Getting infectious: Formation and maturation of plasmodium sporozoites in the Anopheles vector

Cellular Microbiology

Volumn 8, Issue 10, 2006, Pages 1547-1556

  Matuschewski, Kai ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CIRCUMSPOROZOITE PROTEIN; COLLAGEN TYPE 4; LAMININ; PHOSPHOLIPASE; PROTEIN P25; PROTEIN P28;

AEDES; ANOPHELES GAMBIAE; DEVELOPMENTAL GENETICS; DEVELOPMENTAL STAGE; GENE EXPRESSION PROFILING; GENE IDENTIFICATION; HOST PARASITE INTERACTION; HUMAN; MALARIA; MEROZOITE; MOLECULAR MECHANICS; NONHUMAN; OOCYST; PARASITE DEVELOPMENT; PARASITE TRANSMISSION; PARASITE VECTOR; PARASITE VIRULENCE; PLASMODIUM; PLASMODIUM BERGHEI; PLASMODIUM FALCIPARUM; PLASMODIUM GALLINACEUM; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTOZOAL GENETICS; SHORT SURVEY; SPOROZOITE;

ANIMALS; ANOPHELES; HUMANS; INSECT VECTORS; LIFE CYCLE STAGES; MALARIA; PLASMODIUM; SALIVARY GLANDS; SPOROZOITES;

EID: 33748445868     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2006.00778.x     Document Type: Short Survey

References (78)

