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

Cristino, Alexandre S.; Barchuk, Angel Roberto; Freitas, Flávia Cristina de Paula; Narayanan, Ramesh; Biergans, Stephanie; Zhao, Zhengyang; Simões, Zilá Luz Paulino; Reinhard, Judith; Claudianos, Charles

doi:10.1038/ncomms6529

Cited by 71 publications

(111 citation statements)

References 70 publications

(103 reference statements)

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“…The capacity of honeybees to learn how to reach food sources and communicate that knowledge to conspecifics makes them powerful models to understand the basis of cognition (Chittka and Niven 2009;Menzel 2012). Moreover, their small, plastic, and versatile brain allows researchers to trace the routes of memory formation at cellular and molecular levels (Menzel 2014;Cristino et al 2014;Haberkern and Jayaraman 2016). Thus, it is worth noting here some of the general aspects of honeybee brain biology.…”

Section: Honeybee Diphenism and Caste Differentiationmentioning

confidence: 99%

The ontogenetic saga of a social brain

et al. 2017

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-Queen and worker honeybees differ in a number of life-history traits, including the size of certain brain regions, such as the mushroom bodies (MBs), which are larger in workers. However, during the larval period, the differential feeding offered to queens promotes faster brain development. As a result, members of this caste have larger brains than workers. This developmental process is accompanied by the higher expression of several neurogenic genes. Nonetheless, a caste-specific shift in relative brain growth occurs during the next developmental stage. The suggested molecular underpinnings of this phenomenon are variations in hormonal environments, which may mediate higher cell death rates in the queen's brain than in the workers'. The brain development of this highly eusocial bee is thus a paradoxical case that may represent an evolutionary by-product of the reproductive division of labour in species with female size diphenism.Apis mellifera / honey bee / development / caste / phenotypic plasticity

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Section: Honeybee Diphenism and Caste Differentiationmentioning

confidence: 99%

The ontogenetic saga of a social brain

et al. 2017

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“…In Drosophila, miR-932 can specifically target Hh coreceptor Boi to modulate hedgehog signaling (Gao et al 2013). And in the honeybee Apis mellifera, miR-932 can affect the memory by controlling actinrelated plasticity mechanisms (Cristino et al 2014). In this study, we find that the miR-932-mimic-injected mosquitoes become more resistant to deltamethrin, while the miR-932-inhibitor-injected mosquitoes become more susceptible to deltamethrin, suggesting that miR-932 participates in the regulation of pyrethroid resistance.…”

Section: Discussionmentioning

confidence: 99%

MiR-932 Regulates Pyrethroid Resistance inCulex pipiens pallens(Diptera: Culicidae)

Liu¹,

Tian²,

Guo³

et al. 2016

J Med Entomol

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MicroRNAs (miRNAs) play notable role in regulation of gene expression at the posttranscription level, and have been involved in many biological processes, including insecticide resistance. In this study, we investigated the role of miR-932 in the molecular mechanisms of pyrethroid resistance in Culex pipiens pallens (L.). Overexpression of miR-932 in the DS-strain made the mosquitoes more resistant to deltamethrin, while inhibiting the expression of miR-932 in the DR-strain made the mosquitoes more sensitive to deltamethrin. Further, we also identified CpCPR5 as a target gene of miR-932. Sustained overexpression of miR-932 resulted in repression of CpCPR5, and that knockdown of miR-932 increased CpCPR5 expression. In addition, knockdown of CpCPR5 decreased the sensitivity of mosquitoes to deltamethrin in the DS-strain. In conclusion, our study finds a molecular link between miR-932 and CpCPR5 and provides a novel insight into the mechanism of insecticide resistance.Key words: Culex pipiens pallens, pyrethroid, microRNA, CpCPR5Mosquitoes transmit a lot of pathogens, causing severe diseases such as malaria, dengue fever, West Nile fever, encephalitis, and filariasis, which threat public health worldwide (Andriessen et al. 2015, Fortuna et al. 2015, Paredes-Esquivel et al. 2015. Recent estimates show that there are about 400 million infections of dengue fever annually around the world (Sood et al. 2015). According to the WHO world malaria report, there are still 214 million new infections worldwide in 2015. Therefore, it is imperative for controlling and preventing mosquito-borne diseases. However, due to the lack of effective vaccines and drugs, vector control mostly relies on insecticides to reduce the number of mosquitoes (Glunt et al. 2015). But continuous and lasting application of insecticides has led to a constant increasing resistance, which makes antivector strategies more challenging (Rasic et al. 2015). Insecticide resistance arises from complex polygenic inheritance and many genes involved , Bonizzoni et al. 2015. These genes can be regulated at transcriptional and posttranscriptional levels and microRNA (miRNA) is known to be a posttranscriptional gene regulator (Wang et al. 2016).MiRNA is a class of small noncoding RNA, with about 22 nucleotides in length. It has been shown to repress translation via imperfectly pairing with complementary sites within the 3'UTR of target mRNA (Liu et al. 2014, Munoz et al. 2015. In diverse cellular programs, miRNA plays a key role and involves in cell growth, differentiation, apoptosis, and many other physiological processes , Park et al. 2015. In insects, the studies on miRNAs are mostly focused on the development, behavior, and hostpathogen interactions (Lucas et al. 2015). Recent evidence has shown that a few miRNAs participate in the regulation of insecticide resistance in mosquitoes, but the exact role of miRNA in pyrethroid resistance is still under little attention yet .Here, according to our previous study, we identified many different expressed miRNAs...

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“…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%

“…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%

“…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%

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

Cited by 71 publications

References 70 publications

The ontogenetic saga of a social brain

The ontogenetic saga of a social brain

MiR-932 Regulates Pyrethroid Resistance inCulex pipiens pallens(Diptera: Culicidae)

DNA methylation and the regulation of stimulus-specific memory formation

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