CircRNA-regulated immune responses of asian honey bee workers to microsporidian infection

Zhu, Zhiwei; Wang, Jie; Fan, Xiangtao; Long, Qi; Chen, Huazhi; Ye, Yaping; Zhang, Kaiyao; Ren, Zhongmin; Zhang, Yang; Niu, Qingsheng; Chen, Dafu; Guo, Rui

doi:10.3389/fgene.2022.1013239

Cited by 15 publications

(11 citation statements)

References 88 publications

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“…On the basis of our previously established method, the midgut tissues of A. c. cerana workers at 7 dpi and 10 dpi with N. ceranae spores (AcT7 and AcT10 groups), as well as corresponding uninoculated workers’ midgut tissues (AcCK7 and AcCK10 groups), were, respectively, dissected and then subjected to RNA isolation, cDNA library construction, and Illumina sequencing (Guangzhou Gene Denovo Biotechnology Co., Ltd., Guangzhou, China), followed by strict quality control of the raw data [ 15 ], which were deposited in the NCBI SRA database ( (accessed on 5 September 2022)) and linked to BioProject number: PRJNA562787 [ 14 ].…”

Section: Methodsmentioning

confidence: 99%

“…We previously investigated the dynamics of miRNAs in the A. c. cerana workers’ midguts infected by N. ceranae and revealed the potential role of DEmiRNAs in host immune responses [ 14 ]. Recently, we analyzed the differential expression pattern of circular RNAs (circRNAs) in the midguts of A. c. ceran a workers during N. ceranae infection, and we uncovered that DEcircRNAs were likely to modulate host cellular and humoral immune responses through the regulation of the transcription of source genes or absorption of target miRNAs to affect the downstream gene expression [ 15 ]. As a vital layer of post-transcription regulation, lncRNAs are able to not only directly modulate gene expression, but also interact with other ncRNAs such as miRNAs to indirectly regulate the expression of target genes [ 16 ].…”

Section: Introductionmentioning

confidence: 99%

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Systematic Characterization and Regulatory Role of lncRNAs in Asian Honey Bees Responding to Microsporidian Infestation

Wang

Fan

et al. 2023

IJMS

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Long noncoding RNAs (lncRNAs) are pivotal regulators in gene expression and diverse biological processes, such as immune defense and host–pathogen interactions. However, little is known about the roles of lncRNAs in the response of the Asian honey bee (Apis cerana) to microsporidian infestation. Based on our previously obtained high-quality transcriptome datasets from the midgut tissues of Apis cerana cerana workers at 7 days post inoculation (dpi) and 10 dpi with Nosema ceranae (AcT7 and AcT10 groups) and the corresponding un-inoculated midgut tissues (AcCK7 and AcCK10 groups), the transcriptome-wide identification and structural characterization of lncRNAs were conducted, and the differential expression pattern of lncRNAs was then analyzed, followed by investigation of the regulatory roles of differentially expressed lncRNAs (DElncRNAs) in host response. Here, 2365, 2322, 2487, and 1986 lncRNAs were, respectively, identified in the AcCK7, AcT7, AcCK7, and AcT10 groups. After removing redundant ones, a total of 3496 A. c. cerana lncRNAs were identified, which shared similar structural characteristics with those discovered in other animals and plants, such as shorter exons and introns than mRNAs. Additionally, 79 and 73 DElncRNAs were screened from the workers’ midguts at 7 dpi and 10 dpi, respectively, indicating the alteration of the overall expression pattern of lncRNAs in host midguts after N. ceranae infestation. These DElncRNAs could, respectively, regulate 87 and 73 upstream and downstream genes, involving a suite of functional terms and pathways, such as metabolic process and Hippo signaling pathway. Additionally, 235 and 209 genes co-expressed with DElncRNAs were found to enrich in 29 and 27 terms, as well as 112 and 123 pathways, such as ABC transporters and the cAMP signaling pathway. Further, it was detected that 79 (73) DElncRNAs in the host midguts at 7 (10) dpi could target 321 (313) DEmiRNAs and further target 3631 (3130) DEmRNAs. TCONS_00024312 and XR_001765805.1 were potential precursors for ame-miR-315 and ame-miR-927, while TCONS_00006120 was the putative precursor for both ame-miR-87-1 and ame-miR-87-2. These results together suggested that DElncRNAs are likely to play regulatory roles in the host response to N. ceranae infestation through the regulation of neighboring genes via a cis-acting effect, modulation of co-expressed mRNAs via trans-acting effect, and control of downstream target genes’ expression via competing endogenous RNA networks. Our findings provide a basis for disclosing the mechanism underlying DElncRNA-mediated host N. ceranae response and a new perspective into the interaction between A. c. cerana and N. ceranae.

