Effects of Charge Sequence Pattern and Lysine-to-Arginine Substitution on the Structural Stability of Bioinspired Polyampholytes

Dinic, Jelena; Tirrell, Matthew V.

doi:10.1021/acs.biomac.4c00002

Title: Effects of Charge Sequence Pattern and Lysine-to-Arginine Substitution on the Structural Stability of Bioinspired Polyampholytes

Journal Article · 03 April 2024 · Biomacromolecules

DOI: https://doi.org/10.1021/acs.biomac.4c00002 · OSTI ID:2333064

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Pritzker School of Molecular Engineering, University of Chicago, Chicago, Illinois 60637, United States, Center for Molecular Engineering and Materials Science Division, Argonne National Laboratory, Lemont, Illinois 60439, United States

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Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES)

OSTI ID:: 2333064

Journal Information:: Biomacromolecules, Journal Name: Biomacromolecules Journal Issue: 5 Vol. 25; ISSN 1525-7797

Publisher:: American Chemical SocietyCopyright Statement

Country of Publication:: United States

Language:: English

References (71)

Parameters of helix-coil transition theory for alanine-based peptides of varying chain lengths in water Scholtz, J. Martin; Qian, Hong; York, Eunice J. Biopolymers, Vol. 31, Issue 13 https://doi.org/10.1002/bip.360311304	journal	November 1991
Polyampholyte Nanoparticles Prepared by Self‐Complexation of Cationized Poly(γ‐glutamic acid) for Protein Carriers Shen, Heyun; Akagi, Takami; Akashi, Mitsuru Macromolecular Bioscience, Vol. 12, Issue 8 https://doi.org/10.1002/mabi.201200062	journal	June 2012
Synthetic and natural polyampholytes: Structural and behavioral similarity Kudaibergenov, Sarkyt E. Polymers for Advanced Technologies, Vol. 32, Issue 3 https://doi.org/10.1002/pat.5145	journal	October 2020
Helical peptides with three pairs of Asp‐Arg and Glu‐Arg residues in different orientations and spacings Huyghues‐Despointes, Beatrice M. P.; Martin Scholtz, J.; Baldwin, Robert L. Protein Science, Vol. 2, Issue 1 https://doi.org/10.1002/pro.5560020108	journal	January 1993
Elucidating the Folding Problem of Helical Peptides using Empirical Parameters. II†. Helix Macrodipole Effects and Rational Modification of the Helical Content of Natural Peptides Muñoz, Victor; Serrano, Luis Journal of Molecular Biology, Vol. 245, Issue 3 https://doi.org/10.1006/jmbi.1994.0023	journal	January 1995
Free Energy Determinants of Secondary Structure Formation: I. α-Helices Yang, An-Suei; Honig, Barry Journal of Molecular Biology, Vol. 252, Issue 3 https://doi.org/10.1006/jmbi.1995.0502	journal	September 1995
Role of Backbone Hydration and Salt-Bridge Formation in Stability of α-Helix in Solution Ghosh, Tuhin; Garde, Shekhar; García, Angel E. Biophysical Journal, Vol. 85, Issue 5 https://doi.org/10.1016/S0006-3495(03)74736-5	journal	November 2003
Recent advances in helix–coil theory Doig, Andrew J. Biophysical Chemistry, Vol. 101-102 https://doi.org/10.1016/S0301-4622(02)00170-9	journal	December 2002
Influence of Glu/Arg, Asp/Arg, and Glu/Lys Salt Bridges on α -Helical Stability and Folding Kinetics Meuzelaar, Heleen; Vreede, Jocelyne; Woutersen, Sander Biophysical Journal, Vol. 110, Issue 11 https://doi.org/10.1016/j.bpj.2016.04.015	journal	June 2016
Polyampholyte physics: Liquid–liquid phase separation and biological condensates Dinic, Jelena; Marciel, Amanda B.; Tirrell, Matthew V. Current Opinion in Colloid & Interface Science, Vol. 54 https://doi.org/10.1016/j.cocis.2021.101457	journal	August 2021
Biological importance of arginine: A comprehensive review of the roles in structure, disorder, and functionality of peptides and proteins Gupta, Munishwar Nath; Uversky, Vladimir N. International Journal of Biological Macromolecules, Vol. 257 https://doi.org/10.1016/j.ijbiomac.2023.128646	journal	February 2024
