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Can the host immune system promote multiple invasions of erythrocytes in vivo? Differential effects of medication and host sex in a wild malaria-like model

Published online by Cambridge University Press:  04 December 2006

J. MARTÍNEZ-DE LA PUENTE ,
S. MERINO ,
G. TOMÁS ,
J. MORENO ,
J. MORALES ,
E. LOBATO  and
S. GARCÍA-FRAILE
J. MARTÍNEZ-DE LA PUENTE*
Affiliation:
Departamento de Ecología Evolutiva, Museo Nacional de Ciencias Naturales-C.S.I.C., C\ José Gutiérrez Abascal, 2. E-28006 Madrid, Spain
S. MERINO
Affiliation:
Departamento de Ecología Evolutiva, Museo Nacional de Ciencias Naturales-C.S.I.C., C\ José Gutiérrez Abascal, 2. E-28006 Madrid, Spain
G. TOMÁS
Affiliation:
Departamento de Ecología Evolutiva, Museo Nacional de Ciencias Naturales-C.S.I.C., C\ José Gutiérrez Abascal, 2. E-28006 Madrid, Spain
J. MORENO
Affiliation:
Departamento de Ecología Evolutiva, Museo Nacional de Ciencias Naturales-C.S.I.C., C\ José Gutiérrez Abascal, 2. E-28006 Madrid, Spain
J. MORALES
Affiliation:
Departamento de Ecología Evolutiva, Museo Nacional de Ciencias Naturales-C.S.I.C., C\ José Gutiérrez Abascal, 2. E-28006 Madrid, Spain
E. LOBATO
Affiliation:
Departamento de Ecología Evolutiva, Museo Nacional de Ciencias Naturales-C.S.I.C., C\ José Gutiérrez Abascal, 2. E-28006 Madrid, Spain
S. GARCÍA-FRAILE
Affiliation:
Departamento de Ecología Evolutiva, Museo Nacional de Ciencias Naturales-C.S.I.C., C\ José Gutiérrez Abascal, 2. E-28006 Madrid, Spain
*
*Corresponding author. Tel: +34914111328. Fax: +34915645078. E-mail: [email protected]
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Summary

Multiple invasions (MIs) or infections, i.e. those by more than 1 parasite in the same erythrocyte, could be the result of parasite density or, alternatively, to parasite-related factors or host-related factors. According to the last possibility, to our knowledge, only 3 laboratory studies of malaria have found an increase in the occurrence of MIs when antibodies to parasite antigens were present. Therefore, we tested the possibility that MIs were influenced by the host immune status, using as model the malaria-like parasite Haemoproteus infecting blue tits (Cyanistes caeruleus). Avian hosts infected with Haemoproteus were medicated with primaquine or injected with saline solution and the density of infection and the presence of MIs counted. Medication treatment reduced significantly the density of infection by Haemoproteus in females but not in males. For females, the presence of MIs was positively associated with both the density of infection and the immunoglobulin levels on each capture, but no association was found between the treatment and the presence of MIs. For males, the density of infection but not the immunoglobulin levels was positively associated with the presence of MIs. In addition, medicated males supported more MIs than controls. Our results represent the first line of evidence in the wild for a possible role of the host immune system promoting MIs.

Keywords

multiple invasionshost immunityHaemoproteusPlasmodiumhost-parasite interactionsmalariasexual differences
Type
Research Article
Information
Parasitology , Volume 134 , Issue 5 , May 2006 , pp. 651 - 655
Copyright
Copyright © Cambridge University Press 2006

