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. 1997 Sep;65(9):3834–3837. doi: 10.1128/iai.65.9.3834-3837.1997

Leukocytes in a Plasmodium falciparum-infected blood meal reduce transmission of malaria to Anopheles mosquitoes.

A H Lensen 1, M Bolmer-Van de Vegte 1, G J van Gemert 1, W M Eling 1, R W Sauerwein 1
PMCID: PMC175547  PMID: 9284160

Abstract

Mosquitoes are infected with Plasmodium falciparum by taking a blood meal from a gametocyte carrier. Since a mosquito takes a volume of 1 to 2 microl, a blood meal may contain 1 x 10(4) to 3 x 10(4) leukocytes (WBC). The majority of WBC are composed of neutrophils which may phagocytose and kill developing gametes inside the mosquito midgut. Phagocytosis was measured in vitro by a luminol-dependent chemiluminescence (CL) assay. In the presence of P. falciparum gametes, sera from areas of endemicity had an increased CL response compared to controls. In mosquito membrane feeding experiments some such sera showed a transmission reduction which was related to the presence of viable WBC. The results of this study suggest that phagocytosis of opsonized gametes inside the mosquito midgut occurs and can contribute to a reduction in the transmission of P. falciparum parasites.

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Selected References

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  1. Carter R., Graves P. M., Quakyi I. A., Good M. F. Restricted or absent immune responses in human populations to Plasmodium falciparum gamete antigens that are targets of malaria transmission-blocking antibodies. J Exp Med. 1989 Jan 1;169(1):135–147. doi: 10.1084/jem.169.1.135. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Easmon C. S., Cole P. J., Williams A. J., Hastings M. The measurement of opsonic and phagocytic function by Luminol-dependent chemiluminescence. Immunology. 1980 Sep;41(1):67–74. [PMC free article] [PubMed] [Google Scholar]
  3. Graves P. M., Carter R., Burkot T. R., Quakyi I. A., Kumar N. Antibodies to Plasmodium falciparum gamete surface antigens in Papua New Guinea sera. Parasite Immunol. 1988 Mar;10(2):209–218. doi: 10.1111/j.1365-3024.1988.tb00215.x. [DOI] [PubMed] [Google Scholar]
  4. Kumaratilake L. M., Ferrante A., Jaeger T., Rzepczyk C. M. Effects of cytokines, complement, and antibody on the neutrophil respiratory burst and phagocytic response to Plasmodium falciparum merozoites. Infect Immun. 1992 Sep;60(9):3731–3738. doi: 10.1128/iai.60.9.3731-3738.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Kumaratilake L. M., Ferrante A., Jaeger T., Rzepczyk C. GM-CSF-induced priming of human neutrophils for enhanced phagocytosis and killing of asexual blood stages of Plasmodium falciparum: synergistic effects of GM-CSF and TNF. Parasite Immunol. 1996 Mar;18(3):115–123. doi: 10.1046/j.1365-3024.1996.d01-64.x. [DOI] [PubMed] [Google Scholar]
  6. Lensen A., van Druten J., Bolmer M., van Gemert G., Eling W., Sauerwein R. Measurement by membrane feeding of reduction in Plasmodium falciparum transmission induced by endemic sera. Trans R Soc Trop Med Hyg. 1996 Jan-Feb;90(1):20–22. doi: 10.1016/s0035-9203(96)90464-2. [DOI] [PubMed] [Google Scholar]
  7. Medley G. F., Sinden R. E., Fleck S., Billingsley P. F., Tirawanchai N., Rodriguez M. H. Heterogeneity in patterns of malarial oocyst infections in the mosquito vector. Parasitology. 1993 Jun;106(Pt 5):441–449. doi: 10.1017/s0031182000076721. [DOI] [PubMed] [Google Scholar]
  8. Naotunne T. S., Karunaweera N. D., Mendis K. N., Carter R. Cytokine-mediated inactivation of malarial gametocytes is dependent on the presence of white blood cells and involves reactive nitrogen intermediates. Immunology. 1993 Apr;78(4):555–562. [PMC free article] [PubMed] [Google Scholar]