Effect of pH and urea on the proteins secondary structure at the water/air interface and in solution Guckeisen, Tobias; Hosseinpour, Saman; Peukert, Wolfgang Journal of Colloid and Interface Science, Vol. 590 https://doi.org/10.1016/j.jcis.2021.01.015	journal	May 2021
A zwitterionic block-copolymer, based on glutamic acid and lysine, reduces the biofouling of UF and RO membranes Piatkovsky, Maria; Acar, Handan; Marciel, Amanda B. Journal of Membrane Science, Vol. 549 https://doi.org/10.1016/j.memsci.2017.12.042	journal	March 2018
Influence of polymer molar mass and mixture stoichiometry on polyelectrolyte complexes of poly(l-arginine) and Poly(l-glutamic acid) Castelletto, Valeria; de Mello, Lucas; Arfara, Foteini Polymer, Vol. 263 https://doi.org/10.1016/j.polymer.2022.125497	journal	December 2022
Arginine “Magic”: Guanidinium Like-Charge Ion Pairing from Aqueous Salts to Cell Penetrating Peptides Vazdar, Mario; Heyda, Jan; Mason, Philip E. Accounts of Chemical Research, Vol. 51, Issue 6 https://doi.org/10.1021/acs.accounts.8b00098	journal	May 2018
Arginine to Lysine Mutations Increase the Aggregation Stability of a Single-Chain Variable Fragment through Unfolded-State Interactions Austerberry, James I.; Thistlethwaite, Angela; Fisher, Karl Biochemistry, Vol. 58, Issue 32 https://doi.org/10.1021/acs.biochem.9b00367	journal	July 2019
Structures and Antifouling Properties of Self-Assembled Zwitterionic Peptide Monolayers: Effects of Peptide Charge Distributions and Divalent Cations Li, Chuanxi; Liu, Chunjiang; Li, Minglun Biomacromolecules, Vol. 21, Issue 6 https://doi.org/10.1021/acs.biomac.0c00062	journal	April 2020
Sequence-Controlled Secondary Structures and Stimuli Responsiveness of Bioinspired Polyampholytes Dinic, Jelena; Schnorenberg, Mathew R.; Tirrell, Matthew V. Biomacromolecules, Vol. 23, Issue 9 https://doi.org/10.1021/acs.biomac.2c00666	journal	August 2022
Generalized Born Implicit Solvent Models Do Not Reproduce Secondary Structures of De Novo Designed Glu/Lys Peptides Lang, Eric J. M.; Baker, Emily G.; Woolfson, Derek N. Journal of Chemical Theory and Computation, Vol. 18, Issue 7 https://doi.org/10.1021/acs.jctc.1c01172	journal	June 2022
All-Atom Simulations Reveal Protein Charge Decoration in the Folded and Unfolded Ensemble Is Key in Thermophilic Adaptation Sawle, Lucas; Huihui, Jonathan; Ghosh, Kingshuk Journal of Chemical Theory and Computation, Vol. 13, Issue 10 https://doi.org/10.1021/acs.jctc.7b00545	journal	September 2017
Helical Polyampholyte Sequences Have Unique Thermodynamic Properties Batchelor, Matthew; Paci, Emanuele The Journal of Physical Chemistry B, Vol. 122, Issue 49 https://doi.org/10.1021/acs.jpcb.8b08344	journal	October 2018
Complete Phase Diagram for Liquid–Liquid Phase Separation of Intrinsically Disordered Proteins McCarty, James; Delaney, Kris T.; Danielsen, Scott P. O. The Journal of Physical Chemistry Letters, Vol. 10, Issue 8 https://doi.org/10.1021/acs.jpclett.9b00099	journal	March 2019
Distinct and Nonadditive Effects of Urea and Guanidinium Chloride on Peptide Solvation Ganguly, Pritam; Shea, Joan-Emma The Journal of Physical Chemistry Letters, Vol. 10, Issue 23 https://doi.org/10.1021/acs.jpclett.9b03004	journal	November 2019
Antifouling Properties of a Self-Assembling Glutamic Acid-Lysine Zwitterionic Polymer Surface Coating Ziemba, Christopher; Khavkin, Maria; Priftis, Dimitris Langmuir, Vol. 35, Issue 5 https://doi.org/10.1021/acs.langmuir.8b00181	journal	April 2018
Effect of Charge Distribution on the Dynamics of Polyampholytic Disordered Proteins Devarajan, Dinesh Sundaravadivelu; Rekhi, Shiv; Nikoubashman, Arash Macromolecules, Vol. 55, Issue 20 https://doi.org/10.1021/acs.macromol.2c01390	journal	October 2022
