Potential of mean force and molecular dynamics study on the transient interactions between α and β synuclein that drive inhibition of α-synuclein aggregation

References

• Andrusier, N., Nussinov, R., & Wolfson, H. J. (2007). FireDock: Fast interaction refinement in molecular docking. Proteins, 69, 139–159. doi:10.1002/prot.21495
   PubMed Web of Science ®Google Scholar
• Angot, E., Steiner, J. A., LemaTome, C. M., Ekstrom, P., Mattsson, B., Bjorklund, A., & Brundin, P. (2012). α-Synuclein cell-to-cell transfer and seeding in grafted dopaminergic neurons in vivo. PLoS ONE, 7, e39465. doi:10.1371/journal.pone.0039465
   PubMed Web of Science ®Google Scholar
• Bendor, J. T., Logan, T. P., & Edwards, R. H. (2013). The function of α-synuclein. Neuron, 79, 1044–1066. doi:10.1016/j.neuron.2013.09.004
   PubMed Web of Science ®Google Scholar
• Berhanu, W. M., & Masunov, A. E. (2014). Atomistic mechanism of polyphenol amyloid aggregation inhibitors: molecular dynamics study of Curcumin, Exifone, and Myricetin interaction with the segment of tau peptide oligomer. Journal of Biomolecular Structure and Dynamics, 33, 1399–1411. doi:10.1080/07391102.2014.951689
   PubMed Web of Science ®Google Scholar
• Berman, H. M., Westbrook, J., Feng, Z., Gilliland, G., Bhat, T. N., Weissig, H., … Bourne, P. E. (2000). The protein data bank. Nucleic Acids Research, 28, 235–242. doi:10.1107/97809553602060000722
   PubMed Web of Science ®Google Scholar
• Biere, A. L., Wood, S. J., Wypych, J., Steavenson, S., Jiang, Y., Anafi, D., … Citron, M. (2000). Parkinson’s disease-associated α-synuclein is more fibrillogenic than β and γ-synuclein and cannot cross-seed its homologs. Journal of Biological Chemistry, 275, 34574–34579. doi:10.1074/jbc.m005514200
   PubMed Web of Science ®Google Scholar
• Bisaglia, M., Mammi, S., & Bubacco, L. (2009). Structural insights on physiological functions and pathological effects of α-synuclein. FASEB Journal, 23, 329–340. doi:10.1096/fj.08-119784
   PubMed Web of Science ®Google Scholar
• Case, D. A., Darden, T. A., Cheatham, T. E., III, Simmerling, C. L., Wang, J., Duke, R. E., … Kollman, P. A. (2012). AMBER 12. San Francisco, CA: University of California.
   Google Scholar
• Clayton, D. F., & George, J. M. (1998). The synucleins: A family of proteins involved in synaptic function, plasticity, neurodegeneration and disease. Trends in Neurosciences, 21, 249–254. doi:10.1016/s0166-2236(97)01213-7
   PubMed Web of Science ®Google Scholar
• Deleersnijder, A., Gerard, M., Debyser, Z., & Baekelandt, V. (2013). The remarkable conformational plasticity of α-synuclein: Blessing or curse? Trends in Molecular Medicine, 19, 368–377. doi:10.1016/j.molmed.2013.04.002
   PubMed Web of Science ®Google Scholar
• Duhovny, D., Nussinov, R., & Wolfson, H. J. (2002). Efficient unbound docking of rigid molecules (pp. 185–200). Berlin Heidelberg: Springer-Verlag. doi:10.1007/3-540-45784-4_14.
