Sexual Dimorphisms in Innate Immunity and Responses to Infection in Drosophila melanogaster

Belmonte, Rebecca L.; Corbally, Mary-Kate; Duneau, David; Regan, Jennifer C.

doi:10.3389/fimmu.2019.03075

Cited by 89 publications

(110 citation statements)

References 204 publications

(244 reference statements)

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“…This could potentially indicate that in comparison to females, younger males are able to tolerate higher FHV loads, but that this ability becomes impaired with age and results in more rapid death. Indeed, it is increasingly recognized that sexual dimorphism in immune function exists in Drosophila although the precise mechanisms underlying these age-dependent dimorphic differences are poorly understood (reviewed in (BELMONTE et al 2019)). More work is needed to elucidate this important aspect of immunity.…”

Section: Discussionmentioning

confidence: 99%

Age-dependent impairment of disease tolerance is associated with a robust transcriptional response following RNA virus infection inDrosophila

Sheffield

Sciambra

Evans

et al. 2020

Preprint

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SummaryAdvanced age in humans is associated with greater susceptibility to and higher mortality rates from infections, including infections with some RNA viruses. The underlying innate immune mechanisms, which represent the first line of defense against pathogens, remain incompletely understood. Drosophila melanogaster is able to mount potent and evolutionarily conserved innate immune defenses against a variety of microorganisms including viruses and serves as an excellent model organism for studying host-pathogen interactions. With its relatively short lifespan, Drosophila also is an organism of choice for aging studies. Despite numerous advantages that this model offers, Drosophila has not been used to its potential to investigate the response of the aged host to viral infection. Here we show that in comparison to younger flies, aged Drosophila succumb more rapidly to infection with the RNA-containing Flock House Virus (FHV) due to an age-dependent defect in disease tolerance. In comparison to younger individuals, we find that older Drosophila mount larger transcriptional responses characterized by differential regulation of more genes and genes regulated to a greater extent. Our results indicate that loss of disease tolerance to FHV with age possibly results from a stronger regulation of genes involved in apoptosis, activation of the Drosophila Immune deficiency (IMD) NF-kB pathway or from downregulation of genes whose products function in mitochondria and mitochondrial respiration. Our work shows that Drosophila can serve as a model to investigate host-virus interactions during aging and sets the stage for future analysis of the age-dependent mechanisms that govern survival and control of virus infections at older age.

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Section: Discussionmentioning

confidence: 99%

Age-dependent impairment of disease tolerance is associated with a robust transcriptional response following RNA virus infection inDrosophila

Sheffield

Sciambra

Evans

et al. 2020

Preprint

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“…The differential responses of male and female D. citri and their endosymbionts to CLas may contribute to the reported, albeit inconsistent, sex differences in susceptibility to CLas [46,47,19,48]. From invertebrates to vertebrates, many animal species display sex-dependent immunity and susceptibility to infectious diseases [49][50][51]. Yet, despite potential sexual dimorphism in D. citri immune response and susceptibility to CLas, the underlying differences and similarities between males and females in their molecular responses to CLas have largely been uncharacterized.…”

Section: Plos Onementioning

confidence: 99%

“…citri and their endosymbionts to CLas may contribute to the reported, albeit inconsistent, sex differences in susceptibility to CLas [ 46 , 47 , 19 , 48 ]. From invertebrates to vertebrates, many animal species display sex-dependent immunity and susceptibility to infectious diseases [ 49 – 51 ]. Yet, despite potential sexual dimorphism in D .…”

Section: Introductionmentioning

confidence: 99%

Development on Citrus medica infected with ‘Candidatus Liberibacter asiaticus’ has sex-specific and -nonspecific impacts on adult Diaphorina citri and its endosymbionts

et al. 2020

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Huanglongbing (HLB) is a deadly, incurable citrus disease putatively caused by the unculturable bacterium, 'Candidatus Liberibacter asiaticus' (CLas), and transmitted by Diaphorina citri. Prior studies suggest D. citri transmits CLas in a circulative and propagative manner; however, the precise interactions necessary for CLas transmission remain unknown, and the impact of insect sex on D. citri-CLas interactions is poorly understood despite reports of sex-dependent susceptibilities to CLas. We analyzed the transcriptome, proteome, metabolome, and microbiome of male and female adult D. citri reared on healthy or CLas-infected Citrus medica to determine shared and sex-specific responses of D. citri and its endosymbionts to CLas exposure. More sex-specific than shared D. citri responses to CLas were observed, despite there being no difference between males and females in CLas density or relative abundance. CLas exposure altered the abundance of proteins involved in immunity and cellular and oxidative stress in a sex-dependent manner. CLas exposure impacted cuticular proteins and enzymes involved in chitin degradation, as well as energy metabolism and abundance of the endosymbiont 'Candidatus Profftella armatura' in both sexes similarly. Notably, diaphorin, a toxic Profftella-derived metabolite, was more abundant in both sexes with CLas exposure. The responses reported here resulted from a combination of CLas colonization of D. citri as well as the effect of CLas infection on C. medica. Elucidating these impacts on D. citri and their endosymbionts contributes to our understanding of the HLB pathosystem and identifies the responses potentially critical to limiting or promoting CLas acquisition and propagation in both sexes.

