Dual RNA-seq of Parasite and Host Reveals Gene Expression Dynamics during Filarial Worm–Mosquito Interactions
Identifieur interne : 001C10 ( Pmc/Checkpoint ); précédent : 001C09; suivant : 001C11Dual RNA-seq of Parasite and Host Reveals Gene Expression Dynamics during Filarial Worm–Mosquito Interactions
Auteurs : Young-Jun Choi ; Matthew T. Aliota ; George F. Mayhew ; Sara M. Erickson ; Bruce M. ChristensenSource :
- PLoS Neglected Tropical Diseases [ 1935-2727 ] ; 2014.
Abstract
Parasite biology, by its very nature, cannot be understood without integrating it with that of the host, nor can the host response be adequately explained without considering the activity of the parasite. However, due to experimental limitations, molecular studies of parasite-host systems have been predominantly one-sided investigations focusing on either of the partners involved. Here, we conducted a dual RNA-seq time course analysis of filarial worm parasite and host mosquito to better understand the parasite processes underlying development in and interaction with the host tissue, from the establishment of infection to the development of infective-stage larva.
Using the
The data presented herein provide the research community with information to design wet lab experiments and select candidates for future study to more fully dissect the whole set of molecular interactions of both organisms in this mosquito-filarial worm symbiotic relationship. Furthermore, characterization of the transcriptional program over the complete life cycle of the parasite, including stages within the mosquito, could help devise novel targets for control strategies.
Url:
DOI: 10.1371/journal.pntd.0002905
PubMed: 24853112
PubMed Central: 4031193
Affiliations:
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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Dual RNA-seq of Parasite and Host Reveals Gene Expression Dynamics during Filarial Worm–Mosquito Interactions</title><author><name sortKey="Choi, Young Jun" sort="Choi, Young Jun" uniqKey="Choi Y" first="Young-Jun" last="Choi">Young-Jun Choi</name><affiliation><nlm:aff id="aff1"></nlm:aff></affiliation></author><author><name sortKey="Aliota, Matthew T" sort="Aliota, Matthew T" uniqKey="Aliota M" first="Matthew T." last="Aliota">Matthew T. Aliota</name><affiliation><nlm:aff id="aff1"></nlm:aff></affiliation></author><author><name sortKey="Mayhew, George F" sort="Mayhew, George F" uniqKey="Mayhew G" first="George F." last="Mayhew">George F. Mayhew</name><affiliation><nlm:aff id="aff1"></nlm:aff></affiliation></author><author><name sortKey="Erickson, Sara M" sort="Erickson, Sara M" uniqKey="Erickson S" first="Sara M." last="Erickson">Sara M. Erickson</name><affiliation><nlm:aff id="aff1"></nlm:aff></affiliation></author><author><name sortKey="Christensen, Bruce M" sort="Christensen, Bruce M" uniqKey="Christensen B" first="Bruce M." last="Christensen">Bruce M. Christensen</name><affiliation><nlm:aff id="aff1"></nlm:aff></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">24853112</idno><idno type="pmc">4031193</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4031193</idno><idno type="RBID">PMC:4031193</idno><idno type="doi">10.1371/journal.pntd.0002905</idno><date when="2014">2014</date><idno type="wicri:Area/Pmc/Corpus">004357</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">004357</idno><idno type="wicri:Area/Pmc/Curation">004356</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Curation">004356</idno><idno type="wicri:Area/Pmc/Checkpoint">001C10</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Checkpoint">001C10</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Dual RNA-seq of Parasite and Host Reveals Gene Expression Dynamics during Filarial Worm–Mosquito Interactions</title><author><name sortKey="Choi, Young Jun" sort="Choi, Young Jun" uniqKey="Choi Y" first="Young-Jun" last="Choi">Young-Jun Choi</name><affiliation><nlm:aff id="aff1"></nlm:aff></affiliation></author><author><name sortKey="Aliota, Matthew T" sort="Aliota, Matthew T" uniqKey="Aliota M" first="Matthew T." last="Aliota">Matthew T. Aliota</name><affiliation><nlm:aff id="aff1"></nlm:aff></affiliation></author><author><name sortKey="Mayhew, George F" sort="Mayhew, George F" uniqKey="Mayhew G" first="George F." last="Mayhew">George F. Mayhew</name><affiliation><nlm:aff id="aff1"></nlm:aff></affiliation></author><author><name sortKey="Erickson, Sara M" sort="Erickson, Sara M" uniqKey="Erickson S" first="Sara M." last="Erickson">Sara M. Erickson</name><affiliation><nlm:aff