Modelling and analysis of early aggregation events of BMHP1-derived self-assembling peptides

References

• Auer, S., Dobson, C. M., & Vendruscolo, M. (2007). Characterization of the nucleation barriers for protein aggregation and amyloid formation. Hfsp Journal, 1, 137–146.
   PubMed Web of Science ®Google Scholar
• Bagautdinov, B., Kuroishi, C., Sugahara, M., & Kunishima, N. (2005). Crystal structures of biotin protein ligase from Pyrococcus horikoshii OT3 and its complexes: Structural basis of biotin activation. Journal of Molecular Biology, 353, 322–333.
   PubMedGoogle Scholar
• Berendsen, H. J. C., Postma, J. P. M., van Gunsteren, W. F., & Hermans, J. (1989). Interaction models for water in relation to protein hydration. In B. E. Pullman (Ed.), Intermolecular forces (pp. 331–342). Dordrecht: D. Reidel Publishing Company.
   Google Scholar
• Berendsen, H. J. C., Postma, J. P. M., Vangunsteren, W. F., Dinola, A., & Haak, J. R. (1984). Molecular-dynamics with coupling to an external bath. Journal of Chemical Physics, 81, 3684–3690.
   Web of Science ®Google Scholar
• Bowerman, C. J., Ryan, D. M., Nissan, D. A., & Nilsson, B. L. (2009). The effect of increasing hydrophobicity on the self-assembly of amphipathic beta-sheet peptides. Molecular Biosystems, 5, 1058–1069.
   PubMedGoogle Scholar
• Burley, S. K., & Petsko, G. A. (1985). Aromatic-aromatic interaction – A mechanism of protein-structure stabilization. Science, 229, 23–28.
   PubMed Web of Science ®Google Scholar
• Bussi, G., Donadio, D., & Parrinello, M. (2007). Canonical sampling through velocity rescaling. Journal of Chemical Physics, 126, 014101.
   Google Scholar
• Chapman-Smith, A., & Cronan, J. E. (1999). The enzymatic biotinylation of proteins: a post-translational modification of exceptional specificity. Trends in Biochemical Sciences, 24, 359–363.
   PubMed Web of Science ®Google Scholar
• Chilkoti, A., Tan, P. H., & Stayton, P. S. (1995). Site-directed mutagenesis studies of the high-affinity streptavidin-biotin complex – Contributions of tryptophan residue-79, residue-108, and residue-120. Proceedings of the National Academy of Sciences of the United States of America, 92, 1754–1758.
   PubMedGoogle Scholar
• Colombo, G., Daidone, I., Gazit, E., Amadei, A., & Di Nola, A. (2005). Molecular dynamics simulation of the aggregation of the core-recognition motif of the islet amylolid polypeptide in explicit water. Proteins-Structure Function and Bioinformatics, 59, 519–527.
   PubMed Web of Science ®Google Scholar
• Cross, S., Kuttel, M. M., Stone, J. E., & Gain, J. E. (2009). Visualisation of cyclic and multi-branched molecules with VMD. Journal of Molecular Graphics & Modelling, 28, 131–139.
   PubMedGoogle Scholar
• Darden, T., York, D., & Pedersen, L. (1993). Particle Mesh Ewald – An N.Log(N) Method for Ewald Sums in Large Systems. Journal of Chemical Physics, 98, 10089–10092.
   Web of Science ®Google Scholar
• Daura, X., Gademann, K., Jaun, B., Seebach, D., van Gunsteren, W. F., & Mark, A. E. (1999). Peptide folding: When simulation meets experiment. Angewandte Chemie-International Edition, 38, 236–240.
   Web of Science ®Google Scholar
• Dixit, S. B., & Chipot, C. (2001). Can absolute free energies of association be estimated from molecular mechanical simulations? The biotin-streptavidin system revisited. Journal of Physical Chemistry, A105, 9795–9799.
   Google Scholar
• Dolker, N., Zachariae, U., & Grubmuller, H. (2010). Hydrophilic linkers and polar contacts affect aggregation of FG repeat peptides. Biophysical Journal, 98, 2653–2661.
