α-Synuclein misfolding assessed with single molecule AFM force spectroscopy: Effect of pathogenic mutations

Biochemistry

Volumn 52, Issue 42, 2013, Pages 7377-7386

  Krasnoslobodtsev, Alexey V ^a   Volkov, Ivan L ^a,c   Asiago, Josephat M ^b   Hindupur, Jagadish ^b   Rochet, Jean Christophe ^b   Lyubchenko, Yuri L ^a  

^a UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^b PURDUE UNIVERSITY   (United States)

^c ST PETERSBURG STATE UNIVERSITY   (Russian Federation)

Author keywords

[No Author keywords available]

Indexed keywords

MOLECULES; NEURODEGENERATIVE DISEASES; PROTEINS;

DIMER DISSOCIATION; FORCE SPECTROSCOPY; INTERACTION PATTERN; MOLECULAR MECHANISM; PARKINSON'S DISEASE; PATHOGENIC MUTATION; SINGLE-POINT MUTATION; STRUCTURAL DETAILS;

DIMERS;

ALPHA SYNUCLEIN; DIMER;

ARTICLE; ATOMIC FORCE MICROSCOPY; CONTROLLED STUDY; CORRELATION ANALYSIS; DIMERIZATION; HUMAN; PH; POINT MUTATION; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN ASSEMBLY; PROTEIN FOLDING; PROTEIN INTERACTION; PROTEIN STRUCTURE; SINGLE MOLECULE FORCE SPECTROSCOPY; SPECTROSCOPY;

EID: 84886777232     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi401037z     Document Type: Article

References (55)

