Defensins from the tick Ixodes scapularis are effective against phytopathogenic fungi and the human bacterial pathogen Listeria grayi

Abstract Background Ixodes scapularis is the most common tick species in North America and a vector of important pathogens that cause diseases in humans and animals including Lyme disease, anaplasmosis and babesiosis. Tick defensins have been identified as a new source of antimicrobial agents with p...

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Main Authors: Miray Tonk, Alejandro Cabezas-Cruz, James J Valdés, Ryan OM Rego, Tereza Chrudimská, Martin Strnad, Radek Šíma, Lesley Bell-Sakyi, Zdeněk Franta, Andreas Vilcinskas, Libor Grubhoffer, Mohammad Rahnamaeian
Format: Article
Language:English
Published: BMC 2014-12-01
Series:Parasites & Vectors
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Online Access:https://doi.org/10.1186/s13071-014-0554-y
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author Miray Tonk
Alejandro Cabezas-Cruz
James J Valdés
Ryan OM Rego
Tereza Chrudimská
Martin Strnad
Radek Šíma
Lesley Bell-Sakyi
Zdeněk Franta
Andreas Vilcinskas
Libor Grubhoffer
Mohammad Rahnamaeian
author_facet Miray Tonk
Alejandro Cabezas-Cruz
James J Valdés
Ryan OM Rego
Tereza Chrudimská
Martin Strnad
Radek Šíma
Lesley Bell-Sakyi
Zdeněk Franta
Andreas Vilcinskas
Libor Grubhoffer
Mohammad Rahnamaeian
author_sort Miray Tonk
collection DOAJ
description Abstract Background Ixodes scapularis is the most common tick species in North America and a vector of important pathogens that cause diseases in humans and animals including Lyme disease, anaplasmosis and babesiosis. Tick defensins have been identified as a new source of antimicrobial agents with putative medical applications due to their wide-ranging antimicrobial activities. Two multigene families of defensins were previously reported in I. scapularis. The objective of the present study was to characterise the potential antimicrobial activity of two defensins from I. scapularis with emphasis on human pathogenic bacterial strains and important phytopathogenic fungi. Methods Scapularisin-3 and Scapularisin-6 mature peptides were chemically synthesised. In vitro antimicrobial assays were performed to test the activity of these two defensins against species of different bacterial genera including Gram-positive bacteria Staphylococcus aureus, Staphylococcus epidermidis, and Listeria spp. as well as Gram-negative bacteria Escherichia coli, Pseudomonas aeruginosa along with two plant-pathogenic fungi from the genus Fusarium. In addition, the tissue-specific expression patterns of Scapularisin-3 and Scapularisin-6 in I. scapularis midgut, salivary glands and embryo-derived cell lines were determined using PCR. Finally, tertiary structures of the two defensins were predicted and structural analyses were conducted. Results Scapularisin-6 efficiently killed L. grayi, and both Scapularisin-3 and Scapularisin-6 caused strong inhibition (IC50 value: ~1 μM) of the germination of plant-pathogenic fungi Fusarium culmorum and Fusarium graminearum. Scapularisin-6 gene expression was observed in I. scapularis salivary glands and midgut. However, Scapularisin-3 gene expression was only detected in the salivary glands. Transcripts from the two defensins were not found in the I. scapularis tick cell lines ISE6 and ISE18. Conclusion Our results have two main implications. Firstly, the anti-Listeria and antifungal activities of Scapularisin-3 and Scapularisin-6 suggest that these peptides may be useful for (i) treatment of antibiotic-resistant L. grayi in humans and (ii) plant protection. Secondly, the antimicrobial properties of the two defensins described in this study may pave the way for further studies regarding pathogen invasion and innate immunity in I. scapularis.