   PubMedGoogle Scholar
• Ellis-Behnke, R. G., Liang, Y. X., You, S. W., Tay, D. K. C., Zhang, S. G., So, K. F., & Schneider, G. E. (2006). Nano neuro knitting: Peptide nanofiber scaffold for brain repair and axon regeneration with functional return of vision. Proceedings of the National Academy of Sciences of the United States of America, 103, 5054–5059.
   PubMed Web of Science ®Google Scholar
• Freitag, S., Le Trong, I., Chilkoti, A., Klumb, L. A., Stayton, P. S., & Stenkamp, R. E. (1998). Structural studies of binding site tryptophan mutants in the high-affinity streptavidin–biotin complex. Journal of Molecular Biology, 279, 211–221.
   PubMedGoogle Scholar
• Freitag, S., LeTrong, I., Klumb, L., Stayton, P. S., & Stenkamp, R. E. (1997). Structural studies of the streptavidin binding loop. Protein Science, 6, 1157–1166.
   PubMed Web of Science ®Google Scholar
• Gazit, E. (2002). A possible role for pi-stacking in the self-assembly of amyloid fibrils. Faseb Journal, 16, 77–83.
   PubMed Web of Science ®Google Scholar
• Gelain, F., Horii, A., & Zhang, S. G. (2007). Designer self-assembling peptide scaffolds for 3-D tissue cell cultures and regenerative medicine. Macromolecular Bioscience, 7, 544–551.
   PubMed Web of Science ®Google Scholar
• Gelain, F., Panseri, S., Antonini, S., Cunha, C., Donega, M., Lowery, J., … Vescovi, A. (2011a). Transplantation of nanostructured composite scaffolds results in the regeneration of chronically injured spinal cords. ACS Nano, 5, 227–236.
   PubMedGoogle Scholar
• Gelain, F., Silva, D., Caprini, A., Taraballi, F., Natalello, A., Villa, O., … Vescovi, A. (2011b). BMHP1-derived self-assembling peptides: Hierarchically assembled structures with self-healing propensity and potential for tissue engineering applications. ACS Nano, 5, 1845–1859.
   PubMedGoogle Scholar
• Gravel, R. A., & Narang, M. A. (2005). Molecular genetics of biotin metabolism: Old vitamin, new science. Journal of Nutritional Biochemistry, 16, 428–431.
   PubMed Web of Science ®Google Scholar
• Green, N. M. (1975). Avidin. Advances in Protein Chemistry, 29, 85–133.
   PubMedGoogle Scholar
• Gsponer, J., & Vendruscolo, M. (2006). Theoretical approaches to protein aggregation. Protein and Peptide Letters, 13, 287–293.
   PubMedGoogle Scholar
• Halley, J. D., & Winkler, D. A. (2008). Consistent concepts of self-organization and self-assembly. Complexity, 14, 10–17.
   Web of Science ®Google Scholar
• Hess, B., Bekker, H., Berendsen, H. J. C., & Fraaije, J. G. E. M. (1997). LINCS: A linear constraint solver for molecular simulations. Journal of Computational Chemistry, 18, 1463–1472.
   Web of Science ®Google Scholar
• Hills, R. D., & Brooks, C. L. (2007). Hydrophobic cooperativity as a mechanism for amyloid nucleation. Journal of Molecular Biology, 368, 894–901.
   PubMedGoogle Scholar
• Humphrey, W., Dalke, A., & Schulten, K. (1996). VMD: Visual molecular dynamics. Journal of Molecular Graphics & Modelling, 14, 33–38.
   Web of Science ®Google Scholar
• Hunter, C. A., & Sanders, J. K. M. (1990). The nature of Pi–Pi interactions. Journal of the American Chemical Society, 112, 5525–5534.
   Web of Science ®Google Scholar
• Kabsch, W., & Sander, C. (1983). Dictionary of protein secondary structure – pattern-recognition of hydrogen-bonded and geometrical features. Biopolymers, 22, 2577–2637.
