Regulation of physiological processes by microRNAs in insects

Lucas, Keira J.; Zhao, Bo; Liu, Shiping; Raikhel, Alexander S.

doi:10.1016/j.cois.2015.06.004

Cited by 65 publications

(44 citation statements)

References 63 publications

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“…An important innovation that explains most of the insect evolutionary success has been the holometabolan metamorphosis, by which the juvenile stages can adopt a body plan very different from that of the adult, thus allowing the exploitation of new resources8. Recent reviews emphasize the importance that miRNAs play in insects910, also in metamorphosis11.…”

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confidence: 99%

The microRNA toolkit of insects

Ylla

Fromm

Piulachs

et al. 2016

Sci Rep

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Is there a correlation between miRNA diversity and levels of organismic complexity? Exhibiting extraordinary levels of morphological and developmental complexity, insects are the most diverse animal class on earth. Their evolutionary success was in particular shaped by the innovation of holometabolan metamorphosis in endopterygotes. Previously, miRNA evolution had been linked to morphological complexity, but astonishing variation in the currently available miRNA complements of insects made this link unclear. To address this issue, we sequenced the miRNA complement of the hemimetabolan Blattella germanica and reannotated that of two other hemimetabolan species, Locusta migratoria and Acyrthosiphon pisum, and of four holometabolan species, Apis mellifera, Tribolium castaneum, Bombyx mori and Drosophila melanogaster. Our analyses show that the variation of insect miRNAs is an artefact mainly resulting from poor sampling and inaccurate miRNA annotation, and that insects share a conserved microRNA toolkit of 65 families exhibiting very low variation. For example, the evolutionary shift toward a complete metamorphosis was accompanied only by the acquisition of three and the loss of one miRNA families.

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confidence: 99%

The microRNA toolkit of insects

Ylla

Fromm

Piulachs

et al. 2016

Sci Rep

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“…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 .…”

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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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“…Hence, miRNAs play significant roles in governing multiple functions in animals and plants via integrating sophisticated miRNA-mRNA regulatory networks (10,11). In the mosquito, previous studies have shown that several miRNAs manipulate host-pathogen interactions, contributing to maintenance of endosymbiont Wolbachia infection or resistance to DENV (dengue virus) infection (12)(13)(14).…”

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microRNA-309 targets the Homeobox gene SIX4 and controls ovarian development in the mosquito Aedes aegypti

Zhang

Zhao

Roy

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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106

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Obligatory blood-triggered reproductive strategy is an evolutionary adaptation of mosquitoes for rapid egg development. It contributes to the vectorial capacity of these insects. Therefore, understanding the molecular mechanisms underlying reproductive processes is of particular importance. Here, we report that microRNA-309 (miR-309) plays a critical role in mosquito reproduction. A spatiotemporal expression profile of miR-309 displayed its blood feeding-dependent onset and ovary-specific manifestation in female Aedes aegypti mosquitoes. Antagomir silencing of miR-309 impaired ovarian development and resulted in nonsynchronized follicle growth. Furthermore, the genetic disruption of miR-309 by CRISPR/Cas9 system led to the developmental failure of primary follicle formation. Examination of genomic responses to miR-309 depletion revealed that several pathways associated with ovarian development are down-regulated. Comparative analysis of genes obtained from the high-throughput RNA sequencing of ovarian tissue from the miR-309 antagomirsilenced mosquitoes with those from the in silico computation target prediction identified that the gene-encoding SIX homeobox 4 protein (SIX4) is a putative target of miR-309. Reporter assay and RNA immunoprecipitation confirmed that SIX4 is a direct target of miR-309. RNA interference of SIX4 was able to rescue phenotypic manifestations caused by miR-309 depletion. Thus, miR-309 plays a critical role in mosquito reproduction by targeting SIX4 in the ovary and serves as a regulatory switch permitting a stage-specific degradation of the ovarian SIX4 mRNA. In turn, this microRNA (miRNA)-targeted degradation is required for appropriate initiation of a blood feeding-triggered phase of ovarian development, highlighting involvement of this miRNA in mosquito reproduction.Homeobox protein gene | microRNA | CRISPR/Cas9 | ovary | fast evolution T ransmission of mosquito-borne diseases brings enormous human suffering, with more than 1 million deaths worldwide annually. The yellow fever mosquito Aedes aegypti has reemerged as one of the most dangerous vectors of human diseases, transmitting Dengue fever, Yellow fever, Chikungunya, and Zika virus (1-4). Because of the lack of effective vaccines and increasing drug resistance in pathogens, biological control is considered one of the most promising strategies for preventing disease transmission. In particular, female hematophagous mosquitoes rely on acquisition of blood to initiate a series of physiological events promoting egg development (5, 6). Therefore, understanding the molecular mechanisms underlying ovarian activation is of great significance for the development of effective approaches to control mosquito-borne diseases (7,8).MicroRNAs (miRNAs) are small noncoding RNAs that regulate gene expression at the posttranscriptional level through translational repression or mRNA decay (9). Hence, miRNAs play significant roles in governing multiple functions in animals and plants via integrating sophisticated miRNA-mRNA regulatory networks (10, 11...

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Regulation of physiological processes by microRNAs in insects

Cited by 65 publications

References 63 publications

The microRNA toolkit of insects

The microRNA toolkit of insects

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

microRNA-309 targets the Homeobox gene SIX4 and controls ovarian development in the mosquito Aedes aegypti

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