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spelling doaj.art-5b8489f5556d489699c67d5b7c1c23c82023-06-04T11:21:29ZengBMCParasites & Vectors1756-33052014-12-01711810.1186/s13071-014-0554-yDefensins from the tick Ixodes scapularis are effective against phytopathogenic fungi and the human bacterial pathogen Listeria grayiMiray Tonk0Alejandro Cabezas-Cruz1James J Valdés2Ryan OM Rego3Tereza Chrudimská4Martin Strnad5Radek Šíma6Lesley Bell-Sakyi7Zdeněk Franta8Andreas Vilcinskas9Libor Grubhoffer10Mohammad Rahnamaeian11Biology Centre of the AS CR, Institute of ParasitologySaBio. Instituto de Investigación en Recursos Cinegéticos IREC, CSIC-UCLM-JCCMBiology Centre of the AS CR, Institute of ParasitologyBiology Centre of the AS CR, Institute of ParasitologyBiology Centre of the AS CR, Institute of ParasitologyBiology Centre of the AS CR, Institute of ParasitologyBiology Centre of the AS CR, Institute of ParasitologyThe Pirbright InstituteDepartment of Bioresources, Fraunhofer Institute for Molecular Biology and Applied EcologyDepartment of Bioresources, Fraunhofer Institute for Molecular Biology and Applied EcologyBiology Centre of the AS CR, Institute of ParasitologyDepartment of Bioresources, Fraunhofer Institute for Molecular Biology and Applied EcologyAbstract Background Ixodes scapularis is the most common tick species in North America and a vector of important pathogens that cause diseases in humans and animals including Lyme disease, anaplasmosis and babesiosis. Tick defensins have been identified as a new source of antimicrobial agents with putative medical applications due to their wide-ranging antimicrobial activities. Two multigene families of defensins were previously reported in I. scapularis. The objective of the present study was to characterise the potential antimicrobial activity of two defensins from I. scapularis with emphasis on human pathogenic bacterial strains and important phytopathogenic fungi. Methods Scapularisin-3 and Scapularisin-6 mature peptides were chemically synthesised. In vitro antimicrobial assays were performed to test the activity of these two defensins against species of different bacterial genera including Gram-positive bacteria Staphylococcus aureus, Staphylococcus epidermidis, and Listeria spp. as well as Gram-negative bacteria Escherichia coli, Pseudomonas aeruginosa along with two plant-pathogenic fungi from the genus Fusarium. In addition, the tissue-specific expression patterns of Scapularisin-3 and Scapularisin-6 in I. scapularis midgut, salivary glands and embryo-derived cell lines were determined using PCR. Finally, tertiary structures of the two defensins were predicted and structural analyses were conducted. Results Scapularisin-6 efficiently killed L. grayi, and both Scapularisin-3 and Scapularisin-6 caused strong inhibition (IC50 value: ~1 μM) of the germination of plant-pathogenic fungi Fusarium culmorum and Fusarium graminearum. Scapularisin-6 gene expression was observed in I. scapularis salivary glands and midgut. However, Scapularisin-3 gene expression was only detected in the salivary glands. Transcripts from the two defensins were not found in the I. scapularis tick cell lines ISE6 and ISE18. Conclusion Our results have two main implications. Firstly, the anti-Listeria and antifungal activities of Scapularisin-3 and Scapularisin-6 suggest that these peptides may be useful for (i) treatment of antibiotic-resistant L. grayi in humans and (ii) plant protection. Secondly, the antimicrobial properties of the two defensins described in this study may pave the way for further studies regarding pathogen invasion and innate immunity in I. scapularis.https://doi.org/10.1186/s13071-014-0554-yAntimicrobial peptideDefensinListeria grayiFusarium sppIxodes scapularisTick cell line
spellingShingle Miray Tonk
Alejandro Cabezas-Cruz
James J Valdés
Ryan OM Rego
Tereza Chrudimská
Martin Strnad
Radek Šíma
Lesley Bell-Sakyi
Zdeněk Franta
Andreas Vilcinskas
Libor Grubhoffer
Mohammad Rahnamaeian
Defensins from the tick Ixodes scapularis are effective against phytopathogenic fungi and the human bacterial pathogen Listeria grayi
Parasites & Vectors
Antimicrobial peptide
Defensin
Listeria grayi
Fusarium spp
Ixodes scapularis
Tick cell line
title Defensins from the tick Ixodes scapularis are effective against phytopathogenic fungi and the human bacterial pathogen Listeria grayi
title_full Defensins from the tick Ixodes scapularis are effective against phytopathogenic fungi and the human bacterial pathogen Listeria grayi
title_fullStr Defensins from the tick Ixodes scapularis are effective against phytopathogenic fungi and the human bacterial pathogen Listeria grayi
title_full_unstemmed Defensins from the tick Ixodes scapularis are effective against phytopathogenic fungi and the human bacterial pathogen Listeria grayi
title_short Defensins from the tick Ixodes scapularis are effective against phytopathogenic fungi and the human bacterial pathogen Listeria grayi
title_sort defensins from the tick ixodes scapularis are effective against phytopathogenic fungi and the human bacterial pathogen listeria grayi
topic Antimicrobial peptide
Defensin
Listeria grayi
Fusarium spp
Ixodes scapularis
Tick cell line
url https://doi.org/10.1186/s13071-014-0554-y
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