Abstract
Onchocerca ochengi, a filarial parasite of cattle, represents the closest relative of the human pathogen, Onchocerca volvulus. Both species harbour Wolbachia endosymbionts and are remarkable in that adult female worms remain viable but sessile for many years while surrounded by host cells and antibodies. The basis of the symbiosis between filariae and Wolbachia is thought to be metabolic, although a role for Wolbachia in immune evasion has received little attention. Neutrophils are attracted to Wolbachia, but following antibiotic chemotherapy they are replaced by eosinophils that degranulate on the worm cuticle. However, it is unclear whether the eosinophils are involved in parasite killing or if they are attracted secondarily to dying worms. In this study, cattle infected with Onchocerca ochengi received adulticidal regimens of oxytetracycline or melarsomine. In contrast to oxytetracycline, melarsomine did not directly affect Wolbachia viability. Eosinophil degranulation increased significantly only in the oxytetracycline group; whereas nodular gene expression of bovine neutrophilic chemokines was lowest in this group. Moreover, intense eosinophil degranulation was initially associated with worm vitality, not degeneration. Taken together, these data offer strong support for the hypothesis that Wolbachia confers longevity on O. ochengi through a defensive mutualism, which diverts a potentially lethal effector cell response.
Highlights
The maternally transmitted a-proteobacterium, Wolbachia, infects an estimated two-thirds of all arthropod species [1], but it has a more limited distribution in certain parasitic nematodes
Filarial nematodes harbouring Wolbachia cause two major neglected tropical diseases, lymphatic filariasis and onchocerciasis (River Blindness), which are responsible for a combined global morbidity of greater than 6 million disability-adjusted life-years [9]
Eosinophils were implicated in worm killing because a relatively short, non-adulticidal antibiotic regimen caused a transient depletion of Wolbachia and a partial transition in the nodule towards eosinophilia
Summary
The maternally transmitted a-proteobacterium, Wolbachia, infects an estimated two-thirds of all arthropod species [1], but it has a more limited distribution in certain parasitic nematodes (the family Onchocercidae, superfamily Filarioidea, order Spirurida [2,3]; and the family Pratylenchidae, order Tylenchida [4]). One group was treated with melarsomine (MEL; Cymelarsan, Merial) solution at 4 mg kg intravenously, every other day for 3 days, which has been demonstrated to be 100 per cent adulticidal [23] This drug kills the majority of worms by 20 weeks, some nodules containing fragments of degenerated parasites may persist for several years after treatment [18]. A modest increase in the eosinophil : neutrophil ratio was observed in the MEL group, culminating in a shift towards eosinophilia in resolving nodules at the termination of the experiment, this was not statistically significant (figure 1a; Friedman test: x2 1⁄4 6.0, p 1⁄4 0.473). There was a marked, statistically significant peak in DE in the OXY group at 12 wpt (figure 1c; Friedman test: x2 1⁄4 11.9, p 1⁄4 0.042) and the maximum score of 3 (greater than 10 DE per worm section) was only recorded . One-hundred-and-forty such clusters were identified, 89 per cent of which were in OXY-treated onchocercomata
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