Sodium-salt adduct fullerenes prevent self-association and amyloid β fibril formation: molecular dynamics approach

References

• Zhang, Y.; Thompson, R.; Zhang, H.; Xu, H. APP Processing in Alzheimer’s Disease, Mol. Brain. 2011, 4, 3. DOI: 10.1186/1756-6606-4-3.
   Web of Science ®Google Scholar
• Kawarabayashi, T.; Shoji, M.; Younkin, L. H.; Wen-Lang, L.; Dickson, D. W.; Murakami, T.; Matsubara, E.; Abe, K.; Ashe, K. H.; Younkin, S. G. Dimeric Amyloid β Protein Rapidly Accumulates in Lipid Rafts Followed by Apolipoprotein E and Phosphorylated Tau Accumulation in the Tg2576 Mouse Model of Alzheimer’s Disease. J. Neurosci. 2004, 24, 3801. DOI: 10.1523/JNEUROSCI.5543-03.2004.
   PubMed Web of Science ®Google Scholar
• Sciacca, M. F. M.; Kotler, S. A.; Brender, J. R.; Chen, J.; Lee, D.; Ramamoorthy, A. Two-step Mechanism of Membrane Disruption by Aβ through Membrane Fragmentation and Pore Formation. Biophys. J. 2012, 103, 702–710. DOI: 10.1016/j.bpj.2012.06.045.
   PubMed Web of Science ®Google Scholar
• Talantova, M.; Sanz-Blasco, S.; Zhang, X.; Xia, P.; Akhtar, M. W.; Okamoto, S.; Dziewczapolski, G.; Nakamura, T.; Cao, G.; Pratt, A. E.; et al. Aβ Induces Astrocytic Glutamate Release, Extrasynaptic NMDA Receptor Activation, and Synaptic Loss. Proc. Natl. Acad. Sci. 2013, 110, E2518. DOI: 10.1073/pnas.1306832110.
   PubMed Web of Science ®Google Scholar
• Um, J. W.; Nygaard, H. B.; Heiss, J. K.; Kostylev, M. A.; Stagi, M.; Vortmeyer, A.; Wisniewski, T.; Gunther, E. C.; Strittmatter, S. M. Alzheimer amyloid-β Oligomer Bound to Postsynaptic Prion Protein Activates Fyn to Impair Neurons, Nat. Neurosci. 2012, 15, 1227. DOI: 10.1038/nn.3178.
   PubMed Web of Science ®Google Scholar
• Lee, S. J. C.; Nam, E.; Lee, H. J.; Savelieff, M. G.; Lim, M. H. Towards an Understanding of amyloid-β Oligomers: Characterization, Toxicity Mechanisms, and Inhibitors. Chem. Soc. Rev. 2017, 46, 310–323. DOI: 10.1039/C6CS00731G.
   PubMed Web of Science ®Google Scholar
• Sisodia, S. S.; St George-Hyslop, P. H. γ-Secretase, Notch, Aβ and Alzheimer’s Disease: Where Do the Presenilins Fit In? Nat. Rev. Neurosci. 2002, 3, 281–290. DOI: 10.1038/nrn785.
   PubMed Web of Science ®Google Scholar
• Orgogozo, J.-M.; Gilman, S.; Dartigues, J.-F.; Laurent, B.; Puel, M.; Kirby, L. C.; Jouanny, P.; Dubois, B.; Eisner, L.; Flitman, S.; et al. Subacute Meningoencephalitis in a Subset of Patients with AD after Aβ42 Immunization. Neurology. 2003, 61, 46. DOI: 10.1212/01.WNL.0000073623.84147.A8.
   PubMed Web of Science ®Google Scholar
• V, B.; E, M.-B. D.; Uro-Coste, G.; Russano de Paiva, C.; Guilbeau-Frugier, N.; Sastre, P. J.; Ousset, N. A.; da Silva, V. Lavialle-Guillotreau, Cerebral Amyloid Angiopathy and Microhemorrhages after Amyloid Beta Vaccination: Case Report and Brief Review. 2010. DOI: 10.5414/NPP29209.
   Google Scholar
• Young, L. M.; Saunders, J. C.; Mahood, R. A.; Revill, C. H.; Foster, R. J.; Tu, L.-H.; Raleigh, D. P.; Radford, S. E.; Ashcroft, A. E. Screening and Classifying Small-molecule Inhibitors of Amyloid Formation Using Ion Mobility Spectrometry–mass Spectrometry. Nat. Chem. 2014, 7, 73. DOI: 10.1038/nchem.2129.