1. Bisaglia, M., Mammi, S., and Bubacco, L. (2009) Structural insights on physiological functions and pathological effects of alpha-synuclein FASEB J. 23, 329-340
2. Weinreb, P. H., Zhen, W., Poon, A. W., Conway, K. A., and Lansbury, P. T., Jr. (1996) NACP, a protein implicated in Alzheimer's disease and learning, is natively unfolded Biochemistry 35, 13709-13715
3. Eliezer, D., Kutluay, E., Bussell, R., Jr., and Browne, G. (2001) Conformational properties of alpha-synuclein in its free and lipid-associated states J. Mol. Biol. 307, 1061-1073
4. Conway, K. A., Harper, J. D., and Lansbury, P. T., Jr. (2000) Fibrils formed in vitro from alpha-synuclein and two mutant forms linked to Parkinson's disease are typical amyloid Biochemistry 39, 2552-2563
5. Iwai, A., Yoshimoto, M., Masliah, E., and Saitoh, T. (1995) Non-A beta component of Alzheimer's disease amyloid (NAC) is amyloidogenic Biochemistry 34, 10139-10145
6. Spillantini, M. G., Schmidt, M. L., Lee, V. M. Y., Trojanowski, J. Q., Jakes, R., and Goedert, M. (1997) [alpha]-Synuclein in Lewy bodies Nature 388, 839-840
7. Baba, M., Nakajo, S., Tu, P. H., Tomita, T., Nakaya, K., Lee, V. M., Trojanowski, J. Q., and Iwatsubo, T. (1998) Aggregation of alpha-synuclein in Lewy bodies of sporadic Parkinson's disease and dementia with Lewy bodies Am. J. Pathol. 152, 879-884
8. McClendon, S., Rospigliosi, C. C., and Eliezer, D. (2009) Charge neutralization and collapse of the C-terminal tail of alpha-synuclein at low pH Protein Sci. 18, 1531-1540
9. Uversky, V. N., Li, J., and Fink, A. L. (2001) Evidence for a partially folded intermediate in alpha-synuclein fibril formation J. Biol. Chem. 276, 10737-10744
10. Kruger, R., Kuhn, W., Muller, T., Woitalla, D., Graeber, M., Kosel, S., Przuntek, H., Epplen, J. T., Schols, L., and Riess, O. (1998) Ala30Pro mutation in the gene encoding alpha-synuclein in Parkinson's disease Nat. Genet. 18, 106-108
11. Polymeropoulos, M. H., Lavedan, C., Leroy, E., Ide, S. E., Dehejia, A., Dutra, A., Pike, B., Root, H., Rubenstein, J., Boyer, R., Stenroos, E. S., Chandrasekharappa, S., Athanassiadou, A., Papapetropoulos, T., Johnson, W. G., Lazzarini, A. M., Duvoisin, R. C., Di Iorio, G., Golbe, L. I., and Nussbaum, R. L. (1997) Mutation in the α-synuclein gene identified in families with Parkinson's disease Science 276, 2045-2047
12. Zarranz, J. J., Alegre, J., Gómez-Esteban, J. C., Lezcano, E., Ros, R., Ampuero, I., Vidal, L., Hoenicka, J., Rodriguez, O., Atarés, B., Llorens, V., Tortosa, E. G., del Ser, T., Muñoz, D. G., and de Yebenes, J. G. (2004) The new mutation, E46K, of α-synuclein causes parkinson and Lewy body dementia Ann. Neurol. 55, 164-173
13. Uversky, V. N., Li, J., and Fink, A. L. (2001) Metal-triggered structural transformations, aggregation, and fibrillation of human alpha-synuclein. A possible molecular link between Parkinson's disease and heavy metal exposure J. Biol. Chem. 276, 44284-44296
14. Krasnoslobodtsev, A. V., Peng, J., Asiago, J. M., Hindupur, J., Rochet, J. C., and Lyubchenko, Y. L. (2012) Effect of spermidine on misfolding and interactions of alpha-synuclein PLoS One 7, e38099
15. Greenbaum, E. A., Graves, C. L., Mishizen-Eberz, A. J., Lupoli, M. A., Lynch, D. R., Englander, S. W., Axelsen, P. H., and Giasson, B. I. (2005) The E46K mutation in alpha-synuclein increases amyloid fibril formation J. Biol. Chem. 280, 7800-7807
16. Conway, K. A., Harper, J. D., and Lansbury, P. T. (1998) Accelerated in vitro fibril formation by a mutant alpha-synuclein linked to early-onset Parkinson disease Nat. Med. 4, 1318-1320
17. Conway, K. A., Lee, S. J., Rochet, J. C., Ding, T. T., Williamson, R. E., and Lansbury, P. T., Jr. (2000) Acceleration of oligomerization, not fibrillization, is a shared property of both alpha-synuclein mutations linked to early-onset Parkinson's disease: implications for pathogenesis and therapy Proc. Natl. Acad. Sci. U.S.A. 97, 571-576
