Premammalian origin of the sperm‐specific Slo3 channel

Vicens, Alberto; Andrade-López, Karla; Cortez, Diego; Gutiérrez, Ranier; Treviño, Claudia L.

doi:10.1002/2211-5463.12186

Cited by 11 publications

(11 citation statements)

References 43 publications

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“…Although the mechanism responsible for membrane hyperpolarization by SFKs in chicken sperm remains unclear, previous studies using heterologous expression systems combined with pharmacological murine sperm experiments suggested that potassium efflux occurs via SLO3, a sperm-specific potassium channel, in response to SFK activation, which eventually stimulates membrane hyperpolarization preceding a series of capacitation processes [ 25 ]. Despite the fact that capacitation processes have not been recognized in birds, reptiles, and fish, SLO3 is predominantly expressed in their testes, accordant to mammalian SLO3 [ 55 ]. Our results suggest investigation for the relationship among chicken SFK, SLO3, and membrane potential, using heterologous expression system.…”

Section: Discussionmentioning

confidence: 99%

Src family kinases-mediated negative regulation of sperm acrosome reaction in chickens (Gallus gallus domesticus)

et al. 2020

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The acrosome reaction (AR) is a strictly-regulated, synchronous exocytosis that is required for sperm to penetrate ova. This all-or-nothing process occurs only once in the sperm lifecycle through a sequence of signaling pathways. Spontaneous, premature AR therefore compromises fertilization potential. Although protein kinase A (PKA) pathways play a central role in AR across species, the signaling network used for AR induction is poorly understood in birds. Mechanistic studies of mammalian sperm AR demonstrate that PKA activity is downstreamly regulated by Src family kinases (SFKs). Using SFK inhibitors, our study shows that in chicken sperm, SFKs play a role in the regulation of PKA activity and spontaneous AR without affecting motility. Furthermore, we examined the nature of SFK phosphorylation using PKA and protein tyrosine phosphatase inhibitors, which demonstrated that unlike in mammals, SFK phosphorylation in birds does not occur downstream of PKA and is primarily regulated by calcium-dependent tyrosine phosphatase activity. Functional characterization of SFKs in chicken sperm showed that SFK activation modulates the membrane potential and plays a role in inhibiting spontaneous AR. Employing biochemical isolation, we also found that membrane rafts are involved in the regulation of SFK phosphorylation. This study demonstrates a unique mechanism for regulating AR induction inherent to avian sperm that ensure fertilization potential despite prolonged storage.

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Section: Discussionmentioning

confidence: 99%

Src family kinases-mediated negative regulation of sperm acrosome reaction in chickens (Gallus gallus domesticus)

et al. 2020

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“…It will be important to explore whether the signalling cascade of the chemoattractant established in sea urchin sperm is conserved in other marine invertebrates. On the other hand, in many vertebrates, including mammals, Slo3 appears to have replaced the function of tetraKCNG/CNGK [87]. Namely, in the mouse, Slo3 together with sNHE and sAC seem to play an important role in controlling CatSper.…”

Section: Discussionmentioning

confidence: 99%

Comparative genomic analysis suggests that the sperm-specific sodium/proton exchanger and soluble adenylyl cyclase are key regulators of CatSper among the Metazoa

