Skip to main content
Proceedings of the Royal Society B: Biological Sciences logoLink to Proceedings of the Royal Society B: Biological Sciences
. 2001 Nov 22;268(1483):2325–2330. doi: 10.1098/rspb.2001.1808

The effect of partial host immunity on the transmission of malaria parasites.

A Buckling 1, A F Read 1
PMCID: PMC1088883  PMID: 11703872

Abstract

Experiments were carried out to determine the effect of partial host immunity against the rodent malaria parasite Plasmodium chabaudi on the transmission success of the parasite. There was a fourfold reduction in both the blood-stage, asexually replicating parasite density and the gametocyte (transmissable stage) density in immunized hosts. Some of the reduction in asexual parasite densities was due to strain-specific immunity, but there was no evidence that strain-specific immunity affected gametocyte densities. However, immunity did affect transmission in a strain-specific manner, with a fivefold reduction in gametocyte infectivity to mosquitoes in homologous challenges compared with heterologous challenges or non-immunized controls. This implies the existence of a mechanism of strain-specific infectivity-reducing immunity that does not affect the density of gametocytes circulating in peripheral blood. The proportion of asexual parasites that produced gametocytes increased during the course of infection in both non-immunized and in immunized hosts, but immunity increased gametocyte production early in the infection.

Full Text

The Full Text of this article is available as a PDF (235.7 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Bates M. D., Newbold C. I., Jarra W., Brown K. N. Protective immunity to malaria: studies with cloned lines of Plasmodium chabaudi chabaudi in CBA/Ca mice. III. Protective and suppressive responses induced by immunization with purified antigens. Parasite Immunol. 1988 Jan;10(1):1–15. doi: 10.1111/j.1365-3024.1988.tb00199.x. [DOI] [PubMed] [Google Scholar]
  2. Buckling A. G., Read A. F. The effect of chloroquine treatment on the infectivity of Plasmodium chabaudi gametocytes. Int J Parasitol. 1999 Apr;29(4):619–625. doi: 10.1016/s0020-7519(98)00230-6. [DOI] [PubMed] [Google Scholar]
  3. Buckling A. G., Taylor L. H., Carlton J. M., Read A. F. Adaptive changes in Plasmodium transmission strategies following chloroquine chemotherapy. Proc Biol Sci. 1997 Apr 22;264(1381):553–559. doi: 10.1098/rspb.1997.0079. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Buckling A., Crooks L., Read A. Plasmodium chabaudi: effect of antimalarial drugs on gametocytogenesis. Exp Parasitol. 1999 Sep;93(1):45–54. doi: 10.1006/expr.1999.4429. [DOI] [PubMed] [Google Scholar]
  5. Buckling A., Ranford-Cartwright L. C., Miles A., Read A. F. Chloroquine increases Plasmodium falciparum gametocytogenesis in vitro. Parasitology. 1999 Apr;118(Pt 4):339–346. doi: 10.1017/s0031182099003960. [DOI] [PubMed] [Google Scholar]
  6. Cadigan F. C., Jr, Chaicumpa V. Plasmodium falciparum in the white-handed gibbon: protection afforded by previous infection with homologous and heterologous strains obtained in Thailand. Mil Med. 1969 Sep;134(10):1135–1139. [PubMed] [Google Scholar]
  7. Gautret P., Miltgen F., Gantier J. C., Chabaud A. G., Landau I. Enhanced gametocyte formation by Plasmodium chabaudi in immature erythrocytes: pattern of production, sequestration, and infectivity to mosquitoes. J Parasitol. 1996 Dec;82(6):900–906. [PubMed] [Google Scholar]
  8. Goodier M. R., Targett G. A. Polyclonal T-cell responses to Plasmodium falciparum gametocytes in malaria nonexposed donors. Parasite Immunol. 1997 Sep;19(9):419–425. doi: 10.1046/j.1365-3024.1997.d01-238.x. [DOI] [PubMed] [Google Scholar]
  9. Graves P. M., Burkot T. R., Carter R., Cattani J. A., Lagog M., Parker J., Brabin B. J., Gibson F. D., Bradley D. J., Alpers M. P. Measurement of malarial infectivity of human populations to mosquitoes in the Madang area, Papua, New Guinea. Parasitology. 1988 Apr;96(Pt 2):251–263. doi: 10.1017/s003118200005825x. [DOI] [PubMed] [Google Scholar]
  10. 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]
  11. Graves P. M., Doubrovsky A., Beckers P. Antibody responses to Plasmodium falciparum gametocyte antigens during and after malaria attacks in schoolchildren from Madang, Papua New Guinea. Parasite Immunol. 1991 May;13(3):291–299. doi: 10.1111/j.1365-3024.1991.tb00283.x. [DOI] [PubMed] [Google Scholar]
