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The ecdysteroid receptor regulates salivary gland degeneration through apoptosis in Rhipicephalus haemaphysaloides

It is well established that ecdysteroid hormones play an important role in arthropod development and reproduction, mediated by ecdysteroid receptors. Ticks are obligate hematophagous arthropods and vectors of pathogens. The salivary gland plays an essential role in tick growth and reproduction and i...

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Published in:Parasites & vectors 2021-12, Vol.14 (1), p.612-612, Article 612
Main Authors: Lu, Xiaojuan, Zhang, Zhipeng, Yuan, Dongqi, Zhou, Yongzhi, Cao, Jie, Zhang, Houshuang, da Silva Vaz, Jr, Itabajara, Zhou, Jinlin
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container_title Parasites & vectors
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creator Lu, Xiaojuan
Zhang, Zhipeng
Yuan, Dongqi
Zhou, Yongzhi
Cao, Jie
Zhang, Houshuang
da Silva Vaz, Jr, Itabajara
Zhou, Jinlin
description It is well established that ecdysteroid hormones play an important role in arthropod development and reproduction, mediated by ecdysteroid receptors. Ticks are obligate hematophagous arthropods and vectors of pathogens. The salivary gland plays an essential role in tick growth and reproduction and in the transmission of pathogens to vertebrate hosts. During tick development, the salivary gland undergoes degeneration triggered by ecdysteroid hormones and activated by apoptosis. However, it is unknown how the ecdysteroid receptor and apoptosis regulate salivary gland degeneration. Here, we report the functional ecdysteroid receptor (a heterodimer of the ecdysone receptor [EcR] and ultraspiracle [USP]) isolated from the salivary gland of the tick Rhipicephalus haemaphysaloides and explore the molecular mechanism of ecdysteroid receptor regulation of salivary gland degeneration. The full length of RhEcR and RhUSP open reading frames (ORFs) was obtained from the transcriptome. The RhEcR and RhUSP proteins were expressed in a bacterial heterologous system, Escherichia coli. Polyclonal antibodies were produced against synthetic peptides and were able to recognize recombinant and native proteins. Quantitative real-time PCR and western blot were used to detect the distribution of RhEcR, RhUSP, and RhCaspases in the R. haemaphysaloides organs. A proteomics approach was used to analyze the expression profiles of the ecdysteroid receptors, RhCaspases, and other proteins. To analyze the function of the ecdysteroid receptor, RNA interference (RNAi) was used to silence the genes in adult female ticks. Finally, the interaction of RhEcR and RhUSP was identified by heterologous co-expression assays in HEK293T cells. We identified the functional ecdysone receptor (RhEcR/RhUSP) of 20-hydroxyecdysone from the salivary gland of the tick R. haemaphysaloides. The RhEcR and RhUSP genes have three and two isoforms, respectively, and belong to a nuclear receptor family but with variable N-terminal A/B domains. The RhEcR gene silencing inhibited blood-feeding, blocked engorgement, and restrained salivary gland degeneration, showing the biological role of the RhEcR gene in ticks. In the ecdysteroid signaling pathway, RhEcR silencing inhibited salivary gland degeneration by suppressing caspase-dependent apoptosis. The heterologous expression in mammalian HEK293T cells showed that RhEcR1 interacts with RhUSP1 and induces caspase-dependent apoptosis. These data show that RhEcR has an ess
