A sperm-activating peptide controls a cGMP-signaling pathway in starfish sperm

Midori Matsumoto, Johannes Solzin, Annika Helbig, Volker Hagen, Sei ichi Ueno, Osamu Kawase, Yoshinori Maruyama, Manabu Ogiso, Matthias Godde, Hiroyuki Minakata, U. Benjamin Kaupp, Motonori Hoshi, Ingo Weyand

Research output: Contribution to journalArticle

76 Citations (Scopus)

Abstract

Peptides released from eggs of marine invertebrates play a central role in fertilization. About 80 different peptides from various phyla have been isolated, however, with one exception, their respective receptors on the sperm surface have not been unequivocally identified and the pertinent signaling pathways remain ill defined. Using rapid mixing techniques and novel membrane-permeable caged compounds of cyclic nucleotides, we show that the sperm-activating peptide asterosap evokes a fast and transient increase of the cGMP concentration in sperm of the starfish Asterias amurensis, followed by a transient cGMP-stimulated increase in the Ca2+ concentration. In contrast, cAMP levels did not change significantly and the Ca2+ response evoked by photolysis of caged cAMP was significantly smaller than that using caged cGMP. By cloning of cDNA and chemical crosslinking, we identified a receptor-type guanylyl cyclase in the sperm flagellum as the asterosap-binding protein. Sperm respond exquisitely sensitive to picomolar concentrations of asterosap, suggesting that the peptide serves a chemosensory function like resact, a peptide involved in chemotaxis of sperm of the sea urchin Arbacia punctulata. A unifying principle emerges that chemosensory transduction in sperm of marine invertebrates uses cGMP as the primary messenger, although there may be variations in the detail.

Original languageEnglish
Pages (from-to)314-324
Number of pages11
JournalDevelopmental Biology
Volume260
Issue number2
DOIs
Publication statusPublished - 2003 Aug 15

Keywords

  • Caged compounds
  • Chemotaxis
  • Cyclic nucleotides
  • Kinetic measurements
  • Sperm

ASJC Scopus subject areas

  • Molecular Biology
  • Developmental Biology
  • Cell Biology

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    Matsumoto, M., Solzin, J., Helbig, A., Hagen, V., Ueno, S. I., Kawase, O., Maruyama, Y., Ogiso, M., Godde, M., Minakata, H., Kaupp, U. B., Hoshi, M., & Weyand, I. (2003). A sperm-activating peptide controls a cGMP-signaling pathway in starfish sperm. Developmental Biology, 260(2), 314-324. https://doi.org/10.1016/S0012-1606(03)00236-7