The energetics of ion-pair and hydrogen-bonding interactions in a helical peptide Scholtz, J. Martin; Qian, Hong; Robbins, Virginia H. Biochemistry, Vol. 32, Issue 37 https://doi.org/10.1021/bi00088a019	journal	September 1993
A Phosphoserine−Lysine Salt Bridge within an α-Helical Peptide, the Strongest α-Helix Side-Chain Interaction Measured to Date ^† Errington, Neil; Doig, Andrew J. Biochemistry, Vol. 44, Issue 20 https://doi.org/10.1021/bi050297j	journal	May 2005
Salting-Out Effect in Aqueous NaCl Solutions: Trends with Size and Polarity of Solute Molecules Endo, Satoshi; Pfennigsdorff, Andrea; Goss, Kai-Uwe Environmental Science & Technology, Vol. 46, Issue 3 https://doi.org/10.1021/es203183z	journal	January 2012
Interaction of Urea with Amino Acids: Implications for Urea-Induced Protein Denaturation Stumpe, Martin C.; Grubmüller, Helmut Journal of the American Chemical Society, Vol. 129, Issue 51 https://doi.org/10.1021/ja076216j	journal	December 2007
Quantitative Assessments of the Distinct Contributions of Polypeptide Backbone Amides versus Side Chain Groups to Chain Expansion via Chemical Denaturation Holehouse, Alex S.; Garai, Kanchan; Lyle, Nicholas Journal of the American Chemical Society, Vol. 137, Issue 8 https://doi.org/10.1021/ja512062h	journal	February 2015
Salt-Specific Stability and Denaturation of a Short Salt-Bridge-Forming α-Helix Dzubiella, Joachim Journal of the American Chemical Society, Vol. 130, Issue 42 https://doi.org/10.1021/ja805562g	journal	October 2008
Salting Effects on Protein Components in Aqueous NaCl and Urea Solutions: Toward Understanding of Urea-Induced Protein Denaturation Li, Weifeng; Zhou, Ruhong; Mu, Yuguang The Journal of Physical Chemistry B, Vol. 116, Issue 4 https://doi.org/10.1021/jp210769q	journal	January 2012
The Molecular Origin of Like-Charge Arginine−Arginine Pairing in Water Vondrášek, Jiří; Mason, Philip E.; Heyda, Jan The Journal of Physical Chemistry B, Vol. 113, Issue 27 https://doi.org/10.1021/jp902377q	journal	July 2009
Urea-Mediated Protein Denaturation: A Consensus View Das, Atanu; Mukhopadhyay, Chaitali The Journal of Physical Chemistry B, Vol. 113, Issue 38 https://doi.org/10.1021/jp906350s	journal	August 2009
Salt-Specific Stability of Short and Charged Alanine-Based α-Helices Dzubiella, Joachim The Journal of Physical Chemistry B, Vol. 113, Issue 52 https://doi.org/10.1021/jp9077932	journal	November 2009
Like-Charge Ion Pairing in Water: An Ab Initio Molecular Dynamics Study of Aqueous Guanidinium Cations Vazdar, Mario; Uhlig, Frank; Jungwirth, Pavel The Journal of Physical Chemistry Letters, Vol. 3, Issue 15 https://doi.org/10.1021/jz3007657	journal	July 2012
Lysine and Arginine Content of Proteins: Computational Analysis Suggests a New Tool for Solubility Design Warwicker, Jim; Charonis, Spyros; Curtis, Robin A. Molecular Pharmaceutics, Vol. 11, Issue 1 https://doi.org/10.1021/mp4004749	journal	November 2013
Local and macroscopic electrostatic interactions in single α-helices Baker, Emily G.; Bartlett, Gail J.; Crump, Matthew P. Nature Chemical Biology, Vol. 11, Issue 3 https://doi.org/10.1038/nchembio.1739	journal	February 2015
Elucidating the folding problem of helical peptides using empirical parameters Muñoz, Victor; Serrano, Luis Nature Structural & Molecular Biology, Vol. 1, Issue 6 https://doi.org/10.1038/nsb0694-399	journal	June 1994
Reentrant liquid condensate phase of proteins is stabilized by hydrophobic and non-ionic interactions Krainer, Georg; Welsh, Timothy J.; Joseph, Jerelle A. Nature Communications, Vol. 12, Issue 1 https://doi.org/10.1038/s41467-021-21181-9	journal	February 2021
Hydrophobicity of arginine leads to reentrant liquid-liquid phase separation behaviors of arginine-rich proteins Hong, Yuri; Najafi, Saeed; Casey, Thomas Nature Communications, Vol. 13, Issue 1 https://doi.org/10.1038/s41467-022-35001-1	journal	November 2022