18. Li, J., Uversky, V. N., and Fink, A. L. (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
19. Mukhopadhyay, S., Krishnan, R., Lemke, E. A., Lindquist, S., and Deniz, A. A. (2007) A natively unfolded yeast prion monomer adopts an ensemble of collapsed and rapidly fluctuating structures Proc. Natl. Acad. Sci. U.S.A. 104, 2649-2654
20. Ahmad, B., Chen, Y., and Lapidus, L. J. (2012) Aggregation of alpha-synuclein is kinetically controlled by intramolecular diffusion Proc. Natl. Acad. Sci. U.S.A. 109, 2336-2341
21. Ahmad, B. and Lapidus, L. J. (2012) Curcumin prevents aggregation in alpha-synuclein by increasing reconfiguration rate J. Biol. Chem. 287, 9193-9199
22. Lapidus, L. J. (2013) Understanding protein aggregation from the view of monomer dynamics Mol. Biosyst. 9, 29-35
23. Rubinstein, A., Lyubchenko, Y. L., and Sherman, S. (2009) Dynamic properties of pH-dependent structural organization of the amyloidogenic beta-protein (1-40) Prion 3, 31-43
24. Huang, A. and Stultz, C. M. (2009) Finding order within disorder: elucidating the structure of proteins associated with neurodegenerative disease Future Med. Chem. 1, 467-482
25. Ullman, O., Fisher, C. K., and Stultz, C. M. (2011) Explaining the structural plasticity of alpha-synuclein J. Am. Chem. Soc. 133, 19536-19546
26. Uversky, V. N. (2003) A protein-chameleon: conformational plasticity of alpha-synuclein, a disordered protein involved in neurodegenerative disorders J. Biomol. Struct. Dyn. 21, 211-234
27. Brucale, M., Sandal, M., Di Maio, S., Rampioni, A., Tessari, I., Tosatto, L., Bisaglia, M., Bubacco, L., and Samori, B. (2009) Pathogenic mutations shift the equilibria of alpha-synuclein single molecules towards structured conformers ChemBioChem 10, 176-183
28. Sandal, M., Valle, F., Tessari, I., Mammi, S., Bergantino, E., Musiani, F., Brucale, M., Bubacco, L., and Samori, B. (2008) Conformational equilibria in monomeric alpha-synuclein at the single-molecule level PLoS Biol. 6, e6
29. Lyubchenko, Y. L., Kim, B. H., Krasnoslobodtsev, A. V., and Yu, J. (2010) Nanoimaging for protein misfolding diseases Wiley Interdiscip. Rev. Nanomed. Nanobiotechnol 2, 526-543
30. Kransnoslobodtsev, A. V., Shlyakhtenko, L. S., Ukraintsev, E., Zaikova, T. O., Keana, J. F., and Lyubchenko, Y. L. (2005) Nanomedicine and protein misfolding diseases Nanomedicine 1, 300-305
31. Rochet, J.-C. and Lansbury, P. T., Jr. (2000) Amyloid fibrillogenesis: themes and variations Curr. Opin. Struct. Biol. 10, 60-68
32. Rief, M., Gautel, M., Oesterhelt, F., Fernandez, J. M., and Gaub, H. E. (1997) Reversible unfolding of individual titin immunoglobulin domains by AFM Science 276, 1109-1112
33. Tskhovrebova, L., Trinick, J., Sleep, J. A., and Simmons, R. M. (1997) Elasticity and unfolding of single molecules of the giant muscle protein titin Nature 387, 308-312
34. Stirnemann, G., Giganti, D., Fernandez, J. M., and Berne, B. J. (2013) Elasticity, structure, and relaxation of extended proteins under force Proc. Natl. Acad. Sci. U.S.A. 110, 3847-3852
35. Sarkar, A., Caamano, S., and Fernandez, J. M. (2007) The mechanical fingerprint of a parallel polyprotein dimer Biophys. J. 92, L36-38
36. Oesterhelt, F., Oesterhelt, D., Pfeiffer, M., Engel, A., Gaub, H. E., and Müller, D. J. (2000) Unfolding pathways of individual bacteriorhodopsins Science 288, 143-146
37. Yu, J., Malkova, S., and Lyubchenko, Y. L. (2008) alpha-Synuclein misfolding: single molecule AFM force spectroscopy study J. Mol. Biol. 384, 992-1001
38. Yang, G., Cecconi, C., Baase, W. A., Vetter, I. R., Breyer, W. A., Haack, J. A., Matthews, B. W., Dahlquist, F. W., and Bustamante, C. (2000) Solid-state synthesis and mechanical unfolding of polymers of T4 lysozyme Proc. Natl. Acad. Sci. U.S.A. 97, 139-144
