Skip to main content Accessibility help
×
Home

Malaria, sexual development and transmission: retrospect and prospect

  • R. E. SINDEN (a1)

Summary

It is difficult to recapture the excitement of recent research into the malaria parasites. Plasmodium has shown itself to be a most elegant, resourceful and downright devious cell. To reveal any of its manifold secrets is a hard-won privilege. The thrill of this intellectual endeavour, however, has to be tempered by the realism that we have made unremarkable progress in attacking malaria in the field, where it remains almost as omnipresent as it ever was in the 19th and 20th centuries, and both the parasite and vector have become more difficult to control than ever before. This personal view looks back at the significant progress made, and forward to the challenges of the future, focusing on work on sexual development.

Copyright

Corresponding author

*Tel: 020 7594 5425. Fax: 020 7594 5424. E-mail: r.sinden@ic.ac.uk

References

Hide All
Ahmed, A. M., Maingon, R. D., Taylor, P. J. and Hurd, H. (1999). The effects of infection with Plasmodium yoelii nigeriensis on the reproductive fitness of the mosquito Anopheles gambiae. Invertebrate Reproduction and Development 36, 217222.
Al-Olayan, E. B., Beetsma, A. L., Butcher, G. A., Sinden, R. E. and Hurd, H. (2002). Complete development of the mosquito phases of the malaria parasite in vitro. Science 295, 677679.
Alano, P., Read, D., Bruce, M., Aikawa, M., Kaido, T., Tegoshi, T., Bhatti, S., Smith, D. K., Luo, C., Hansra, S., Carter, R. and Elliott, J. F. (1995). COS cell expression cloning of Pfg377, a Plasmodium falciparum gametocyte antigen associated with osmiophilic bodies. Molecular and Biochemical Parasitology 74, 143156.
Alavi, Y., Arai, M., Mendoza, J., Tufet-Bayona, M., Sinha, R., Fowler, R., Billker, O., Franke-Fayard, B., Janse, C. J., Waters, A. P. and Sinden, R. E. (2003). The dynamics of interactions between Plasmodium and the mosquito: a study of the infectivity of Plasmodium berghei and Plasmodium gallinaceum, and their transmission by Anopheles stephensi, Anopheles gambiae and Aedes aegypti. International Journal for Parasitology 33, 933943.
Amino, R., Giovannini, D., Thiberge, S., Gueirard, P., Boisson, B., Dubremetz, J. F., Prévost, M. C., Ishino, T., Yuda, M. and Ménard, R. (2008). Host cell traversal is important for progression of the malaria parasite through the dermis to the liver. Cell Host and Microbe 3, 8896.
Baer, K., Roosevelt, M., Clarkson, A. B. Jr., van Rooijen, N., Schneider, T. and Frevert, U. (2007). Kupffer cells are obligatory for Plasmodium yoelii sporozoite infection of the liver. Cellular Microbiology 9, 397412.
Bass, C. C. and Johns, F. M. (1912). The cultivation of malarial Plasmodia (Plasmodium vivax and Plasmodium falciparum) in vitro. Journal of Experimental Medicine 16, 567579.
Billker, O., Dechamps, S., Tewari, R., Wenig, G., Franke-Fayard, B. and Brinkmann, V. (2004). Calcium and a calcium-dependent protein kinase regulate gamete formation and mosquito transmission in a malaria parasite. Cell 117, 503514.
Billker, O., Lindo, V., Panico, M., Etienne, T., Paxton, T., Dell, A., Rogers, M., Sinden, R. E. and Morris, H. (1998). Identification of the putative inducer of malaria development in the mosquito as xanthurenic acid. Nature, London 392, 289292.
Billker, O., Shaw, M. K., Margos, G. and Sinden, R. E. (1997). The roles of temperature pH and mosquito factors as triggers of male and female gametogenesis of Plasmodium berghei in vitro. Parasitology 114, 17.
Blandin, S. and Levashina, E. A. (2004). Mosquito immune responses against malaria parasites. Current Opinion in Immunology 16, 1620.
Boyd, M. F. (1949). Malariology, a Comprehensive Survey of all Aspects of this Group of Diseases from a Global Standpoint. W.B. Saunders and Company, Philadelphia, USA and London, UK.
