桔小实蝇细胞因子受体Domeless的表征及BdDomeless3参与对类共生病毒的免疫

doi:10.1016/j.jia.2023.10.003

摘要/Abstract

摘要：

JAK/STAT（Janus kinase/signal transducers and activators of transcription）是无脊椎动物重要的先天免疫信号通路，细胞因子受体Domeless是其上游通路的核心组分。分析发现，桔小实蝇有3个Domeless受体（BdDomeless1、BdDomeless2和BdDomeless3），均具有5个纤连蛋白Ⅲ型（FN Ⅲ）胞外结构域和1个跨膜结构域，且在成虫期高表达，并对病原物侵染具有一定的诱导响应。进一步分析发现，仅BdDomelss3在关键免疫组织脂肪体中显著高表达，并能够响应类共生病毒的侵染；RNAi靶向BdDomeless3可促进Bactrocera dorsalis cripavirus（BdCV）和Bactrocera dorsalis picorna-like virus（BdPLV）复制，说明细胞因子受体BdDomeless3参与抵抗桔小实蝇类共生病毒的复制过程，暗示JAK/STAT通路在桔小实蝇免疫系统中具有重要作用。本研究首次对实蝇类昆虫JAK/STAT通路细胞因子受体进行了表征，并探究了BdDomeless3的免疫功能，为揭示桔小实蝇的先天免疫机制提供了新见解。

Abstract:

The Janus kinase/signal transducers and activators of transcription (JAK/STAT) signaling pathway play a pivotal role in innate immunity. Among invertebrates, Domeless receptors serve as the key upstream regulators of this pathway. In our study on Bactrocera dorsalis, we identified three cytokine receptors: BdDomeless1, BdDomeless2, and BdDomeless3. Each receptor encompasses five fibronectin-type-III-like (FN III) extracellular domains and a transmembrane domain. Furthermore, these receptors exhibit the increased responsiveness to diverse pathogenic challenges. Notably, only BdDomeless3 is upregulated during symbiont-like viral infections. Moreover, silencing BdDomeless3 enhanced the infectivity of Bactrocera dorsalis cripavirus (BdCV) and B. dorsalis picorna-like virus (BdPLV), underscoring BdDomeless3’s crucial role in antiviral defense of B. dorsalis. Following the suppression of Domeless3 expression, six antimicrobial peptide genes displayed decreased expression, potentially correlating with the rise in viral infectivity. To our knowledge, this is the first study identifying cytokine receptors associated with the JAK/STAT pathway in tephritid flies, shedding light on the immune mechanisms of B. dorsalis.

Key words: Bactrocera dorsalis , JAK/STAT pathway , Domeless receptors , antiviral immunity , symbiont-like virus

. 桔小实蝇细胞因子受体Domeless的表征及BdDomeless3参与对类共生病毒的免疫[J]. Journal of Integrative Agriculture, 2024, 23(4): 1274-1284.

Wei Zhang, Shaoyang Li, Rong Li, Jinzhi Niu, Jinjun Wang. Characterization of Domeless receptors and the role of BdDomeless3 in anti-symbiont-like virus defense in Bactrocera dorsalis[J]. Journal of Integrative Agriculture, 2024, 23(4): 1274-1284.

参考文献

Bang I S. 2019. JAK/STAT signaling in insect innate immunity. Entomological Research, 49, 339–353.

Bonning B C, Saleh M C. 2021. The interplay between viruses and RNAi pathways in insects. Annual Review of Entomology, 66, 61–79.

Brown S, Hu N, Hombria J C. 2001. Identification of the first invertebrate interleukin JAK/STAT receptor, the Drosophila gene domeless. Current Biology, 11, 1700–1705.

Buchon N, Silverman N, Cherry S. 2014. Immunity in Drosophila melanogaster--from microbial recognition to whole-organism physiology. Nature Reviews Immunology, 14, 796–810.

Maktura G C, Paranhos B J, Marques-Souza H. 2021. RNAi in fruit flies (Diptera: Tephritidae): Successes and challenges. Journal of Applied Entomology, 145, 740–756.

Chen E H, Wei D, Wei D D, Yuan G R, Wang J J. 2013. The effect of dietary restriction on longevity, fecundity, and antioxidant responses in the oriental fruit fly, Bactrocera dorsalis (Hendel) (Diptera: Tephritidae). Journal of Insect Physiology, 59, 1008–1016.

