A K+-selective cGMP-gated ion channel controls chemosensation of sperm.
Eggs attract sperm by chemical factors, a process called chemotaxis. Sperm from marine invertebrates use cGMP signalling to transduce incident chemoattractants into changes in the Ca2+ concentration in the flagellum, which control the swimming behaviour during chemotaxis. The signalling pathway downstream of the synthesis of cGMP by a guanylyl cyclase is ill-defined. In particular, the ion channels that are involved in Ca2+ influx and their mechanisms of gating are not known. Using rapid voltage-sensitive dyes and kinetic techniques, we record the voltage response that is evoked by the chemoattractant in sperm from the sea urchin Arbacia punctulata. We show that the chemoattractant evokes a brief hyperpolarization followed by a sustained depolarization. The hyperpolarization is caused by the opening of K+-selective cyclic-nucleotide-gated (CNG) channels in the flagellum. Ca2+ influx commences at the onset of recovery from hyperpolarization. The voltage threshold of Ca2+ entry indicates the involvement of low-voltage-activated Ca(v) channels. These results establish a model of chemosensory transduction in sperm whereby a cGMP-induced hyperpolarization opens Ca(v) channels by a 'recovery-from-inactivation' mechanism and unveil an evolutionary kinship between transduction mechanisms in sperm and photoreceptors.
Strünker
Timo
T
Institut für Neurowissenschaft und Biophysik, Abteilung Zelluläre Signalverarbeitung, INB-1, Forschungszentrum Jülich, 52425 Jülich, Germany.
Weyand
Ingo
I
Bönigk
Wolfgang
W
Van
Qui
Q
Loogen
Astrid
A
Brown
Joel E
JE
Kashikar
Nachiket
N
Hagen
Volker
V
Krause
Eberhard
E
Kaupp
U Benjamin
UB
D000818:Animals; D047308:Arbacia / Q000737:chemistry; D002118:Calcium / Q000378:metabolism; D020013:Calcium Signaling / Q000502:physiology*; D002633:Chemotaxis; D006152:Cyclic GMP / Q000378:metabolism*; D006162:Guanylate Cyclase / Q000378:metabolism; D015640:Ion Channel Gating; D007473:Ion Channels; D008297:Male; D011188:Potassium / Q000378:metabolism*; D015398:Signal Transduction; D013094:Spermatozoa / Q000378:metabolism*
D007473:Ion Channels; D006162:Guanylate Cyclase; D006152:Cyclic GMP; D011188:Potassium; D002118:Calcium