Hostname: page-component-848d4c4894-2pzkn Total loading time: 0 Render date: 2024-06-09T16:43:56.294Z Has data issue: false hasContentIssue false

Role of heat-labile serum factor or host complement in the inhibition of Plasmodium falciparum sporogonic stages in Anopheles stephensi by gametocyte carriers' serological factors

Published online by Cambridge University Press:  24 July 2007

L. C. GOUAGNA*
Affiliation:
Organisation de Coordination pour la lutte contre les Endémies en Afrique Centrale (OCEAC), Laboratoire de Recherche sur le Paludisme, BP 288, Yaoundé, Cameroon Unité de Recherche 016 – Antenne de l'Institut de Recherche pour le Développement (IRD), BP 171 Bobo Dioulasso, Burkina Faso
M. VAN DER KOLK
Affiliation:
Organisation de Coordination pour la lutte contre les Endémies en Afrique Centrale (OCEAC), Laboratoire de Recherche sur le Paludisme, BP 288, Yaoundé, Cameroon Department of Medical Microbiology, Radboud University Nijmegen Medical Centre, CRCN 395, P.O. Box 9101, 6500 HB Nijmegen, The Netherlands
W. ROEFFEN
Affiliation:
Department of Medical Microbiology, Radboud University Nijmegen Medical Centre, CRCN 395, P.O. Box 9101, 6500 HB Nijmegen, The Netherlands
J.-P. VERHAVE
Affiliation:
Department of Medical Microbiology, Radboud University Nijmegen Medical Centre, CRCN 395, P.O. Box 9101, 6500 HB Nijmegen, The Netherlands
W. ELING
Affiliation:
Department of Medical Microbiology, Radboud University Nijmegen Medical Centre, CRCN 395, P.O. Box 9101, 6500 HB Nijmegen, The Netherlands
R. SAUERWEIN
Affiliation:
Department of Medical Microbiology, Radboud University Nijmegen Medical Centre, CRCN 395, P.O. Box 9101, 6500 HB Nijmegen, The Netherlands
C. BOUDIN
Affiliation:
Organisation de Coordination pour la lutte contre les Endémies en Afrique Centrale (OCEAC), Laboratoire de Recherche sur le Paludisme, BP 288, Yaoundé, Cameroon Unité de Recherche 077 – Institut de Recherche pour le Développement (IRD), Dakar
*
Corresponding author: Unité de Recherche 016 – Institut de Recherche pour le Développement, Antenne IRD. 01 BP 171 Bobo Dioulasso, Burkina Faso. Tel: +226 974987. Fax: +226 2097 0942. E-mail: Louis-Clement.Gouagna@ird.bf

Summary

This study investigated the significance of serum complement on transmission-reducing activity (TRA) of field sera from 24 infected Plasmodium falciparum gametocyte carriers (from Cameroon) against cultured NF54 P. falciparum. Laboratory-reared Anopheles stephensi were given infectious blood meals prepared either with sera from naïve Dutch donor (AB type) or pair-matched field serum samples, both with and without active complement. TRA of serum factors and host complement on mosquito infection rate and oocyst intensity were divided into the various components involved in the early stages of sporogony. The majority (>80%) of sera tested showed positive antibody titres to Pfs230, the relevant complement-dependent target of transmission-reducing mechanisms. Regardless of the presence of active complement, bloodmeals with field sera exhibited significantly lower infection rates and oocyst intensity than the control group. Serological reactivity in Capture-ELISA against Pfs230 was significantly correlated with the reduction of parasite infectivity. Contrary to our expectation, the presence of active complement in the mosquito bloodmeal did not increase parasite losses and therefore the magnitude of transmission reduction by individual immune sera. Our findings on P. falciparum are consistent with previous studies on animal hosts of Plasmodium, indicating that early P. falciparum sporogonic stages may be insensitive to the antibody-dependent pathways of complement in human serum.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2007

