Histidine‐Mediated Ion Specific Effects Enable Salt Tolerance of a Pore‐Forming Marine Antimicrobial Peptide

Xian, Wujing; Hennefarth, Matthew R.; Lee, Michelle W.; Do, Tran; Lee, Ernest Y.; Alexandrova, Anastassia N.; Wong, Gerard C. L.

doi:10.1002/ange.202108501

Histidine‐Mediated Ion Specific Effects Enable Salt Tolerance of a Pore‐Forming Marine Antimicrobial Peptide

Journal Article · Thu Apr 21 00:00:00 EDT 2022 · Angewandte Chemie

DOI:https://doi.org/10.1002/ange.202108501· OSTI ID:1864371

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Department of Bioengineering University of California, Los Angeles Los Angeles CA 90095 USA
Department of Chemistry and Biochemistry University of California, Los Angeles Los Angeles CA 90095 USA
Department of Chemistry and Biochemistry University of California, Los Angeles Los Angeles CA 90095 USA, California Nano Systems Institute University of California, Los Angeles Los Angeles CA 90095 USA
Department of Bioengineering University of California, Los Angeles Los Angeles CA 90095 USA, California Nano Systems Institute University of California, Los Angeles Los Angeles CA 90095 USA

Abstract

Antimicrobial peptides (AMPs) preferentially permeate prokaryotic membranes via electrostatic binding and membrane remodeling. Such action is drastically suppressed by high salt due to increased electrostatic screening, thus it is puzzling how marine AMPs can possibly work. We examine as a model system, piscidin‐1, a histidine‐rich marine AMP, and show that ion‐histidine interactions play unanticipated roles in membrane remodeling at high salt: Histidines can simultaneously hydrogen‐bond to a phosphate and coordinate with an alkali metal ion to neutralize phosphate charge, thereby facilitating multidentate bonds to lipid headgroups in order to generate saddle‐splay curvature, a prerequisite to pore formation. A comparison among Na ⁺ , K ⁺ , and Cs ⁺ indicates that histidine‐mediated salt tolerance is ion specific. We conclude that histidine plays a unique role in enabling protein/peptide‐membrane interactions that occur in marine or other high‐salt environment.

View Accepted Manuscript (Publisher)

Sponsoring Organization:: USDOE

Grant/Contract Number:: AC02-76SF00515

OSTI ID:: 1864371

Journal Information:: Angewandte Chemie, Journal Name: Angewandte Chemie Journal Issue: 25 Vol. 134; ISSN 0044-8249

Publisher:: Wiley Blackwell (John Wiley & Sons)Copyright Statement

Country of Publication:: Germany

Language:: English

References (43)

