Wolbachia Stimulates Immune Gene Expression and Inhibits Plasmodium Development in Anopheles gambiae

Kambris, Zakaria; Blagborough, Andrew M.; Pinto, Sofia B.; Blagrove, Marcus S. C.; Godfray, H. Charles J.; Sinden, Robert E.; Sinkins, Steven P.

doi:10.1371/journal.ppat.1001143

Cited by 297 publications

(316 citation statements)

References 41 publications

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“…aegypti has been shown to produce up-regulation of a number of immune genes, and given the possibility that this could be responsible for or contribute to the viral inhibition phenotypes, the effects of wMel transinfection on transcription levels were investigated for four Aedes albopictus immune genes. These four genes were selected to represent a range of immune gene categories including important antimicrobial effectors [a cecropin, a peptoglycan recognition protein (PGRP), and a thioester-containing protein (TEP) (15,(24)(25)(26)(27)], and also because their orthologs were previously shown to be up-regulated in the presence of wMelPop (12). The transcription of immune genes was measured by qRT-PCR using G 5 Uju.wMel, UjuT, and Ascoli Fig.…”

Section: Resultsmentioning

confidence: 99%

“…aegypti and Ae. albopictus using intrathoracic inoculation as described previously (15,28). Adult females were injected with suspensions of Wolbachia purified from Ae.…”

Section: Resultsmentioning

confidence: 99%

“…3A) was statistically significant for three of the four genes in one experiment, but on a much lower scale than that observed in a stably wMelPop-infected line of Ae. aegypti (12) or transiently wMelPop-transinfected Anopheles gambiae (15). By G 10 , no significant up-regulation was observed, possibly due to coadaption between the host and the transinfecting strain.…”

Section: Daymentioning

confidence: 95%

“…aegypti (13,14). A general role of immune up-regulation in pathogen inhibition is also supported by the knockdown of the major immune gene TEP1, which partially rescues the inhibitory effect of the presence of wMelPop on Plasmodium berghei development in transiently infected Anopheles gambiae (15). The fact that the wAlbB transinfection caused dengue inhibition in Ae.…”

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confidence: 88%

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WolbachiastrainwMel induces cytoplasmic incompatibility and blocks dengue transmission inAedes albopictus

Blagrove

Arias-Goeta

Failloux

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

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301

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Wolbachia inherited bacteria are able to invade insect populations using cytoplasmic incompatibility and provide new strategies for controlling mosquito-borne tropical diseases, such as dengue. The overreplicating wMelPop strain was recently shown to strongly inhibit the replication of dengue virus when introduced into Aedes aegypti mosquitoes, as well as to stimulate chronic immune upregulation. Here we show that stable introduction of the wMel strain of Drosophila melanogaster into Aedes albopictus, a vector of dengue and other arboviruses, abolished the transmission capacity of dengue virus-challenged mosquitoes. Immune up-regulation was observed in the transinfected line, but at a much lower level than that previously found for transinfected Ae. aegypti. Transient infection experiments suggest that this difference is related to Ae. albopictus immunotolerance of Wolbachia, rather than to the Wolbachia strain used. This study provides an example of strong pathogen inhibition in a naturally Wolbachia-infected mosquito species, demonstrating that this inhibition is not limited to naturally naïve species, and suggests that the Wolbachia strain is more important than host background for viral inhibition. Complete bidirectional cytoplasmic incompatibility was observed with WT strains infected with the naturally occurring Ae. albopictus Wolbachia, and this provides a mechanism for introducing wMel into natural populations of this species.

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Section: Resultsmentioning

confidence: 99%

“…aegypti and Ae. albopictus using intrathoracic inoculation as described previously (15,28). Adult females were injected with suspensions of Wolbachia purified from Ae.…”

Section: Resultsmentioning

confidence: 99%

Section: Daymentioning

confidence: 95%

mentioning

confidence: 88%

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WolbachiastrainwMel induces cytoplasmic incompatibility and blocks dengue transmission inAedes albopictus

Blagrove

Arias-Goeta

Failloux

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

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301

260

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“…Autophagy is not the only host-defense mechanism that can be activated by Wolbachia. Natural and experimental infections of Drosophila and mosquitoes with the overreplicating and lifeshortening wMelPop strain can induce up-regulation of host immune responses and inhibit microbial infection with viruses, protozoa, and helminth parasites (27)(28)(29)(30). Nevertheless, not all Wolbachia-host associations lead to activation of host immunity, and among the strains that do not activate host immunity are natural strains infecting Drosophila and Aedes aegypti (31,32).…”

