Investigating the Disordered and Membrane-Active Peptide A-Cage-C Using Conformational Ensembles
Abstract
:1. Introduction
2. Results
2.1. Selected Predicted Properties of A-Cage-C
2.2. Isotope Labelling of A-Cage-C and Preparation of Bicelles
2.3. pH-Induced Conformational Changes
2.4. Structural Ensembles in the Presence and Absence of Bicelles
2.5. Molecular Dynamics Simulations in the Presence of Bilayers
3. Discussion
4. Materials and Methods
4.1. Primary Sequence Analysis
4.2. Protein Expression and Purification
4.3. Preparation and Characterization of Bicelles
4.4. NMR Acquisition and Resonance Assignment
4.5. Flexible-Meccano and Cluster Analysis
4.6. Molecular Dynamics Simulations
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
Sample Availability
References
- Muller, G.; Bandlow, W. An amphitropic cAMP-binding protein in yeast mitochondria. 2. Phospholipid nature of the membrane anchor. Biochemistry 1989, 28, 9968–9973. [Google Scholar] [CrossRef] [Green Version]
- Cornell, R.B.; Ridgway, N.D. CTP:phosphocholine cytidylyltransferase: Function, regulation, and structure of an amphitropic enzyme required for membrane biogenesis. Prog. Lipid. Res. 2015, 59, 147–171. [Google Scholar] [CrossRef] [PubMed]
- Goni, F.M.; Goñi, F.M. Non-permanent proteins in membranes: When proteins come as visitors (Review). Mol. Membr. Biol. 2002, 19, 237–245. [Google Scholar] [CrossRef]
- Halskau, Ø.; Muga, A.; Martínez, A. Linking New Paradigms in Protein Chemistry to Reversible Membrane-Protein Interactions. Curr. Protein Pept. Sci. 2009, 10, 339–359. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Babiychuk, E.B.; Draeger, A. Annexins in cell membrane dynamics. Ca(2+)-regulated association of lipid microdomains. J. Cell Biol. 2000, 150, 1113–1124. [Google Scholar] [CrossRef] [PubMed]
- Kovacic, J.; Bozic, B.; Svetina, S. Budding of giant unilamellar vesicles induced by an amphitropic protein beta2-glycoprotein I. Biophys. Chem. 2010, 152, 46–54. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Karlsson, T.; Altankhuyag, A.; Dobrovolska, O.; Turcu, D.C.; Lewis, A.E. A polybasic motif in ErbB3-binding protein 1 (EBP1) has key functions in nucleolar localization and polyphosphoinositide interaction. Biochem. J. 2016, 473, 2033–2047. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Babiychuk, E.B.; Palstra, R.J.; Schaller, J.; Kampfer, U.; Draeger, A. Annexin VI participates in the formation of a reversible, membrane-cytoskeleton complex in smooth muscle cells. J. Biol. Chem. 1999, 274, 35191–35195. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Johnson, J.E.; Cornell, R.B. Amphitropic proteins: Regulation by reversible membrane interactions. Mol. Membr. Biol. 1999, 16, 217–235. [Google Scholar] [CrossRef]
- Guerin, M.E.; Kordulakova, J.; Schaeffer, F.; Svetlikova, Z.; Buschiazzo, A.; Giganti, D.; Gicquel, B.; Mikusova, K.; Jackson, M.; Alzari, P.M. Molecular recognition and interfacial catalysis by the essential phosphatidylinositol mannosyltransferase PimA from mycobacteria. J. Biol. Chem. 2007, 282, 20705–20714. [Google Scholar] [CrossRef] [Green Version]
- Vogler, O.; Barcelo, J.M.; Ribas, C.; Escriba, P. V Membrane interactions of G proteins and other related proteins. Biochim. Biophys. Acta 2008, 1778, 1640–1652. [Google Scholar] [CrossRef] [Green Version]
