Wolbachia Modulates Lipid Metabolism in Aedes albopictus Mosquito Cells

Molloy, Jenny; Sommer, Ulf; Viant, Mark R.; Sinkins, Steven P.

doi:10.1128/aem.00275-16

Cited by 100 publications

(102 citation statements)

References 69 publications

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“…Thus, replication of Wolbachia is likely to place exceptional demands on host lipid metabolism. Our results are also in accord with a recent study demonstrating that the presence of Wolbachia significantly alters lipid metabolism of Aedes albopictus mosquito cells (Molloy et al 2016). Significantly, the titer of Spiroplasma, another maternally inherited insect endosymbiont, is also limited by the levels of host lipids (Herren et al 2014).…”

Section: Discussionsupporting

confidence: 82%

Reliance of Wolbachia on High Rates of Host Proteolysis Revealed by a Genome-Wide RNAi Screen of Drosophila Cells

et al. 2017

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Wolbachia are gram-negative, obligate, intracellular bacteria carried by a majority of insect species worldwide. Here we use a Wolbachia-infected Drosophila cell line and genome-wide RNA interference (RNAi) screening to identify host factors that influence Wolbachia titer. By screening an RNAi library targeting 15,699 transcribed host genes, we identified 36 candidate genes that dramatically reduced Wolbachia titer and 41 that increased Wolbachia titer. Host gene knockdowns that reduced Wolbachia titer spanned a broad array of biological pathways including genes that influenced mitochondrial function and lipid metabolism. In addition, knockdown of seven genes in the host ubiquitin and proteolysis pathways significantly reduced Wolbachia titer. To test the in vivo relevance of these results, we found that drug and mutant inhibition of proteolysis reduced levels of Wolbachia in the Drosophila oocyte. The presence of Wolbachia in either cell lines or oocytes dramatically alters the distribution and abundance of ubiquitinated proteins. Functional studies revealed that maintenance of Wolbachia titer relies on an intact host Endoplasmic Reticulum (ER)-associated protein degradation pathway (ERAD). Accordingly, electron microscopy studies demonstrated that Wolbachia is intimately associated with the host ER and dramatically alters the morphology of this organelle. Given Wolbachia lack essential amino acid biosynthetic pathways, the reliance of Wolbachia on high rates of host proteolysis via ubiquitination and the ERAD pathways may be a key mechanism for provisioning Wolbachia with amino acids. In addition, the reliance of Wolbachia on the ERAD pathway and disruption of ER morphology suggests a previously unsuspected mechanism for Wolbachia's potent ability to prevent RNA virus replication.

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Section: Discussionsupporting

confidence: 82%

Reliance of Wolbachia on High Rates of Host Proteolysis Revealed by a Genome-Wide RNAi Screen of Drosophila Cells

et al. 2017

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“…However, some Wolbachia can be mutualists [6], involved in nutritional mechanisms reported in Drosophila melanogaster [58] and recently in Cimex lectularius (Linneaus) [59] and Aedes albopictus (Skuse) [60]. Our results suggest that Wolbachia plays an important role in CBB reproduction.…”

Section: Discussionsupporting

confidence: 59%

Wolbachia Affects Reproduction and Population Dynamics of the Coffee Berry Borer (Hypothenemus hampei): Implications for Biological Control

Mariño

Rodrigues

Bayman

2017

Insects

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Wolbachia are widely distributed endosymbiotic bacteria that influence the reproduction and fitness of their hosts. In recent years the manipulation of Wolbachia infection has been considered as a potential tool for biological control. The coffee berry borer (CBB), Hypothenemus hampei, is the most devastating coffee pest worldwide. Wolbachia infection in the CBB has been reported, but until now the role of Wolbachia in CBB reproduction and fitness has not been tested. To address this issue we reared the CBB in artificial diets with and without tetracycline (0.1% w/v) for ten generations. Tetracycline reduced significantly the relative proportion of Wolbachia in the CBB microbiota from 0.49% to 0.04%. This reduction affected CBB reproduction: females fed with tetracycline had significantly fewer progeny, lower fecundity, and fewer eggs per female. Tetracycline also reduced the population growth rate (λ), net reproductive rate (R0), and mean generation time (T) in CBB; the reduction in population growth was mostly due to variation in fertility, according to life time response experiments (LTREs) analysis. Our results suggest that Wolbachia contribute to the reproductive success of the CBB and their manipulation represents a possible approach to CBB biocontrol mediated by microbiome management.