   Google Scholar
• Fan, Y., Limprasert, P., Murray, I. V. J., Smith, A. C., Lee, V. M. Y., Trojanowski, J. Q., … Spada, A. R. L. (2006). β-synuclein modulates α-synuclein neurotoxicity by reducing α-synuclein protein expression. Human Molecular Genetics, 15, 3002–3011. doi:10.1093/hmg/ddl242
   PubMed Web of Science ®Google Scholar
• Galvin, J. E., Uryu, K., Lee, V. M., & Trojanowski, J. Q. (1999). Axon pathology in Parkinson’s disease and Lewy body dementia hippocampus contains α-, β-, and gamma-synuclein. Proceedings of the National Academy Science USA, 96, 13450–13455. doi:10.1073/pnas.96.23.13450
   PubMed Web of Science ®Google Scholar
• Ghosh, S., Pandey, N. K., Banerjee, P., Chaudhury, K., Nagy, N. V., & Dasgupta, S. (2014). Copper (II) directs formation of toxic amorphous aggregates resulting in inhibition of hen egg white lysozyme fibrillation under alkaline salt-mediated conditions. Journal of Biomolecular Structure and Dynamics, 33, 991–1007. doi:10.1080/07391102.2014.921864
   PubMed Web of Science ®Google Scholar
• Grossfield, A. (1995). Multidimensional free-energy calculations using the weighted histogram analysis method. Journal of Computational Chemistry, 16, 1339–1350. doi:10.1002/jcc.540161104
   Web of Science ®Google Scholar
• Hashimoto, M., Bar-on, P., Ho, G., Takenouchi, T., Rockenstein, E., Crews, L., & Masliah, E. (2004). β-synuclein regulates Akt activity in neuronal cells. A possible mechanism for neuroprotection in Parkinson’s disease. Journal of Biological Chemistry, 279, 23622–23629. doi:10.1074/jbc.m313784200
   PubMed Web of Science ®Google Scholar
• Hashimoto, M., Rockenstein, E., Mante, M., Crews, L., Bar-On, P., Gage, F. H., … Masliah, E. (2004). An anti-aggregation gene therapy strategy for Lewy body disease utilizing β-synuclein lentivirus in a transgenic model. Gene Therapy, 11, 1713–1723. doi:10.1038/sj.gt.3302349
   PubMed Web of Science ®Google Scholar
• Hashimoto, M., Rockenstein, E., Mante, M., Mallory, M., & Masliah, E. (2001). β-Synuclein inhibits α-synuclein aggregation: A possible role as an anti-parkinsonian factor. Neuron, 32, 213–223. doi:10.1016/s0896-6273(01)00462-7
   PubMed Web of Science ®Google Scholar
• Hornak, V., Abel, R., Okur, A., Strockbine, B., Roitberg, A., & Simmerling, C. (2006). Comparison of multiple Amber force fields and development of improved protein backbone parameters. Proteins: Structure Function and Bioinformatics, 65, 712–725. doi:10.1002/prot.21123
   PubMed Web of Science ®Google Scholar
• Horvath, I., Weiset, C. F., Andersson, E. K., Chorell, E., Sellstedt, M., Bengtsson, C., … Wittung Stafshede, P. (2012). Mechanisms of protein oligomerization: inhibitor of functional amyloids templates α-synuclein fibrillation. Journal of the American Chemical Society, 134, 3439–3444. doi:10.1021/ja209829m
   PubMed Web of Science ®Google Scholar
• Jain, N., Bhasne, K., Hemaswasthi, M., & Mukhopadhyay, S. (2013). Structural and dynamical insights into the membrane-bound α-synuclein. PLoS ONE, 8, e83752. doi:10.1371/journal.pone.0083752
   PubMed Web of Science ®Google Scholar
• Jakes, R., Spillantini, M. G., & Goedert, M. (1994). Identification of two distinct synucleins from human brain. FEBS Letter, 345, 27–32. doi:10.1016/0014-5793(94)00395-5
   PubMed Web of Science ®Google Scholar
• Janowska, M. K., Wu, K. P., & Baum, J. (2015). Unveiling transient protein-protein interactions that modulate inhibition of alpha-synuclein aggregation by beta-synuclein, a pre-synaptic protein that co-localizes with alpha-synuclein. Scientific Reports, 5, 15164. doi:10.1038/srep15164
   PubMed Web of Science ®Google Scholar