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Ticks are obligate hematophagous arthropods and vectors of pathogens. The salivary gland plays an essential role in tick growth and reproduction and in the transmission of pathogens to vertebrate hosts. During tick development, the salivary gland undergoes degeneration triggered by ecdysteroid hormones and activated by apoptosis. However, it is unknown how the ecdysteroid receptor and apoptosis regulate salivary gland degeneration. Here, we report the functional ecdysteroid receptor (a heterodimer of the ecdysone receptor [EcR] and ultraspiracle [USP]) isolated from the salivary gland of the tick Rhipicephalus haemaphysaloides and explore the molecular mechanism of ecdysteroid receptor regulation of salivary gland degeneration. The full length of RhEcR and RhUSP open reading frames (ORFs) was obtained from the transcriptome. The RhEcR and RhUSP proteins were expressed in a bacterial heterologous system, Escherichia coli. Polyclonal antibodies were produced against synthetic peptides and were able to recognize recombinant and native proteins. Quantitative real-time PCR and western blot were used to detect the distribution of RhEcR, RhUSP, and RhCaspases in the R. haemaphysaloides organs. A proteomics approach was used to analyze the expression profiles of the ecdysteroid receptors, RhCaspases, and other proteins. To analyze the function of the ecdysteroid receptor, RNA interference (RNAi) was used to silence the genes in adult female ticks. Finally, the interaction of RhEcR and RhUSP was identified by heterologous co-expression assays in HEK293T cells. We identified the functional ecdysone receptor (RhEcR/RhUSP) of 20-hydroxyecdysone from the salivary gland of the tick R. haemaphysaloides. The RhEcR and RhUSP genes have three and two isoforms, respectively, and belong to a nuclear receptor family but with variable N-terminal A/B domains. The RhEcR gene silencing inhibited blood-feeding, blocked engorgement, and restrained salivary gland degeneration, showing the biological role of the RhEcR gene in ticks. In the ecdysteroid signaling pathway, RhEcR silencing inhibited salivary gland degeneration by suppressing caspase-dependent apoptosis. The heterologous expression in mammalian HEK293T cells showed that RhEcR1 interacts with RhUSP1 and induces caspase-dependent apoptosis. These data show that RhEcR has an essential role in tick physiology and represents a putative target for the control of ticks and tick-borne diseases.</description><identifier>ISSN: 1756-3305</identifier><identifier>EISSN: 1756-3305</identifier><identifier>DOI: 10.1186/s13071-021-05052-2</identifier><identifier>PMID: 34930413</identifier><language>eng</language><publisher>England: BioMed Central Ltd</publisher><subject>Animals ; Antibodies ; Apoptosis ; Apoptosis - physiology ; Arthropods ; Body organs ; Caspase ; Cells ; Cloning ; Cloning, Molecular ; Degeneration ; E coli ; Ecdysone ; Ecdysone receptor ; Ecdysteroid receptors ; Ecdysteroids ; Engorgement ; Exocrine glands ; Feeding Behavior ; Female ; Females ; Gene expression ; Gene Expression Regulation - physiology ; Gene silencing ; Genes ; HEK293 Cells ; Hormones ; Humans ; Identification ; Insect hormones ; Insects ; Isoforms ; Laboratories ; Maximum likelihood method ; Metabolism ; Metabolites ; Morphology ; Nitrogen ; Nucleotide sequence ; Open Reading Frames ; Organs ; Ovaries ; Parasitic diseases ; Pathogens ; PCR ; Peptides ; Physiological aspects ; Polyclonal antibodies ; Proteins ; Proteomics ; Receptor mechanisms ; Receptors ; Receptors, Steroid - genetics ; Receptors, Steroid - metabolism ; Recombinants ; Reproduction ; Rhipicephalus - metabolism ; Rhipicephalus haemaphysaloides ; RNA Interference ; RNA, Double-Stranded ; RNA-mediated interference ; Salivary gland ; Salivary gland degeneration ; Salivary glands ; Salivary Glands - physiology ; Signal transduction ; Software ; Steroids ; Synthetic peptides ; Tick ; Tick-borne diseases ; Ticks ; Transcriptomes ; Ultraspiracle ; Vectors ; Vertebrates</subject><ispartof>Parasites &amp; vectors, 2021-12, Vol.14 (1), p.612-612, Article 612</ispartof><rights>2021. The Author(s).