- Skjevik, Å.A.; Mileni, M.; Baumann, A.; Halskau, Ø.; Teigen, K.; Stevens, R.C.; Martinez, A. The N-Terminal Sequence of Tyrosine Hydroxylase Is a Conformationally Versatile Motif That Binds 14-3-3 Proteins and Membranes. J. Mol. Biol. 2013, 426, 150–168. [Google Scholar] [CrossRef] [Green Version]
- Schillinger, A.S.; Grauffel, C.; Khan, H.M.; Halskau, Ø.; Reuter, N. Two homologous neutrophil serine proteases bind to POPC vesicles with different affinities: When aromatic amino acids matter. Biochim. Biophys. Acta Biomembr. 2014, 1838, 3191–3202. [Google Scholar] [CrossRef] [Green Version]
- Ma, J.; Yoshimura, M.; Yamashita, E.; Nakagawa, A.; Ito, A.; Tsukihara, T. Structure of rat monoamine oxidase A and its specific recognitions for substrates and inhibitors. J. Mol. Biol. 2004, 338. [Google Scholar] [CrossRef] [PubMed]
- Butko, P.; Huang, F.; Pusztai-Carey, M.; Surewicz, W.K. Interaction of the delta-endotoxin CytA from Bacillus thuringiensis var. israelensis with lipid membranes. Biochemistry 1997, 36, 12862–12868. [Google Scholar] [CrossRef]
- Mo, Y.; Campos, B.; Mealy, T.R.; Commodore, L.; Head, J.F.; Dedman, J.R.; Seaton, B.A. Interfacial basic cluster in annexin V couples phospholipid binding and trimer formation on membrane surfaces. J. Biol. Chem. 2003, 278, 2437–2443. [Google Scholar] [CrossRef] [Green Version]
- Johnson, J.E.; Xie, M.; Singh, L.M.R.; Edge, R.; Cornell, R.B. Both acidic and basic amino acids in an amphitropic enzyme, CTP:phosphocholine cytidylyltransferase, dictate its selectivity for anionic membranes. J. Biol. Chem. 2003, 278, 514–522. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Halskau, O.; Froystein, N.A.; Muga, A.; Martinez, A. The membrane-bound conformation of alpha-lactalbumin studied by NMR-monitored 1H exchange. J. Mol. Biol. 2002, 321, 99–110. [Google Scholar] [CrossRef]
- Grauffel, C.; Yang, B.; He, T.; Roberts, M.F.; Gershenson, A.; Reuter, N. Cation-pi interactions as lipid-specific anchors for phosphatidylinositol-specific phospholipase C. J. Am. Chem. Soc. 2013, 135, 5740–5750. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Di Venere, A.; Nicolai, E.; Ivanov, I.; Dainese, E.; Adel, S.; Angelucci, B.C.; Kuhn, H.; Maccarrone, M.; Mei, G. Probing conformational changes in lipoxygenases upon membrane binding: Fine-tuning by the active site inhibitor ETYA. Biochim. Biophys. Acta 2014, 1841, 1–10. [Google Scholar] [CrossRef] [PubMed]
- Stöckl, M.; Fischer, P.; Wanker, E.; Herrmann, A. α-Synuclein Selectively Binds to Anionic Phospholipids Embedded in Liquid-Disordered Domains. J. Mol. Biol. 2008, 375, 1394–1404. [Google Scholar] [CrossRef] [PubMed]
- Halskau, Ø.; Ying, M.; Baumann, A.; Kleppe, R.; Rodriguez-Larrea, D.; Almås, B.; Haavik, J.; Martinez, A. Three-way interaction between 14-3-3 proteins, the N-terminal region of tyrosine hydroxylase, and negatively charged membranes. J. Biol. Chem. 2009, 284, 32758–32769. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Määttä, T.A.; Rettel, M.; Sridharan, S.; Helm, D.; Kurzawa, N.; Stein, F.; Savitski, M.M. Aggregation and disaggregation features of the human proteome. Mol. Syst. Biol. 2020. [Google Scholar] [CrossRef] [PubMed]
- Yanagisawa, K.; McLaurin, J.; Michikawa, M.; Chakrabartty, A.; Ihara, Y. Amyloid beta-protein (A beta) associated with lipid molecules: Immunoreactivity distinct from that of soluble A beta. FEBS Lett. 1997, 420, 43–46. [Google Scholar] [CrossRef] [Green Version]
