Two adenine nucleotide translocase paralogues involved in cell proliferation and spermatogenesis in the silkworm Bombyx mori

Ryohei Sugahara, Akiya Jouraku, Takayo Nakakura, Takahiro Kusakabe, Takenori Yamamoto, Yasuo Shinohara, Hideto Miyoshi, Takahiro Shiotsuki

Research output: Contribution to journalArticle

13 Citations (Scopus)

Abstract

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.

Original languageEnglish
Article numbere0119429
JournalPloS one
Volume10
Issue number3
DOIs
Publication statusPublished - Mar 5 2015

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ATP Translocases Mitochondrial ADP
Bombyx
Cell proliferation
Spermatogenesis
Bombyx mori
silkworms
spermatogenesis
cell proliferation
Cell Proliferation
Mammals
energy metabolism
Energy Metabolism
Testis
testes
Proteins
proteins
Lepidoptera
mammals
Spermatocytes
Reptiles

All Science Journal Classification (ASJC) codes

  • Biochemistry, Genetics and Molecular Biology(all)
  • Agricultural and Biological Sciences(all)
  • General

Cite this

Two adenine nucleotide translocase paralogues involved in cell proliferation and spermatogenesis in the silkworm Bombyx mori. / Sugahara, Ryohei; Jouraku, Akiya; Nakakura, Takayo; Kusakabe, Takahiro; Yamamoto, Takenori; Shinohara, Yasuo; Miyoshi, Hideto; Shiotsuki, Takahiro.

In: PloS one, Vol. 10, No. 3, e0119429, 05.03.2015.

Research output: Contribution to journalArticle

Sugahara, R, Jouraku, A, Nakakura, T, Kusakabe, T, Yamamoto, T, Shinohara, Y, Miyoshi, H & Shiotsuki, T 2015, 'Two adenine nucleotide translocase paralogues involved in cell proliferation and spermatogenesis in the silkworm Bombyx mori', PloS one, vol. 10, no. 3, e0119429. https://doi.org/10.1371/journal.pone.0119429
Sugahara, Ryohei ; Jouraku, Akiya ; Nakakura, Takayo ; Kusakabe, Takahiro ; Yamamoto, Takenori ; Shinohara, Yasuo ; Miyoshi, Hideto ; Shiotsuki, Takahiro. / Two adenine nucleotide translocase paralogues involved in cell proliferation and spermatogenesis in the silkworm Bombyx mori. In: PloS one. 2015 ; Vol. 10, No. 3.
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