Comparative Genome Analysis of Three Eukaryotic Parasites with Differing Abilities To Transform Leukocytes Reveals Key Mediators of <italic toggle="yes">Theileria</italic>-Induced Leukocyte Transformation

ABSTRACT We sequenced the genome of Theileria orientalis, a tick-borne apicomplexan protozoan parasite of cattle. The focus of this study was a comparative genome analysis of T. orientalis relative to other highly pathogenic Theileria species, T. parva and T. annulata. T. parva and T. annulata induc...

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Autores principales: Kyoko Hayashida, Yuichiro Hara, Takashi Abe, Chisato Yamasaki, Atsushi Toyoda, Takehide Kosuge, Yutaka Suzuki, Yoshiharu Sato, Shuichi Kawashima, Toshiaki Katayama, Hiroyuki Wakaguri, Noboru Inoue, Keiichi Homma, Masahito Tada-Umezaki, Yukio Yagi, Yasuyuki Fujii, Takuya Habara, Minoru Kanehisa, Hidemi Watanabe, Kimihito Ito, Takashi Gojobori, Hideaki Sugawara, Tadashi Imanishi, William Weir, Malcolm Gardner, Arnab Pain, Brian Shiels, Masahira Hattori, Vishvanath Nene, Chihiro Sugimoto
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Publicado: American Society for Microbiology 2012
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spelling oai:doaj.org-article:8ef5bb2567d144238fd0123a21dd123e2021-11-15T15:39:12ZComparative Genome Analysis of Three Eukaryotic Parasites with Differing Abilities To Transform Leukocytes Reveals Key Mediators of <italic toggle="yes">Theileria</italic>-Induced Leukocyte Transformation10.1128/mBio.00204-122150-7511https://doaj.org/article/8ef5bb2567d144238fd0123a21dd123e2012-11-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00204-12https://doaj.org/toc/2150-7511ABSTRACT We sequenced the genome of Theileria orientalis, a tick-borne apicomplexan protozoan parasite of cattle. The focus of this study was a comparative genome analysis of T. orientalis relative to other highly pathogenic Theileria species, T. parva and T. annulata. T. parva and T. annulata induce transformation of infected cells of lymphocyte or macrophage/monocyte lineages; in contrast, T. orientalis does not induce uncontrolled proliferation of infected leukocytes and multiplies predominantly within infected erythrocytes. While synteny across homologous chromosomes of the three Theileria species was found to be well conserved overall, subtelomeric structures were found to differ substantially, as T. orientalis lacks the large tandemly arrayed subtelomere-encoded variable secreted protein-encoding gene family. Moreover, expansion of particular gene families by gene duplication was found in the genomes of the two transforming Theileria species, most notably, the TashAT/TpHN and Tar/Tpr gene families. Gene families that are present only in T. parva and T. annulata and not in T. orientalis, Babesia bovis, or Plasmodium were also identified. Identification of differences between the genome sequences of Theileria species with different abilities to transform and immortalize bovine leukocytes will provide insight into proteins and mechanisms that have evolved to induce and regulate this process. The T. orientalis genome database is available at http://totdb.czc.hokudai.ac.jp/. IMPORTANCE Cancer-like growth of leukocytes infected with malignant Theileria parasites is a unique cellular event, as it involves the transformation and immortalization of one eukaryotic cell by another. In this study, we sequenced the whole genome of a nontransforming Theileria species, Theileria orientalis, and compared it to the published sequences representative of two malignant, transforming species, T. parva and T. annulata. The genome-wide comparison of these parasite species highlights significant genetic diversity that may be associated with evolution of the mechanism(s) deployed by an intracellular eukaryotic parasite to transform its host cell.Kyoko HayashidaYuichiro HaraTakashi AbeChisato YamasakiAtsushi ToyodaTakehide KosugeYutaka SuzukiYoshiharu SatoShuichi KawashimaToshiaki KatayamaHiroyuki WakaguriNoboru InoueKeiichi HommaMasahito Tada-UmezakiYukio YagiYasuyuki FujiiTakuya HabaraMinoru KanehisaHidemi WatanabeKimihito ItoTakashi GojoboriHideaki SugawaraTadashi ImanishiWilliam WeirMalcolm GardnerArnab PainBrian ShielsMasahira HattoriVishvanath NeneChihiro SugimotoAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 3, Iss 5 (2012)
institution DOAJ
collection DOAJ
language EN
topic Microbiology
QR1-502
spellingShingle Microbiology
QR1-502
Kyoko Hayashida
Yuichiro Hara
Takashi Abe
Chisato Yamasaki
Atsushi Toyoda
Takehide Kosuge
Yutaka Suzuki
Yoshiharu Sato
Shuichi Kawashima
Toshiaki Katayama
Hiroyuki Wakaguri
Noboru Inoue
Keiichi Homma
Masahito Tada-Umezaki
Yukio Yagi
Yasuyuki Fujii
Takuya Habara
Minoru Kanehisa
Hidemi Watanabe
Kimihito Ito
Takashi Gojobori
Hideaki Sugawara
Tadashi Imanishi
William Weir
Malcolm Gardner
Arnab Pain
Brian Shiels