Bozdech, Z., Zhu, J., Joachimiak, M. P., Cohen, F. E., Pulliam, B. and DeRisi, J. L. (2003). Expression profiling of the schizont and trophozoite stages of Plasmodium falciparum with a long-oligonucleotide microarray. Genome Biology 4, R9.
Brown, K. M. and Kreier, J. P. (1986). Effect of macrophage activation on phagocyte-Plasmodium interaction. Infection and Immunity 51, 744749.
Bruce, M. C., Alano, P., Duthie, S. and Carter, R. (1990). Commitment of the malaria parasite Plasmodium falciparum to sexual and asexual development. Parasitology 100, 191200.
Bruce-Chwatt, L. J. (1985). Essential Malariology, 2nd Edn.Heinemann Medical Books, London, UK.
Butcher, G. A. (1997). Antimalarial drugs and the mosquito transmission of Plasmodium. I International Journal for Parasitology 27, 975987.
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.
Carter, R., Mendis, K. N. and Roberts, D. (2000). Spatial targeting of interventions against malaria. Bulletin of the World Health Organization 78, 14011411.
Chao, J. and Ball, G. H. (1964). Cultivation of the insect cycle of Plasmodia. American Journal of Tropical Medicine and Hygiene 13, 181192.
Coatney, G. R., Collins, W. E., Warren, MCW. and Contacos, P. G. (1971). The Primate Malarias, 2nd Edn. U.S. Department of Health, Education and Welfare, NIH, Bethesda, Maryland, USA.
Collins, F. H., Sakai, R. K., Vernick, K. D., Paskewitz, S., Seeley, D. C., Miller, L. H., Collins, W. E., Campbell, C. C. and Gwadz, R. W. (1986). Genetic selection of a plasmodium refractory strain of the malaria vector Anopheles gambiae. Science 234, 607610.
Creasey, A. M., Ranford-Cartwright, L. C., Moore, D. J., Williamson, D. H., Wilson, R. J. M., Walliker, D. and Carter, R. (1993). Uniparental inheritance of the mitochondrial gene cytochrome-b in Plasmodium falciparum. Current Genetics 23, 360364.
Dawes, E. J., Zhuang, S., Sinden, R. E. and Basáñez, M. G. (2009). The temporal dynamics of Plasmodium density through the sporogonic cycle within Anopheles mosquitoes. Transactions of the Royal Society of Tropical Medicine and Hygiene. Apr 4. [Epub ahead of print]
Dimopoulos, G., Muller, H-M., Levashina, E. A. and Kafatos, F. C. (2001). Innate immune defense against malaria infection in the mosquito. Current Opinion in Immunology 13, 7988.
Florens, L., Washburn, M. P., Raine, J. D., Anthony, R. M., Grainger, M., Haynes, J. D., Moch, J. K., Muster, N., Sacci, J. B., Tabb, D. L., Witney, A. A., Wolters, D., Wu, Y., Gardner, M. J., Holder, A. A., Sinden, R. E., Yates, J. R. and Carucci, D. J. (2002). A proteomic view of the Plasmodium falciparum life cycle. Natur, Londone 419, 520526.
Garnham, P. C. C. (1966). Malaria Parasites and other Haemosporidia. Blackwell Scientific Publications. Oxford, UK.
Geissbühler, Y., Kannady, K., Chaki, P. P, Emidi, B., Govella, N. J., Mayagaya, V., Kiama, M., Mtasiwa, D., Mshinda, H., Lindsay, S. W., Tanner, M., Fillinger, U., de Castro, M. C. and Killeen, G. F. (2009). Microbial larvicide application by a large-scale, community-based program reduces malaria infection prevalence in Urban Dar Es Salaam, Tanzania. PLoS One 4, e5107, Epub 2009 Mar 31.
Greenwood, B. (2009). Can malaria be eliminated? Research, education and capacity development in resource-poor settings – a Festschrift for Professor M.E. Molyneux OBE. Transactions of the Royal Society of Tropical Medicine and Hygiene 103, (Suppl. 1), S2S5.
Hall, N., Karras, M., Raine, J. D., Carlton, J. M., Kooij, T. W. J., Berriman, M., Florens, L., Janssen, C. S., Pain, A., Christophides, G. K., James, K., Rutherford, K., Harris, B., Harris, D. B., Churcher, C., Quail, M. A., Ormond, D., Doggett, J., Trueman, H. E., Mendoza, J., Bidwell, S. L., Rajandream, M-A., Carucci, D. J., Yates, J. R. III, Kafatos, F. C., Janse, C. J., Barrell, B., Turner, C. M. R., Waters, A. P. and Sinden, R. E. (2005). A comprehensive survey of the Plasmodium life cycle by genomic, transcriptomic, and proteomic analyses. Science 307, 8286.
