Neuronal cAMP-dependent protein kinase type II is concentrated in mushroom bodies ofDrosophila melanogaster and the honeybeeApis mellifera

Müller, Uli

doi:10.1002/(sici)1097-4695(199707)33:1<33::aid-neu4>3.0.co;2-e

Cited by 73 publications

(55 citation statements)

References 35 publications

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“…5b). Using antibodies against the PKA type II, which accounts for ϳ90% of the total PKA activity in the bee brain (Müller, 1997), we detected no difference in the amount of PKA between animals with different satiation status (optical lobes: t test, p ϭ 0.26; central brain: t test, p ϭ 0.96) (Fig. 5c).…”

Section: Feeding Status But Not Sucrose Responsiveness Affects the mentioning

confidence: 88%

“…The remaining binding sites of the microtiter were blocked for 1.5 hr with PBS containing 0.5% BSA. Primary antibodies against the regulatory subunit II of PKA (Müller, 1997(Müller, , 2002 were incubated overnight at 4°C in PBS, 0.5% BSA. After incubation with biotinylated anti-mouse antibody (2 hr, 20°C) and avidinalkaline phosphatase (1 hr, 20°C), the conversion of o-nitro phenyl phosphate was measured with an ELISA reader at 405 nm (vs 620 nm background).…”

Section: Methodsmentioning

confidence: 99%

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Learning at Different Satiation Levels Reveals Parallel Functions for the cAMP–Protein Kinase A Cascade in Formation of Long-Term Memory

Friedrich¹,

Thomas²,

Müller³

2004

J. Neurosci.

100

105

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Learning and memory formation in intact animals is generally studied under defined parameters, including the control of feeding. We used associative olfactory conditioning of the proboscis extension response in honeybees to address effects of feeding status on processes of learning and memory formation. Comparing groups of animals with different but defined feeding status at the time of conditioning reveals new and characteristic features in memory formation. In animals fed 18 hr earlier, three-trial conditioning induces a stable memory that consists of different phases: a mid-term memory (MTM), translation-dependent early long-term memory (eLTM; 1–2 d), and a transcription-dependent late LTM (lLTM; ≥3 d). Additional feeding of a small amount of sucrose 4 hr before conditioning leads to a loss of all of these memory phases. Interestingly, the basal activity of the cAMP-dependent protein kinase A (PKA), a key player in LTM formation, differs in animals with different satiation levels. Pharmacological rescue of the low basal PKA activity in animals fed 4 hr before conditioning points to a specific function of cAMP–PKA cascade in mediating satiation-dependent memory formation. An increase in PKA activity during conditioning rescues only transcription-dependent lLTM; acquisition, MTM, and eLTM are still impaired. Thus, during conditioning, the cAMP–PKA cascade mediates the induction of the transcription-dependent lLTM, depending on the satiation level. This result provides the first evidence for a central and distinct function of the cAMP–PKA cascade connecting satiation level with learning.

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Section: Feeding Status But Not Sucrose Responsiveness Affects the mentioning

confidence: 88%

Section: Methodsmentioning

confidence: 99%

Learning at Different Satiation Levels Reveals Parallel Functions for the cAMP–Protein Kinase A Cascade in Formation of Long-Term Memory

Friedrich¹,

Thomas²,

Müller³

2004

J. Neurosci.

100

105

View full text Add to dashboard Cite

show abstract

“…This will be of special importance, because, in contrast to the extensive knowledge of mushroom body function in Drosophila learning (Davis, 2005), there is only little information on signaling cascades critical for learning and memory formation in the honeybee mushroom bodies. Although the cAMP-dependent protein kinase A (PKA), a central player in LTM formation throughout the animal kingdom, shows a high expression in Drosophila and honeybee mushroom bodies (Müller, 1997), its role in mushroom bodies has been demonstrated convincingly only in Drosophila. In contrast, in the honeybee, the PKA activity in the antennal lobes, another brain area implicated in associative olfactory learning (Hammer and Menzel, 1998), has been demonstrated to be required for induction of late-memory phases (Mül-ler, 2000).…”

Section: Discussionmentioning

confidence: 99%

Focal and Temporal Release of Glutamate in the Mushroom Bodies Improves Olfactory Memory inApis mellifera

Locatelli

Bundrock²,

Müller³

2005

J. Neurosci.

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In contrast to vertebrates, the role of the neurotransmitter glutamate in learning and memory in insects has hardly been investigated. The reason is that a pharmacological characterization of insect glutamate receptors is still missing; furthermore, it is difficult to locally restrict pharmacological interventions. In this study, we overcome these problems by using locally and temporally defined photo-uncaging of glutamate to study its role in olfactory learning and memory formation in the honeybee, Apis mellifera. Uncaging glutamate in the mushroom bodies immediately after a weak training protocol induced a higher memory rate 2 d after training, mimicking the effect of a strong training protocol. Glutamate release before training does not facilitate memory formation, suggesting that glutamate mediates processes triggered by training and required for memory formation. Uncaging glutamate in the antennal lobes shows no effect on memory formation. These results provide the first direct evidence for a temporally and locally restricted function of glutamate in memory formation in honeybees and insects.

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“…NOS activity is detected in the optic lobes, the mushroom bodies, the central body complex, the lateral protocerebral lobes, and the antennal lobes (Watanabe et al 2007), and PKA activity is increased in a NO-dependent manner in the ALs following multiple-trial olfactory learning (Müller 2000). Higher levels of immunoreactivity for type-II PKA (PKAII) can be found in the MBs compared to other neuropiles (Müller 1997). Accordingly, the gene of a PKA catalytic subunit is predominantly expressed in the MBs (Eisenhardt et al 2001).…”

Section: Molecular Actors and Brain Regions In The Honeybeementioning

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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Neuronal cAMP-dependent protein kinase type II is concentrated in mushroom bodies ofDrosophila melanogaster and the honeybeeApis mellifera

Cited by 73 publications

References 35 publications

Learning at Different Satiation Levels Reveals Parallel Functions for the cAMP–Protein Kinase A Cascade in Formation of Long-Term Memory

Learning at Different Satiation Levels Reveals Parallel Functions for the cAMP–Protein Kinase A Cascade in Formation of Long-Term Memory

Focal and Temporal Release of Glutamate in the Mushroom Bodies Improves Olfactory Memory inApis mellifera

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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