Modulation of L-type Calcium Channels in Drosophila via a Pituitary Adenylyl Cyclase-activating Polypeptide (PACAP)-mediated Pathway

Bhattacharya, Anindya; Lakhman, Sukhwinder S.; Singh, Satpal

doi:10.1074/jbc.m403819200

Cited by 41 publications

(28 citation statements)

References 55 publications

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“…3A). Animals injected with 1 mM DDA (Wenzel et al 2002;Bhattacharya et al 2004) or 1 mM SQ22536 (Zhang et al 1999;Heinrich et al 2001), an adenylyl cyclase inhibitor, also exhibited normal retention at 30 min, but exhibited a complete decay of memory at 3 h after conditioning (Fig. 3B).…”

Section: Impairment Of Ltm Formation By Inhibitors Of the No-cgmp Or mentioning

confidence: 95%

Critical role of nitric oxide-cGMP cascade in the formation of cAMP-dependent long-term memory

Matsumoto

Unoki²,

Aonuma³

et al. 2006

Learn. Mem.

106

140

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Cyclic AMP pathway plays an essential role in formation of long-term memory (LTM). In some species, the nitric oxide (NO)-cyclic GMP pathway has been found to act in parallel and complementary to the cAMP pathway for LTM formation. Here we describe a new role of the NO-cGMP pathway, namely, stimulation of the cAMP pathway to induce LTM. We have studied the signaling cascade underlying LTM formation by systematically coinjecting various "LTM-inducing" and "LTM-blocking" drugs in crickets. Multiple-trial olfactory conditioning led to LTM that lasted for several days, while memory induced by single-trial conditioning decayed away within several hours. Injection of inhibitors of the enzyme forming NO, cGMP, or cAMP into the hemolymph prior to multiple-trial conditioning blocked LTM, whereas injection of an NO donor, cGMP analog, or cAMP analog prior to single-trial conditioning induced LTM. Induction of LTM by injection of an NO donor or cGMP analog paired with single-trial conditioning was blocked by inhibitors of the cAMP pathway, but induction of LTM by a cAMP analog was unaffected by inhibitors of the NO-cGMP pathway. Inhibitors of cyclic nucleotide-gated channel (CNG channel) or calmodulin-blocked induction of LTM by cGMP analog paired with single-trial conditioning, but they did not affect induction of LTM by cAMP analog. Our findings suggest that the cAMP pathway is a downstream target of the NO-cGMP pathway for the formation of LTM, and that the CNG channel and calcium-calmodulin intervene between the NO-cGMP pathway and the cAMP pathway.In both vertebrates and invertebrates, nervous systems store information for short-term memory (STM) and long-term memory (LTM) by changing the strength of their synaptic connections (Kandel 2001). Studies in many species, including mollusca Aplysia, fruitflies Drosophila, and mice, suggest that STM storage is accompanied by transient changes in the strength of synaptic connections by covalent modifications of pre-existing proteins and that LTM storage, in contrast, is accompanied by enduring changes in synaptic strength that require transcription and translation of genes (Montarolo et al. 1986;DeZazzo and Tully 1995). In all of these species, formation of LTM requires an increase in intracellular cAMP and recruitment of the cAMP-dependent protein kinase (PKA) that phosphorylates the transcription factor, cAMP-responsive element-binding protein (CREB) (Bartsch et al. 1995;Yin et al. 1995;Abel et al. 1997).The roles of the cAMP pathway in the formation of LTM are often supplemented by other signaling pathways, most notably by the nitric oxide (NO)-cGMP signaling pathway (Lewin and Walters 1999;Lu et al. 1999). NO is a membrane-permeable molecule that functions in intercellular signaling in the brain (Garthwaite et al. 1988). In mice, NO contributes to late-phase longterm potentiation of synaptic transmission by stimulating soluble guanylate cyclase in target cells, and the resulting increase in cGMP concentration stimulates cGMP-dependent protein kinase (PKG), which acts in p...

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Section: Impairment Of Ltm Formation By Inhibitors Of the No-cgmp Or mentioning

confidence: 95%

Critical role of nitric oxide-cGMP cascade in the formation of cAMP-dependent long-term memory

Matsumoto

Unoki²,

Aonuma³

et al. 2006

Learn. Mem.

