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Apoptosis-like death as a feature of malaria infection in mosquitoes

Published online by Cambridge University Press:  03 October 2006

H. HURD ,
K. M. GRANT  and
S. C. ARAMBAGE
H. HURD
Affiliation:
Centre for Applied Entomology and Parasitology, Institute for Science and Technology in Medicine, University of Keele, Staffordshire, ST5 5BG, UK
K. M. GRANT
Affiliation:
Centre for Applied Entomology and Parasitology, Institute for Science and Technology in Medicine, University of Keele, Staffordshire, ST5 5BG, UK
S. C. ARAMBAGE
Affiliation:
Centre for Applied Entomology and Parasitology, Institute for Science and Technology in Medicine, University of Keele, Staffordshire, ST5 5BG, UK
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Abstract

Malaria parasites of the genus Plasmodium make a hazardous journey through their mosquito vectors. The majority die in the process, many as a result of the action of mosquito defence mechanisms. The mosquito too is not unscathed by the encounter with these parasites. Tissue damage occurs as a result of mid-gut invasion and reproductive fitness is lost when many developing ovarian follicles are resorbed. Here we discuss some of the mechanisms that are involved in killing the parasite and in the self-defence mechanisms employed by the mosquito to repair the mid-gut epithelium and to manipulate resources altering the trade-off position that balances reproduction and survival. In all cases, cells die by apoptotic-like mechanisms. In the midgut cells, apoptosis-induction pathways are being elucidated, the molecules involved in apoptosis are being recognised and Drosophila homologues sought. The death of ookinetes in the mosquito mid-gut lumen is associated with caspase-like activity and, although homologues of mammalian caspases are not present in the malaria genome, other cysteine proteases that are potential candidates have been discussed. In the ovary, apoptosis of patches of follicular epithelial cells is followed by resorption of the developing follicle and a subsequent loss of egg production in that follicle.

Keywords

ApoptosisPlasmodiummalariamosquito cysteine proteases
Type
Research Article
Information
Parasitology , Volume 132 , Supplement S1: Programmed cell death and the protozoan parasite , March 2006 , pp. S33 - S47
Copyright
© 2006 Cambridge University Press

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References

REFERENCES

Abraham, E. G., Islam, S., Srinivasan, P., Ghosh, A. K., Valenzuela, J. G., Ribeiro, J. M., Kafatos, F. C., Dimopoulos, G. and Jacobs-Lorena, M. ( 2004). Analysis of the Plasmodium and Anopheles transcriptional repertoire during ookinete development and midgut invasion. Journal of Biological Chemistry 279, 5573–5580.CrossRefGoogle Scholar
Abraham, E. G., Pinto, S. B., Ghosh, A., Vanlandingham, D. L., Budd, A., Higgs, S., Kafatos, F. C., Jacobs-Lorena, M. and Michel, K. ( 2005). An immune-responsive serpin, SRPN6, mediates mosquito defense against malaria parasites. Proceedings of the National Academy of Sciences, USA 279, 5573–5580.CrossRefGoogle Scholar
Ahmed, A. M., Baggott, S., Maingon, R. and Hurd, H. ( 2002). The costs of mounting an immune response are reflected in the reproductive fitness of Anopheles gambiae. Oikos 97, 371–377.CrossRefGoogle Scholar
Ahmed, A. M. and Hurd, H. ( 2006). Immune stimulation and malaria infection impose reproductive costs in Anopheles gambiae via follicular apoptosis. Microbes and Infection 8, 308–315.CrossRefGoogle Scholar