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Blandin, S., Shiao, S. H., Moita, L. F., Janse, C. J., Waters, A. P., Kafatos, F. C. and Levashina, E. A. (2004). Complement-like protein TEP1 is a determinant of vectorial capacity in the malaria vector Anopheles gambiae. Cell 116, 661670.CrossRefGoogle ScholarPubMed
Bonnet, S., Paul, R. E., Gouagna, L. C., Safeukui, I., Meunier, J. Y., Gounoue, R. and Boudin, C. (2002). Level and dynamics of malaria transmission and morbidity in an equatorial area of South Cameroon. Tropical Medicine and International Health. 7, 249256.CrossRefGoogle Scholar
Carter, R. and Gwadz, R. W. (1980). Infectiousness and gamete immunization in malaria. In Malaria, Vol. 3 (ed. Kreier, J. P.), pp 263277. Academic Press, New York.CrossRefGoogle Scholar
Carter, R. and Mendis, K. (1992). Transmission immunity in malaria – Reflections on the underlying immune mechanisms during natural infections and following artificial immunization. Memorias do Instituto Oswaldo Cruz 87, 169173.CrossRefGoogle ScholarPubMed
Carter, R., Kumar, N., Quakyi, I., Good, M., Mendis, K., Graves, P. and Miller, L. (1988). Immunity to sexual stages of malaria parasites. Progress in Allergy 41, 193214.Google ScholarPubMed
Carter, R., Mendis, K. N., Miller, L. H., Molineaux, L. and Saul, A. (2000). Malaria transmission-blocking vaccines: how can their development be supported? Nature Medicine 6, 241244.CrossRefGoogle ScholarPubMed
Dimopoulos, G., Seeley, D., Wolf, A. and Kafatos, F. C. (1998). Malaria infection of the mosquito Anopheles gambiae activates immune-responsive genes during critical transition stages of the parasite life cycle. The EMBO Journal 17, 61156123.CrossRefGoogle ScholarPubMed
Drakeley, C. J., Mulder, L., Tchuinkam, T., Gupta, S., Sauerwein, R. W. and Targett, G. A. T. (1998). Transmission-blocking effects of sera from malaria-exposed individuals on Plasmodium falciparum isolates from gametocyte carriers. Parasitology 116, 417423.CrossRefGoogle ScholarPubMed
Good, M. F. and Miller, L. H. (1989). Involvement of T cells in malaria immunity: implications for vaccine development. Vaccine 7, 39.CrossRefGoogle ScholarPubMed
Gouagna, L. C., Bonnet, S., Gounoue, R., Verhave, J. P., Eling, W., Sauerwein, R. W. and Boudin, C. (2004). Stage-specific effects of host plasma factors on the early sporogony of autologous Plasmodium falciparum isolates within Anopheles gambiae. Tropical Medicine and International Health 9, 937948.CrossRefGoogle ScholarPubMed
Gouagna, L. C., Mulder, B., Noubissi, E., Tchuinkam, T., Verhave, J. P. and Boudin, C. (1998). The early sporogonic cycle of Plasmodium falciparum in laboratory-infected Anopheles gambiae: an estimation of parasite efficacy. Tropical Medicine and International Health 3, 2128.CrossRefGoogle ScholarPubMed
Graves, P. M., Carter, R., Burkot, T. R., Quakyi, I. A. and Kumar, N. K. (1988). Antibodies to Plasmodium falciparum gamete surface antigens in Papua New Guinea sera. Parasite Immunology 10, 208215.CrossRefGoogle ScholarPubMed
Grotendorst, C. A. and Carter, R. (1987). Complement effects on the infectivity of Plasmodium gallinaceum to Aedes aegypti mosquitoes. II. Changes in sensitivity to complement-like factors during zygote development. Journal of Parasitology 73, 980984.CrossRefGoogle ScholarPubMed
Grotendorst, C. A., Carter, R., Rosenberg, R. and Koontz, L. C. (1986). Complement effects on the infectivity of Plasmodium gallinaceum to Aedes aegypti mosquitoes. I. Resistance of zygotes to the alternative pathway of complement. Journal of Immunology 136, 42704274.CrossRefGoogle Scholar
Healer, J., McGuinness, D., Carter, R. and Riley, E. (1999). Transmission-blocking immunity to Plasmodium falciparum in malaria-immune individuals is associated with antibodies to the gamete surface protein Pfs230. Parasitology 119, 425433.CrossRefGoogle Scholar
