Transition between protein-like and polymer-like dynamic behavior: Internal friction in unfolded apomyoglobin depends on denaturing conditions.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
31 01 2020
31 01 2020
Historique:
received:
14
11
2019
accepted:
06
01
2020
entrez:
2
2
2020
pubmed:
2
2
2020
medline:
18
11
2020
Statut:
epublish
Résumé
Equilibrium dynamics of different folding intermediates and denatured states is strongly connected to the exploration of the conformational space on the nanosecond time scale and might have implications in understanding protein folding. For the first time, the same protein system apomyoglobin has been investigated using neutron spin-echo spectroscopy in different states: native-like, partially folded (molten globule) and completely unfolded, following two different unfolding paths: using acid or guanidinium chloride (GdmCl). While the internal dynamics of the native-like state can be understood using normal mode analysis based on high resolution structural information of myoglobin, for the unfolded and even for the molten globule states, models from polymer science are employed. The Zimm model accurately describes the slowly-relaxing, expanded GdmCl-denaturated state, ignoring the individuality of the different aminoacid side chain. The dynamics of the acid unfolded and molten globule state are similar in the framework of the Zimm model with internal friction, where the chains still interact and hinder each other: the first Zimm relaxation time is as large as the internal friction time. Transient formation of secondary structure elements in the acid unfolded and presence of α-helices in the molten globule state lead to internal friction to a similar extent.
Identifiants
pubmed: 32005832
doi: 10.1038/s41598-020-57775-4
pii: 10.1038/s41598-020-57775-4
pmc: PMC6994677
doi:
Substances chimiques
Apoproteins
0
Myoglobin
0
Polymers
0
apomyoglobin
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1570Références
Frauenfelder, H. et al. A unified model of protein dynamics. Proc. Natl. Acad. Sci. USA 106, 5129 (2009).
doi: 10.1073/pnas.0900336106
pubmed: 19251640
pmcid: 19251640
Jamin, M. The folding process of apomyoglobin. Protein Peptide Lett. 12, 229 (2005).
doi: 10.2174/0929866053587174
Pace, N. C. & Vanderburg, K. E. Determining globular protein stability: guanidine hydrochloride denaturation of myoglobin. Biochem. 18, 288–292 (1979).
doi: 10.1021/bi00569a008
Klecknera, I. R. & Foster, M. P. An introduction to nmr-based approaches for measuring protein dynamics. Biochim Biophys Acta. 1814, 942–968 (2011).
doi: 10.1016/j.bbapap.2010.10.012
Ishima, R. & Torchia, D. Protein dynamics from NMR. Nat Struct Biol. 7, 740 (2000).
doi: 10.1038/78963
pubmed: 10966641
pmcid: 10966641
Schuler, B. Probing the dynamics and interactions of disordered proteins with single-molecule spectroscopy. Biophys. J. 116, 12a (2019).
doi: 10.1016/j.bpj.2018.11.107
Borgia, A. et al. Extreme disorder in an ultrahigh-affinity protein complex. Nature 555, 61 (2018).
doi: 10.1038/nature25762
pubmed: 6264893
pmcid: 6264893
Mezei, F., Pappas, C.,& Gutberlet, T. Neutron Spin Echo Spectroscopy- Basics, Trends and Applications, 1st ed. (Springer-Verlag, Berlin Heidelberg, 2003).
Mezei, F. Neutron spin echo, Proceedings of a Laue-Langevin Institut Workshop Grenoble, https://doi.org/10.1007/3-540-10004-0 (1979).
Callaway, D. J., Farago, B. & Bu, Z. Nanoscale protein dynamics: A new frontier for neutron spin echo spectroscopy. Eur. Phys. J. E. 36, 1 (2013).
doi: 10.1140/epje/i2013-13076-1
Fitter, J., Gutberlet, T.,& Katsaras, J. Neutron Scattering in Biology- Techniques and Applications, 1st ed. (Springer-Verlag, Berlin Heidelberg, 2006).
