Calcium-Independent Calcium/Calmodulin-Dependent Protein Kinase II in the Adult<i>Drosophila</i>CNS Enhances the Training of Pheromonal Cues

Mehren, Jennifer E.; Griffith, Leslie C.

doi:10.1523/jneurosci.3560-04.2004

Cited by 39 publications

(55 citation statements)

References 44 publications

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“…For example, to determine which aminergic neurons cause the increase in courtship that we observe, any number of GAL4 drivers that include, but are not absolutely specific for aminergic cells in the CNS may be employed. 11,12,85,86 Finally, we suggest that flies overexpressing DVMAT-A may provide a genetic model for the study of amine-linked changes in motor activity and other complex behavior. Importantly, dopaminergic and serotonergic pathways also play a critical role in regulating motor activity and other stereotypic behavioral patterns of mammals, 87 and in humans, aminergic agents are used in treatment of depression, bipolar disorder, obsessive-compulsive disorder and tic-related disorders such as Tourette's syndrome.…”

Section: Discussionmentioning

confidence: 92%

Overexpression of the Drosophila vesicular monoamine transporter increases motor activity and courtship but decreases the behavioral response to cocaine

Chang¹,

Grygoruk²,

Es³

et al. 2005

Mol Psychiatry

114

134

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Aminergic signaling pathways have been implicated in a variety of neuropsychiatric illnesses, but the mechanisms by which these pathways influence complex behavior remain obscure. Vesicular monoamine transporters (VMATs) have been shown to regulate the amount of monoamine neurotransmitter that is stored and released from synaptic vesicles in mammalian systems, and an increase in their expression has been observed in bipolar patients. The model organism Drosophila melanogaster provides a powerful, but underutilized genetic system for studying how dopamine (DA) and serotonin (5HT) may influence behavior. We show that a Drosophila isoform of VMAT (DVMAT-A) is expressed in both dopaminergic and serotonergic neurons in the adult Drosophila brain. Overexpression of DVMAT-A in these cells potentiates stereotypic grooming behaviors and locomotion and can be reversed by reserpine, which blocks DVMAT activity, and haloperidol, a DA receptor antagonist. We also observe a prolongation of courtship behavior, a decrease in successful mating and a decrease in fertility, suggesting a role for aminergic circuits in the modulation of sexual behaviors. Finally, we find that DMVAT-A overexpression decreases the fly's sensitivity to cocaine, suggesting that the synaptic machinery responsible for this behavior may be downregulated. DVMAT transgenes may be targeted to additional neuronal pathways using standard Drosophila techniques, and our results provide a novel paradigm to study the mechanisms by which monoamines regulate complex behaviors relevant to neuropsychiatric illness.

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Section: Discussionmentioning

confidence: 92%

Overexpression of the Drosophila vesicular monoamine transporter increases motor activity and courtship but decreases the behavioral response to cocaine

Chang¹,

Grygoruk²,

Es³

et al. 2005

Mol Psychiatry

114

134

View full text Add to dashboard Cite

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“…To determine whether courtship suppression during training was sensitive to the absolute level of constitutively active CaMKII, we expressed T287D CaMKII under control of a tripartite GAL4/UAS/ tet-off driver system (Mehren and Griffith 2004). This system allows for both spatial and temporal control of the level of transgene expression.…”

Section: Resultsmentioning

confidence: 99%

“…Males with additional T287D CaMKII begin to suppress courtship immediately without the characteristic lag seen in wild-type animals ( Fig. 1B) (Mehren and Griffith 2004). But in contrast to the effects of T287D dosage on initial courtship, the effects on the trainerspecific component are more graded over the range of doses administered.…”

mentioning

confidence: 91%

Cholinergic neurons mediate CaMKII-dependent enhancement of courtship suppression

Mehren¹,

Griffith²

2006

Learn. Mem.

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In Drosophila, calcium/calmodulin-dependent protein kinase II (CaMKII) activity is crucial in associative courtship conditioning for both memory formation and suppression of courtship during training with a mated female. We have previously shown that increasing levels of constitutively active CaMKII, but not calcium-dependent CaMKII, in a subset of neurons can decrease the initial level of courtship and enhance the rate of suppression of courtship in response to a mated female. In this study, we demonstrate that a subpopulation of noncholinergic, nondopaminergic, non-GABAergic neurons can cause CaMKII-dependent reductions in initial courtship, but only cholinergic neurons enhance training-dependent suppression. These data suggest that processing of pheromonal signals in two subpopulations of neurons, likely antennal lobe projection neurons, is critical for behavioral plasticity.Modification of behavior on short time scales requires fast, likely cell signaling, changes in neuronal circuits. One molecule that has been shown in many systems to be responsible for both short-term and long-term changes in neuronal activity is calcium/calmodulin-dependent protein kinase II (CaMKII). This kinase can act a molecular switch, becoming calcium independent after autophosphorylation at T287. Production of constitutively active kinase is believed to be a first step toward establishing short-and long-term changes in neuronal properties that underlie learning (for review, see Lisman et al. 2002).In Drosophila courtship conditioning, CaMKII is important for behavioral changes that occur during the training period and for formation of associative memory (Griffith et al. 1993; Griffith 1997, 1999). In this behavioral paradigm, a male is exposed to a previously mated female for 1 h, and the effects of training are assessed by measuring courtship of a subsequently presented virgin female. Naive males exposed to virgin females sense female-specific stimulatory pheromones and rapidly initiate courtship, usually copulating within 15 min. In comparison, trained males show reduced courtship of virgins, and this is believed to be the result of association of stimulatory pheromones with an aversive substance given off by mated females (Tompkins et al. 1983). Memory formation can be blocked by inhibition of CaMKII in mushroom bodies, central complex, and parts of the lateral protocerebrum (Joiner and Griffith 1999). The behavior of males during training is also plastic; they initiate vigorous courtship, but over the course of training they decrease their intensity of courtship and rarely copulate. The suppression of courtship during training is driven by a neuronal circuit distinct from that mediating associative memory formation, involving neurons in the antennal lobes and lateral protocerebrum (Joiner and Griffith 1999).The requirement for CaMKII activity was determined using spatially restricted expression of a peptide, which inhibits both the calcium-dependent and the calcium-independent (autophosphorylated at T287) forms of the kinase. ...

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“…In the pond snail Lymnaea stagnalis, for instance, CaMKII is necessary for acquisition and late consolidation, but not early or intermediate consolidation or retrieval of LTM (Wan et al 2010). In Drosophila, CaMKII is necessary for courtship-associated learning and memory (Mehren and Griffith 2004) and for LTM formation following odor-shock pairing (Akalal et al 2010). In the latter case, flies that experienced spaced odor-shock pairings exhibit an increase in calcium influx into a subclass of Kenyon cells, the g neurons, when tested between 18 and 48 h after training.…”

Section: The Role Of Camkii In L-ltm Formation In Honeybeesmentioning

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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Calcium-Independent Calcium/Calmodulin-Dependent Protein Kinase II in the AdultDrosophilaCNS Enhances the Training of Pheromonal Cues

Cited by 39 publications

References 44 publications

Overexpression of the Drosophila vesicular monoamine transporter increases motor activity and courtship but decreases the behavioral response to cocaine

Overexpression of the Drosophila vesicular monoamine transporter increases motor activity and courtship but decreases the behavioral response to cocaine

Cholinergic neurons mediate CaMKII-dependent enhancement of courtship suppression

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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