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Gen L Takei Department of Regulatory Physiology, Dokkyo Medical University, Mibu-Machi, Tochigi, Japan

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Masakatsu Fujinoki Department of Regulatory Physiology, Dokkyo Medical University, Mibu-Machi, Tochigi, Japan

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Abstract

Mammalian sperm motility has to be hyperactivated to be fertilization-competent. Hyperactivation is regulated by extracellular environment. Osmolality of mammalian semen is higher than that in female reproductive tract; however, the effect of them on hyperactivation has not been investigated. So we investigated the effect of osmotic environment on hyperactivation using hamster spermatozoa at first. Increase in the osmolality of the media (∼370 mOsm) by increasing the concentration of NaCl (∼150 mmol/L) caused the delay of the expression of hyperactivation. When NaCl concentration varied in the same range (75–150 mmol/L) whereas the osmolality was fixed at 370 mOsm by adding mannitol, the delay of hyperactivation occurred dependent on NaCl concentration. Increase in NaCl concentration also caused suppression of curvilinear velocity, bend angle, and sliding velocity of the flagellum at the onset of incubation, suggesting that NaCl concentration affect both activation and hyperactivation in hamster spermatozoa. Hamster sperm intracellular Ca2+ concentration decreased as extracellular NaCl concentration increased, whereas membrane potential and intracellular pH were unaffected by extracellular NaCl concentration. SN-6 and SEA0400, inhibitors of Na+-Ca2+ exchanger (NCX), increased intracellular Ca2+ and accelerated hyperactivation in the presence of 150 mmol/L NaCl. Tyrosine phosphorylation on fibrous sheath proteins was unaffected by extracellular NaCl concentration. These results suggest that extracellular Na+ suppresses hamster sperm hyperactivation by reducing intracellular Ca2+ via an action of NCX in a tyrosine phosphorylation-independent manner. It seems that the removal of suppression by extracellular Na+ leads to the expression of hyperactivated motility.

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Gen L Takei Department of Pharmacology and Toxicology, Dokkyo Medical University, Kitakobayashi, Mibu-Machi, Shimotsuga-gun, Tochigi, Japan

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Yasuhiro Horibata Department of Biochemistry, Dokkyo Medical University, Kitakobayashi, Mibu-Machi, Shimotsuga-gun, Tochigi, Japan

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Fubito Toyama School of Engineering, Utsunomiya University, Yoto, Utsunomiya, Tochigi, Japan

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Keitaro Hayashi Department of Pharmacology and Toxicology, Dokkyo Medical University, Kitakobayashi, Mibu-Machi, Shimotsuga-gun, Tochigi, Japan

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Asuka Morita Department of Pharmacology and Toxicology, Dokkyo Medical University, Kitakobayashi, Mibu-Machi, Shimotsuga-gun, Tochigi, Japan

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Motoshi Ouchi Department of Pharmacology and Toxicology, Dokkyo Medical University, Kitakobayashi, Mibu-Machi, Shimotsuga-gun, Tochigi, Japan
Department of Health Promotion in Nursing and Midwifery, Innovative Nursing for Life Course, Graduate School of Nursing, Chiba University, Inohana, Chuo-ku, Chiba-shi, Chiba, Japan

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Tomoe Fujita Department of Pharmacology and Toxicology, Dokkyo Medical University, Kitakobayashi, Mibu-Machi, Shimotsuga-gun, Tochigi, Japan

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In brief

Mammalian spermatozoa actively generate reactive oxygen species (ROS) during capacitation, a maturational process necessary for fertilization in vivo. This study shows that hypotaurine, a precursor of taurine present in the oviduct, is incorporated and concentrated in hamster sperm cells via the taurine transporter, TauT, for cytoprotection against self-produced ROS.

Abstract

To achieve fertilization competence, mammalian spermatozoa undergo capacitation, during which they actively generate reactive oxygen species (ROS). Therefore, mammalian spermatozoa must protect themselves from these self-generated ROS. The mammalian oviductal fluid is rich in hypotaurine, a taurine precursor, which reportedly protects mammalian spermatozoa, including those of hamsters, from ROS; however, its precise mechanism remains unknown. This study aimed to elucidate the mechanism underlying hypotaurine-mediated protection of spermatozoa from ROS using hamsters, particularly focusing on the taurine/hypotaurine transporter TauT. The effect of hypotaurine on sperm motility and ROS levels was tested using sperm motility analysis and the CellROX dye and luminol assays. RNA sequencing analysis was performed to verify TauT expression. We found that hypotaurine was necessary for maintaining sperm motility and hyperactivated motility. Hypotaurine did not scavenge extracellular ROS but lowered intracellular ROS levels and was incorporated and concentrated in hamster spermatozoa. TauT was detected at both mRNA and protein levels. β-Alanine blocked hypotaurine transport, increased intracellular ROS levels, and inhibited hyperactivation. Elimination of Na+ or Cl ions inhibited hypotaurine transport and increased intracellular ROS levels. Thus, these results indicated that hamster spermatozoa incorporated and concentrated hypotaurine in sperm cells via TauT to protect themselves from self-generated ROS.

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