A sperm-activating peptide controls a cGMP-signaling pathway in starfish sperm.
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 Ca(2+) concentration. In contrast, cAMP levels did not change significantly and the Ca(2+) 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.
Matsumoto
Midori
M
Center for Life Science and Technology, Graduate School of Science and Technology, Keio University, 3-14-1, Hiyoshi Kouhoku, Yokohama 223-8522, Japan. mmatsumo@bio.keio.ac.jp
Solzin
Johannes
J
Helbig
Annika
A
Hagen
Volker
V
Ueno
Sei-ichi
S
Kawase
Osamu
O
Maruyama
Yoshinori
Y
Ogiso
Manabu
M
Godde
Matthias
M
Minakata
Hiroyuki
H
Kaupp
U Benjamin
UB
Hoshi
Motonori
M
Weyand
Ingo
I
D000595:Amino Acid Sequence; D000818:Animals; D002118:Calcium / Q000378:metabolism; D003001:Cloning, Molecular; D006152:Cyclic GMP / Q000378:metabolism*; D018076:DNA, Complementary; D006162:Guanylate Cyclase / Q000187:drug effects / Q000378:metabolism; D008297:Male; D008969:Molecular Sequence Data; D010455:Peptides / Q000235:genetics* / Q000378:metabolism / Q000494:pharmacology*; D017386:Sequence Homology, Amino Acid; D015398:Signal Transduction / Q000502:physiology*; D013082:Sperm Tail / Q000378:metabolism; D013094:Spermatozoa / Q000187:drug effects / Q000378:metabolism*; D013215:Starfish / Q000378:metabolism*; D013737:Testis / Q000502:physiology
D018076:DNA, Complementary; D010455:Peptides; D006162:Guanylate Cyclase; D006152:Cyclic GMP; D002118:Calcium