Masahira Hattori
Vishvanath Nene
Chihiro Sugimoto
Comparative Genome Analysis of Three Eukaryotic Parasites with Differing Abilities To Transform Leukocytes Reveals Key Mediators of <italic toggle="yes">Theileria</italic>-Induced Leukocyte Transformation
description ABSTRACT We sequenced the genome of Theileria orientalis, a tick-borne apicomplexan protozoan parasite of cattle. The focus of this study was a comparative genome analysis of T. orientalis relative to other highly pathogenic Theileria species, T. parva and T. annulata. T. parva and T. annulata induce transformation of infected cells of lymphocyte or macrophage/monocyte lineages; in contrast, T. orientalis does not induce uncontrolled proliferation of infected leukocytes and multiplies predominantly within infected erythrocytes. While synteny across homologous chromosomes of the three Theileria species was found to be well conserved overall, subtelomeric structures were found to differ substantially, as T. orientalis lacks the large tandemly arrayed subtelomere-encoded variable secreted protein-encoding gene family. Moreover, expansion of particular gene families by gene duplication was found in the genomes of the two transforming Theileria species, most notably, the TashAT/TpHN and Tar/Tpr gene families. Gene families that are present only in T. parva and T. annulata and not in T. orientalis, Babesia bovis, or Plasmodium were also identified. Identification of differences between the genome sequences of Theileria species with different abilities to transform and immortalize bovine leukocytes will provide insight into proteins and mechanisms that have evolved to induce and regulate this process. The T. orientalis genome database is available at http://totdb.czc.hokudai.ac.jp/. IMPORTANCE Cancer-like growth of leukocytes infected with malignant Theileria parasites is a unique cellular event, as it involves the transformation and immortalization of one eukaryotic cell by another. In this study, we sequenced the whole genome of a nontransforming Theileria species, Theileria orientalis, and compared it to the published sequences representative of two malignant, transforming species, T. parva and T. annulata. The genome-wide comparison of these parasite species highlights significant genetic diversity that may be associated with evolution of the mechanism(s) deployed by an intracellular eukaryotic parasite to transform its host cell.
format article
author Kyoko Hayashida
Yuichiro Hara
Takashi Abe
Chisato Yamasaki
Atsushi Toyoda
Takehide Kosuge
Yutaka Suzuki
Yoshiharu Sato
Shuichi Kawashima
Toshiaki Katayama
Hiroyuki Wakaguri
Noboru Inoue
Keiichi Homma
Masahito Tada-Umezaki
Yukio Yagi
Yasuyuki Fujii
Takuya Habara
Minoru Kanehisa
Hidemi Watanabe
Kimihito Ito
Takashi Gojobori
Hideaki Sugawara
Tadashi Imanishi
William Weir
Malcolm Gardner
Arnab Pain
Brian Shiels
Masahira Hattori
Vishvanath Nene
Chihiro Sugimoto
author_facet Kyoko Hayashida
Yuichiro Hara
Takashi Abe
Chisato Yamasaki
Atsushi Toyoda
Takehide Kosuge
Yutaka Suzuki
Yoshiharu Sato
Shuichi Kawashima
Toshiaki Katayama
Hiroyuki Wakaguri
Noboru Inoue
Keiichi Homma
Masahito Tada-Umezaki
Yukio Yagi
Yasuyuki Fujii
Takuya Habara
Minoru Kanehisa
Hidemi Watanabe
Kimihito Ito
Takashi Gojobori
Hideaki Sugawara
Tadashi Imanishi
William Weir
Malcolm Gardner
Arnab Pain
Brian Shiels
Masahira Hattori
Vishvanath Nene
Chihiro Sugimoto
author_sort Kyoko Hayashida
title Comparative Genome Analysis of Three Eukaryotic Parasites with Differing Abilities To Transform Leukocytes Reveals Key Mediators of <italic toggle="yes">Theileria</italic>-Induced Leukocyte Transformation
title_short Comparative Genome Analysis of Three Eukaryotic Parasites with Differing Abilities To Transform Leukocytes Reveals Key Mediators of <italic toggle="yes">Theileria</italic>-Induced Leukocyte Transformation
title_full Comparative Genome Analysis of Three Eukaryotic Parasites with Differing Abilities To Transform Leukocytes Reveals Key Mediators of <italic toggle="yes">Theileria</italic>-Induced Leukocyte Transformation
title_fullStr Comparative Genome Analysis of Three Eukaryotic Parasites with Differing Abilities To Transform Leukocytes Reveals Key Mediators of <italic toggle="yes">Theileria</italic>-Induced Leukocyte Transformation
title_full_unstemmed Comparative Genome Analysis of Three Eukaryotic Parasites with Differing Abilities To Transform Leukocytes Reveals Key Mediators of <italic toggle="yes">Theileria</italic>-Induced Leukocyte Transformation
title_sort comparative genome analysis of three eukaryotic parasites with differing abilities to transform leukocytes reveals key mediators of <italic toggle="yes">theileria</italic>-induced leukocyte transformation
publisher American Society for Microbiology
publishDate 2012
url https://doaj.org/article/8ef5bb2567d144238fd0123a21dd123e
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