Immune and stress response ‘cross-talk’ in the Drosophila Malpighian tubule

Davies, Shireen-A.; Overend, Gayle; Sebastian, Sujith; Cundall, Maria; Cabrero, Pablo; Dow, Julian A. T.; Terhzaz, Selim

doi:10.1016/j.jinsphys.2012.01.008

Cited by 61 publications

(49 citation statements)

References 77 publications

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“…Tissue-specific transcriptomics of D. melanogaster (Chintapalli et al, 2007;Wang et al, 2004) have led the way in assigning novel functions to D. melanogaster tubules (Dow, 2009). Importantly, assignation of novel functions such as detoxification and xenobiotic handling, and stress sensing of oxidative, osmotic (ionic/salt) and immune challenges by transcriptomics analysis (Chintapalli et al, 2007;Dow, 2009;Wang et al, 2004), has been underpinned by functional and physiological analysis (Chahine and O'Donnell, 2011;Daborn et al, 2012;Davies et al, 2012;Naikkhwah and O'Donnell, 2011;Torrie et al, 2004;Yang et al, 2007). Thus, the tubules are mission-critical tissues for insect survival.…”

Section: The Malpighian Tubules As Stress Sensorsmentioning

confidence: 99%

Cell signalling mechanisms for insect stress tolerance

Davies

Cabrero

Overend

et al. 2014

Journal of Experimental Biology

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Insects successfully occupy most environmental niches and this success depends on surviving a broad range of environmental stressors including temperature, desiccation, xenobiotic, osmotic and infection stress. Epithelial tissues play key roles as barriers between the external and internal environments and therefore maintain homeostasis and organismal tolerance to multiple stressors. As such, the crucial role of epithelia in organismal stress tolerance cannot be underestimated. At a molecular level, multiple cell-specific signalling pathways including cyclic cAMP, cyclic cGMP and calcium modulate tissue, and hence, organismal responses to stress. Thus, epithelial cell-specific signal transduction can be usefully studied to determine the molecular mechanisms of organismal stress tolerance in vivo. This review will explore cell signalling modulation of stress tolerance in insects by focusing on cell signalling in a fluid transporting epithelium -the Malpighian tubule. Manipulation of specific genes and signalling pathways in only defined tubule cell types can influence the survival outcome in response to multiple environmental stressors including desiccation, immune, salt (ionic) and oxidative stress, suggesting that studies in the genetic model Drosophila melanogaster may reveal novel pathways required for stress tolerance.

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Section: The Malpighian Tubules As Stress Sensorsmentioning

confidence: 99%

Cell signalling mechanisms for insect stress tolerance

Davies

Cabrero

Overend

et al. 2014

Journal of Experimental Biology

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“…While the general impact of the heatshock response on expression programs during hyperthermia is better elucidated, less clear is the role of immune defense during recovery. Emerging evidence increasingly supports molecular "cross-talk" between innate immune (specifically AMP expression) and other stress responses such as oxidative, osmotic, and nutrient stress (reviewed in Davies et al 2012), as well as hypothermia (Sinclair Stress-Induced Transcriptome Complexityet al 2013). Aside from cross-talk or shared stress/immunity pathways, heat stress may elicit the immune response due to increased bacterial load resulting from thermal mismatching between the fly and flora.…”

Section: Gene-level Analysesmentioning

confidence: 99%

“…Profile 26 was enriched for genes involved in signaling, protein and sugar disassembly (proteolysis, glycosidases), and starch and sugar metabolism (Table S4 and Table S5). Given the specificity of stimuli required for immune pathway activation (Davies et al 2012) the genes enriched for innate immune defense responses during recovery from thermal stress were explored in greater detail. First, genes involved in any aspect of fly immunity were identified from the CV term report generated by searching "immune system process, GO ID GO:0002376" (Flybase version 2013_03).…”