1. Adini, A., and Warburg, A. (1999) Interaction of Plasmodium gallinaceum ookinetes and oocysts with extracellular matrix proteins. Parasitology 119: 331-336.
2. Al-Olayan, E.M., Beemtsma, A.L., Butcher, G.A., Sinden, R.E., and Hurd, H. (2002) Complete development of mosquito phases of malaria parasite in vitro. Science 295: 677-679.
3. Aly, A., and Matuschewski, K. (2005) A malarial cysteine protease is necessary for Plasmodium sporozoite egress from oocysts. J Exp Med 202: 225-230.
4. Amino, R., Thiberge, S., Martin, B., Celli, S., Shorte, S., Frischknecht, F., and Ménard, R. (2006) Quantitative imaging of Plasmodium transmission from mosquito to mammal. Nat Med 12: 220-224.
5. Baldacci, P., and Ménard, R. (2004) The elusive malaria sporozoite in the mammalian host. Mol Microbiol 54: 298-306.
6. Baton, L.A., and Ranford-Cartwright, L.C. (2005) Spreading the seeds of million-murdering death: Metamorphoses of malaria in the mosquito. Trends Parasitol 21: 573-580.
7. Beier, J.C., Vaughan, J.A., Madani, A., and Noden, B.H. (1992) Plasmodium falciparum: Release of circumsporozoite protein by sporozoites in the mosquito vector. Exp Parasitol 75: 248-256.
8. Bhanot, P., Schauer, K., Coppens, I., and Nussenzweig, V. (2005) A surface phospholipase is involved in the migration of Plasmodium sporozoites through cells. J Biol Chem 280: 6752-6760.
9. 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: 503-514.
10. Blandin, S., Shiao, S.H., Moita, L.F., Janse, J.C., 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: 661-670.
11. Claudianos, C., Trueman, H.E., Dessens, J.T., Arai, M., Mendoza, J., Butcher, G.A., et al. (2002) A malaria scavenger receptor-like protein essential for parasite development. Mol Microbiol 45: 1473-1484.
12. Dessens, J.T., Siden-Kiamos, I., Mendoza, J., Mahiraki, V., Khater, E., Vlachou, D., et al. (2003) SOAP, a novel malaria ookinete protein involved in mosquito midgut invasion and oocyst development. Mol Microbiol 49: 319-329.
13. van Dijk, M.R., Douradinha, B., Franke-Fayard, B., Heussler, V., van Dooren, M.W., van Schaijk, B., et al. (2005) Genetically attenuated, P36p-deficient malarial sporozoites induce protective immunity and apoptosis of infected liver cells. Proc Natl Acad Sci USA 102: 12194-12199.
14. Engelmann, S., Sinnis, P., and Matuschewski, K. (2006) Transgenic Plasmodium berghei sporozoites expressing β-galactosidase for quantification of sporozoite transmission. Mol Biochem Parasitol 146: 30-37.
15. Franke-Fayard, B., Trueman, H., Ramesar, J., Mendoza, J., van der Keur, M., van der Linden, R., et al. (2004) A Plasmodium berghei reference line that constitutively expresses GFP at a high level throughout the complete life cycle. Mol Biochem Parasitol 137: 23-33.
16. Frevert, U. (2006) Nomadic or sessile: Can Kupffer cells function as portals for malaria sporozoites to the liver? Cell Micobiol 8, in press. doi: 10.1111/j.1462-5822.2006.00777.x.
17. Frevert, U., Engelmann, S., Zougbédé, S., Stange, J., Ng, B., Matuschewski, K., et al. (2005) Intravital observation of Plasmodium berghei sporozoite infection of the liver. PLoS Biol 3: E192.
18. Frischknecht, F., Baldacci, P., Martin, B., Zimmer, C., Thiberge, S., Olivo-Martin, J.-C., et al. (2004) Imaging movement of malaria parasites during transmission by Anopheles mosquitoes. Cell Microbiol 6: 687-694.
19. Hamilton, A.J., Davies, C.S., and Sinden, R.E. (1988) Expression of circumsporozoite proteins revealed in situ in the mosquito stages of Plasmodium berghei by Lowicryl-immunogold techniques. Parasitology 96: 273-280.
20. Hynes, R.O., and Zhao, Q. (2000) The evolution of cell adhesion. J Cell Biol 150: F89-F95.
21. Ishino, T., Yano, K., Chinzei, Y., and Yuda, M. (2004) Cell-passage activity is required for the malarial parasite to cross the liver sinusoidal cell layer. PLoS Biol 2: E4.
22. Ishino, T., Chinzei, Y., and Yuda, M. (2005a) Two proteins with 6-cys motifs are required for malarial parasites to commit to infection of the hepatocyte. Mol Microbiol 58: 1264-1275.
23. Ishino, T., Chinzei, Y., and Yuda, M. (2005b) A Plasmodium sporozoite protein with a membrane attack complex domain is required for breaching the liver sinusoidal cell layer prior to hepatocyte infection. Cell Microbiol 7: 199-208.
24. Kaiser, K., Camargo, N., and Kappe, S.H.I. (2003) Transformation of sporozoites into early exoerythrocytic malaria parasites does not require host cells. J Exp Med 197: 1045-1050.
25. Kappe, S., Bruderer, T., Gantt, S., Fujioka, H., Nussenzweig, V., and Ménard, R. (1999) Conservation of a gliding motility and cell invasion machinery in Apicomplexan parasites. J Cell Biol 147: 937-944.
26. Kappe, S.H., Buscaglia, C.A., and Nussenzweig, V. (2004a) Plasmodium sporozoite molecular cell biology. Annu Rev Cell Dev Biol 20: 29-59.