Alavi, Y., Arai, M., Mendoza, J., Tufet-Bayona, M., Sinha, R., Fowler, K., Billker, O., Franke-Fayard, B., Janse, C. J., Waters, A. 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, 933–943.CrossRefGoogle Scholar
Al-Olayan, E. M., Williams, G. T. and Hurd, H. ( 2002). Apoptosis in the malaria protozoan, Plasmodium berghei: a possible mechanism for limiting intensity of infection in the mosquito. International Journal for Parasitology 32, 1133–1143.CrossRefGoogle Scholar
Alvarez, B. and Radi, R. ( 2003). Peroxynitrite reactivity with amino acids and proteins. Amino Acids 25, 295–311.CrossRefGoogle Scholar
Atamna, H. and Ginsburg, H. ( 1993). Origin of reactive oxygen species in erythrocytes infected with Plasmodium falciparum. Molecular and Biochemical Parasitology 61, 231–241.CrossRefGoogle Scholar
Bai, P., Bakondi, E., Szabo, E., Gergely, P., Szabo, C. and Virag, L. ( 2001). Partial protection by poly(ADP-ribose) polymerase inhibitors from nitroxyl-induced cytotoxity in thymocytes. Free Radical Biology and Medicine 31, 1616–1623.CrossRefGoogle Scholar
Balmer, P., Phillips, H. M., Maestre, A. E., McMonagle, F. A. and Phillips, R. S. ( 2000). The effect of nitric oxide on the growth of Plasmodium falciparum, P. chabaudi and P. berghei in vitro. Parasite Immunology 22, 97–106.CrossRefGoogle Scholar
Barrett, A. J. and Rawlings, N. D. ( 2001). Evolutionary lines of cysteine peptidases. Biological Chemistry 382, 727–733.CrossRefGoogle Scholar
Baton, L. A. and Ranford-Cartwright, L. C. ( 2004). Plasmodium falciparum ookinete invasion of the midgut epithelium of Anopheles stephensi is consistent with the Time Bomb model. Parasitology 129, 663–676.CrossRefGoogle Scholar
Baton, L. A. and Ranford-Cartwright, L. C. ( 2005 a). How do malaria ookinetes cross the mosquito midgut wall? Trends in Parasitology 21, 22–28.Google Scholar
Baton, L. A. and Ranford-Cartwright, L. C. ( 2005 b). Spreading the seeds of million-murdering death: metamorphoses of malaria in the mosquito. Trends in Parasitology 21, 573–580.Google Scholar
Blandin, S. and Levashina, E. A. ( 2004). Mosquito immune responses against malaria parasites. Current Opinion in Immunology 16, 16–20.CrossRefGoogle Scholar
Blomgren, K., Zhu, C., Wang, X., Karlsson, J. O., Leverin, A. L., Bahr, B. A., Mallard, C. and Hagberg, H. ( 2001). Synergistic activation of caspase-3 by m-calpain after neonatal hypoxia-ischemia: a mechanism of “pathological apoptosis”? Journal of Biological Chemistry 276, 10191–10198.Google Scholar
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 Epub.CrossRefGoogle Scholar
Bursch, W. ( 2001). The autophagosomal-lysosomal compartment in programmed cell death. Cell Death and Differentiation 8, 569–581.CrossRefGoogle Scholar
Chao, S. and Nagoshi, R. N. ( 1999). Induction of apoptosis in the germline and follicle layer of Drosophila egg chambers. Mechanisms of Development 88, 159–172.CrossRefGoogle Scholar
Christophides, G. K., Zdobnov, E., Barillas-Mury, C., Birney, E., Blandin, S., Blass, C., Brey, P. T., Collins, F. H., Danielli, A., Dimopoulos, G., Hetru, C., Hoa, N. T., Hoffmann, J. A., Kanzok, S. M., Letunic, I., Levashina, E. A., Loukeris, T. G., Lycett, G., Meister, S., Michel, K., Moita, L. F., Muller, H. M., Osta, M. A., Paskewitz, S. M., Reichhart, J. M., Rzhetsky, A., Troxler, L., Vernick, K. D., Vlachou, D., Volz, J., von Mering, C., Xu, J., Zheng, L., Bork, P. and Kafatos, F. C. ( 2002). Immunity-related genes and gene families in Anopheles gambiae. Science 298, 159–165.CrossRefGoogle Scholar
Clark, I. A., Rockett, K. A. and Burgner, D. ( 2003). Genes, nitric oxide and malaria in African children. Trends in Parasitology 19, 335–337.CrossRefGoogle Scholar
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, 607–610.CrossRefGoogle Scholar
