Tyrosine phosphorylation activates surface chaperones facilitating sperm-zona recognition

Kelly L. Asquith, Rosa M. Baleato, Eileen A. McLaughlin, Brett Nixon, R. John Aitken

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Abstract

Mammalian spermatozoa undergo a series of molecular and biochemical changes collectively termed capacitation prior to acquiring the ability to fertilise the oocyte. Although phosphorylation of sperm proteins on tyrosine residues has been recognised as an important component of this process, the precise relationship between the phosphorylation status of mammalian spermatozoa and their capacity for fertilisation has remained unclear. In this study we demonstrate a causal relationship between tyrosine phosphorylation in spermatozoa and sperm-zona interaction. The phosphotyrosine expression associated with sperm capacitation localised to internal flagellar structures in permeabilised cells but could also be detected on the exterior surface of the sperm head in live cells. Importantly, almost all spermatozoa bound to the zona pellucida demonstrated this pattern of phosphoprotein localisation, compared to fewer than 15% of the free-swimming population. These data suggest that tyrosine phosphorylation plays a significant role in remodelling the sperm surface, so that these cells are able to recognise the zona pellucida. Phosphoproteome analysis yielded the first evidence of molecular chaperones, endoplasmin (erp99) and heat shock protein 60 (hsp60), as targets for phosphorylation on the surface of mouse spermatozoa, whereas immunofluorescence localised these proteins to the precise region of the sperm head that participates in zona recognition. Based on these results, we propose a novel mechanism for mammalian gamete interaction whereby the activation of sperm-surface chaperones by tyrosine phosphorylation during capacitation may trigger conformational changes facilitating the formation of a functional zona pellucida receptor complex on the surface of mammalian spermatozoa.

Original languageEnglish
Pages (from-to)3645-3657
Number of pages13
JournalJournal of Cell Science
Volume117
Issue number16
DOIs
Publication statusPublished - 2004
Externally publishedYes

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Asquith, K. L., Baleato, R. M., McLaughlin, E. A., Nixon, B., & Aitken, R. J. (2004). Tyrosine phosphorylation activates surface chaperones facilitating sperm-zona recognition. Journal of Cell Science, 117(16), 3645-3657. https://doi.org/10.1242/jcs.01214