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The genomes of four tapeworm species reveal adaptations to parasitism.

Identifieur interne : 000834 ( PubMed/Checkpoint ); précédent : 000833; suivant : 000835

The genomes of four tapeworm species reveal adaptations to parasitism.

Auteurs : Isheng J. Tsai [Royaume-Uni] ; Magdalena Zarowiecki ; Nancy Holroyd ; Alejandro Garciarrubio ; Alejandro Sanchez-Flores ; Karen L. Brooks ; Alan Tracey ; Raúl J. Bobes ; Gladis Fragoso ; Edda Sciutto ; Martin Aslett ; Helen Beasley ; Hayley M. Bennett ; Jianping Cai ; Federico Camicia ; Richard Clark ; Marcela Cucher ; Nishadi De Silva ; Tim A. Day ; Peter Deplazes ; Karel Estrada ; Cecilia Fernández ; Peter W H. Holland ; Junling Hou ; Songnian Hu ; Thomas Huckvale ; Stacy S. Hung ; Laura Kamenetzky ; Jacqueline A. Keane ; Ferenc Kiss ; Uriel Koziol ; Olivia Lambert ; Kan Liu ; Xuenong Luo ; Yingfeng Luo ; Natalia Macchiaroli ; Sarah Nichol ; Jordi Paps ; John Parkinson ; Natasha Pouchkina-Stantcheva ; Nick Riddiford ; Mara Rosenzvit ; Gustavo Salinas ; James D. Wasmuth ; Mostafa Zamanian ; Yadong Zheng ; Xuepeng Cai ; Xavier Sober N ; Peter D. Olson ; Juan P. Laclette ; Klaus Brehm ; Matthew Berriman

Source :

RBID : pubmed:23485966

English descriptors

Abstract

Tapeworms (Cestoda) cause neglected diseases that can be fatal and are difficult to treat, owing to inefficient drugs. Here we present an analysis of tapeworm genome sequences using the human-infective species Echinococcus multilocularis, E. granulosus, Taenia solium and the laboratory model Hymenolepis microstoma as examples. The 115- to 141-megabase genomes offer insights into the evolution of parasitism. Synteny is maintained with distantly related blood flukes but we find extreme losses of genes and pathways that are ubiquitous in other animals, including 34 homeobox families and several determinants of stem cell fate. Tapeworms have specialized detoxification pathways, metabolism that is finely tuned to rely on nutrients scavenged from their hosts, and species-specific expansions of non-canonical heat shock proteins and families of known antigens. We identify new potential drug targets, including some on which existing pharmaceuticals may act. The genomes provide a rich resource to underpin the development of urgently needed treatments and control.

DOI: 10.1038/nature12031
PubMed: 23485966


Affiliations:


