Investigating amyloid nanofibril self-assembly, with an emphasis on the electromechanical property of amyloid peptides, namely, piezoelectricity, may have several important implications: 1) the self-assembly process can hinder the biological stability and give rise to the formation of amyloid structures associated with neurodegenerative diseases; 2) investigations in this field may lead to an improved understanding of high-performance, functional biological nanomaterials, 3) new technologies could be established based on peptide self-assembly and the resultant functional properties, e.g., in the creation of a piezoelectric device formed with vertical diphenylalanine peptide tubes as a piezoelectric biosensor, and 4) new knowledge can be generated about neurodegenerative disorders, potentially yielding new therapies. Therefore, in this review, we will present the current investigations associated with self-assembly of amyloid-beta, the mechanisms that generate new structures, as well as theoretical calculations exploring the functionality of the structures under physiological pressure and electric field.
References
[1]
McGowan, D.P., van Roon-Mom, W., Holloway, H., Bates, G.P., Mangiarini, L., Cooper, G.J.S., Faull, R.L.M. and Snell, R.G. (2000) Amyloid-Like Inclusions in Huntington’s Disease. Neuroscience, 100, 677-680.
https://doi.org/10.1016/S0306-4522(00)00391-2
[2]
Gu, L. and Guo, Z.F. (2013) Alzheimer’s Aβ42 and Aβ40 Peptides form Interlaced Amyloid Fibrils. Journal of Neurochemistry, 126, 305-311.
https://doi.org/10.1111/jnc.12202
[3]
Grimm, M.O.W., Grimm, H.S. and Hartmann, T. (2007) Amyloid Beta as a Regulator of Lipid Homeostasis. Trends in Molecular Medicine, 13, 337-344.
https://doi.org/10.1016/j.molmed.2007.06.004
[4]
Colfen, H. and Mann, S. (2003) Higher-Order Organization by Mesoscale Self-Assembly and Transformation of Hybrid Nanostructures. Angewandte Chemie International Edition, 42, 2350-2365. https://doi.org/10.1002/anie.200200562
[5]
Kerrigan, T.L., Atkinson, L., Peers, C. and Pearson, H.A. (2008) Modulation of ‘A’-Type K+ Current by Rodent and Human Forms of Amyloid β Protein. NeuroReport, 19, 839-843. https://doi.org/10.1097/WNR.0b013e3282ff636b
[6]
Scragg, J.L., Fearon, I.M., Boyle, J.P., Ball, S.G., Varadi, G. and Peers, C. (2005) Alzheimer’s Amyloid Peptides Mediate Hypoxic Up-Regulation of L-Type Ca2+ Channels. The FASEB Journal, 19, 150-152. https://doi.org/10.1096/fj.04-2659fje
[7]
Castelletto, V., Hamley, I.W. and Harris, P.J.F. (2008) Self-Assembly in Aqueous Solution of a Modified Amyloid Beta Peptide Fragment. Biophysical Chemistry, 138, 29-35. https://doi.org/10.1016/j.bpc.2008.08.007
[8]
Heredia, A., Bdikin, I., Kopyl, S., Mishina, E., Semin, S., Sigov, A., German, K., Bystrov, V., Gracio, J. and Kholkin, A.L. (2010) Temperature-Driven Phase Transformation in Self-Assembled Diphenylalanine Peptide Nanotubes. Journal of Physics D: Applied Physics, 43, Article ID: 462001.
https://doi.org/10.1088/0022-3727/43/46/462001
[9]
Kholkin, A., Amdursky, N., Bdikin, I., Gazit, E. and Rosenman, G. (2010) Strong Piezoelectricity in Bioinspired Peptide Nanotubes. ACS Nano, 4, 610-614.
https://doi.org/10.1021/nn901327v
[10]
Kol, N., Adler-Abramovich, L., Barlam, D., Shneck, R.Z., Gazit, E. and Rousso, I. (2005) Self-Assembled Peptide Nanotubes are Uniquely Rigid Bioinspired Supramolecular Structures. Nano Letters, 5, 1343-1346.
