Brugia pahangi:Differential Induction and Regulation of Jird Inflammatory Responses by Life-Cycle Stages

Nasarre, Carmen; Coleman, Sharon U.; Rao, U. R.; Klei, Thomas R.

doi:10.1006/expr.1997.4179

Cited by 11 publications

(12 citation statements)

References 26 publications

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“…Approximately 30 years ago, several researchers reported intracellular bacteria in filarial nematodes (31,37,54). These bacteria have since been identified as relatives of the arthropod symbiont Wolbachia (46).…”

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Removal of Wolbachia from Brugia pahangi Is Closely Linked to Worm Death and Fecundity but Does Not Result in Altered Lymphatic Lesion Formation in Mongolian Gerbils ( Meriones unguiculatus )

Chirgwin¹,

Coleman²,

Porthouse³

et al. 2003

Infect Immun

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Approximately 30 years ago, researchers reported intracellular bacteria in filarial nematodes. These bacteria are relatives of the arthropod symbiont Wolbachia and occur in many filarial nematodes, including Brugia pahangi and Brugia malayi. Wolbachia bacteria have been implicated in a variety of roles, including filaria development and fecundity and the pathogenesis of lymphatic lesions associated with filarial infections. However, the role of the bacteria in worm biology or filarial disease is still not clear. The present experiments support previous data showing that tetracycline eliminates or reduces Wolbachia bacteria in B. pahangi in vivo. The elimination of Wolbachia was closely linked to a reduction in female fecundity and the viability of both sexes, suggesting that the killing of Wolbachia is detrimental to B. pahangi. The gerbils treated with tetracycline showed reduced levels of interleukin-4 (IL-4) and IL-5 mRNA in renal lymph nodes and spleens compared with the levels in B. pahangi-infected gerbils not treated with tetracycline. However, similar findings were noted in B. pahangi-infected gerbils treated with ivermectin, suggesting that the loss of circulating microfilariae, not the reduction of Wolbachia bacteria, was associated with the altered cytokine profile. Despite the change in T-cell cytokines, there was no difference in the sizes of renal lymph nodes isolated from gerbils in each treatment group. Furthermore, the numbers, sizes, or cellular compositions of granulomas examined in the lymphatics or renal lymph nodes did not differ with treatment. These data suggest that Wolbachia may not play a primary role in the formation of lymphatic lesions in gerbils chronically infected with B. pahangi.Lymphatic filariasis is caused primarily by the filarial nematodes Wuchereria bancrofti and Brugia malayi and affects more than 120 million people throughout the tropics and subtropics. The disease presents as a broad range of clinical and subclinical symptoms, including fever, acute and chronic inflammation, lymphatic edema, and elephantiasis. While much research has focused on the disease caused by infection with Brugia or Wuchereria, the mechanism(s) underlying the pathogenesis of lymphatic filariasis has not been clearly defined. In both acute and chronic infections, these mechanisms probably involve a diverse range of inflammatory reactions attributable to the parasite, host inflammatory responses, and opportunistic infections (40).Approximately 30 years ago, several researchers reported intracellular bacteria in filarial nematodes (31, 37, 54). These bacteria have since been identified as relatives of the arthropod symbiont Wolbachia (46). Wolbachia bacteria have now been reported to exist in many filarial nematodes, including B. malayi and Brugia pahangi (3,30,49,55). Interestingly, Wolbachia has recently been proposed to play a role in the induction of the host immune response to filariae (9,44,50,51). Some researchers suggest that lipopolysaccharide (LPS)-like molecules from filarial Wolbachia b...

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“…and the inflammatory lesions associated with lymphatic filariasis (1,2,16,21,27,32,37,38). Gerbils develop chronic infections with B. pahangi that result in lymphatic damage through the formation of well-characterized granulomatous lesions (21,54).…”

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confidence: 99%

Removal of Wolbachia from Brugia pahangi Is Closely Linked to Worm Death and Fecundity but Does Not Result in Altered Lymphatic Lesion Formation in Mongolian Gerbils ( Meriones unguiculatus )

Chirgwin¹,

Coleman²,

Porthouse³

et al. 2003

Infect Immun

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“…Gerbils are excellent animal models for studying diseases caused by filarial nematodes Nasarre et al, 1997;Storey, 1993). They have been used extensively to investigate serious human diseases such as lymphatic filariasis caused by Wuchereria bancrofti (Cross et al, 1981;Zielke, 1979) and Brugia malayi (Li et al, 1991;Partono and Purnomo, 1987;Trpis, 1994).…”

