Entamoeba mitosomes play an important role in encystation by association with cholesteryl sulfate synthesis

Fumika Mi-ichi, Tomofumi Miyamoto, Shouko Takao, Ghulam Jeelani, Tetsuo Hashimoto, Hiromitsu Hara, Tomoyoshi Nozaki, Hiroki Yoshida

研究成果: ジャーナルへの寄稿記事

26 引用 (Scopus)

抄録

Hydrogenosomes and mitosomes are mitochondrion-related organelles (MROs) that have highly reduced and divergent functions in anaerobic/microaerophilic eukaryotes. Entamoeba histolytica, a microaerophilic, parasitic amoebozoan species, which causes intestinal and extraintestinal amoebiasis in humans, possesses mitosomes, the existence and biological functions of which have been a longstanding enigma in the evolution of mitochondria. We previously demonstrated that sulfate activation, which is not generally compartmentalized to mitochondria, is a major function of E. histolytica mitosomes. However, because the final metabolites of sulfate activation remain unknown, the overall scheme of this metabolism and the role of mitosomes in Entamoeba have not been elucidated. In this study we purified and identified cholesteryl sulfate (CS) as a final metabolite of sulfate activation. We then identified the gene encoding the cholesteryl sulfotransferase responsible for synthesizing CS. Addition of CS to culture media increased the number of cysts, the dormant form that differentiates from proliferative trophozoites. Conversely, chlorate, a selective inhibitor of the first enzyme in the sulfate-activation pathway, inhibited cyst formation in a dose-dependent manner. These results indicate that CS plays an important role in differentiation, an essential process for the transmission of Entamoeba between hosts. Furthermore, we show that Mastigamoeba balamuthi, an anaerobic, free-living amoebozoan species, which is a close relative of E. histolytica, also has the sulfate-activation pathway in MROs but does not possess the capacity for CS production. Hence, we propose that a unique function of MROs in Entamoeba contributes to its adaptation to its parasitic life cycle.

元の言語英語
ページ(範囲)E2884-E2890
ジャーナルProceedings of the National Academy of Sciences of the United States of America
112
発行部数22
DOI
出版物ステータス出版済み - 6 2 2015

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Entamoeba
Sulfates
Mitochondria
Entamoeba histolytica
Organelles
Cysts
Chlorates
Amoebic Dysentery
Sulfotransferases
Trophozoites
Enzyme Inhibitors
Life Cycle Stages
Eukaryota
Culture Media
cholesteryl sulfate
Genes

All Science Journal Classification (ASJC) codes

  • General

これを引用

Entamoeba mitosomes play an important role in encystation by association with cholesteryl sulfate synthesis. / Mi-ichi, Fumika; Miyamoto, Tomofumi; Takao, Shouko; Jeelani, Ghulam; Hashimoto, Tetsuo; Hara, Hiromitsu; Nozaki, Tomoyoshi; Yoshida, Hiroki.

:: Proceedings of the National Academy of Sciences of the United States of America, 巻 112, 番号 22, 02.06.2015, p. E2884-E2890.

研究成果: ジャーナルへの寄稿記事

Mi-ichi, Fumika ; Miyamoto, Tomofumi ; Takao, Shouko ; Jeelani, Ghulam ; Hashimoto, Tetsuo ; Hara, Hiromitsu ; Nozaki, Tomoyoshi ; Yoshida, Hiroki. / Entamoeba mitosomes play an important role in encystation by association with cholesteryl sulfate synthesis. :: Proceedings of the National Academy of Sciences of the United States of America. 2015 ; 巻 112, 番号 22. pp. E2884-E2890.
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abstract = "Hydrogenosomes and mitosomes are mitochondrion-related organelles (MROs) that have highly reduced and divergent functions in anaerobic/microaerophilic eukaryotes. Entamoeba histolytica, a microaerophilic, parasitic amoebozoan species, which causes intestinal and extraintestinal amoebiasis in humans, possesses mitosomes, the existence and biological functions of which have been a longstanding enigma in the evolution of mitochondria. We previously demonstrated that sulfate activation, which is not generally compartmentalized to mitochondria, is a major function of E. histolytica mitosomes. However, because the final metabolites of sulfate activation remain unknown, the overall scheme of this metabolism and the role of mitosomes in Entamoeba have not been elucidated. In this study we purified and identified cholesteryl sulfate (CS) as a final metabolite of sulfate activation. We then identified the gene encoding the cholesteryl sulfotransferase responsible for synthesizing CS. Addition of CS to culture media increased the number of cysts, the dormant form that differentiates from proliferative trophozoites. Conversely, chlorate, a selective inhibitor of the first enzyme in the sulfate-activation pathway, inhibited cyst formation in a dose-dependent manner. These results indicate that CS plays an important role in differentiation, an essential process for the transmission of Entamoeba between hosts. Furthermore, we show that Mastigamoeba balamuthi, an anaerobic, free-living amoebozoan species, which is a close relative of E. histolytica, also has the sulfate-activation pathway in MROs but does not possess the capacity for CS production. Hence, we propose that a unique function of MROs in Entamoeba contributes to its adaptation to its parasitic life cycle.",
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AU - Miyamoto, Tomofumi

AU - Takao, Shouko

AU - Jeelani, Ghulam

AU - Hashimoto, Tetsuo

AU - Hara, Hiromitsu

AU - Nozaki, Tomoyoshi

AU - Yoshida, Hiroki

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AB - Hydrogenosomes and mitosomes are mitochondrion-related organelles (MROs) that have highly reduced and divergent functions in anaerobic/microaerophilic eukaryotes. Entamoeba histolytica, a microaerophilic, parasitic amoebozoan species, which causes intestinal and extraintestinal amoebiasis in humans, possesses mitosomes, the existence and biological functions of which have been a longstanding enigma in the evolution of mitochondria. We previously demonstrated that sulfate activation, which is not generally compartmentalized to mitochondria, is a major function of E. histolytica mitosomes. However, because the final metabolites of sulfate activation remain unknown, the overall scheme of this metabolism and the role of mitosomes in Entamoeba have not been elucidated. In this study we purified and identified cholesteryl sulfate (CS) as a final metabolite of sulfate activation. We then identified the gene encoding the cholesteryl sulfotransferase responsible for synthesizing CS. Addition of CS to culture media increased the number of cysts, the dormant form that differentiates from proliferative trophozoites. Conversely, chlorate, a selective inhibitor of the first enzyme in the sulfate-activation pathway, inhibited cyst formation in a dose-dependent manner. These results indicate that CS plays an important role in differentiation, an essential process for the transmission of Entamoeba between hosts. Furthermore, we show that Mastigamoeba balamuthi, an anaerobic, free-living amoebozoan species, which is a close relative of E. histolytica, also has the sulfate-activation pathway in MROs but does not possess the capacity for CS production. Hence, we propose that a unique function of MROs in Entamoeba contributes to its adaptation to its parasitic life cycle.

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