Expression of Tas1 taste receptors in mammalian spermatozoa

Background: During their transit through the female genital tract,
sperm have to recognize and discriminate numerous chemical
compounds. However, our current knowledge of the molecular identity
of appropriate chemosensory receptor proteins in sperm is still
rudimentary. Considering that members of the Tas1r family of taste
receptors are able to discriminate between a broad diversity of
hydrophilic chemosensory substances, the expression of taste
receptors in mammalian spermatozoa was examined.
Methodology/Principal Findings: The present manuscript documents
that Tas1r1 and Tas1r3, which form the functional receptor for
monosodium glutamate (umami) in taste buds on the tongue, are
expressed in murine and human spermatozoa, where their localization
is restricted to distinct segments of the flagellum and the
acrosomal cap of the sperm head. Employing a Tas1r1-deficient
mCherry reporter mouse strain, we found that Tas1r1 gene deletion
resulted in spermatogenic abnormalities. In addition, a significant
increase in spontaneous acrosomal reaction was observed in Tas1r1
null mutant sperm whereas acrosomal secretion triggered by isolated
zona pellucida or the Ca2+ ionophore A23187 was not different from
wild-type spermatozoa. Remarkably, cytosolic Ca2+ levels in freshly
isolated Tas1r1-deficient sperm were significantly higher compared
to wild-type cells. Moreover, a significantly higher basal cAMP
concentration was detected in freshly isolated Tas1r1-deficient
epididymal spermatozoa, whereas upon inhibition of
phosphodiesterase or sperm capacitation, the amount of cAMP was not
different between both genotypes. Conclusions/Significance: Since
Ca2+ and cAMP control fundamental processes during the sequential
process of fertilization, we propose that the identified taste
receptors and coupled signaling cascades keep sperm in a
chronically quiescent state until they arrive in the vicinity of
the egg - either by constitutive receptor activity and/or by tonic
receptor activation by gradients of diverse chemical compounds in
different compartments of the female reproductive tract.