Regulation of DUOX by the Gαq-Phospholipase Cβ-Ca2+ Pathway in Drosophila Gut Immunity

Ha, Eun-Mi; Lee, Kyung‐Ah; Park, Seon Hwa; Kim, Sunghee; Nam, Hyuck‐Jin; Lee, Hyo-Young; Kang, Dongmin; Lee, Won–Jae

doi:10.1016/j.devcel.2008.12.015

Cited by 202 publications

(244 citation statements)

References 57 publications

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“…The silencing of the BdDuox gene led to an increase in intestinal bacterial density and altered both the structure and richness of the intestinal indigenous bacterial community. This is consistent with a previous observation that DUOX inactivation led to uncontrolled propagation of the dietary yeast in the gut of Drosophila (Ha et al, 2009a). The resulting dysbiosis, in turn, stimulated an immune response by activating the BdDuox gene.…”

Section: Discussionsupporting

confidence: 81%

“…Previous research has found that Imd pathway-mutant flies lacking AMP expression are usually resistant to gut infection except ROS-resistant bacteria (Ha et al, 2005;Ryu et al, 2006), and could still control the dietary yeast, S. cerevisiae. In contrast, the DUOX inactivation led to uncontrolled propagation of S. cerevisiae in the gut of Drosophila (Ha et al, 2009a), underlying that ROS generation system has the primordial role in the gut antimicrobial response (Ha et al, 2005(Ha et al, , 2009a. In this study, we found that B. dorsalis also used the BdDuox-dependent immune response as a defense in the gut as previously characterized in Drosophila (Ha et al, 2005;Bae et al, 2010).…”

Section: Discussionmentioning

confidence: 46%

“…Interestingly, the diverse NOX and DUOX family enzymes are not only expressed in phagocytic cells, but also in various nonphagocytic cells, including mucosal epithelial cells (Ha et al, 2005;Allaoui et al, 2009;Fischer, 2009), indicating their potential biological roles in these cells. In addition, several recent studies have shown that ROS are microbicidal effector molecules in the gut epithelia (El Hassani et al, 2005;Ha et al, 2005Ha et al, , 2009a. In Drosophila, there is only one Duox gene and one Nox gene in the genome, and genetic analysis has shown that Duox-knockout flies, but not Nox-knockout flies, cannot produce infection-induced ROS (Ha et al, 2005).…”

Section: Introductionmentioning

confidence: 99%

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The dual oxidase gene BdDuox regulates the intestinal bacterial community homeostasis of Bactrocera dorsalis

Yao¹,

Wang²,

Li³

et al. 2015

The ISME Journal

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The guts of metazoans are in permanent contact with the microbial realm that includes beneficial symbionts, nonsymbionts, food-borne microbes and life-threatening pathogens. However, little is known concerning how host immunity affects gut bacterial community. Here, we analyze the role of a dual oxidase gene (BdDuox) in regulating the intestinal bacterial community homeostasis of the oriental fruit fly Bactrocera dorsalis. The results showed that knockdown of BdDuox led to an increased bacterial load, and to a decrease in the relative abundance of Enterobacteriaceae and Leuconostocaceae bacterial symbionts in the gut. The resulting dysbiosis, in turn, stimulates an immune response by activating BdDuox and promoting reactive oxygen species (ROS) production that regulates the composition and structure of the gut bacterial community to normal status by repressing the overgrowth of minor pathobionts. Our results suggest that BdDuox plays a pivotal role in regulating the homeostasis of the gut bacterial community in B. dorsalis.

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Section: Discussionsupporting

confidence: 81%

Section: Discussionmentioning

confidence: 46%

Section: Introductionmentioning

confidence: 99%

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The dual oxidase gene BdDuox regulates the intestinal bacterial community homeostasis of Bactrocera dorsalis

Yao¹,

Wang²,

Li³

et al. 2015

The ISME Journal

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“…To measure ROS production in vitro, S2 cells were maintained in Insect-XPRESS protein-free insect cell medium (Lonza, Switzerland) at 27°C. Soluble microbial extracts was prepared as described previously (57). In brief, bacteria were grown under the following conditions.…”

Section: Methodsmentioning

confidence: 99%

RNA Interference Directed against the Transglutaminase Gene Triggers Dysbiosis of Gut Microbiota in Drosophila