https://doi.org/10.1021/nl0505896
[11]
Niu, L., Chen, X., Allen, S. and Tendler, S.J.B. (2007) Using the Bending Beam Model to Estimate the Elasticity of Diphenylalanine Nanotubes. Langmuir, 23, 7443-7446. https://doi.org/10.1021/la7010106
[12]
Mann, S. (2009) Self-Assembly and Transformation of Hybrid Nano-Objects and Nanostructures under Equilibrium and Non-Equilibrium Conditions. Nature Materials, 8, 781-792. https://doi.org/10.1038/nmat2496
[13]
Adler-Abramovich, L., Aronov, D., Beker, P., Yevnin, M., Stempler, S., Buzhansky, L., Rosenman, G. and Gazit, E. (2009) Self-Assembled Arrays of Peptide Nanotubes by Vapour Deposition. Nature Nanotechnology, 4, 849-854.
https://doi.org/10.1038/nnano.2009.298
[14]
Mann, S., Archibald, D.D., Didymus, J.M., Douglas, T., Heywood, B.R., Meldrum, F.C. and Reeves, N.J. (1993) Crystallization at Inorganic-Organic Interfaces: Biominerals and Biomimetic Synthesis. Science, 261, 1286-1292.
https://doi.org/10.1126/science.261.5126.1286
[15]
Gazit, E. (2002) A Possible Role for π-Stacking in the Self-Assembly of Amyloid Fibrils. The FASEB Journal, 16, 77-83. https://doi.org/10.1096/fj.01-0442hyp
[16]
Gorbitz, C.H. (2001) Nanotube Formation by Hydrophobic Dipeptides. Chemistry—A European Journal, 7, 5153-5159.
https://doi.org/10.1002/1521-3765(20011203)7:23<5153::AID-CHEM5153>3.0.CO;2-N
[17]
Wang, M.J., Du, L.J., Wu, X.L., Xiong, S.J. and Chu, P.K. (2011) Charged Diphenylalanine Nanotubes and Controlled Hierarchical Self-Assembly. ACS Nano, 5, 4448-4454. https://doi.org/10.1021/nn2016524
[18]
Perriman, A.W., Brogan, A.P.S., Colfen, H., Tsoureas, N., Owen, G.R. and Mann, S. (2010) Reversible Dioxygen Binding in Solvent-Free Liquid Myoglobin. Nature Chemistry, 2, 622-626. https://doi.org/10.1038/nchem.700
[19]
Huang, R.L., Su, R.X., Qi, W., Zhao, J. and He, Z.M. (2011) Hierarchical, Interface-Induced Self-Assembly of Diphenylalanine: Formation of Peptide Nanofibers and Microvesicles. Nanotechnology, 22, Article ID: 245609.
https://doi.org/10.1088/0957-4484/22/24/245609
[20]
Reches, M. and Gazit, E. (2003) Casting Metal Nanowires within Discrete Self-Assembled Peptide Nanotubes. Science, 300, 625-627.
https://doi.org/10.1126/science.1082387
[21]
Reches, M. and Gazit, E. (2006) Controlled Patterning of Aligned Self-Assembled Peptide Nanotubes. Nature Nanotechnology, 1, 195-200.
https://doi.org/10.1038/nnano.2006.139
[22]
Kelly, C.M., Northey, T., Ryan, K., Brooks, B.R., Kholkin, A.L., Rodriguez, B.J. and Buchete, N.V. (2015) Conformational Dynamics and Aggregation Behavior of Piezoelectric Diphenylalanine Peptides in an External Electric Field. Biophysical Chemistry, 196, 16-24. https://doi.org/10.1016/j.bpc.2014.08.009
[23]
Walsh, D.M., Lomakin, A., Benedek, G.B., Condron, M.M. and Teplow, D.B. (1997) Amyloid β-Protein Fibril-logenesis: Detection of a Protofibrillar Intermediate. Journal of Biological Chemistry, 272, 22364-22372.
