heimburg, T., B. Angerstein, and D. Marsh. 1999. Binding of peripheral proteins to mixed lipid membranes: the effect of local demixing upon binding. Biophys. J. 76:2575-2586.
49. Cole, N. B., D. D. Murphy, T. Grider, S. Rueter, D. Brasaemle, et al. 2002. Lipid droplet binding and oligomerization properties of the Parkinson's disease protein alpha-synuclein. J. Biol. Chem. 277:6344-6352.
50. Evans, E., and R. Kwok. 1982. Mechanical calorimetry of large dimyristoylphosphatidylcholine vesicles in the phase transition region. Biochemistry. 21:4874-4879.
51. Heimburg, T. 1998. Mechanical aspects of membrane thermodynamics. Estimation of the mechanical properties of lipid membranes close to the chain melting transition from calorimetry. Biochim. Biophys. Acta. 1415:147-162.
52. Jørgensen, K., J. H. Ipsen, O. G. Mouritsen, and M. J. Zuckermann. 1993. The effect of anaesthetics on the dynamic heterogeneity of lipid membranes. Chem. Phys. Lipids. 65:205-216.
53. Westh, P., and C. Trandum. 1999. Thermodynamics of alcohol-lipid bilayer interactions: application of a binding model. Biochim. Biophys. Acta. 1421:261-272.
54. Peter, B. J., H. M. Kent, I. G. Mills, Y. Vallis, P. J. Butler, et al. 2003. BAR domains as sensors of membrane curvature: the amphiphysin BAR structure. Science. 303:495-499.
55. Huang, H., J. M. Ball, J. T. Billheimer, and F. Schroeder. 1999. Interaction of the N-terminus of sterol carrier protein 2 with membranes: role of membrane curvature. Biochem. J. 344 Pt 2:593-603.
56. Shi, J., C. W. Heegaard, J. T. Rasmussen, and G. E. Gilbert. 2004. Lactadherin binds selectively to membranes containing phosphatidyl-L-serine and increased curvature. Biochim. Biophys. Acta. 1667:82-90.
57. Schullery, S. E., C. F. Schmidt, P. Felgner, T. W. Tillack, and T. E. Thompson. 1980. Fusion of dipalmitoylphosphatidylcholine vesicles. Biochemistry. 19:3919-3923.
58. Ivanova, V. P. 2000. Theoretical and experimental study of protein-lipid interactions. University of Göttingen.
59. Ivanova, V. P., and T. Heimburg. 2001. A histogram method to obtain heat capacities in lipid monolayers, curved bilayers and membranes containing peptides. Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 63:1914-1925.
60. Cantor, R. S. 1999. Lipid composition and the lateral pressure profile in bilayers. Biophys. J. 76:2625-2639.
61. Murphy, D. D., S. M. Rueter, J. Q. Trojanowski, and V. M. Lee. 2000. Synucleins are developmentally expressed, and alpha-synuclein regulates the size of the presynaptic vesicular pool in primary hippocampal neurons. J. Neurosci. 20:3214-3220.
62. Abeliovich, A., Y. Schmitz, D. Farinas, W. H. Choi-Lundberg, C. P. E. Ho, et al. 2000. Mice lacking alpha-synuclein display functional deficits in the nigrostriatal dopamine system. Neuron. 25:239-252.
63. Cooper, A. 2008. Neurodegeneration and protein misfolding - What's gone wrong with the cell? Australian Biochemist. 39:15-20.
64. Wojcik, S. M., and N. Brose. 2007. Regulation of membrane fusion in synaptic excitation-secretion coupling: speed and accuracy matter. Neuron. 55:11-24.