Ciepluch, K. et al. Influence of pegylation on domain dynamics of phosphoglycerate kinase: Peg acts like entropic spring for the protein. Bioconjugate Chem. 29, 1950–1960 (2018).
doi: 10.1021/acs.bioconjchem.8b00203
Monkenbusch, M. et al. Fast internal dynamics in alcohol dehydrogenase. J. Chem. Phys. 143, 075101 (2015).
doi: 10.1063/1.4928512
Alpert, Y. et al. Segmental flexibility in pig immunoglobulin g studied by neutron spin-echo technique. Biopolym. 24, 1769 (1985).
doi: 10.1002/bip.360240908
Stingaciu, L. R., Ivanova, O., Ohl, M., Biehl, R. & Richter, D. Fast antibody fragment motion: flexible linkers act as entropic spring. Sci. Rep. 6, 22148 (2016).
doi: 10.1038/srep22148
pubmed: 4810366
pmcid: 4810366
Bu, Z., Biehl, R., Monkenbusch, M., Richter, D. & Callaway, D. J. E. Coupled protein domain motion in taq polymerase revealed by neutron spin-echo spectroscopy. PNAS 102, 17646–17651 (2005).
doi: 10.1073/pnas.0503388102
Ameseder, F., Biehl, R., Holderer, O., Richter, D. & Stadler, A. M. Localised contacts lead to nanosecond hinge motions in dimeric bovine serum albumin. Phys. Chem. Chem. Phys. 21, 18477 (2019).
doi: 10.1039/C9CP01847F
Sill, C. et al. Structure and domain dynamics of human lactoferrin in solution and the influence of Fe(iii)-ion ligand binding. BMC Biophysics 9, 7 (2016).
doi: 10.1186/s13628-016-0032-3
pubmed: 5095980
pmcid: 5095980
Farago, B., Li, J., Cornilescu, G., Callaway, D. J. & Bu, Z. Activation of nanoscale allosteric protein domain motion revealed by neutron spin echo spectroscopy. Biophys J. 99, 3473–3482 (2010).
doi: 10.1016/j.bpj.2010.09.058
pubmed: 2980739
pmcid: 2980739
Stadler, A. M. et al. Internal nanosecond dynamics in the intrinsically disordered myelin basic protein. J. Am. Chem. Soc. 136, 6987–6994 (2014).
doi: 10.1021/ja502343b
Ameseder, F. et al. Relevance of internal friction and structural constraints for the dynamics of denatured bovine serum albumin. J. Phys. Chem. Lett. 9, 2469–2473 (2018).
doi: 10.1021/acs.jpclett.8b00825
Doi, M. & Edwards, S. F. eds The Theory of Polymer Dynamics, 1st ed. (Oxford science publications, Oxford, UK, 1988).
Teraoka, I. ed. Polymer Solutions: An Introduction to Physical Properties, 1st ed. (John Wiley & Sons, Inc., Oxford, UK, 2002).
Khatri, B. S. & McLeish, T. B. C. Rouse Model with Internal Friction: A Coarse Grained Framework for Single Biopolymer Dynamics. Macromolecules 40, 6770–6777 (2007).
doi: 10.1021/ma071175x
Mark, C. et al. Polymer Chain Conformation and Dynamical Confinement in a Model One-Component Nanocomposite. Phys. Rev. Lett. 119, 047801 (2017).
doi: 10.1103/PhysRevLett.119.047801
Samanta, N. & Chakrabarti, R. Looping dynamics of a flexible chain with internal friction at different degrees of compactness. Phys. A. 436, 377–386 (2015).
doi: 10.1016/j.physa.2015.05.042
Samanta, N. & Chakrabarti, R. Reconfiguration dynamics in folded and intrinsically disordered protein with internal friction: Effect of solvent quality and denaturant. Phys. A: 450, issue C 450, 165–179 (2016).
doi: 10.1016/j.physa.2015.12.147
Khatri, B. S. & McLeish, T. B. C. Loop formation and translational diffusion of intrinsically disordered proteins. Phys. Rev. E. 100, 052405 (2019).
doi: 10.1103/PhysRevE.100.052405
Hammouda, B. A new guinier-porod model. J. Appl. Cryst. 43, 716 (2010).
doi: 10.1107/S0021889810015773
Nygaard, M., Kragelund, B. B., Papaleo, E. & Lindorff-Larsen, K. An efficient method for estimating the hydrodynamic radius of disordered protein conformations. Biophys. J. 113, 550–557 (2017).