Loosening of Lipid Packing Promotes Oligoarginine Entry into Cells Murayama, Tomo; Masuda, Toshihiro; Afonin, Sergii Angewandte Chemie, Vol. 129, Issue 26 https://doi.org/10.1002/ange.201703578	journal	June 2017
Loosening of Lipid Packing Promotes Oligoarginine Entry into Cells Murayama, Tomo; Masuda, Toshihiro; Afonin, Sergii Angewandte Chemie International Edition, Vol. 56, Issue 26 https://doi.org/10.1002/anie.201703578	journal	June 2017
The Cell-Penetrating Peptide TAT(48-60) Induces a Non-Lamellar Phase in DMPC Membranes Afonin, Sergii; Frey, Alexander; Bayerl, Sybille ChemPhysChem, Vol. 7, Issue 10 https://doi.org/10.1002/cphc.200600306	journal	October 2006
Electron density modeling and reconstruction of infinite periodic minimal surfaces (IPMS) based phases in lipid-water systems. I. Modeling IPMS-based phases Harper, P. E.; Gruner, S. M. The European Physical Journal E, Vol. 2, Issue 3 https://doi.org/10.1007/PL00013660	journal	July 2000
The Curvature Induction of Surface-Bound Antimicrobial Peptides Piscidin 1 and Piscidin 3 Varies with Lipid Chain Length Perrin, B. Scott; Sodt, Alexander J.; Cotten, Myriam L. The Journal of Membrane Biology, Vol. 248, Issue 3 https://doi.org/10.1007/s00232-014-9733-1	journal	October 2014
Studies of the thermotropic phase behavior of phosphatidylcholines containing 2-alkyl substituted fatty acyl chains: a new class of phosphatidylcholines forming inverted nonlamellar phases Lewis, R. N.; McElhaney, R. N.; Harper, P. E. Biophysical Journal, Vol. 66, Issue 4 https://doi.org/10.1016/S0006-3495(94)80890-2	journal	April 1994
Investigating molecular recognition and biological function at interfaces using piscidins, antimicrobial peptides from fish Chekmenev, Eduard Y.; Vollmar, Breanna S.; Forseth, Kristen T. Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1758, Issue 9 https://doi.org/10.1016/j.bbamem.2006.03.034	journal	September 2006
Antimicrobial activity of histidine-rich peptides is dependent on acidic conditions Kacprzyk, Lukasz; Rydengård, Victoria; Mörgelin, Matthias Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1768, Issue 11 https://doi.org/10.1016/j.bbamem.2007.06.020	journal	November 2007
Two interdependent mechanisms of antimicrobial activity allow for efficient killing in nylon-3-based polymeric mimics of innate immunity peptides Lee, Michelle W.; Chakraborty, Saswata; Schmidt, Nathan W. Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1838, Issue 9 https://doi.org/10.1016/j.bbamem.2014.04.007	journal	September 2014
Arginine-Rich Peptides Destabilize the Plasma Membrane, Consistent with a Pore Formation Translocation Mechanism of Cell-Penetrating Peptides Herce, H. D.; Garcia, A. E.; Litt, J. Biophysical Journal, Vol. 97, Issue 7 https://doi.org/10.1016/j.bpj.2009.05.066	journal	October 2009
Electrostatics of rigid polyelectrolytes Wong, Gerard C. L. Current Opinion in Colloid & Interface Science, Vol. 11, Issue 6 https://doi.org/10.1016/j.cocis.2006.12.003	journal	December 2006
Antimicrobial peptides and induced membrane curvature: Geometry, coordination chemistry, and molecular engineering Schmidt, Nathan W.; Wong, Gerard C. L. Current Opinion in Solid State and Materials Science, Vol. 17, Issue 4 https://doi.org/10.1016/j.cossms.2013.09.004	journal	August 2013
Effects of Lipid Composition on the Entry of Cell-Penetrating Peptide Oligoarginine into Single Vesicles Sharmin, Sabrina; Islam, Md. Zahidul; Karal, Mohammad Abu Sayem Biochemistry, Vol. 55, Issue 30 https://doi.org/10.1021/acs.biochem.6b00189	journal	July 2016
Beyond the Hofmeister Series: Ion-Specific Effects on Proteins and Their Biological Functions Okur, Halil I.; Hladílková, Jana; Rembert, Kelvin B. The Journal of Physical Chemistry B, Vol. 121, Issue 9 https://doi.org/10.1021/acs.jpcb.6b10797	journal	February 2017