Han, Y. S., Thompson, J., Kafatos, F. C. and Barillas-Mury, C. (2000). Molecular interactions between Anopheles stephensi midgut cells and Plasmodium berghei: the time bomb theory of ookinete invasion of mosquitoes. The EMBO Journal 19, 60306040.
Hayward, R. E., DeRisi, J. L., Alfadhli, S., Kaslow, D. C., Brown, P. O. and Rathod, P. K. (2000). Shotgun DNA microarrays and stage-specific gene expression in Plasmodium falciparum malaria. Molecular Microbiology 35, 6–14.
Hulls, R. H. (1971). The adverse effects of a microsporidian on the sporogony and infectivity of Plasmodium berghei. Transactions of the Royal Society of Tropical Medicine and Hygiene 65, 421422.
Janse, C. J., Mons, B., Rouwenhorst, R. J., Klooster van der, P. F. J., Overdulve, J. P. and Kaay van der, H. J. (1985). In vitro formation of ookinetes and functional maturity of Plasmodium berghei gametocytes. Parasitology 91, 1929.
Khan, S. M., Franke-Fayard, B., Mair, G. R., Lasonder, E., Janse, C. J., Mann, M. and Waters, A. P. (2005). Proteome analysis of separated male and female gametocytes reveals novel sex-specific Plasmodium biology. Cell 121, 675687.
Krotoski, W. A. (1985). Discovery of the hypnozoite and a new theory of malarial relapse. Transactions of the Royal Society of Tropical Medicine and Hygiene 79, 111.
Kumar, S. and Barillas-Mury, C. (2005). Ookinete-induced midgut peroxidases detonate the time bomb in anopheline mosquitoes. Insect Biochemistry and Molecular Biology 35, 721727.
Lal, K., Delves, M. J., Bromley, E., Wastling, J. M., Tomley, F. M. and Sinden, R. E. (2009 a). Plasmodium male development gene-1 (mdv-1) is important for female sexual development and identifies a polarised plasma membrane during zygote development. International Journal for Parasitology 39, 755761.
Lal, K., Bromley, E., Prieto, H., Sanderson, S. J., Yates, J. R. III, Wastling, J. M., Tomley, F. M. and Sinden, R. E. (2009 b). Characterisation of Plasmodium invasive organelles, an ookinete microneme proteome. Proteomics 9, 11421151.
Landau, I., Chabaud, A. G., Mora-Silvera, E., Coquelin, F., Boulard, Y., Rénia, L. and Snounou, G. (1999). Survival of rodent malaria merozoites in the lymphatic network: potential role in chronicity of the infection. Parasite 6, 311322.
Lasonder, E., Ishihama, Y., Andersen, J. S., Vermunt, A. M. W., Paln, A., Sauervein, R. W., Eling, W. M. C., Hall, N., Waters, A. P., Stunnenberg, H. G. and Mann, M. (2002). Analysis of the Plasmodium falciparum proteome by high-accuracy mass spectrometry. Nature, London 419, 537542.
Lasonder, E., Janse, C. J., van Gemert, G.-J., Mair, G. R., Vermunt, A. M. W., Douradinha, B. G., van Noort, V., Huynen, M. A., Luty, A. J. F., Kroeze, H., Khan, S. M., Sauerwein, R. W., Waters, A. P., Mann, M. and Stunnenberg, H. G. (2008). Proteomic profiling of Plasmodium sporozoite maturation identifies new proteins essential for parasite development and infectivity. PLoS Pathogens 4, e1000195.
Le Roch, K. G., Johnson, J. R., Florens, L., Zhou, Y., Santrosyan, A., Grainger, M., Yan, S. F., Williamson, K. C., Holder, A. A., Carucci, D. J., Yates, J. R. III. and Winzeler, E. A. (2004). Global analysis of transcript and protein levels across the Plasmodium falciparum life cycle. Genome Research 14, 23082318.
Le Roch, K. G., Zhou, Y., Blair, P. L., Grainger, M., Moch, J. K., Haynes, J. D., de la Vega, P., Holder, A. A., Batalov, S., Carucci, D. J. and Winzeler, E. A. (2003). Discovery of gene function by expression profiling of the malaria parasite life cycle. Science 301, 15031508.
Levashina, E. A., Moita, L. F., Blandin, S., Vriend, G., Lagueux, M. and Kafatos, F. C. (2001). Conserved role of a complement-like protein in phagocytosis revealed by dsRNA knockout in cultured cells of the mosquito, Anopheles gambiae. Cell 104, 709718.
