Chemotactic behavior of egg mitochondria in response to sperm fusion in mice

Maki Iwai; Yuichirou Harada; Rinako Miyabayashi; Woojin Kang; Akihiro Nakamura; Natsuko Kawano; Yoshitaka Miyamoto; Mitsutoshi Yamada; Toshio Hamatani; Mami Miyado; Keiichi Yoshida; Hidekazu Saito; Mamoru Tanaka; Akihiro Umezawa; Kenji Miyado

doi:10.1016/j.heliyon.2018.e00944

Chemotactic behavior of egg mitochondria in response to sperm fusion in mice

Heliyon. 2018 Nov 16;4(11):e00944. doi: 10.1016/j.heliyon.2018.e00944. eCollection 2018 Nov.

Authors

Maki Iwai^{1

2}, Yuichirou Harada³, Rinako Miyabayashi⁴, Woojin Kang^{2

5}, Akihiro Nakamura^{1

2}, Natsuko Kawano^{2

6}, Yoshitaka Miyamoto², Mitsutoshi Yamada¹, Toshio Hamatani¹, Mami Miyado⁷, Keiichi Yoshida⁸, Hidekazu Saito⁵, Mamoru Tanaka¹, Akihiro Umezawa², Kenji Miyado²

Affiliations

¹ Department of Obstetrics and Gynecology, Keio University School of Medicine, 35 Shinanomachi, Shinjuku, Tokyo 160-8582, Japan.
² Department of Reproductive Biology, National Research Institute for Child Health and Development, 2-10-1 Okura, Setagaya, Tokyo 157-8535, Japan.
³ Department of Molecular Pathology, Tokyo Medical University, 6-1-1 Shinjuku, Shinjuku, Tokyo 192-0397, Japan.
⁴ Shinbashi YUME Clinic, 2-5-1 Shinbashi, Miyato, Tokyo 105-0004, Japan.
⁵ Department of Perinatal Medicine and Oocyte Care, National Center for Child Health and Development, 2-10-1 Okura, Setagaya, Tokyo 157-8535, Japan.
⁶ Department of Life Sciences, School of Agriculture, Meiji University, 1-1-1 Higashimita, Tama, Kawasaki, Kanagawa 214-8571, Japan.
⁷ Department of Molecular Endocrinology, National Research Institute for Child Health and Development, 2-10-1 Okura, Setagaya, Tokyo 157-8535, Japan.
⁸ Advanced Medicine, Innovation and Clinical Research Center, Tottori University Hospital, 36-1 Nishicho, Yonago, Tottori 683-8504, Japan.

Abstract

Mitochondria are the powerhouses of eukaryotic cells and their positioning contributes to fertilization and early developmental processes. We report that sperm fusion triggers Ca²⁺ oscillations and mitochondrial movement toward fused sperm (mitochondrial chemotaxis) in mouse eggs. Mitochondria functioned in Ca²⁺ storage and were colocalized with endoplasmic reticulum (ER) during Ca²⁺ oscillations. Mitochondria then moved toward the fused sperm. Sperm extracts lacking nuclei induced Ca²⁺ oscillations, but did not promote mitochondrial chemotaxis. Our results suggest that sperm fusion motivates Ca²⁺ oscillation-independent mitochondrial chemotaxis. This phenomenon indicates that egg mitochondria interact with sperm materials, presumably nuclear substances, and their network tethers egg and sperm nuclei at the early stage of zygote formation.

Keywords: Cell biology; Developmental biology; Molecular biology; Zoology.