Crampton, A. and Luckhart, S. ( 2001). The role of As60A, a TGF-beta homolog, in Anopheles stephensi innate immunity and defense against Plasmodium infection. Infection Genetics and Evolution 1, 131–141.CrossRefGoogle Scholar
Danielli, A., Barillas-Mury, C., Kumar, S., Kafatos, F. C. and Loukeris, T. G. ( 2005). Overexpression and altered nucleocytoplasmic distribution of Anopheles ovalbumin-like SRPN10 serpins in Plasmodium-infected midgut cells. Cellular Microbiology 7, 181–190.CrossRefGoogle Scholar
Deponte, M. and Becker, K. ( 2004). Plasmodium falciparum – do killers commit suicide? Trends in Parasitology 20, 165–169.Google Scholar
Dimopoulos, G. ( 2003). Insect immunity and its implication in mosquito-malaria interactions. Cell Microbiology 5, 3–14.CrossRefGoogle Scholar
Eksi, S., Czesny, B., Greenbaum, D. C., Bogyo, M. and Williamson, K. C. ( 2004). Targeted disruption of Plasmodium falciparum cysteine protease, falcipain 1, reduces oocyst production, not erythrocytic stage growth. Molecular Microbiology 53, 243–250.CrossRefGoogle Scholar
Fox, B. A. and Bzik, D. J. ( 1994). Analysis of stage-specific transcripts of the Plasmodium falciparum serine repeat antigen (SERA) gene and transcription from the SERA locus. Molecular and Biochemical Parasitology 68, 133–144.CrossRefGoogle Scholar
Gamboa de Dominguez, N. D. and Rosenthal, P. J. ( 1996). Cysteine proteinase inhibitors block early steps in hemoglobin degradation by cultured malaria parasites. Blood 87, 4448–4454.Google Scholar
Gardner, M. J., Hall, N., Fung, E., White, O., Berriman, M., Hyman, R. W., Carlton, J. M., Pain, A., Nelson, K. E., Bowman, S., Paulsen, I. T., James, K., Eisen, J. A., Rutherford, K., Salzberg, S. L., Craig, A., Kyes, S., Chan, M. S., Nene, V., Shallom, S. J., Suh, B., Peterson, J., Angiuoli, S., Pertea, M., Allen, J., Selengut, J., Haft, D., Mather, M. W., Vaidya, A. B., Martin, D. M., Fairlamb, A. H., Fraunholz, M. J., Roos, D. S., Ralph, S. A., McFadden, G. I., Cummings, L. M., Subramanian, G. M., Mungall, C., Venter, J. C., Carucci, D. J., Hoffman, S. L., Newbold, C., Davis, R. W., Fraser, C. M. and Barrell, B. ( 2002). Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 419, 498–511.CrossRefGoogle Scholar
Ghosh, A., Edwards, M. J. and Jacobs-Lorena, M. ( 2000). The journey of the malaria parasite in the mosquito: hopes for the new century. Parasitology Today 16, 196–201.CrossRefGoogle Scholar
Goh, S. L., Goh, L. L. and Sim, T. S. ( 2005). Cysteine protease falcipain 1 in Plasmodium falciparum is biochemically distinct from its isozymes. Parasitology Research 97, 295–301.CrossRefGoogle Scholar
Gor, D. O., Li, A. C., Wiser, M. F. and Rosenthal, P. J. ( 1998). Plasmodial serine repeat antigen homologues with properties of schizont cysteine proteases. Molecular and Biochemical Parasitology 95, 153–158.CrossRefGoogle Scholar
Gupta, L., Kumar, S., Han, Y. S., Pimenta, P. F. and Barillas-Mury, C. ( 2005). Midgut epithelial responses of different mosquito-Plasmodium combinations: the actin cone zipper repair mechanism in Aedes aegypti. Proceedings of the National Academy of Sciences, USA 102, 4010–4015.CrossRefGoogle Scholar
Hall, N., Karras, M., Raine, J. D., Carlton, J. M., Kooij, T. W., Berriman, M., Florens, L., Janssen, C. S., Pain, A., Christophides, G. K., James, K., Rutherford, K., Harris, B., Harris, D., 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., 3rd, Kafatos, F. C., Janse, C. J., Barrell, B., Turner, C. M., Waters, A. P. and Sinden, R. E. ( 2005). A comprehensive survey of the Plasmodium life cycle by genomic, transcriptomic, and proteomic analyses. Science 307, 82–86.CrossRefGoogle Scholar