Healer, J., McGuinness, D., Hopcroft, P., Haley, S., Carter, R. and Riley, E. (1997). Complement-mediated lysis of Plasmodium falciparum gametes by malaria-immune human sera is associated with antibodies to the gamete surface antigen Pfs230. Infection and Immunity 65, 30173023.CrossRefGoogle Scholar
Hommel, M. (1991). Steps toward a malaria vaccine. Research in Immunology 142, 618631.CrossRefGoogle Scholar
Kaslow, D. C., Isaacs, S. N., Quakyi, I. A., Gwadz, R. W., Moss, B. and Keister, D. B. (1991). Induction of Plasmodium falciparum transmission-blocking antibodies by recombinant vaccinia virus. Science 252, 13101312.CrossRefGoogle ScholarPubMed
Kaslow, D. C., Nussenzweig, V. and Miller, L. (1994). Meeting on parasites and the invertebrate vector. Memorias do Instituto Oswaldo Cruz 89, 279295.CrossRefGoogle ScholarPubMed
Kaushal, D. C., Carter, R., Rener, J., Grotendorst, C. A., Miller, L. H. and Howard, R. J. (1983). Monoclonal antibodies against surface determinants on gametes of Plasmodium gallinaceum block transmission of malaria parasites to mosquitoes. Journal of Immunology 131, 25572562.CrossRefGoogle ScholarPubMed
Kumar, N. (1987). Target antigens of malaria transmission-blocking exist as a stable membrane bound complex. Parasite Immunology 9, 321335.CrossRefGoogle ScholarPubMed
Kumar, N. and Carter, R. (1984). Biosynthesis of the target antigens of antibodies-blocking transmission of Plasmodium falciparum. Molecular and Biochemical Parasitology 13, 333342.CrossRefGoogle ScholarPubMed
Lensen, A., Van Druten, J., Bolmer, M., Van Gemert, G., Eling, W. and Sauerwein, R. W. (1996). Measurement by membrane feeding of reduction in Plasmodium falciparum transmission reducing by endemic sera. Transactions of the Royal Society of Tropical Medicine and Hygiene 90, 2022.CrossRefGoogle ScholarPubMed
Lensen, A., Mulder, L., Tchuinkam, T., Willemsen, L., Vaidya, A. B. and Sauerwein, R. W. (1998). Mechanisms that reduce transmission of Plasmodium falciparum malaria in semiimmune and nonimmune persons. Journal of Infectious Diseases 177, 13581363.CrossRefGoogle ScholarPubMed
Margos, G., Navarette, S., Butcher, G., Davies, A., Willer, C., Sinden, R. E. and Lachmann, P. J. (2001). Interaction between host complement and mosquito-midgut-stage Plasmodium berghei. Infection and Immunity 69, 50645071.CrossRefGoogle ScholarPubMed
Meis, J. F. G. M., Pool, G., Van Germert, G. J., Lensen, A. H. W., Ponnudurai, T. and Meuwissen, J. H. E. Th. (1989). Plasmodium falciparum ookinetes migrate intercellularly through Anopheles stephensi midgut epithelium. Parasitology Research 76, 1319.CrossRefGoogle ScholarPubMed
Meunier, J. Y., Safeukui, I., Fontenille, D. and Boudin, C. (1999). Etude de la transmission du paludisme dans une future zone d'essai vaccinal en foret équatoriale du sud Cameroun. Bulletin de la Societé de Pathologie Exotique 92, 309312.Google Scholar
Mulder, B., Tchuinkam, T., Dechering, K., Verhave, J. P., Carnevale, P., Meuwissen, J. H. E. Th. and Robert, V. (1994). Malaria transmission-blocking activity in experimental infections of Anopheles gambiae from naturally Plasmodium falciparum gametocyte carriers. Transactions of the Royal Society of Tropical Medicine and Hygiene 88, 121125.CrossRefGoogle ScholarPubMed
Mulder, B., Lensen, T., Tchuinkam, T., Roeffen, W., Verhave, J. P., Boudin, C. and Sauerwein, R. W. (1999). Plasmodium falciparum: membrane feeding assays and competition ELISAs for the measurement of transmission reduction in sera from Cameroon. Experimental Parasitology 92, 8186.CrossRefGoogle ScholarPubMed
