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2-Cys peroxiredoxin is required in successful blood-feeding, reproduction, and antioxidant response in the hard tick Haemaphysalis longicornis

BACKGROUND: Ticks are obligate hematophagous arthropods that feed on vertebrate blood that contains iron. Ticks also concentrate host blood with iron; this concentration of the blood leads to high levels of iron in ticks. The host-derived iron reacts with oxygen in the tick body and this may generat...

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Autores principales: Kusakisako, Kodai, Galay, Remil Linggatong, Umemiya-Shirafuji, Rika, Hernandez, Emmanuel Pacia, Maeda, Hiroki, Talactac, Melbourne Rio, Tsuji, Naotoshi, Mochizuki, Masami, Fujisaki, Kozo, Tanaka, Tetsuya
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4992251/
https://www.ncbi.nlm.nih.gov/pubmed/27542835
http://dx.doi.org/10.1186/s13071-016-1748-2
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author Kusakisako, Kodai
Galay, Remil Linggatong
Umemiya-Shirafuji, Rika
Hernandez, Emmanuel Pacia
Maeda, Hiroki
Talactac, Melbourne Rio
Tsuji, Naotoshi
Mochizuki, Masami
Fujisaki, Kozo
Tanaka, Tetsuya
author_facet Kusakisako, Kodai
Galay, Remil Linggatong
Umemiya-Shirafuji, Rika
Hernandez, Emmanuel Pacia
Maeda, Hiroki
Talactac, Melbourne Rio
Tsuji, Naotoshi
Mochizuki, Masami
Fujisaki, Kozo
Tanaka, Tetsuya
author_sort Kusakisako, Kodai
collection PubMed
description BACKGROUND: Ticks are obligate hematophagous arthropods that feed on vertebrate blood that contains iron. Ticks also concentrate host blood with iron; this concentration of the blood leads to high levels of iron in ticks. The host-derived iron reacts with oxygen in the tick body and this may generate high levels of reactive oxygen species, including hydrogen peroxide (H(2)O(2)). High levels of H(2)O(2) cause oxidative stress in organisms and therefore, antioxidant responses are necessary to regulate H(2)O(2). Here, we focused on peroxiredoxin (Prx), an H(2)O(2)-scavenging enzyme in the hard tick Haemaphysalis longicornis. METHODS: The mRNA and protein expression profiles of 2-Cys peroxiredoxin (HlPrx2) in H. longicornis were investigated in whole ticks and internal organs, and developmental stages, using real-time PCR and Western blot analysis during blood-feeding. The localization of HlPrx2 proteins in tick tissues was also observed by immunostaining. Moreover, knockdown experiments of HlPrx2 were performed using RNA interference to evaluate its function in ticks. RESULTS: Real-time PCR showed that HlPrx2 gene expression in whole ticks and internal organs was significantly upregulated by blood-feeding. However, protein expression, except in the midgut, was constant throughout blood-feeding. Knockdown of the HlPrx2 gene caused significant differences in the engorged body weight, egg weight and hatching rate for larvae as compared to the control group. Finally, detection of H(2)O(2) after knockdown of HlPrxs in ticks showed that the concentration of H(2)O(2) significantly increased before and after blood-feeding. CONCLUSION: Therefore, HlPrx2 can be considered important for successful blood-feeding and reproduction through the regulation of H(2)O(2) concentrations in ticks before and after blood-feeding. This study contributes to the search for a candidate target for tick control and further understanding of the tick’s oxidative stress coping mechanism during blood-feeding. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s13071-016-1748-2) contains supplementary material, which is available to authorized users.