• Kahle, P. J., Neumann, M., Ozmen, L., Muller, V., Odoy, S., Okamoto, N., … Haass, C. (2001). Selective insolubility of α-synuclein in human lewy body diseases is recapitulated in a transgenic mouse model. American Journal of Pathology, 159, 2215–2225. doi:10.1016/s0002-9440(10)63072-6
   PubMed Web of Science ®Google Scholar
• Kirkwood, J. G. (1935). Statistical mechanics of fluid mixtures. Journal of Chemical Physics, 3, 300–313. doi:10.1063/1.1749657
   Web of Science ®Google Scholar
• Kumar, S., Bouzida, D., Swendsen, R. H., Kollman, P. A., & Rosenberg, J. M. (1992). THE weighted histogram analysis method for free-energy calculations on biomolecules. I. The method. Journal of Computational Chemistry, 13, 1011–1021. doi:10.1002/jcc.540130812
   Web of Science ®Google Scholar
• Kumar, A., Srivastava, S., Tripathi, S., Singh, S. K., Srikrishna, S., & Sharma, A. (2015). Molecular insight into amyloid oligomer destabilizing mechanism of flavonoid derivative 2-(4′benzyloxyphenyl)-3-hydroxy-chromen-4-one through docking and molecular dynamics simulations. Journal of Biomolecular Structure and Dynamics, 34, 1252–1263. doi:10.1080/07391102.2015.1074943
   PubMed Web of Science ®Google Scholar
• Lamberto, C. R., Torres-Monserrat, V., Bertoncini, C. W., Salvatella, X., Zweckstetter, M., Griesinger, C., & Fernandez, C. O. (2011). Toward the discovery of effective polycyclic inhibitors of α-synuclein amyloid assembly. Journal of Biological Chemistry, 286, 32036–32044. doi:10.1074/jbc.m111.242958
   PubMed Web of Science ®Google Scholar
• Laskowski, R. A. (2001). PDBsum: summaries and analyses of PDB structures. Nucleic Acids Research, 29, 221–222. doi:10.1093/nar/29.1.221
   PubMed Web of Science ®Google Scholar
• Lavedan, C. (1998). The synuclein family. Genome Research, 8, 871–880.
   PubMed Web of Science ®Google Scholar
• Lendel, C., Bertoncini, C. W., Cremades, N., Waudby, C. A., Vendruscolo, M., Dobson, C. M., … Toth, G. (2009). On the mechanism of nonspecific inhibitors of protein aggregation: Dissecting the interactions of alpha-synuclein with congo red and lacmoid. Biochemistry, 48, 8322–8334. doi:10.1021/bi901285x
   PubMed Web of Science ®Google Scholar
• Masliah, E., Hansen, L. A., Rockenstein, E., & Hashimoto, M. (2002). Progress in the development of new treatments for combined Alzheimer’s and Parkinson’s diseases. Drug Development Research, 56, 282–292. doi:10.1002/ddr.10082
   Web of Science ®Google Scholar
• Meng, X. Y., Munishkina, L. A., Fink, A. L., & Uversky, V. N. (2009). Molecular mechanisms underlying the flavonoid-induced inhibition of α-synuclein fibrillation. Biochemistry, 48, 8206–8224. doi:10.1021/bi900506b
   PubMed Web of Science ®Google Scholar
• Park, J. Y., & Lansbury, P. T., Jr. (2003). β-synuclein inhibits formation of α-synuclein protofibrils: A possible therapeutic strategy against Parkinson’s disease. Biochemistry, 42, 3696–3700. doi:10.1021/bi020604a
   PubMed Web of Science ®Google Scholar
• Park, S. B., Yoon, J., Jang, S., Lee, K., & Shin, S. (2015). The role of the acidic domain of α-synuclein in amyloid fibril formation: A molecular dynamics study. Journal of Biomolecular Structure and Dynamics, 34, 376–383. doi:10.1080/07391102.2015.1033016
   PubMed Web of Science ®Google Scholar
• Rao, J. N., Dua, V., & Ulmer, T. S. (2008). Characterization of α-synuclein interactions with selected aggregation-inhibiting small molecules. Biochemistry, 47, 4651–4656. doi:10.1021/bi8002378
   PubMed Web of Science ®Google Scholar
• Rice, P., Longden, I., & Bleasby, A. (2000). EMBOSS: The european molecular biology open software suite. Trends in Genetics, 16, 276–277. doi:10.1016/s0168-9525(00)02024-2