27. Kappe, S.H., Buscaglia, C.A., Bergman, L.W., Coppens, I., and Nussenzweig, V. (2004b) Apicomplexan gliding motility and host cell invasion: Overhauling the motor model. Trends Parasitol 20: 13-16.
28. Kappe, S.H.I., Noe, A.R., Fraser, T.S., Blair, P.L., and Adams, J.H. (1998) A family of chimeric erythrocyte binding proteins of malaria parasites. Proc Natl Acad Sci USA 95: 1230-1235.
29. Kariu, T., Yuda, M., Yano, K., and Chinzei, Y. (2002) MAEBL is essential for malaria sporozoite infection of the mosquito salivary gland. J Exp Med 195: 1317-1323.
30. Khater, E.I., Sinden, R.E., and Dessens, J.T. (2004) A malaria membrane skeletal protein is essential for normal morphogenesis, motility, and infectivity of sporozoites. J Cell Biol 167: 425-432.
31. Kooij, T.W.A., Carlton, J.M., Bidwell, S.L., Hall, N., Ramesar, J., Janse, C.J., and Waters, A.P. (2005) A Plasmodium whole-genome synteny map: Indels and synteny breakpoints as foci for species-specific genes. PloS Pathogens 1: E44.
32. Korochkina, S., Barreau, C., Pradel, G., Jeffrey, E., Li, J., Natarajan, R., et al. (2006) A mosquito-specific protein family includes candidate receptors for malaria sporozoite invasion of salivary glands. Cell Microbiol 8: 163-175.
33. Lehane, M.J., Aksoy, S., and Levashina, E. (2004) Immune responses and parasite transmission in blood-feeding insects. Trends Parasitol 20: 433-439.
34. Mahairaki, V., Vojatzi, T., Siden-Kiamos, I., and Louis, C. (2005) The Anopheles gambiae gamma1 laminin directly binds the Plasmodium berghei circumsporozoite- and TRAP-related protein (CTRP). Mol Biochem Parasitol 140: 119-121.
35. Mann, T., and Beckers, C. (2001) Characterization of the subpellicular network, a filamentous membrane skeletal component in the parasite Toxoplasma gondii. Mol Biochem Parasitol 115: 257-268.
36. Mann, T., Gaskins, E., and Beckers, C. (2002) Proteolytic processing of TgIMC1 during maturation of the membrane skeleton of Toxoplasma gondii. J Biol Chem 277: 41240-41246.
37. Matuschewski, K., Nunes, A.C., Nussenzwig, V., and Ménard, R. (2002a) Plasmodium sporozoite invasion into insect and mammalian cells is directed by the same dual binding system. EMBO J 21: 1597-1606.
38. Matuschewski, K., Ross, J., Brown, S.M., Kaiser, K., Nussenzweig, V., and Kappe, S.H.I. (2002b) Infectivity-associated changes in the transcriptional repertoire of the malaria parasite sporozoite stage. J Biol Chem 277: 41948-41953.
39. Ménard, R., Sultan, A.A., Cortes, C., Altszuler, R., van Dijk, M.R., Janse, C.J., et al. (1997) Circumsporozoite protein is required for development of malaria sporozoites in mosquitoes. Nature 385: 336-340.
40. Miller, S.K., Good, R.T., Drew, D.R., Delorenzi, M., Sanders, P.R., Hodder, A.N., et al. (2002) A subset of Plasmodium falciparum SERA genes are expressed and appear to play an important role in the erythrocytic cycle. J Biol Chem 277: 47524-47532.
41. Mota, M.M., Pradel, G., Vanderberg, J.P., Hafalla, J.C.R., Frevert, U., Nussenzweig, R.S., et al. (2001) Migration of Plasmodium sporozoites through cells before infection. Science 291: 141-144.
42. Mueller, A.K., Labaied, M., Kappe, S.H.I., and Matuschewski, K. (2005a) Genetically modified Plasmodium parasites as a protective experimental malaria vaccine. Nature 433: 164-167.
43. Mueller, A.K., Camargo, N., Kaiser, K., Andorfer, C., Frevert, U., Matuschewski, K., and Kappe, S.H.I. (2005b) Plasmodium liver stage developmental arrest by depletion of a protein at the parasite-host interface. Proc Natl Acad Sci USA 102: 3022-3027.
44. Myung, J.M., Marshall, P., and Sinnis, P. (2004) The Plasmodium circumsporozoite protein is involved in salivary gland invasion by sporozoites. Mol Biochem Parasitol 133: 53-59.
45. Natarajan, R., Thathy, V., Mota, M.M., Hafala, J.C., Ménard, R., and Vernick, K.D. (2001) Fluorescent Plasmodium berghei sporozoites and pre-erythrocytic stages: A new tool to study mosquito and mammalian host interactions with malaria parasites. Cell Microbiol 3: 371-379.
46. Osta, M., Christophides, G.K., and Kafatos, F.C. (2004) Effects of mosquito genes on Plasmodium development. Science 303: 2030-2032.
47. Pimenta, P.F., Touray, M., and Miller, L.H. (1994) The journey of malaria sporozoites in the mosquito salivary gland. J Euk Microbiol 41: 608-624.
48. Posthuma, G., Meis, J.F., Verhave, J.P., Hollingdale, M.R., Ponnudurai, T., Meuwissen, J.H., and Geuze, H.J. (1988) Immunogold localization of circumsporozoite protein of the malaria parasite Plasmodium falciparum during sporogony in Anopheles stephensi midguts. Eur J Cell Biol 46: 18-24.
49. Preiser, P., Renia, L., Singh, N., Balu, B., Jarra, W., Voza, T., et al. (2004) Antibodies against MAEBL ligand domains M1 and M2 inhibit sporozoite development in vitro. Infect Immun 72: 3604-3608.
50. Riehle, M.M., Markianos, K., Niaré, O., Xu, J., Li, J., Touré, A.M., et al. (2006) Natural malaria infection in Anopheles gambiae is regulated by a single genomic control region. Science 312: 577-579.