id="aff1"></nlm:aff></affiliation></author><author><name sortKey="Christensen, Bruce M" sort="Christensen, Bruce M" uniqKey="Christensen B" first="Bruce M." last="Christensen">Bruce M. Christensen</name><affiliation><nlm:aff id="aff1"></nlm:aff></affiliation></author></analytic><series><title level="j">PLoS Neglected Tropical Diseases</title><idno type="ISSN">1935-2727</idno><idno type="eISSN">1935-2735</idno><imprint><date when="2014">2014</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><sec><title>Background</title><p>Parasite biology, by its very nature, cannot be understood without integrating it with that of the host, nor can the host response be adequately explained without considering the activity of the parasite. However, due to experimental limitations, molecular studies of parasite-host systems have been predominantly one-sided investigations focusing on either of the partners involved. Here, we conducted a dual RNA-seq time course analysis of filarial worm parasite and host mosquito to better understand the parasite processes underlying development in and interaction with the host tissue, from the establishment of infection to the development of infective-stage larva.</p></sec><sec><title>Methodology/Principal Findings</title><p>Using the <italic>Brugia malayi</italic>–<italic>Aedes aegypti</italic> system, we report parasite gene transcription dynamics, which exhibited a highly ordered developmental program consisting of a series of cyclical and state-transitioning temporal patterns. In addition, we contextualized these parasite data in relation to the concurrent dynamics of the host transcriptome. Comparative analyses using uninfected tissues and different host strains revealed the influence of parasite development on host gene transcription as well as the influence of the host environment on parasite gene transcription. We also critically evaluated the life-cycle transcriptome of <italic>B. malayi</italic> by comparing developmental stages in the mosquito relative to those in the mammalian host, providing insight into gene expression changes underpinning the mosquito-borne parasitic lifestyle of this heteroxenous parasite.</p></sec><sec><title>Conclusions/Significance</title><p>The data presented herein provide the research community with information to design wet lab experiments and select candidates for future study to more fully dissect the whole set of molecular interactions of both organisms in this mosquito-filarial worm symbiotic relationship. 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uniqKey="Mayhew G">GF Mayhew</name></author><author><name sortKey="Zink, Rl" uniqKey="Zink R">RL Zink</name></author><author><name sortKey="Erickson, Sm" uniqKey="Erickson S">SM Erickson</name></author><author><name sortKey="Fuchs, Jf" uniqKey="Fuchs J">JF Fuchs</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Li, B W" uniqKey="Li B">B-W Li</name></author><author><name sortKey="Rush, Ac" uniqKey="Rush A">AC Rush</name></author><author><name sortKey="Jiang, D J" uniqKey="Jiang D">D-J Jiang</name></author><author><name sortKey="Mitreva, M" uniqKey="Mitreva M">M Mitreva</name></author><author><name sortKey="Abubucker, S" uniqKey="Abubucker S">S Abubucker</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Li, B W" uniqKey="Li B">B-W Li</name></author><author><name sortKey="Wang, Z" uniqKey="Wang Z">Z Wang</name></author><author><name sortKey="Rush, Ac" uniqKey="Rush A">AC Rush</name></author><author><name sortKey="Mitreva, 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<front><journal-meta><journal-id journal-id-type="nlm-ta">PLoS Negl Trop Dis</journal-id><journal-id journal-id-type="iso-abbrev">PLoS Negl Trop Dis</journal-id><journal-id journal-id-type="publisher-id">plos</journal-id><journal-id journal-id-type="pmc">plosntds</journal-id><journal-title-group><journal-title>PLoS Neglected Tropical Diseases</journal-title></journal-title-group><issn pub-type="ppub">1935-2727</issn><issn pub-type="epub">1935-2735</issn><publisher><publisher-name>Public Library of Science</publisher-name><publisher-loc>San Francisco, USA</publisher-loc></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">24853112</article-id><article-id pub-id-type="pmc">4031193</article-id><article-id pub-id-type="publisher-id">PNTD-D-14-00034</article-id><article-id pub-id-type="doi">10.1371/journal.pntd.0002905</article-id><article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject></subj-group><subj-group subj-group-type="Discipline-v2"><subject>Medicine and Health