Naotunne, T. S., Karunaweera, N. D., Mendis, K. N. and Carter, R. (1993). Cytokine-mediated inactivation of malarial gametocytes is dependent on the presence of white blood cells and involves reactive nitrogen intermediates. Immunology 78, 555562.Google ScholarPubMed
Nogueira, N., Bianco, C. and Cohn, Z. A. (1975). Studies on the selective lysis and purification of Trypanosoma cruzi. Journal of Experimental Medicine 142, 224.CrossRefGoogle ScholarPubMed
Osta, M. A., Christophide, G. K. and Kafatos, F. C. (2004). Effects of mosquito genes on Plasmodium development. Science 303, 20302032.CrossRefGoogle ScholarPubMed
Pearson, R. D. and Steigbigel, R. T. (1980). Mechanism of lethal effect of human serum upon Leishmania donovani. Journal of Immunology 125, 2195.CrossRefGoogle ScholarPubMed
Ponnudurai, T., Lensen, A. H. W., Van Gemert, G. J. A., Bensink, M. P. E., Bolmer, M. and Meuwissen, J. H. E. Th. (1989). Infectivity of cultured Plasmodium falciparum gametocytes to mosquitoes. Parasitology 98, 165173.CrossRefGoogle ScholarPubMed
Ponnudurai, T., Meuwissen, J. H. E. Th., Leeuwemberg, A. D. E. M., Verhave, J. P. and Lensen, A. H. W. (1982). The production of mature gametocytes of Plasmodium falciparum in continuous cultures of different isolates infective to mosquitoes. Transactions of the Royal Society of Tropical Medicine and Hygiene 76, 242250.CrossRefGoogle ScholarPubMed
Premawansa, S., Mendis, G. A., Perera, L., Begarnie, S., Mendis, K. and Carter, R. (1994). Plasmodium falciparum malaria transmissoin-blocking immunity under conditions of low endemicity as in Sri lanka. Parasite Immunology 16, 3542.CrossRefGoogle ScholarPubMed
Quakyi, I. A., Carter, R., Rener, J., Kumar, N., Good, M. F. and Miller, L. H. (1987). The 230-kDa Gamete Surface Protein of Plasmodium falciparum is also a target for transmission-blocking antibodies. Journal of Immunology 139, 42134217.CrossRefGoogle ScholarPubMed
Ranawaka, G., Alejo-Blanco, R. and Sinden, R. E. (1993). The effect of transmission-blocking antibody ingested in primary and secondary bloodfeeds, upon the development of Plasmodium berghei in the mosquito vector. Parasitology 107, 225231.CrossRefGoogle ScholarPubMed
Read, D., Lensen, A. H., Begarnie, S., Haley, S., Raza, A. and Carter, R. (1994). Transmission-blocking antibodies against multiple, non-variant target epitopes of the Plasmodium falciparum gamete surface protein Pfs230 are all complement fixing. Parasite Immunology 16, 511519.CrossRefGoogle ScholarPubMed
Rener, J., Carter, R., Rosenberg, Y. and Miller, L. H. (1980). Anti-gamete monoclonal antibodies synergistically block transmission of malaria by preventing fertilization in the mosquito. Proceedings of the National Academy of Sciences, USA 77, 67976799.CrossRefGoogle ScholarPubMed
Rener, J., Graves, P. M., Carter, R., Williams, J. and Burkot, T. R. (1983). Target antigens of transmission-blocking immunity on gametes of Plasmodium falciparum. Journal of Experimental Medicine 158, 976981.CrossRefGoogle ScholarPubMed
Richman, A., Dimopoulos, G., Seeley, D. and Kafatos, F. (1997). Plasmodium activates the innate immune response of Anopheles gambiae mosquitoes. The EMBO Journal 16, 61146119.CrossRefGoogle ScholarPubMed
Riehle, M. A., Srinivasan, P., Moreira, C. K. and Jacobs-Lorena, M. (2003). Towards genetic manipulation of wild mosquito populations to combat malaria: advances and challenges – review. Journal of Experimental Biology 206, 38093816.CrossRefGoogle Scholar
Robert, V., LeGoff, G., Essong, J., Tchuinkam, T., Fass, B. and Verhave, J. P. (1995). Detection of falciparum malaria preoocyst form in naturally infected anophelines using a fluorescent monoclonal antibody anti-25 KD in Cameroun. American Journal of Tropical Medicine and Hygiene 52, 366369.CrossRefGoogle Scholar
