Aquaporins in sperm osmoadaptation: an emerging role for volume regulation

Abstract

Upon ejaculation, mammalian sperm experience a natural osmotic decrease during male to female reproductive tract transition. This hypo-osmotic exposure not only activates sperm motility, but also poses potential harm to sperm structure and function by inducing unwanted cell swelling. In this physiological context, regulatory volume decrease (RVD) is the major mechanism that protects cells from detrimental swelling, and is essential to sperm survival and normal function. Aquaporins are selective water channels that enable rapid water transport across cell membranes. Aquaporins have been implicated in sperm osmoregulation. Recent discoveries show that Aquaporin-3 (AQP3), a water channel protein, is localized in sperm tail membranes and that AQP3 mutant sperm show defects in volume regulation and excessive cell swelling upon physiological hypotonic stress in the female reproductive tract, thereby highlighting the importance of AQP3 in the postcopulatory sperm RVD process. In this paper, we discuss current knowledge, remaining questions and hypotheses about the function and mechanismic basis of aquaporins for volume regulation in sperm and other cell types. Efficient sperm volume regulation is a prerequisite for normal sperm functionIn most mammalian species studied, the journey of sperm from the male to the female reproductive tract experience a natural osmotic decrease [1] , an evolutionary vestige from freshwater fi sh species [2] . Before ejaculation, the mammalian sperm are quiescent in the relatively hypertonic male reproductive tract with no or very low motility. Upon copulation, the sperm enter into the relatively hypotonic female reproductive tract and quickly show motility activation [3,4] , indicating that osmotic changes are beneficial for initial sperm motility activation. However, postcopulatory hypotonic stress also has a negative effects as it induces osmotic cell swelling, which if uncontrolled, can be detrimental to sperm function and survival [5] . Mammalian sperm have evolved to effectively reduce the negative impact of hypotonic cell swelling by means of regulatory volume decrease (RVD), which was proposed to involve efficient volume regulation driven by active solute transport and rapid transmembrane water movement [6] .Functional importance of aquaporins in sperm volume regulation: emerging evidence from AQP3 knockout miceIn the early 1970s, it was demonstrated that the water permeability coefficient of bull spermatozoa was quite high, about four times greater than that of bovine erythrocytes and between ten and thirty times greater than that of artificial bimolecular lipid membranes [7] . According to these observations, the author made an insightful conclusion that the chief route for the passage of water through the sperm membrane must be via "pores" [7] . Similar high water permeability coefficients have been discovered in other mammalian species, including humans [8,9] .In the past two decades, the understanding of the movement of water through cell membranes has been greatly advanced by ...

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