- Hellstrand, E.; Nowacka, A.; Topgaard, D.; Linse, S.; Sparr, E. Membrane Lipid Co-Aggregation with α-Synuclein Fibrils. PLoS ONE 2013, 8, e77235. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kayed, R.; Sokolov, Y.; Edmonds, B.; McIntire, T.M.; Milton, S.C.; Hall, J.E.; Glabe, C.G. Permeabilization of Lipid Bilayers Is a Common Conformation-dependent Activity of Soluble Amyloid Oligomers in Protein Misfolding Diseases. J. Biol. Chem. 2004, 279, 46363–46366. [Google Scholar] [CrossRef] [Green Version]
- Butterfield, S.M.; Lashuel, H.A. Amyloidogenic protein-membrane interactions: Mechanistic insight from model systems. Angew. Chem. Int. Ed. 2010, 49, 5628–5654. [Google Scholar] [CrossRef]
- Brew, K.; Vanaman, T.C.; Hill, R.L. The role of alpha-lactalbumin and the A protein in lactose synthetase: A unique mechanism for the control of a biological reaction. Proc. Natl. Acad. Sci. USA 1968, 59, 491–497. [Google Scholar] [CrossRef] [Green Version]
- Banuelos, S.; Muga, A. Structural requirements for the association of native and partially folded conformations of alpha-lactalbumin with model membranes. Biochemistry 1996, 35, 3892–3898. [Google Scholar] [CrossRef] [PubMed]
- Banuelos, S.; Muga, A. Interaction of native and partially folded conformations of alpha-lactalbumin with lipid bilayers: Characterization of two membrane-bound states. FEBS Lett. 1996, 386, 21–25. [Google Scholar] [CrossRef] [Green Version]
- Chenal, A.; Vernier, G.; Savarin, P.; Bushmarina, N.A.; Geze, A.; Guillain, F.; Gillet, D.; Forge, V. Conformational states and thermodynamics of alpha-lactalbumin bound to membranes: A case study of the effects of pH, calcium, lipid membrane curvature and charge. J. Mol. Biol. 2005, 349, 890–905. [Google Scholar] [CrossRef] [PubMed]
- Agasøster, A.V.; Halskau, Ø.; Fuglebakk, E.; Frøystein, N.Å.; Muga, A.; Holmsen, H.; Martínez, A. The Interaction of Peripheral Proteins and Membranes Studied with α-Lactalbumin and Phospholipid Bilayers of Various Compositions. J. Biol. Chem. 2003, 278, 21790–21797. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Baumann, A.; Gjerde, A.U.; Ying, M.; Svanborg, C.; Holmsen, H.; Glomm, W.R.; Martinez, A.; Halskau, E.; Halskau, Ø. HAMLET forms annular oligomers when deposited with phospholipid monolayers. J. Mol. Biol. 2012, 418, 90–102. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Strømland, Ø.; Handegård, Ø.S.; Govasli, M.L.; Wen, H.; Halskau, Ø. Peptides derived from α-lactalbumin membrane binding helices oligomerize in presence of lipids and disrupt bilayers. Biochim. Biophys. Acta Biomembr. 2017, 1859, 1029–1039. [Google Scholar] [CrossRef]
- Neidigh, J.W.; Fesinmeyer, R.M.; Andersen, N.H. Designing a 20-residue protein. Nat. Struct. Biol. 2002, 9, 425–430. [Google Scholar] [CrossRef] [PubMed]
- Delavari, B.; Mamashli, F.; Bigdeli, B.; Poursoleiman, A.; Karami, L.; Zolmajd-Haghighi, Z.; Ghasemi, A.; Samaei-Daryan, S.; Hosseini, M.; Haertlé, T.; et al. A biophysical study on the mechanism of interactions of DOX or PTX with α-lactalbumin as a delivery carrier. Sci. Rep. 2018, 8, 1–21. [Google Scholar] [CrossRef] [Green Version]
- Tanford, C. Amino acid scale: Hydrophobicity scale—Contribution of hydrophobic interactions to the stability of the globular conformation of proteins). J. Am. Chem. Soc. 1962, 84, 4240–4274. [Google Scholar] [CrossRef]
- Jones, D.T. Protein secondary structure prediction based on position-specific scoring matrices. J. Mol. Biol. 1999. [Google Scholar] [CrossRef] [Green Version]
