Stimulation of the cAMP system by the nitric oxide-cGMP system underlying the formation of long-term memory in an insect.
The nitric oxide (NO)-cGMP signaling system and cAMP system play critical roles in the formation of multiple-trial induced, protein synthesis-dependent long-term memory (LTM) in many vertebrates and invertebrates. The relationship between the NO-cGMP system and cAMP system, however, remains controversial. In honey bees, the two systems have been suggested to converge on protein kinase A (PKA), based on the finding in vitro that cGMP activates PKA when sub-optimal dose of cAMP is present. In crickets, however, we have suggested that NO-cGMP pathway operates on PKA via activation of adenylyl cyclase and production of cAMP for LTM formation. To resolve this issue, we compared the effect of multiple-trial conditioning against the effect of an externally applied cGMP analog for LTM formation in crickets, in the presence of sub-optimal dose of cAMP analog and in condition in which adenylyl cyclase was inhibited. The obtained results suggest that an externally applied cGMP analog activates PKA when sub-optimal dose of cAMP analog is present, as is suggested in honey bees, but cGMP produced by multiple-trial conditioning cannot activate PKA even when sub-optimal dose of cAMP analog is present, thus indicating that cGMP produced by multiple-trial conditioning is not accessible to PKA. We conclude that the NO-cGMP system stimulates the cAMP system for LTM formation. We propose that LTM is formed by an interplay of two classes of neurons, namely, NO-producing neurons regulating LTM formation and NO-receptive neurons that are more directly involved in the formation of long-term synaptic plasticity underlying LTM formation.
Matsumoto
Yukihisa
Y
Graduate School of Life Science, Hokkaido University, Kita 10, Nishi 8, Kita-ku, Sapporo 060-0810, Japan.
Hatano
Ai
A
Unoki
Sae
S
Mizunami
Makoto
M
D000067956:Adenylyl Cyclase Inhibitors; D000818:Animals; D003994:Bucladesine / Q000494:pharmacology; D003214:Conditioning, Classical; D003216:Conditioning, Operant; D000242:Cyclic AMP / Q000502:physiology*; D017868:Cyclic AMP-Dependent Protein Kinases / Q000037:antagonists & inhibitors / Q000502:physiology; D006152:Cyclic GMP / Q000031:analogs & derivatives / Q000494:pharmacology / Q000502:physiology*; D016048:Dideoxyadenosine / Q000031:analogs & derivatives / Q000494:pharmacology; D004789:Enzyme Activation; D006135:Gryllidae / Q000502:physiology*; D008297:Male; D008568:Memory / Q000187:drug effects / Q000502:physiology; D009569:Nitric Oxide / Q000502:physiology*
D000067956:Adenylyl Cyclase Inhibitors; C016276:8-bromocyclic GMP; D009569:Nitric Oxide; D016048:Dideoxyadenosine; D003994:Bucladesine; C021008:2',5'-dideoxyadenosine; D000242:Cyclic AMP; D017868:Cyclic AMP-Dependent Protein Kinases; D006152:Cyclic GMP