doi: 10.1016/j.bpj.2017.06.042
pubmed: 28793210
pmcid: 28793210
Akcasu, A. & Han, C. Molecular weight and temperature dependence of polymer dimensions in solution. Macrom. 12, 276 (1979).
doi: 10.1021/ma60068a022
Petrescu, A.-J., Receveur, V., Calmettes, P., Durand, D. & Smith, J. C. Excluded volume in the configurational distribution of a strongly-denatured protein. Prot. Sci. 7, 1396 (1998).
doi: 10.1002/pro.5560070616
Petrescu, A.-J. et al. Small-angle neutron scattering by a strongly denatured protein: Analysis using random polymer theory. Biophys. J. 72, 335 (1997).
doi: 10.1016/S0006-3495(97)78672-7
pubmed: 1184322
pmcid: 1184322
Edwards, S. F. The statistical mechanics of polymers with excluded volume. Proc. Phys. Soc. 85, 613 (1965).
doi: 10.1088/0370-1328/85/4/301
Heyda, J. et al. Guanidinium can both cause and prevent the hydrophobic collapse of biomacromolecules. J. Am. Chem. Soc. 139, 863–870 (2017).
doi: 10.1021/jacs.6b11082
pubmed: 5499822
pmcid: 5499822
Borgia, A. et al. Consistent view of polypeptide chain expansion in chemical denaturants from multiple experimental methods. J. Am. Chem. Soc. 138, 11714–11726 (2016).
doi: 10.1021/jacs.6b05917
pubmed: 27583570
pmcid: 27583570
Huerta-Viga, A. & Woutersen, S. Protein denaturation with guanidinium: A 2d-ir study. J. Phys. Chem. Lett. 4, 3397–3401 (2013).
doi: 10.1021/jz401754b
pubmed: 24163724
pmcid: 24163724
Eliezer, D. et al. Evidence of an associative intermediate on the myoglobin refolding pathway. Biophys. J. 65, 912 (1993).
doi: 10.1016/S0006-3495(93)81124-X
pubmed: 1225792
pmcid: 1225792
Flory, P. Principles of Polymer Chemistry, 1st ed. (Cornell University Press, Ithaca and London, 1953).
de Gennes, P.-G. Scaling Concepts in Polymer Physics, 1st ed. (Cornell University Press, Ithaca and London, 1979).
Baumgartner, A. & Binder, K. Monte carlo studies on the freely jointed polymer chain with excluded volume interaction. J. Chem. Phys. 71, 2541 (1979).
doi: 10.1063/1.438608
Belloni, L. Colloidal interactions. J. Phys.: Condens. Matter 12, R549 (2000).
Hansen, J.-P. & Hayter, J. B. A rescaled msa structure factor for dilute charged colloidal dispersions. Molecular Physics: An International Journal at the Interface Between Chemistry and Physics 46, 651 (1982).
doi: 10.1080/00268978200101471
Biehl, R. Jscatter, a program for evaluation and analysis of experimental data, PLoS One (2019).
Hayter, J. B. & Penfold, J. An analytic structure factor for macroion solutions. Mol. Phys. 42, 109 (1981).
doi: 10.1080/00268978100100091
Gasteiger, E. Expasy: the proteomics server for in-depth protein knowledge and analysis. Nucl. Acids Res. 31, 3784 (2003).
doi: 10.1093/nar/gkg563
Ortega, D. A. A. & de la Torre, J. G. Prediction of hydrodynamic and other solution properties of rigid proteins from atomic- and residue-level models. Biophys. J. 101, 892 (2011).
doi: 10.1016/j.bpj.2011.06.046
pubmed: 3175065
pmcid: 3175065
Richter, D. Neutron Spin Echo in Polymer Systems, 1st ed. (Springer-Verlag, Berlin Heidelberg, 2005).
Biehl, M. M. R.,& Richter, D. Exploring internal protein dynamics by neutron spin echo spectroscopy, Soft Matter, 1299 (2011).
