The integrative analysis of microRNA and mRNA expression in <i>Apis mellifera</i> following maze‐based visual pattern learning

Qin, Qiuhong; Wang, Zilong; Tian, Li; Gan, Hui-Li; Zhang, Shao Wu; Zeng, Zhen

doi:10.1111/1744-7917.12065

Cited by 31 publications

(57 citation statements)

References 93 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 . Although these studies did not test their candidate miRNAs for a functional role in learning and memory, their findings nevertheless substantiate our conclusion that there is a robust preconfigured network of miRNAs that regulate memory formation in bees.…”

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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“…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%

“…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. Even though the exact reason for this effect is unknown, the upregulation of microRNAs -repressive regulators of translation -at the same time point (Qin et al, 2014;Cristino et al, 2014) suggests the possibility that regulatory mechanisms could 'over-shoot' when adjusting transcription levels of plastic genes back to baseline.…”

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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Age‐dependent transcriptional and epigenomic responses to light exposure in the honey bee brain

et al. 2016

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Light is a powerful environmental stimulus of special importance in social honey bees that undergo a behavioral transition from in‐hive to outdoor foraging duties. Our previous work has shown that light exposure induces structural neuronal plasticity in the mushroom bodies ( MB s), a brain center implicated in processing inputs from sensory modalities. Here, we extended these analyses to the molecular level to unravel light‐induced transcriptomic and epigenomic changes in the honey bee brain. We have compared gene expression in brain compartments of 1‐ and 7‐day‐old light‐exposed honey bees with age‐matched dark‐kept individuals. We have found a number of differentially expressed genes ( DEG s), both novel and conserved, including several genes with reported roles in neuronal plasticity. Most of the DEG s show age‐related changes in the amplitude of light‐induced expression and are likely to be both developmentally and environmentally regulated. Some of the DEG s are either known to be methylated or are implicated in epigenetic processes suggesting that responses to light exposure are at least partly regulated at the epigenome level. Consistent with this idea light alters the DNA methylation pattern of bgm , one of the DEG s affected by light exposure, and the expression of micro RNA miR‐932 . This confirms the usefulness of our approach to identify candidate genes for neuronal plasticity and provides evidence for the role of epigenetic processes in driving the molecular responses to visual stimulation.

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The integrative analysis of microRNA and mRNA expression in Apis mellifera following maze‐based visual pattern learning

Cited by 31 publications

References 93 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

Age‐dependent transcriptional and epigenomic responses to light exposure in the honey bee brain

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