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PSN-PC: a Novel Antimicrobial and Anti-Biofilm Peptide from the Skin

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PSN-PC: a Novel Antimicrobial and Anti-Biofilm Peptide from the Skin PSN-PC: A Novel Antimicrobial and Anti-Biofilm Peptide from the Skin Secretion of Phyllomedusa-camba with Cytotoxicity on Human Lung Cancer Cell Wu, X., Pan, J., Wu, Y., Xi, X., Ma, C., Wang, L., Zhou, M., & Chen, T. (2017). PSN-PC: A Novel Antimicrobial and Anti-Biofilm Peptide from the Skin Secretion of Phyllomedusa-camba with Cytotoxicity on Human Lung Cancer Cell. Molecules, 22(1896), 1-16. https://doi.org/10.3390/molecules22111896 Published in: Molecules Document Version: Publisher's PDF, also known as Version of record Queen's University Belfast - Research Portal: Link to publication record in Queen's University Belfast Research Portal Publisher rights Copyright 2017 the authors. This is an open access article published under a Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution and reproduction in any medium, provided the author and source are cited. General rights Copyright for the publications made accessible via the Queen's University Belfast Research Portal is retained by the author(s) and / or other copyright owners and it is a condition of accessing these publications that users recognise and abide by the legal requirements associated with these rights. Take down policy The Research Portal is Queen's institutional repository that provides access to Queen's research output. Every effort has been made to ensure that content in the Research Portal does not infringe any person's rights, or applicable UK laws. If you discover content in the Research Portal that you believe breaches copyright or violates any law, please contact [email protected]. Download date:23. Sep. 2021 molecules Article PSN-PC: A Novel Antimicrobial and Anti-Biofilm Peptide from the Skin Secretion of Phyllomedusa-camba with Cytotoxicity on Human Lung Cancer Cell Xianhui Wu 1,2, Jinhuo Pan 1,*, Yue Wu 2, Xinping Xi 2, Chengbang Ma 2, Lei Wang 2, Mei Zhou 2 ID and Tianbao Chen 2 ID 1 School of Pharmacy, Nanjing University of Chinese Medicine, Nanjing 210000, China; [email protected] 2 Natural Drug Discovery Group, School of Pharmacy, Queen’s University, Belfast BT9 7BL, Northern Ireland, UK; [email protected] (Y.W.); [email protected] (X.X.); [email protected] (C.M.); [email protected] (L.W.); [email protected] (M.Z.); [email protected] (T.C.) * Correspondence: [email protected]; Tel.: +86-25-8581-1517 Received: 17 October 2017; Accepted: 2 November 2017; Published: 7 November 2017 Abstract: Peptides derived from amphibian skin secretion are promising drug prototypes for combating widespread infection. In this study, a novel peptide belonging to the phylloseptin family of antimicrobial peptides was isolated from the skin secretion of the Phyllomedusa camba, namely phylloseptin-PC (PSN-PC). The biosynthetic precursor was obtained by molecular cloning and the mature peptide sequence was confirmed through tandem mass spectrometry (MS/MS) fragmentation sequencing in the skin secretion. The synthetic replicate exhibited a broad spectrum antimicrobial activity against Staphylococcus aureus, methicillin-resistant Staphylococcus aureus, Escherichia coli, Pseudomonas aeruginosa, Candida albicans at concentrations of 2, 2, 8, 32 and 2 µM, respectively. It also showed the capability of eliminating S. aureus biofilm with a minimal biofilm eradication concentration of 8 µM. The haemolysis of this peptide was not significant at low concentrations but had a considerable increase at high concentrations. Additionally, this peptide showed an anti-proliferation effect on the non-small cell lung cancer cell line (NCI-H157), with low cytotoxicity on the human microvascular endothelial cell line (HMEC-1). The discovery of the novel peptide may provide useful clues for new drug discoveries. Keywords: antimicrobial peptide; phylloseptin; anti-biofilm activity; cancer cell cytotoxicity 1. Introduction Amphibian skin secretion consists of various bioactive peptides that play an essential role in amphibian survival. These peptides demonstrated multifunctional activities against Gram-negative and Gram-positive bacteria, fungi, enveloped viruses and even cancer cells [1]. Additionally, some other peptides are considered potentially to be immunomodulatory and anti-diabetic agents [2], and even contraceptives, as they can be cytotoxic to sperm [3]. These skin-derived antimicrobial peptides (AMPs) are especially predominant and demonstrate board spectrum antimicrobial activity, which make them potential drug candidates in the treatment of bacterial infections. These AMPs are able to efficiently kill antibiotic-resistant bacteria and have little chance for inducing serious drug resistance [4]. Some AMPs have been reported to be capable of