- Linding, R.; Jensen, L.J.; Diella, F.; Bork, P.; Gibson, T.J.; Russell, R.B. Protein disorder prediction: Implications for structural proteomics. Structure 2003. [Google Scholar] [CrossRef] [Green Version]
- Tsolis, A.; Papandreou, N.; Iconomidou, V.A.; Hamodrakas, S.J. A Consensus Method for the Prediction of ‘Aggregation-Prone’ Peptides in Globular Proteins. PLoS ONE 2013, 8, e54175. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Moores, B.; Drolle, E.; Attwood, S.J.; Simons, J.; Leonenko, Z. Effect of Surfaces on Amyloid Fibril Formation. PLoS ONE 2011, 6, e25954. [Google Scholar] [CrossRef] [PubMed]
- Eliezer, D. Biophysical characterization of intrinsically disordered proteins. Curr. Opin. Struct. Biol. 2009, 19, 23–30. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sanders, C.R.; Sönnichsen, F. Solution NMR of membrane proteins: Practice and challenges. Magn. Reson. Chem. 2006, 44, S24–S40. [Google Scholar] [CrossRef]
- Kleckner, I.R.; Foster, M.P. An introduction to NMR-based approaches for measuring protein dynamics. Biochim. Biophys. Acta Proteins Proteom. 2011, 1814, 942–968. [Google Scholar] [CrossRef] [Green Version]
- Sanders, C.R.; Prosser, R.S. Bicelles: A model membrane system for all seasons? Structure 1998. [Google Scholar] [CrossRef] [Green Version]
- Vestergaard, M.; Kraft, J.F.; Vosegaard, T.; Thøgersen, L.; Schiøtt, B. Bicelles and Other Membrane Mimics: Comparison of Structure, Properties, and Dynamics from MD Simulations. J. Phys. Chem. B 2015, 119, 15831–15843. [Google Scholar] [CrossRef]
- Glover, K.J.; Whiles, J.A.; Wu, G.; Yu, N.J.; Deems, R.; Struppe, J.O.; Stark, R.E.; Komives, E.A.; Vold, R.R. Structural evaluation of phospholipid bicelles for solution-state studies of membrane-associated biomolecules. Biophys. J. 2001, 81, 2163–2171. [Google Scholar] [CrossRef] [Green Version]
- Diller, A.; Loudet, C.; Aussenac, F.; Raffard, G.; Fournier, S.; Laguerre, M.; Grélard, A.; Opella, S.J.; Marassi, F.M.; Dufourc, E.J. Bicelles: A natural “molecular goniometer” for structural, dynamical and topological studies of molecules in membranes. Biochimie 2009, 91, 744–751. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Dufourc, E.J. Bicelles and nanodiscs for biophysical chemistry1. Biochim. Biophys. Acta Biomembr. 2021, 1863. [Google Scholar] [CrossRef] [PubMed]
- Wu, H.; Su, K.; Guan, X.; Sublette, M.E.; Stark, R.E. Assessing the size, stability, and utility of isotropically tumbling bicelle systems for structural biology. Biochim. Biophys. Acta Biomembr. 2010, 1798, 482–488. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Morrison, E.A.; Henzler-Wildman, K.A. Reconstitution of integral membrane proteins into isotropic bicelles with improved sample stability and expanded lipid composition profile. Biochim. Biophys. Acta Biomembr. 2012. [Google Scholar] [CrossRef] [Green Version]
- Ujwal, R.; Bowie, J.U. Crystallizing membrane proteins using lipidic bicelles. Methods 2011, 55, 337–341. [Google Scholar] [CrossRef] [Green Version]
- Bosco, M.; Culeddu, N.; Toffanin, R.; Pollesello, P. Organic solvent systems for 31P nuclear magnetic resonance analysis of lecithin phospholipids: Applications to two-dimensional gradient-enhanced 1H-detected heteronuclear multiple quantum coherence experiments. Anal. Biochem. 1997, 245, 38–47. [Google Scholar] [CrossRef] [PubMed]