   PubMed Web of Science ®Google Scholar
• Saunders, J. C.; Young, L. M.; Mahood, R. A.; Jackson, M. P.; Revill, C. H.; Foster, R. J.; Smith, D. A.; Ashcroft, A. E.; Brockwell, D. J.; Radford, S. E. An in Vivo Platform for Identifying Inhibitors of Protein Aggregation. Nat. Chem. Biol. 2015, 12, 94. DOI: 10.1038/nchembio.1988.
   PubMed Web of Science ®Google Scholar
• Zhang, Z.; Wang, J.; Song, Y.; Wang, Z.; Dong, M.; Liu, L. Disassembly of Alzheimer’s Amyloid Fibrils by Functional Upconversion Nanoparticles under Near-infrared Light Irradiation. Colloids Surf. B Biointerfaces. 2019, 181, 341–348. DOI: 10.1016/j.colsurfb.2019.05.053.
   PubMed Web of Science ®Google Scholar
• Kim, J. E.; Lee, M. Fullerene Inhibits β-Amyloid Peptide Aggregation. Biochem. Biophys. Res. Commun. 2003, 303, 576–579. DOI: 10.1016/S0006-291X(03)00393-0.
   PubMed Web of Science ®Google Scholar
• Ishida, Y.; Fujii, T.; Oka, K.; Takahashi, D.; Toshima, K. Inhibition of Amyloid β Aggregation and Cytotoxicity by Photodegradation Using a Designed Fullerene Derivative. Chem. – Asian J. 2011, 6, 2312–2315. DOI: 10.1002/asia.201100421.
   PubMed Web of Science ®Google Scholar
• Bobylev, A. G.; Kornev, A. B.; Bobyleva, L. G.; Shpagina, M. D.; Fadeeva, I. S.; Fadeev, R. S.; Deryabin, D. G.; Balzarini, J.; Troshin, P. A.; Podlubnaya, Z. A. Fullerenolates: Metallated Polyhydroxylated Fullerenes with Potent Anti-amyloid Activity. Org. Biomol. Chem. 2011, 9, 5714–5719. DOI: 10.1039/C1OB05067B.
   PubMed Web of Science ®Google Scholar
• Raoof, M.; Mackeyev, Y.; Cheney, M. A.; Wilson, L. J.; Curley, S. A. Internalization of C60 Fullerenes into Cancer Cells with Accumulation in the Nucleus via the Nuclear Pore Complex. Biomaterials. 2012, 33, 2952–2960. DOI: 10.1016/j.biomaterials.2011.12.043.
   PubMed Web of Science ®Google Scholar
• Johnson-Lyles, D. N.; Peifley, K.; Lockett, S.; Neun, B. W.; Hansen, M.; Clogston, J.; Stern, S. T.; McNeil, S. E. Fullerenol Cytotoxicity in Kidney Cells Is Associated with Cytoskeleton Disruption, Autophagic Vacuole Accumulation, and Mitochondrial Dysfunction. Toxicol. Appl. Pharmacol. 2010, 248, 249–258. DOI: 10.1016/j.taap.2010.08.008.
   PubMed Web of Science ®Google Scholar
• Su, Y.; Xu, J.; Shen, P.; Li, J.; Wang, L.; Li, Q.; Li, W.; Xu, G.; Fan, C.; Huang, Q. Cellular Uptake and Cytotoxic Evaluation of Fullerenol in Different Cell Lines. Toxicology. 2010, 269, 155–159. DOI: 10.1016/j.tox.2009.11.015.
   PubMed Web of Science ®Google Scholar
• Nakamura, E.; Isobe, H.; Tomita, N.; Sawamura, M.; Jinno, S.; Okayama, H. Functionalized Fullerene as an Artificial Vector for Transfection. Angew. Chemie Int. Ed. 2000, 39, 4254–4257. DOI: 10.1002/1521-3773(20001201)39:23<4254::AID-ANIE4254>3.0.CO;2-O.
   PubMed Web of Science ®Google Scholar
• Isobe, H.; Nakanishi, W.; Tomita, N.; Jinno, S.; Okayama, H.; Nakamura, E. Nonviral Gene Delivery by Tetraamino Fullerene. Mol. Pharm. 2006, 3, 124–134. DOI: 10.1021/mp050068r.
