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A chitin deacetylase-like protein is a predominant constituent of tick peritrophic membrane that influences the persistence of Lyme disease pathogens within the vector
Ixodes scapularis is the specific arthropod vector for a number of globally prevalent infections, including Lyme disease caused by the bacterium Borrelia burgdorferi. A feeding-induced and acellular epithelial barrier, known as the peritrophic membrane (PM) is detectable in I. scapularis. However, w...
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Published in: | PloS one 2013-10, Vol.8 (10), p.e78376-e78376 |
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description | Ixodes scapularis is the specific arthropod vector for a number of globally prevalent infections, including Lyme disease caused by the bacterium Borrelia burgdorferi. A feeding-induced and acellular epithelial barrier, known as the peritrophic membrane (PM) is detectable in I. scapularis. However, whether or how the PM influences the persistence of major tick-borne pathogens, such as B. burgdorferi, remains largely unknown. Mass spectrometry-based proteome analyses of isolated PM from fed ticks revealed that the membrane contains a few detectable proteins, including a predominant and immunogenic 60 kDa protein with homology to arthropod chitin deacetylase (CDA), herein termed I. scapularis CDA-like protein or IsCDA. Although IsCDA is primarily expressed in the gut and induced early during tick feeding, its silencing via RNA interference failed to influence either the occurrence of the PM or spirochete persistence, suggesting a redundant role of IsCDA in tick biology and host-pathogen interaction. However, treatment of ticks with antibodies against IsCDA, one of the most predominant protein components of PM, affected B. burgdorferi survival, significantly augmenting pathogen levels within ticks but without influencing the levels of total gut bacteria. These studies suggested a preferential role of tick PM in limiting persistence of B. burgdorferi within the vector. Further understanding of the mechanisms by which vector components contribute to pathogen survival may help the development of new strategies to interfere with the infection. |
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A feeding-induced and acellular epithelial barrier, known as the peritrophic membrane (PM) is detectable in I. scapularis. However, whether or how the PM influences the persistence of major tick-borne pathogens, such as B. burgdorferi, remains largely unknown. Mass spectrometry-based proteome analyses of isolated PM from fed ticks revealed that the membrane contains a few detectable proteins, including a predominant and immunogenic 60 kDa protein with homology to arthropod chitin deacetylase (CDA), herein termed I. scapularis CDA-like protein or IsCDA. Although IsCDA is primarily expressed in the gut and induced early during tick feeding, its silencing via RNA interference failed to influence either the occurrence of the PM or spirochete persistence, suggesting a redundant role of IsCDA in tick biology and host-pathogen interaction. However, treatment of ticks with antibodies against IsCDA, one of the most predominant protein components of PM, affected B. burgdorferi survival, significantly augmenting pathogen levels within ticks but without influencing the levels of total gut bacteria. These studies suggested a preferential role of tick PM in limiting persistence of B. burgdorferi within the vector. Further understanding of the mechanisms by which vector components contribute to pathogen survival may help the development of new strategies to interfere with the infection.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0078376</identifier><identifier>PMID: 24147133</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Amidohydrolases - genetics ; Amidohydrolases - metabolism ; Analysis ; Animals ; Antibodies ; Arachnid Vectors - enzymology ; Arachnid Vectors - microbiology ; Arachnids ; Arthropoda ; Arthropods ; Bacteria ; Bacterial infections ; Borrelia burgdorferi ; Chitin ; Chitin deacetylase ; Feeding ; Gastrointestinal Tract - metabolism ; Health aspects ; Homology ; Immunogenicity ; Infection ; Infections ; Insects ; Laboratory animals ; Leishmania ; Lyme disease ; Lyme Disease - transmission ; Mass spectrometry ; Mass spectroscopy ; Microbiota (Symbiotic organisms) ; Pathogenic microorganisms ; Pathogens ; Peritrophic membrane ; Physiology ; Proteins ; Proteomes ; Ribonucleic acid ; RNA ; RNA-mediated interference ; Spirochaetales - metabolism ; Spirochetes ; Studies ; Survival ; Ticks ; Ticks - enzymology ; Ticks - microbiology ; Vaccines ; Vector-borne diseases ; Veterinary colleges ; Veterinary medicine</subject><ispartof>PloS one, 2013-10, Vol.8 (10), p.e78376-e78376</ispartof><rights>COPYRIGHT 2013 Public Library of Science</rights><rights>2013 Kariu et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: https://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. 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A feeding-induced and acellular epithelial barrier, known as the peritrophic membrane (PM) is detectable in I. scapularis. However, whether or how the PM influences the persistence of major tick-borne pathogens, such as B. burgdorferi, remains largely unknown. Mass spectrometry-based proteome analyses of isolated PM from fed ticks revealed that the membrane contains a few detectable proteins, including a predominant and immunogenic 60 kDa protein with homology to arthropod chitin deacetylase (CDA), herein termed I. scapularis CDA-like protein or IsCDA. Although IsCDA is primarily expressed in the gut and induced early during tick feeding, its silencing via RNA interference failed to influence either the occurrence of the PM or spirochete persistence, suggesting a redundant role of IsCDA in tick biology and host-pathogen interaction. However, treatment of ticks with antibodies against IsCDA, one of the most predominant protein components of PM, affected B. burgdorferi survival, significantly augmenting pathogen levels within ticks but without influencing the levels of total gut bacteria. These studies suggested a preferential role of tick PM in limiting persistence of B. burgdorferi within the vector. Further understanding of the mechanisms by which vector components contribute to pathogen survival may help the development of new strategies to interfere with the infection.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>24147133</pmid><doi>10.1371/journal.pone.0078376</doi><tpages>e78376</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Amidohydrolases - genetics Amidohydrolases - metabolism Analysis Animals Antibodies Arachnid Vectors - enzymology Arachnid Vectors - microbiology Arachnids Arthropoda Arthropods Bacteria Bacterial infections Borrelia burgdorferi Chitin Chitin deacetylase Feeding Gastrointestinal Tract - metabolism Health aspects Homology Immunogenicity Infection Infections Insects Laboratory animals Leishmania Lyme disease Lyme Disease - transmission Mass spectrometry Mass spectroscopy Microbiota (Symbiotic organisms) Pathogenic microorganisms Pathogens Peritrophic membrane Physiology Proteins Proteomes Ribonucleic acid RNA RNA-mediated interference Spirochaetales - metabolism Spirochetes Studies Survival Ticks Ticks - enzymology Ticks - microbiology Vaccines Vector-borne diseases Veterinary colleges Veterinary medicine |
title | A chitin deacetylase-like protein is a predominant constituent of tick peritrophic membrane that influences the persistence of Lyme disease pathogens within the vector |
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