- Jakubec, M.; Bariås, E.; Furse, S.; Govasli, M.L.; George, V.; Turcu, D.; Iashchishyn, I.A.; Morozova-Roche, L.A.; Halskau, Ø. Cholesterol-containing lipid nanodiscs promote an α-synuclein binding mode that accelerates oligomerization. FEBS J. 2020. [Google Scholar] [CrossRef] [PubMed]
- Shortridge, M.D.; Hage, D.S.; Harbison, G.S.; Powers, R. Estimating Protein-Ligand Binding Affinity using High- Throughput Screening by NMR. J. Comb. Chem. 2009, 10, 948–958. [Google Scholar] [CrossRef] [Green Version]
- Ozenne, V.; Bauer, F.; Salmon, L.; Huang, J.R.; Jensen, M.R.; Segard, S.; Bernadó, P.; Charavay, C.; Blackledge, M. Flexible-meccano: A tool for the generation of explicit ensemble descriptions of intrinsically disordered proteins and their associated experimental observables. Bioinformatics 2012. [Google Scholar] [CrossRef] [PubMed]
- Davies, D.L.; Bouldin, D.W. A cluster separation measure. IEEE Trans. Pattern Anal. Mach. Intell 1979, 1, 224–227. [Google Scholar] [CrossRef] [PubMed]
- Shao, J.; Tanner, S.W.; Thompson, N.; Cheatham, T.E., III. Clustering Molecular Dynamics Trajectories: 1. Characterizing the Performance of Different Clustering Algorithms. J. Chem. Theory Comput. 2007, 3, 2312–2334. [Google Scholar] [CrossRef] [PubMed]
- Luchette, P.A.; Vetman, T.N.; Prosser, R.S.; Hancock, R.E.W.; Nieh, M.P.; Glinka, C.J.; Krueger, S.; Katsaras, J. Morphology of fast-tumbling bicelles: A small angle neutron scattering and NMR study. Biochim. Biophys. Acta Biomembr. 2001, 1513, 83–94. [Google Scholar] [CrossRef]
- Sarker, M.; Speckert, M.; Rainey, J.K. Bicelle composition-dependent modulation of phospholipid dynamics by apelin peptides. Biochem. Cell Biol. 2019, 97, 325–332. [Google Scholar] [CrossRef] [PubMed]
- Bodor, A.; Kövér, K.E.; Mäler, L. Membrane interactions in small fast-tumbling bicelles as studied by 31P NMR. Biochim. Biophys. Acta Biomembr. 2015. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Piana, S.; Donchev, A.G.; Robustelli, P.; Shaw, D.E. Water dispersion interactions strongly influence simulated structural properties of disordered protein states. J. Phys. Chem. B 2015, 119, 5113–5123. [Google Scholar] [CrossRef] [PubMed]
- Zapletal, V.; Mládek, A.; Melková, K.; Louša, P.; Nomilner, E.; Jaseňáková, Z.; Kubáň, V.; Makovická, M.; Laníková, A.; Žídek, L.; et al. Choice of Force Field for Proteins Containing Structured and Intrinsically Disordered Regions. Biophys. J. 2020, 118, 1621–1633. [Google Scholar] [CrossRef] [PubMed]
- Mossberg, A.-K.; Puchades, M.; Halskau, Ø.; Baumann, A.; Lanekoff, I.; Chao, Y.; Martinez, A.; Svanborg, C.; Karlsson, R. HAMLET Interacts with Lipid Membranes and Perturbs Their Structure and Integrity. PLoS ONE 2010, 5, e9384. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Voegele, A.; Subrini, O.; Sapay, N.; Ladant, D.; Chenal, A. Membrane-Active Properties of an Amphitropic Peptide from the CyaA Toxin Translocation Region. Toxins 2017, 9, 369. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Rodland, I.; Halskau, O.; Martinez, A.; Holmsen, H. alpha-Lactalbumin binding and membrane integrity--effect of charge and degree of unsaturation of glycerophospholipids. Biochim. Biophys. Acta 2005, 1717, 11–20. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Aliakbari, F.; Mohammad-Beigi, H.; Rezaei-Ghaleh, N.; Becker, S.; Dehghani Esmatabad, F.; Eslampanah Seyedi, H.A.; Bardania, H.; Tayaranian Marvian, A.; Collingwood, J.F.; Christiansen, G.; et al. The potential of zwitterionic nanoliposomes against neurotoxic alpha-synuclein aggregates in Parkinson’s Disease. Nanoscale 2018. [Google Scholar] [CrossRef]
