DNA Methylation Mediates the Discriminatory Power of Associative Long-Term Memory in Honeybees

Biergans, Stephanie; Jones, Julia C.; Treiber, Nadine; Galizia, C. Giovanni; Szyszka, Paul

doi:10.1371/journal.pone.0039349

Cited by 69 publications

(152 citation statements)

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“…Furthermore, stimulus-specific memory changes in a transcription-dependent manner Lefer et al, 2013). These studies are supported by findings that both extinction and stimulus-specific memory are also dependent on transcriptional regulation by DNA methylation (Lockett et al, 2010;Biergans et al, 2012Biergans et al, , 2015.…”

Section: Molecular Mechanisms Of Honey Bee Memory Formationsupporting

confidence: 52%

“…Furthermore memory performance and transcription and translation dependency varies with factors such as age (Ray and Ferneyhough, 1997;Laloi et al, 2001;Behrends et al, 2007), the exact training protocol (Menzel et al, 2001;Lefer et al, 2013) and satiation levels (Friedrich et al, 2004). Interestingly, 24 hour memory has been repeatedly shown to be dependent on epigenetic -transcription regulating -mechanisms in bees (Lockett et al, 2010;Merschbaecher et al, 2012;Biergans et al, 2012Biergans et al, , 2015 (see: section 1.2.4). This suggests that the question of when a transcription-dependent memory is established in bees is more complex than previously thought.…”

Section: Molecular Mechanisms Of Honey Bee Memory Formationmentioning

confidence: 99%

“…Epigenetic mechanisms regulate chromatin structure directly and can change its accessibility, 3D structure and the proteins bound to it. The epigenetic writers Histone acteyltransferases, deacetylases and DNA methyltransferases (Dnmts) are all involved in honey bee memory formation (Lockett et al, 2010;Merschbaecher et al, 2012;Biergans et al, 2012Biergans et al, , 2015.…”

Section: Memory-associated Genesmentioning

confidence: 99%

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DNA methylation and the regulation of stimulus-specific memory formation

Biergans¹

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Memory formation is a crucial task of the brain. It allows animals to dynamically respond to a changing environment by combining information about current and previous experiences. Thus, it promotes complex behaviours such as living in social groups and elaborate foraging tactics. The ability to form memories is present across the animal kingdom in a variety of forms. The honeybee -an eusocial insect -is capable of both 'simple' associative and complex rule learning. Despite decades of research into the mechanisms of memory formation, however, much remains unknown.One little-understood aspect is the regulation of molecular mechanisms during memory formation.Understanding regulation of transcription is particularly important in this context, as transcription is a requirement for any stable memory. Epigenetic mechanisms regulate transcription by directly interacting with chromatin. Importantly, epigenetic mechanisms are conserved across species as distinct as humans and honeybees. This thesis aims to investigate one particular epigenetic mechanism -DNA methylation -and its role in honey bee memory formation by using behavioural, physiological and molecular assays.First, I studied the role of DNA methyltransferases (Dnmts), which catalyse DNA methylation, after olfactory reward learning. Bees were trained to associate an odour with a sugar reward. Dnmts were then blocked after conditioning using a pharmacological inhibitor. 24 hours later, bees were tested for memory retention and generalisation. Dnmt inhibition increased the generalisation to an odour that was not present during the training, thus impairing stimulus-specific memory. This effect was learning-dependent, as bees' response to odours or sugar water alone did not change after treatment. Furthermore, this effect was robust against alterations in the training paradigm, but the directionality depended on the number of training trials. Next, I used Ca2+ -imaging of the bees' primary olfactory centre (i.e. antennal lobe, AL) to investigate whether Dnmts affect changes in AL processing established during memory formation. The AL is involved in odour discrimination and olfactory learning; both processes are also crucial for stimulus-specific memory formation. If Dnmts were inhibited after olfactory reward learning, the AL response to a new odour changed 48 hours later. This effect potentially serves as a functional explanation for the behavioural phenotype observed after Dnmt inhibition. Furthermore, this study provides the first in vivo evidence for Dnmt-mediated regulation of neuronal networks during memory formation.As DNA methylation regulates transcription, I next investigated the effect of Dnmt inhibition on gene expression. Using qPCR I studied 30 memory-associated genes. In response to Dnmt inhibition, 9 genes were upregulated after conditioning. For some of these genes I then investigated their i methylation patterns using a bisulfite conversion based Mass spectrometry approach. Memory formation changed the methylation pattern compared to both...

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Section: Molecular Mechanisms Of Honey Bee Memory Formationsupporting

confidence: 52%

Section: Molecular Mechanisms Of Honey Bee Memory Formationmentioning

confidence: 99%

Section: Memory-associated Genesmentioning

confidence: 99%

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DNA methylation and the regulation of stimulus-specific memory formation

Biergans¹

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“…In insects, such as honey bees, DNA methyltransferase activity (Wang et al, 2006) is crucial for memory formation (Biergans et al, 2012(Biergans et al, , 2015. DNA methylation also plays a role in the preservation of long term vertebrate memories.…”

Section: Introductionmentioning

confidence: 99%

“…Miller et al (2010) showed that rat long term memory (30 days after training) was disrupted by zeb. In invertebrates, such epigenetic mechanisms are also necessary for learning and memory (Lockett et al, 2010;Biergans et al, 2012Biergans et al, , 2015. Thus, DNA methylation is likely an ancestral and conserved mechanism of memory formation.…”

Section: Introductionmentioning

confidence: 99%

Inhibiting DNA methylation alters olfactory extinction but not acquisition learning in Apis cerana and Apis mellifera

Gong

Wang

Nieh

et al. 2016

Journal of Insect Physiology

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a b s t r a c t DNA methylation plays a key role in invertebrate acquisition and extinction memory. Honey bees have excellent olfactory learning, but the role of DNA methylation in memory formation has, to date, only been studied in Apis mellifera. We inhibited DNA methylation by inhibiting DNA methyltransferase (DNMT) with zebularine (zeb) and studied the resulting effects upon olfactory acquisition and extinction memory in two honey bee species, Apis cerana and A. mellifera. We used the proboscis extension reflex (PER) assay to measure memory. We provide the first demonstration that DNA methylation is also important in the olfactory extinction learning of A. cerana. DNMT did not reduce acquisition learning in either species. However, zeb bidirectionally and differentially altered extinction learning in both species. In particular, zeb provided 1 h before acquisition learning improved extinction memory retention in A. mellifera, but reduced extinction memory retention in A. cerana. The reasons for these differences are unclear, but provide a basis for future studies to explore species-specific differences in the effects of methylation on memory formation.

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Exploring the Roles of Genetics and the Epigenetic Mechanism DNA Methylation in Honey Bee ( Apis Mellifera ) Behavior

Burden

Bobek

2017

Handbook of Neurobehavioral Genetics and Phenotyping

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DNA Methylation Mediates the Discriminatory Power of Associative Long-Term Memory in Honeybees

Cited by 69 publications

References 51 publications

DNA methylation and the regulation of stimulus-specific memory formation

DNA methylation and the regulation of stimulus-specific memory formation

Inhibiting DNA methylation alters olfactory extinction but not acquisition learning in Apis cerana and Apis mellifera

Exploring the Roles of Genetics and the Epigenetic Mechanism DNA Methylation in Honey Bee ( Apis Mellifera ) Behavior

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