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pubmed:23485966

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<name sortKey="De Silva, Nishadi" sort="De Silva, Nishadi" uniqKey="De Silva N" first="Nishadi" last="De Silva">Nishadi De Silva</name>
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<name sortKey="Estrada, Karel" sort="Estrada, Karel" uniqKey="Estrada K" first="Karel" last="Estrada">Karel Estrada</name>
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<name sortKey="Hung, Stacy S" sort="Hung, Stacy S" uniqKey="Hung S" first="Stacy S" last="Hung">Stacy S. Hung</name>
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<name sortKey="Lambert, Olivia" sort="Lambert, Olivia" uniqKey="Lambert O" first="Olivia" last="Lambert">Olivia Lambert</name>
</author>
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<name sortKey="Liu, Kan" sort="Liu, Kan" uniqKey="Liu K" first="Kan" last="Liu">Kan Liu</name>
</author>
<author>
<name sortKey="Luo, Xuenong" sort="Luo, Xuenong" uniqKey="Luo X" first="Xuenong" last="Luo">Xuenong Luo</name>
</author>
<author>
<name sortKey="Luo, Yingfeng" sort="Luo, Yingfeng" uniqKey="Luo Y" first="Yingfeng" last="Luo">Yingfeng Luo</name>
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<name sortKey="Macchiaroli, Natalia" sort="Macchiaroli, Natalia" uniqKey="Macchiaroli N" first="Natalia" last="Macchiaroli">Natalia Macchiaroli</name>
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<name sortKey="Nichol, Sarah" sort="Nichol, Sarah" uniqKey="Nichol S" first="Sarah" last="Nichol">Sarah Nichol</name>
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<name sortKey="Paps, Jordi" sort="Paps, Jordi" uniqKey="Paps J" first="Jordi" last="Paps">Jordi Paps</name>
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<name sortKey="Parkinson, John" sort="Parkinson, John" uniqKey="Parkinson J" first="John" last="Parkinson">John Parkinson</name>
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<name sortKey="Pouchkina Stantcheva, Natasha" sort="Pouchkina Stantcheva, Natasha" uniqKey="Pouchkina Stantcheva N" first="Natasha" last="Pouchkina-Stantcheva">Natasha Pouchkina-Stantcheva</name>
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<name sortKey="Riddiford, Nick" sort="Riddiford, Nick" uniqKey="Riddiford N" first="Nick" last="Riddiford">Nick Riddiford</name>
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<name sortKey="Rosenzvit, Mara" sort="Rosenzvit, Mara" uniqKey="Rosenzvit M" first="Mara" last="Rosenzvit">Mara Rosenzvit</name>
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<name sortKey="Salinas, Gustavo" sort="Salinas, Gustavo" uniqKey="Salinas G" first="Gustavo" last="Salinas">Gustavo Salinas</name>
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<name sortKey="Wasmuth, James D" sort="Wasmuth, James D" uniqKey="Wasmuth J" first="James D" last="Wasmuth">James D. Wasmuth</name>
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<name sortKey="Zamanian, Mostafa" sort="Zamanian, Mostafa" uniqKey="Zamanian M" first="Mostafa" last="Zamanian">Mostafa Zamanian</name>
</author>
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<name sortKey="Zheng, Yadong" sort="Zheng, Yadong" uniqKey="Zheng Y" first="Yadong" last="Zheng">Yadong Zheng</name>
</author>
<author>
<name sortKey="Cai, Xuepeng" sort="Cai, Xuepeng" uniqKey="Cai X" first="Xuepeng" last="Cai">Xuepeng Cai</name>
</author>
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<name sortKey="Sober N, Xavier" sort="Sober N, Xavier" uniqKey="Sober N X" first="Xavier" last="Sober N">Xavier Sober N</name>
</author>
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<name sortKey="Olson, Peter D" sort="Olson, Peter D" uniqKey="Olson P" first="Peter D" last="Olson">Peter D. Olson</name>
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<name sortKey="Laclette, Juan P" sort="Laclette, Juan P" uniqKey="Laclette J" first="Juan P" last="Laclette">Juan P. Laclette</name>