https://doi.org/10.1074/jbc.272.35.22364
[24]
Yuan, J.H., Chen, J.R., Wu, X.H., Fang, K.M. and Niu, L. (2011) A NADH Biosensor Based on Diphenylalanine Peptide/Carbon Nanotube Nanocomposite. Journal of Electroanalytical Chemistry, 656, 120-124.
https://doi.org/10.1016/j.jelechem.2010.12.018
[25]
Morgan, C., Colombres, M., Nunez, M.T. and Inestrosa, N.C. (2004) Structure and Function of Amyloid in Alzheimer’s Disease. Progress in Neurobiology, 74, 323-349.
https://doi.org/10.1016/j.pneurobio.2004.10.004
[26]
Kim, J.B, Han, T.H., Kim, Y.I., Park, J.S., Choi, J.W., Churchill, D.G., Kim, S.O. and Ihee, H. (2010) Role of Water in Directing Diphenylalanine Assembly into Nanotubes and Nanowires. Advance Materials, 22, 583-587.
https://doi.org/10.1002/adma.200901973
[27]
Mori, H., Takio, K., Ogawarag, M. and Selkoen, D.J. (1992) Mass Spectrometry of Purified Amyloid Beta Protein in Alzheimer’s Disease. Journal of Biological Chemistry, 267, 17082-17086. https://www.jbc.org/content/267/24/17082.short
[28]
Schmidt, M., Sachse, C., Richter, W., Xu, C., Fandrich, M. and Grigorieff, N. (2009) Comparison of Alzheimer Aβ(1-40) and Aβ(1-42) Amyloid Fibrils Reveals Similar Protofilament Structures. Proceedings of the National Academy of Sciences of the United States of America, 106, 19813-19818.
https://doi.org/10.1073/pnas.0905007106
[29]
Perutz, M.F., Finch, J.T., Berriman, J. and Lesk, A. (2002) Amyloid Fibers Are Water-Filled Nanotubes. Proceedings of the National Academy of Sciences of the United States of America, 99, 5591-5595. https://doi.org/10.1073/pnas.042681399
[30]
Widenbrant, M.J.O., Rajadas, J., Sutardja, C. and Fuller, G.G. (2006) Lipid-Induced β-Amyloid Peptide Assemblage Fragmentation. Biophysical Journal, 91, 4071-4080.
https://doi.org/10.1529/biophysj.106.085944
Nie, Q., Du, X.G. and Geng, M.Y. (2011) Small Molecule Inhibitors of Amyloid β Peptide Aggregation as a Potential Therapeutic Strategy for Alzheimer’s Disease. Acta Pharmacologica Sinica, 32, 545-551. https://doi.org/10.1038/aps.2011.14
[33]
Nikiforov, M.P., Thompson, G.L., Reukov, V.V., Jesse, S., Guo, S., Rodriguez, B.J., Seal, K., Vertegel, A.A. and Kalinin, S.V. (2010) Double-Layer Mediated Electromechanical Response of Amyloid Fibrils in Liquid Environment. ACS Nano, 4, 689-698. https://doi.org/10.1021/nn901127k
[34]
Tuszynski, J.A., John, T., Craddock, A. and Carpenter, E.J. (2008) Bio-Ferroelectricity at the Nanoscale Bio-Ferroelectricity at the Nanoscale. Journal of Computational and Theoretical Nanoscience, 5, 2022-2032.
https://doi.org/10.1166/jctn.2008.1008
[35]
Heredia, A., Bui, C.C., Suter, U., Young, P. and Schaffer, T.E. (2007) AFM Combines Functional and Morphological Analysis of Peripheral Myelinated and Demyelinated Nerve Fibers. Neuroimage, 37, 1218-1226.
https://doi.org/10.1016/j.neuroimage.2007.06.007
[36]
Heredia, A., Bdikin, I., Baltazar, G. and Kholkin, A. (2010) Ferroelectric Properties of Dried Rat Embryonic Neurons from the Substantia Nigra by the Piezoresponse Force Microscopy. European Cells and Materials, 20, 292.