Effects of Mechanical Properties of Lipid Bilayers on the Entry of Cell-Penetrating Peptides into Single Vesicles Islam, Md. Zahidul; Sharmin, Sabrina; Levadnyy, Victor Langmuir, Vol. 33, Issue 9 https://doi.org/10.1021/acs.langmuir.6b03111	journal	February 2017
Membrane Interaction of Chrysophsin-1, a Histidine-Rich Antimicrobial Peptide from Red Sea Bream Mason, A. James; Bertani, Philippe; Moulay, Gilles Biochemistry, Vol. 46, Issue 51 https://doi.org/10.1021/bi701344m	journal	December 2007
Criterion for Amino Acid Composition of Defensins and Antimicrobial Peptides Based on Geometry of Membrane Destabilization Schmidt, Nathan W.; Mishra, Abhijit; Lai, Ghee Hwee Journal of the American Chemical Society, Vol. 133, Issue 17 https://doi.org/10.1021/ja200079a	journal	May 2011
Molecular Basis for Nanoscopic Membrane Curvature Generation from Quantum Mechanical Models and Synthetic Transporter Sequences Schmidt, Nathan W.; Lis, Michael; Zhao, Kun Journal of the American Chemical Society, Vol. 134, Issue 46 https://doi.org/10.1021/ja308459j	journal	November 2012
High-Resolution Structures and Orientations of Antimicrobial Peptides Piscidin 1 and Piscidin 3 in Fluid Bilayers Reveal Tilting, Kinking, and Bilayer Immersion Perrin, B. Scott; Tian, Ye; Fu, Riqiang Journal of the American Chemical Society, Vol. 136, Issue 9 https://doi.org/10.1021/ja411119m	journal	January 2014
Divalent Metal Ion Triggered Activity of a Synthetic Antimicrobial in Cardiolipin Membranes Som, Abhigyan; Yang, Lihua; Wong, Gerard C. L. Journal of the American Chemical Society, Vol. 131, Issue 42 https://doi.org/10.1021/ja9067063	journal	October 2009
Structure and Function in Antimicrobial Piscidins: Histidine Position, Directionality of Membrane Insertion, and pH-Dependent Permeabilization Mihailescu, Mihaela; Sorci, Mirco; Seckute, Jolita Journal of the American Chemical Society, Vol. 141, Issue 25 https://doi.org/10.1021/jacs.9b00440	journal	May 2019
Why Do Arginine and Lysine Organize Lipids Differently? Insights from Coarse-Grained and Atomistic Simulations Wu, Zhe; Cui, Qiang; Yethiraj, Arun The Journal of Physical Chemistry B, Vol. 117, Issue 40 https://doi.org/10.1021/jp4068729	journal	September 2013
Water−Protein Interactions of an Arginine-Rich Membrane Peptide in Lipid Bilayers Investigated by Solid-State Nuclear Magnetic Resonance Spectroscopy Li, Shenhui; Su, Yongchao; Luo, Wenbin The Journal of Physical Chemistry B, Vol. 114, Issue 11 https://doi.org/10.1021/jp912283r	journal	March 2010
Peptide antibiotics in mast cells of fish Silphaduang, Umaporn; Noga, Edward J. Nature, Vol. 414, Issue 6861 https://doi.org/10.1038/35104690	journal	November 2001
Pore formation in lipid membrane I: Continuous reversible trajectory from intact bilayer through hydrophobic defect to transversal pore Akimov, Sergey A.; Volynsky, Pavel E.; Galimzyanov, Timur R. Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/s41598-017-12127-7	journal	September 2017
Insertion mechanism of cell-penetrating peptides into supported phospholipid membranes revealed by X-ray and neutron reflection Choi, D.; Moon, J. H.; Kim, H. Soft Matter, Vol. 8, Issue 32 https://doi.org/10.1039/c2sm25913c	journal	January 2012
Mechanism of a prototypical synthetic membrane-active antimicrobial: Efficient hole-punching via interaction with negative intrinsic curvature lipids Yang, L.; Gordon, V. D.; Trinkle, D. R. Proceedings of the National Academy of Sciences, Vol. 105, Issue 52 https://doi.org/10.1073/pnas.0806456105	journal	December 2008
Translocation of HIV TAT peptide and analogues induced by multiplexed membrane and cytoskeletal interactions Mishra, A.; Lai, G. H.; Schmidt, N. W. Proceedings of the National Academy of Sciences, Vol. 108, Issue 41 https://doi.org/10.1073/pnas.1108795108	journal	October 2011
