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Kastor and Polluks polypeptides encoded by a single gene locus cooperatively regulate VDAC and spermatogenesis

Author

Listed:
  • Shintaro Mise

    (Kyushu University, Fukuoka)

  • Akinobu Matsumoto

    (Kyushu University, Fukuoka)

  • Keisuke Shimada

    (Osaka University)

  • Toshiaki Hosaka

    (RIKEN Center for Biosystems Dynamics Research)

  • Masatomo Takahashi

    (Kyushu University, Fukuoka)

  • Kazuya Ichihara

    (Kyushu University, Fukuoka)

  • Hideyuki Shimizu

    (Kyushu University, Fukuoka
    Tokyo Medical and Dental University)

  • Chisa Shiraishi

    (Kyushu University, Fukuoka)

  • Daisuke Saito

    (Kyushu University, Fukuoka)

  • Mikita Suyama

    (Kyushu University, Fukuoka)

  • Tomoharu Yasuda

    (Hiroshima University, Hiroshima)

  • Toru Ide

    (Okayama University, Okayama)

  • Yoshihiro Izumi

    (Kyushu University, Fukuoka)

  • Takeshi Bamba

    (Kyushu University, Fukuoka)

  • Tomomi Kimura-Someya

    (RIKEN Center for Biosystems Dynamics Research)

  • Mikako Shirouzu

    (RIKEN Center for Biosystems Dynamics Research)

  • Haruhiko Miyata

    (Osaka University)

  • Masahito Ikawa

    (Osaka University
    The University of Tokyo)

  • Keiichi I. Nakayama

    (Kyushu University, Fukuoka)

Abstract

Although several long noncoding RNAs (lncRNAs) have recently been shown to encode small polypeptides, those in testis remain largely uncharacterized. Here we identify two sperm-specific polypeptides, Kastor and Polluks, encoded by a single mouse locus (Gm9999) previously annotated as encoding a lncRNA. Both Kastor and Polluks are inserted in the outer mitochondrial membrane and directly interact with voltage-dependent anion channel (VDAC), despite their different amino acid sequences. Male VDAC3-deficient mice are infertile as a result of reduced sperm motility due to an abnormal mitochondrial sheath in spermatozoa, and deficiency of both Kastor and Polluks also severely impaired male fertility in association with formation of a similarly abnormal mitochondrial sheath. Spermatozoa lacking either Kastor or Polluks partially recapitulate the phenotype of those lacking both. Cooperative function of Kastor and Polluks in regulation of VDAC3 may thus be essential for mitochondrial sheath formation in spermatozoa and for male fertility.

Suggested Citation

  • Shintaro Mise & Akinobu Matsumoto & Keisuke Shimada & Toshiaki Hosaka & Masatomo Takahashi & Kazuya Ichihara & Hideyuki Shimizu & Chisa Shiraishi & Daisuke Saito & Mikita Suyama & Tomoharu Yasuda & To, 2022. "Kastor and Polluks polypeptides encoded by a single gene locus cooperatively regulate VDAC and spermatogenesis," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-28677-y
    DOI: 10.1038/s41467-022-28677-y
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    References listed on IDEAS

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    1. Qian Chu & Thomas F. Martinez & Sammy Weiser Novak & Cynthia J. Donaldson & Dan Tan & Joan M. Vaughan & Tina Chang & Jolene K. Diedrich & Leo Andrade & Andrew Kim & Tong Zhang & Uri Manor & Alan Sagha, 2019. "Regulation of the ER stress response by a mitochondrial microprotein," Nature Communications, Nature, vol. 10(1), pages 1-13, December.
    2. Akinobu Matsumoto & Alessandra Pasut & Masaki Matsumoto & Riu Yamashita & Jacqueline Fung & Emanuele Monteleone & Alan Saghatelian & Keiichi I. Nakayama & John G. Clohessy & Pier Paolo Pandolfi, 2017. "mTORC1 and muscle regeneration are regulated by the LINC00961-encoded SPAR polypeptide," Nature, Nature, vol. 541(7636), pages 228-232, January.
    3. Shigeomi Shimizu & Masashi Narita & Yoshihide Tsujimoto & Yoshihide Tsujimoto, 1999. "Bcl-2 family proteins regulate the release of apoptogenic cytochrome c by the mitochondrial channel VDAC," Nature, Nature, vol. 399(6735), pages 483-487, June.
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