39. El-Agnaf, O. M., Bodles, A. M., Guthrie, D. J., Harriott, P., and Irvine, G. B. (1998) The N-terminal region of non-A beta component of Alzheimer's disease amyloid is responsible for its tendency to assume beta-sheet and aggregate to form fibrils Eur. J. Biochem. 258, 157-163
40. Yu, J., Warnke, J., and Lyubchenko, Y. L. (2011) Nanoprobing of alpha-synuclein misfolding and aggregation with atomic force microscopy Nanomed.: Nanotechnol., Biol., Med. 7, 146-152
41. McAllister, C., Karymov, M. A., Kawano, Y., Lushnikov, A. Y., Mikheikin, A., Uversky, V. N., and Lyubchenko, Y. L. (2005) Protein interactions and misfolding analyzed by AFM force spectroscopy J. Mol. Biol. 354, 1028-1042
42. Bernstein, S. L., Liu, D., Wyttenbach, T., Bowers, M. T., Lee, J. C., Gray, H. B., and Winkler, J. R. (2004) α-Synuclein: stable compact and extended monomeric structures and pH dependence of dimer formation J. Am. Soc. Mass Spectrom. 15, 1435-1443
43. Trexler, A. J. and Rhoades, E. (2010) Single molecule characterization of alpha-synuclein in aggregation-prone states Biophys. J. 99, 3048-3055
44. Wu, K. P., Weinstock, D. S., Narayanan, C., Levy, R. M., and Baum, J. (2009) Structural reorganization of alpha-synuclein at low pH observed by NMR and REMD simulations J. Mol. Biol. 391, 784-796
45. Hoyer, W., Antony, T., Cherny, D., Heim, G., Jovin, T. M., and Subramaniam, V. (2002) Dependence of alpha-synuclein aggregate morphology on solution conditions J. Mol. Biol. 322, 383-393
46. Kim, B. H., Palermo, N. Y., Lovas, S., Zaikova, T., Keana, J. F., and Lyubchenko, Y. L. (2011) Single-molecule atomic force microscopy force spectroscopy study of Abeta-40 interactions Biochemistry 50, 5154-5162
47. Comellas, G., Lemkau, L. R., Nieuwkoop, A. J., Kloepper, K. D., Ladror, D. T., Ebisu, R., Woods, W. S., Lipton, A. S., George, J. M., and Rienstra, C. M. (2011) Structured regions of α-synuclein fibrils include the early-onset Parkinson's disease mutation sites J. Mol. Biol. 411, 881-895
48. Heise, H., Celej, M. S., Becker, S., Riedel, D., Pelah, A., Kumar, A., Jovin, T. M., and Baldus, M. (2008) Solid-state NMR reveals structural differences between fibrils of wild-type and disease-related A53T mutant alpha-synuclein J. Mol. Biol. 380, 444-450
49. Giasson, B. I., Murray, I. V., Trojanowski, J. Q., and Lee, V. M. (2001) A hydrophobic stretch of 12 amino acid residues in the middle of alpha-synuclein is essential for filament assembly J. Biol. Chem. 276, 2380-2386
50. Rospigliosi, C. C., McClendon, S., Schmid, A. W., Ramlall, T. F., Barre, P., Lashuel, H. A., and Eliezer, D. (2009) E46K Parkinson's-linked mutation enhances C-terminal-to-N-terminal contacts in alpha-synuclein J. Mol. Biol. 388, 1022-1032
51. Cho, M.-K., Nodet, G., Kim, H.-Y., Jensen, M. R., Bernado, P., Fernandez, C. O., Becker, S., Blackledge, M., and Zweckstetter, M. (2009) Structural characterization of α-synuclein in an aggregation prone state Protein Sci. 18, 1840-1846
52. Fernandez, C. O., Hoyer, W., Zweckstetter, M., Jares-Erijman, E. A., Subramaniam, V., Griesinger, C., and Jovin, T. M. (2004) NMR of alpha-synuclein-polyamine complexes elucidates the mechanism and kinetics of induced aggregation EMBO J. 23, 2039-2046
53. Choi, W., Zibaee, S., Jakes, R., Serpell, L. C., Davletov, B., Crowther, R. A., and Goedert, M. (2004) Mutation E46K increases phospholipid binding and assembly into filaments of human alpha-synuclein FEBS Lett. 576, 363-368
54. Chen, M., Margittai, M., Chen, J., and Langen, R. (2007) Investigation of alpha-synuclein fibril structure by site-directed spin labeling J. Biol. Chem. 282, 24970-24979
55. Vilar, M., Chou, H. T., Luhrs, T., Maji, S. K., Riek-Loher, D., Verel, R., Manning, G., Stahlberg, H., and Riek, R. (2008) The fold of alpha-synuclein fibrils Proc. Natl. Acad. Sci. U.S.A. 105, 8637-8642