Mapping membrane activity in undiscovered peptide sequence space using machine learning Lee, Ernest Y.; Fulan, Benjamin M.; Wong, Gerard C. L. Proceedings of the National Academy of Sciences, Vol. 113, Issue 48 https://doi.org/10.1073/pnas.1609893113	journal	November 2016
Unifying structural signature of eukaryotic α-helical host defense peptides Yount, Nannette Y.; Weaver, David C.; Lee, Ernest Y. Proceedings of the National Academy of Sciences, Vol. 116, Issue 14 https://doi.org/10.1073/pnas.1819250116	journal	March 2019
TAT-RasGAP _317-326 kills cells by targeting inner-leaflet–enriched phospholipids Serulla, Marc; Ichim, Gabriel; Stojceski, Filip Proceedings of the National Academy of Sciences, Vol. 117, Issue 50 https://doi.org/10.1073/pnas.2014108117	journal	November 2020
Discovery and Characterization of Two Isoforms of Moronecidin, a Novel Antimicrobial Peptide from Hybrid Striped Bass Lauth, Xavier; Shike, Hiroko; Burns, Jane C. Journal of Biological Chemistry, Vol. 277, Issue 7 https://doi.org/10.1074/jbc.M109173200	journal	February 2002
Copper regulates the interactions of antimicrobial piscidin peptides from fish mast cells with formyl peptide receptors and heparin Kim, So Young; Zhang, Fuming; Gong, Wanghua Journal of Biological Chemistry, Vol. 293, Issue 40 https://doi.org/10.1074/jbc.RA118.001904	journal	October 2018
HELIQUEST: a web server to screen sequences with specific -helical properties Gautier, R.; Douguet, D.; Antonny, B. Bioinformatics, Vol. 24, Issue 18 https://doi.org/10.1093/bioinformatics/btn392	journal	July 2008
APD2: the updated antimicrobial peptide database and its application in peptide design Wang, Guangshun; Li, Xia; Wang, Zhe Nucleic Acids Research, Vol. 37, Issue suppl_1 https://doi.org/10.1093/nar/gkn823	journal	October 2008
Nuclease activity gives an edge to host‐defense peptide piscidin 3 over piscidin 1, rendering it more effective against persisters and biofilms Libardo, M. Daben J.; Bahar, Ali A.; Ma, Buyong The FEBS Journal, Vol. 284, Issue 21 https://doi.org/10.1111/febs.14263	journal	September 2017
Easy Strategy To Increase Salt Resistance of Antimicrobial Peptides Yu, Hui-Yuan; Tu, Chih-Hsiung; Yip, Bak-Sau Antimicrobial Agents and Chemotherapy, Vol. 55, Issue 10 https://doi.org/10.1128/AAC.00202-11	journal	October 2011
Enhanced Membrane Disruption and Antibiotic Action against Pathogenic Bacteria by Designed Histidine-Rich Peptides at Acidic pH Mason, A. James; Gasnier, Claire; Kichler, Antoine Antimicrobial Agents and Chemotherapy, Vol. 50, Issue 10 https://doi.org/10.1128/AAC.00490-06	journal	October 2006
A Novel Target-Specific, Salt-Resistant Antimicrobial Peptide against the Cariogenic Pathogen Streptococcus mutans Mai, Junni; Tian, Xiao-Lin; Gallant, Jeffrey W. Antimicrobial Agents and Chemotherapy, Vol. 55, Issue 11 https://doi.org/10.1128/AAC.05175-11	journal	November 2011
Effects of pH and salinity on the antimicrobial properties of clavanins Lee, I. H.; Cho, Y.; Lehrer, R. I. Infection and Immunity, Vol. 65, Issue 7 https://doi.org/10.1128/iai.65.7.2898-2903.1997	journal	July 1997
IPC – Isoelectric Point Calculator Kozlowski, Lukasz P. Biology Direct, Vol. 11, Issue 1 https://doi.org/10.1186/s13062-016-0159-9	journal	October 2016
Identification of novel antimicrobial peptide from Asian sea bass (Lates calcarifer) by in silico and activity characterization Taheri, Behrouz; Mohammadi, Mohsen; Nabipour, Iraj PLOS ONE, Vol. 13, Issue 10 https://doi.org/10.1371/journal.pone.0206578	journal	October 2018
Genetic, cellular, and structural characterization of the membrane potential-dependent cell-penetrating peptide translocation pore Trofimenko, Evgeniya; Grasso, Gianvito; Heulot, Mathieu eLife, Vol. 10 https://doi.org/10.7554/eLife.69832	journal	October 2021

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