Guanidinium can both Cause and Prevent the Hydrophobic Collapse of Biomacromolecules
Jazyk angličtina Země Spojené státy americké Médium print-electronic
Typ dokumentu časopisecké články, práce podpořená grantem, Research Support, U.S. Gov't, Non-P.H.S.
PubMed
28054487
PubMed Central
PMC5499822
DOI
10.1021/jacs.6b11082
Knihovny.cz E-zdroje
- MeSH
- guanidin chemie MeSH
- hydrofobní a hydrofilní interakce MeSH
- kationty MeSH
- peptidy chemie MeSH
- spektroskopie infračervená s Fourierovou transformací MeSH
- termodynamika MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Research Support, U.S. Gov't, Non-P.H.S. MeSH
- Názvy látek
- guanidin MeSH
- kationty MeSH
- peptidy MeSH
A combination of Fourier transform infrared and phase transition measurements as well as molecular computer simulations, and thermodynamic modeling were performed to probe the mechanisms by which guanidinium (Gnd+) salts influence the stability of the collapsed versus uncollapsed state of an elastin-like polypeptide (ELP), an uncharged thermoresponsive polymer. We found that the cation's action was highly dependent upon the counteranion with which it was paired. Specifically, Gnd+ was depleted from the ELP/water interface and was found to stabilize the collapsed state of the macromolecule when paired with well-hydrated anions such as SO42-. Stabilization in this case occurred via an excluded volume (or depletion) effect, whereby SO42- was strongly partitioned away from the ELP/water interface. Intriguingly, at low salt concentrations, Gnd+ was also found to stabilize the collapsed state of the ELP when paired with SCN-, which is a strong binder for the ELP. In this case, the anion and cation were both found to be enriched in the collapsed state of the polymer. The collapsed state was favored because the Gnd+ cross-linked the polymer chains together. Moreover, the anion helped partition Gnd+ to the polymer surface. At higher salt concentrations (>1.5 M), GndSCN switched to stabilizing the uncollapsed state because a sufficient amount of Gnd+ and SCN- partitioned to the polymer surface to prevent cross-linking from occurring. Finally, in a third case, it was found that salts which interacted in an intermediate fashion with the polymer (e.g., GndCl) favored the uncollapsed conformation at all salt concentrations. These results provide a detailed, molecular-level, mechanistic picture of how Gnd+ influences the stability of polypeptides in three distinct physical regimes by varying the anion. It also helps explain the circumstances under which guanidinium salts can act as powerful and versatile protein denaturants.
Chemistry Department Texas A and M University 3255 TAMU College Station Texas 77843 United States
Division of Theoretical Chemistry Lund University POB 124 22 100 Lund Sweden
Institut für Physik Humboldt Universität zu Berlin Newtonstr 15 12489 Berlin Germany
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Jungwirth P.; Cremer P. S. Beyond Hofmeister. Nat. Chem. 2014, 6, 261–263. 10.1038/nchem.1899. PubMed DOI
Kunz W.; Lo Nostro P.; Ninham B. W. The Present State of Affairs with Hofmeister Effects. Curr. Opin. Colloid Interface Sci. 2004, 9, 1–18. 10.1016/j.cocis.2004.05.004. DOI
Leontidis E. Hofmeister Anion Effects on Surfactant Self-Assembly and the Formation of Mesoporous Solids. Curr. Opin. Colloid Interface Sci. 2002, 7, 81–91. 10.1016/S1359-0294(02)00010-9. DOI
Zhang Y.; Cremer P. S. The Inverse and Direct Hofmeister Series for Lysozyme. Proc. Natl. Acad. Sci. U. S. A. 2009, 106, 15249–15253. 10.1073/pnas.0907616106. PubMed DOI PMC
Paterova J.; Rembert K. B.; Heyda J.; Kurra Y.; Okur H. I.; Liu W. S. R.; Hilty C.; Cremer P. S.; Jungwirth P. Reversal of the Hofmeister Series: Specific Ion Effects on Peptides. J. Phys. Chem. B 2013, 117, 8150–8158. 10.1021/jp405683s. PubMed DOI
Schwierz N.; Horinek D.; Netz R. R. Anionic and Cationic Hofmeister Effects on Hydrophobic and Hydrophilic Surfaces. Langmuir 2013, 29, 2602–2614. 10.1021/la303924e. PubMed DOI