   PubMed Web of Science ®Google Scholar
• Le Trong, I., Freitag, S., Klumb, L. A., Chu, V., Stayton, P. S., & Stenkamp, R. E. (2003). Structural studies of hydrogen bonds in the high-affinity streptavidin–biotin complex: Mutations of amino acids interacting with the ureido oxygen of biotin. Acta Crystallographica Section D-Biological Crystallography, 59, 1567–1573.
   PubMed Web of Science ®Google Scholar
• Lehn, J. M. (1995). Supramolecular chemistry: Concepts and perspectives: A personal account built upon the George Fisher Baker lectures in chemistry at Cornell University [and] Lezioni Lincee, Accademia nazionale dei Lincei, Roma. Weinheim, NY: VCH.
   Google Scholar
• Li, Q. B., Gusarov, S., Evoy, S., & Kovalenko, A. (2009). Electronic structure, binding energy, and solvation structure of the streptavidin–biotin supramolecular complex: ONIOM and 3D-RISM study. Journal of Physical Chemistry, B113, 9958–9967.
   Google Scholar
• Liu, L., Busuttil, K., Zhang, S., Yang, Y. L., Wang, C., Besenbacher, F., & Dong, M. D. (2011). The role of self-assembling polypeptides in building nanomaterials. Physical Chemistry Chemical Physics, 13, 17435–17444.
   PubMedGoogle Scholar
• Lu, Y., Derreumaux, P., Guo, Z., Mousseau, N., & Wei, G. (2009). Thermodynamics and dynamics of amyloid peptide oligomerization are sequence dependent. Proteins-Structure Function and Genetics, 75, 954–963.
   PubMedGoogle Scholar
• Frisch, M., Trucks, G. W., Schlegel, H. B., Scuseria, G. E., Robb, M. A., Cheeseman, J. R., … Pople, J. A. (2004). Gaussian03, revision C.02. Wallingford, CT: Gaussian.
   Google Scholar
• Ma, B. Y., & Nussinov, R. (2002). Molecular dynamics simulations of alanine rich beta-sheet oligomers: Insight into amyloid formation. Protein Science, 11, 2335–2350.
   PubMed Web of Science ®Google Scholar
• Massi, F., & Straub, J. E. (2001). Energy landscape theory for Alzheimer’s amyloid beta-peptide fibril elongation. Proteins-Structure Function and Genetics, 42, 217–229.
   PubMed Web of Science ®Google Scholar
• Matson, J. B., & Stupp, S. I. (2012). Self-assembling peptide scaffolds for regenerative medicine. Chem Commun (Camb), 48, 26–33.
   PubMed Web of Science ®Google Scholar
• Matthes, D., Gapsys, V., Daebel, V., & de Groot, B. L. (2011). Mapping the conformational dynamics and pathways of spontaneous steric zipper peptide oligomerization. PLoS One, 6, e19129.
   Google Scholar
• Miyamoto, S., & Kollman, P. A. (1992). Settle – An analytical version of the shake and rattle algorithm for rigid water models. Journal of Computational Chemistry, 13, 952–962.
   Web of Science ®Google Scholar
• Miyamoto, S., & Kollman, P. A. (1993). Absolute and relative binding free-energy calculations of the interaction of biotin and its analogs with streptavidin using molecular-dynamics free-energy perturbation approaches. Proteins-Structure Function and Genetics, 16, 226–245.
   PubMed Web of Science ®Google Scholar
• Mu, Y., & Gao, Y. Q. (2009). Self-assembly of polypeptides into left-handedly twisted fibril-like structures. Physical Review E: Statistical, Nonlinear, and Soft Matter Physics, 80, 041927.
   Google Scholar
• Nam, H. B., Kouza, M., Zung, H., & Li, M. S. (2010). Relationship between population of the fibril-prone conformation in the monomeric state and oligomer formation times of peptides: Insights from all-atom simulations. Journal of Chemical Physics, 132, 165104.