Han, Y. S. and Barillas-Mury, C. ( 2002). Implications of Time Bomb model of ookinete invasion of midgut cells. Insect Biochemistry and Molecular Biology 32, 1311–1316.CrossRefGoogle Scholar
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, 6030–6040.CrossRefGoogle Scholar
Harada, M., Owhashi, M., Suguri, S., Kumatori, A., Nakamura, M., Kanbara, H., Matsuoka, H. and Ishii, A. ( 2001). Superoxide-dependent and -independent pathways are involved in the transmission blocking of malaria. Parasitology Research 87, 605–608.CrossRefGoogle Scholar
Herrera-Ortiz, A., Lanz-Mendoza, H., Martinez-Barnetche, J., Hernandez-Martinez, S., Villarreal-Trevino, C., Aguilar-Marcelino, L. and Rodriguez, M. H. ( 2004). Plasmodium berghei ookinetes induce nitric oxide production in Anopheles pseudopunctipennis midguts cultured in vitro. Insect Biochemistry and Molecular Biology 34, 893–901.CrossRefGoogle Scholar
Hodder, A. N., Drew, D. R., Epa, V. C., Delorenzi, M., Bourgon, R., Miller, S. K., Moritz, R. L., Frecklington, D. F., Simpson, R. J., Speed, T. P., Pike, R. N. and Crabb, B. S. ( 2003). Enzymic, phylogenetic, and structural characterization of the unusual papain-like protease domain of Plasmodium falciparum SERA5. Journal of Biological Chemistry 278, 48169–48177.CrossRefGoogle Scholar
Holt, R. A., Subramanian, G. M., Halpern, A., Sutton, G. G., Charlab, R., Nusskern, D. R., Wincker, P., Clark, A. G., Ribeiro, J. M., Wides, R., Salzberg, S. L., Loftus, B., Yandell, M., Majoros, W. H., Rusch, D. B., Lai, Z., Kraft, C. L., Abril, J. F., Anthouard, V., Arensburger, P., Atkinson, P. W., Baden, H., de Berardinis, V., Baldwin, D., Benes, V., Biedler, J., Blass, C., Bolanos, R., Boscus, D., Barnstead, M., Cai, S., Center, A., Chaturverdi, K., Christophides, G. K., Chrystal, M. A., Clamp, M., Cravchik, A., Curwen, V., Dana, A., Delcher, A., Dew, I., Evans, C. A., Flanigan, M., Grundschober-Freimoser, A., Friedli, L., Gu, Z., Guan, P., Guigo, R., Hillenmeyer, M. E., Hladun, S. L., Hogan, J. R., Hong, Y. S., Hoover, J., Jaillon, O., Ke, Z., Kodira, C., Kokoza, E., Koutsos, A., Letunic, I., Levitsky, A., Liang, Y., Lin, J. J., Lobo, N. F., Lopez, J. R., Malek, J. A., McIntosh, T. C., Meister, S., Miller, J., Mobarry, C., Mongin, E., Murphy, S. D., O'Brochta, D. A., Pfannkoch, C., Qi, R., Regier, M. A., Remington, K., Shao, H., Sharakhova, M. V., Sitter, C. D., Shetty, J., Smith, T. J., Strong, R., Sun, J., Thomasova, D., Ton, L. Q., Topalis, P., Tu, Z., Unger, M. F., Walenz, B., Wang, A., Wang, J., Wang, M., Wang, X., Woodford, K. J., Wortman, J. R., Wu, M., Yao, A., Zdobnov, E. M., Zhang, H., Zhao, Q., Zhao, S., Zhu, S. C., Zhimulev, I., Coluzzi, M., della Torre, A., Roth, C. W., Louis, C., Kalush, F., Mural, R. J., Myers, E. W., Adams, M. D., Smith, H. O., Broder, S., Gardner, M. J., Fraser, C. M., Birney, E., Bork, P., Brey, P. T., Venter, J. C., Weissenbach, J., Kafatos, F. C., Collins, F. H. and Hoffman, S. L. ( 2002). The genome sequence of the malaria mosquito Anopheles gambiae. Science 298, 129–149.CrossRefGoogle Scholar
Hopwood, J. A., Ahmed, A. M., Polwart, A., Williams, G. T. and Hurd, H. ( 2001). Malaria-induced apoptosis in mosquito ovaries: a mechanism to control vector egg production. Journal of Experimental Biology 204, 2773–2780.Google Scholar
Hurd, H. ( 2003). Manipulation of medically important insect vectors by their parasites. Annual Review of Entomology 48, 141–161.CrossRefGoogle Scholar
Hurd, H. and Carter, V. ( 2004). The role of programmed cell death in Plasmodium-mosquito interactions. International Journal for Parasitology 34, 1459–1472.CrossRefGoogle Scholar