Rembert K. B.; Paterova J.; Heyda J.; Hilty C.; Jungwirth P.; Cremer P. S. Molecular Mechanisms of Ion-Specific Effects on Proteins. J. Am. Chem. Soc. 2012, 134, 10039–10046. 10.1021/ja301297g. PubMed DOI
Rembert K. B.; Okur H. I.; Hilty C.; Cremer P. S. An NH Moiety Is Not Required for Anion Binding to Amides in Aqueous Solution. Langmuir 2015, 31, 3459–3464. 10.1021/acs.langmuir.5b00127. PubMed DOI
Okur H. I.; Kherb J.; Cremer P. S. Cations Bind Only Weakly to Amides in Aqueous Solutions. J. Am. Chem. Soc. 2013, 135, 5062–5067. 10.1021/ja3119256. PubMed DOI
Bonner O. D. The Osmotic and Activity Coefficients of Some Guanidinium Salts at 298.15 K. J. Chem. Thermodyn. 1976, 8, 1167–1172. 10.1016/0021-9614(76)90124-5. DOI
Wernersson E.; Heyda J.; Vazdar M.; Lund M.; Mason P. E.; Jungwirth P. Orientational Dependence of the Affinity of Guanidinium Ions to the Water Surface. J. Phys. Chem. B 2011, 115, 12521–12526. 10.1021/jp207499s. PubMed DOI
Vazdar M.; Uhlig F.; Jungwirth P. Like-Charge Ion Pairing in Water: An Ab Initio Molecular Dynamics Study of Aqueous Guanidinium Cations. J. Phys. Chem. Lett. 2012, 3, 2021–2024. 10.1021/jz3007657. DOI
Mason P. E.; Neilson G. W.; Dempsey C. E.; Barnes A. C.; Cruickshank J. M. The Hydration Structure of Guanidinium and Thiocyanate Ions: Implications for Protein Stability in Aqueous Solution. Proc. Natl. Acad. Sci. U. S. A. 2003, 100, 4557–4561. 10.1073/pnas.0735920100. PubMed DOI PMC
Mason P. E.; Dempsey C. E.; Neilson G. W.; Kline S. R.; Brady J. W. Preferential Interactions of Guanidinum Ions with Aromatic Groups over Aliphatic Groups. J. Am. Chem. Soc. 2009, 131, 16689–16696. 10.1021/ja903478s. PubMed DOI PMC
Dooley K. H.; Castellino Fj Solubility of Amino-Acids in Aqueous Guanidinium Thiocyanate Solutions. Biochemistry 1972, 11, 1870–1874. 10.1021/bi00760a022. PubMed DOI
Jha S. K.; Marqusee S. Kinetic Evidence for a Two-Stage Mechanism of Protein Denaturation by Guanidinium Chloride. Proc. Natl. Acad. Sci. U. S. A. 2014, 111, 4856–4861. 10.1073/pnas.1315453111. PubMed DOI PMC
Zheng W. W.; Borgia A.; Buholzer K.; Grishaev A.; Schuler B.; Best R. B. Probing the Action of Chemical Denaturant on an Intrinsically Disordered Protein by Simulation and Experiment. J. Am. Chem. Soc. 2016, 138, 11702–11713. 10.1021/jacs.6b05443. PubMed DOI PMC
Xia Z.; Das P.; Shakhnovich E. I.; Zhou R. H. Collapse of Unfolded Proteins in a Mixture of Denaturants. J. Am. Chem. Soc. 2012, 134, 18266–18274. 10.1021/ja3031505. PubMed DOI
Meuzelaar H.; Panman M. R.; Woutersen S. Guanidinium-Induced Denaturation by Breaking of Salt Bridges. Angew. Chem., Int. Ed. 2015, 54, 15255–15259. 10.1002/anie.201508601. PubMed DOI
Lim W. K.; Rosgen J.; Englander S. W. Urea, but Not Guanidinium, Destabilizes Proteins by Forming Hydrogen Bonds to the Peptide Group. Proc. Natl. Acad. Sci. U. S. A. 2009, 106, 2595–2600. 10.1073/pnas.0812588106. PubMed DOI PMC
Huerta-Viga A.; Woutersen S. Protein Denaturation with Guanidinium: A 2d-IR Study. J. Phys. Chem. Lett. 2013, 4, 3397–3401. 10.1021/jz401754b. PubMed DOI PMC
Dempsey C. E.; Mason P. E.; Brady J. W.; Neilson G. W. The Reversal by Sulfate of the Denaturant Activity of Guanidinium. J. Am. Chem. Soc. 2007, 129, 15895–15902. 10.1021/ja074719j. PubMed DOI
Meyer D. E.; Chilkoti A. Genetically Encoded Synthesis of Protein-Based Polymers with Precisely Specified Molecular Weight and Sequence by Recursive Directional Ligation: Examples from the Elastin-Like Polypeptide System. Biomacromolecules 2002, 3, 357–367. 10.1021/bm015630n. PubMed DOI
Cho Y.; Zhang Y.; Christensen T.; Sagle L. B.; Chilkoti A.; Cremer P. S. Effects of Hofmeister Anions on the Phase Transition Temperature of Elastin-Like Polypeptides. J. Phys. Chem. B 2008, 112, 13765–13771. 10.1021/jp8062977. PubMed DOI PMC
Heyda J.; Muzdalo A.; Dzubiella J. Rationalizing Polymer Swelling and Collapse under Attractive Cosolvent Conditions. Macromolecules 2013, 46, 1231–1238. 10.1021/ma302320y. DOI
Frenkel D.; Smit B.. Understanding Molecular Simulation: From Algorithms to Applications; Academic Press: New York, 2002.
