Gene expression analysis following olfactory learning in Apis mellifera

Wang, Zilong; Wang, Huan; Qin, Qiuhong; Zeng, Zhen

doi:10.1007/s11033-012-2212-9

Cited by 17 publications

(38 citation statements)

References 42 publications

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“…Our findings are in agreement with recent studies that show there is a general downregulation of protein-coding genes and upregulation of miRNAs associated with learning and memory in honeybees 34,35 . These studies report genes involved with cytoskeleton organization, as well as lipid, protein and glucose metabolism are downregulated, and six out of the seven miRNAs reported upregulated in our study after learning were also found upregulated in their work 35 .…”

Section: Discussionsupporting

confidence: 94%

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Neuroligin-associated microRNA-932 targets actin and regulates memory in the honeybee

et al. 2014

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Increasing evidence suggests small non-coding RNAs (ncRNAs) such as microRNAs (miRNAs) control levels of mRNA expression during experience-related remodelling of the brain. Here we use an associative olfactory learning paradigm in the honeybee Apis mellifera to examine gene expression changes in the brain during memory formation. Brain transcriptome analysis reveals a general downregulation of protein-coding genes, including asparagine synthetase and actin, and upregulation of ncRNAs. miRNA-mRNA network predictions together with PCR validation suggest miRNAs including miR-210 and miR-932 target the downregulated protein-coding genes. Feeding cholesterol-conjugated antisense RNA to bees results in the inhibition of miR-210 and of miR-932. Loss of miR-932 impairs long-term memory formation, but not memory acquisition. Functional analyses show that miR-932 interacts with Act5C, providing evidence for direct regulation of actin expression by an miRNA. An activity-dependent increase in miR-932 expression may therefore control actin-related plasticity mechanisms and affect memory formation in the brain.

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Section: Discussionsupporting

confidence: 94%

“…This observation was also made by previous studies using both olfactory 34 and visual 35 learning paradigms in honeybees. Similarly in mammals, there is a pronounced downregulation of gene expression 24 h after long-term-potentiation (LTP) induction, which appears to be partially mediated via timedependent regulation of miRNA expression 45 .…”

Section: Discussionsupporting

confidence: 83%

Neuroligin-associated microRNA-932 targets actin and regulates memory in the honeybee

et al. 2014

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“…Among the DEGs discovered in these studies was a GABA receptor (Qin et al, 2014;Wang et al, 2013). Ionotropic GABA receptors in the MB calyces are crucial for reversal learning, but not extinction or discriminatory learning in general (Boitard et al, 2015).…”

Section: Memory-associated Genesmentioning

confidence: 99%

“…1.2). Changes in gene transcription Menzel et al, 2001;Friedrich et al, 2004;Lefer et al, 2013;Qin et al, 2014;Wang et al, 2013;Cristino et al, 2014), translation Friedrich et al, 2004;Stollhoff et al, 2005) and protein degradation (Felsenberg et al, 2012(Felsenberg et al, , 2014 are all crucial for memory formation. Here I will particularly focus DNA methylation and memory formation in bees on transcription and its role in memory formation.…”

Section: Molecular Mechanisms Of Honey Bee Memory Formationmentioning

confidence: 99%

“…Whole transcriptome approaches established that 24 hours or later after olfactory and visual conditioning the majority of differentially expressed genes (DEGs) are down-regulated (Qin et al, 2014;Wang et al, 2013;Cristino et al, 2014). This suggests that, following the initial transcription waves during the first hours after training (Lefer et al, 2013), the transcription of most genes is restricted again.…”

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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Searching beyond the streetlight: Neonicotinoid exposure alters the neurogenomic state of worker honey bees

Tsvetkov

Zayed

2021

Ecology and Evolution

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Neonicotinoid insecticides have been implicated in honey bee declines, with many studies showing that sublethal exposure impacts bee behaviors such as foraging, learning, and memory. Despite the large number of ecotoxicological studies carried out to date, most focus on a handful of worker phenotypes leading to a “streetlight effect” where the a priori choice of phenotypes to measure may influence the results and conclusions arising from the studies. This bias can be overcome with the use of toxicological transcriptomics, where changes in gene expression can provide a more objective view of how pesticides alter animal traits. Here, we used RNA sequencing to examine the changes in neurogenomic states of nurse and forager honey bees that were naturally exposed to neonicotinoids in the field and artificially exposed to neonicotinoids in a controlled experiment. We found that neonicotinoid exposure influenced the neurogenomic state of foragers and nurses in different ways; foragers experienced shifts in expression of genes involved in cognition and development, while nurses experienced shifts in expression of genes involved in metabolism. Our study suggests that neonicotinoids influence nurse and forager bees in a different manner. We also found no to minimal overlap in the differentially expressed genes in our study and in previously published studies, which might help reconcile the seemingly contradictory results often reported in the neonicotinoid literature.

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Gene expression analysis following olfactory learning in Apis mellifera

Cited by 17 publications

References 42 publications

Neuroligin-associated microRNA-932 targets actin and regulates memory in the honeybee

Neuroligin-associated microRNA-932 targets actin and regulates memory in the honeybee

DNA methylation and the regulation of stimulus-specific memory formation

Searching beyond the streetlight: Neonicotinoid exposure alters the neurogenomic state of worker honey bees

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