http://www.scopus.com/inward/record.url?eid=2-s2.0-84860891306&partnerID=MN8TOARS
[37]
Heredia, A., Machado, M., Bdikin, I.K., Gracio, J., Yudin, S., Fridkin, V.M., Delgadillo, I. and Kholkin, A.L. (2010) Preferred Deposition of Phospholipids onto Ferroelectric P(VDF-TrFE) Films via Polarization Patterning. Journal of Physics D: Applied Physics, 43, Article ID: 335301.
https://doi.org/10.1088/0022-3727/43/33/335301
[38]
Kühnle, A. (2009) Self-Assembly of Organic Molecules at Metal Surfaces. Current Opinion in Colloid & Interface Science, 14, 157-168.
https://doi.org/10.1016/j.cocis.2008.01.001
[39]
Lu, K., Jacob, J., Thiyagarajan, P., Conticello, V.P. and Lynn, D.G. (2003) Exploiting Amyloid Pibril Lamination for Nanotube Self-Assembly. Journal of the American Chemical Society, 125, 6391-6393. https://doi.org/10.1021/ja0341642
[40]
Meinhardt, J., Sachse, C., Hortschansky, P., Grigorieff, N. and Fandrich, M. (2009) Aβ(1-40) Fibril Polymorphism Implies Diverse Interaction Patterns in Amyloid Fibrils. Journal of Molecular Biology, 386, 869-877.
https://doi.org/10.1016/j.jmb.2008.11.005
[41]
Faller, P., Hureau, C. and Berthoumieu, O. (2013) Role of Metal Ions in the Self-Assembly of the Alzheimer’s Amyloid-β Peptide. Inorganic Chemistry, 52, 12193-12206. https://doi.org/10.1021/ic4003059
[42]
Huang, R.L., Wang, Y.F., Qi, W., Su, R.X. and He, Z.M. (2014) Temperature-Induced Reversible Self-Assembly of Diphenylalanine Peptide and the Structural Transition from Organogel to Crystalline Nanowires. Nanoscale Research Letters, 9, Article No. 653. https://doi.org/10.1186/1556-276X-9-653
[43]
Kalinin, S.V., Rodriguez, B.J., Jesse, S., Thundat, T. and Gruverman, A. (2005) Electromechanical Imaging of Biological Systems with Sub-10nm Resolution. Applied Physics Letters, 87, Article ID: 053901. https://doi.org/10.1063/1.2006984
[44]
Zandomeneghi, G., Krebs, M.R.H., McCammon, M.G. and Fandrich, M. (2009) FTIR Reveals Structural Differences between Native β-Sheet Proteins and Amyloid Fibrils. Protein Science, 13, 3314-3321. https://doi.org/10.1110/ps.041024904
[45]
Dave, N., Lórenz-Fonfría, V.A., Leblanc, G. and Padrós, E. (2008) FTIR Spectroscopy of Secondary-Structure Reorientation of Melibiose Permease Modulated by Substrate Binding. Biophysical Journal, 94, 3659-3670.
https://doi.org/10.1529/biophysj.107.115550
[46]
Nguyen, V., Zhu, R., Jenkins, K. and Yang, R. (2016) Self-Assembly of Diphenylalanine Peptide with Controlled Polarization for Power Generation. Nature Communications, 7, Article No. 13566. https://doi.org/10.1038/ncomms13566
[47]
Wetzel, R., Shivaprasad, S. and Williams, A.D. (2007) Plasticity of Amyloid Fibrils. Biochemistry, 46, 1-10. https://doi.org/10.1021/bi0620959
[48]
Varghese, K., Molnar, P., Das, M., Bhargava, N., Lambert, S., Kindy, M.S. and Hickman, J.J. (2010) A New Target for Amyloid Beta Toxicity Validated by Standard and High-Throughput Electrophysiology. PLoS ONE, 5, e8643.
https://doi.org/10.1371/journal.pone.0008643
[49]
Brünger, A., kuriyan, J and karplus, M. (1987) Crystallographic R Factor Refinement by Molecular Dynamics. Science, 235, 458-460.