Hurd, H., Carter, V. and Nacer, A. ( 2005). Interactions between malaria and mosquitoes: the role of apoptosis in parasite establishment and vector response to infection. Current Topics in Microbiology and Immunology 289, 185–217.CrossRefGoogle Scholar
Hurd, H., Taylor, P., Adams, D., Underhill, A. and Eggleston, P. ( 2006). Evaluating the costs of mosquito resistance to malaria. Evolution 59, 2560–2572.Google Scholar
Kiefer, M. C., Crawford, K. A., Boley, L. J., Landsberg, K. E., Gibson, H. L., Kaslow, D. C. and Barr, P. J. ( 1996). Identification and cloning of a locus of serine repeat antigen (sera)-related genes from Plasmodium vivax. Molecular and Biochemical Parasitology 78, 55–65.CrossRefGoogle Scholar
Kriventseva, E. V., Koutsos, A. C., Blass, C., Kafatos, F. C., Christophides, G. K. and Zdobnov, E. M. ( 2005). AnoEST: toward A. gambiae functional genomics. Genome Research 15, 893–899.Google Scholar
Kumar, S. and Barillas-Mury, C. ( 2005). Ookinete-induced midgut peroxidases detonate the time bomb in anopheline mosquitoes. Insect Biochemistry and Molecular Biology 35, 721–727.CrossRefGoogle Scholar
Kumar, S., Gupta, L., Han, Y. S. and Barillas-Mury, C. ( 2004). Inducible peroxidases mediate nitration of anopheles midgut cells undergoing apoptosis in response to Plasmodium invasion. Journal of Biological Chemistry 279, 53475–53482.CrossRefGoogle Scholar
Lanz-Mendoza, H., Hernandez-Martinez, S., Ku-Lopez, M., Rodriguez Mdel, C., Herrera-Ortiz, A. and Rodriguez, M. H. ( 2002). Superoxide anion in Anopheles albimanus hemolymph and midgut is toxic to Plasmodium berghei ookinetes. Journal of Parasitology 88, 702–706.CrossRefGoogle Scholar
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, 1503–1508.CrossRefGoogle Scholar
Lensen, A., Mulder, L., Tchuinkam, T., Willemsen, L., Eling, W. and Sauerwein, R. ( 1998). Mechanisms that reduce transmission of Plasmodium falciparum malaria in semiimmune and nonimmune persons. Journal of Infectious Disease 177, 1358–1363.CrossRefGoogle Scholar
Lim, J., Gowda, D. C., Krishnegowda, G. and Luckhart, S. ( 2005). Induction of nitric oxide synthase in Anopheles stephensi by Plasmodium falciparum: mechanism of signaling and the role of parasite glycosylphosphatidylinositols. Infection and Immunity 73, 2778–2789.CrossRefGoogle Scholar
Luckhart, S., Crampton, A. L., Zamora, R., Lieber, M. J., Dos Santos, P. C., Peterson, T. M., Emmith, N., Lim, J., Wink, D. A. and Vodovotz, Y. ( 2003). Mammalian transforming growth factor beta1 activated after ingestion by Anopheles stephensi modulates mosquito immunity. Infection and Immunity 71, 3000–3009.CrossRefGoogle Scholar
Luckhart, S., Vodovotz, Y., Cui, L. 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, 5700–5705.CrossRefGoogle Scholar
Madeo, F., Herker, E., Maldener, C., Wissing, S., Lachelt, S., Herlan, M., Fehr, M., Lauber, K., Sigrist, S. J., Wesselborg, S. and Frohlich, K. U. ( 2002). A caspase-related protease regulates apoptosis in yeast. Molecular Cell 9, 911–917.CrossRefGoogle Scholar
Mazzoni, C., Herker, E., Palermo, V., Jungwirth, H., Eisenberg, T., Madeo, F. and Falcone, C. ( 2005). Yeast caspase 1 links messenger RNA stability to apoptosis in yeast. EMBO Reports 6, 1076–1081.CrossRefGoogle Scholar
McCall, K. ( 2004). Eggs over easy: cell death in the Drosophila ovary. Developmental Biology 274, 3–14.CrossRefGoogle Scholar
McIntosh, M. T., Elliott, D. A. and Joiner, K. A. ( 2005). Plasmodium falciparum: discovery of peroxidase active organelles. Experimental Parasitology 111, 133–136.CrossRefGoogle Scholar
Michel, K. and Kafatos, F. C. ( 2005). Mosquito immunity against Plasmodium. Insect Biochemistry and Molecular Biology 35, 677–689.CrossRefGoogle Scholar