   PubMed Web of Science ®Google Scholar
• Rivers, R. C., Kumita, J. R., Tartaglia, G. G., Dedmon, M. M., Pawar, A., Vendruscolo, M., … Christodoulou, J. (2008). Molecular determinants of the aggregation behavior of α- and β-synuclein. Protein Science, 17, 887–898. doi:10.1110/ps.073181508
   PubMed Web of Science ®Google Scholar
• Roodveldt, C., Andersson, A., De Genst, E. J., Labrador-Garrido, A., Buell, A. K., Dobson, C. M., … Vendruscolo, M. (2012). A rationally designed six-residue swap generates comparability in the aggregation behavior of α-synuclein and β-synuclein. Biochemistry, 51, 8771–8778. doi:10.1021/bi300558q
   PubMed Web of Science ®Google Scholar
• Souaille, M., & Roux, B. (2001). Extension to the weighted histogram analysis method: Combining umbrella sampling with free energy calculations. Computer PhysicsCommunications, 135, 40–57. doi:10.1016/s0010-4655(00)00215-0
   Web of Science ®Google Scholar
• Taschenberger, G., Toloe, J., Tereshchenko, J., Akerboom, J., Wales, P., Benz, R., … Kugler, S. (2013). β-synuclein aggregates and induces neurodegeneration in dopaminergic neurons. Annals of Neurology, 74, 109–118. doi:10.1002/ana.23905
   PubMed Web of Science ®Google Scholar
• Torrie, G. M., & Valleau, J. P. (1974). Modeling condensed phase reaction dynamics. Chemical Physics Letters, 28, 578–581.10.1016/0009-2614(74)80109-0
   Web of Science ®Google Scholar
• Tsigelny, I. F., Bar-On, P., Sharikov, Y., Crews, L., Hashimoto, M., Miller, M. A., … Mashiah, E. (2007). Dynamics of α-synuclein aggregation and inhibition of pore-like oligomer development by β-synuclein. FEBS Journal, 274, 1862–1877. doi:10.1111/j.1742-4658.2007.05733.x
   PubMed Web of Science ®Google Scholar
• Ueda, K., Fukushima, H., Masliah, E., Xia, Y., Iwai, A., Yoshimoto, M., … Saitoh, T. (1993). Molecular cloning of cDNA encoding anunrecognized component of amyloid in Alzheimer disease. Proceedings in National Academy of Sciences, 9, 11282–11286. doi:10.1073/pnas.90.23.11282
   Web of Science ®Google Scholar
• Uversky, V. N. (2003). A protein-chameleon: Conformational plasticity of alpha-synuclein, a disordered protein involved in neurodegenerative disorders. Journal of Biomolecular and Structure Dynamics, 21, 211–234. doi:10.1080/07391102.2003.10506918
   PubMed Web of Science ®Google Scholar
• Uversky, V. N., Li, J., Souillac, P., Millett, I. S., Doniach, S., Jakes, R., … Fink, A. L. (2002). Biophysical properties of the synucleins and their propensities to fibrillate: Inhibition of α-synuclein assembly by β- and gamma-synucleins. Journal of Biology Chemistry, 277, 11970–11978. doi:10.1074/jbc.m109541200
   PubMed Web of Science ®Google Scholar
• Yoon, J., Park, J., Jang, S., Lee, K., & Shin, S. (2008). Conformational characteristics of unstructured peptides: Alpha-synuclein. Journal of Biomolecular Structure and Dynamics, 25, 505–515. doi:10.1080/07391102.2008.10507197
   PubMed Web of Science ®Google Scholar
• Zhang, Y. (2008). I-TASSER server for protein 3D structure prediction. BMC Bioinformatics, 9, 40. doi:10.1186/1471-2105-9-40
   PubMed Web of Science ®Google Scholar
• Zhang, C., Vasmatzis, G., Cornette, J. L., & DeLisi, C. (1997). Determination of atomic desolvation energies from the structures of crystallized proteins. Journal of Molecular Biology, 267, 707–726. doi:10.1006/jmbi.1996.0859
   PubMed Web of Science ®Google Scholar
• Zibaee, S., Jakes, R., Fraser, G., Serpell, L. C., Crowther, R. A., & Goedert, M. (2007). Sequence determinants for amyloid fibrillogenesis of human α-synuclein. Journal of Molecular Biology, 374, 454–464. doi:10.1016/j.jmb.2007.09.039
   PubMed Web of Science ®Google Scholar