Guanidinium can both Cause and Prevent the Hydrophobic Collapse of Biomacromolecules

. 2017 Jan 18 ; 139 (2) : 863-870. [epub] 20170105

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.

Perzistentní odkaz   https://www.medvik.cz/link/pmid28054487

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.

Zobrazit více v PubMed

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

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...