Sciences</subject><subj-group><subject>Pathology and Laboratory Medicine</subject><subj-group><subject>Pathogenesis</subject><subj-group><subject>Host-Pathogen Interactions</subject></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v2"><subject>Biology and Life Sciences</subject><subj-group><subject>Computational Biology</subject><subj-group><subject>Genome Analysis</subject><subj-group><subject>Transcriptome Analysis</subject><subj-group><subject>Genome Expression Analysis</subject></subj-group></subj-group></subj-group></subj-group><subj-group><subject>Genetics</subject><subj-group><subject>Genomics</subject></subj-group></subj-group><subj-group><subject>Microbiology</subject></subj-group><subj-group><subject>Parasitology</subject></subj-group><subj-group><subject>Zoology</subject><subj-group><subject>Entomology</subject><subject>Helminthology</subject></subj-group></subj-group></subj-group></article-categories><title-group><article-title>Dual RNA-seq of Parasite and Host Reveals Gene Expression Dynamics during Filarial Worm–Mosquito Interactions</article-title><alt-title alt-title-type="running-head">RNA-seq of Mosquito–Filarial Worm Interactions</alt-title></title-group><contrib-group><contrib contrib-type="author" equal-contrib="yes"><name><surname>Choi</surname><given-names>Young-Jun</given-names></name><xref ref-type="aff" rid="aff1"></xref><xref ref-type="author-notes" rid="fn1"><sup>¤a</sup></xref></contrib><contrib contrib-type="author" equal-contrib="yes"><name><surname>Aliota</surname><given-names>Matthew T.</given-names></name><xref ref-type="aff" rid="aff1"></xref></contrib><contrib contrib-type="author"><name><surname>Mayhew</surname><given-names>George F.</given-names></name><xref ref-type="aff" rid="aff1"></xref><xref ref-type="author-notes" rid="fn2"><sup>¤b</sup></xref></contrib><contrib contrib-type="author"><name><surname>Erickson</surname><given-names>Sara M.</given-names></name><xref ref-type="aff" rid="aff1"></xref><xref ref-type="author-notes" rid="fn3"><sup>¤c</sup></xref></contrib><contrib contrib-type="author"><name><surname>Christensen</surname><given-names>Bruce M.</given-names></name><xref ref-type="aff" rid="aff1"></xref><xref ref-type="corresp" rid="cor1"><sup>*</sup></xref></contrib></contrib-group><aff id="aff1"><addr-line>Department of Pathobiological Sciences, University of Wisconsin-Madison, Madison, Wisconsin, United States of America</addr-line></aff><contrib-group><contrib contrib-type="editor"><name><surname>Cantacessi</surname><given-names>Cinzia</given-names></name><role>Editor</role><xref ref-type="aff" rid="edit1"></xref></contrib></contrib-group><aff id="edit1"><addr-line>James Cook University, Australia</addr-line></aff><author-notes><corresp id="cor1">* E-mail: <email>christensen@svm.vetmed.wisc.edu</email></corresp><fn fn-type="conflict"><p>The authors have declared that no competing interests exist.</p></fn><fn fn-type="con"><p>Conceived and designed the experiments: YJC MTA GFM SME BMC. Performed the experiments: YJC MTA SME. Analyzed the data: YJC MTA GFM BMC. Contributed reagents/materials/analysis tools: BMC. Wrote the paper: YJC MTA GFM BMC.</p></fn><fn id="fn1" fn-type="current-aff"><label>¤a</label><p>Current address: The Genome Institute, Washington University, St. Louis, Missouri, United States of America</p></fn><fn id="fn2" fn-type="current-aff"><label>¤b</label><p>Current address: Roche-Nimblegen Inc., Madison, Wisconsin, United States of America</p></fn><fn id="fn3" fn-type="current-aff"><label>¤c</label><p>Current address: Division of Infection and Immunity, The Walter and Eliza Hall Institute of Medical Research, Parkville, Victoria, Australia</p></fn></author-notes><pub-date pub-type="collection"><month>5</month><year>2014</year></pub-date><pub-date pub-type="epub"><day>22</day><month>5</month><year>2014</year></pub-date><volume>8</volume><issue>5</issue><elocation-id>e2905</elocation-id><history><date date-type="received"><day>8</day><month>1</month><year>2014</year></date><date date-type="accepted"><day>14</day><month>4</month><year>2014</year></date></history><permissions><copyright-year>2014</copyright-year><copyright-holder>Choi et al</copyright-holder><license><license-p>This is an open-access article distributed under the terms of the <ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0/">Creative Commons Attribution License</ext-link>, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.