Abstract
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.
Highlights
Fertilization involves the fusion of male and female gametes which is the first step in creating a new individual
We previously showed that the SLO3 sperm-specific, high conductance K+ channel was the key channel involved in membrane hyperpolarization during capacitation [2]
What was unclear was 1) what is the contribution of SLO3 channels relative to other ion channel types to this hyperpolarization? and 2) what is the overall degree to which SLO3 channels are coupled to other capacitation related processes?
Summary
Fertilization involves the fusion of male and female gametes which is the first step in creating a new individual. Sperm must regulate their membrane potential (Em) and adapt to these changes in external ion concentration, while achieving membrane hyperpolarization at appropriate times. We previously showed that the SLO3 sperm-specific, high conductance K+ channel was the key channel involved in membrane hyperpolarization during capacitation [2]. What was unclear was 1) what is the contribution of SLO3 channels relative to other ion channel types to this hyperpolarization? 2) what is the overall degree to which SLO3 channels are coupled to other capacitation related processes? What was unclear was 1) what is the contribution of SLO3 channels relative to other ion channel types to this hyperpolarization? and 2) what is the overall degree to which SLO3 channels are coupled to other capacitation related processes?
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