   PubMed Web of Science ®Google Scholar
• Chen, Z.; Mao, R.; Liu, Y. Fullerenes for Cancer Diagnosis and Therapy: Preparation, Biological and Clinical Perspectives, Curr. Drug Metab. 2012, 13, 1035–1045. DOI: 10.2174/138920012802850128.
   Google Scholar
• Prylutskyy, Y. I.; Petrenko, V. I.; Ivankov, O. I.; Kyzyma, O. A.; Bulavin, L. A.; Litsis, O. O.; Evstigneev, M. P.; Cherepanov, V. V.; Naumovets, A. G.; Ritter, U. On the Origin of C60 Fullerene Solubility in Aqueous Solution. Langmuir. 2014, 30, 3967–3970. DOI: 10.1021/la404976k.
   PubMed Web of Science ®Google Scholar
• Boltalina, O. V.; Popov, A. A.; Kuvychko, I. V.; Shustova, N. B.; Strauss, S. H. Perfluoroalkylfullerenes. Chem. Rev. 2015, 115, 1051–1105. DOI: 10.1021/cr5002595.
   PubMed Web of Science ®Google Scholar
• Zhou, S.; Ouyang, J.; Golas, P.; Wang, F.; Pan, Y. Structural Study of the Self-Assembled Fullerene Carboxylates: Monoadducts versus Bisadducts. J. Phys. Chem. B. 2005, 109, 19741–19747. DOI: 10.1021/jp053978x.
   PubMed Web of Science ®Google Scholar
• Hasunuma, N.; Kawakami, M.; Hiramatsu, H.; Nakabayashi, T. Preparation and Photo-induced Activities of Water-soluble Amyloid β-C60 Complexes. RSC Adv. 2018, 8, 17847–17853. DOI: 10.1039/C8RA02789G.
   PubMed Web of Science ®Google Scholar
• Injac, R.; Prijatelj, M.; Strukelj, B. Fullerenol Nanoparticles: Toxicity and Antioxidant Activity. In Oxidative Stress Nanotechnol. Methods Protoc.; Armstrong, D., Bharali, D. J., Eds.; Humana Press: Totowa, NJ, 2013; pp 75–100. DOI: 10.1007/978-1-62703-475-3_5.
   Google Scholar
• Bobylev, A. G.; Kraevaya, O. A.; Bobyleva, L. G.; Khakina, E. A.; Fadeev, R. S.; Zhilenkov, A. V.; Mishchenko, D. V.; Penkov, N. V.; Teplov, I. Y.; Yakupova, E. I.; et al. Anti-amyloid Activities of Three Different Types of Water-soluble Fullerene Derivatives. Colloids Surf. B. Biointerfaces. 2019, 183, 110426. DOI: 10.1016/j.colsurfb.2019.110426.
   PubMed Web of Science ®Google Scholar
• Adams, G. B.; O’Keeffe, M.; Ruoff, R. S. Van Der Waals Surface Areas and Volumes of Fullerenes. J. Phys. Chem. 1994, 98, 9465–9469. DOI: 10.1021/j100089a018.
   Web of Science ®Google Scholar
• Bingel, C.;. Cyclopropanierung von Fullerenen. Chem. Ber. 1993, 126, 1957–1959. DOI: 10.1002/cber.19931260829.
   Google Scholar
• Hirsch, A.; Lamparth, I.; Karfunkel, H. R. Fullerene Chemistry in Three Dimensions: Isolation of Seven Regioisomeric Bisadducts and Chiral Trisadducts of C60 and Di(ethoxycarbonyl)methylene. Angew. Chemie Int. Ed. English 1994, 33, 437–438. DOI: 10.1002/anie.199404371.
   Web of Science ®Google Scholar
• Biglova, Y. N.; Mustafin, A. G. Nucleophilic Cyclopropanation of [60]fullerene by the Addition–elimination Mechanism. RSC Adv. 2019, 9, 22428–22498. DOI: 10.1039/c9ra04036f.
   PubMed Web of Science ®Google Scholar
• Martínez-Herrera, M.; Figueroa-Gerstenmaier, S.; García-Sierra, F.; Beltrán, H. I.; Rivera-Fernández, N.; Lerma-Romero, J. A.; Basurto-Islas, L.-C. P. Y., G. Fullerenemalonates Inhibit Amyloid Beta Aggregation, in Vitro and in Silico Evaluation. RSC Adv. 2018, 8, 39667–39677. DOI: 10.1039/C8RA07643J.