</license-p></license></permissions><abstract><sec><title>Background</title><p>Parasite biology, by its very nature, cannot be understood without integrating it with that of the host, nor can the host response be adequately explained without considering the activity of the parasite. However, due to experimental limitations, molecular studies of parasite-host systems have been predominantly one-sided investigations focusing on either of the partners involved. Here, we conducted a dual RNA-seq time course analysis of filarial worm parasite and host mosquito to better understand the parasite processes underlying development in and interaction with the host tissue, from the establishment of infection to the development of infective-stage larva.</p></sec><sec><title>Methodology/Principal Findings</title><p>Using the <italic>Brugia malayi</italic>–<italic>Aedes aegypti</italic> system, we report parasite gene transcription dynamics, which exhibited a highly ordered developmental program consisting of a series of cyclical and state-transitioning temporal patterns. In addition, we contextualized these parasite data in relation to the concurrent dynamics of the host transcriptome. Comparative analyses using uninfected tissues and different host strains revealed the influence of parasite development on host gene transcription as well as the influence of the host environment on parasite gene transcription. We also critically evaluated the life-cycle transcriptome of <italic>B. malayi</italic> by comparing developmental stages in the mosquito relative to those in the mammalian host, providing insight into gene expression changes underpinning the mosquito-borne parasitic lifestyle of this heteroxenous parasite.</p></sec><sec><title>Conclusions/Significance</title><p>The data presented herein provide the research community with information to design wet lab experiments and select candidates for future study to more fully dissect the whole set of molecular interactions of both organisms in this mosquito-filarial worm symbiotic relationship. Furthermore, characterization of the transcriptional program over the complete life cycle of the parasite, including stages within the mosquito, could help devise novel targets for control strategies.</p></sec></abstract><abstract abstract-type="summary"><title>Author Summary</title><p>In a parasitic relationship, both host and parasite genotypes influence the parameters of their relationship. Previous studies examining host-parasite systems have examined the effects of the genotype of the host or the parasite on the relationship, but due to limitations of technology, have rarely examined interactions between the two genotypes. Here, we utilized a dual RNA sequencing (RNA-seq) approach to examine the entirety of the known transcriptomes and their interactions in the dynamic process of filarial worm development in the mosquito. In addition, the unprecedented sequencing depth achieved with this technology allowed us to compare, for the first time, parasite gene expression of larval developmental stages within the intermediate host with those life cycle stages found within the mammalian definitive host. These data provide a strong foundation for understanding how <italic>Brugia malayi</italic> interacts with its vector's transcriptome temporally during its complex life cycle and also simultaneously provides information on how <italic>Aedes aegypti</italic> responds to filarial worm infection. These data are extremely valuable for future studies of the underlying mechanisms of this mosquito-filarial worm relationship.</p></abstract><funding-group><funding-statement>Financial support for this study was provided by National Institutes of Health (NIH) grant # AI019769. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.</funding-statement></funding-group><counts><page-count count="13"></page-count></counts></article-meta></front></pmc><affiliations><list></list><tree><noCountry><name sortKey="Aliota, Matthew T" sort="Aliota, Matthew T" uniqKey="Aliota M" first="Matthew T." last="Aliota">Matthew T. Aliota</name><name sortKey="Choi, Young Jun" sort="Choi, Young Jun" uniqKey="Choi Y" first="Young-Jun" last="Choi">Young-Jun Choi</name><name sortKey="Christensen, Bruce M" sort="Christensen, Bruce M" uniqKey="Christensen B" first="Bruce M." last="Christensen">Bruce M. Christensen</name><name sortKey="Erickson, Sara M" sort="Erickson, Sara M" uniqKey="Erickson S" first="Sara M." last="Erickson">Sara M. Erickson</name><name sortKey="Mayhew, George F" sort="Mayhew, George F" uniqKey="Mayhew G" first="George F." last="Mayhew">George F. 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