- Viennet, T.; Wördehoff, M.M.; Uluca, B.; Poojari, C.; Shaykhalishahi, H.; Willbold, D.; Strodel, B.; Heise, H.; Buell, A.K.; Hoyer, W.; et al. Structural insights from lipid-bilayer nanodiscs link α-Synuclein membrane-binding modes to amyloid fibril formation. Commun. Biol. 2018, 1, 1–12. [Google Scholar] [CrossRef] [Green Version]
- Fantini, J.; Yahi, N. Molecular insights into amyloid regulation by membrane cholesterol and sphingolipids: Common mechanisms in neurodegenerative diseases. Expert Rev. Mol. Med. 2010, 12, 1–22. [Google Scholar] [CrossRef] [PubMed]
- Lundback, A.K.; van den Berg, S.; Hebert, H.; Berglund, H.; Eshaghi, S. Exploring the activity of tobacco etch virus protease in detergent solutions. Anal. Biochem 2008, 382, 69–71. [Google Scholar] [CrossRef] [PubMed]
- Conchillo-Solé, O.; de Groot, N.S.; Avilés, F.X.; Vendrell, J.; Daura, X.; Ventura, S. AGGRESCAN: A server for the prediction and evaluation of “hot spots” of aggregation in polypeptides. BMC Bioinformatics 2007, 8. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- O’Donnell, C.W.; Waldispühl, J.; Lis, M.; Halfmann, R.; Devadas, S.; Lindquist, S.; Berger, B. A method for probing the mutational landscape of amyloid structure. Bioinformatics 2011, 27. [Google Scholar] [CrossRef] [Green Version]
- De la Paz, M.L.; Serrano, L. Sequence determinants of amyloid fibril formation. Proc. Natl. Acad. Sci. USA 2004, 101, 87–92. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Galzitskaya, O.V.; Garbuzynskiy, S.O.; Lobanov, M.Y. Prediction of amyloidogenic and disordered regions in protein chains. PLoS Comput. Biol. 2006, 2, 1639–1648. [Google Scholar] [CrossRef] [PubMed]
- Zibaee, S.; Makin, O.S.; Goedert, M.; Serpell, L.C. A simple algorithm locates β-strands in the amyloid fibril core of α-synuclein, Aβ, and tau using the amino acid sequence alone. Protein Sci. 2007, 16, 906–918. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhang, Z.; Chen, H.; Lai, L. Identification of amyloid fibril-forming segments based on structure and residue-based statistical potential. Bioinformatics 2007, 23, 2218–2225. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kim, C.; Choi, J.; Lee, S.J.; Welsh, W.J.; Yoon, S. NetCSSP: Web application for predicting chameleon sequences and amyloid fibril formation. Nucleic Acids Res. 2009, 37. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Tian, J.; Wu, N.; Guo, J.; Fan, Y. Prediction of amyloid fibril-forming segments based on a support vector machine. BMC Bioinform. 2009, 10, S45. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hamodrakas, S.J.; Liappa, C.; Iconomidou, V.A. Consensus prediction of amyloidogenic determinants in amyloid fibril-forming proteins. Int. J. Biol. Macromol. 2007, 41, 295–300. [Google Scholar] [CrossRef] [PubMed]
- Maurer-Stroh, S.; Debulpaep, M.; Kuemmerer, N.; De La Paz, M.L.; Martins, I.C.; Reumers, J.; Morris, K.L.; Copland, A.; Serpell, L.; Serrano, L.; et al. Exploring the sequence determinants of amyloid structure using position-specific scoring matrices. Nat. Methods 2010, 7, 237–242. [Google Scholar] [CrossRef] [PubMed]
- Fernandez-Escamilla, A.M.; Rousseau, F.; Schymkowitz, J.; Serrano, L. Prediction of sequence-dependent and mutational effects on the aggregation of peptides and proteins. Nat. Biotechnol. 2004, 22, 1302–1306. [Google Scholar] [CrossRef] [PubMed]