</author>
<author>
<name sortKey="Brehm, Klaus" sort="Brehm, Klaus" uniqKey="Brehm K" first="Klaus" last="Brehm">Klaus Brehm</name>
</author>
<author>
<name sortKey="Berriman, Matthew" sort="Berriman, Matthew" uniqKey="Berriman M" first="Matthew" last="Berriman">Matthew Berriman</name>
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<series>
<title level="j">Nature</title>
<idno type="eISSN">1476-4687</idno>
<imprint>
<date when="2013" type="published">2013</date>
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<keywords scheme="KwdEn" xml:lang="en">
<term>Adaptation, Physiological (genetics)</term>
<term>Animals</term>
<term>Biological Evolution</term>
<term>Cestoda (drug effects)</term>
<term>Cestoda (genetics)</term>
<term>Cestoda (physiology)</term>
<term>Cestode Infections (drug therapy)</term>
<term>Cestode Infections (metabolism)</term>
<term>Conserved Sequence (genetics)</term>
<term>Echinococcus granulosus (genetics)</term>
<term>Echinococcus multilocularis (drug effects)</term>
<term>Echinococcus multilocularis (genetics)</term>
<term>Echinococcus multilocularis (metabolism)</term>
<term>Genes, Helminth (genetics)</term>
<term>Genes, Homeobox (genetics)</term>
<term>Genome, Helminth (genetics)</term>
<term>HSP70 Heat-Shock Proteins (genetics)</term>
<term>Humans</term>
<term>Hymenolepis (genetics)</term>
<term>Metabolic Networks and Pathways (genetics)</term>
<term>Molecular Targeted Therapy</term>
<term>Parasites (drug effects)</term>
<term>Parasites (genetics)</term>
<term>Parasites (physiology)</term>
<term>Proteome (genetics)</term>
<term>Stem Cells (cytology)</term>
<term>Stem Cells (metabolism)</term>
<term>Taenia solium (genetics)</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="genetics" xml:lang="en">
<term>HSP70 Heat-Shock Proteins</term>
<term>Proteome</term>
</keywords>
<keywords scheme="MESH" qualifier="cytology" xml:lang="en">
<term>Stem Cells</term>
</keywords>
<keywords scheme="MESH" qualifier="drug effects" xml:lang="en">
<term>Cestoda</term>
<term>Echinococcus multilocularis</term>
<term>Parasites</term>
</keywords>
<keywords scheme="MESH" qualifier="drug therapy" xml:lang="en">
<term>Cestode Infections</term>
</keywords>
<keywords scheme="MESH" qualifier="genetics" xml:lang="en">
<term>Adaptation, Physiological</term>
<term>Cestoda</term>
<term>Conserved Sequence</term>
<term>Echinococcus granulosus</term>
<term>Echinococcus multilocularis</term>
<term>Genes, Helminth</term>
<term>Genes, Homeobox</term>
<term>Genome, Helminth</term>
<term>Hymenolepis</term>
<term>Metabolic Networks and Pathways</term>
<term>Parasites</term>
<term>Taenia solium</term>
</keywords>
<keywords scheme="MESH" qualifier="metabolism" xml:lang="en">
<term>Cestode Infections</term>
<term>Echinococcus multilocularis</term>
<term>Stem Cells</term>
</keywords>
<keywords scheme="MESH" qualifier="physiology" xml:lang="en">
<term>Cestoda</term>
<term>Parasites</term>
</keywords>
<keywords scheme="MESH" xml:lang="en">
<term>Animals</term>
<term>Biological Evolution</term>
<term>Humans</term>
<term>Molecular Targeted Therapy</term>
</keywords>
</textClass>
</profileDesc>
</teiHeader>
<front>
<div type="abstract" xml:lang="en">Tapeworms (Cestoda) cause neglected diseases that can be fatal and are difficult to treat, owing to inefficient drugs. Here we present an analysis of tapeworm genome sequences using the human-infective species Echinococcus multilocularis, E. granulosus, Taenia solium and the laboratory model Hymenolepis microstoma as examples. The 115- to 141-megabase genomes offer insights into the evolution of parasitism. Synteny is maintained with distantly related blood flukes but we find extreme losses of genes and pathways that are ubiquitous in other animals, including 34 homeobox families and several determinants of stem cell fate. Tapeworms have specialized detoxification pathways, metabolism that is finely tuned to rely on nutrients scavenged from their hosts, and species-specific expansions of non-canonical heat shock proteins and families of known antigens. We identify new potential drug targets, including some on which existing pharmaceuticals may act. The genomes provide a rich resource to underpin the development of urgently needed treatments and control.</div>