</rights><rights>COPYRIGHT 2021 BioMed Central Ltd.</rights><rights>2021. This work is licensed under http://creativecommons.org/licenses/by/4.0/ (the “License”). 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Ticks are obligate hematophagous arthropods and vectors of pathogens. The salivary gland plays an essential role in tick growth and reproduction and in the transmission of pathogens to vertebrate hosts. During tick development, the salivary gland undergoes degeneration triggered by ecdysteroid hormones and activated by apoptosis. However, it is unknown how the ecdysteroid receptor and apoptosis regulate salivary gland degeneration. Here, we report the functional ecdysteroid receptor (a heterodimer of the ecdysone receptor [EcR] and ultraspiracle [USP]) isolated from the salivary gland of the tick Rhipicephalus haemaphysaloides and explore the molecular mechanism of ecdysteroid receptor regulation of salivary gland degeneration. The full length of RhEcR and RhUSP open reading frames (ORFs) was obtained from the transcriptome. The RhEcR and RhUSP proteins were expressed in a bacterial heterologous system, Escherichia coli. Polyclonal antibodies were produced against synthetic peptides and were able to recognize recombinant and native proteins. Quantitative real-time PCR and western blot were used to detect the distribution of RhEcR, RhUSP, and RhCaspases in the R. haemaphysaloides organs. A proteomics approach was used to analyze the expression profiles of the ecdysteroid receptors, RhCaspases, and other proteins. To analyze the function of the ecdysteroid receptor, RNA interference (RNAi) was used to silence the genes in adult female ticks. Finally, the interaction of RhEcR and RhUSP was identified by heterologous co-expression assays in HEK293T cells. We identified the functional ecdysone receptor (RhEcR/RhUSP) of 20-hydroxyecdysone from the salivary gland of the tick R. haemaphysaloides. The RhEcR and RhUSP genes have three and two isoforms, respectively, and belong to a nuclear receptor family but with variable N-terminal A/B domains. The RhEcR gene silencing inhibited blood-feeding, blocked engorgement, and restrained salivary gland degeneration, showing the biological role of the RhEcR gene in ticks. In the ecdysteroid signaling pathway, RhEcR silencing inhibited salivary gland degeneration by suppressing caspase-dependent apoptosis. The heterologous expression in mammalian HEK293T cells showed that RhEcR1 interacts with RhUSP1 and induces caspase-dependent apoptosis. These data show that RhEcR has an essential role in tick physiology and represents a putative target for the control of ticks and tick-borne diseases.</description><subject>Animals</subject><subject>Antibodies</subject><subject>Apoptosis</subject><subject>Apoptosis - physiology</subject><subject>Arthropods</subject><subject>Body organs</subject><subject>Caspase</subject><subject>Cells</subject><subject>Cloning</subject><subject>Cloning, Molecular</subject><subject>Degeneration</subject><subject>E coli</subject><subject>Ecdysone</subject><subject>Ecdysone receptor</subject><subject>Ecdysteroid receptors</subject><subject>Ecdysteroids</subject><subject>Engorgement</subject><subject>Exocrine glands</subject><subject>Feeding Behavior</subject><subject>Female</subject><subject>Females</subject><subject>Gene expression</subject><subject>Gene Expression Regulation - physiology</subject><subject>Gene silencing</subject><subject>Genes</subject><subject>HEK293 Cells</subject><subject>Hormones</subject><subject>Humans</subject><subject>Identification</subject><subject>Insect