Section: Use In Researchmentioning

confidence: 99%

“…Wuchereria bancrofti and B. malayi are responsible for 90% and 10%, respectively, of the 90 million infections worldwide in Latin America, sub-Saharan Africa, and Southeast Asia. Other filarial nematodes used in gerbils include B. pahangi (Nasarre et al, 1997) and Loa loa, the African eye worm (Suswillo et al, 1977;Wanji et al, 2002). Other filarial nematodes used in gerbils include B. pahangi (Nasarre et al, 1997) and Loa loa, the African eye worm (Suswillo et al, 1977;Wanji et al, 2002).…”

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confidence: 99%

Biology and Diseases of Other Rodents

Donnelly

Bergin

Ihrig

2015

Laboratory Animal Medicine

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“…However, the lack of long-term parasite survival and the nonpermissive nature of most strains of mice suggest that infection in these animals may not truly mimic human infection, thereby limiting the usefulness of this model. The Mongolian gerbil (Meriones unguiculatus) has proven to be an excellent permissive rodent model for the study of lymphatic filariasis using B. pahangi (21,22,42) or B. malayi (40). Upon infection, gerbils develop chronic infections with persistent microfilaremia and are susceptible to reinfection (33).…”

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Infection Outcome and Cytokine Gene Expression inBrugia pahangi- Infected Gerbils (Meriones unguiculatus) Sensitized withBrucella abortus

et al. 2002

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Filarial infections have been associated with the development of a strongly polarized Th2 host immune response and a severe impairment of mitogen-driven proliferation and type 1 cytokine production in mice and humans. The role of this polarization in the development of the broad spectra of clinical manifestations of lymphatic filariasis is still unknown. Recently, data gathered from humans as well as from immunocompromised mouse models suggest that filariasis elicits a complex host immune response involving both Th1 and Th2 components. However, responses of a similar nature have not been reported in immunologically intact permissive models of Brugia infection. Brucella abortus-killed S19 was inoculated into the Brugia-permissive gerbil host to induce gamma interferon (IFN-␥) production. Gerbils were then infected with B. pahangi, and the effect of the polarized Th1 responses on worm establishment and host cellular response was measured. Animals infected with both B. abortus and B. pahangi showed increased IFN-␥ and interleukin-10 (IL-10) and decreased IL-4 and IL-5 mRNA levels compared with those in animals infected with B. pahangi alone. These data suggest that the prior sensitization with B. abortus may induce a down regulation of the Th2 response associated with Brugia infection. This reduced Th2 response was associated with a reduced eosinophilia and an increased neutrophilia in the peritoneal exudate cells. The changes in cytokine and cellular environment did not inhibit the establishment of B. pahangi intraperitoneally. The data presented here suggest a complex relationship between the host immune response and parasite establishment and survival that cannot be simply ascribed to the Th1/Th2 paradigm.Human lymphatic filariasis, caused by the filarial nematodes Wuchereria bancrofti and Brugia malayi, affects a large proportion of people in tropical and subtropical regions of the world. Infection in humans is accompanied by the development of a prominent Th2-type host response, reflected by an expansion of interleukin-4 (IL-4)-and IL-5-producing CD4 ϩ cells, an increase in serum immunoglobulin E (IgE) and IgG4 levels, (20,24), and a pronounced eosinophilia (20). This response is accompanied by a severe impairment of mitogen-driven proliferation and IL-2 and gamma interferon (IFN-␥) production in mice and humans (36).In regions of endemic filariasis, most infected individuals are microfilaremic but asymptomatic and are considered to be immunologically hyporesponsive to filariae. These impaired responses to filarial antigens are manifested by a reduction in T-cell proliferation (43,46,48) and impaired production of immunoglobulin to parasite antigens in vitro (44). In contrast, patients who develop pathological signs such as elephantiasis are characteristically amicrofilaremic and mount strong cellular and humoral immune responses to the parasite. These responses, in conjunction with extrinsic immune-independent factors, are reported to contribute to the pathological changes observed in such people (13).The que...

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Brugia pahangi:Differential Induction and Regulation of Jird Inflammatory Responses by Life-Cycle Stages

Cited by 11 publications

References 26 publications

Removal of Wolbachia from Brugia pahangi Is Closely Linked to Worm Death and Fecundity but Does Not Result in Altered Lymphatic Lesion Formation in Mongolian Gerbils ( Meriones unguiculatus )

Removal of Wolbachia from Brugia pahangi Is Closely Linked to Worm Death and Fecundity but Does Not Result in Altered Lymphatic Lesion Formation in Mongolian Gerbils ( Meriones unguiculatus )

Biology and Diseases of Other Rodents

Infection Outcome and Cytokine Gene Expression inBrugia pahangi- Infected Gerbils (Meriones unguiculatus) Sensitized withBrucella abortus

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