</front>
</TEI>
<pubmed>
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<PMID Version="1">23485966</PMID>
<DateCreated>
<Year>2013</Year>
<Month>04</Month>
<Day>04</Day>
</DateCreated>
<DateCompleted>
<Year>2013</Year>
<Month>05</Month>
<Day>01</Day>
</DateCompleted>
<DateRevised>
<Year>2017</Year>
<Month>02</Month>
<Day>20</Day>
</DateRevised>
<Article PubModel="Print-Electronic">
<Journal>
<ISSN IssnType="Electronic">1476-4687</ISSN>
<JournalIssue CitedMedium="Internet">
<Volume>496</Volume>
<Issue>7443</Issue>
<PubDate>
<Year>2013</Year>
<Month>Apr</Month>
<Day>04</Day>
</PubDate>
</JournalIssue>
<Title>Nature</Title>
<ISOAbbreviation>Nature</ISOAbbreviation>
</Journal>
<ArticleTitle>The genomes of four tapeworm species reveal adaptations to parasitism.</ArticleTitle>
<Pagination>
<MedlinePgn>57-63</MedlinePgn>
</Pagination>
<ELocationID EIdType="doi" ValidYN="Y">10.1038/nature12031</ELocationID>
<Abstract>
<AbstractText>Tapeworms (Cestoda) cause neglected diseases that can be fatal and are difficult to treat, owing to inefficient drugs. Here we present an analysis of tapeworm genome sequences using the human-infective species Echinococcus multilocularis, E. granulosus, Taenia solium and the laboratory model Hymenolepis microstoma as examples. The 115- to 141-megabase genomes offer insights into the evolution of parasitism. Synteny is maintained with distantly related blood flukes but we find extreme losses of genes and pathways that are ubiquitous in other animals, including 34 homeobox families and several determinants of stem cell fate. Tapeworms have specialized detoxification pathways, metabolism that is finely tuned to rely on nutrients scavenged from their hosts, and species-specific expansions of non-canonical heat shock proteins and families of known antigens. We identify new potential drug targets, including some on which existing pharmaceuticals may act. The genomes provide a rich resource to underpin the development of urgently needed treatments and control.</AbstractText>
</Abstract>
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<Author ValidYN="Y">
<LastName>Tsai</LastName>
<ForeName>Isheng J</ForeName>
<Initials>IJ</Initials>
<AffiliationInfo>
<Affiliation>Parasite Genomics, Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge CB10 1SA, UK.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Zarowiecki</LastName>
<ForeName>Magdalena</ForeName>
<Initials>M</Initials>
</Author>
<Author ValidYN="Y">
<LastName>Holroyd</LastName>
<ForeName>Nancy</ForeName>
<Initials>N</Initials>
</Author>
<Author ValidYN="Y">
<LastName>Garciarrubio</LastName>
<ForeName>Alejandro</ForeName>
<Initials>A</Initials>
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<Author ValidYN="Y">
<LastName>Sanchez-Flores</LastName>
<ForeName>Alejandro</ForeName>
<Initials>A</Initials>
</Author>
<Author ValidYN="Y">
<LastName>Brooks</LastName>
<ForeName>Karen L</ForeName>
<Initials>KL</Initials>
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<Author ValidYN="Y">
<LastName>Tracey</LastName>
<ForeName>Alan</ForeName>
<Initials>A</Initials>
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<LastName>Bobes</LastName>
<ForeName>Raúl J</ForeName>
<Initials>RJ</Initials>
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<LastName>Fragoso</LastName>
<ForeName>Gladis</ForeName>
<Initials>G</Initials>
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<LastName>Sciutto</LastName>
