Two adenine nucleotide translocase paralogues involved in cell proliferation and spermatogenesis in the silkworm Bombyx mori.
Mitochondrial adenine nucleotide translocase (ANT) specifically acts in ADP/ATP exchange through the mitochondrial inner membrane. This transporter protein thereby plays a significant role in energy metabolism in eukaryotic cells. Most mammals have four paralogous ANT genes (ANT1-4) and utilize these paralogues in different types of cells. The fourth paralogue of ANT (ANT4) is present only in mammals and reptiles and is exclusively expressed in testicular germ cells where it is required for meiotic progression in the spermatocytes. Here, we report that silkworms harbor two ANT paralogues, the homeostatic paralogue (BmANTI1) and the testis-specific paralogue (BmANTI2). The BmANTI2 protein has an N-terminal extension in which the positions of lysine residues in the amino acid sequence are distributed as in human ANT4. An expression analysis showed that BmANTI2 transcripts were restricted to the testis, suggesting the protein has a role in the progression of spermatogenesis. By contrast, BmANTI1 was expressed in all tissues tested, suggesting it has an important role in homeostasis. We also observed that cultured silkworm cells required BmANTI1 for proliferation. The ANTI1 protein of the lepidopteran Plutella xylostella (PxANTI1), but not those of other insect species (or PxANTI2), restored cell proliferation in BmANTI1-knockdown cells suggesting that ANTI1 has similar energy metabolism functions across the Lepidoptera. Our results suggest that BmANTI2 is evolutionarily divergent from BmANTI1 and has developed a specific role in spermatogenesis similar to that of mammalian ANT4.
Insect Growth Regulation Research Unit, National Institute of Agrobiological Sciences, Tsukuba, Ibaraki, Japan.
Ryohei
R
Sugahara
Insect Genome Research Unit, National Institute of Agrobiological Sciences, Tsukuba, Ibaraki, Japan.
Akiya
A
Jouraku
Insect Growth Regulation Research Unit, National Institute of Agrobiological Sciences, Tsukuba, Ibaraki, Japan.
Takayo
T
Nakakura
Laboratory of Silkworm Science, Kyushu University Graduate School of Bioresource and Bioenvironmental Sciences, Fukuoka, Japan.
Takahiro
T
Kusakabe
Institute for Genome Research, University of Tokushima, Tokushima, Japan.
Takenori
T
Yamamoto
Institute for Genome Research, University of Tokushima, Tokushima, Japan.
Yasuo
Y
Shinohara
Division of Applied Life Sciences, Graduate School of Agriculture, Kyoto University, Kyoto, Japan.
Hideto
H
Miyoshi
Insect Growth Regulation Research Unit, National Institute of Agrobiological Sciences, Tsukuba, Ibaraki, Japan.
Takahiro
T
Shiotsuki
D000595:Amino Acid Sequence; D000818:Animals; D012831:Bombyx / Q000378:metabolism*; D049109:Cell Proliferation; D003001:Cloning, Molecular; D008297:Male; D000226:Mitochondrial ADP, ATP Translocases / Q000737:chemistry / Q000235:genetics / Q000378:metabolism*; D008969:Molecular Sequence Data; D010802:Phylogeny; D012333:RNA, Messenger / Q000235:genetics; D017386:Sequence Homology, Amino Acid; D013091:Spermatogenesis; D013737:Testis / Q000378:metabolism
D012333:RNA, Messenger; D000226:Mitochondrial ADP, ATP Translocases