  12. Hayward R. E., Tiwari B., Piper K. P., Baruch D. I., Day K. P. Virulence and transmission success of the malarial parasite Plasmodium falciparum. Proc Natl Acad Sci U S A. 1999 Apr 13;96(8):4563–4568. doi: 10.1073/pnas.96.8.4563. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Jarra W., Brown K. N. Protective immunity to malaria: studies with cloned lines of Plasmodium chabaudi and P. berghei in CBA/Ca mice. I. The effectiveness and inter- and intra-species specificity of immunity induced by infection. Parasite Immunol. 1985 Nov;7(6):595–606. doi: 10.1111/j.1365-3024.1985.tb00103.x. [DOI] [PubMed] [Google Scholar]
  14. Jarra W., Hills L. A., March J. C., Brown K. N. Protective immunity to malaria. Studies with cloned lines of Plasmodium chabaudi chabaudi and P. berghei in CBA/Ca mice. II. The effectiveness and inter- or intra-species specificity of the passive transfer of immunity with serum. Parasite Immunol. 1986 May;8(3):239–254. doi: 10.1111/j.1365-3024.1986.tb01036.x. [DOI] [PubMed] [Google Scholar]
  15. Mackinnon M. J., Hastings I. M. The evolution of multiple drug resistance in malaria parasites. Trans R Soc Trop Med Hyg. 1998 Mar-Apr;92(2):188–195. doi: 10.1016/s0035-9203(98)90745-3. [DOI] [PubMed] [Google Scholar]
  16. McLean A. P., Lainson F. A., Sharkey A. M., Walliker D. Genetic studies on a major merozoite surface antigen of the malaria parasite of rodents, Plasmodium chabaudi. Parasite Immunol. 1991 Jul;13(4):369–378. doi: 10.1111/j.1365-3024.1991.tb00290.x. [DOI] [PubMed] [Google Scholar]
  17. McLean S. A., Pearson C. D., Phillips R. S. Plasmodium chabaudi: antigenic variation during recrudescent parasitaemias in mice. Exp Parasitol. 1982 Dec;54(3):296–302. doi: 10.1016/0014-4894(82)90038-8. [DOI] [PubMed] [Google Scholar]
  18. Mendis K. N., Munesinghe Y. D., de Silva Y. N., Keragalla I., Carter R. Malaria transmission-blocking immunity induced by natural infections of Plasmodium vivax in humans. Infect Immun. 1987 Feb;55(2):369–372. doi: 10.1128/iai.55.2.369-372.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Motard A., Marussig M., Rénia L., Baccam D., Landau I., Mattei D., Targett G., Mazier D. Immunization with the malaria heat shock like protein hsp70-1 enhances transmission to the mosquito. Int Immunol. 1995 Jan;7(1):147–150. doi: 10.1093/intimm/7.1.147. [DOI] [PubMed] [Google Scholar]
  20. Mulder B., Tchuinkam T., Dechering K., Verhave J. P., Carnevale P., Meuwissen J. H., Robert V. Malaria transmission-blocking activity in experimental infections of Anopheles gambiae from naturally infected Plasmodium falciparum gametocyte carriers. Trans R Soc Trop Med Hyg. 1994 Jan-Feb;88(1):121–125. doi: 10.1016/0035-9203(94)90534-7. [DOI] [PubMed] [Google Scholar]
  21. Ono T., Nakai T., Nakabayashi T. Induction of gametocytogenesis in Plasmodium falciparum by the culture supernatant of hybridoma cells producing anti-P. falciparum antibody. Biken J. 1986 Dec;29(3-4):77–81. [PubMed] [Google Scholar]
  22. Phillips R. S., Brannan L. R., Balmer P., Neuville P. Antigenic variation during malaria infection--the contribution from the murine parasite Plasmodium chabaudi. Parasite Immunol. 1997 Sep;19(9):427–434. doi: 10.1046/j.1365-3024.1997.d01-239.x. [DOI] [PubMed] [Google Scholar]
  23. Read A., Viney M. Helminth immunogenetics: Why bother? Parasitol Today. 1996 Sep;12(9):337–343. doi: 10.1016/0169-4758(96)10056-9. [DOI] [PubMed] [Google Scholar]
  24. Sadun E. H., Hickman R. L., Wellde B. T., Moon A. P., Udeozo I. O. Active and passive immunization of chimpanzees infected with West African and Southeast Asian strains of Plasmodium falciparum. Mil Med. 1966 Sep;131(9 Suppl):1250–1262. [PubMed] [Google Scholar]
  25. Smalley M. E., Brown J. Plasmodium falciparum gametocytogenesis stimulated by lymphocytes and serum from infected Gambian children. Trans R Soc Trop Med Hyg. 1981;75(2):316–317. doi: 10.1016/0035-9203(81)90348-5. [DOI] [PubMed] [Google Scholar]
  26. Taylor L. H., Read A. F. Why so few transmission stages? Reproductive restraint by malaria parasites. Parasitol Today. 1997 Apr;13(4):135–140. doi: 10.1016/s0169-4758(97)89810-9. [DOI] [PubMed] [Google Scholar]
  27. Taylor L. H., Walliker D., Read A. F. Mixed-genotype infections of the rodent malaria Plasmodium chabaudi are more infectious to mosquitoes than single-genotype infections. Parasitology. 1997 Aug;115(Pt 2):121–132. doi: 10.1017/s0031182097001145. [DOI] [PubMed] [Google Scholar]

Articles from Proceedings of the Royal Society B: Biological Sciences are provided here courtesy of The Royal Society

RESOURCES