Section: Discussionmentioning

confidence: 99%

Autophagy regulates Wolbachia populations across diverse symbiotic associations

Voronin

Cook

Steven

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

114

117

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Wolbachia are widespread and abundant intracellular symbionts of arthropods and filarial nematodes. Their symbiotic relationships encompass obligate mutualism, commensalism, parasitism, and pathogenicity. A consequence of these diverse associations is that Wolbachia encounter a wide range of host cells and intracellular immune defense mechanisms of invertebrates, which they must evade to maintain their populations and spread to new hosts. Here we show that autophagy, a conserved intracellular defense mechanism and regulator of cell homeostasis, is a major immune recognition and regulatory process that determines the size of Wolbachia populations. The regulation of Wolbachia populations by autophagy occurs across all distinct symbiotic relationships and can be manipulated either chemically or genetically to modulate the Wolbachia population load. The recognition and activation of host autophagy is particularly apparent in rapidly replicating strains of Wolbachia found in somatic tissues of Drosophila and filarial nematodes. In filarial nematodes, which host a mutualistic association with Wolbachia, the use of antibiotics such as doxycycline to eliminate Wolbachia has emerged as a promising approach to their treatment and control. Here we show that the activation of host nematode autophagy reduces bacterial loads to the same magnitude as antibiotic therapy; thus we identify a bactericidal mode of action targeting Wolbachia that can be exploited for the development of chemotherapeutic agents against onchocerciasis, lymphatic filariasis, and heartworm.Brugia malayi | innate immunity | chemotherapy | helminth | endosymbiont W olbachia is a widespread and abundant endosymbiotic bacterium of arthropods and filarial nematodes that resides in vacuoles of host germline and somatic cells. Wolbachia show a diverse variety of symbiotic associations with their host, ranging from obligate mutualism in filarial nematodes to commensal, parasitic, or pathogenic associations in insects and other arthropod hosts (1-5).In filarial nematodes Wolbachia is obligatory for normal larval growth and development, embryogenesis, and survival of adult worms (1). Although the molecular basis of this mutualistic relationship remains unknown, a comparison of host and bacterial genomes suggests that intact biosynthetic pathways for haem, nucleotides, riboflavin, and FAD may be among the contributions of the bacteria to the biology of the nematode host (6-8). The biological processes most sensitive to Wolbachia loss include larval growth and development and embryogenesis in adult females. These processes have a high metabolic demand because of the rapid growth, development, and organogenesis of the nematode and are associated with the rapid expansion of Wolbachia populations following larval infection of mammalian hosts and in reproductively active adult females (9). Loss of Wolbachia results in extensive apoptosis of germline and somatic cells of embryos, microfilariae, and fourth-stage (L4) larvae, presumably because of the lack of provision of ...

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Isolation and characterization of Pseudomonas cedrina infecting Plutella xylostella (Lepidoptera: Plutellidae)

Liu

Lin

Kang

et al. 2019

Arch Insect Biochem Physiol

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The diamondback moth, Plutella xylostella, is one of the most destructive pests worldwide and its management relies exclusively on frequent application of chemical insecticides. Resistance to common insecticides is now widespread, and novel classes of insecticides are needed.Entomopathogenic bacteria and their related products play an important role in the management of this pest.In the present work, one bacterial strain was separated from infected pupae of P. xylostella collected from field and its pathogenicity was evaluated. On the basis of the 16S ribosomal RNA sequencing, BLASTN, and phylogenetic analysis, this bacterial isolate was identified as Pseudomonas cedrina. Oral administration of P. cedrina at levels above 10,000 CFU/ml gave significant mortality to P. xylostella larvae. The pathogenicity was also observed by reduced longevity and fecundity in adult females. However, when live bacterial cells were removed, the cultured broth lost any pathogenicity. In response to the bacterial infection, P. xylostella expressed antimicrobial and stress-associated genes. A mixture treatment of P. cedrina and Bacillus thuringiensis showed an additive effect on larval mortality of P. xylostella. These results indicated that P. cedrina is an opportunistic entomopathogen without secretion of toxins. Furthermore, the additive effect of P. cedrina and B. thuringiensis provide a new insight to develop new strategy for controlling P. xylostella. K E Y W O R D S additive effect, opportunistic pathogen, Plutella xylostella, Pseudomonas cedrina

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Wolbachia Stimulates Immune Gene Expression and Inhibits Plasmodium Development in Anopheles gambiae

Cited by 297 publications

References 41 publications

WolbachiastrainwMel induces cytoplasmic incompatibility and blocks dengue transmission inAedes albopictus

WolbachiastrainwMel induces cytoplasmic incompatibility and blocks dengue transmission inAedes albopictus

Autophagy regulates Wolbachia populations across diverse symbiotic associations

Isolation and characterization of Pseudomonas cedrina infecting Plutella xylostella (Lepidoptera: Plutellidae)

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