   PubMed Web of Science ®Google Scholar
• Li, L.; Bedrov, D.; Smith, G. D. A Molecular-dynamics Simulation Study of Solvent-induced Repulsion between C60 Fullerenes in Water. J. Chem. Phys. 2005, 123, 204504. DOI: 10.1063/1.2121647.
   PubMed Web of Science ®Google Scholar
• Keshri, S.; Tembe, B. L. Thermodynamics of Hydration of Fullerols [C60(oh)n] and Hydrogen Bond Dynamics in Their Hydration Shells. J. Chem. Phys. 2017, 146, 074501. DOI: 10.1063/1.4975230.
   PubMed Web of Science ®Google Scholar
• Choudhury, N.;. Dynamics of Water in the Hydration Shells of C60: Molecular Dynamics Simulation Using a Coarse-Grained Model. J. Phys. Chem. B. 2007, 111, 10474–10480. DOI: 10.1021/jp073571n.
   PubMedGoogle Scholar
• Li, L.; Bedrov, D.; Smith, G. D. Repulsive Solvent-induced Interaction Between C60 Fullerenes in Water. Phys. Rev. E. 2005, 71, 11502. DOI: 10.1103/PhysRevE.71.011502.
   Web of Science ®Google Scholar
• Banerjee, S.;. Molecular Dynamics Study of Self-agglomeration of Charged Fullerenes in Solvents. J. Chem. Phys. 2013, 138, 044318. DOI: 10.1063/1.4789304.
   PubMedGoogle Scholar
• Liu, Z.; Zou, Y.; Zhang, Q.; Chen, P.; Liu, Y.; Qian, Z. Distinct Binding Dynamics, Sites and Interactions of Fullerene and Fullerenols with Amyloid-β Peptides Revealed by Molecular Dynamics Simulations. Int. J. Mol. Sci. 2019, 20. DOI: 10.3390/ijms20082048.
   Web of Science ®Google Scholar
• Zhou, X.; Xi, W.; Luo, Y.; Cao, S.; Wei, G. Interactions of a Water-Soluble Fullerene Derivative with Amyloid-β Protofibrils: Dynamics, Binding Mechanism, and the Resulting Salt-Bridge Disruption. J. Phys. Chem. B. 2014, 118, 6733–6741. DOI: 10.1021/jp503458w.
   PubMed Web of Science ®Google Scholar
• Sun, Y.; Qian, Z.; Wei, G. The Inhibitory Mechanism of a Fullerene Derivative against amyloid-β Peptide Aggregation: An Atomistic Simulation Study. Phys. Chem. Chem. Phys. 2016, 18, 12582–12591. DOI: 10.1039/C6CP01014H.
   PubMed Web of Science ®Google Scholar
• Bednarikova, Z.; Huy, P. D. Q.; Mocanu, -M.-M.; Fedunova, D.; Li, M. S.; Gazova, Z. Fullerenol C60(OH)16 Prevents Amyloid Fibrillization of Aβ40 – In Vitro and in Silico Approach. Phys. Chem. Chem. Phys. 2016, 18, 18855–18867. DOI: 10.1039/C6CP00901H.
   PubMed Web of Science ®Google Scholar
• Abraham, M. J.; Murtola, T.; Schulz, R.; Páll, S.; Smith, J. C.; Hess, B.; Lindahl, E. GROMACS: High Performance Molecular Simulations through Multi-level Parallelism from Laptops to Supercomputers. SoftwareX. 2015, 1–2, 19–25. DOI: 10.1016/j.softx.2015.06.001.
   Google Scholar
• Hanwell, M. D.; Curtis, D. E.; Lonie, D. C.; Vandermeerschd, T.; Zurek, E.; Hutchison, G. R. Avogadro: An Advanced Semantic Chemical Editor, Visualization, and Analysis Platform. J. Cheminform. 2012, 4. DOI:10.1186/1758-2946-4-17
   PubMed Web of Science ®Google Scholar
• Malde, A. K.; Zuo, L.; Breeze, M.; Stroet, M.; Poger, D.; Nair, P. C.; Oostenbrink, C.; Mark, A. E. An Automated Force Field Topology Builder (ATB) and Repository: Version 1.0. J. Chem. Theory Comput. 2011, 7, 4026–4037. DOI: 10.1021/ct200196m.
