The Arf GAP SMAP2 is necessary for organized vesicle budding from the trans-Golgi network and subsequent acrosome formation in spermiogenesis

Tomo Funaki, Shunsuke Kon, Kenji Tanabe, Waka Natsume, Sayaka Sato, Tadafumi Shimizu, Naomi Yoshida, Won Fen Wong, Atsuo Ogura, Takehiko Ogawa, Kimiko Inoue, Narumi Ogonuki, Hiromi Miki, Keiji Mochida, Keisuke Endoh, Kentarou Yomogida, Manabu Fukumoto, Reiko Horai, Yoichiro Iwakura, Chizuru ItoKiyotaka Toshimori, Toshio Watanabe, Masanobu Satake

Research output: Contribution to journalArticle

25 Citations (Scopus)

Abstract

The trans-Golgi network (TGN) functions as a hub organelle in the exocytosis of clathrin-coated membrane vesicles, and SMAP2 is an Arf GTPase-activating protein that binds to both clathrin and the clathrin assembly protein (CALM). In the present study, SMAP2 is detected on the TGN in the pachytene spermatocyte to the round spermatid stages of spermatogenesis. Gene targeting reveals that SMAP2-deficient male mice are healthy and survive to adulthood but are infertile and exhibit globozoospermia. In SMAP2-deficient spermatids, the diameter of proacrosomal vesicles budding from TGN increases, TGN structures are distorted, acrosome formation is severely impaired, and reorganization of the nucleus does not proceed properly. CALM functions to regulate vesicle sizes, and this study shows that CALM is not recruited to the TGN in the absence of SMAP2. Furthermore, syntaxin2, a component of the soluble N-ethylmaleimide-sensitive factor attachment protein receptor (SNARE) complex, is not properly concentrated at the site of acrosome formation. Thus this study reveals a link between SMAP2 and CALM/syntaxin2 in clathrin-coated vesicle formation from the TGN and subsequent acrosome formation. SMAP2-deficient mice provide a model for globozoospermia in humans.

Original languageEnglish
Pages (from-to)2633-2644
Number of pages12
JournalMolecular biology of the cell
Volume24
Issue number17
DOIs
Publication statusPublished - 2013 Sep 1

ASJC Scopus subject areas

  • Molecular Biology
  • Cell Biology

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    Funaki, T., Kon, S., Tanabe, K., Natsume, W., Sato, S., Shimizu, T., Yoshida, N., Wong, W. F., Ogura, A., Ogawa, T., Inoue, K., Ogonuki, N., Miki, H., Mochida, K., Endoh, K., Yomogida, K., Fukumoto, M., Horai, R., Iwakura, Y., ... Satake, M. (2013). The Arf GAP SMAP2 is necessary for organized vesicle budding from the trans-Golgi network and subsequent acrosome formation in spermiogenesis. Molecular biology of the cell, 24(17), 2633-2644. https://doi.org/10.1091/mbc.E13-05-0234