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Switching cytolytic nanopores into antimicrobial fractal ruptures by a single side chain mutation

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Hammond, Katharine, Cipcigan, Flaviu, Al Nahas, Kareem, Losasso, Valeria, Lewis, Helen, Cama, Jehangir, Martelli, Fausto, Simcock, Patrick W., Fletcher, Marcus, Ravi, Jascindra, Stansfeld, Phillip J., Pagliara, Stefano, Hoogenboom, Bart W., Keyser, Ulrich F., Sansom, Mark S. P., Crain, Jason and Ryadnov, Maxim G. (2021) Switching cytolytic nanopores into antimicrobial fractal ruptures by a single side chain mutation. ACS Nano, 15 (6). pp. 9679-9689. doi:10.1021/acsnano.1c00218 ISSN 1936-0851.

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Official URL: http://dx.doi.org/10.1021/acsnano.1c00218

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Abstract

Disruption of cell membranes is a fundamental host defense response found in virtually all forms of life. The molecular mechanisms vary but generally lead to energetically favored circular nanopores. Here, we report an elaborate fractal rupture pattern induced by a single side-chain mutation in ultrashort (8–11-mers) helical peptides, which otherwise form transmembrane pores. In contrast to known mechanisms, this mode of membrane disruption is restricted to the upper leaflet of the bilayer where it exhibits propagating fronts of peptide-lipid interfaces that are strikingly similar to viscous instabilities in fluid flow. The two distinct disruption modes, pores and fractal patterns, are both strongly antimicrobial, but only the fractal rupture is nonhemolytic. The results offer wide implications for elucidating differential membrane targeting phenomena defined at the nanoscale.

Item Type: Journal Article
Subjects: Q Science > QH Natural history
Q Science > QP Physiology
R Medicine > RM Therapeutics. Pharmacology
Divisions: Faculty of Science, Engineering and Medicine > Science > Life Sciences (2010- )
Library of Congress Subject Headings (LCSH): Cell membranes , Antibiotics , Nanopores , Scanning probe microscopy, Bilayer lipid membranes
Journal or Publication Title: ACS Nano
Publisher: American Chemical Society
ISSN: 1936-0851
Official Date: 22 April 2021
Dates:
DateEvent
22 April 2021Published
13 April 2021Accepted
Volume: 15
Number: 6
Page Range: pp. 9679-9689
DOI: 10.1021/acsnano.1c00218
Status: Peer Reviewed
Publication Status: Published
Reuse Statement (publisher, data, author rights): “This document is the Accepted Manuscript version of a Published Work that appeared in final form in ACS Nano, copyright © American Chemical Society after peer review and technical editing by the publisher. To access the final edited and published work see [insert ACS Articles on Request author-directed link to Published Work, see http://pubs.acs.org/page/policy/articlesonrequest/index.html].”
Access rights to Published version: Restricted or Subscription Access
Copyright Holders: © 2021 American Chemical Society
Date of first compliant deposit: 18 June 2021
Date of first compliant Open Access: 22 April 2022
RIOXX Funder/Project Grant:
Project/Grant IDRIOXX Funder NameFunder ID
UNSPECIFIEDDepartment for Business, Energy and Industrial Strategyhttp://dx.doi.org/10.13039/100011693
204909/Z/16/ZWellcome Trusthttp://dx.doi.org/10.13039/100010269
204909/Z/16/ZWellcome Trusthttp://dx.doi.org/10.13039/100010269
WT097835/Z/11/ZWellcome Trusthttp://dx.doi.org/10.13039/100010269
Designer-Pores 647144European Research Councilhttp://dx.doi.org/10.13039/501100000781
StudentshipNational Physical Laboratoryhttp://dx.doi.org/10.13039/501100007851
Winton Programme for the Physics of SustainabilityUniversity of Cambridge. Department of Physicshttp://viaf.org/viaf/305307816
Trinity-Henry Barlow Scholarship Trinity College, University of Cambridgehttp://dx.doi.org/10.13039/501100000727
MCPC17189[MRC] Medical Research Councilhttp://dx.doi.org/10.13039/501100000265
RG180007Royal Societyhttp://dx.doi.org/10.13039/501100000288
WT097835/Z/11/ZWellcome Trusthttp://dx.doi.org/10.13039/100010269
iCASE studentship[EPSRC] Engineering and Physical Sciences Research Councilhttp://dx.doi.org/10.13039/501100000266

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