The genomes of four tapeworm species reveal adaptations to parasitism

Isheng J Tsai; 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 Soberón; Peter D Olson; Juan P Laclette; Taenia solium Genome Consortium

doi:10.1038/nature12031

The genomes of four tapeworm species reveal adaptations to parasitism

Isheng J Tsai, 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 DeplazesKarel 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 Soberón, Peter D Olson, Juan P Laclette, Taenia solium Genome Consortium

Research output: Contribution to journal › Article › peer-review

562 Citations (Scopus)

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.

Original language	English
Pages (from-to)	57-63
Number of pages	7
Journal	NATURE
Volume	496
Issue number	7443
DOIs	https://doi.org/10.1038/nature12031
Publication status	Published - 4 Apr 2013

Keywords

Adaptation, Physiological
Animals
Biological Evolution
Cestoda
Cestode Infections
Conserved Sequence
Echinococcus granulosus
Echinococcus multilocularis
Genes, Helminth
Genes, Homeobox
Genome, Helminth
HSP70 Heat-Shock Proteins
Humans
Hymenolepis
Metabolic Networks and Pathways
Molecular Targeted Therapy
Parasites
Proteome
Stem Cells
Taenia solium

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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10.1038/nature12031Licence: CC BY-NC-SA

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Tsai, I. J., Zarowiecki, M., Holroyd, N., Garciarrubio, A., Sanchez-Flores, A., Brooks, K. L., Tracey, A., Bobes, R. J., Fragoso, G., Sciutto, E., Aslett, M., Beasley, H., Bennett, H. M., Cai, J., Camicia, F., Clark, R., Cucher, M., De Silva, N., Day, T. A., ... Taenia solium Genome Consortium (2013). The genomes of four tapeworm species reveal adaptations to parasitism. NATURE, 496(7443), 57-63. https://doi.org/10.1038/nature12031

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title = "The genomes of four tapeworm species reveal adaptations to parasitism",

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.",

keywords = "Adaptation, Physiological, Animals, Biological Evolution, Cestoda, Cestode Infections, Conserved Sequence, Echinococcus granulosus, Echinococcus multilocularis, Genes, Helminth, Genes, Homeobox, Genome, Helminth, HSP70 Heat-Shock Proteins, Humans, Hymenolepis, Metabolic Networks and Pathways, Molecular Targeted Therapy, Parasites, Proteome, Stem Cells, Taenia solium",

author = "Tsai, {Isheng J} and Magdalena Zarowiecki and Nancy Holroyd and Alejandro Garciarrubio and Alejandro Sanchez-Flores and Brooks, {Karen L} and Alan Tracey and Bobes, {Ra{\'u}l J} and Gladis Fragoso and Edda Sciutto and Martin Aslett and Helen Beasley and Bennett, {Hayley M} and Jianping Cai and Federico Camicia and Richard Clark and Marcela Cucher and {De Silva}, Nishadi and Day, {Tim A} and Peter Deplazes and Karel Estrada and Cecilia Fern{\'a}ndez and Holland, {Peter W H} and Junling Hou and Songnian Hu and Thomas Huckvale and Hung, {Stacy S} and Laura Kamenetzky and Keane, {Jacqueline A} and Ferenc Kiss and Uriel Koziol and Olivia Lambert and Kan Liu and Xuenong Luo and Yingfeng Luo and Natalia Macchiaroli and Sarah Nichol and Jordi Paps and John Parkinson and Natasha Pouchkina-Stantcheva and Nick Riddiford and Mara Rosenzvit and Gustavo Salinas and Wasmuth, {James D} and Mostafa Zamanian and Yadong Zheng and Xuepeng Cai and Xavier Sober{\'o}n and Olson, {Peter D} and Laclette, {Juan P} and {Taenia solium Genome Consortium}",

