A long and winding road: The Plasmodium sporozoite's journey in the mammalian host

Parasitology International

Volumn 56, Issue 3, 2007, Pages 171-178

  Sinnis, Photini ^a   Coppi, Alida ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN;

DERMIS; HOST; INFECTION; LIVER; LIVER CELL; NONHUMAN; PARASITE MIGRATION; PLASMODIUM; PRIORITY JOURNAL; REVIEW; SKIN; SPERMATOZOON MOTILITY; SPOROZOITE;

ANIMALS; HEPATOCYTES; HOST-PARASITE RELATIONS; HUMANS; PLASMODIUM; PROTOZOAN PROTEINS; SKIN; SPOROZOITES;

MAMMALIA;

EID: 34250777898     PISSN: 13835769     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.parint.2007.04.002     Document Type: Review

References (87)

1. Gardner M.J., Hall N., Fung E., White O., Berriman M., Hyman R.W., et al. Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 419 (2002) 498-511
2. Carlton J.M., Angiuoli S.V., Suh B.B., Kooij T.W., Pertea M., Silva J.C., et al. Genome sequence and comparative analysis of the model rodent malaria parasite Plasmodium yoelii yoelii. Nature 419 (2002) 512-519
3. van Dijk M.R., Waters A.P., and Janse C.J. Stable transfection of malaria parasite blood stages. Science 268 (1995) 1358-1362
4. Wu Y., Kirkman L.A., and Wellems T.E. Transformation of Plasmodium falciparum malaria parasites by homologous integration of plasmids that confer resistance to pyrimethamine. Proc Natl Acad Sci U S A 93 (1996) 1130-1134
5. Carvalho T.G., Thiberge S., Sakamoto H., and Menard R. Conditional mutagenesis using site-specific recombination in Plasmodium berghei. Proc Natl Acad Sci U S A 101 (2004) 14931-14936
6. Amino R., Menard R., and Frischknecht F. In vivo imaging of malaria parasites - recent advances and future directions. Curr Opin Microbiol 8 (2005) 407-414
7. King C.A. Cell motility of sporozoan protozoa. Parasitol Today 4 (1988) 315-319
8. Russell D.G., and Sinden R.E. The role of the cytoskeleton in the motility of coccidian sporozoites. J Cell Sci 50 (1981) 345-359
9. Kappe S.H., Buscaglia C.A., Bergman L.W., Coppens I., and Nussenzweig V. Apicomplexan gliding motility and host cell invasion: overhauling the motor model. Trends Parasitol 20 (2004) 13-16
10. Keeley A., and Soldati D. The glideosome: a molecular machine powering motility and host-cell invasion by Apicomplexa. Trends Cell Biol 14 (2004) 528-532
11. Matsuoka H., Yoshida S., Hirai M., and Ishii A. A rodent malaria, Plasmodium berghei, is experimentally transmitted to mice by merely probing of infective mosquito, Anopheles stephensi. Parasitol Int 51 (2002) 17-23
12. Sidjanski S., and Vanderberg J.P. Delayed migration of Plasmodium sporozoites from the mosquito bite site to the blood. Am J Trop Med Hyg 57 (1997) 426-429
13. Beier J., Davis J., Vaughan J., Noden B., and Beier M. Quantitation of Plasmodium falciparum sporozoites transmitted in vitro by experimentally infected Anopheles gambiae and Anopheles stephensi. Am J Trop Med Hyg 44 (1991) 564-570
14. Rosenberg R., Wirtz R.A., Schneider I., and Burge R. An estimation of the number of malaria sporozoites ejected by a feeding mosquito. Trans R Soc Trop Med Hyg 84 (1990) 209-212
15. Ponnudurai T., Lensen A.H.W., van Gemert G.J.A., Bolmer M.G., and Meuwissen J.H.E.T. Feeding behavior and sporozoite ejection by infected Anopheles stephensi. Trans R Soc Trop Med Hyg 85 (1991) 175-180
16. Medica D.L., and Sinnis P. Quantitative dynamics of Plasmodium yoelii sporozoite transmission by infected Anopheline mosquitoes feeding on vertebrate hosts. Infect Immun 73 (2005) 4363-4369
17. Amino R., Thiberge S., Martin B., Celli S., Shorte S., Frischknecht F., et al. Quantitative imaging of Plasmodium transmission from mosquito to mammal. Nat Med 12 (2006) 220-224
18. Vanderberg J., and Frevert U. Intravital microscopy demonstrating antibody-mediated immobilisation of Plasmodium berghei sporozoites injected into skin by mosquitoes. Int J Parasitol 34 (2004) 991-996
19. Vanderberg J.P. Studies on the motility of Plasmodium sporozoites. J Protozool 21 (1974) 527-537
20. Yamauchi L.M., Coppi A., Snounou G., and Sinnis P. Plasmodium sporozoites trickle out of the injection site. Cell Micro 9 (2007) 1215-1222
21. Mota M., Pradel G., Vanderberg J.P., Hafalla J.C.R., Frevert U., Nussenzweig R.S., et al. Migration of Plasmodium sporozoites through cells before infection. Science 291 (2001) 141-144
22. Han Y.S., Thompson J., Kafatos F.C., and Barillas-Mury C. Molecular interactions between Anopheles stephensi midgut cells and Plasmodium berghei: the time bomb theory of ookinete invasion of mosquitoes. EMBO J 19 (2000) 6030-6040
23. Danforth H.D., Entzeroth R., and Chobotar B. Scanning and transmission electron microscopy of host cell pathology associated with penetration by Eimeria papillata sporozoites. Parasitol Res 78 (1992) 570-573
24. Speer C.A., