Early skin immunological disturbance after Plasmodium-infected mosquito bites

Silva, Henrique Borges da; Caetano, Susana S.; Monteiro, Isadora; Gómez-Conde, Iván; Hanson, Kirsten K.; Penha‐Gonçalves, Carlos; Olivieri, David N.; Mota, Maria M.; Marinho, Cláudio R. F.; Lima, Maria Regina D’Império; Tadokoro, Carlos E.

doi:10.1016/j.cellimm.2012.06.003

Cited by 20 publications

(17 citation statements)

References 28 publications

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“…This is supported by recent observations of induction of Treg migration in the skin of naive mice within 5-20 min following intradermal infection with malaria sporozoites (34). Hapten exposure has been shown to induce activation of an innate inflammatory response via pathways including release of danger-associated molecular patterns and pattern recognition receptor activation (28).…”

Section: Discussionsupporting

confidence: 55%

Dermal Regulatory T Cells Display Distinct Migratory Behavior That Is Modulated during Adaptive and Innate Inflammation

Chow

Mueller

Deane

et al. 2013

The Journal of Immunology

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Regulatory T cells (Tregs) are important in controlling skin inflammation, an effect dependent on their ability to home to this organ. However, little is known regarding their behavior in the skin. Here we used multiphoton imaging in Foxp3‐GFP mice to examine the behavior of endogenous Tregs in skin. While Tregs were readily detectable in the uninflamed dermis, most were non‐motile. Induction of contact sensitivity increased the proportion of motile Tregs, as well as inducing Treg recruitment. This response was significantly blunted in mice challenged with an irrelevant hapten, and by inhibition of effector cell recruitment, indicating a role for T cell‐dependent inflammation in induction of Treg migration. Moreover, induction of Treg migration was inhibited by local injection of a CCR4 antagonist, indicating a role for CCR4 in this response. Exposure of naïve mice to hapten also induced an increase in the proportion of migratory Tregs, demonstrating that innate signals can also induce Treg migration. Simultaneous examination of the migration of CD4+ effector cells and Tregs in the same region of uninflamed skin demonstrated that effector cells behaved differently, being uniformly highly migratory. These findings indicate that Treg behavior in skin differs from that of CD4+ effector cells, in that only a low proportion of Tregs are migratory under resting conditions. However, during inflammation the proportion of migratory Tregs increases, raising the possibility that this response may be important in controlling skin inflammation.

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Section: Discussionsupporting

confidence: 55%

Dermal Regulatory T Cells Display Distinct Migratory Behavior That Is Modulated during Adaptive and Innate Inflammation

Chow

Mueller

Deane

et al. 2013

The Journal of Immunology

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“…Normal skin has a particularly high proportion of regulatory T cells (Tregs) in the steady state (28) and a meta-analysis of malaria vaccine studies suggested that Plasmodium -specific Tregs are induced during the skin stage of infection, potentially mediating immune tolerance to sporozoites as well as to the subsequent blood-stage of infection (30). Consistent with these results are experiments in mice that show that skin Tregs and DCs are mobilized within 30 minutes of sporozoite inoculation and that DCs downregulate MHC II and CD86 suggesting a tolerogenic response (31). The immunoregulatory environment of the skin may be reinforced by chronic immune activation or immune dysregulation due to repeated exposures to sporozoites and liver stage antigens (32).…”

Section: Human Immunity and Malariasupporting

confidence: 54%

Malaria Immunity in Man and Mosquito: Insights into Unsolved Mysteries of a Deadly Infectious Disease

Crompton

Moebius

Portugal

et al. 2014

Annu. Rev. Immunol.

274

248

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Malaria is a mosquito-borne disease caused by parasites of the obligate intracellular Apicomplexa family, the most deadly of which, Plasmodium falciparum, prevails in Africa. Malaria imposes a huge health burden on the world’s most vulnerable populations, claiming the lives of nearly a million children and pregnant women each year in Africa alone. Although there is keen interest in eradicating malaria, we do not yet have the necessary tools to meet this challenge, including an effective malaria vaccine and adequate vector control strategies. Here we review what is known about the mechanisms at play in immune resistance to malaria in both the human and mosquito hosts at each step in the parasite’s complex life cycle with a view towards developing the tools that will contribute to the prevention of disease and death and ultimately the goal of malaria eradication. In so doing we hope to inspire immunologists to participate in defeating this devastating disease.

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“…The saliva also increases the levels of immunosuppressive IL-10 in the dLN, which could contribute to downregulation of Ag (OVA)-specific T cell priming in an IL-10-dependent manner (68). Another study reported that 30 min after injection by mosquitoes, P. berghei sporozoites increased the motility of regulatory T cells and decreased expression of MHC class II and CD86 in CD11c + cells in the skin of mice, corroborating the notion that regulatory T cells might suppress activation of APCs in the skin and dLN (69).…”

Section: Discussionmentioning

confidence: 67%

Local Immune Response to Injection of Plasmodium Sporozoites into the Skin

Mac-Daniel

Buckwalter

Berthet

et al. 2014

The Journal of Immunology

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Malarial infection is initiated when the sporozoite form of the Plasmodium parasite is inoculated into the skin by a mosquito. Sporozoites invade hepatocytes in the liver and develop into the erythrocyte-infecting form of the parasite, the cause of clinical blood infection. Protection against parasite development in the liver can be induced by injection of live attenuated parasites that do not develop in the liver and thus do not cause blood infection. Radiation-attenuated sporozoites (RAS) and genetically attenuated parasites are now considered as lead candidates for vaccination of humans against malaria. Although the skin appears as the preferable administration route, most studies in rodents, which have served as model systems, have been performed after i.v. injection of attenuated sporozoites. In this study, we analyzed the early response to Plasmodium berghei RAS or wild-type sporozoites (WTS) injected intradermally into C57BL/6 mice. We show that RAS have a similar in vivo distribution to WTS and that both induce a similar inflammatory response consisting of a biphasic recruitment of polymorphonuclear neutrophils and inflammatory monocytes in the skin injection site and proximal draining lymph node (dLN). Both WTS and RAS associate with neutrophils and resident myeloid cells in the skin and the dLN, transform inside CD11b+ cells, and induce a Th1 cytokine profile in the dLN. WTS and RAS are also similarly capable of priming parasite-specific CD8+ T cells. These studies delineate the early and local response to sporozoite injection into the skin, and suggest that WTS and RAS prime the host immune system in a similar fashion.

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Early skin immunological disturbance after Plasmodium-infected mosquito bites

Cited by 20 publications

References 28 publications

Dermal Regulatory T Cells Display Distinct Migratory Behavior That Is Modulated during Adaptive and Innate Inflammation

Dermal Regulatory T Cells Display Distinct Migratory Behavior That Is Modulated during Adaptive and Innate Inflammation

Malaria Immunity in Man and Mosquito: Insights into Unsolved Mysteries of a Deadly Infectious Disease

Local Immune Response to Injection of Plasmodium Sporozoites into the Skin

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