   PubMedGoogle Scholar
• Nelson, R., Sawaya, M. R., Balbirnie, M., Madsen, A. O., Riekel, C., Grothe, R., & Eisenberg, D. (2005). Structure of the cross-beta spine of amyloid-like fibrils. Nature, 435, 773–778.
   PubMed Web of Science ®Google Scholar
• Nguyen, H. D., & Hall, C. K. (2004). Molecular dynamics simulations of spontaneous fibril formation by random-coil peptides. Proceedings of the National Academy of Sciences of the United States of America, 101, 16180–16185.
   PubMed Web of Science ®Google Scholar
• Nguyen, P. H., Li, M. S., Stock, G., Straub, J. E., & Thirumalai, D. (2007). Monomer adds to preformed structured oligomers of A beta-peptides by a two-stage dock-lock mechanism. Proceedings of the National Academy of Sciences of the United States of America, 104, 111–116.
   PubMed Web of Science ®Google Scholar
• Nguyen Truong, C., & Li, M. S. (2012). New method for determining size of critical nucleus of fibril formation of polypeptide chains. Journal of Chemical Physics, 137, 095101.
   Google Scholar
• Nowakowski, G. S., Dooner, M. S., Valinski, H. M., Mihaliak, A. M., Quesenberry, P. J., & Becker, P. S. (2004). A specific heptapeptide from a phage display peptide library homes to bone marrow and binds to primitive hematopoietic stem cells. Stem cells, 22, 1030–1038.
   PubMedGoogle Scholar
• Oostenbrink, C., Villa, A., Mark, A. E., & Van Gunsteren, W. F. (2004). A biomolecular force field based on the free enthalpy of hydration and solvation: The GROMOS force-field parameter sets 53A5 and 53A6. Journal of Computational Chemistry, 25, 1656–1676.
   PubMed Web of Science ®Google Scholar
• Pacheco-Alvarez, D., Solorzano-Vargas, R. S., & Del Rio, A. L. (2002). Biotin in metabolism and its relationship to human disease. Archives of Medical Research, 33, 439–447.
   PubMed Web of Science ®Google Scholar
• Seeber, M., Cecchini, M., Rao, F., Settanni, G., & Caflisch, A. (2007). Wordom: A program for efficient analysis of molecular dynamics simulations. Bioinformatics, 23, 2625–2627.
   PubMed Web of Science ®Google Scholar
• Senguen, F. T., Lee, N. R., Gu, X. F., Ryan, D. M., Doran, T. M., Anderson, E. A., & Nilsson, B. L. (2011). Probing aromatic, hydrophobic, and steric effects on the self-assembly of an amyloid-beta fragment peptide. Molecular Biosystems, 7, 486–496.
   PubMedGoogle Scholar
• Serpell, L. C. (2000). Alzheimer’s amyloid fibrils: Structure and assembly. Biochimica Et Biophysica Acta-Molecular Basis of Disease, 1502, 16–30.
   PubMed Web of Science ®Google Scholar
• Song, W., Wei, G. H., Mousseau, N., & Derreumaux, P. (2008). Self-assembly of the beta 2-microglobulin NHVTLSQ peptide using a coarse-grained protein model reveals beta-barrel species. Journal of Physical Chemistry, B112, 4410–4418.
   Google Scholar
• Straub, J. E., & Thirumalai, D. (2010). Principles governing oligomer formation in amyloidogenic peptides. Current Opinion in Structural Biology, 20, 187–195.
   PubMedGoogle Scholar
• Taraballi, F., Natalello, A., Campione, M., Villa, O., Doglia, S. M., Paleari, A., & Gelain, F. (2010). Glycine-spacers influence functional motifs exposure and self-assembling propensity of functionalized substrates tailored for neural stem cell cultures. Front Neuroeng, 3, 1–9.
   PubMedGoogle Scholar
• Thirumalai, D., Klimov, D. K., & Dima, R. I. (2003). Emerging ideas on the molecular basis of protein and peptide aggregation. Current Opinion in Structural Biology, 13, 146–159.
