In vivo imaging of tissue eosinophilia and eosinopoietic responses to schistosome worms and eggs

Davies, Stephen J.; Smith, Steven J.; Lim, K. C.; Zhang, Hongbing; Purchio, Anthony F.; McKerrow, James H.; West, David B.

doi:10.1016/j.ijpara.2005.02.017

Cited by 23 publications

(15 citation statements)

References 43 publications

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“…However, there are reasons to suspect that responses to schistosome worms during prepatent infection are more complex. First, there is evidence of both circulating eosinophilia [26] and increased eosinopoiesis [27] during the first weeks of infection, responses typically mediated by the Th2 cytokine IL-5 [4]. Second, analyses of cutaneous responses to cercariae suggest that invading schistosome larvae stimulate a mixed T helper response in the skin, with evidence of both Th1 and Th2 polarization at the site of infection [28, 29].…”

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Induction of Type 2 Responses by Schistosome Worms during Prepatent Infection

et al. 2010

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During natural schistosome infection, the induction of T helper type 2 (Th2) responses has been ascribed to parasite eggs, because exposure of the host to this life-cycle stage elicits a polarized Th2 response to egg antigens. In the present study, we show that schistosome worms also elicit systemic, antigen-specific type 2 responses during prepatent infection, before egg deposition begins. CD4+ T cells producing interleukin (IL)–4 were induced by both male and female worms during single-sex infections, demonstrating that this response is independent of exposure to eggs. The Th2 response was accompanied by production of immunoglobulin E and the sensitization of circulating basophils to produce additional IL-4 in response to schistosome antigens. Together, our data show that schistosome worms establish an immunologic milieu where CD4+ T cells and basophils are both primed to produce IL-4 before eggs are laid, suggesting that worms play a role in establishment of the Th2 response that is critical for host survival and parasite transmission.

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Induction of Type 2 Responses by Schistosome Worms during Prepatent Infection

et al. 2010

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“…Eosinophils are also considered important against several parasitic infections, particularly against helminths (21,26). In Schistosoma mansoni infection, eosinophils constitute a prominent cell type in granulomas, and there is increased eosinophilopoiesis on infection (27), a process dependent on the interleukin (IL)-5 secreted during Th2 response to eggs (28,29). Mice deficient in IL-5, which have decreased eosinophilopoiesis, present reduced liver granuloma sizes with decreased numbers of eosinophils on S. mansoni infection (30).…”

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confidence: 99%

“…Mice deficient in IL-5, which have decreased eosinophilopoiesis, present reduced liver granuloma sizes with decreased numbers of eosinophils on S. mansoni infection (30). In fact, eosinophils have been found to kill the S. mansoni parasite in vitro (26) and to invade dying and sick schistosomes in vivo (29), suggesting that they might be an important defense mechanism against the parasite. However, two mouse lineages deficient in eosinophils were recently studied on S. mansoni infection and found to have no gross alterations in worm burden, granuloma formation, or liver fibrosis (31).…”

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Macrophage migration inhibitory factor is critical to interleukin‐5‐driven eosinophilopoiesis and tissue eosinophilia triggered by Schistosoma mansoni infection

Magalhães¹,

Paiva²,

Souza³

et al. 2008

FASEB j.

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Macrophage migration inhibitory factor (MIF) participates in the pathogenesis of inflammatory diseases, including asthma, in which it enhances airway hypersensitivity and tissue eosinophilia. Herein, we investigated the role of MIF in eosinophilopoiesis and tissue eosinophilia using Schistosoma mansoni infection. MIF-deficient (Mif(-/-)) mice had similar numbers of adult worms, eggs, and granulomas compared to wild-type mice, but the size of granulomas was strikingly reduced due to smaller numbers of eosinophils. MIF did not affect the acquired response to infection, as Mif(-/-) mice produced normal amounts of Th2 cytokines and IgE. Nevertheless, recombinant MIF (rMIF) behaved as a chemoattractant for eosinophils, what could partially explain the reduced eosinophilia in infected Mif(-/-) mice. Moreover, the percentage of eosinophils was reduced in bone marrows of Mif(-/-) mice chronically infected with S. mansoni compared to wild type. Mif(-/-) had impaired eosinophilopoiesis in response to interleukin (IL)-5 and addition of rMIF to bone marrow cultures from IL-5 transgenic mice enhanced the generation of eosinophils. In the absence of MIF, eosinophil precursors were unable to survive the IL-5-supplemented cell culture, and were ingested by macrophages. Treatment with pancaspase inhibitor z-VAD or rMIF promoted the survival of eosinophil progenitors. Together, these results indicate that MIF participates in IL-5-driven maturation of eosinophils and in tissue eosinophilia associated with S. mansoni infection.

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“…Adoptive transfer of radioactively labeled eosinophils into helminth-infected rats demonstrated their recruitment to the lung and intestine according to the known migration pattern of the parasites (9). Recently, transgenic mice expressing luciferase in eosinophils were used to demonstrate eosinophil migration in mice during infection with Schistosoma mansoni (10). The strength of this technique is the possibility to perform noninvasive real-time measurements of the kinetics of eosinophil migration in the same animal over a long time period.…”

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Analysis of Eosinophil Turnover In Vivo Reveals Their Active Recruitment to and Prolonged Survival in the Peritoneal Cavity

Ohnmacht

Pullner

Rooijen

et al. 2007

The Journal of Immunology

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Eosinophils are potent effector cells associated with allergic inflammation and parasite infections. However, limited information exists about their turnover, migration, and survival in vivo. To address these important questions, we determined murine eosinophil turnover under steady state and inflammatory conditions by flow cytometric analysis of BrdU incorporation and analyzed their migration pattern and survival in different tissues after adoptive transfer into recipient mice. In naive mice ∼50% of bone marrow eosinophils were labeled with BrdU during a 15-h pulse, whereas only 10% of splenic eosinophils were labeled within this time frame. Unexpectedly, the rate of eosinophil production did not change during acute infection with the helminth parasite Nippostrongylus brasiliensis despite massive eosinophilia in several tissues. Eosinophils present in lung and peritoneum remained largely BrdU negative, indicating that eosinophilia in end organs was mainly caused by increased survival of already existing eosinophils rather than increased production of new eosinophils in the bone marrow. Adoptive transfer experiments revealed that eosinophils preferentially migrated to the peritoneum in a macrophage-independent and pertussis toxin-sensitive manner, where they survived for several days. Peritoneal eosinophils expressed high levels of the inhibitory receptor Siglec-F, released less eosinophil peroxidase compared with eosinophils from the spleen, and could recirculate to other organs. These results demonstrate that the peritoneum serves as reservoir for eosinophils.

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In vivo imaging of tissue eosinophilia and eosinopoietic responses to schistosome worms and eggs

Cited by 23 publications

References 43 publications

Induction of Type 2 Responses by Schistosome Worms during Prepatent Infection

Induction of Type 2 Responses by Schistosome Worms during Prepatent Infection

Macrophage migration inhibitory factor is critical to interleukin‐5‐driven eosinophilopoiesis and tissue eosinophilia triggered by Schistosoma mansoni infection

Analysis of Eosinophil Turnover In Vivo Reveals Their Active Recruitment to and Prolonged Survival in the Peritoneal Cavity

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