Lactic acid is a sperm motility inactivation factor in the sperm storage tubules

Matsuzaki, Mei; Mizushima, Shusei; Hiyama, Gen; Hirohashi, Noritaka; Shiba, Kogiku; Inaba, Kazuo; Suzuki, Tomohiro; Dohra, Hideo; Ohnishi, Toshiyuki; Sato, Yoshikatsu; Kohsaka, Tetsuya; Ichikawa, Yoshinobu; Atsumi, Yusuke; Yoshimura, Takashi; Sasanami, Tomohiro

doi:10.1038/srep17643

Cited by 54 publications

(74 citation statements)

References 52 publications

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“…In our recent research, we found that lactic acid in the SST lumen immobilized the resident sperm through cytoplasmic acidification that led to the inactivation of dynein ATPase (Matsuzaki et al, 2015). In contrast, BisII-mediated sperm motility inactivation is not related to pH i ( Fig.…”

Section: Discussionmentioning

confidence: 88%

Effects of a Protein Kinase Inhibitor on Sperm Motility in the Japanese Quail

et al. 2017

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Sperm motility is an essential trait for successful fertilization in animals. In birds, ejaculated sperm migrate into sperm storage tubules before fertilization and are stored in a quiescent state. We previously reported that this type of sperm's flagellar quiescence was induced by lactic acid through flagellar dynein ATPase inactivation following cytoplasmic acidification (＜pH 6.0). However, signal transduction in the sperm cells leading to motility inactivation is not well understood. The aim of the present study was to investigate the role of protein kinases in putative signal transduction in quail spermatozoa motility in vitro. Following incubation with bisindolylmaleimide II (BisII), a potent-competitive protein kinase C (PKC) inhibitor, sperm motility decreased in a dose related-manner. However, no such inhibitory effect was found in sperm exposed to bisindolylmaleimide V, H-89, or LY294002, a weak inhibitor of PKC, a potent inhibitor of protein kinase A (PKA) and a selective inhibitor of phosphatidylinositol 3-kinase, respectively. BisII-treated sperm exhibited no significant differences in pH i , [Ca 2+ ] i , mitochondrial activity, intracellular cAMP or ATP concentration, as well as dynein ATPase activity, compared to the control sperm. However, when the phosphorylated substrate proteins by PKC were detected by Western blot analysis, the intensity of the band in sperm incubated in the presence of BisII decreased. Moreover, immunoreactive PKCι and μ isoforms in the sperm lysates were also detected. These results indicated that the PKC signaling pathway may be involved in sperm motility regulation, and protein phosphorylation by PKC may be required to maintain flagellar movement in the Japanese quail.

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Section: Discussionmentioning

confidence: 88%

Effects of a Protein Kinase Inhibitor on Sperm Motility in the Japanese Quail

et al. 2017

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“…5A). Because high concentrations of lactate were detected in the seminal receptacle, this metabolite might help to sustain sperm survival under anaerobic conditions (31).…”

Section: Discussionmentioning

confidence: 99%

“…Future studies should address the molecular and cellular mechanisms of how squid spermatozoa are capable of storing glycogen at different levels. The physiological role of lactate efflux for sperm quiescence should also be considered in this species (31). These studies will open up new avenues in the field of andrology with the hope of developing treatments for human male infertility associated with flagellar motility deficiencies (39).…”

Section: Discussionmentioning

confidence: 99%

Sneaker Male Squid Produce Long-lived Spermatozoa by Modulating Their Energy Metabolism