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Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Systematic Characterization and Regulatory Role of lncRNAs in Asian Honey Bees Responding to Microsporidian Infestation

Wang

Fan

et al. 2023

IJMS

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“…Interestingly, only a small number of circRNAs were found to be differentially expressed at different infection times in A. cerana after N. ceranae infection. These circRNAs modulate various immune pathways, including endocytosis, lysosomes, phagosomes, ubiquitin-mediated proteolysis, the metabolism of xenobiotics by cytochrome P450, and insect hormone biosynthesis [ 117 ]. In addition, evidence demonstrates that circRNAs have a crucial role in detecting damage caused to the midgut epithelial cell structure by N. ceranae infection.…”

Section: Circrnas In the Innate Immunity Of Insectsmentioning

confidence: 99%

“…It also appears that the circRNAs of the host are employed to regulate source gene transcription, thereby modulating the Hippo signaling pathway to facilitate cell renewal and regulate the immune response [ 118 , 119 ]. Thus, it is evident that N. ceranae altered the expression pattern of circRNAs in the midguts of A. c. cerana , and the circRNAs are likely to regulate host cellular and humoral immune response to microsporidian infection [ 117 ]. Another study determined the impact of the parasite Vairimorpha ceranae on adult honey bees, which can cause diseases such as nosemosis.…”

Section: Circrnas In the Innate Immunity Of Insectsmentioning

confidence: 99%

The Potential Biological Roles of Circular RNAs in the Immune Systems of Insects to Pathogen Invasion

Abbas

Kausar

Gul

et al. 2023

Genes

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Circular RNAs (circRNAs) are a newly discovered class of endogenously expressed non-coding RNAs (ncRNAs). They are highly stable, covalently closed molecules that frequently exhibit tissue-specific expression in eukaryotes. A small number of circRNAs are abundant and have been remarkably conserved throughout evolution. Numerous circRNAs are known to play important biological roles by acting as microRNAs (miRNAs) or protein inhibitors (‘sponges’), by regulating the function of proteins, or by being translated themselves. CircRNAs have distinct cellular functions due to structural and production differences from mRNAs. Recent advances highlight the importance of characterizing circRNAs and their targets in a variety of insect species in order to fully understand how they contribute to the immune responses of these insects. Here, we focus on the recent advances in our understanding of the biogenesis of circRNAs, regulation of their abundance, and biological roles, such as serving as templates for translation and in the regulation of signaling pathways. We also discuss the emerging roles of circRNAs in regulating immune responses to various microbial pathogens. Furthermore, we describe the functions of circRNAs encoded by microbial pathogens that play in their hosts.

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“…Honey bees are of great importance due to their pollination of numerous wildflowers and agricultural crops, production of api -products such as royal jelly and propolis, and scientific model applications [1]. However, as a kind of representative eusocial insect, honey bees are prone to infection by pathogens and parasites [2,3]. Among these, Ascosphaera apis , an obligate fungal pathogen of honey bee brood, causes chalkbrood disease, which results in a dramatic decline of colony strength and productivity alone or in combination with other biotic or abiotic factors [4].…”

Section: Introductionmentioning

confidence: 99%

Effect ofAscosphaera apisinfestation on the activities of four antioxidant enzymes in Asian honey bee larval guts

Zhang

Fan

et al. 2022

Preprint

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Ascosphaera apis exclusively infects bee larvae and causes chalkbrood, a lethal fungal disease that results in the sharp reduction in adult bees and colony productivity. However, little is known about the effect of A. apis infestation on the activities of antioxidant enzymes in bee larvae. Here, A. apis spores were purified and used to inoculate Asian honey bee (Apis cerana) larvae, followed by detection of the host survival rate and evaluation of the activities of four major antioxidant enzymes. At 6 days post inoculation (dpi) with A. apis spores, white mycelia penetrated the posterior end of the larva, extended to the anterior end, and eventually covered the entire larval body surface, presenting an obvious symptom of chalkbrood disease similar to that occurs in Apis mellifera larvae. Additionally, PCR identification showed that the expected fragment was amplified from the A. apis-inoculated larval guts and the A. apis spores, verifying the A. apis infection of A. cerana larvae. The survival rate of larvae inoculated with A. apis was high at 1–2 dpi, sharply decreased to 4.16% at 4 dpi, and reached 0% at 5 dpi; whereas that of un-inoculated larvae was always high at 1~8 dpi, with an average survival rate of 95.37%, indicating the negative impact of A. apis infection on larval survival. Furthermore, in comparison with those in the corresponding un-inoculated groups, the superoxide dismutase (SOD) and catalase (CAT) activities in the 4-day-old larval gut in the A. apis-inoculated groups were reduced (p > 0.05), while those in the 5- and 6-day-old larval guts were significantly decreased (p < 0.05); the glutathione S-transferase (GST) activity in the 4- and 5-day-old larval guts was significantly increased (p < 0.05), while that in the 6-day-old larval gut was reduced (p > 0.05); the polyphenol oxidase (PPO) activity in 4-day-old larval gut was increased (p > 0.05) and that in the 5-day-old larval gut was significantly increased (p < 0.05), whereas that in the 6-day-old larval gut was significantly reduced (p < 0.01). These results together suggested that the activities of SOD and CAT in the larval guts were suppressed during the process of A. apis infestation, while the GST activity was induced to activation, and the PPO activity was first enhanced and then inhibited. Our findings not only unravel the response of A. cerana larvae to A. apis infestation from a biochemical perspective, but also offer a valuable insight into the interaction between Asian honey bee larvae and A. apis.

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CircRNA-regulated immune responses of asian honey bee workers to microsporidian infection

Cited by 15 publications

References 88 publications

Systematic Characterization and Regulatory Role of lncRNAs in Asian Honey Bees Responding to Microsporidian Infestation

Systematic Characterization and Regulatory Role of lncRNAs in Asian Honey Bees Responding to Microsporidian Infestation

The Potential Biological Roles of Circular RNAs in the Immune Systems of Insects to Pathogen Invasion

Effect ofAscosphaera apisinfestation on the activities of four antioxidant enzymes in Asian honey bee larval guts

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