inhibiting biofilm formation as well as eradicating mature biofilm [5], which makes bacteria 1,000-fold more resistant to conventional antimicrobial agents than their planktonic counterparts. Among all the AMPs, α-helical antimicrobial peptides, such as magainins [6] and dermaseptins [7], have been extensively studied regarding their biosynthesis, antimicrobial activity, mechanism Molecules 2017, 22, 1896; doi:10.3390/molecules22111896 www.mdpi.com/journal/molecules Molecules 2017, 22, 1896 2 of 16 Molecules 2017, 22, 1896 2 of 16 action,of action, three-dimensional three-dimensional structures, structures, and further and further applications. applications. However, However, the phylloseptins the phylloseptins have not attractedhave not much attracted attention. much Several attention. phylloseptins Several phylloseptins were first identified were first in 2005, identified showing in 2005, anti-bacterial showing andanti-bacterial anti-protozoan and anti-protozoan peptide activities, peptide activities,from the from skin the secretion skin secretion of the of theBrazilian Brazilian tree-frogs, tree-frogs, PhyllomedusaPhyllomedusa hypochondrialis hypochondrialis andand PhyllomedusaPhyllomedusa oreades oreades [8].[8]. Besides, Besides, Yasser Yasser et et al. al. found found a a phylloseptin phylloseptin fromfrom the the skin ofof thethe frogfrogHylomantis Hylomantis lemur lemurinduced induced insulin insulin release release from from the the rat rat BRIN-BD11 BRIN-BD11 clonal clonalβ cell β cellline, line, providing providing a promising a promising alternative alternative for treatingfor treating Type Type 2 diabetes 2 diabetes [9]. [9]. InIn the the present present study, study, the the isolation isolation of of a a novel novel phylloseptin phylloseptin precursor precursor from from the the PhyllomedusaPhyllomedusa camba camba skinskin secretion, secretion, which which has has been been rarely rarely studied studied so so far, far, was was conducted conducted by by ”shotgun” ”shotgun” molecular molecular cloning. cloning. TheThe primary primary structure structure of of the the peptide peptide was was conf confirmedirmed by tandem mass spectrometry (MS/MS) fragmentationfragmentation and and named named phylloseptin-PC phylloseptin-PC (PSN-PC). (PSN-PC). The The replicate replicate was was then then chemically chemically synthesised synthesised andand purifiedpurified forfor downstream downstream study. study. Subsequently, Subsequently experiments, experiments were designedwere designed to evaluate to evaluate the effects the of effectsPSN-PC ofon PSN-PC microorganisms, on microorganism cancer cells, linescancer and cell its lines toxicity and to its horse toxi erythrocytescity to horse and erythrocytes normal human and normalcells of thehuman human cells microvascular of the human endothelial microvascular cell line en (HMEC-1).dothelial cell Furthermore, line (HMEC-1). the secondary Furthermore, structure the secondaryof this novel structure peptide of this was novel predicted peptide and was time-killing predicted curvesand time-killing along with curves bacterial along cell with membrane bacterial cellpermeability membrane assays permeability were performed assays were to explore performed its mechanism to explore ofits action.mechanism of action. 2.2. Results Results 2.1.2.1. Molecular Molecular Cloning Cloning of of a a Novel Novel AMP AMP Precu Precursor-Encodingrsor-Encoding cDNA cDNA and and Bioinformatic Bioinformatic Analyses Analyses AA full-length full-length cDNA cDNA encoding encoding the the biosynthetic biosynthetic precursor precursor of of PSN-PC PSN-PC was was consistently consistently and and successfullysuccessfully cloned cloned from from the the skin skin secretion secretion librar libraryy (Figure (Figure 11).). The alignment of phylloseptins shows thatthat the the members members share share a a highly-conserved highly-conserved amino amino acid acid sequence sequence in in the the phylloseptin phylloseptin family family (Figure (Figure 2).2). ThereThere were were several typical characteristics in in the the translated open open reading frame: (1) (1) a highly-conserved putativeputative signal peptidepeptide regionregion of of 22 22 amino amino acid acid residues, residues, which which is homologous is homologous to each to each other; other; (2) acidic (2) acidicspacer spacer peptide peptide region region consisting consisting of Glu, of Glu, Asp Asp and and other other hydrophilic hydrophilic amino amino acids; acids; (3)(3) a classical classical propeptidepropeptide convertase convertase processing processing site site (-KR-); (-KR-); (4 (4)) a a mature mature active active peptide peptide encoding encoding domain domain that that containedcontained 19 19 amino amino acid acid residues; residues; and and (5) (5) the the C-terminal C-terminal glycine
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