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A worm's best friend: recruitment of neutrophils by Wolbachia confounds eosinophil degranulation against the filarial nematode Onchocerca ochengi.

Hansen RD, Trees AJ, Bah GS, Hetzel U, Martin C, Bain O, Tanya VN, Makepeace BL - Proc. Biol. Sci. (2010)

Bottom Line: 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.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.

View Article: PubMed Central - PubMed

Affiliation: Liverpool School of Tropical Medicine, School of Veterinary Science and Institute of Infection and Global Health, University of Liverpool, , Liverpool L69 7ZJ, UK.

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.

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Related in: MedlinePlus

Quantification of bovine transcripts (normalized against 28S rRNA) for the neutrophilic chemokines (a) interleukin-8 (IL-8) and (b) the growth-regulated (GRO) protein family in onchocercomata treated with oxytetracycline (n = 6) or melarsomine (n = 5), or in the absence of treatment (n = 5). Lines represent the mean ± s.e. (a,b) Dotted line, control; dashed line, melarsomine; solid line, oxytetracycline.
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RSPB20102367F4: Quantification of bovine transcripts (normalized against 28S rRNA) for the neutrophilic chemokines (a) interleukin-8 (IL-8) and (b) the growth-regulated (GRO) protein family in onchocercomata treated with oxytetracycline (n = 6) or melarsomine (n = 5), or in the absence of treatment (n = 5). Lines represent the mean ± s.e. (a,b) Dotted line, control; dashed line, melarsomine; solid line, oxytetracycline.

Mentions: To assess local cellular immune responses to different treatments in the bovine host, transcripts for key cytokines involved in the activation and chemotaxis of neutrophils (interleukin-8 (IL-8) and growth-regulated (GRO) family) and eosinophils (IL-5 and eotaxin) were quantified between 8 and 24 wpt. In the OXY group, the IL-8 : 28S rRNA ratio was significantly lower than that observed in the CON group (figure 4a; GLM repeated measures, Tukey's post hoc test: mean difference = −1.0 log, p = 0.010; see the electronic supplementary material, appendix S4, for additional statistical details); whereas in the MEL group, IL-8 levels were not significantly different to those in CON nodules (Tukey's test: mean difference = −0.7 log, p = 0.107). Similarly, the GRO : 28S rRNA ratio was significantly reduced in the OXY group relative to CON levels (figure 4b; GLM repeated measures, Tukey's post hoc test: mean difference = −0.7 log, p = 0.044), but not between the MEL and CON groups (Tukey's post hoc test: mean difference = −0.4 log, p = 0.296). However, neither treatment had a significant effect on the expression of IL-5 (GLM repeated measures, Tukey's post hoc test, MEL versus CON: mean difference = 0.09 log, p = 0.918; OXY versus CON: mean difference = −0.03 log, p = 0.991; data not shown) or eotaxin genes (GLM repeated measures, Tukey's post hoc test, MEL versus CON: mean difference = −0.5 log, p = 0.641; OXY versus CON: mean difference = −0.3 log, p = 0.814; data not shown).Figure 4.


A worm's best friend: recruitment of neutrophils by Wolbachia confounds eosinophil degranulation against the filarial nematode Onchocerca ochengi.

Hansen RD, Trees AJ, Bah GS, Hetzel U, Martin C, Bain O, Tanya VN, Makepeace BL - Proc. Biol. Sci. (2010)

Quantification of bovine transcripts (normalized against 28S rRNA) for the neutrophilic chemokines (a) interleukin-8 (IL-8) and (b) the growth-regulated (GRO) protein family in onchocercomata treated with oxytetracycline (n = 6) or melarsomine (n = 5), or in the absence of treatment (n = 5). Lines represent the mean ± s.e. (a,b) Dotted line, control; dashed line, melarsomine; solid line, oxytetracycline.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3119012&req=5

RSPB20102367F4: Quantification of bovine transcripts (normalized against 28S rRNA) for the neutrophilic chemokines (a) interleukin-8 (IL-8) and (b) the growth-regulated (GRO) protein family in onchocercomata treated with oxytetracycline (n = 6) or melarsomine (n = 5), or in the absence of treatment (n = 5). Lines represent the mean ± s.e. (a,b) Dotted line, control; dashed line, melarsomine; solid line, oxytetracycline.
Mentions: To assess local cellular immune responses to different treatments in the bovine host, transcripts for key cytokines involved in the activation and chemotaxis of neutrophils (interleukin-8 (IL-8) and growth-regulated (GRO) family) and eosinophils (IL-5 and eotaxin) were quantified between 8 and 24 wpt. In the OXY group, the IL-8 : 28S rRNA ratio was significantly lower than that observed in the CON group (figure 4a; GLM repeated measures, Tukey's post hoc test: mean difference = −1.0 log, p = 0.010; see the electronic supplementary material, appendix S4, for additional statistical details); whereas in the MEL group, IL-8 levels were not significantly different to those in CON nodules (Tukey's test: mean difference = −0.7 log, p = 0.107). Similarly, the GRO : 28S rRNA ratio was significantly reduced in the OXY group relative to CON levels (figure 4b; GLM repeated measures, Tukey's post hoc test: mean difference = −0.7 log, p = 0.044), but not between the MEL and CON groups (Tukey's post hoc test: mean difference = −0.4 log, p = 0.296). However, neither treatment had a significant effect on the expression of IL-5 (GLM repeated measures, Tukey's post hoc test, MEL versus CON: mean difference = 0.09 log, p = 0.918; OXY versus CON: mean difference = −0.03 log, p = 0.991; data not shown) or eotaxin genes (GLM repeated measures, Tukey's post hoc test, MEL versus CON: mean difference = −0.5 log, p = 0.641; OXY versus CON: mean difference = −0.3 log, p = 0.814; data not shown).Figure 4.

Bottom Line: 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.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.

View Article: PubMed Central - PubMed

Affiliation: Liverpool School of Tropical Medicine, School of Veterinary Science and Institute of Infection and Global Health, University of Liverpool, , Liverpool L69 7ZJ, UK.

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.

Show MeSH
Related in: MedlinePlus