106

140

View full text Add to dashboard Cite

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“…In Drosophilia, mutations in the amnesiac gene, which encodes a peptide homologous to human PACAP, reduce the L-type current in larval muscles (42). Store-operated calcium influx channels in human myeloid cells resemble L-type calcium channel lacking a voltage sensor (43).…”

Section: Discussionmentioning

confidence: 99%

Differential Calcium Regulation of Proinflammatory Activities in Human Neutrophils Exposed to the Neuropeptide Pituitary Adenylate Cyclase-Activating Protein

Harfi

Corazza

D’Hondt

et al. 2005

The Journal of Immunology

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The neuropeptide pituitary adenylate cyclase-activating protein (PACAP) acts via the G protein-coupled receptor vasoactive intestinal peptide/PACAP receptor-1 to induce phospholipase C/calcium and MAPK-dependent proinflammatory activities in human polymorphonuclear neutrophils (PMNs). In this study, we evaluate other mechanisms that regulate PACAP-evoked calcium transients, the nature of the calcium sources, and the role of calcium in proinflammatory activities. Reduction in the activity of PMNs to respond to PACAP was observed after cell exposure to inhibitors of the cAMP/protein kinase A, protein kinase C, and PI3K pathways, to pertussis toxin, genistein, and after chelation of intracellular calcium or after extracellular calcium depletion. Mobilization of intracellular calcium stores was based on the fact that PACAP-associated calcium transient was decreased after exposure to 1) thapsigargin, 2) Xestospongin C, and 3) the protonophore carbonyl cyanide 4-(trifluoromethoxy) phenyl hydrazone; inhibition of calcium increase by calcium channel blockers, by nifedipine and verapamil, indicated that PACAP was also acting on calcium influx. Such mobilization was not dependent on a functional actin cytoskeleton. Homologous desensitization with nanomoles of PACAP concentration and heterologous receptors desensibilization by G protein-coupled receptor agonists were observed. Intracellular calcium depletion modulated PACAP-associated ERK but not p38 phosphorylation; in contrast, extracellular calcium depletion modulated PACAP-associated p38 but not ERK phosphorylation. In PACAP-treated PMNs, reactive oxygen species production and CD11b membrane up-regulation in contrast to lactoferrin release were dependent on both intra- and extracellular calcium, whereas matrix metalloproteinase-9 release was unaffected by extracellular calcium depletion. These data indicate that both extracellular and intracellular calcium play key roles in PACAP proinflammatory activities.

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“…However, whether direct inhibition of AC affects honeybee learning and memory remains to be determined. In order to study the implication of AC in olfactory acquisition and 3-d retention, we injected bees 20 min before training with saline (n ¼ 100) or with 2 ′ ,5 ′ -dideoxyadenosine (DDA), a P-site specific AC inhibitor (Bhattacharya et al 2004). DDA was injected at three different concentrations, 0.5 mM (n ¼ 65), 1 mM (n ¼ 66), and 5 mM (n ¼ 69).…”

Section: Experiments 6: Inhibition Of Ac Impairs L-ltm Retentionmentioning

confidence: 99%

Cyclic nucleotide–gated channels, calmodulin, adenylyl cyclase, and calcium/calmodulin-dependent protein kinase II are required for late, but not early, long-term memory formation in the honeybee

et al. 2014

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Memory is a dynamic process that allows encoding, storage, and retrieval of information acquired through individual experience. In the honeybee Apis mellifera, olfactory conditioning of the proboscis extension response (PER) has shown that besides short-term memory (STM) and mid-term memory (MTM), two phases of long-term memory (LTM) are formed upon multiple-trial conditioning: an early phase (e-LTM) which depends on translation from already available mRNA, and a late phase (l-LTM) which requires de novo transcription and translation. Here we combined olfactory PER conditioning and neuropharmacological inhibition and studied the involvement of the NO-cGMP pathway, and of specific molecules, such as cyclic nucleotide-gated channels (CNG), calmodulin (CaM), adenylyl cyclase (AC), and Ca 2+ /calmodulin-dependent protein kinase (CaMKII), in the formation of olfactory LTM in bees. We show that in addition to NO-cGMP and cAMP-PKA, CNG channels, CaM, AC, and CaMKII also participate in the formation of a l-LTM (72-h post-conditioning) that is specific for the learned odor. Importantly, the same molecules are dispensable for olfactory learning and for the formation of both MTM (in the minute and hour range) and e-LTM (24-h post-conditioning), thus suggesting that the signaling pathways leading to l-LTM or e-LTM involve different molecular actors.

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Modulation of L-type Calcium Channels in Drosophila via a Pituitary Adenylyl Cyclase-activating Polypeptide (PACAP)-mediated Pathway

Cited by 41 publications

References 55 publications

Critical role of nitric oxide-cGMP cascade in the formation of cAMP-dependent long-term memory

Critical role of nitric oxide-cGMP cascade in the formation of cAMP-dependent long-term memory

Differential Calcium Regulation of Proinflammatory Activities in Human Neutrophils Exposed to the Neuropeptide Pituitary Adenylate Cyclase-Activating Protein

Cyclic nucleotide–gated channels, calmodulin, adenylyl cyclase, and calcium/calmodulin-dependent protein kinase II are required for late, but not early, long-term memory formation in the honeybee

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