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

Parasitology

Volumn 132, Issue SUPPL. 1, 2006, Pages

  Hurd, H ^a   Grant, K M ^a   Arambage, S C ^a  

^a KEELE UNIVERSITY   (United Kingdom)

Author keywords

Apoptosis; Malaria; Mosquito cysteine proteases; Plasmodium

Indexed keywords

CALPAIN; CALPASTATIN; CASPASE; CATHEPSIN; CYSTEINE PROTEINASE; NITRIC OXIDE;

APOPTOSIS; BIOCHEMISTRY; DROSOPHILA; EGG PRODUCTION; ENZYME ACTIVITY; EPITHELIUM CELL; GENOME; HOST PARASITE INTERACTION; HOST RESISTANCE; INTESTINE CELL; MALARIA; MAMMAL; MAMMAL CELL; MIDGUT; MOSQUITO; NONHUMAN; NUCLEOTIDE SEQUENCE; OVARY FOLLICLE; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PARASITE SURVIVAL; PARASITE TRANSMISSION; PARASITE VECTOR; PLASMODIUM BERGHEI; PLASMODIUM GALLINACEUM; PLASMODIUM MALARIAE; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW; TIME;

ANIMALS; APOPTOSIS; CALPAIN; CASPASES; CATHEPSINS; CULICIDAE; FEMALE; HOST-PARASITE RELATIONS; INSECT VECTORS; INTESTINAL MUCOSA; INTESTINES; NITRIC OXIDE; OVARY; PLASMODIUM; TIME FACTORS;

MAMMALIA;

EID: 33750341991     PISSN: 00311820     EISSN: 14698161     Source Type: Journal    
DOI: 10.1017/S0031182006000849     Document Type: Review

References (107)

1. 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.
2. 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.
3. 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.
4. 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.
5. 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.
6. 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.
7. Alvarez, B. and Radi, R. (2003). Peroxynitrite reactivity with amino acids and proteins. Amino Acids 25, 295-311.
8. Atamna, H. and Ginsburg, H. (1993). Origin of reactive oxygen species in erythrocytes infected with Plasmodium falciparum. Molecular and Biochemical Parasitology 61, 231-241.
9. 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.
10. 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.
11. Barrett, A. J. and Rawlings, N. D. (2001). Evolutionary lines of cysteine peptidases. Biological Chemistry 382, 727-733.
12. 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.
13. Baton, L. A. and Ranford-Cartwright, L. C. (2005a). How do malaria ookinetes cross the mosquito midgut wall? Trends in Parasitology 21, 22-28.
14. Baton, L. A. and Ranford-Cartwright, L. C. (2005b). Spreading the seeds of million-murdering death: metamorphoses of malaria in the mosquito. Trends in Parasitology 21, 573-580.
15. Blandin, S. and Levashina, E. A. (2004). Mosquito immune responses against malaria parasites. Current Opinion in Immunology 16, 16-20.
16. 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.
17. 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.
18. Bursch, W. (2001). The autophagosomal-lysosomal compartment in programmed cell death. Cell Death and Differentiation 8, 569-581.
19. 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.
20. 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.
21. Clark, I. A., Rockett, K. A. and Burgner, D. (2003). Genes, nitric oxide and malaria in African children. Trends in Parasitology 19, 335-337.
22. 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.
23. 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.
24. 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.
25. Deponte, M. and Becker, K. (2004). Plasmodium falciparum - do killers commit suicide? Trends in Parasitology 20, 165-169.
26. Dimopoulos, G. (2003). Insect immunity and its implication in mosquito-malaria interactions. Cell Microbiology 5, 3-14.
27. 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.
28. 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.
29. 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.
30. 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.
31. 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.
32. 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.
33. 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.
34. 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.
35. 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.
36. 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.
37. 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.
38. 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.
39. 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.
40. 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.
41. 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.
42. 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.
43. Hurd, H. (2003). Manipulation of medically important insect vectors by their parasites. Annual Review of Entomology 48, 141-161.
44. Hurd, H. and Carter, V. (2004). The role of programmed cell death in Plasmodium-mosquito interactions. International Journal for Parasitology 34, 1459-1472.
45. 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.
46. Hurd, H., Taylor, P., Adams, D., Underhill, A. and Eggleston, P. (2006). Evaluating the costs of mosquito resistance to malaria. Evolution 59, 2560-2572.
47. 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.
48. 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.
49. 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.
50. 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.
51. 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.
52. 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.
53. 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.
54. 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.
55. 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.
56. 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.
57. 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.
58. 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.
59. McCall, K. (2004). Eggs over easy: cell death in the Drosophila ovary. Developmental Biology 274, 3-14.
60. McIntosh, M. T., Elliott, D. A. and Joiner, K. A. (2005). Plasmodium falciparum: discovery of peroxidase active organelles. Experimental Parasitology 111, 133-136.
61. Michel, K. and Kafatos, F. C. (2005). Mosquito immunity against Plasmodium. Insect Biochemistry and Molecular Biology 35, 677-689.
62. 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.
63. 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.
64. 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.
65. Müller, S. (2004). Redox and antioxidant systems of the malaria parasite Plasmodium falciparum. Molecular Microbiology 53, 1291-1305.
66. Murphy, M. P. (1999). Nitric oxide and cell death. Biochimica et Biophysica Acta 1411, 401-414.
67. 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.
68. 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.
69. Osta, M. A., Christophides, G. K. and Kafatos, F. C. (2004a). Effects of mosquito genes on Plasmodium development. Science 303, 2030-2032.
70. Osta, M. A., Christophides, G. K., Vlachou, D. and Kafatos, F. C. (2004b). Innate immunity in the malaria vector Anopheles gambiae: comparative and functional genomics. Journal of Experimental Biology 207, 2551-2563.
71. 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.
72. 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.
73. 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.
74. 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.
75. 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.
76. Rosenthal, P. J. (1995). Plasmodium falciparum: effects of proteinase inhibitors on globin hydrolysis by cultured malaria parasites. Experimental Parasitology 80, 272-281.
77. Rosenthal, P. J. (2004). Cysteine proteases of malaria parasites. International Journal for Parasitology 34, 1489-1499.
78. 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.
79. 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.
80. 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.
81. Sinden, R. E. (2002). Molecular interactions between Plasmodium and its insect vectors. Cellular Microbiology 4, 713-724.
82. 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.
83. 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.
84. Squier, M. K. and Cohen, J. J. (1997). Calpain, an upstream regulator of thymocyte apoptosis. Journal of Immunology 158, 3690-3697.
85. 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.
86. 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.
87. 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.
88. 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.
89. Thornberry, N. A. (1997). The caspase family of cysteine proteases. British Medical Bulletin 53, 478-490.
90. 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.
91. Toler, S. (2005). The plasmodial apicoplast was retained under evolutionary selective pressure to assuage blood oxidative stress. Medical Hypothesis 65, 683-690.
92. 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.
93. 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.
94. Vaughan, J. A., Hensley, L. and Beier, J. C. (1994a). Sporogonic development of Plasmodium yoelii in five anopheline species. Journal of Parasitology 80, 674-681.
95. Vaughan, J. A., Noden, B. H. and Beier, J. C. (1994b). Sporogonic development of cultured Plasmodium falciparum in six species of laboratory-reared Anopheles mosquitoes. American Journal of Tropical Medicine and Hygiene 51, 233-243.
96. 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.
97. 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.
98. 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.
99. 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.
100. 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.
101. 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.
102. 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.
103. 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.
104. 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.
105. 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.
106. 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.
107. 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.