Roeffen, W., Lensen, T., Mulder, B., Teelen, K., Sauerwein, R., Van Druten, J., Eling, W., Meuwissen, J. H. E. T. and Beckers, P. J. A. (1995 a). A compararison of transmission-blocking activity with reactivity in Plasmodium falciparum 48/45 kD Molecule-Specific Competion ELISA. American Journal of Tropical Medicine and Hygiene 52, 6065.CrossRefGoogle Scholar
Roeffen, W., Beckers, P. J. A., Teelen, K., Verhave, J. P., Eling, W. and Sauerwein, R. (1993). Comparison of serological tests and bio-assay for malaria transmission blocking capacity in field sera. Parassitologia 35, 9597.Google ScholarPubMed
Roeffen, W., Beckers, P. J. A., Teelen, K., Sauerwein, R., Meuwissen, J. H. E. Th. and Eling, W. (1995 b). Plasmodium falciparum: A comparison of the activity of Pfs230-specific antibodies in an assay of transmission-blocking immunity and specific competition ELISAs. Experimental Parasitology 80, 1526.CrossRefGoogle Scholar
Shahabuddin, M. and Costero, A. (2001). Spatial distribution of factors that determine sporogonic development of malaria parasites in mosquitoes. Insect Biochemistry and Molecular Biology 31, 231240.CrossRefGoogle ScholarPubMed
Sinden, R. E. (1983). Sexual development of malarial parasites. Advances in Parasitology 22, 153216.CrossRefGoogle ScholarPubMed
Sinden, R. E. (2002). Molecular interactions between Plasmodium and its insect vectors. Cell Microbiology 4, 713724.CrossRefGoogle ScholarPubMed
Sinden, R. E., Butcher, G. A., Billker, O. and Fleck, S. L. (1996). Regulation of infectivity of Plasmodium to the mosquito vector. Advances in Parasitology 38, 53117.CrossRefGoogle Scholar
Tahar, R., Boudin, C., Thiery, I. and Bourgouin, C. (2002). Immune response of Anopheles gambiae to the early sporogonic stages of the human malaria parasite Plasmodium falciparum. The EMBO Journal 21, 66736680.CrossRefGoogle Scholar
Targett, G. A. T., Harte, P. G., Eida, S., Rogers, N. C. and Ong, C. S. L. (1990). Plasmodium falciparum sexual stage antigens: immunogenicity and cell mediated responses. Immunology Letters 25, 7782.CrossRefGoogle ScholarPubMed
Tsuboi, T., Cao, Y. M., Torii, M., Hitsumoto, Y. and Kanbara, H. (1995). Murine complement reduces infectivity of Plasmodium yoelii to mosquitoes. Infection and Immunity 63, 37023704.CrossRefGoogle ScholarPubMed
Umotong, A. B., Amanor-Boadu, S. D., Okerengwo, A. A. and Hedo, C. C. (1994). Serum complement levels in asymptomatic Plasmodium falciparum parasitaemic children. Tropical Geography and Medicine 46, 134147.Google ScholarPubMed
Van der Kolk, M., De Vlas, S. J., Van de Vegte-Bolmer, M., Eling, W. M., Saul, A. and Sauerwein, R. W. (2005). Evaluation of the standard membrane-feeding assay for the determination of malaria transmission reducing activity using empirical data. Parasitology 130, 1322.CrossRefGoogle ScholarPubMed
Van der Kolk, M., deVlas, S. J. and Sauerwein, R. W. (2006). Reduction and enhancement of Plasmodium falciparum transmission by endemic human sera. International Journal for Parasitology 36, 10911095.CrossRefGoogle ScholarPubMed
Vaughan, J. A., Noden, B. H. and Beier, J. C. (1992). Population dynamics of Plasmodium falciparum sporogony in laboratory-infected Anopheles gambiae. Journal of Parasitology 78, 716724.CrossRefGoogle ScholarPubMed
Vermeulen, A. N., Ponnudurai, T., Beckers, P. J. A., Verhave, J. P., Smits, M. and Meuwissen, J. H. E. T. (1985). Sequential expression of antigens on sexual stages of Plasmodium falciparum accessible to transmission-blocking antibodies in the mosquito. Journal of Experimental Medicine 162, 14601476.CrossRefGoogle ScholarPubMed
Walport, M. J. (2001). Complement – Review. New England Journal of Medicine 344, 10581066.CrossRefGoogle Scholar
Williamson, K. C. (2003). Pfs230: from malaria transmission-blocking vaccine candidate toward function – Review. Parasite Immunology 25, 351359.CrossRefGoogle Scholar