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Anti-filarial Activity of Antibiotic Therapy Is Due to Extensive Apoptosis after Wolbachia Depletion from Filarial Nematodes
Open accessAbstract
Filarial nematodes maintain a mutualistic relationship with the endosymbiont Wolbachia. Depletion of Wolbachia produces profound defects in nematode development, fertility and viability and thus has great promise as a novel approach for treating filarial diseases. However, little is known concerning the basis for this mutualistic relationship. Here we demonstrate using whole mount confocal microscopy that an immediate response to Wolbachia depletion is extensive apoptosis in the adult germline, and in the somatic cells of the embryos, microfilariae and fourth-stage larvae (L4). Surprisingly, apoptosis occurs in the majority of embryonic cells that had not been infected prior to antibiotic treatment. In addition, no apoptosis occurs in the hypodermal chords, which are populated with large numbers of Wolbachia, although disruption of the hypodermal cytoskeleton occurs following their depletion. Thus, the induction of apoptosis upon Wolbachia depletion is non-cell autonomous and suggests the involvement of factors originating from Wolbachia in the hypodermal chords. The pattern of apoptosis correlates closely with the nematode tissues and processes initially perturbed following depletion of Wolbachia, embryogenesis and long-term sterilization, which are sustained for several months until the premature death of the adult worms. Our observations provide a cellular mechanism to account for the sustained reductions in microfilarial loads and interruption of transmission that occurs prior to macrofilaricidal activity following antibiotic therapy of filarial nematodes.
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“Those studies showed that the elimination of Wolbachia induces the extensive apoptosis of germ cells in adults and of somatic cells in embryos, microfilariae, and L4 larvae but not in hypodermal cords”
From Human and animal dirofilariasis: The emergence of a zoonotic mosaic (2012) · cites this paper as [222]
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“suggesting that symbiotic bacteria regulate apoptosis in the nematodes that host them.”
From Human and animal dirofilariasis: The emergence of a zoonotic mosaic (2012) · cites this paper as [222]
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Metadata
- Authors
- Landmann, F., Voronin, D., Sullivan, W., & Taylor, M. J.
- Affiliations
- Liverpool School of Tropical Medicine (GB)
- University of California, Santa Cruz (US)
- Corresponding author
- Taylor, Mark J.
- Venue
- PLoS Pathogens
- Publisher
- Public Library of Science (PLoS)
- Published
- 2011-11-03
- Volume
- 7
- Issue
- 11
- Pages
- e1002351
- ISSN
- 1553-7366 (ISSN-L)
- 1553-7374
- PMC
- PMC3207916
- OpenAlex
- W2135804039
- Cited by
- 134
- References
- 34
- Citations by year
- 2026: 6 · 2025: 9 · 2024: 8 · 2023: 10 · 2022: 11 · 2021: 5 · 2020: 15 · 2019: 7 · 2018: 12 · 2017: 6 · 2016: 11 · 2015: 7 · 2014: 10 · 2013: 7 · 2012: 9
- FWCI
- 5.83
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- PLoS Pathogens (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- LSTM Online Archive (Liverpool School of Tropical Medicine) (acceptedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- Bill and Melinda Gates Foundation
- Topics
- Health Sciences › Medicine › Infectious Diseases › Parasitic Diseases Research and Treatment
- Life Sciences › Immunology and Microbiology › Parasitology › Parasites and Host Interactions
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Nematode management and characterization studies
- Keywords
- filarial nematodes, apoptosis, antibiotic therapy, cytoskeleton disruption, embryonic development, microfilariae, fourth-stage larvae, transmission interruption
- MeSH terms
- Animals, Anti-Bacterial Agents, Doxycycline, Female, Filariasis, Gerbillinae, Humans, Larva, Male, Symbiosis, Tetracycline, Helminth Proteins, Brugia malayi, Apoptosis, In Situ Nick-End Labeling, Wolbachia, Caspase 3
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