<ForeName>Edda</ForeName>
<Initials>E</Initials>
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<LastName>Aslett</LastName>
<ForeName>Martin</ForeName>
<Initials>M</Initials>
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<ForeName>Helen</ForeName>
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<ForeName>Hayley M</ForeName>
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<LastName>Cai</LastName>
<ForeName>Jianping</ForeName>
<Initials>J</Initials>
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<LastName>Camicia</LastName>
<ForeName>Federico</ForeName>
<Initials>F</Initials>
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<LastName>Clark</LastName>
<ForeName>Richard</ForeName>
<Initials>R</Initials>
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<LastName>Cucher</LastName>
<ForeName>Marcela</ForeName>
<Initials>M</Initials>
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<Author ValidYN="Y">
<LastName>De Silva</LastName>
<ForeName>Nishadi</ForeName>
<Initials>N</Initials>
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<Author ValidYN="Y">
<LastName>Day</LastName>
<ForeName>Tim A</ForeName>
<Initials>TA</Initials>
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<LastName>Deplazes</LastName>
<ForeName>Peter</ForeName>
<Initials>P</Initials>
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<LastName>Estrada</LastName>
<ForeName>Karel</ForeName>
<Initials>K</Initials>
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<Author ValidYN="Y">
<LastName>Fernández</LastName>
<ForeName>Cecilia</ForeName>
<Initials>C</Initials>
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<Author ValidYN="Y">
<LastName>Holland</LastName>
<ForeName>Peter W H</ForeName>
<Initials>PW</Initials>
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<Author ValidYN="Y">
<LastName>Hou</LastName>
<ForeName>Junling</ForeName>
<Initials>J</Initials>
</Author>
<Author ValidYN="Y">
<LastName>Hu</LastName>
<ForeName>Songnian</ForeName>
<Initials>S</Initials>
</Author>
<Author ValidYN="Y">
<LastName>Huckvale</LastName>
<ForeName>Thomas</ForeName>
<Initials>T</Initials>
</Author>
<Author ValidYN="Y">
<LastName>Hung</LastName>
<ForeName>Stacy S</ForeName>
<Initials>SS</Initials>
</Author>
<Author ValidYN="Y">
<LastName>Kamenetzky</LastName>
<ForeName>Laura</ForeName>
<Initials>L</Initials>
</Author>
<Author ValidYN="Y">
<LastName>Keane</LastName>
<ForeName>Jacqueline A</ForeName>
<Initials>JA</Initials>
</Author>
<Author ValidYN="Y">
<LastName>Kiss</LastName>
<ForeName>Ferenc</ForeName>
<Initials>F</Initials>
</Author>
<Author ValidYN="Y">
<LastName>Koziol</LastName>
<ForeName>Uriel</ForeName>
<Initials>U</Initials>
</Author>
<Author ValidYN="Y">
<LastName>Lambert</LastName>
<ForeName>Olivia</ForeName>
<Initials>O</Initials>
</Author>
<Author ValidYN="Y">
<LastName>Liu</LastName>
<ForeName>Kan</ForeName>
<Initials>K</Initials>
</Author>
<Author ValidYN="Y">
<LastName>Luo</LastName>
<ForeName>Xuenong</ForeName>
<Initials>X</Initials>
</Author>
<Author ValidYN="Y">
<LastName>Luo</LastName>
<ForeName>Yingfeng</ForeName>
<Initials>Y</Initials>
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<Author ValidYN="Y">
<LastName>Macchiaroli</LastName>
<ForeName>Natalia</ForeName>
<Initials>N</Initials>
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<Author ValidYN="Y">
<LastName>Nichol</LastName>
<ForeName>Sarah</ForeName>
<Initials>S</Initials>
</Author>
<Author ValidYN="Y">
<LastName>Paps</LastName>
<ForeName>Jordi</ForeName>
<Initials>J</Initials>
</Author>
<Author ValidYN="Y">
<LastName>Parkinson</LastName>
<ForeName>John</ForeName>
<Initials>J</Initials>
</Author>
<Author ValidYN="Y">
<LastName>Pouchkina-Stantcheva</LastName>
<ForeName>Natasha</ForeName>
<Initials>N</Initials>
</Author>
<Author ValidYN="Y">
<LastName>Riddiford</LastName>
<ForeName>Nick</ForeName>
<Initials>N</Initials>
