Immunopathology and immune homeostasis during viral infection in insects

González-González, Andrea; Wayne, Marta L.

doi:10.1016/bs.aivir.2020.06.001

Cited by 27 publications

(4 citation statements)

References 148 publications

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“…Interestingly, A. aegypti males systemically challenged with E. cloacae had a sharp drop in survival, but the surviving males completely cleared the infection. This suggests that although male initial mortality was greater, they did not succumb due to infection, but might have died from an exacerbated immune reaction (53). On the other hand, females presented the opposite scenario, they endured the initial challenge having high levels of bacteria, which could indicate tolerance to the infection [i.e.…”

Section: Discussionmentioning

confidence: 99%

Sexual Dimorphism in Immune Responses and Infection Resistance in Aedes aegypti and Other Hematophagous Insect Vectors

Barletta¹,

Bahia²,

Pitaluga³

et al. 2022

Front. Trop. Dis

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Sexual dimorphism in immune function is prevalent across different species, where males trade their ability to fight pathogens for a practical reproductive function while females favor an extended lifespan. In insects, these differences in immune function reflect an evolutionary life strategy, where females have a presumably more robust immune system than insect males. Here, we evaluate immune functioning in four male and female insect vectors, Aedes aegypti (Diptera, Culicidae), Anopheles aquasalis (Diptera, Culicidae), Lutzomyia longipalpis (Diptera, Psychodidae) and Rhodnius prolixus (Hemiptera, Reduviidae). We show evidence that challenges the concept of immune sexual dimorphism in three of these insect vectors. In the three Diptera species, A. aegypti, A. aquasalis and L. longipalpis that transmit arboviruses, Plasmodium spp. (Haemospororida, Plasmodiidae) and Leishmania spp. (Trypanosomatida, Trypanosomatidae), respectively, unchallenged adult males express higher levels of immune-related genes than adult females and immature developmental stages. The main components of the Toll, IMD, and Jak/STAT pathways and antimicrobial effectors are highly expressed in whole-body males. Additionally, males present lower midgut basal microbiota levels than females. In A. aegypti mosquitoes, the differences in immune gene expression and microbiota levels are established in adult mosquitoes but are not present at the recently emerged adults and pupal stage. Antibiotic treatment does not affect the consistently higher expression of immune genes in males, except defensin, which is reduced significantly after microbiota depletion and restored after re-introduction. Our data suggest that Diptera males have a basal state of activation of the immune system and that activation of a more robust response through systemic immune challenge acutely compromises their survival. The ones who survive clear the infection entirely. Females follow a different strategy where a moderate immune reaction render higher tolerance to infection and survival. In contrast, hematophagous adult males of the Hemiptera vector R. prolixus, which transmits Trypanosoma cruzi, present no differences in immune activation compared to females, suggesting that diet differences between males and females may influence immune sexual dimorphism. These findings expand our understanding of the biology of insect vectors of human pathogens, which can help to direct the development of new strategies to limit vector populations.

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Section: Discussionmentioning

confidence: 99%

Sexual Dimorphism in Immune Responses and Infection Resistance in Aedes aegypti and Other Hematophagous Insect Vectors

Barletta¹,

Bahia²,

Pitaluga³

et al. 2022

Front. Trop. Dis

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“…Additional transcriptomic analysis at later time points of infection, during which significant differences in survival between age groups are observed and also warranted. Such analysis could help to draw a more complete picture about differential regulation of genes and virus-induced immunopathology in insects, which remains a largely understudied field ( Gonzalez-Gonzalez and Wayne 2020 ).…”

Section: Discussionmentioning

confidence: 99%

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

Sheffield

Sciambra

Evans

et al. 2021

G3 Genes|Genomes|Genetics

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Advanced 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 full 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. Relative to younger individuals, we find that older Drosophila mount transcriptional responses characterized by differential regulation of more genes and genes regulated to a greater extent. We show that loss of disease tolerance to FHV with age associates with a stronger regulation of genes involved in apoptosis, some genes of the Drosophila Immune deficiency (IMD) NF-kB pathway and 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 furthermore 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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“…The long-term association between arboviruses and their insect vectors involves evolutionary trade-offs that maintain a balance between insect fitness cost and persistent viral transmission. During persistent viral infection in insect vectors, arboviruses induce immune homeostasis to modulate vector-virus coexistence [ 38 ]. However, the mechanisms by which arboviruses modulate immune homeostasis remain poorly understood.…”

Section: Discussionmentioning

confidence: 99%

“…During persistent viral infection in insect vectors, arboviruses induce immune homeostasis to modulate vector-virus coexistence [38]. However, the mechanisms by which arboviruses modulate immune homeostasis remain poorly understood.…”

Section: Plos Pathogensmentioning

confidence: 99%

Arboviruses antagonize insect Toll antiviral immune signaling to facilitate the coexistence of viruses with their vectors

Jia,

Luo,

Guan

et al. 2024

PLoS Pathog

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Many plant arboviruses are persistently transmitted by piercing-sucking insect vectors. However, it remains largely unknown how conserved insect Toll immune response exerts antiviral activity and how plant viruses antagonize it to facilitate persistent viral transmission. Here, we discover that southern rice black-streaked dwarf virus (SRBSDV), a devastating planthopper-transmitted rice reovirus, activates the upstream Toll receptors expression but suppresses the downstream MyD88-Dorsal-defensin cascade, resulting in the attenuation of insect Toll immune response. Toll pathway-induced the small antibacterial peptide defensin directly interacts with viral major outer capsid protein P10 and thus binds to viral particles, finally blocking effective viral infection in planthopper vector. Furthermore, viral tubular protein P7-1 directly interacts with and promotes RING E3 ubiquitin ligase-mediated ubiquitinated degradation of Toll pathway adaptor protein MyD88 through the 26 proteasome pathway, finally suppressing antiviral defensin production. This virus-mediated attenuation of Toll antiviral immune response to express antiviral defensin ensures persistent virus infection without causing evident fitness costs for the insects. E3 ubiquitin ligase also is directly involved in the assembly of virus-induced tubules constructed by P7-1 to facilitate viral spread in planthopper vector, thereby acting as a pro-viral factor. Together, we uncover a previously unknown mechanism used by plant arboviruses to suppress Toll immune response through the ubiquitinated degradation of the conserved adaptor protein MyD88, thereby facilitating the coexistence of arboviruses with their vectors in nature.

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Immunopathology and immune homeostasis during viral infection in insects

Cited by 27 publications

References 148 publications

Sexual Dimorphism in Immune Responses and Infection Resistance in Aedes aegypti and Other Hematophagous Insect Vectors

Sexual Dimorphism in Immune Responses and Infection Resistance in Aedes aegypti and Other Hematophagous Insect Vectors

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

Arboviruses antagonize insect Toll antiviral immune signaling to facilitate the coexistence of viruses with their vectors

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