Members of the Salivary Gland Surface Protein (SGS) Family Are Major Immunogenic Components of Mosquito Saliva

King, J. W. B.; Vernick, Kenneth D.; Hillyer, Julián F.

doi:10.1074/jbc.m111.280552

Cited by 42 publications

(45 citation statements)

References 55 publications

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“…It is plausible that during transmission of complex eukaryotic pathogens, such as Plasmodium, mosquito saliva affects immunogenicity but not infectivity, whereas during viral transmission the immune modulatory effects are broader. The recent identification of two major immunogenic salivary gland proteins provides a molecular framework to gain a better understanding of immune modulation by mosquito saliva (65). Alternatively, differences in the antigenic repertoire or in shedding of antigenic surface proteins during transmigration between hemocoel and salivary gland sporozoites might contribute to dissimilar immunogenicity.…”

Section: Discussionmentioning

confidence: 99%

Plasmodium berghei Sporozoites Acquire Virulence and Immunogenicity during Mosquito Hemocoel Transit

2014

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bMalaria is a vector-borne disease caused by the single-cell eukaryote Plasmodium. The infectious parasite forms are sporozoites, which originate from midgut-associated oocysts, where they eventually egress and reach the mosquito hemocoel. Sporozoites actively colonize the salivary glands in order to be transmitted to the mammalian host. Whether residence in the salivary glands provides distinct and vital cues for the development of infectivity remains unsolved. In this study, we systematically compared the infectivity of Plasmodium berghei sporozoites isolated from the mosquito hemocoel and salivary glands. Hemocoel sporozoites display a lower proportion of gliding motility but develop into liver stages when added to cultured hepatoma cells or after intravenous injection into mice. Mice infected by hemocoel sporozoites had blood infections similar to those induced by sporozoites liberated from salivary glands. These infected mice display indistinguishable systemic inflammatory cytokine responses and develop experimental cerebral malaria. When used as metabolically active, live attenuated vaccine, hemocoel sporozoites elicit substantial protection against sporozoite challenge infections. Collectively, these findings show that salivary gland colonization does not influence parasite virulence in the mammalian host when sporozoites are administered intravenously. This conclusion has important implications for in vitro sporozoite production and manufacturing of whole-sporozoite vaccines.

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Section: Discussionmentioning

confidence: 99%

Plasmodium berghei Sporozoites Acquire Virulence and Immunogenicity during Mosquito Hemocoel Transit

2014

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“…Consistent with this, in a study in Senegal, children who experienced low and moderate exposure exhibited decreased antibody concentrations clearly after more than 3 months (10) . Another study showed that the IgG antibody response to salivary gland proteins appearing after exposure to mosquito bites lasts 3-6 weeks (8) . Although the duration of the IgG response to salivary gland proteins may be brief (between 1 and 4 months), this response can detect specifi c proteins of the salivary gland, i.e., gSG6, in children exposed to very infrequent Anopheles bites.…”

Section: Immunogenic Proteins Found In Anopheles Sundaicus Salivary Gmentioning

confidence: 99%

“…Many studies have been conducted to identify and characterize immunogenic salivary proteins from malaria vectors in Africa; however, malaria vectors in Asia, particularly An. sundaicus, have not been studied (8) (17) (18) .…”

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confidence: 99%

“…Injection of saliva into the host's skin also induces the production of antibodies against salivary proteins (8) . The immunogenicity of salivary proteins has been demonstrated in previous studies, which showed that salivary proteins can induce the host immune response by producing immunoglobulin G (IgG) and immunoglobulin E (IgE) via hypersensitivity reactions (9) .…”

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confidence: 99%

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Detection of immunogenic proteins from Anopheles sundaicussalivary glands in the human serum

Armiyanti¹,

Nuryady²,

Arifianto³

et al. 2015

Rev. Soc. Bras. Med. Trop.

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“…Of interest here, Anopheles antigens are known humoral immune targets; antibody titers against mosquito salivary gland extracts are even indicative of mosquito biting intensity (18). Constituent salivary gland proteins are increasingly well identified (19), and some proteins, such as salivary gland protein-4 and -5, are known antibody targets (20). Aside from humoral immunity, A. stephensi bites also activate mast cells and contribute to T cell hyperplasia in lymph nodes (21).…”

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confidence: 99%

Purification of Plasmodium Sporozoites Enhances Parasite-Specific CD8 ⁺ T Cell Responses

2016

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cMalaria infection caused by Plasmodium parasites continues to cause enormous morbidity and mortality in areas where it is endemic, and there is no licensed vaccine capable of inducing sterile protection. Hyperimmunization with attenuated whole sporozoites can induce sterile protective immune responses targeting preerythrocytic antigens. Most animal models of hyperimmunization rely on sporozoites dissected from mosquito salivary glands and injected without further purification. In BALB/c mice, repeated small doses of P. yoelii sporozoites progressively expand the population of sporozoite-specific CD8 ؉ T cells. In this study, large secondary doses of unpurified sporozoites unexpectedly led to contraction of sporozoite-specific CD8 ؉ T cell responses in sporozoite-primed mice. While sporozoite-primed CD8 ؉ T cells alternatively can be expanded by secondary exposure to Listeria monocytogenes expressing recombinant Plasmodium antigens, such expansion was potently inhibited by coinjection of large doses of unpurified sporozoites and by uninfected salivary glands alone. Purification of sporozoites away from mosquito salivary gland debris by density gradient centrifugation eliminated salivary gland-associated inhibition. Thus, the inhibitory effect appears to be due to exposure to uninfected mosquito salivary glands rather than sporozoites. To further assess the effect of salivary gland exposure on later sporozoite vaccinations, mice were immunized with uninfected salivary glands from a single mosquito. Compared to naive mice, salivary gland presensitization reduced subsequent liver burdens by 71%. These data show that a component(s) in mosquito salivary glands reduces liver infection, thereby limiting antigen dose and contributing to lower-magnitude T cell responses. These findings suggest that sporozoite immunogenicity studies be performed using purified sporozoites whenever feasible.

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Members of the Salivary Gland Surface Protein (SGS) Family Are Major Immunogenic Components of Mosquito Saliva

Cited by 42 publications

References 55 publications

Plasmodium berghei Sporozoites Acquire Virulence and Immunogenicity during Mosquito Hemocoel Transit

Plasmodium berghei Sporozoites Acquire Virulence and Immunogenicity during Mosquito Hemocoel Transit

Detection of immunogenic proteins from Anopheles sundaicussalivary glands in the human serum

Purification of Plasmodium Sporozoites Enhances Parasite-Specific CD8 ⁺ T Cell Responses

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Members of the Salivary Gland Surface Protein (SGS) Family Are Major Immunogenic Components of Mosquito Saliva

Cited by 42 publications

References 55 publications

Plasmodium berghei Sporozoites Acquire Virulence and Immunogenicity during Mosquito Hemocoel Transit

Plasmodium berghei Sporozoites Acquire Virulence and Immunogenicity during Mosquito Hemocoel Transit

Detection of immunogenic proteins from Anopheles sundaicussalivary glands in the human serum

Purification of Plasmodium Sporozoites Enhances Parasite-Specific CD8 + T Cell Responses

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Purification of Plasmodium Sporozoites Enhances Parasite-Specific CD8 ⁺ T Cell Responses