Cheng G, Liu Y, Wang P, Xiao X. 2016. Mosquito defense strategies against viral infection. Trends in Parasitology, 32, 177–186.

Dagil R, Knudsen M J, Olsen J G, O’Shea C, Franzmann M, Goffin V, Teilum K, Breinholt J, Kragelund B B. 2012. The WSXWS motif in cytokine receptors is a molecular switch involved in receptor activation: insight from structures of the prolactin receptor. Structure, 20, 270–282.

Deddouche S, Matt N, Budd A, Mueller S, Kemp C, Galiana-Arnoux D, Dostert C, Antoniewski C, Hoffmann J A, Imler J L. 2008. The DExD/H-box helicase Dicer-2 mediates the induction of antiviral activity in drosophila. Nature Immunology, 9, 1425–1432.

Dong X, Li Q, Zhang H. 2016. The noa gene is functionally linked to the activation of the Toll/Imd signaling pathways in Bactrocera dorsalis (Hendel). Developmental & Comparative Immunology, 55, 233–240.

Gao J, Zhao B R, Zhang H, You Y L, Li F, Wang X W. 2021. Interferon functional analog activates antiviral Jak/Stat signaling through integrin in an arthropod. Cell Reports, 36, 109761.

Hu X, Li J, Fu M, Zhao X, Wang W. 2021. The JAK/STAT signaling pathway: From bench to clinic. Signal Transduction and Targeted Therapy, 6, 402.

Kemp C, Mueller S, Goto A, Barbier V, Paro S, Bonnay F, Dostert C, Troxler L, Hetru C, Meignin C, Pfeffer S, Hoffmann J A, Imler J L. 2013. Broad RNA interference-mediated antiviral immunity and virus-specific inducible responses in Drosophila. Journal of Immunology, 190, 650–658.

Kingsolver M B, Huang Z, Hardy R W. 2013. Insect antiviral innate immunity: Pathways, effectors, and connections. Journal of Molecular Biology, 425, 4921–4936.

Li Q, Dong X, Zheng W, Zhang H. 2017. The PLA2 gene mediates the humoral immune responses in Bactrocera dorsalis (Hendel). Developmental & Comparative Immunology, 67, 293–299.

Li W, Dou W, Wang J J. 2023. BdcSP10 is a prophenoloxidase-activating protease in Bactrocera dorsalis. Developmental & Comparative Immunology, 138, 104558.

Lourido F, Quenti D, Salgado-Canales D, Tobar N. 2021. Domeless receptor loss in fat body tissue reverts insulin resistance induced by a high-sugar diet in Drosophila melanogaster. Scientific Reports, 11, 3263.

Nguyen L T, Schmidt H A, von Haeseler A, Minh B Q. 2015. IQ-TREE: A fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Molecular Biology and Evolution, 32, 268–274.

Paradkar P N, Trinidad L, Voysey R, Duchemin J B, Walker P J. 2012. Secreted Vago restricts West Nile virus infection in Culex mosquito cells by activating the Jak-STAT pathway. Proceedings of the National Academy of Sciences of the United States of America, 109, 18915–18920.

Philips R L, Wang Y, Cheon H, Kanno Y, Gadina M, Sartorelli V, Horvath C M, Darnell Jr J E, Stark G R, O’Shea J J. 2022. The JAK-STAT pathway at 30: Much learned, much more to do. Cell, 185, 3857–3876.

Sabin L R, Hanna S L, Cherry S. 2010. Innate antiviral immunity in Drosophila. Current Opinion in Immunology, 22, 4–9.

Sharpe S R, Morrow J L, Brettell L E, Shearman D C, Gilchrist A S, Cook J M, Riegler M. 2021. Tephritid fruit flies have a large diversity of co-occurring RNA viruses. Journal of Invertebrate Pathology, 186, 107569.

Shen G M, Jiang H B, Wang X N, Wang J J. 2010. Evaluation of endogenous references for gene expression profiling in different tissues of the oriental fruit fly Bactrocera dorsalis (Diptera: Tephritidae). BMC Molecular Biology, 11, 76.

Shi M, Lin X D, Tian J H, Chen L J, Chen X, Li C X, Qin X C, Li J, Cao J P, Eden J S, Buchmann J, Wang W, Xu J, Holmes E C, Zhang Y Z. 2016. Redefining the invertebrate RNA virosphere. Nature, 540, 539–543.

