Parasitic infection improves survival from septic peritonitis by enhancing mast cell responses to bacteria in mice.
Mammals are serially infected with a variety of microorganisms, including bacteria and parasites. Each infection reprograms the immune system's responses to re-exposure and potentially alters responses to first-time infection by different microorganisms. To examine whether infection with a meta...
| Main Authors: | , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Public Library of Science (PLoS)
2011-01-01
|
| Series: | PLoS ONE |
| Online Access: | http://europepmc.org/articles/PMC3217977?pdf=render |
| _version_ | 1818484074718691328 |
|---|---|
| author | Rachel E Sutherland Xiang Xu Sophia S Kim Eric J Seeley George H Caughey Paul J Wolters |
| author_facet | Rachel E Sutherland Xiang Xu Sophia S Kim Eric J Seeley George H Caughey Paul J Wolters |
| author_sort | Rachel E Sutherland |
| collection | DOAJ |
| description | Mammals are serially infected with a variety of microorganisms, including bacteria and parasites. Each infection reprograms the immune system's responses to re-exposure and potentially alters responses to first-time infection by different microorganisms. To examine whether infection with a metazoan parasite modulates host responses to subsequent bacterial infection, mice were infected with the hookworm-like intestinal nematode Nippostrongylus brasiliensis, followed in 2-4 weeks by peritoneal injection of the pathogenic bacterium Klebsiella pneumoniae. Survival from Klebsiella peritonitis two weeks after parasite infection was better in Nippostrongylus-infected animals than in unparasitized mice, with Nippostrongylus-infected mice having fewer peritoneal bacteria, more neutrophils, and higher levels of protective interleukin 6. The improved survival of Nippostrongylus-infected mice depends on IL-4 because the survival benefit is lost in mice lacking IL-4. Because mast cells protect mice from Klebsiella peritonitis, we examined responses in mast cell-deficient Kit(W-sh)/Kit(W-sh) mice, in which parasitosis failed to improve survival from Klebsiella peritonitis. However, adoptive transfer of cultured mast cells to Kit(W-sh)/Kit(W-sh) mice restored survival benefits of parasitosis. These results show that recent infection with Nippostrongylus brasiliensis protects mice from Klebsiella peritonitis by modulating mast cell contributions to host defense, and suggest more generally that parasitosis can yield survival advantages to a bacterially infected host. |
| first_indexed | 2024-12-10T15:50:34Z |
| format | Article |
| id | doaj.art-6529f34e57034673a0907a340c66d092 |
| institution | Directory Open Access Journal |
| issn | 1932-6203 |
| language | English |
| last_indexed | 2024-12-10T15:50:34Z |
| publishDate | 2011-01-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS ONE |
| spelling | doaj.art-6529f34e57034673a0907a340c66d0922022-12-22T01:42:49ZengPublic Library of Science (PLoS)PLoS ONE1932-62032011-01-01611e2756410.1371/journal.pone.0027564Parasitic infection improves survival from septic peritonitis by enhancing mast cell responses to bacteria in mice.Rachel E SutherlandXiang XuSophia S KimEric J SeeleyGeorge H CaugheyPaul J WoltersMammals are serially infected with a variety of microorganisms, including bacteria and parasites. Each infection reprograms the immune system's responses to re-exposure and potentially alters responses to first-time infection by different microorganisms. To examine whether infection with a metazoan parasite modulates host responses to subsequent bacterial infection, mice were infected with the hookworm-like intestinal nematode Nippostrongylus brasiliensis, followed in 2-4 weeks by peritoneal injection of the pathogenic bacterium Klebsiella pneumoniae. Survival from Klebsiella peritonitis two weeks after parasite infection was better in Nippostrongylus-infected animals than in unparasitized mice, with Nippostrongylus-infected mice having fewer peritoneal bacteria, more neutrophils, and higher levels of protective interleukin 6. The improved survival of Nippostrongylus-infected mice depends on IL-4 because the survival benefit is lost in mice lacking IL-4. Because mast cells protect mice from Klebsiella peritonitis, we examined responses in mast cell-deficient Kit(W-sh)/Kit(W-sh) mice, in which parasitosis failed to improve survival from Klebsiella peritonitis. However, adoptive transfer of cultured mast cells to Kit(W-sh)/Kit(W-sh) mice restored survival benefits of parasitosis. These results show that recent infection with Nippostrongylus brasiliensis protects mice from Klebsiella peritonitis by modulating mast cell contributions to host defense, and suggest more generally that parasitosis can yield survival advantages to a bacterially infected host.http://europepmc.org/articles/PMC3217977?pdf=render |
| spellingShingle | Rachel E Sutherland Xiang Xu Sophia S Kim Eric J Seeley George H Caughey Paul J Wolters Parasitic infection improves survival from septic peritonitis by enhancing mast cell responses to bacteria in mice. PLoS ONE |
| title | Parasitic infection improves survival from septic peritonitis by enhancing mast cell responses to bacteria in mice. |
| title_full | Parasitic infection improves survival from septic peritonitis by enhancing mast cell responses to bacteria in mice. |
| title_fullStr | Parasitic infection improves survival from septic peritonitis by enhancing mast cell responses to bacteria in mice. |
| title_full_unstemmed | Parasitic infection improves survival from septic peritonitis by enhancing mast cell responses to bacteria in mice. |
| title_short | Parasitic infection improves survival from septic peritonitis by enhancing mast cell responses to bacteria in mice. |
| title_sort | parasitic infection improves survival from septic peritonitis by enhancing mast cell responses to bacteria in mice |
| url | http://europepmc.org/articles/PMC3217977?pdf=render |
| work_keys_str_mv | AT rachelesutherland parasiticinfectionimprovessurvivalfromsepticperitonitisbyenhancingmastcellresponsestobacteriainmice AT xiangxu parasiticinfectionimprovessurvivalfromsepticperitonitisbyenhancingmastcellresponsestobacteriainmice AT sophiaskim parasiticinfectionimprovessurvivalfromsepticperitonitisbyenhancingmastcellresponsestobacteriainmice AT ericjseeley parasiticinfectionimprovessurvivalfromsepticperitonitisbyenhancingmastcellresponsestobacteriainmice AT georgehcaughey parasiticinfectionimprovessurvivalfromsepticperitonitisbyenhancingmastcellresponsestobacteriainmice AT pauljwolters parasiticinfectionimprovessurvivalfromsepticperitonitisbyenhancingmastcellresponsestobacteriainmice |