Miller, S. K., Good, R. T., Drew, D. R., Delorenzi, M., Sanders, P. R., Hodder, A. N., Speed, T. P., Cowman, A. F., Koning-ward, T. F. and Crabb, B. S. ( 2002). A subset of Plasmodium falciparum SERA genes are expressed and appear to play an important role in the erythrocytic cycle. Journal of Biological Chemistry 277, 47524–47532.CrossRefGoogle Scholar
Motard, A., Landau, I., Nussler, A., Grau, G., Baccam, D., Mazier, D. and Targett, G. A. ( 1993). The role of reactive nitrogen intermediates in modulation of gametocyte infectivity of rodent malaria parasites. Parasite Immunology 15, 21–26.CrossRefGoogle Scholar
Mottram, J. C., Helms, M. J., Coombs, G. H. and Sajid, M. ( 2003). Clan CD cysteine peptidases of parasitic protozoa. Trends in Parasitology 19, 182–187.CrossRefGoogle Scholar
Müller, S. ( 2004). Redox and antioxidant systems of the malaria parasite Plasmodium falciparum. Molecular Microbiology 53, 1291–1305.CrossRefGoogle Scholar
Murphy, M. P. ( 1999). Nitric oxide and cell death. Biochimica et Biophysica Acta 1411, 401–414.CrossRefGoogle Scholar
Nakagawa, T. and Yuan, J. ( 2000). Cross-talk between two cysteine protease families. Activation of caspase-12 by calpain in apoptosis. Journal of Cell Biology 150, 887–894.CrossRefGoogle Scholar
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, 555–562.Google Scholar
Osta, M. A., Christophides, G. K. and Kafatos, F. C. ( 2004 a). Effects of mosquito genes on Plasmodium development. Science 303, 2030–2032.Google Scholar
Osta, M. A., Christophides, G. K., Vlachou, D. and Kafatos, F. C. ( 2004 b). Innate immunity in the malaria vector Anopheles gambiae: comparative and functional genomics. Journal of Experimental Biology 207, 2551–2563.Google Scholar
Pang, X. L., Mitamura, T. and Horii, T. ( 1999). Antibodies reactive with the N-terminal domain of Plasmodium falciparum serine repeat antigen inhibit cell proliferation by agglutinating merozoites and schizonts. Infection and Immunity 67, 1821–1827.Google Scholar
Peterson, T. m. L. and Luckhart, S. ( 2006). A mosquito 2-Cys peroxiredoxin protects against nitrosative and oxidative stresses associated with malaria parasite infection. Free Radical Biology and Medicine 40, 1067–1082.CrossRefGoogle Scholar
Picot, S., Burnod, J., Bracchi, V., Chumpitazi, B. f. F. and Ambroise-Thomas, P. ( 1997). Apoptosis related to chloroquine sensitivity of the human malaria parasite Plasmodium falciparum. Transactions of the Royal Society of Tropical Medicine and Hygiene 91, 590–591.CrossRefGoogle Scholar
Richman, A. M., Dimopoulos, G., Seeley, D. and Kafatos, F. C. ( 1997). Plasmodium activates the innate immune response of Anopheles gambiae mosquitoes. EMBO Journal 16, 6114–6119.CrossRefGoogle Scholar
Rockett, K. A., Awburn, M. M., Cowden, W. B. and Clark, I. A. ( 1991). Killing of Plasmodium falciparum in vitro by nitric oxide derivatives. Infection and Immunity 59, 3280–3283.Google Scholar
Rosenthal, P. J. ( 1995). Plasmodium falciparum: effects of proteinase inhibitors on globin hydrolysis by cultured malaria parasites. Experimental Parasitology 80, 272–281.CrossRefGoogle Scholar
Rosenthal, P. J. ( 2004). Cysteine proteases of malaria parasites. International Journal for Parasitology 34, 1489–1499.CrossRefGoogle Scholar
Rosenthal, P. J., Olson, J. E., Lee, G. K., Palmer, J. T., Klaus, J. L. and Rasnick, D. ( 1996). Antimalarial effects of vinyl sulfone cysteine proteinase inhibitors. Antimicrobial Agents and Chemotherapy 40, 1600–1603.Google Scholar