Wakil W, Usman M, Piñero J C, Wu S, Toews M D, Shapiro-Ilan D I. 2022. Combined application of entomopathogenic nematodes and fungi against fruit flies, Bactrocera zonata and B. dorsalis (Diptera:Tephritidae): Laboratory cups to field study. Pest Management Science, 78, 2779–2791.

Wang D, Liang Q, Chen M, Ye H, Liao Y, Yin J, Lü L, Lei Y, Cai D, Jaleel W, He Y. 2021. Susceptibility of oriental fruit fly, Bactrocera dorsalis (Diptera: Tephritidae) pupae to entomopathogenic fungi. Applied Entomology and Zoology, 56, 269–275.

Wang Y, Zhou L, Liang W, Dang Z, Wang S, Zhang Y, Zhao P, Lu Z. 2022. Cytokine receptor DOME controls wing disc development in Bombyx mori. Insect Biochemistry and Molecular Biology, 148, 103828.

Wei D, Liu Y W, Zhang Y X, Wang J J. 2019. Characterization and function of two short peptidoglycan recognition proteins involved in the immunity of Bactrocera dorsalis (Hendel). Insects, 10, 79.

Yang H, Kronhamn J, Ekstrom J O, Korkut G G, Hultmark D. 2015. JAK/STAT signaling in Drosophila muscles controls the cellular immune response against parasitoid infection. EMBO Reports, 16, 1664–1672.

Yang Y, Jiang H B, Liang C H, Ma Y P, Dou W, Wang J J. 2023. Chromosome-level genome assembly reveals potential epigenetic mechanisms of the thermal tolerance in the oriental fruit fly, Bactrocera dorsalis. International Journal of Biological Macromolecules, 225, 430–441.

Yao Z, Cai Z, Ma Q, Bai S, Wang Y, Zhang P, Guo Q, Gu J, Lemaitre B, Zhang H. 2022. Compartmentalized PGRP expression along the dipteran Bactrocera dorsalis gut forms a zone of protection for symbiotic bacteria. Cell Reports, 41, 111523.

Yasukawa H, Ohishi M, Mori H, Murakami M, Chinen T, Aki D, Hanada T, Takeda K, Akira S, Hoshijima M, Hirano T, Chien K R, Yoshimura A. 2003. IL-6 induces an anti-inflammatory response in the absence of SOCS3 in macrophages. Nature Immunology, 4, 551–556.

Yu S, Luo F, Xu Y, Zhang Y, Jin L H. 2022. Drosophila innate immunity involves multiple signaling pathways and coordinated communication between different tissues. Frontiers in Immunology, 13, 905370.

Zhang R, Zhang S, Li T, Li H, Zhang H, Zheng W. 2023. RNA sequencing identifies an ovary-enriched microRNA, miR-311-3p, involved in ovarian development and fecundity by targeting Endophilin B1 in Bactrocera dorsalis. Pest Management Science, 79, 688–700.

Zhang W, Gu Q, Niu J, Wang J J. 2020. The RNA virome and its dynamics in an invasive fruit fly, Bactrocera dorsalis, imply interactions between host and viruses. Microbial Ecology, 80, 423–434.

Zhang W, Zhang Y C, Wang Z G, Gu Q Y, Niu J Z, Wang J J. 2022. The diversity of viral community in invasive fruit flies (Bactrocera and Zeugodacus) revealed by meta-transcriptomics. Microbial Ecology, 83, 739–752.

Zhang Y, Liu S, De Meyer M, Liao Z, Zhao Y, Virgilio M, Feng S, Qin Y, Singh S, Wee S L, Jiang F, Guo S, Li H, Deschepper P, Vanbergen S, Delatte H, van Sauers-Muller A, Syamsudin T S, Kawi A P, Kasina M, et al. 2022. Genomes of the cosmopolitan fruit pest Bactrocera dorsalis (Diptera: Tephritidae) reveal its global invasion history and thermal adaptation. Journal of Advanced Research, 53, 61–74.

Zhang Y Z, Shi M, Holmes E C. 2018. Using metagenomics to characterize an expanding virosphere. Cell, 172, 1168–1172.

Zhou Q H, Zhang Q, Yang R L, Yuan G R, Wang J J, Dou W. 2022. RNAi-mediated knockdown of juvenile hormone acid O-methyltransferase disrupts larval development in the oriental fruit fly, Bactrocera dorsalis (Hendel). Pesticide Biochemistry and Physiology, 188, 105285.