Comparative genome analysis of three eukaryotic parasites with differing abilities to transform leukocytes reveals key mediators of theileria-induced leukocyte transformation

Kyoko Hayashida, Yuichiro Hara, Takashi Abe, C. Y. Chisato Yamasaki, Atsushi Toyoda, Takehide Kosuge, Yutaka Suzuki, Yoshiharu Sato, Shuichi Kawashima, Toshiaki Katayama, Hiroyuki Wakaguri, N. I. Noboru Inoue, K. H. Keiichi Homma, Masahito Tada-Umezaki, Yukio Yagi, Y. F. Yasuyuki Fujii, T. H. Takuya Habara, Minoru Kanehisa, H. W. Hidemi Watanabe, Kimihito ItoTakashi Gojobori, H. S. Hideaki Sugawara, Tadashi Imanishi, William Weir, Malcolm Gardner, A. P. Arnab Pain, Brian Shiels, Masahira Hattori, Vishvanath Nene, Chihiro Sugimoto

Research output: Contribution to journalArticle

41 Citations (Scopus)

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 Plasmo-dium 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/.

Original languageEnglish
JournalmBio
Volume3
Issue number5
DOIs
Publication statusPublished - 2012
Externally publishedYes

Fingerprint

Theileria
Parasites
Leukocytes
Genome
Babesia bovis
Genes
Synteny
Tars
Gene Duplication
Ticks
Monocytes
Proteins
Chromosomes
Erythrocytes
Macrophages
Databases
Lymphocytes

ASJC Scopus subject areas

  • Microbiology
  • Virology

Cite this

Comparative genome analysis of three eukaryotic parasites with differing abilities to transform leukocytes reveals key mediators of theileria-induced leukocyte transformation. / Hayashida, Kyoko; Hara, Yuichiro; Abe, Takashi; Chisato Yamasaki, C. Y.; Toyoda, Atsushi; Kosuge, Takehide; Suzuki, Yutaka; Sato, Yoshiharu; Kawashima, Shuichi; Katayama, Toshiaki; Wakaguri, Hiroyuki; Noboru Inoue, N. I.; Keiichi Homma, K. H.; Tada-Umezaki, Masahito; Yagi, Yukio; Yasuyuki Fujii, Y. F.; Takuya Habara, T. H.; Kanehisa, Minoru; Hidemi Watanabe, H. W.; Ito, Kimihito; Gojobori, Takashi; Hideaki Sugawara, H. S.; Imanishi, Tadashi; Weir, William; Gardner, Malcolm; Arnab Pain, A. P.; Shiels, Brian; Hattori, Masahira; Nene, Vishvanath; Sugimoto, Chihiro.

In: mBio, Vol. 3, No. 5, 2012.

Research output: Contribution to journalArticle

Hayashida, K, Hara, Y, Abe, T, Chisato Yamasaki, CY, Toyoda, A, Kosuge, T, Suzuki, Y, Sato, Y, Kawashima, S, Katayama, T, Wakaguri, H, Noboru Inoue, NI, Keiichi Homma, KH, Tada-Umezaki, M, Yagi, Y, Yasuyuki Fujii, YF, Takuya Habara, TH, Kanehisa, M, Hidemi Watanabe, HW, Ito, K, Gojobori, T, Hideaki Sugawara, HS, Imanishi, T, Weir, W, Gardner, M, Arnab Pain, AP, Shiels, B, Hattori, M, Nene, V & Sugimoto, C 2012, 'Comparative genome analysis of three eukaryotic parasites with differing abilities to transform leukocytes reveals key mediators of theileria-induced leukocyte transformation', mBio, vol. 3, no. 5. https://doi.org/10.1128/mBio.00204-12
Hayashida, Kyoko ; Hara, Yuichiro ; Abe, Takashi ; Chisato Yamasaki, C. Y. ; Toyoda, Atsushi ; Kosuge, Takehide ; Suzuki, Yutaka ; Sato, Yoshiharu ; Kawashima, Shuichi ; Katayama, Toshiaki ; Wakaguri, Hiroyuki ; Noboru Inoue, N. I. ; Keiichi Homma, K. H. ; Tada-Umezaki, Masahito ; Yagi, Yukio ; Yasuyuki Fujii, Y. F. ; Takuya Habara, T. H. ; Kanehisa, Minoru ; Hidemi Watanabe, H. W. ; Ito, Kimihito ; Gojobori, Takashi ; Hideaki Sugawara, H. S. ; Imanishi, Tadashi ; Weir, William ; Gardner, Malcolm ; Arnab Pain, A. P. ; Shiels, Brian ; Hattori, Masahira ; Nene, Vishvanath ; Sugimoto, Chihiro. / Comparative genome analysis of three eukaryotic parasites with differing abilities to transform leukocytes reveals key mediators of theileria-induced leukocyte transformation. In: mBio. 2012 ; Vol. 3, No. 5.
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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 Plasmo-dium 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/.",
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AU - Hayashida, Kyoko

AU - Hara, Yuichiro

AU - Abe, Takashi

AU - Chisato Yamasaki, C. Y.

AU - Toyoda, Atsushi

AU - Kosuge, Takehide

AU - Suzuki, Yutaka

AU - Sato, Yoshiharu

AU - Kawashima, Shuichi

AU - Katayama, Toshiaki

AU - Wakaguri, Hiroyuki

AU - Noboru Inoue, N. I.

AU - Keiichi Homma, K. H.

AU - Tada-Umezaki, Masahito

AU - Yagi, Yukio

AU - Yasuyuki Fujii, Y. F.

AU - Takuya Habara, T. H.

AU - Kanehisa, Minoru

AU - Hidemi Watanabe, H. W.

AU - Ito, Kimihito

AU - Gojobori, Takashi

AU - Hideaki Sugawara, H. S.

AU - Imanishi, Tadashi

AU - Weir, William

AU - Gardner, Malcolm

AU - Arnab Pain, A. P.

AU - Shiels, Brian

AU - Hattori, Masahira

AU - Nene, Vishvanath

AU - Sugimoto, Chihiro

PY - 2012

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