- Keller, R. Optimizing the process of nuclear magnetic resonance spectrum analysis and computer aided resonance assignment. Swiss Fed. Inst. Technol. Zurich 2004. [Google Scholar] [CrossRef]
- Marsh, J.A.; Singh, V.K.; Jia, Z.; Forman-Kay, J.D. Sensitivity of secondary structure propensities to sequence differences between α- and γ-synuclein: Implications for fibrillation. Protein Sci. 2006. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Case, D.A.; Betz, R.M.; Botello-Smith, W.; Cerutti, D.S.; Cheatham, T.E., III.; Darden, T.A.; Duke, R.E.; Giese, T.J.; Gohlke, H.; Götz, A.W.; et al. AMBER 16 2016 Reference Manual, 1–923. Available online: http://ambermd.org/doc12/Amber16.pdf (accessed on 10 June 2021).
- Roe, D.R.; Cheatham III, T.E. PTRAJ and CPPTRAJ: Software for processing and analysis of molecular dynamics trajectory data. J. Chem. Theory Comput. 2013, 9, 3084–3095. [Google Scholar] [CrossRef]
- Humphrey, W.; Dalke, A.; Schulten, K. VMD: Visual molecular dynamics. J. Mol. Graph. 1996, 14, 33–38. [Google Scholar] [CrossRef]
- Kabsch, W.; Sander, C. Dictionary of protein secondary structure: Pattern recognition of hydrogen-bonded and geometrical features. Biopolymers 1983, 22, 2577–2637. [Google Scholar] [CrossRef]
- Weiser, J.; Shenkin, P.S.; Still, W.C. Approximate atomic surfaces from linear combinations of pairwise overlaps (LCPO). J. Comput Chem. 1999, 20, 217–230. [Google Scholar] [CrossRef]
- Maier, J.A.; Martinez, C.; Kasavajhala, K.; Wickstrom, L.; Hauser, K.E.; Simmerling, C. ff14SB: Improving the Accuracy of Protein Side Chain and Backbone Parameters from ff99SB. J. Chem. Theory Comput. 2015, 11, 3696–3713. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Jorgensen, W.L.; Chandrasekhar, J.; Madura, J.D.; Impey, R.W.; Klein, M.L. Comparison of simple potential functions for simulating liquid water. J. Chem. Phys. 1983, 79, 926–935. [Google Scholar] [CrossRef]
- Dickson, C.J.; Madej, B.D.; Skjevik, Å.A.; Betz, R.M.; Teigen, K.; Gould, I.R.; Walker, R.C. Lipid14: The amber lipid force field. J. Chem. Theory Comput. 2014, 10, 865–879. [Google Scholar] [CrossRef] [PubMed]
- Skjevik, Å.A.; Madej, B.D.; Dickson, C.J.; Lin, C.; Teigen, K.; Walker, R.C.; Gould, I.R. Simulation of lipid bilayer self-assembly using all-atom lipid force fields. Phys. Chem. Chem. Phys. 2016, 18, 10573–10584. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Åqvist, J. Ion-water interaction potentials derived from free energy perturbation simulations. J. Phys. Chem. 1990, 94, 8021–8024. [Google Scholar] [CrossRef]
- Götz, A.W.; Williamson, M.J.; Xu, D.; Poole, D.; Le Grand, S.; Walker, R.C. Routine microsecond molecular dynamics simulations with AMBER on GPUs. 1. generalized born. J. Chem. Theory Comput. 2012, 8, 1542–1555. [Google Scholar] [CrossRef] [PubMed]
- Salomon-Ferrer, R.; Götz, A.W.; Poole, D.; Le Grand, S.; Walker, R.C. Routine microsecond molecular dynamics simulations with AMBER on GPUs. 2. Explicit solvent particle mesh ewald. J. Chem. Theory Comput. 2013, 9, 3878–3888. [Google Scholar] [CrossRef] [PubMed]
- Case, D.A.; Betz, R.M.; Botello-Smith, W.; Cerutti, D.S.; Cheatham, T.E.; Darden, T.A.; Duke, R.E.; Giese, T.J.; Gohlke, H.; Götz, A.W.; et al. AMBER 18 2018 Reference Manual, pp. 1–927. Available online: https://ambermd.org/doc12/Amber18.pdf (accessed on 10 June 2021).
