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Premammalian origin of the sperm-specific Slo3 channel.

ABSTRACT: Slo3 is a sperm-specific potassium (K+) channel essential for male fertility. Slo3 channels have so far been considered to be specific to mammals. Through exploratory genomics, we identified the Slo3 gene in the genome of terrestrial (birds and reptiles) and aquatic (fish) vertebrates. In the case of fish, Slo3 has undergone several episodes of gene loss. Transcriptomic analysis showed that vertebrate Slo3 transcript orthologues are predominantly expressed in testis, in concordance with the mammalian Slo3. We conclude that the Slo3 gene arose during the radiation of early vertebrates, much earlier than previously thought. Our findings add to the growing evidence indicating that the phylogenetic profiles of sperm-specific channels are intermittent throughout metazoan evolution, which probably reflects the adaptation of sperm to different ionic milieus and fertilization environments.

SUBMITTER: Vicens A

PROVIDER: S-EPMC5337896 | biostudies-literature | 2017 Mar

REPOSITORIES: biostudies-literature

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Premammalian origin of the sperm-specific Slo3 channel.

Vicens Alberto A Andrade-López Karla K Cortez Diego D Gutiérrez Rosa María RM Treviño Claudia L CL

FEBS open bio 20170217 3

Slo3 is a sperm-specific potassium (K+) channel essential for male fertility. Slo3 channels have so far been considered to be specific to mammals. Through exploratory genomics, we identified the Slo3 gene in the genome of terrestrial (birds and reptiles) and aquatic (fish) vertebrates. In the case of fish, Slo3 has undergone several episodes of gene loss. Transcriptomic analysis showed that vertebrate Slo3 transcript orthologues are predominantly expressed in testis, in ...[more]

PMID: 28286733

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Project description:Unlike most cells of the body which function in an ionic environment controlled within narrow limits, spermatozoa must function in a less controlled external environment. In order to better understand how sperm control their membrane potential in different ionic conditions, we measured mouse sperm membrane potentials under a variety of conditions and at different external K(+) concentrations, both before and after capacitation. Experiments were undertaken using both wild-type, and mutant mouse sperm from the knock-out strain of the sperm-specific, pH-sensitive, SLO3 K(+) channel. Membrane voltage data were fit to the Goldman-Hodgkin-Katz equation. Our study revealed a significant membrane permeability to both K(+) and Cl(-) before capacitation, as well as Na(+). The permeability to both K(+) and Cl(-) has the effect of preventing large changes in membrane potential when the extracellular concentration of either ion is changed. Such a mechanism may protect against undesired shifts in membrane potential in changing ionic environments. We found that a significant portion of resting membrane potassium permeability in wild-type sperm was contributed by SLO3 K(+) channels. We also found that further activation of SLO3 channels was the essential mechanism producing membrane hyperpolarization under two separate conditions, 1) elevation of external pH prior to capacitation and 2) capacitating conditions. Both conditions produced a significant membrane hyperpolarization in wild-type which was absent in SLO3 mutant sperm. Hyperpolarization in both conditions may result from activation of SLO3 channels by raising intracellular pH; however, demonstrating that SLO3-dependent hyperpolarization is achieved by an alkaline environment alone shows that SLO3 channel activation might occur independently of other events associated with capacitation. For example sperm may undergo stages of membrane hyperpolarization when reaching alkaline regions of the female genital tract. Significantly, other events associated with sperm capacitation, occur in SLO3 mutant sperm and thus proceed independently of hyperpolarization.

Dataset Information

Premammalian origin of the sperm-specific Slo3 channel.

Publications

Premammalian origin of the sperm-specific Slo3 channel.

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