Sekihara¹,

Shibata²,

Hyakkendani

et al. 2016

Journal of Biological Chemistry

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Edited by Luke O'NeillWe recently reported that transglutaminase (TG) suppresses immune deficiency pathway-controlled antimicrobial peptides (IMD-AMPs), thereby conferring immune tolerance to gut microbes, and that RNAi of the TG gene in flies decreases the lifespan compared with non-TG-RNAi flies. Here, analysis of the bacterial composition of the Drosophila gut by next-generation sequencing revealed that gut microbiota comprising one dominant genus of Acetobacter in non-TG-RNAi flies was shifted to that comprising two dominant genera of Acetobacter and Providencia in TG-RNAi flies. Four bacterial strains, including Acetobacter persici SK1 and Acetobacter indonesiensis SK2, Lactobacillus pentosus SK3, and Providencia rettgeri SK4, were isolated from the midgut of TG-RNAi flies. SK1 exhibited the highest resistance to the IMD-AMPs Cecropin A1 and Diptericin among the isolated bacteria. In contrast, SK4 exhibited considerably lower resistance against Cecropin A1, whereas SK4 exhibited high resistance to hypochlorous acid. The resistance of strains SK1-4 against IMD-AMPs in in vitro assays could not explain the shift of the microbiota in the gut of TGRNAi flies. The lifespan was reduced in gnotobiotic flies that ingested both SK4 and SK1, concomitant with the production of reactive oxygen species and apoptosis in the midgut, whereas the survival rate was not altered in gnotobiotic flies that monoingested either SK4 or SK1. Interestingly, significant amounts of reactive oxygen species were detected in the midgut of gnotobiotic flies that ingested SK4 and SK2, concomitant with no significant apoptosis in the midgut. In gnotobiotic flies that co-ingested SK4 and SK1, an additional unknown factor(s) may be required to cause midgut apoptosis.Foreign substances, including foods, minerals, and microbes, continually pass through the intestinal tract and attach to the gut epithelium. Development of physical and immunologic barriers against foreign substances is thus essential to protect the gut epithelia. Healthy and balanced gut microbiota provide essential nutrients for their host and help to maintain gut immune homeostasis, whereas disruption of the balance, called dysbiosis, is associated with various animal diseases (1, 2). The fruit fly, Drosophila melanogaster, is a useful model for investigating the close relationship between bacteria and bacteria or host and bacteria interactions (3, 4), and the gut microbial community of Drosophila comprises ϳ10 5 microbes of ϳ20 species (5-7). The Drosophila gut is functionally analogous to the mammalian intestinal tract (8, 9), producing antimicrobial peptides (AMPs) 2 and reactive oxygen species (ROS) (10, 11). Microbes or microbe-derived immune elicitors in the fly gut can initiate several immune signaling pathways, such as the immune deficiency (IMD) pathway activated by peptidoglycans to produce AMPs and the dual oxidase (DUOX) signaling pathway activated by uracils to produce . In addition to pathogenic bacteria, commensal microbe-derived peptidoglycans constitutively acti...

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“…Duox activity is stimulated by uracil, a microbe-derived ligand, which is released by pathogenic bacteria and certain members of the microbiota that can become pathogenic (sometimes referred to as pathobionts) [82]. To prevent excessive epithelial damage by the production of ROS, Drosophila employs an inducible catalase and negative regulators of Duox activity [83,84]. Another recently identified host response to microbes is the coordination of these effectors (ROS and AMPs) with homeostatic pathways, in particular JAK/STAT, JNK and EGFR pathways, to respond to tissue damage through stem cell proliferation and epithelium renewal [63,65,75,79,[85][86][87].…”

Section: Amps and Gut Immune Responsesmentioning

confidence: 99%

Friend, foe or food? Recognition and the role of antimicrobial peptides in gut immunity and Drosophila –microbe interactions

Broderick

2016

Phil. Trans. R. Soc. B

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One contribution of 13 to a theme issue 'Evolutionary ecology of arthropod antimicrobial peptides'. Drosophila melanogaster lives, breeds and feeds on fermenting fruit, an environment that supports a high density, and often a diversity, of microorganisms. This association with such dense microbe-rich environments has been proposed as a reason that D. melanogaster evolved a diverse and potent antimicrobial peptide (AMP) response to microorganisms, especially to combat potential pathogens that might occupy this niche. Yet, like most animals, D. melanogaster also lives in close association with the beneficial microbes that comprise its microbiota, or microbiome, and recent studies have shown that antimicrobial peptides (AMPs) of the epithelial immune response play an important role in dictating these interactions and controlling the host response to gut microbiota. Moreover, D. melanogaster also eats microbes for food, consuming fermentative microbes of decaying plant material and their by-products as both larvae and adults. The processes of nutrient acquisition and host defence are remarkably similar and use shared functions for microbe detection and response, an observation that has led to the proposal that the digestive and immune systems have a common evolutionary origin. In this manner, D. melanogaster provides a powerful model to understand how, and whether, hosts differentiate between the microbes they encounter across this spectrum of associations.This article is part of the themed issue 'Evolutionary ecology of arthropod antimicrobial peptides'.

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Regulation of DUOX by the Gαq-Phospholipase Cβ-Ca2+ Pathway in Drosophila Gut Immunity

Cited by 202 publications

References 57 publications

The dual oxidase gene BdDuox regulates the intestinal bacterial community homeostasis of Bactrocera dorsalis

The dual oxidase gene BdDuox regulates the intestinal bacterial community homeostasis of Bactrocera dorsalis

RNA Interference Directed against the Transglutaminase Gene Triggers Dysbiosis of Gut Microbiota in Drosophila

Friend, foe or food? Recognition and the role of antimicrobial peptides in gut immunity and Drosophila –microbe interactions

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