Liu, Y., Tewari, R., Ning, J., Blagborough, A. M., Pei, J., Grishin, N. V., Steele, R. E., Sinden, R. E., Snell, W. J. and Billker, O. (2008). A conserved mechanism for gamete fusion. Genes and Development 22, 10511068.
Luckhart, S., Vodovotz, Y., Cui, L. W. and Rosenberg, R. (1998). The mosquito Anopheles stephensi limits malaria parasite development with inducible synthesis of nitric oxide. Proceedings of the National Academy of Sciences, USA 95, 57005705.
Maegraith, B. G. (1948). Pathological Processes in Malaria and Blackwater Fever. Blackwell Scientific Publications, Oxford, UK.
Mair, G., Braks, J. A. M., Garver, L. S., Wiegant, J. C. A. G., Hall, N., Dirks, R. W., Khan, S. M., Dimopoulos, G., Janse, C. J. and Waters, A. P. (2006). Regulation of sexual development of Plasmodium by translational repression. Science 313, 667669.
Osta, M. A., Christophides, G. K. and Kafatos, F. C. (2004). Effects of mosquito genes on Plasmodium development. Science 303, 20302032.
Paton, M. G., Barker, G. C., Matsuoka, H., Ramesar, J., Janse, C. J., Waters, A. P. and Sinden, R. E. (1993). Structure and expression of a conserved and post-transcriptionally regulated gene encoding a surface protein of the sexual stages from malaria parasite Plasmodium berghei. Molecular and Biochemical Parasitology 59, 263276.
Patra, K. P., Johnson, J. R., Cantin, G. T., Yates, J. R. III. and Vinetz, J. M. (2008). Proteomic analysis of zygote and ookinete stages of the avian malaria parasite Plasmodium gallinaceum deliniates the homologous proteomes of the lethal human malaria parasite Plasmodium falciparum. Proteomics 8, 24922499.
Poudel, S., Newman, R. A. and Vaughan, J. A. (2008). Rodent Plasmodium: population dynamics of early sporogony within Anopheles stephensi mosquitoes. The Journal of Parasitology 94, 999–1008.
Povolones, M., Waterhouse, R. M., Kafatos, F. and Christophides, G. K. (2009). Leucine-rich repeat protein complex activates mosquito complement in defense against Plasmodium parasites. Science 324, 258261.
Pradel, G. and Frevert, U. (2001). Malaria sporozoites actively enter and pass through rat Kupffer cells prior to hepatocyte invasion. Hepatology 33, 11541165.
Raine, J. D., Ecker, A., Mendoza, J., Tewari, R., Stanway, R. R. and Sinden, R. E. (2007). Female inheritance of malarial lap genes is essential for mosquito transmission. PLoS Pathogens 3, e30.
Read, A. F., Lynch, P. A. and Thomas, M. B. (2009). How to make evolution-proof insecticides for malaria control. PLoS Biology 7, e1000058.
Rowland, M. and Boersma, E. (1988). Changes in the spontaneous flight activity of the mosquito Anopheles stephensi by parasitization with the rodent malaria Plasmodium yoelii. Parasitology 97, 221227.
Schiefer, B. A., Ward, R. A. and Eldridge, B. F. (1977). Plasmodium cynomologi: effects of malaria infection on laboratory flight performance of Anopheles stephensi mosquitoes. Experimental Parasitology 41, 397404.
Schneider, I. and Vanderberg, J. P. (1980). Culture of the invertebrate stages of plasmodia and the culture of mosquito tissues. In Malaria (ed. Kreier, J. P.), pp. 235270. Academic Press, New York, USA.
Silvestrini, F., Alano, P. and Williams, J. L. (2000). Commitment to the production of male and female gametocytes in the human malaria parasite Plasmodium falciparum. Parasitology 121, 465471.
Silvestrini, F., Bozdech, Z., Lanfrancotti, A., Di Guilio, E., Bultrini, E., Picci, L., deRisi, J. L., Pizzi, E. and Alano, P. (2005). Genome-wide identification of genes upregulated at the onset of gametocytogenesis in Plasmodium falciparum. Molecular and Biochemical Parasitology 143, 100110.
Sinden, R. E., Canning, E. U. and Spain, B. (1976). Gametogenesis and fertilization in Plasmodium yoelii nigeriensis: a transmission electron microscope study. Proceedings of the Royal Society of London, B 193, 5576.
Sinden, R. E., Dawes, E. J., Alavi, Y., Waldock, J., Finney, O., Mendoza, J., Butcher, G. A., Andrews, L., Hill, A. V., Gilbert, S. C. and Basanez, M-G. (2008). Progression of Plasmodium berghei through Anopheles stephensi is density-dependent. PLoS Pathogens 3, e195.