   PubMed Web of Science ®Google Scholar
• Schmid, N.; Eichenberger, A. P.; Choutko, A.; Riniker, S.; Winger, M.; Mark, A. E.; Van Gunsteren, W. F. Definition and Testing of the GROMOS Force-field Versions 54A7 and 54B7. Eur. Biophys. J. 2011, 40, 843–856. DOI: 10.1007/s00249-011-0700-9.
   PubMed Web of Science ®Google Scholar
• Berendsen, H. J. C.; Grigera, J. R.; Straatsma, T. P. The Missing Term in Effective Pair Potentials. J. Phys. Chem. 2002, 91, 6269–6271. DOI: 10.1021/j100308a038.
   Google Scholar
• Bussi, G.; Donadio, D.; Parrinello, M. Canonical Sampling through Velocity Rescaling. J. Chem. Phys. 2007, 126. DOI: 10.1063/1.2408420.
   PubMed Web of Science ®Google Scholar
• Parrinello, M.; Rahman, A. Polymorphic Transitions in Single Crystals: A New Molecular Dynamics Method. J. Appl. Phys. 1981, 52, 7182–7190. DOI: 10.1063/1.328693.
   Web of Science ®Google Scholar
• Nosé, S.; Klein, M. L. Constant Pressure Molecular Dynamics for Molecular Systems. Mol. Phys. 1983, 50, 1055–1076. DOI: 10.1080/00268978300102851.
   Web of Science ®Google Scholar
• Heinz, D. W.; Baase, W. A.; Dahlquist, F. W.; Matthews, B. W. How Amino-acid Insertions are Allowed in an α-helix of T4 Lysozyme. Nature. 1993, 361, 561–564. DOI: 10.1038/361561a0.
   PubMed Web of Science ®Google Scholar
• Melchor, M. H.; Susana, F. G.; Francisco, G. S.; Beltran, H. I.; Norma, R. F.; Lerma-Romero, J. A.; Lopez-Camacho, P. Y.; Gustavo, B. I. Fullerenemalonates Inhibit Amyloid Beta Aggregation, in Vitro and in Silico Evaluation. RSC Adv. 2018, 8, 39667–39677. DOI: 10.1039/c8ra07643j.
   PubMed Web of Science ®Google Scholar
• Allen, M. P.; Tildesley, D. J. Computer Simulation of Liquids. 1991, 383. Oxford University Press. https://global.oup.com/academic/product/computer-simulation-of-liquids-9780198803201?q=molecular%20simulation&lang=en&cc=mx
   Google Scholar
• Darden, T.; York, D.; Pedersen, L. Particle Mesh Ewald: An N·log(N) Method for Ewald Sums in Large Systems. J. Chem. Phys. 1993, 98, 10089–10092. DOI: 10.1063/1.464397.
   Web of Science ®Google Scholar
• Hess, B.;. P-LINCS: A Parallel Linear Constraint Solver for Molecular Simulation. J. Chem. Theory Comput. 2007, 4, 116–122. DOI: 10.1021/ct700200b.
   Web of Science ®Google Scholar
• van der Spoel, D.; van Buuren, A. R.; Apol, E.; Meulenhoff, P. J.; Tieleman, D. P.; Sijbers, A. L. T. M.; Hess, B.; Feenstra, K. A.; Lindahl, E.; van Drunen, R.; et al., GROMACS Reference Manual Contributions From. 2005. www.gromacs.org.
   Google Scholar
• Eisenhaber, F.; Lijnzaad, P.; Argos, P.; Sander, C.; Scharf, M. The Double Cubic Lattice Method. J. Comput. Chem. 1995, 273–284. doi:10.1002/jcc.540160303.
   Google Scholar
• Lee, B.; Richards, F. M. The Interpretation of Protein Structures: Estimation of Static Accessibility. J. Mol. Biol. 1971, 55, 379–IN4. DOI: 10.1016/0022-2836(71)90324-X.
   PubMed Web of Science ®Google Scholar
• Guldi, D. M.; Hungerbühler, H.; Janata, E.; Asmus, K. D. Redox Processes and Alkylation Reactions of C60 as Studied by Pulse Radiolysis. J. Phys. Chem. 1993, 97, 11258–11264. DOI: 10.1021/j100145a024.
   Web of Science ®Google Scholar