Arginine side chain interactions and the role of arginine as a gating charge carrier in voltage sensitive ion channels Armstrong, Craig T.; Mason, Philip E.; Anderson, J. L. Ross Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep21759	journal	February 2016
Characterization of long and stable de novo single alpha-helix domains provides novel insight into their stability Wolny, Marcin; Batchelor, Matthew; Bartlett, Gail J. Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/srep44341	journal	March 2017
Sequence-dependent self-coacervation in high charge-density polyampholytes Madinya, Jason J.; Chang, Li-Wei; Perry, Sarah L. Molecular Systems Design & Engineering, Vol. 5, Issue 3 https://doi.org/10.1039/C9ME00074G	journal	January 2020
Theory of the Phase Transition between Helix and Random Coil in Polypeptide Chains Zimm, B. H.; Bragg, J. K. The Journal of Chemical Physics, Vol. 31, Issue 2 https://doi.org/10.1063/1.1730390	journal	August 1959
Conformational transitions of a weak polyampholyte Narayanan Nair, Arun Kumar; Uyaver, Sahin; Sun, Shuyu The Journal of Chemical Physics, Vol. 141, Issue 13 https://doi.org/10.1063/1.4897161	journal	October 2014
A theoretical method to compute sequence dependent configurational properties in charged polymers and proteins Sawle, Lucas; Ghosh, Kingshuk The Journal of Chemical Physics, Vol. 143, Issue 8 https://doi.org/10.1063/1.4929391	journal	August 2015
Theory of polyelectrolyte complexation—Complex coacervates are self-coacervates Delaney, Kris T.; Fredrickson, Glenn H. The Journal of Chemical Physics, Vol. 146, Issue 22 https://doi.org/10.1063/1.4985568	journal	June 2017
Sequence charge decoration dictates coil-globule transition in intrinsically disordered proteins Firman, Taylor; Ghosh, Kingshuk The Journal of Chemical Physics, Vol. 148, Issue 12 https://doi.org/10.1063/1.5005821	journal	March 2018
Small ion effects on self-coacervation phenomena in block polyampholytes Danielsen, Scott P. O.; McCarty, James; Shea, Joan-Emma The Journal of Chemical Physics, Vol. 151, Issue 3 https://doi.org/10.1063/1.5109045	journal	July 2019
A unified analytical theory of heteropolymers for sequence-specific phase behaviors of polyelectrolytes and polyampholytes Lin, Yi-Hsuan; Brady, Jacob P.; Chan, Hue Sun The Journal of Chemical Physics, Vol. 152, Issue 4 https://doi.org/10.1063/1.5139661	journal	January 2020
-Helical stabilization by side chain shielding of backbone hydrogen bonds Garcia, A. E.; Sanbonmatsu, K. Y. Proceedings of the National Academy of Sciences, Vol. 99, Issue 5 https://doi.org/10.1073/pnas.042496899	journal	February 2002
The intrinsic conformational propensities of the 20 naturally occurring amino acids and reflection of these propensities in proteins Beck, D. A. C.; Alonso, D. O. V.; Inoyama, D. Proceedings of the National Academy of Sciences, Vol. 105, Issue 34 https://doi.org/10.1073/pnas.0706527105	journal	August 2008
Dynamic charge interactions create surprising rigidity in the ER/K -helical protein motif Sivaramakrishnan, S.; Spink, B. J.; Sim, A. Y. L. Proceedings of the National Academy of Sciences, Vol. 105, Issue 36 https://doi.org/10.1073/pnas.0806256105	journal	September 2008
Urea, but not guanidinium, destabilizes proteins by forming hydrogen bonds to the peptide group Lim, Woon Ki; Rösgen, Jörg; Englander, S. Walter Proceedings of the National Academy of Sciences, Vol. 106, Issue 8 https://doi.org/10.1073/pnas.0812588106	journal	February 2009
The molecular basis for the chemical denaturation of proteins by urea Bennion, B. J.; Daggett, V. Proceedings of the National Academy of Sciences, Vol. 100, Issue 9 https://doi.org/10.1073/pnas.0930122100	journal	April 2003