Sinden, R. E., Hartley, R. H. and Winger, L. (1985). The development of Plasmodium ookinetes in vitro: an ultrastructural study including a description of meiotic division. Parasitology 91, 227244.
Smalley, M. E. (1976). Plasmodium falciparum gametocytogenesis in vitro. Nature, London 264, 271272.
Smith, T. G., Lourenço, P., Carter, R., Walliker, D. and Ranford-Cartwright, L. C. (2000). Commitment to sexual differentiation in the human malaria parasite, Plasmodium falciparum. Parasitology 91, 127133.
Strome, C. P. A., DeSantis, P. L. and Beaudoin, R. L. (1979). The cultivation of the exoerythrocytic stages of Plasmodium berghei from sporozoites. In Vitro 15, 531536.
Sullivan, M., Li, J., Kumar, S., Rogers, M. J. and McCutchan, T. F. (2000). Effects of interruption of apicoplast function on malaria infection, development and transmission. Molecular and Biochemical Parasitology 109, 1723.
Tarun, A. S., Peng, X., Dumpit, R. F., Ogata, Y., Silva-Rivera, H., Camargo, N., Bergman, L. W. and Kappe, S. H. I. (2008). A combined transcriptome and proteome survey of malaria parasite liver stages. Proceedings of the National Academy of Sciences, USA 105, 305310.
Terenius, O., Marinotti, O., Sieglaff, D. and James, A. A. (2008). Molecular genetic manipulation of vector mosquitoes. Cell Host and Microbe 4, 417423.
Thomas, M. B. and Read, A. F. (2007). Can fungal pesticides control malaria? Nature Reviews Microbiology 5, 377383.
Trager, W. and Jensen, J. B. (1976). Human malaria parasites in continuous culture. Science 193, 673675.
Vaidya, A. B., Morrisey, J., Plowe, C. V., Kaslow, D. C. and Wellems, T. E. (1993). Unidirectional dominance of cytoplasmic inheritance in two genetic crosses of Plasmodium falciparum. Molecular Cell Biology 13, 73497357.
Valkiunas, G. (2005). Avian Malaria Parasites and other Haemosporidia. CRC Press, Boca Raton, London, New York and Washington DC, USA.
van Dijk, M. R., Janse, C. J., Thompson, J., Waters, A. P., Braks, J. A. M., Dodemont, H. J., Stunnenberg, H. G., van Gemert, G-J., Sauerwein, R. W. and Eling, W. (2001). A central role for P48/45 in malaria parasite male gamete fertility. Cell 104, 153164.
van Schaijk, B. C. L., van Dijk, M. R., van de Vegte-Bolmer, M., van Gemert, G-J., van Dooren, M. W., Eksi, S., Roeffen, W. F. G., Janse, C. J., Waters, A. P. and Sauerwein, R. W. (2006). Pfs47, paralog of the male fertility factor Pfs48/45, is a female specific surface protein in Plasmodium falciparum. Molecular and Biochemical Parasitology 149, 216222.
Vaughan, J. A. (2006). Population dynamics of Plasmodium sprorogony. Trends in Parasitology 2, 6370.
Vernick, K. D., Fujioka, H., Seeley, D. C., Tandler, B., Aikawa, M. and Miller, L. H. (1995). Plasmodium gallinaceum: a refractory mechanism of ookinete killing in the mosquito, anopheles gambiae. Experimental Parasitology 80, 583595.
Wernsdsorfer, W. H. and McGregor, I. (1988). Malaria. Principles and Practice of Malariology. Vols 1 and 2, Churchill Livingstone, Edinburgh, London, Melbourne and New York.
Yoeli, M. and Upmanis, R. S. (1968). Plasmodium berghei ookinete formation in vitro. Experimental Parasitology 22, 122128.
Young, J. A., Fivelman, Q. L., Blair, P. L., de la Vega, P., Le Roch, K. G., Zhou, Y., Carucci, D. J., Baker, D. A. and Winzeler, E. A. (2005). The Plasmodium falciparum sexual development transcriptome: a microaaray analysis using ontology-based pattern identification. Molecular and Biochemical Parasitology 143, 6779.
Yuda, M., Iwanaga, S., Shigenobu, S., Mair, G. R., Janse, C. J., Waters, A. P., Kato, T. and Kaneko, I. (2009). Identification of a transcription factor in the mosquito-invasive stage of malaria parasites. Molecular Microbiology 71, 14021414.

Keywords

Metrics

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed