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Genes (Basel). 2019 Jan 8;10(1). pii: E29. doi: 10.3390/genes10010029.

Novel Characteristics of Mitochondrial Electron Transport Chain from Eimeria tenella.

Author information

1
Division of Veterinary Science, Graduate School of Life and Environmental Sciences, Osaka Prefecture University, 1-58, Rinku Orai Kita, Izumisano, Osaka 598-8531, Japan. matsubayashi@vet.osakafu-u.ac.jp.
2
School of Tropical Medicine and Global Health, Nagasaki University, 1-12-4, Sakamoto, Nagasaki 852-8523, Japan. danielken@nagasaki-u.ac.jp.
3
Department of Host-Defense Biochemistry, Institute of Tropical Medicine (NEKKEN), Nagasaki University, 1-12-4, Sakamoto, Nagasaki 852-8523, Japan. danielken@nagasaki-u.ac.jp.
4
Department of Biomedical Chemistry, Graduate School of Medicine, The University of Tokyo, 7-3-1, Hongo, Bunkyo-ku, Tokyo 113-0033, Japan. danielken@nagasaki-u.ac.jp.
5
Department of Biomedical Chemistry, Graduate School of Medicine, The University of Tokyo, 7-3-1, Hongo, Bunkyo-ku, Tokyo 113-0033, Japan. keisuke-kiyose@kcf.biglobe.ne.jp.
6
Department of Parasitology, Kitasato University School of Medicine, 1-15-1, Kitasato, Minami-ku, Sagamihara, Kanagawa 252-0374, Japan. htakeshi@med.kitasato-u.ac.jp.
7
Mocky Poultry Practice, Shinmeidai 2-5-33-810, Hamura-shi, Tokyo 205-0023, Japan. funuwo@f7.dion.ne.jp.
8
Department of Biochemistry and Molecular Biology, Faculty of Agriculture and Life Science, Hirosaki University, Aomori 036-8561, Japan. sakamok@hirosaki-u.ac.jp.
9
Department of Infection and Host Defense, Graduate School of Medicine, Chiba University, 1-8-1, Inohana, Chuo-ku, Chiba 260-8670, Japan. hikosaka@chiba-u.jp.
10
Research Center for Zoonosis Control, Hokkaido University, North 20, West 10, Kita-ku, Sapporo, Hokkaido 001-0020, Japan. junya@czc.hokudai.ac.jp.
11
Division of Veterinary Science, Graduate School of Life and Environmental Sciences, Osaka Prefecture University, 1-58, Rinku Orai Kita, Izumisano, Osaka 598-8531, Japan. ksasai@vet.osakafu-u.ac.jp.
12
Department of Applied Biology, Graduate School of Science Technology, Kyoto Institute of Technology, Matsugasaki, Sakyo-ku, Kyoto 606-8585, Japan. tshiba@kit.ac.jp.
13
Department of Applied Biology, Graduate School of Science Technology, Kyoto Institute of Technology, Matsugasaki, Sakyo-ku, Kyoto 606-8585, Japan. harada@kit.ac.jp.
14
Department of Parasitology, Kitasato University School of Medicine, 1-15-1, Kitasato, Minami-ku, Sagamihara, Kanagawa 252-0374, Japan. tsujin@med.kitasato-u.ac.jp.
15
School of Tropical Medicine and Global Health, Nagasaki University, 1-12-4, Sakamoto, Nagasaki 852-8523, Japan. kitak@nagasaki-u.ac.jp.
16
Department of Host-Defense Biochemistry, Institute of Tropical Medicine (NEKKEN), Nagasaki University, 1-12-4, Sakamoto, Nagasaki 852-8523, Japan. kitak@nagasaki-u.ac.jp.
17
Department of Biomedical Chemistry, Graduate School of Medicine, The University of Tokyo, 7-3-1, Hongo, Bunkyo-ku, Tokyo 113-0033, Japan. kitak@nagasaki-u.ac.jp.

Abstract

Eimeria tenella is an intracellular apicomplexan parasite, which infects cecal epithelial cells from chickens and causes hemorrhagic diarrhea and eventual death. We have previously reported the comparative RNA sequence analysis of the E. tenella sporozoite stage between virulent and precocious strains and showed that the expression of several genes involved in mitochondrial electron transport chain (ETC), such as type II NADH dehydrogenase (NDH-2), complex II (succinate:quinone oxidoreductase), malate:quinone oxidoreductase (MQO), and glycerol-3-phosphate dehydrogenase (G3PDH), were upregulated in virulent strain. To study E. tenella mitochondrial ETC in detail, we developed a reproducible method for preparation of mitochondria-rich fraction from sporozoites, which maintained high specific activities of dehydrogenases, such as NDH-2 followed by G3PDH, MQO, complex II, and dihydroorotate dehydrogenase (DHODH). Of particular importance, we showed that E. tenella sporozoite mitochondria possess an intrinsic ability to perform fumarate respiration (via complex II) in addition to the classical oxygen respiration (via complexes III and IV). Further analysis by high-resolution clear native electrophoresis, activity staining, and nano-liquid chromatography tandem-mass spectrometry (nano-LC-MS/MS) provided evidence of a mitochondrial complex II-III-IV supercomplex. Our analysis suggests that complex II from E. tenella has biochemical features distinct to known orthologues and is a potential target for the development of new anticoccidian drugs.

KEYWORDS:

Coccidium; Eimeria tenella; apicomplexa; electron transport chain; inhibitor; membrane protein; mitochondria; succinate dehydrogenase; ubiquinone

PMID:
30626105
DOI:
10.3390/genes10010029
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