Systematic control of protein interaction using a modular ER/K -helix linker Sivaramakrishnan, S.; Spudich, J. A. Proceedings of the National Academy of Sciences, Vol. 108, Issue 51 https://doi.org/10.1073/pnas.1116066108	journal	November 2011
Conformations of intrinsically disordered proteins are influenced by linear sequence distributions of oppositely charged residues Das, R. K.; Pappu, R. V. Proceedings of the National Academy of Sciences, Vol. 110, Issue 33 https://doi.org/10.1073/pnas.1304749110	journal	July 2013
Accurate secondary structure prediction and fold recognition for circular dichroism spectroscopy Micsonai, András; Wien, Frank; Kernya, Linda Proceedings of the National Academy of Sciences, Vol. 112, Issue 24 https://doi.org/10.1073/pnas.1500851112	journal	June 2015
Structural and hydrodynamic properties of an intrinsically disordered region of a germ cell-specific protein on phase separation Brady, Jacob P.; Farber, Patrick J.; Sekhar, Ashok Proceedings of the National Academy of Sciences, Vol. 114, Issue 39 https://doi.org/10.1073/pnas.1706197114	journal	September 2017
Molecular design of self-coacervation phenomena in block polyampholytes Danielsen, Scott P. O.; McCarty, James; Shea, Joan-Emma Proceedings of the National Academy of Sciences, Vol. 116, Issue 17 https://doi.org/10.1073/pnas.1900435116	journal	April 2019
Identifying sequence perturbations to an intrinsically disordered protein that determine its phase-separation behavior Schuster, Benjamin S.; Dignon, Gregory L.; Tang, Wai Shing Proceedings of the National Academy of Sciences, Vol. 117, Issue 21 https://doi.org/10.1073/pnas.2000223117	journal	May 2020
Comparative roles of charge, π , and hydrophobic interactions in sequence-dependent phase separation of intrinsically disordered proteins Das, Suman; Lin, Yi-Hsuan; Vernon, Robert M. Proceedings of the National Academy of Sciences, Vol. 117, Issue 46 https://doi.org/10.1073/pnas.2008122117	journal	November 2020
Physical reasons for the unusual α-helix stabilization afforded by charged or neutral polar residues in alanine-rich peptides Vila, Jorge A.; Ripoll, Daniel R.; Scheraga, H. A. Proceedings of the National Academy of Sciences, Vol. 97, Issue 24 https://doi.org/10.1073/pnas.240455797	journal	November 2000
Helix stabilization by Glu-...Lys+ salt bridges in short peptides of de novo design. Marqusee, S.; Baldwin, R. L. Proceedings of the National Academy of Sciences, Vol. 84, Issue 24 https://doi.org/10.1073/pnas.84.24.8898	journal	December 1987
Urea unfolding of peptide helices as a model for interpreting protein unfolding. Scholtz, J. M.; Barrick, D.; York, E. J. Proceedings of the National Academy of Sciences, Vol. 92, Issue 1 https://doi.org/10.1073/pnas.92.1.185	journal	January 1995
Rules of Physical Mathematics Govern Intrinsically Disordered Proteins Ghosh, Kingshuk; Huihui, Jonathan; Phillips, Michael Annual Review of Biophysics, Vol. 51, Issue 1 https://doi.org/10.1146/annurev-biophys-120221-095357	journal	May 2022
Composition Profiler: a tool for discovery and visualization of amino acid composition differences Vacic, Vladimir; Uversky, Vladimir N.; Dunker, A. Keith BMC Bioinformatics, Vol. 8, Issue 1 https://doi.org/10.1186/1471-2105-8-211	journal	January 2007
Intrinsically Disordered Proteins and Their “Mysterious” (Meta)Physics Uversky, Vladimir N. Frontiers in Physics, Vol. 7 https://doi.org/10.3389/fphy.2019.00010	journal	February 2019
Structural Characterization of Intrinsically Disordered Proteins by NMR Spectroscopy Kosol, Simone; Contreras-Martos, Sara; Cedeño, Cesyen Molecules, Vol. 18, Issue 9 https://doi.org/10.3390/molecules180910802	journal	September 2013
Pi-Pi contacts are an overlooked protein feature relevant to phase separation Vernon, Robert McCoy; Chong, Paul Andrew; Tsang, Brian eLife, Vol. 7 https://doi.org/10.7554/eLife.31486	journal	February 2018

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