hormones</subject><subject>Insects</subject><subject>Isoforms</subject><subject>Laboratories</subject><subject>Maximum likelihood method</subject><subject>Metabolism</subject><subject>Metabolites</subject><subject>Morphology</subject><subject>Nitrogen</subject><subject>Nucleotide sequence</subject><subject>Open Reading Frames</subject><subject>Organs</subject><subject>Ovaries</subject><subject>Parasitic diseases</subject><subject>Pathogens</subject><subject>PCR</subject><subject>Peptides</subject><subject>Physiological aspects</subject><subject>Polyclonal antibodies</subject><subject>Proteins</subject><subject>Proteomics</subject><subject>Receptor mechanisms</subject><subject>Receptors</subject><subject>Receptors, Steroid - genetics</subject><subject>Receptors, Steroid - metabolism</subject><subject>Recombinants</subject><subject>Reproduction</subject><subject>Rhipicephalus - metabolism</subject><subject>Rhipicephalus haemaphysaloides</subject><subject>RNA Interference</subject><subject>RNA, Double-Stranded</subject><subject>RNA-mediated interference</subject><subject>Salivary gland</subject><subject>Salivary gland degeneration</subject><subject>Salivary glands</subject><subject>Salivary Glands - physiology</subject><subject>Signal transduction</subject><subject>Software</subject><subject>Steroids</subject><subject>Synthetic peptides</subject><subject>Tick</subject><subject>Tick-borne diseases</subject><subject>Ticks</subject><subject>Transcriptomes</subject><subject>Ultraspiracle</subject><subject>Vectors</subject><subject>Vertebrates</subject><issn>1756-3305</issn><issn>1756-3305</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><sourceid>PIMPY</sourceid><sourceid>DOA</sourceid><recordid>eNptkl-L1DAUxYso7jr6BXyQgi_60DV_mjR9EZZF3YEFYV2fQ5retBk6TU3axfn23p3ZXXdESmhIfueEezhZ9paSM0qV_JQoJxUtCMMliGAFe5ad0krIgnMinj_Zn2SvUtoQIkkt5MvshJc1JyXlp1m86SEH2-7SDDH4No9gYZpDxE23DGaGlCcz-FsTd3k3mLHNW-hghGhmH8Z87mNYuj43U0BV8in3Y37d-8mjTW-GJeW9ga2Z-h3a4AOQXmcvnBkSvLn_r7KfX7_cXFwWV9-_rS_Orwor6mouJBdU2apxbV03QvCGi4ooI1SjoJKubJhwjFHSMMYAZA0VLRWOVymnHEV8la0Pvm0wGz1Fv8UZdDBe7w9C7LSJs7cDaEudaBVVCoQrZeMaqxrKoOWlVNZgWKvs88FrWpottBbGOZrhyPT4ZvS97sKtVlJJsTf4cG8Qw68F0qy3PlkYMFEIS9JMUsYVL8sK0ff_oJuwxBGjQgoHrgmvxV-qMziAH13Ad-2dqT6XNZdUKARX2dl_KPxa2HobRnAez48EH48EyMzwe-7MkpJe_7g-ZtmBtTGkFME95kGJvmuoPjRUY0P1vqGaoejd0yQfJQ-V5H8A-VnhgA</recordid><startdate>20211220</startdate><enddate>20211220</enddate><creator>Lu, Xiaojuan</creator><creator>Zhang, Zhipeng</creator><creator>Yuan, Dongqi</creator><creator>Zhou, Yongzhi</creator><creator>Cao, Jie</creator><creator>Zhang, Houshuang</creator><creator>da Silva Vaz, Jr, Itabajara</creator><creator>Zhou, Jinlin</creator><general>BioMed Central Ltd</general><general>BioMed Central</general><general>BMC</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>ISR</scope><scope>3V.</scope><scope>7SN</scope><scope>7SS</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BENPR</scope><scope>C1K</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>F1W</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>H95</scope><scope>K9.</scope><scope>L.G</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope><orcidid>https://orcid.org/0000-0002-3383-1084</orcidid></search><sort><creationdate>20211220</creationdate><title>The ecdysteroid receptor regulates salivary gland degeneration through apoptosis in Rhipicephalus haemaphysaloides</title><author>Lu, Xiaojuan ; Zhang, Zhipeng ; Yuan, Dongqi ; Zhou, Yongzhi ; Cao, Jie ; Zhang, Houshuang ; da Silva Vaz, Jr, Itabajara ; Zhou, Jinlin</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c597t-63518c7bfd99b553b35708a58b8e76f4b25f2210b222ee69e714895678f8f13b3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Animals</topic><topic>Antibodies</topic><topic>Apoptosis</topic><topic>Apoptosis - physiology</topic><topic>Arthropods</topic><topic>Body organs</topic><topic>Caspase</topic><topic>Cells</topic><topic>Cloning</topic><topic>Cloning, Molecular</topic><topic>Degeneration</topic><topic>E coli</topic><topic>Ecdysone</topic><topic>Ecdysone receptor</topic><topic>Ecdysteroid receptors</topic><topic>Ecdysteroids</topic><topic>Engorgement</topic><topic>Exocrine glands</topic><topic>Feeding Behavior</topic><topic>Female</topic><topic>Females</topic><topic>Gene expression</topic><topic>Gene Expression Regulation - physiology</topic><topic>Gene silencing</topic><topic>Genes</topic><topic>HEK293 Cells</topic><topic>Hormones</topic><topic>Humans</topic><topic>Identification</topic><topic>Insect hormones</topic><topic>Insects</topic><topic>Isoforms</topic><topic>Laboratories</topic><topic>Maximum likelihood method</topic><topic>Metabolism</topic><topic>Metabolites</topic><topic>Morphology</topic><topic>Nitrogen</topic><topic>Nucleotide sequence</topic><topic>Open Reading Frames</topic><topic>Organs</topic><topic>Ovaries</topic><topic>Parasitic diseases</topic><topic>Pathogens</topic><topic>PCR</topic><topic>Peptides</topic><topic>Physiological aspects</topic><topic>Polyclonal antibodies</topic><topic>Proteins</topic><topic>Proteomics</topic><topic>Receptor mechanisms</topic><topic>Receptors</topic><topic>Receptors, Steroid - genetics</topic><topic>Receptors, Steroid - metabolism</topic><topic>Recombinants</topic><topic>Reproduction</topic><topic>Rhipicephalus - metabolism</topic><topic>Rhipicephalus haemaphysaloides</topic><topic>RNA Interference</topic><topic>RNA, Double-Stranded</topic><topic>RNA-mediated interference</topic><topic>Salivary gland</topic><topic>Salivary gland degeneration</topic><topic>Salivary glands</topic><topic>Salivary Glands - physiology</topic><topic>Signal transduction</topic><topic>Software</topic><topic>Steroids</topic><topic>Synthetic peptides</topic><topic>Tick</topic><topic>Tick-borne diseases</topic><topic>Ticks</topic><topic>Transcriptomes</topic><topic>Ultraspiracle</topic><topic>Vectors</topic><topic>Vertebrates</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Lu, Xiaojuan</creatorcontrib><creatorcontrib>Zhang, Zhipeng</creatorcontrib><creatorcontrib>Yuan, Dongqi</creatorcontrib><creatorcontrib>Zhou, Yongzhi</creatorcontrib><creatorcontrib>Cao, Jie</creatorcontrib><creatorcontrib>Zhang, Houshuang</creatorcontrib><creatorcontrib>da Silva Vaz, Jr, Itabajara</creatorcontrib><creatorcontrib>Zhou, Jinlin</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Science (Gale in Context)</collection><collection>ProQuest Central (Corporate)</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Health &amp; 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vectors</jtitle><addtitle>Parasit Vectors</addtitle><date>2021-12-20</date><risdate>2021</risdate><volume>14</volume><issue>1</issue><spage>612</spage><epage>612</epage><pages>612-612</pages><artnum>612</artnum><issn>1756-3305</issn><eissn>1756-3305</eissn><abstract>It is well established that ecdysteroid hormones play an important role in arthropod development and reproduction, mediated by ecdysteroid receptors. Ticks are obligate hematophagous arthropods and vectors of pathogens. The salivary gland plays an essential role in tick growth and reproduction and in the transmission of pathogens to vertebrate hosts. During tick development, the salivary gland undergoes degeneration triggered by ecdysteroid hormones and activated by apoptosis. However, it is unknown how the ecdysteroid receptor and apoptosis regulate salivary gland degeneration. Here, we report the functional ecdysteroid receptor (a heterodimer of the ecdysone receptor [EcR] and ultraspiracle [USP]) isolated from the salivary gland of the tick Rhipicephalus haemaphysaloides and explore the molecular mechanism of ecdysteroid receptor regulation of salivary gland degeneration. The full length of RhEcR and RhUSP open reading frames (ORFs) was obtained from the transcriptome. The RhEcR and RhUSP proteins were expressed in a bacterial heterologous system, Escherichia coli. Polyclonal antibodies were produced against synthetic peptides and were able to recognize recombinant and native proteins. Quantitative real-time PCR and western blot were used to detect the distribution of RhEcR, RhUSP, and RhCaspases in the R. haemaphysaloides organs. A proteomics approach was used to analyze the expression profiles of the ecdysteroid receptors, RhCaspases, and other proteins. To analyze the function of the ecdysteroid receptor, RNA interference (RNAi) was used to silence the genes in adult female ticks. Finally, the interaction of RhEcR and RhUSP was identified by heterologous co-expression assays in HEK293T cells. We identified the functional ecdysone receptor (RhEcR/RhUSP) of 20-hydroxyecdysone from the salivary gland of the tick R. haemaphysaloides. The RhEcR and RhUSP genes have three and two isoforms, respectively, and belong to a nuclear receptor family but with variable N-terminal A/B domains. The RhEcR gene silencing inhibited blood-feeding, blocked engorgement, and restrained salivary gland degeneration, showing the biological role of the RhEcR gene in ticks. In the ecdysteroid signaling pathway, RhEcR silencing inhibited salivary gland degeneration by suppressing caspase-dependent apoptosis. The heterologous expression in mammalian HEK293T cells showed that RhEcR1 interacts with RhUSP1 and induces caspase-dependent apoptosis. These data show that RhEcR has an essential role in tick physiology and represents a putative target for the control of ticks and tick-borne diseases.</abstract><cop>England</cop><pub>BioMed Central Ltd</pub><pmid>34930413</pmid><doi>10.1186/s13071-021-05052-2</doi><tpages>1</tpages><orcidid>https://orcid.org/0000-0002-3383-1084</orcidid><oa>free_for_read</oa></addata></record>
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identifier ISSN: 1756-3305
ispartof Parasites & vectors, 2021-12, Vol.14 (1), p.612-612, Article 612
issn 1756-3305
1756-3305
language eng
recordid cdi_doaj_primary_oai_doaj_org_article_c1f5d8188e5f46bfbc8b12ed3468ca49
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subjects Animals
Antibodies
Apoptosis
Apoptosis - physiology
Arthropods
Body organs
Caspase
Cells
Cloning
Cloning, Molecular
Degeneration
E coli
Ecdysone
Ecdysone receptor
Ecdysteroid receptors
Ecdysteroids
Engorgement
Exocrine glands
Feeding Behavior
Female
Females
Gene expression
Gene Expression Regulation - physiology
Gene silencing
Genes
HEK293 Cells
Hormones
Humans
Identification
Insect hormones
Insects
Isoforms
Laboratories
Maximum likelihood method
Metabolism
Metabolites
Morphology
Nitrogen
Nucleotide sequence
Open Reading Frames
Organs
Ovaries
Parasitic diseases
Pathogens
PCR
Peptides
Physiological aspects
Polyclonal antibodies
Proteins
Proteomics
Receptor mechanisms
Receptors
Receptors, Steroid - genetics
Receptors, Steroid - metabolism
Recombinants
Reproduction
Rhipicephalus - metabolism
Rhipicephalus haemaphysaloides
RNA Interference
RNA, Double-Stranded
RNA-mediated interference
Salivary gland
Salivary gland degeneration
Salivary glands
Salivary Glands - physiology
Signal transduction
Software
Steroids
Synthetic peptides
Tick
Tick-borne diseases
Ticks
Transcriptomes
Ultraspiracle
Vectors
Vertebrates
title The ecdysteroid receptor regulates salivary gland degeneration through apoptosis in Rhipicephalus haemaphysaloides
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