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References

REFERENCES

Ahmed, F. E. and Mohammed, A. H. H. (1978). Studies of growth and development of gametocytes in Haemoproteus columbae Kruse. Journal of Protozoology 25, 174–177.CrossRefGoogle ScholarPubMed
Elmes, N. J., Bennett, S. M., Abdalla, H., Carthew, T. L. and Edstein, M. D. (2006). Lack of sex effect on the pharmacokinetics of primaquine. American Journal of Tropical Medicine and Hygiene 74, 151–152.CrossRefGoogle ScholarPubMed
Fallis, A. M. and Desser, S. S. (1977). On the species of Leucocytozoon, Haemoproteus, and Hepatocystis. In Parasitic Protozoa, Vol. 3, 1st Edn. (ed. Kreir, J. P.), pp. 239–266. Academic Press, New York.Google Scholar
Franzén, L., Wahlin, B., Wahlgren, M., Aslund, L., Perlmann, P., Wigzell, H. and Pettersson, U. (1989). Enhancement or inhibition of Plasmodium falciparum erythrocyte reinvasion in vitro by antibodies to an asparagines rich protein. Molecular and Biochemical Parasitology 32, 201–212.CrossRefGoogle ScholarPubMed
Godfrey, R. D. JR., Fedynich, A. M. and Pence, D. B. (1987). Quantification of hematozoa in blood smears. Journal of Wildlife Diseases 23, 558–565.CrossRefGoogle ScholarPubMed
Gordi, T., Huong, D. X., Hai, T. N., Nieu, N. T. and Ashton, M. (2002). Artemisinin pharmacokinetics and efficacy in uncomplicated-malaria patients treated with two different dosage regimens. Antimicrobial Agents and Chemotherapy 46, 1026–1031.CrossRefGoogle ScholarPubMed
Inselburg, J. (1983). Gametocyte formation by the progeny of single Plasmodium falciparum schizonts. Journal of Parasitology 69, 584–591.CrossRefGoogle ScholarPubMed
Jovani, R. (2002). Malaria transmission, sex ratio and erythrocytes with two gametocytes. Trends in Parasitology 18, 537–539.CrossRefGoogle ScholarPubMed
Klein, S. L. (2004). Hormonal and immunological mechanisms mediating sex differences in parasite infection. Parasite Immunology 26, 247–264.CrossRefGoogle ScholarPubMed
Martínez, J., Tomás, G., Merino, S., Arriero, E. and Moreno, J. (2003). Detection of serum immunoglobulins in wild birds by direct ELISA: a methodological study to validate the technique in different species using antichicken antibodies. Functional Ecology 17, 700–706.CrossRefGoogle Scholar
Martínez-de la Puente, J., Merino, S., Tomás, G., Moreno, J., Morales, J. and Lobato, E. (2006). Are multiple gametocyte infections in malarial parasites an adaptation to ensure fertility? Parasitology 132, 23–28.CrossRefGoogle ScholarPubMed
Miller, L. H., David, P. H., Hudson, D. E., Hadley, T. J., Richards, R. L. and Aikawa, M. (1984). Monoclonal antibodies to a 140,000 m.W. protein on Plasmodium knowlesi merozoites inhibit their invasion of rhesus erythrocytes. Journal of Immunology 132, 438–442.CrossRefGoogle Scholar
Prasad, R. N., Prasad, H., Virk, K. J. and Sharma, V. P. (1990). Detection of multiple invasión of erythrocytes by Plasmodium vivax. Transactions of the Royal Society of Tropical Medicine and Hygiene 41, 437–438.Google ScholarPubMed
Pinsonneault, J. and Sadée, W. (2003). Pharmacogenomics of multigenic diseases: sex-specific differences in disease and treatment outcome. AAPS PharmSci 5, article 29.CrossRefGoogle ScholarPubMed
Ramasamy, R., Yasawardena, S., Kanagaratnam, R., Buratti, E., Baralle, F. E. and Ramasamy, M. S. (1999). Antibodies to a merozoite surface protein promote multiple invasion of red blood cells by malaria parasites. Parasite Immunology 21, 397–407.CrossRefGoogle ScholarPubMed
Valkiūnas, G. (2005). Avian Malaria Parasites and other Haemosporidia. CRC Press, Boca Raton, Florida.Google Scholar
Wang, C. C. (1970). Multiple invasion of erythrocytes by malaria parasites. Transactions of the Royal Society of Tropical Medicine and Hygiene 64, 268–270.CrossRefGoogle ScholarPubMed
Zuk, M. and McKean, K. A. (1996). Sex differences in parasite infections: patterns and processes. International Journal for Parasitology 26, 1009–1024.CrossRefGoogle ScholarPubMed