   PubMed Web of Science ®Google Scholar
• Tsemekhman, K., Goldschmidt, L., Eisenberg, D., & Baker, D. (2007). Cooperative hydrogen bonding in amyloid formation. Protein Science, 16, 761–764.
   PubMed Web of Science ®Google Scholar
• Van der Spoel, D., Lindahl, E., Hess, B., Groenhof, G., Mark, A. E., & Berendsen, H. J. C. (2005). GROMACS: Fast, flexible, and free. Journal of Computational Chemistry, 26, 1701–1718.
   PubMed Web of Science ®Google Scholar
• Viet, M. H., Ngo, S. T., Lam, N. S., & Li, M. S. (2011). Inhibition of aggregation of amyloid peptides by beta-sheet breaker peptides and their binding affinity. Journal of Physical Chemistry, B115, 7433–7446.
   Google Scholar
• Waters, M. L. (2002). Aromatic interactions in model systems. Current Opinion in Chemical Biology, 6, 736–741.
   PubMed Web of Science ®Google Scholar
• Weber, P. C., Ohlendorf, D. H., Wendoloski, J. J., & Salemme, F. R. (1989). Structural origins of high-affinity biotin binding to streptavidin. Science, 243, 85–88.
   PubMed Web of Science ®Google Scholar
• Weber, P. C., Wendoloski, J. J., Pantoliano, M. W., & Salemme, F. R. (1992). Crystallographic and thermodynamic comparison of natural and synthetic ligands bound to streptavidin. Journal of the American Chemical Society, 114, 3197–3200.
   Web of Science ®Google Scholar
• Wilson, K. P., Shewchuk, L. M., Brennan, R. G., Otsuka, A. J., & Matthews, B. W. (1992). Escherichia-coli biotin holoenzyme synthetase biorepressor crystal-structure delineates the biotin-binding and DNA-binding domains. Proceedings of the National Academy of Sciences of the United States of America, 89, 9257–9261.
   PubMed Web of Science ®Google Scholar
• Wood, Z. A., Weaverl, L. H., Brown, P. H., Beckett, D., & Matthews, B. W. (2006). Co-repressor induced order and biotin repressor dimerization: A case for divergent followed by convergent evolution. Journal of Molecular Biology, 357, 509–523.
   PubMedGoogle Scholar
• Wood, S. J., Wetzel, R., Martin, J. D., & Hurle, M. R. (1995). Prolines and amyloidogenicity in fragments of the Alzheimer’s peptide beta/A4. Biochemistry, 34, 724–730.
   PubMed Web of Science ®Google Scholar
• Xia, Z., Das, P., Shakhnovich, E. I., & Zhou, R. H. (2012). Collapse of unfolded proteins in a mixture of denaturants. Journal of the American Chemical Society, 134, 18266–18274.
   PubMedGoogle Scholar
• Ye, Z. Y., Zhang, H. Y., Luo, H. L., Wang, S. K., Zhou, Q. H., Du, X. P., … Zhao, X. J. (2008). Temperature and pH effects on biophysical and morphological properties of self-assembling peptide RADA16-1. Journal of Peptide Science, 14, 152–162.
   PubMed Web of Science ®Google Scholar
• Zanuy, D., Ma, B. Y., & Nussinov, R. (2003). Short peptide amyloid organization: Stabilities and conformations of the islet amyloid peptide NFGAIL. Biophysical Journal, 84, 1884–1894.
   PubMed Web of Science ®Google Scholar
• Zanuy, D., & Nussinov, R. (2003). The sequence dependence of fiber organization. A comparative molecular dynamics study of the islet amyloid polypeptide segments 22-27 and 22-29. Journal of Molecular Biology, 329, 565–584.
   PubMed Web of Science ®Google Scholar
• Zhao, J. H., Liu, H. L., Liu, Y. F., Lin, H. Y., Fang, H. W., Ho, Y., & Tsai, W. B. (2009). Molecular dynamics simulations to investigate the aggregation behaviors of the a beta(17-42) oligomers. Journal of Biomolecular Structure & Dynamics, 26, 481–490.
   PubMed Web of Science ®Google Scholar