Due to their transcriptionally and translationally suppressed state, spermatozoa are reliant on post translational modifications to drive the generation of new proteoforms, such as phosphorylated proteins, that support their function and survival. Importantly, during transit of the female reproductive tract (termed capacitation), sperm fertilisation competency is established through phosphorylation-mediated signalling. With some kinases considered synonymous with successful sperm capacitation (e.g. protein kinase A), protein phosphorylation forms a dynamic and essential component of the fertilisation cascade. Despite the fundamental nature of phosphorylation to sperm function and fertility, a comprehensive analysis of the phosphoproteomic landscape of capacitating human spermatozoa has yet to be reported.
To characterise the phosphorylation events underpinning human sperm capacitation we performed EasyPhos phosphopeptide enrichment and high-resolution tandem mass spectrometry to quantify protein phosphorylation events in non-capacitated and capacitated human sperm. This strategy successfully identified 2,350 site specific phosphorylation events mapped across 902 unique sperm proteins. In congruence with previous findings indicating the importance of tyrosine phosphorylation to fertilisation, a 2-fold increase (representing a 104% gain) in tyrosine phosphorylated sites was observed following capacitation, compared to a modest 5% gain in the phosphorylation of serine residues under the same conditions. Mapping of phospho-residues to upstream kinases revealed a suite of novel sperm kinases with unexplored functions. Of particular interest, pharmacological inhibition of one of these targets, polo-like kinase 1 (PLK1), hampered sperm progressive motility and prevented tyrosine phosphorylation in human sperm. In vitro validation of these results in mice confirmed equivalent outcomes. These findings provide credence for in vivo proof of concept studies substantiating the utility of PLK1 as a potential non-hormonal contraceptive target.