Romero

Nishigaki

2019

Zoological Lett

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Background CatSper is a sperm-specific calcium ion (Ca 2+ ) channel, which regulates sperm flagellar beating by tuning cytoplasmic Ca 2+ concentrations. Although this Ca 2+ channel is essential for mammalian fertilization, recent bioinformatics analyses have revealed that genes encoding CatSper are heterogeneously distributed throughout the eukaryotes, including vertebrates. As this channel is activated by cytoplasmic alkalization in mammals and sea urchins, it has been proposed that the sperm-specific Na + /H + exchanger (sNHE, a product of the SLC9C gene family) positively regulates its activity. In mouse, sNHE is functionally coupled to soluble adenylyl cyclase (sAC). CatSper, sNHE, and sAC have thus been considered functionally interconnected in the control of sperm motility, at least in mouse and sea urchin. Results We carried out a comparative genomic analysis to explore phylogenetic relationships among CatSper, sNHE and sAC in eukaryotes. We found that sNHE occurs only in Metazoa, although sAC occurs widely across eukaryotes. In animals, we found correlated and restricted distribution patterns of the three proteins, suggesting coevolution among them in the Metazoa. Namely, nearly all species in which CatSper is conserved also preserve sNHE and sAC. In contrast, in species without sAC, neither CatSper nor sNHE is conserved. On the other hand, the distribution of another testis-specific NHE (NHA, a product of the SLC9B gene family) does not show any apparent association with that of CatSper. Conclusions Our results suggest that CatSper, sNHE and sAC form prototypical machinery that functions in regulating sperm flagellar beating in Metazoa. In non-metazoan species, CatSper may be regulated by other H + transporters, or its activity might be independent of cytoplasmic pH. Electronic supplementary material The online version of this article (10.1186/s40851-019-0141-3) contains supplementary material, which is available to authorized users.

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“…Indeed, an increase in K + in an extracellular environment induces an increase in [Ca 2+ ] i in human spermatozoa, along with the addition of progesterone [ 138 ]. SLO1 (also known as the big calcium (BK) channel) is expressed across all metazoa and mainly in neural and muscular cells, whereas SLO3 is unique to mammalian spermatozoa [ 135 ]; however, exploratory genomics has revealed the presence of the Slo3 gene in fish, birds, and reptiles [ 139 ], and recent findings indicate the presence of a cytoplasmic truncated SLO3 isoform in mouse tissues, such as brain, kidneys, and eyes [ 140 ]. Sequence analysis suggests that SLO3 evolved from SLO1 via gene duplication, and that, in humans, the sequences feature a 42% identity [ 135 ].…”

Section: Potassium Channelsmentioning

confidence: 99%

Structure and Function of Ion Channels Regulating Sperm Motility—An Overview

Nowicka-Bauer

Szymczak-Cendlak

2021

IJMS

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Sperm motility is linked to the activation of signaling pathways that trigger movement. These pathways are mainly dependent on Ca2+, which acts as a secondary messenger. The maintenance of adequate Ca2+ concentrations is possible thanks to proper concentrations of other ions, such as K+ and Na+, among others, that modulate plasma membrane potential and the intracellular pH. Like in every cell, ion homeostasis in spermatozoa is ensured by a vast spectrum of ion channels supported by the work of ion pumps and transporters. To achieve success in fertilization, sperm ion channels have to be sensitive to various external and internal factors. This sensitivity is provided by specific channel structures. In addition, novel sperm-specific channels or isoforms have been found with compositions that increase the chance of fertilization. Notably, the most significant sperm ion channel is the cation channel of sperm (CatSper), which is a sperm-specific Ca2+ channel required for the hyperactivation of sperm motility. The role of other ion channels in the spermatozoa, such as voltage-gated Ca2+ channels (VGCCs), Ca2+-activated Cl-channels (CaCCs), SLO K+ channels or voltage-gated H+ channels (VGHCs), is to ensure the activation and modulation of CatSper. As the activation of sperm motility differs among metazoa, different ion channels may participate; however, knowledge regarding these channels is still scarce. In the present review, the roles and structures of the most important known ion channels are described in regard to regulation of sperm motility in animals.

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Premammalian origin of the sperm‐specific Slo3 channel

Cited by 11 publications

References 43 publications

Src family kinases-mediated negative regulation of sperm acrosome reaction in chickens (Gallus gallus domesticus)

Src family kinases-mediated negative regulation of sperm acrosome reaction in chickens (Gallus gallus domesticus)

Comparative genomic analysis suggests that the sperm-specific sodium/proton exchanger and soluble adenylyl cyclase are key regulators of CatSper among the Metazoa

Structure and Function of Ion Channels Regulating Sperm Motility—An Overview

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