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confidence: 99%

New Levels of Transcriptome Complexity at Upper Thermal Limits in WildDrosophilaRevealed by Exon Expression Analysis

et al. 2013

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While the cellular heat-shock response has been a paradigm for studying the impact of thermal stress on RNA metabolism and gene expression, the genome-wide response to thermal stress and its connection to physiological stress resistance remain largely unexplored. Here, we address this issue using an array-based exon expression analysis to interrogate the transcriptome in recently established Drosophila melanogaster stocks during severe thermal stress and recovery. We first demonstrated the efficacy of exon-level analyses to reveal a level of thermally induced transcriptome complexity extending well beyond gene-level analyses. Next, we showed that the upper range of both the cellular and physiological thermal stress response profoundly affected message expression and processing in D. melanogaster, limiting expression to a small subset of transcripts, many that share features of known rapidly responding stress genes. As predicted from cellular heat-shock research, constitutive splicing was blocked in a set of novel genes; we did not detect changes to alternative splicing during heat stress, but rather induction of intronless isoforms of known heatresponsive genes. We observed transcriptome plasticity in the form of differential isoform expression during recovery from heat shock, mediated by multiple mechanisms including alternative transcription and alternative splicing. This affected genes involved in DNA regulation, immune response, and thermotolerance. These patterns highlight the complex nature of innate transcriptome responses under stress and potential for adaptive shifts through plasticity and evolved genetic responses at different hierarchical levels.T HE distribution of ectotherms including Drosophila species can often be linked to their physiological thermal tolerances (Addo-Bediako et al. 2000;Mitchell and Hoffmann 2010;Kellermann et al. 2012). Terrestrial Drosophila from a range of environments may exist close to their maximal range and be constrained to increase upper tolerance limits, posing a threat to persistence under climate warming (Kellermann et al. 2012). Elucidating the factors delimiting upper thermal limits depends on understanding how physiological responses link with the underlying molecular processes in an integrative framework. Limited progress toward this end has been made so far, despite the cellular reaction to heat stress being the most ubiquitous and well-characterized molecular stress response.Seminal work exploiting the tightly controlled conditions of homogeneous cell lines has led to fine-scale molecular dissections of the heat-shock response in wide-ranging taxa including yeast, Drosophila, and humans. At the cellular level, heat shock triggers a dramatic reprogramming of gene expression to favor the rapid turnover of a class of molecular chaperones known as the Heat-shock proteins (Hsps) (Lindquist and Craig 1988;Yost et al. 1990). Apart from the selective activation of a subset of genes predominantly harboring heat-shock factor (HSF) sequence-binding elements, trans...

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“…For instance, starvation can induce antimicrobial peptide genes in non-infected or immunity-defective insects through activating a transcription factor FOXO, independent of pathogen responsive pathways [46]. Similarly, salt stress or high oxygen environment induces immune gene expression [47], [50]. In our study, bergapten-induced increase in the reactive oxygen species level could be responsible for activation of drosomycin genes.…”

Section: Discussionmentioning

confidence: 54%

Antagonistic Regulation, Yet Synergistic Defense: Effect of Bergapten and Protease Inhibitor on Development of Cowpea Bruchid Callosobruchus maculatus

et al. 2012

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The furanocoumarin compound bergapten is a plant secondary metabolite that has anti-insect function. When incorporated into artificial diet, it retarded cowpea bruchid development, decreased fecundity, and caused mortality at a sufficient dose. cDNA microarray analysis indicated that cowpea bruchid altered expression of 543 midgut genes in response to dietary bergapten. Among these bergapten-regulated genes, 225 have known functions; for instance, those encoding proteins related to nutrient transport and metabolism, development, detoxification, defense and various cellular functions. Such differential gene regulation presumably facilitates the bruchids' countering the negative effect of dietary bergapten. Many genes did not have homology (E-value cutoff 10−6) with known genes in a BlastX search (206), or had homology only with genes of unknown function (112). Interestingly, when compared with the transcriptomic profile of cowpea bruchids treated with dietary soybean cysteine protease inhibitor N (scN), 195 out of 200 coregulated midgut genes are oppositely regulated by the two compounds. Simultaneous administration of bergapten and scN attenuated magnitude of change in selected oppositely-regulated genes, as well as led to synergistic delay in insect development. Therefore, targeting insect vulnerable sites that may compromise each other's counter-defensive response has the potential to increase the efficacy of the anti-insect molecules.

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Immune and stress response ‘cross-talk’ in the Drosophila Malpighian tubule

Cited by 61 publications

References 77 publications

Cell signalling mechanisms for insect stress tolerance

Cell signalling mechanisms for insect stress tolerance

New Levels of Transcriptome Complexity at Upper Thermal Limits in WildDrosophilaRevealed by Exon Expression Analysis

Antagonistic Regulation, Yet Synergistic Defense: Effect of Bergapten and Protease Inhibitor on Development of Cowpea Bruchid Callosobruchus maculatus

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