51. Rosenthal, P.J. (2004) Cysteine proteases of malaria parasites. Int J Parasitol 34: 1489-1499.
52. Schüler, H., and Matuschewski, K. (2006) Plasmodium motility: Actin not actin′ like actin. Trends Parasitol 22: 146-147.
53. Sibley, L.D. (2004) Intracellular parasite invasion strategies. Science 304: 248-253.
54. Siden-Kiamos, I., and Louis, C. (2004) Interactions between malaria parasites and their mosquito hosts in the midgut. Insect Biochem Mol Biol 34: 679-685.
55. Sidjanski, S.P., Vanderberg, J.P., and Sinnis, P. (1997) Anopheles stephensi salivary glands bear receptors for region I of the circumsporozoite protein of Plasmodium falciparum. Mol Biochem Parasitol 90: 33-41.
56. Sinden, R.E. (1974) Excystment by sporozoites of malaria parasites. Nature 252: 314.
57. Sinden, R.E., and Matuschewski, K. (2005) The sporozoite. In Molecular Approaches to Malaria. Sherman, I. (ed.). Washington DC: American Society for Microbiology Press, pp. 169-190.
58. Singh, N., Preiser, P., Renia, L., Balu, B., Barnwell, J., Blair, P., et al. (2004) Conservation and developmental control of alternative splicing in MAEBL among malaria parasites. J Mol Biol 343: 589-599.
59. Srinivasan, P., Abraham, E.G., Ghosh, A.K., Valenzuela, J., Ribeiro, J.M.C., Dimopoulos, G., et al. (2004) Analysis of the Plasmodium and Anopheles transcriptomes during oocyst differentiation. J Biol Chem 279: 5581-5587.
60. Sultan, A.A., Thathy, V., Frevert, U., Robson, K.J., Crisanti, A., Nussenzweig, V, et al. (1997) TRAP is necessary for gliding motility and infectivity of Plasmodium sporozoites. Cell 90: 511-522.
61. Terzakis, J.A., Sprinz, H., and Ward, R.A. (1967) The transformation of the Plasmodium gallinaceum oocyst in Aedes aegyptii mosquitoes. J Cell Biol 34: 311-326.
62. Tewari, R., Rathore, D., and Crisanti, A. (2005) Motility and infectivity of Plasmodium berghei sporozoites expressing avian Plasmodium gallinaceum circumsporozoite protein. Cell Microbiol 7: 699-707.
63. Thathy, V., Fujioka, H., Gantt, S., Nussenzweig, R., Nussenzweig, V., and Ménard, R. (2002) Levels of circumsporozoite protein in the Plasmodium oocyst determine sporozoite morphology. EMBO J 21: 1586-1596.
64. Touray, M.G., Warburg, A., Laughinghouse, A., Krettli, A., and Miller, L.H. (1992) Developmentally regulated infectivity of malaria sporozoites for mosquito salivary glands and the vertebrate host. J Exp Med 175: 1607-1612.
65. Triglia, T., and Cowman, A.F. (1999) Plasmodium falciparum: A homologue of p-aminobenzoic acid synthetase. Exp Parasitol 92: 154-158.
66. Vanderberg, J.P. (1974) Studies on the motility of Plasmodium sporozoites. J Protozool 21: 527-537.
67. Vanderberg, J.P. (1975) Development of infectivity by the Plasmodium berghei sporozoite. J Parasitol 61: 43-50.
68. Vanderberg, J.P., and Frevert, U. (2004) Intravital microscopy demonstrating antibody-mediated immobilisation of Plasmodium berghei sporozoites injected into skin by mosquitoes. Int J Parasitol 34: 991-996.
69. Vlachou, D., Lycett, G., Siden-Kiamos, I., Blass, C., Sinden, R.E., and Louis, C. (2001) Anopheles gambiae laminin interacts with the P25 surface protein of Plasmodium berghei ookinetes. Mol Biochem Parasitol 112: 229-237.
70. Vontas, J., Siden-Kiamos, I., Papagiannakis, G., Karras, M., Waters, A.P., and Louis, C. (2005) Gene expression in Plasmodium berghei ookinetes and early oocysts in a co-culture system with mosquito cells. Mol Biochem Parasitol 139: 1-13.
71. Wang, Q., Fujioka, H., and Nussenzweig, V. (2005a) Mutational analysis of the GPI-anchor addition sequence from the circumsporozoite protein of Plasmodium. Cell Microbiol 7: 1616-1626.
72. Wang, Q., Fujioka, H., and Nussenzweig, V. (2005b) Exit of Plasmodium sporozoites from oocysts is an active process that involves the circumsporozoite protein. PloS Pathogens 1: E9.
73. Warburg, A., and Miller, L.H. (1992) Sporogonic development of a malaria parasite in vitro. Science 255: 448-450.
74. Warburg, A., and Schneider, I. (1993) Sporogonic development of Plasmodium falciparum in vitro. Exp Parasitol 76: 121-126.
75. Wengelnik, K., Spaccapelo, R., Naitza, S., Robson, K.J.H., Janse, C.J., Bistoni, F., et al. (1999) The A-domain and the thrombospondin-related motif of Plasmodium falciparum TRAP are implicated in the invasion process of mosquito salivary glands. EMBO J 18: 5195-5204.
76. Whitten, M.M.A., Shiao, S.H., and Levashina, E.A. (2006) Mosquito midguts and malaria: Cell biology, compartimentalization and immunology. Parasite Immunol 28: 121-130.
77. Yuda, M., and Ishino, T. (2004) Liver invasion by malarial parasites - how do malarial parasites break through the host barrier? Cell Microbiol 6: 1119-1125.
78. Zhang, Y., Merali, S., and Meshnick, S.R. (1992) p-Aminobenzoic acid transport by normal and Plasmodium falciparum-infected erythrocytes. Mol Biochem Parasitol 52: 185-194.