Rosenthal, P. J., Sijwali, P. S., Singh, A. and Shenai, B. R. ( 2002). Cysteine proteases of malaria parasites: targets for chemotherapy. Current Pharmaceutical Design 8, 1659–1672.CrossRefGoogle Scholar
Rozman-Pungercar, J., Kopitar-Jerala, N., Bogyo, M., Turk, D., Vasiljeva, O., Stefe, I., Vandenabeele, P., Bromme, D., Puizdar, V., Fonovic, M., Trstenjak-Prebanda, M., Dolenc, I., Turk, V. and Turk, B. ( 2003). Inhibition of papain-like cysteine proteases and legumain by caspase-specific inhibitors: when reaction mechanism is more important than specificity. Cell Death and Differentiation 10, 881–888.CrossRefGoogle Scholar
Sinden, R. E. ( 2002). Molecular interactions between Plasmodium and its insect vectors. Cellular Microbiology 4, 713–724.CrossRefGoogle Scholar
Sinden, R. E., Alavi, Y. and Raine, J. D. ( 2004). Mosquito–malaria interactions: a reappraisal of the concepts of susceptibility and refractoriness. Insect Biochemistry and Molecular Biology 34, 625–629.CrossRefGoogle Scholar
Sobolewski, P., Gramaglia, I., Frangos, J., Intaglietta, M. and van der Heyde, H. C. ( 2005). Nitric oxide bioavailability in malaria. Trends in Parasitology 21, 415–422.CrossRefGoogle Scholar
Squier, M. K. and Cohen, J. J. ( 1997). Calpain, an upstream regulator of thymocyte apoptosis. Journal of Immunology 158, 3690–3697.Google Scholar
Squier, M. K., Miller, A. C., Malkinson, A. M. and Cohen, J. J. ( 1994). Calpain activation in apoptosis. Journal of Cell Physiology 159, 229–237.CrossRefGoogle Scholar
Srinivasan, P., Abraham, E. G., Ghosh, A. K., Valenzuela, J., Ribeiro, J. M., Dimopoulos, G., Kafatos, F. C., Adams, J. H., Fujioka, H. and Jacobs-Lorena, M. ( 2004). Analysis of the Plasmodium and Anopheles transcriptomes during oocyst differentiation. Journal of Biological Chemistry 279, 5581–5587.CrossRefGoogle Scholar
Stoka, V., Turk, B., Schendel, S. L., Kim, T. H., Cirman, T., Snipas, S. J., Ellerby, L. M., Bredesen, D., Freeze, H., Abrahamson, M., Bromme, D., Krajewski, S., Reed, J. C., Yin, X. M., Turk, V. and Salvesen, G. S. ( 2001). Lysosomal protease pathways to apoptosis. Cleavage of bid, not pro-caspases, is the most likely route. Journal of Biological Chemistry 276, 3149–3157.CrossRefGoogle Scholar
Tachado, S. D., Gerold, P., McConville, M. J., Baldwin, T., Quilici, D., Schwarz, R. T. and Schofield, L. ( 1996). Glycosylphosphatidylinositol toxin of Plasmodium induces nitric oxide synthase expression in macrophages and vascular endothelial cells by a protein tyrosine kinase-dependent and protein kinase C-dependent signaling pathway. Journal of Immunology 156, 1897–1907.Google Scholar
Thornberry, N. A. ( 1997). The caspase family of cysteine proteases. British Medical Bulletin 53, 478–490.CrossRefGoogle Scholar
Thornberry, N. A., Rano, T. A., Peterson, E. P., Rasper, D. M., Timkey, T., Garcia-Calvo, M., Houtzager, V. M., Nordstrom, P. A., Roy, S., Vaillancourt, J. P., Chapman, K. T. and Nicholson, D. W. ( 1997). A combinatorial approach defines specificities of members of the caspase family and granzyme B. Functional relationships established for key mediators of apoptosis. Journal of Biological Chemistry 272, 17907–17911.CrossRefGoogle Scholar
Toler, S. ( 2005). The plasmodial apicoplast was retained under evolutionary selective pressure to assuage blood oxidative stress. Medical Hypothesis 65, 683–690.CrossRefGoogle Scholar
Turk, B., Stoka, V., Rozman-Pungercar, J., Cirman, T., Droga-Mazovec, G., Oresic, K. and Turk, V. ( 2002). Apoptotic pathways: involvement of lysosomal proteases. Biological Chemistry 383, 1035–1044.CrossRefGoogle Scholar