https://doi.org/10.1126/science.235.4787.458
[50]
Gupta, V. P. (2016) 12—Characterization of Chemical Reactions. In: Gupta, V.P., Ed., Principles and Applications of Quantum Chemistry, Academic Press, San Diego, 385-433. https://doi.org/10.1016/B978-0-12-803478-1.00012-1
[51]
Bystrov, V.S., Zelenovskiy, P.S., Nuraeva, A.S., Kopyl, S. and Zhulyabina, O.A. (2019) Molecular Modeling and Computational Study of the Chiral-Dependent Structures and Properties of Self-Assembling Diphenylalanine Peptide Nanotubes. Journal of Molecular Modeling, 25, Article No. 199.
https://doi.org/10.1007/s00894-019-4080-x
[52]
Hypercube, Inc. (2003) HyperChemTM Professional 7.51. Hypercube, Inc., Gainesville.
[53]
Dodda, L.S., Cabeza de Vaca, I., Tirado-Rives, J. and Jorgensen, W.L. (2017) LigParGen web Server: An Automatic OPLS-AA Parameter Generator for Organic Ligands. Nucleic Acids Research, 45, W331-W336.
https://doi.org/10.1093/nar/gkx312
[54]
Jorgensen, W.L. and Tirado-Rives, J. (2005) Molecular Modeling of Organic and Biomolecular Systems Using BOSS and MCPRO. Journal of Computational Chemistry, 26, 1689-1700. https://doi.org/10.1002/jcc.20297
[55]
Yabe, M., Mori, K., Ueda, K. and Takeda, M. (2019). Development of PolyParGen Software to Facilitate the Determination of Molecular Dynamics Simulation Parameters for Polymers. Journal of Computer Chemistry, Japan-International Edition, 5, 1-5. https://doi.org/10.2477/jccjie.2018-0034
[56]
Wang, J., Wang, W., Kollman, P.A. and Case, D.A. (2006) Automatic Atom Type and Bond Type Perception in Molecular Mechanical Calculations. Journal of Molecular Graphics and Modelling, 25, 247-260.
https://doi.org/10.1016/j.jmgm.2005.12.005
[57]
Sousa Da Silva, A.W. and Vranken, W.F. (2012) ACPYPE—AnteChamber PYthon Parser interfacE. BMC Research Notes, 5, Article No. 367.
https://doi.org/10.1186/1756-0500-5-367
[58]
Lindahl, E., Abraham, M.J., Hess, B. and van der Spoel, D. (2019) GROMACS 2019.4 Source Code. https://doi.org/10.5281/zenodo.3460414
[59]
Kutzner, C., Páll, S., Fechner, M., Esztermann, A., de Groot, B.L. and Grubmüller, H. (2019) More Bang for Your Buck: Improved Use of GPU Nodes for GROMACS 2018. Journal of Computational Chemistry, 40, 2418-2431.
https://doi.org/10.1002/jcc.26011
[60]
Kutzner, C., Páll, S., Fechner, M., Esztermann, A., de Groot, B.L. and Grubmüller, H. (2015) Best Bang for Your Buck: GPU Nodes for GROMACS Biomolecular Simulations. Journal of Computational Chemistry, 36, 1990-2008.
https://doi.org/10.1002/jcc.24030
[61]
Kilpelainen, T., Shahgholian, H. and Zhong, X. (2007) Growth Estimates Through Scaling for Quasilinear Partial Differential Equations. Annales Academiae Scientiarum Fennicae: Mathematica, 32, 595-599.
http://www.acadsci.fi/mathematica/Vol32/vol32pp595-599.pdf
[62]
Jorgensen, W.L., Maxwell, D.S. and Tirado-Rives, J. (1996) Development and Testing of the OPLS All-Atom Force Field on Conformational Energetics and Properties of Organic Liquids. Journal of the American Chemical Society, 118, 11225-11236.
https://doi.org/10.1021/ja9621760