Hirohashi

Tamura‐Nakano

Nakaya

et al. 2016

Journal of Biological Chemistry

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Spermatozoa released by males should remain viable until fertilization. Hence, sperm longevity is governed by intrinsic and environmental factors in accordance with the male mating strategy. However, whether intraspecific variation of insemination modes can impact sperm longevity remains to be elucidated. In the squid Heterololigo bleekeri, male dimorphism (consort and sneaker) is linked to two discontinuous insemination modes that differ in place and time. Notably, only sneaker male spermatozoa inseminated long before egg spawning can be stored in the seminal receptacle. We found that sneaker spermatozoa exhibited greater persistence in fertilization competence and flagellar motility than consort ones because of a larger amount of flagellar glycogen. Sneaker spermatozoa also showed higher capacities in glucose uptake and lactate efflux. Lactic acidosis was considered to stabilize CO 2 -triggered self-clustering of sneaker spermatozoa, thus establishing hypoxia-induced metabolic changes and sperm survival. These results, together with comparative omics analyses, suggest that postcopulatory reproductive contexts define sperm longevity by modulating the inherent energy levels and metabolic pathways.Sperm traits can evolve through postcopulatory contexts involving sperm competition, cryptic female choice, and insemination/fertilization environments. As consequences of sperm competition (1, 2) and cryptic female choice (3, 4), male individuals of certain species have evolved to produce giant spermatozoa to achieve better fertilization success. Besides morphological traits, the evolutionary forces driven by postcopulatory sexual selection should also favor more effective sperm motility and hence influence their morphological and energetic traits (5), thus facilitating fertilization in polyandrous mating systems. Sperm competition theory predicts that an increased risk of sperm competition (sometimes referred to as female promiscuity) should result in selection for increased sperm swimming velocity. A growing body of evidence has supported this prediction. Thus, a positive relationship between sperm swimming speed and sperm competitiveness was seen not only in external fertilizers such as fish (6 -8) but also in internal fertilizers such as birds (9, 10) and mammals (11). Commonly, polyandrous insemination can occur simultaneously (external fertilization) or sequentially (internal fertilization) toward the same set of eggs. However, in species that employ internal fertilization, female individuals often store spermatozoa in their reproductive tract and use them during multiple ovulation cycles (12-14). Thus, it is possible that spermatozoa with greater longevity might have greater reproductive fitness than those with increased velocity. This implicates that spermatozoa should be able to modulate their energy expenditure adequately depending on the postmating contexts.The coastal squid Heterololigo bleekeri exhibits alternative male mating tactics in which complex polyandrous inseminations occur at different places and...

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“…In animals, sperm motility is regulated by various extracellular cues, such as peptides/proteins and steroids (Clapper & Epel, 1982;Matsuzaki et al, 2015;Oda et al, 1995;Olson et al, 2001;Osanai, Kasuga, & Aigaki, 1989;Pillai, Shields, Yanagimachi, & Cherr, 1993;Strünker et al, 2011;Ward, Brokaw, Garbers, & Vacquier, 1985;Yoshida, Ishikawa, Izumi, DeSantis, & Morisawa, 2002). Each cue is adapted to a species-specific reproductive mode to ensure successful fertilization.…”

Section: Introductionmentioning

confidence: 99%

Sperm motility initiating substance may be insufficient to induce forward motility of Cynops ensicauda sperm

Sato

Endo

Morita

et al. 2017

Molecular Reproduction Devel

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Sperm motility-initiating substance (SMIS) is a key protein for internal fertilization of the newt, Cynops pyrrhogaster, and commonly enhances forward sperm motility in some amphibian species, including external fertilizers. SMIS action varies among different species in correlation with a species-specific reproductive environment. In the present study, we identified the gene of C. ensicauda SMIS (CeSMIS) and examined the mechanism of SMIS action with reference to that of the closely related Cynops species. The CeSMIS was identified by a 176-amino acid sequence including seven amino acids critical for the initiation of sperm motility. The amino acid sequence showed 91% homology to the whole sequence of C. pyrrhogaster SMIS (CpSMIS). By immunostaining with an anti-CpSMIS antibody, CeSMIS was shown to be localized in the outer layer of the egg jelly. A peptide presenting the active site of SMIS was observed to bind to the axial rod of the midpiece in C. ensicauda sperm. The localization and binding patterns of CeSMIS were fundamentally similar to those of CpSMIS. However, the SMIS peptide did not induce forward motility of C. ensicauda sperm, although it induced a fast wave of the undulating membrane. Forward sperm motility was induced in the egg jelly extract containing CeSMIS. These results suggest that the mechanism of initiation of sperm motility is differentiated between C. ensicauda and C. pyrrhogaster.

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Lactic acid is a sperm motility inactivation factor in the sperm storage tubules

Cited by 54 publications

References 52 publications

Effects of a Protein Kinase Inhibitor on Sperm Motility in the Japanese Quail

Effects of a Protein Kinase Inhibitor on Sperm Motility in the Japanese Quail

Sneaker Male Squid Produce Long-lived Spermatozoa by Modulating Their Energy Metabolism

Sperm motility initiating substance may be insufficient to induce forward motility of Cynops ensicauda sperm

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