Abstract
BackgroundThe Mongolian jird (Meriones unguiculatus) has long been recognized as a permissive host for the filarial parasite Brugia malayi; however, it is nonpermissive to another filarial parasite, canine heartworm (Dirofilaria immitis). By elucidating differences in the early response to infection, we sought to identify mechanisms involved in the species-specific clearance of these parasites. We hypothesized that the early clearance of D. immitis in intraperitoneal infection of the jird is immune mediated and parasite species dependent.MethodsJird peritoneal exudate cells (PECs) were isolated and their attachment to parasite larvae assessed in vitro under various conditions: D. immitis and B. malayi cultured separately, co-culture of both parasites, incubation before addition of cells, culture of heat-killed parasites, and culture with PECs isolated from jirds with mature B. malayi infection. The cells attaching to larvae were identified by immunohistochemistry.ResultsIn vitro cell attachment to live D. immitis was high (mean = 99.6%) while much lower for B. malayi (mean = 5.56%). This species-specific attachment was also observed when both filarial species were co-cultured, with no significant change from controls (U(9, 14) = 58.5, p = 0.999). When we replicated these experiments with PECs derived from jirds subcutaneously infected with B. malayi, the results were similar (99.4% and 4.72% of D. immitis and B. malayi, respectively, exhibited cell attachment). Heat-killing the parasites significantly reduced cell attachment to D. immitis (mean = 71.9%; U(11, 14) = 7.5, p < 0.001) while increasing attachment to B. malayi (mean = 16.7%; U(9, 15) = 20, p = 0.002). Cell attachment to both species was reduced when larvae were allowed a 24-h pre-incubation period prior to the addition of cells. The attaching cells were identified as macrophages by immunohistochemistry.ConclusionsThese results suggest a strongly species-dependent response from which B. malayi could not confer protection by proxy in co-culture. The changes in cell attachment following heat-killing and pre-incubation suggest a role for excretory/secretory products in host immune evasion and/or antigenicity. The nature of this attachment is the subject of ongoing study and may provide insight into filarial host specificity.Graphical
Highlights
The Mongolian jird (Meriones unguiculatus) has long been recognized as a permissive host for the filarial parasite Brugia malayi; it is nonpermissive to another filarial parasite, canine heartworm (Dirofilaria immitis)
In vitro culture When cultured separately, almost all D. immitis L3 demonstrated attachment by one or more jird-derived peritoneal exudate cells (PECs) when examined at 20 h, while B. malayi demonstrated very low levels of attachment; this difference was significant (U(14, 15) = 0, p < 0.001; Fig. 1)
Reducing E/S product release by heat-killing yielded significantly reduced cell attachment in D. immitis compared to the live control group (mean = 71.9%; U(11, 14) = 7.5, p < 0.001), while cell attachment to B. malayi was significantly increased (mean = 16.7%; U(9, 15) = 20, p = 0.002)
Summary
The Mongolian jird (Meriones unguiculatus) has long been recognized as a permissive host for the filarial parasite Brugia malayi; it is nonpermissive to another filarial parasite, canine heartworm (Dirofilaria immitis). The intraperitoneal route of infection, in which L3 are injected by needle into the peritoneal cavity, is useful in that adult worms largely remain confined therein and can be recovered; this is an advantage of the jird over other rodents, such as Mastomys spp., which do not support intraperitoneal infection [4, 5], and wild-type mouse strains, which are not permissive to B. malayi infection by any route [6, 7] This parasite has been demonstrated to reach maturity in certain immunodeficient mouse models [7,8,9]. To ascribe the permissivity of the jird in large part to its species-specific immunological characteristics
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