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spelling pubmed-49922512016-08-21 2-Cys peroxiredoxin is required in successful blood-feeding, reproduction, and antioxidant response in the hard tick Haemaphysalis longicornis Kusakisako, Kodai Galay, Remil Linggatong Umemiya-Shirafuji, Rika Hernandez, Emmanuel Pacia Maeda, Hiroki Talactac, Melbourne Rio Tsuji, Naotoshi Mochizuki, Masami Fujisaki, Kozo Tanaka, Tetsuya Parasit Vectors Research BACKGROUND: Ticks are obligate hematophagous arthropods that feed on vertebrate blood that contains iron. Ticks also concentrate host blood with iron; this concentration of the blood leads to high levels of iron in ticks. The host-derived iron reacts with oxygen in the tick body and this may generate high levels of reactive oxygen species, including hydrogen peroxide (H(2)O(2)). High levels of H(2)O(2) cause oxidative stress in organisms and therefore, antioxidant responses are necessary to regulate H(2)O(2). Here, we focused on peroxiredoxin (Prx), an H(2)O(2)-scavenging enzyme in the hard tick Haemaphysalis longicornis. METHODS: The mRNA and protein expression profiles of 2-Cys peroxiredoxin (HlPrx2) in H. longicornis were investigated in whole ticks and internal organs, and developmental stages, using real-time PCR and Western blot analysis during blood-feeding. The localization of HlPrx2 proteins in tick tissues was also observed by immunostaining. Moreover, knockdown experiments of HlPrx2 were performed using RNA interference to evaluate its function in ticks. RESULTS: Real-time PCR showed that HlPrx2 gene expression in whole ticks and internal organs was significantly upregulated by blood-feeding. However, protein expression, except in the midgut, was constant throughout blood-feeding. Knockdown of the HlPrx2 gene caused significant differences in the engorged body weight, egg weight and hatching rate for larvae as compared to the control group. Finally, detection of H(2)O(2) after knockdown of HlPrxs in ticks showed that the concentration of H(2)O(2) significantly increased before and after blood-feeding. CONCLUSION: Therefore, HlPrx2 can be considered important for successful blood-feeding and reproduction through the regulation of H(2)O(2) concentrations in ticks before and after blood-feeding. This study contributes to the search for a candidate target for tick control and further understanding of the tick’s oxidative stress coping mechanism during blood-feeding. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s13071-016-1748-2) contains supplementary material, which is available to authorized users. BioMed Central 2016-08-19 /pmc/articles/PMC4992251/ /pubmed/27542835 http://dx.doi.org/10.1186/s13071-016-1748-2 Text en © The Author(s). 2016 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research
Kusakisako, Kodai
Galay, Remil Linggatong
Umemiya-Shirafuji, Rika
Hernandez, Emmanuel Pacia
Maeda, Hiroki
Talactac, Melbourne Rio
Tsuji, Naotoshi
Mochizuki, Masami
Fujisaki, Kozo
Tanaka, Tetsuya
2-Cys peroxiredoxin is required in successful blood-feeding, reproduction, and antioxidant response in the hard tick Haemaphysalis longicornis
title 2-Cys peroxiredoxin is required in successful blood-feeding, reproduction, and antioxidant response in the hard tick Haemaphysalis longicornis
title_full 2-Cys peroxiredoxin is required in successful blood-feeding, reproduction, and antioxidant response in the hard tick Haemaphysalis longicornis
title_fullStr 2-Cys peroxiredoxin is required in successful blood-feeding, reproduction, and antioxidant response in the hard tick Haemaphysalis longicornis
title_full_unstemmed 2-Cys peroxiredoxin is required in successful blood-feeding, reproduction, and antioxidant response in the hard tick Haemaphysalis longicornis
title_short 2-Cys peroxiredoxin is required in successful blood-feeding, reproduction, and antioxidant response in the hard tick Haemaphysalis longicornis
title_sort 2-cys peroxiredoxin is required in successful blood-feeding, reproduction, and antioxidant response in the hard tick haemaphysalis longicornis
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4992251/
https://www.ncbi.nlm.nih.gov/pubmed/27542835
http://dx.doi.org/10.1186/s13071-016-1748-2
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