</Author>
<Author ValidYN="Y">
<LastName>Rosenzvit</LastName>
<ForeName>Mara</ForeName>
<Initials>M</Initials>
</Author>
<Author ValidYN="Y">
<LastName>Salinas</LastName>
<ForeName>Gustavo</ForeName>
<Initials>G</Initials>
</Author>
<Author ValidYN="Y">
<LastName>Wasmuth</LastName>
<ForeName>James D</ForeName>
<Initials>JD</Initials>
</Author>
<Author ValidYN="Y">
<LastName>Zamanian</LastName>
<ForeName>Mostafa</ForeName>
<Initials>M</Initials>
</Author>
<Author ValidYN="Y">
<LastName>Zheng</LastName>
<ForeName>Yadong</ForeName>
<Initials>Y</Initials>
</Author>
<Author ValidYN="Y">
<CollectiveName>Taenia solium Genome Consortium</CollectiveName>
</Author>
<Author ValidYN="Y">
<LastName>Cai</LastName>
<ForeName>Xuepeng</ForeName>
<Initials>X</Initials>
</Author>
<Author ValidYN="Y">
<LastName>Soberón</LastName>
<ForeName>Xavier</ForeName>
<Initials>X</Initials>
</Author>
<Author ValidYN="Y">
<LastName>Olson</LastName>
<ForeName>Peter D</ForeName>
<Initials>PD</Initials>
</Author>
<Author ValidYN="Y">
<LastName>Laclette</LastName>
<ForeName>Juan P</ForeName>
<Initials>JP</Initials>
</Author>
<Author ValidYN="Y">
<LastName>Brehm</LastName>
<ForeName>Klaus</ForeName>
<Initials>K</Initials>
</Author>
<Author ValidYN="Y">
<LastName>Berriman</LastName>
<ForeName>Matthew</ForeName>
<Initials>M</Initials>
</Author>
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<Language>eng</Language>
<GrantList CompleteYN="Y">
<Grant>
<GrantID>BBG0038151</GrantID>
<Agency>Biotechnology and Biological Sciences Research Council</Agency>
<Country>United Kingdom</Country>
</Grant>
<Grant>
<GrantID>085775</GrantID>
<Agency>Wellcome Trust</Agency>
<Country>United Kingdom</Country>
</Grant>
<Grant>
<GrantID>098051</GrantID>
<Agency>Wellcome Trust</Agency>
<Country>United Kingdom</Country>
</Grant>
<Grant>
<GrantID>MOP#84556</GrantID>
<Agency>Canadian Institutes of Health Research</Agency>
<Country>Canada</Country>
</Grant>
<Grant>
<GrantID>BB/G003815/1</GrantID>
<Agency>Biotechnology and Biological Sciences Research Council</Agency>
<Country>United Kingdom</Country>
</Grant>
<Grant>
<GrantID>TW008588</GrantID>
<Acronym>TW</Acronym>
<Agency>FIC NIH HHS</Agency>
<Country>United States</Country>
</Grant>
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<Year>2013</Year>
<Month>03</Month>
<Day>13</Day>
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<Country>England</Country>
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<RegistryNumber>0</RegistryNumber>
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<Chemical>
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<NameOfSubstance UI="D020543">Proteome</NameOfSubstance>
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<MeshHeadingList>
<MeshHeading>
<DescriptorName UI="D000222" MajorTopicYN="N">Adaptation, Physiological</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="Y">genetics</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D000818" MajorTopicYN="N">Animals</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D005075" MajorTopicYN="N">Biological Evolution</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D002589" MajorTopicYN="N">Cestoda</DescriptorName>
<QualifierName UI="Q000187" MajorTopicYN="N">drug effects</QualifierName>
<QualifierName UI="Q000235" MajorTopicYN="Y">genetics</QualifierName>
<QualifierName UI="Q000502" MajorTopicYN="N">physiology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D002590" MajorTopicYN="N">Cestode Infections</DescriptorName>
<QualifierName UI="Q000188" MajorTopicYN="N">drug therapy</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D017124" MajorTopicYN="N">Conserved Sequence</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D048209" MajorTopicYN="N">Echinococcus granulosus</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
</MeshHeading>
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