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“…We chose to look at the impact of cholesterol on virus growth in Wolbachia-infected cells because Wolbachia bacteria have been shown to compete with the host for cholesterol, lipids, and amino acids (43,44). Wolbachia protection from Drosophila C virus is dependent on cholesterol in Drosophila (37).…”

Section: Discussionmentioning

confidence: 99%

Variable Inhibition of Zika Virus Replication by Different Wolbachia Strains in Mosquito Cell Cultures

Schultz

Isern

Michael

et al. 2017

J Virol

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Mosquito-borne arboviruses are a major source of human disease. One strategy to reduce arbovirus disease is to reduce the mosquito's ability to transmit virus. Mosquito infection with the bacterial endosymbiont Wolbachia pipientis wMel is a novel strategy to reduce Aedes mosquito competency for flavivirus infection. However, experiments investigating cyclic environmental temperatures have shown a reduction in maternal transmission of wMel, potentially weakening the integration of this strain into a mosquito population relative to that of other Wolbachia strains. Consequently, it is important to investigate additional Wolbachia strains. All Zika virus (ZIKV) suppression studies are limited to the wMel Wolbachia strain. Here we show ZIKV inhibition by two different Wolbachia strains: wAlbB (isolated from Aedes albopictus mosquitoes) and wStri (isolated from the planthopper Laodelphax striatellus) in mosquito cells. Wolbachia strain wStri inhibited ZIKV most effectively. Singlecycle infection experiments showed that ZIKV RNA replication and nonstructural protein 5 translation were reduced below the limits of detection in wStri-containing cells, demonstrating early inhibition of virus replication. ZIKV replication was rescued when Wolbachia was inhibited with a bacteriostatic antibiotic. We observed a partial rescue of ZIKV growth when Wolbachia-infected cells were supplemented with cholesterol-lipid concentrate, suggesting competition for nutrients as one of the possible mechanisms of Wolbachia inhibition of ZIKV. Our data show that wAlbB and wStri infection causes inhibition of ZIKV, making them attractive candidates for further in vitro mechanistic and in vivo studies and future vector-centered approaches to limit ZIKV infection and spread.IMPORTANCE Zika virus (ZIKV) has swiftly spread throughout most of the Western Hemisphere. This is due in large part to its replication in and spread by a mosquito vector host. There is an urgent need for approaches that limit ZIKV replication in mosquitoes. One exciting approach for this is to use a bacterial endosymbiont called Wolbachia that can populate mosquito cells and inhibit ZIKV replication. Here we show that two different strains of Wolbachia, wAlbB and wStri, are effective at repressing ZIKV in mosquito cell lines. Repression of virus growth is through the inhibition of an early stage of infection and requires actively replicating Wolbachia. Our findings further the understanding of Wolbachia viral inhibition and provide novel tools that can be used in an effort to limit ZIKV replication in the mosquito vector, thereby interrupting the transmission and spread of the virus.KEYWORDS Wolbachia, Zika virus, arthropod vectors, vector biology

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Wolbachia Modulates Lipid Metabolism in Aedes albopictus Mosquito Cells

Cited by 100 publications

References 69 publications

Reliance of Wolbachia on High Rates of Host Proteolysis Revealed by a Genome-Wide RNAi Screen of Drosophila Cells

Reliance of Wolbachia on High Rates of Host Proteolysis Revealed by a Genome-Wide RNAi Screen of Drosophila Cells

Wolbachia Affects Reproduction and Population Dynamics of the Coffee Berry Borer (Hypothenemus hampei): Implications for Biological Control

Variable Inhibition of Zika Virus Replication by Different Wolbachia Strains in Mosquito Cell Cultures

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