- Le Grand, S.; Götz, A.W.; Walker, R.C. SPFP: Speed without compromise—A mixed precision model for GPU accelerated molecular dynamics simulations. Comput. Phys. Commun. 2013, 184, 374–380. [Google Scholar] [CrossRef]
- 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. [Google Scholar] [CrossRef] [Green Version]
- Ryckaert, J.P.; Ciccotti, G.; Berendsen, H.J.C. Numerical integration of the cartesian equations of motion of a system with constraints: Molecular dynamics of n-alkanes. J. Comput. Phys. 1977, 23, 327–341. [Google Scholar] [CrossRef] [Green Version]
- Loncharich, R.J.; Brooks, B.R.; Pastor, R.W. Langevin dynamics of peptides: The frictional dependence of isomerization rates of N-acetylalanyl-N′-methylamide. Biopolymers 1992, 32, 523–535. [Google Scholar] [CrossRef] [PubMed]
- Berendsen, H.J.C.; Postma, J.P.M.; Van Gunsteren, W.F.; Dinola, A.; Haak, J.R. Molecular dynamics with coupling to an external bath. J. Chem. Phys. 1984, 81, 3684–3690. [Google Scholar] [CrossRef] [Green Version]
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Dobrovolska, O.; Strømland, Ø.; Handegård, Ø.S.; Jakubec, M.; Govasli, M.L.; Skjevik, Å.A.; Frøystein, N.Å.; Teigen, K.; Halskau, Ø. Investigating the Disordered and Membrane-Active Peptide A-Cage-C Using Conformational Ensembles. Molecules 2021, 26, 3607. https://doi.org/10.3390/molecules26123607
Dobrovolska O, Strømland Ø, Handegård ØS, Jakubec M, Govasli ML, Skjevik ÅA, Frøystein NÅ, Teigen K, Halskau Ø. Investigating the Disordered and Membrane-Active Peptide A-Cage-C Using Conformational Ensembles. Molecules. 2021; 26(12):3607. https://doi.org/10.3390/molecules26123607
Chicago/Turabian StyleDobrovolska, Olena, Øyvind Strømland, Ørjan Sele Handegård, Martin Jakubec, Morten L. Govasli, Åge Aleksander Skjevik, Nils Åge Frøystein, Knut Teigen, and Øyvind Halskau. 2021. "Investigating the Disordered and Membrane-Active Peptide A-Cage-C Using Conformational Ensembles" Molecules 26, no. 12: 3607. https://doi.org/10.3390/molecules26123607
APA StyleDobrovolska, O., Strømland, Ø., Handegård, Ø. S., Jakubec, M., Govasli, M. L., Skjevik, Å. A., Frøystein, N. Å., Teigen, K., & Halskau, Ø. (2021). Investigating the Disordered and Membrane-Active Peptide A-Cage-C Using Conformational Ensembles. Molecules, 26(12), 3607. https://doi.org/10.3390/molecules26123607