Uren, A. G., O'Rourke, K., Aravind, L., Pisabarro, M. T., Seshagiri, S., Koonin, E. V. and Dixit, V. M. ( 2000). Identification of paracaspases and metacaspases: two ancient families of caspase-like proteins, one of which plays a key role in MALT lymphoma. Molecular Cell 6, 961–967.CrossRefGoogle Scholar
Vaughan, J. A., Hensley, L. and Beier, J. C. ( 1994 a). Sporogonic development of Plasmodium yoelii in five anopheline species. Journal of Parasitology 80, 674–681.Google Scholar
Vaughan, J. A., Noden, B. H. and Beier, J. C. ( 1994 b). Sporogonic development of cultured Plasmodium falciparum in six species of laboratory-reared Anopheles mosquitoes. American Journal of Tropical Medicine and Hygiene 51, 233–243.Google Scholar
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, 583–595.CrossRefGoogle Scholar
Vlachou, D. and Kafatos, F. C. ( 2005). The complex interplay between mosquito positive and negative regulators of Plasmodium development. Current Opinion in Microbiology 8, 415–421.CrossRefGoogle Scholar
Vlachou, D., Schlegelmilch, T., Christophides, G. K. and Kafatos, F. C. ( 2005). Functional genomic analysis of midgut epithelial responses in Anopheles during Plasmodium invasion. Current Biology 15, 1185–1195.CrossRefGoogle Scholar
Vlachou, D., Zimmermann, T., Cantera, R., Janse, C. J., Waters, A. P. and Kafatos, F. C. ( 2004). Real-time, in vivo analysis of malaria ookinete locomotion and mosquito midgut invasion. Cellular Microbiology 6, 671–685.CrossRefGoogle Scholar
Waterhouse, N. J., Finucane, D. M., Green, D. R., Elce, J. S., Kumar, S., Alnemri, E. S., Litwack, G., Khanna, K., Lavin, M. F. and Watters, D. J. ( 1998). Calpain activation is upstream of caspases in radiation-induced apoptosis. Cell Death and Differentiation 5, 1051–1061.CrossRefGoogle Scholar
Whitten, M. m. A., Shiao, S. H. and Levashina, E. A. ( 2006). Mosquito midguts and malaria: cell biology, compartmentalization and immunology. Parasite Immunology 28, 121–130.CrossRefGoogle Scholar
Wolf, B. B., Schuler, M., Echeverri, F. and Green, D. R. ( 1999). Caspase-3 is the primary activator of apoptotic DNA fragmentation via DNA fragmentation factor-45/inhibitor of caspase-activated DNase inactivation. Journal of Biological Chemistry 274, 30651–30656.CrossRefGoogle Scholar
Wu, Y., Wang, X., Liu, X. and Wang, Y. ( 2003). Data-mining approaches reveal hidden families of proteases in the genome of malaria parasite. Genome Research 13, 601–616.CrossRefGoogle Scholar
Xu, X., Dong, Y., Abraham, E. G., Kocan, A., Srinivasan, P., Ghosh, A. K., Sinden, R. E., Ribeiro, J. M., Jacobs-Lorena, M., Kafatos, F. C. and Dimopoulos, G. ( 2005). Transcriptome analysis of Anopheles stephensi–Plasmodium berghei interactions. Molecular and Biochemical Parasitology 142, 76–87.CrossRefGoogle Scholar
Zheng, L., Wang, S., Romans, P., Zhao, H., Luna, C. and Benedict, M. Q. ( 2003). Quantitative trait loci in Anopheles gambiae controlling the encapsulation response against Plasmodium cynomolgi Ceylon. BMC Genetics 4, 16. Oct 24; 4, 16: http://www.biomedcentral.com/1471-2156/4/16.Google Scholar
Zhu, J., Krishnegowda, G. and Gowda, D. C. ( 2005). Induction of proinflammatory responses in macrophages by the glycosylphosphatidylinositols of Plasmodium falciparum: the requirement of extracellular signal-regulated kinase, p38, c-Jun N-terminal kinase and NF-kappaB pathways for the expression of proinflammatory cytokines and nitric oxide. Journal of Biological Chemistry 280, 8617–8627.CrossRefGoogle Scholar
Zieler, H. and Dvorak, J. A. ( 2000). Invasion in vitro of mosquito midgut cells by the malaria parasite proceeds by a conserved mechanism and results in death of the invaded midgut cells. Proceedings of the National Academy of Sciences, USA 97, 11516–11521.CrossRefGoogle Scholar