Protein kinases: which one is the memory molecule?

Micheau, Jacques; Riedel, Gernot

doi:10.1007/s000180050312

Cited by 127 publications

(70 citation statements)

References 118 publications

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“…While many studies have suggested the importance of cAMP signaling in associative learning (Micheau and Riedel 1999;Fiel et al 2005;Margulies et al 2005;McGuire et al 2005;Hofmann et al 2006), our results implicate the cGMP signaling pathway in mediating reward learning and memory. Specifically, our results suggest a novel role for the foraging gene in larval learning and memory.…”

Section: Discussioncontrasting

confidence: 49%

Natural variation in Drosophila larval reward learning and memory due to a cGMP-dependent protein kinase

Kaun

Hendel²,

Gerber³

et al. 2007

Learn. Mem.

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Animals must be able to find and evaluate food to ensure survival. The ability to associate a cue with the presence of food is advantageous because it allows an animal to quickly identify a situation associated with a good, bad, or even harmful food. Identifying genes underlying these natural learned responses is essential to understanding this ability. Here, we investigate whether natural variation in the foraging (for) gene in Drosophila melanogaster larvae is important in mediating associations between either an odor or a light stimulus and food reward. We found that for influences olfactory conditioning and that the mushroom bodies play a role in this for-mediated olfactory learning. Genotypes associated with high activity of the product of for, cGMP-dependent protein kinase (PKG), showed greater memory acquisition and retention compared with genotypes associated with low activity of PKG when trained with three conditioning trials. Interestingly, increasing the number of training trials resulted in decreased memory retention only in genotypes associated with high PKG activity. The difference in the dynamics of memory acquisition and retention between variants of for suggests that the ability to learn and retain an association may be linked to the foraging strategies of the two variants.Learned associations such as identifying odors as indicators of food, or showing preferences for food-related odors, are conserved across diverse taxa from humans and mice to slugs, honeybees, and fruit flies (Ache and Young 2005). The fruit fly Drosophila melanogaster can use odors as cues for the presence of both a food reward and an aversive stimulus (Tempel et al. 1983;Scherer et al. 2003;Schwaerzel et al. 2003;Margulies et al. 2005;McGuire et al. 2005;Kim et al. 2007). Identifying genes underlying these natural learned responses is essential to understanding this ability. Here, we use classical reward conditioning to investigate how natural variation in the foraging (for) gene affects acquisition and decay of memory in D. melanogaster larvae.for encodes a cGMP-dependent protein kinase (PKG) (Osborne et al. 1997). In mammals, PKG is important for proper induction of long-term potentiation (LTP) and long-term depression (LTD) (Hartell 1994;Zhuo et al. 1994;Lev-Ram et al. 1997;Arancio et al. 2001;Fiel et al. 2003Fiel et al. , 2005Kleppisch et al. 2003;Hofmann et al. 2006). Although LTP and LTD are thought to be important mechanisms underlying learning and memory (Whitlock et al. 2006), few studies have shown a direct role for PKG in learning and memory. This study aims to do this by investigating how learning differs between allelic variants of for in Drosophila larvae.for is an ideal candidate to study how natural genetic variation can affect learning and memory, since natural for variants exist that have subtle but significant variations in PKG activity (Osborne et al. 1997). The rover variants of for (for R ) have higher for transcript levels and higher PKG activities compared with the sitter variants of for (for s ) (Osb...

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Section: Discussioncontrasting

confidence: 49%

Natural variation in Drosophila larval reward learning and memory due to a cGMP-dependent protein kinase

Kaun

Hendel²,

Gerber³

et al. 2007

Learn. Mem.

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“…The Ca 2+ /CaM-dependent protein kinase II (CaMKII) has been linked to neuronal plasticity associated with long-term potentiation as well as with structural synaptic plasticity (Micheau and Riedel 1999). Previous work in adult honeybees has shown that the single CaMKII gene found in honeybees is strongly expressed in the mushroom bodies (MBs) (Kamikouchi et al 2000), brain centers associated with sensory integration, learning, and memory formation (Giurfa 2007;Giurfa and Sandoz 2012).…”

Section: Experiments 5: Inhibition Of Camkii 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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“…That would be a nice starting point: to look for those substrates. The bad news is that now it's known that PKA and the extracellular signal-regulated kinase system are truly enmeshed, cross-talk a lot with each other, and cross-talk with protein kinase C (PKC) a lot (27).…”

Section: Larry Cahillmentioning

confidence: 99%

The brain decade in debate: I. Neurobiology of learning and memory

Baddeley

Bueno

Cahill³

et al. 2000

Braz J Med Biol Res

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This article is a transcription of an electronic symposium in which some active researchers were invited by the Brazilian Society for Neuroscience and Behavior (SBNeC) to discuss the last decade's advances in neurobiology of learning and memory. The way different parts of the brain are recruited during the storage of different kinds of memory (e.g., short-term vs long-term memory, declarative vs procedural memory) and even the property of these divisions were discussed. It was pointed out that the brain does not really store memories, but stores traces of information that are later used to create memories, not always expressing a completely veridical picture of the past experienced reality. To perform this process different parts of the brain act as important nodes of the neural network that encode, store and retrieve the information that will be used to create memories. Some of the brain regions are recognizably active during the activation of short-term working memory (e.g., prefrontal cortex), or the storage of information retrieved as long-term explicit memories (e.g., hippocampus and related cortical areas) or the modulation of the storage of memories related to emotional events (e.g., amygdala). This does not mean that there is a separate neural structure completely supporting the storage of each kind of memory but means that these memories critically depend on the functioning of these neural structures. The current view is that there is no sense in talking about hippocampusbased or amygdala-based memory since this implies that there is a oneto-one correspondence. The present question to be solved is how systems interact in memory. The pertinence of attributing a critical role to cellular processes like synaptic tagging and protein kinase A activation to explain the memory storage processes at the cellular level was also discussed.

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Protein kinases: which one is the memory molecule?

Cited by 127 publications

References 118 publications

Natural variation in Drosophila larval reward learning and memory due to a cGMP-dependent protein kinase

Natural variation in Drosophila larval reward learning and memory due to a cGMP-dependent protein kinase

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

The brain decade in debate: I. Neurobiology of learning and memory

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