Heyda J.; Dzubiella J. Thermodynamic Description of Hofmeister Effects on the LCST of Thermosensitive Polymers. J. Phys. Chem. B 2014, 118, 10979–10988. 10.1021/jp5041635. PubMed DOI
Zhang Y. J.; Furyk S.; Bergbreiter D. E.; Cremer P. S. Specific Ion Effects on the Water Solubility of Macromolecules: PNIPAM and the Hofmeister Series. J. Am. Chem. Soc. 2005, 127, 14505–14510. 10.1021/ja0546424. PubMed DOI
Zhang Y.; Mao H.; Cremer P. S. Probing the Mechanism of Aqueous Two-Phase System Formation for A-Elastin on-Chip. J. Am. Chem. Soc. 2003, 125, 15630–15635. 10.1021/ja037869c. PubMed DOI
Zhang Y.; Trabbic-Carlson K.; Albertorio F.; Chilkoti A.; Cremer P. S. Aqueous Two-Phase System Formation Kinetics for Elastin-Like Polypeptides of Varying Chain Length. Biomacromolecules 2006, 7, 2192–2199. 10.1021/bm060254y. PubMed DOI
Johansson H. O.; Karlstroem G.; Tjerneld F. Experimental and Theoretical Study of Phase Separation in Aqueous Solutions of Clouding Polymers and Carboxylic Acids. Macromolecules 1993, 26, 4478–4483. 10.1021/ma00069a012. DOI
Serrano V.; Liu W.; Franzen S. An Infrared Spectroscopic Study of the Conformational Transition of Elastin-Like Polypeptides. Biophys. J. 2007, 93, 2429–2435. 10.1529/biophysj.106.100594. PubMed DOI PMC
Sagle L. B.; Zhang Y.; Litosh V. A.; Chen X.; Cho Y.; Cremer P. S. Investigating the Hydrogen-Bonding Model of Urea Denaturation. J. Am. Chem. Soc. 2009, 131, 9304–9310. 10.1021/ja9016057. PubMed DOI
Cho Y.; Sagle L. B.; Iimura S.; Zhang Y.; Kherb J.; Chilkoti A.; Scholtz J. M.; Cremer P. S. Hydrogen Bonding of B-Turn Structure Is Stabilized in D2O. J. Am. Chem. Soc. 2009, 131, 15188–15193. 10.1021/ja9040785. PubMed DOI PMC
Record M. T. Jr.; Guinn E.; Pegram L.; Capp M. Introductory Lecture: Interpreting and Predicting Hofmeister Salt Ion and Solute Effects on Biopolymer and Model Processes Using the Solute Partitioning Model. Faraday Discuss. 2013, 160, 9–44. 10.1039/C2FD20128C. PubMed DOI PMC
Pegram L. M.; Wendorff T.; Erdmann R.; Shkel I.; Bellissimo D.; Felitsky D. J.; Record M. T. Jr. Why Hofmeister Effects of Many Salts Favor Protein Folding but Not DNA Helix Formation. Proc. Natl. Acad. Sci. U. S. A. 2010, 107, 7716–7721. 10.1073/pnas.0913376107. PubMed DOI PMC
Pegram L. M.; Record M. T. Thermodynamic Origin of Hofmeister Ion Effects. J. Phys. Chem. B 2008, 112, 9428–9436. 10.1021/jp800816a. PubMed DOI PMC
Heyda J.; Soll S.; Yuan J.; Dzubiella J. Thermodynamic Description of the LCST of Charged Thermoresponsive Copolymers. Macromolecules 2014, 47, 2096–2102. 10.1021/ma402577h. DOI
Cho Y.Thermodynamics and Applications of Elastine-like Polypeptides. Ph.D. Dissertation, Texas A&M University, College Station, Texas, U.S., 2009.
Rodriguez-Ropero F.; Hajari T.; van der Vegt N. F. A. Mechanism of Polymer Collapse in Miscible Good Solvents. J. Phys. Chem. B 2015, 119, 15780–15788. 10.1021/acs.jpcb.5b10684. PubMed DOI
Rodriguez-Ropero F.; van der Vegt N. F. A. Direct Osmolyte-Macromolecule Interactions Confer Entropic Stability to Folded States. J. Phys. Chem. B 2014, 118, 7327–7334. 10.1021/jp504065e. PubMed DOI
Pluhařová E.; Baer M. D.; Mundy C. J.; Schmidt B.; Jungwirth P. Aqueous Cation-Amide Binding: Free Energies and IR Spectral Signatures by Ab Initio Molecular Dynamics. J. Phys. Chem. Lett. 2014, 5, 2235–2240. 10.1021/jz500976m. PubMed DOI
Arakawa T.; Timasheff S. N. Protein Stabilization and Destabilization by Guanidinium Salts. Biochemistry 1984, 23, 5924–5929. 10.1021/bi00320a005. PubMed DOI
Arakawa T.; Timasheff S. N. Preferential Interactions of Proteins with Salts in Concentrated-Solutions. Biochemistry 1982, 21, 6545–6552. 10.1021/bi00268a034. PubMed DOI