year = "2013",

month = apr,

day = "4",

doi = "10.1038/nature12031",

language = "English",

volume = "496",

pages = "57--63",

journal = "NATURE",

issn = "0028-0836",

publisher = "Nature Publishing Group",

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Tsai, IJ, Zarowiecki, M, Holroyd, N, Garciarrubio, A, Sanchez-Flores, A, Brooks, KL, Tracey, A, Bobes, RJ, Fragoso, G, Sciutto, E, Aslett, M, Beasley, H, Bennett, HM, Cai, J, Camicia, F, Clark, R, Cucher, M, De Silva, N, Day, TA, Deplazes, P, Estrada, K, Fernández, C, Holland, PWH, Hou, J, Hu, S, Huckvale, T, Hung, SS, Kamenetzky, L, Keane, JA, Kiss, F, Koziol, U, Lambert, O, Liu, K, Luo, X, Luo, Y, Macchiaroli, N, Nichol, S, Paps, J, Parkinson, J, Pouchkina-Stantcheva, N, Riddiford, N, Rosenzvit, M, Salinas, G, Wasmuth, JD, Zamanian, M, Zheng, Y, Cai, X, Soberón, X, Olson, PD, Laclette, JP & Taenia solium Genome Consortium 2013, 'The genomes of four tapeworm species reveal adaptations to parasitism', NATURE, vol. 496, no. 7443, pp. 57-63. https://doi.org/10.1038/nature12031

TY - JOUR

T1 - The genomes of four tapeworm species reveal adaptations to parasitism

AU - Tsai, Isheng J

AU - Zarowiecki, Magdalena

AU - Holroyd, Nancy

AU - Garciarrubio, Alejandro

AU - Sanchez-Flores, Alejandro

AU - Brooks, Karen L

AU - Tracey, Alan

AU - Bobes, Raúl J

AU - Fragoso, Gladis

AU - Sciutto, Edda

AU - Aslett, Martin

AU - Beasley, Helen

AU - Bennett, Hayley M

AU - Cai, Jianping

AU - Camicia, Federico

AU - Clark, Richard

AU - Cucher, Marcela

AU - De Silva, Nishadi

AU - Day, Tim A

AU - Deplazes, Peter

AU - Estrada, Karel

AU - Fernández, Cecilia

AU - Holland, Peter W H

AU - Hou, Junling

AU - Hu, Songnian

AU - Huckvale, Thomas

AU - Hung, Stacy S

AU - Kamenetzky, Laura

AU - Keane, Jacqueline A

AU - Kiss, Ferenc

AU - Koziol, Uriel

AU - Lambert, Olivia

AU - Liu, Kan

AU - Luo, Xuenong

AU - Luo, Yingfeng

AU - Macchiaroli, Natalia

AU - Nichol, Sarah

AU - Paps, Jordi

AU - Parkinson, John

AU - Pouchkina-Stantcheva, Natasha

AU - Riddiford, Nick

AU - Rosenzvit, Mara

AU - Salinas, Gustavo

AU - Wasmuth, James D

AU - Zamanian, Mostafa

AU - Zheng, Yadong

AU - Cai, Xuepeng

AU - Soberón, Xavier

AU - Olson, Peter D

AU - Laclette, Juan P

AU - Taenia solium Genome Consortium

PY - 2013/4/4

Y1 - 2013/4/4

N2 - 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.

AB - 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.

KW - Adaptation, Physiological

KW - Animals

KW - Biological Evolution

KW - Cestoda

KW - Cestode Infections

KW - Conserved Sequence

KW - Echinococcus granulosus

KW - Echinococcus multilocularis

KW - Genes, Helminth

KW - Genes, Homeobox

KW - Genome, Helminth

KW - HSP70 Heat-Shock Proteins

KW - Humans

KW - Hymenolepis

KW - Metabolic Networks and Pathways

KW - Molecular Targeted Therapy

KW - Parasites

KW - Proteome

KW - Stem Cells

KW - Taenia solium

U2 - 10.1038/nature12031

DO - 10.1038/nature12031

M3 - Article

C2 - 23485966

SN - 0028-0836

VL - 496

SP - 57

EP - 63

JO - NATURE

JF - NATURE

IS - 7443

ER -

The genomes of four tapeworm species reveal adaptations to parasitism

Abstract

Keywords

UN SDGs

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