Stadler, A. M., Koza, M. M. & Fitter, J. Determination of conformational entropy of fully and partially folded conformations of holo- and apomyoglobin. J. Phys. Chem. B. 119, 72 (2015).
doi: 10.1021/jp509732q
pubmed: 25494533
pmcid: 25494533
Hinsen, K. Analysis of domain motions by approximate normal mode calculations. Proteins 33, 417–29 (1998).
doi: 10.1002/(SICI)1097-0134(19981115)33:3<417::AID-PROT10>3.0.CO;2-8
pubmed: 9829700
pmcid: 9829700
Hinsen, K., A.-J., P., Dellerue, S., Bellissent-Funel, M.-C. & G.R., K. Harmonicity in slow protein dynamics. Chem Phys. 261, 25–37 (2000).
doi: 10.1016/S0301-0104(00)00222-6
Hinsen, K. The molecular modeling toolkit: A new approach to molecular simulations. J Comput Chem. 21, 79–85 (2000).
doi: 10.1002/(SICI)1096-987X(20000130)21:2<79::AID-JCC1>3.0.CO;2-B
Soranno, A., Zosel, F. & Hofmann, H. Internal friction in an intrinsically disordered protein-comparing rouse-like models with experiments. J Chem Phys. 148, 123326 (2018).
doi: 10.1063/1.5009286
Pradeep, L. & Udgaonkar, J. B. Diffusional Barrier in the Unfolding of a Small Protein. J. Mol. Biol. 366, 1016–1028 (2007).
doi: 10.1016/j.jmb.2006.11.064
Zheng, W., Hofmann, H., Schuler, B. & Best, R. B. Origin of internal friction in disordered proteins depends on solvent quality. J. Phys. Chem. B. 122, 11478 (2018).
doi: 10.1021/acs.jpcb.8b07425
Stadler, A. M., Demmel, F., Ollivier, J. & Seydel, T. Picosecond to nanosecond dynamics provide a source of conformational entropy for protein folding. Phys. Chem. Chem. Phys. 18, 21527 (2016).
doi: 10.1039/C6CP04146A
Yu, H., Siewny, M. G. W., Edwards, D. T., Sanders, A. W. & Perkins, T. T. Hidden dynamics in the unfolding of individual bacteriorhodopsin proteins. Science 355, 945–950 (2017).
doi: 10.1126/science.aah7124
pubmed: 5436802
pmcid: 5436802
Seelig, J. Cooperative protein unfolding. A statistical-mechanical model for the action of denaturants. Biophysical Chemistry 233, 19–25 (2018).
doi: 10.1016/j.bpc.2017.12.001
Rothgeb, T. & F., G. Physical methods for the study of myoglobins. Methods Enzymol. 52, 473 (1978).
doi: 10.1016/S0076-6879(78)52052-1
Micsonai, A. Bestsel: a web server for accurate protein secondary structure prediction and fold recognition from the circular dichroism spectra. Nucl. Acids Res. 46, W315 (2018).
doi: 10.1093/nar/gky497
Balacescu, L. et al. In situ dynamic light scattering complementing neutron spin echo measurements on protein samples, Journal of Surface Investigation: X-ray, Synchrotron and Neutron Techniques (2019).
Heinz Maier-Leibnitz Zentrum, Kws-2: Small angle scattering diffractometer, JLSRF1, A29 (2015).
Holderer, O., Zolnierczuk, P., Pasini, S., Stingaciu, L. & Monkenbusch, M. A better view through new glasses: Developments at the jülich neutron spin echo spectrometers. Physica B. 562, 9 (2019).
doi: 10.1016/j.physb.2018.11.021
Pasini, S., Holderer, O., Kozielewski, T., Richter, D. & Monkenbusch, M. J-nse-phoenix, a neutron spin-echo spectrometer with optimized superconducting precession coils at the mlz in garching. Rev. Sci. Ins. 90, 043107 (2019).
doi: 10.1063/1.5084303
Zolnierczuk, P. A. et al. Efficient data extraction from neutron time-of-flight spin-echo raw data. J. Appl. Chrys. 52, 1 (2019).
doi: 10.1107/S1600576718018009
Zolnierczuk, P. A., Holderer, O. & Monkenbusch, M. DrSPINE: Data reduction for SPIN echo experiments. AIP Conference Proceedings 1969, 050003 (2018).
doi: 10.1063/1.5039300