  9. Ong C. S., Zhang K. Y., Eida S. J., Graves P. M., Dow C., Looker M., Rogers N. C., Chiodini P. L., Targett G. A. The primary antibody response of malaria patients to Plasmodium falciparum sexual stage antigens which are potential transmission blocking vaccine candidates. Parasite Immunol. 1990 Sep;12(5):447–456. doi: 10.1111/j.1365-3024.1990.tb00980.x. [DOI] [PubMed] [Google Scholar]
  10. Ponnudurai T., Lensen A. H., Leeuwenberg A. D., Meuwissen J. H. Cultivation of fertile Plasmodium falciparum gametocytes in semi-automated systems. 1. Static cultures. Trans R Soc Trop Med Hyg. 1982;76(6):812–818. doi: 10.1016/0035-9203(82)90116-x. [DOI] [PubMed] [Google Scholar]
  11. Ponnudurai T., Lensen A. H., Van Gemert G. J., Bensink M. P., Bolmer M., Meuwissen J. H. Infectivity of cultured Plasmodium falciparum gametocytes to mosquitoes. Parasitology. 1989 Apr;98(Pt 2):165–173. doi: 10.1017/s0031182000062065. [DOI] [PubMed] [Google Scholar]
  12. Ponnudurai T., Meuwissen J. H., Leeuwenberg A. D., Verhave J. P., Lensen A. H. The production of mature gametocytes of Plasmodium falciparum in continuous cultures of different isolates infective to mosquitoes. Trans R Soc Trop Med Hyg. 1982;76(2):242–250. doi: 10.1016/0035-9203(82)90289-9. [DOI] [PubMed] [Google Scholar]
  13. Ponnudurai T., van Gemert G. J., Bensink T., Lensen A. H., Meuwissen J. H. Transmission blockade of Plasmodium falciparum: its variability with gametocyte numbers and concentration of antibody. Trans R Soc Trop Med Hyg. 1987;81(3):491–493. doi: 10.1016/0035-9203(87)90172-6. [DOI] [PubMed] [Google Scholar]
  14. Read D., Lensen A. H., Begarnie S., Haley S., Raza A., Carter R. Transmission-blocking antibodies against multiple, non-variant target epitopes of the Plasmodium falciparum gamete surface antigen Pfs230 are all complement-fixing. Parasite Immunol. 1994 Oct;16(10):511–519. doi: 10.1111/j.1365-3024.1994.tb00305.x. [DOI] [PubMed] [Google Scholar]
  15. Roeffen W., Lensen T., Mulder B., Teelen K., Sauerwein R., Eling W., Meuwissen J. H., Beckers P. Transmission blocking immunity as observed in a feeder system and serological reactivity to Pfs 48/45 and Pfs230 in field sera. Mem Inst Oswaldo Cruz. 1994;89 (Suppl 2):13–15. doi: 10.1590/s0074-02761994000600004. [DOI] [PubMed] [Google Scholar]
  16. Salmon D., Vilde J. L., Andrieu B., Simonovic R., Lebras J. Role of immune serum and complement in stimulation of the metabolic burst of human neutrophils by Plasmodium falciparum. Infect Immun. 1986 Mar;51(3):801–806. doi: 10.1128/iai.51.3.801-806.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Schwarzer E., Turrini F., Ulliers D., Giribaldi G., Ginsburg H., Arese P. Impairment of macrophage functions after ingestion of Plasmodium falciparum-infected erythrocytes or isolated malarial pigment. J Exp Med. 1992 Oct 1;176(4):1033–1041. doi: 10.1084/jem.176.4.1033. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Sinden R. E., Smalley M. E. Gametocytes of Plasmodium falciparum: phagocytosis by leucocytes in vivo and in vitro. Trans R Soc Trop Med Hyg. 1976;70(4):344–345. doi: 10.1016/0035-9203(76)90096-1. [DOI] [PubMed] [Google Scholar]
  19. Vermeulen A. N., Ponnudurai T., Beckers P. J., Verhave J. P., Smits M. A., Meuwissen J. H. Sequential expression of antigens on sexual stages of Plasmodium falciparum accessible to transmission-blocking antibodies in the mosquito. J Exp Med. 1985 Nov 1;162(5):1460–1476. doi: 10.1084/jem.162.5.1460. [DOI] [PMC free article] [PubMed] [Google Scholar]

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