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“…A caveat to our interpretations is that genes influenced by the interaction of Spiroplasma X wasp treatments could also reflect sex differences in response to wasp parasitism, due to the mixed sex (Spiroplasma-free) vs. all female (Spiroplasma-infected) comparisons. Evidence of sex differences in immunity against other natural enemies has been reported (reviewed by Belmonte et al, 2020). Further studies controlling for sex (e.g., separating males and females in the Spiroplasma-free treatment) are needed to address this.…”

Section: Discussionmentioning

confidence: 99%

Differential gene expression in a tripartite interaction:Drosophila,Spiroplasmaand parasitic wasps

Alvear

Mateos

Cortez

et al. 2021

PeerJ

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Background Several facultative bacterial symbionts of insects protect their hosts against natural enemies. Spiroplasma poulsonii strain sMel (hereafter Spiroplasma), a male-killing heritable symbiont of Drosophila melanogaster, confers protection against some species of parasitic wasps. Several lines of evidence suggest that Spiroplasma-encoded ribosome inactivating proteins (RIPs) are involved in the protection mechanism, but the potential contribution of the fly-encoded functions (e.g., immune response), has not been deeply explored. Methods Here we used RNA-seq to evaluate the response of D. melanogaster to infection by Spiroplasma and parasitism by the Spiroplasma-susceptible wasp Leptopilina heterotoma, and the Spiroplasma-resistant wasp Ganaspis sp. In addition, we used quantitative (q)PCR to evaluate the transcript levels of the Spiroplasma-encoded Ribosomal inactivation protein (RIP) genes. Results In the absence of Spiroplasma infection, we found evidence of Drosophila immune activation by Ganaspis sp., but not by L. heterotoma, which in turn negatively influenced functions associated with male gonad development. As expected for a symbiont that kills males, we detected extensive downregulation in the Spiroplasma-infected treatments of genes known to have male-biased expression. We detected very few genes whose expression patterns appeared to be influenced by the Spiroplasma-L. heterotoma interaction, and these genes are not known to be associated with immune response. For most of these genes, parasitism by L. heterotoma (in the absence of Spiroplasma) caused an expression change that was at least partly reversed when both L. heterotoma and Spiroplasma were present. It is unclear whether such genes are involved in the Spiroplasma-mediated mechanism that leads to wasp death and/or fly rescue. Nonetheless, the expression pattern of some of these genes, which reportedly undergo expression shifts during the larva-to-pupa transition, is suggestive of an influence of Spiroplasma on the development time of L. heterotoma-parasitized flies. One of the five RIP genes (RIP2) was consistently highly expressed independently of wasp parasitism, in two substrains of sMel. Finally, the RNAseq data revealed evidence consistent with RIP-induced damage in the ribosomal (r)RNA of the Spiroplasma-susceptible, but not the Spiroplasma-resistant, wasp. Acknowledging the caveat that we lacked adequate power to detect the majority of DE genes with fold-changes lower than 3, we conclude that immune priming is unlikely to contribute to the Spiroplasma-mediated protection against wasps, and that the mechanism by which Ganaspis sp. resists/tolerates Spiroplasma does not involve inhibition of RIP transcription.

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Sexual Dimorphisms in Innate Immunity and Responses to Infection in Drosophila melanogaster

Cited by 89 publications

References 204 publications

Age-dependent impairment of disease tolerance is associated with a robust transcriptional response following RNA virus infection inDrosophila

Age-dependent impairment of disease tolerance is associated with a robust transcriptional response following RNA virus infection inDrosophila

Development on Citrus medica infected with ‘Candidatus Liberibacter asiaticus’ has sex-specific and -nonspecific impacts on adult Diaphorina citri and its endosymbionts

Differential gene expression in a tripartite interaction:Drosophila,Spiroplasmaand parasitic wasps

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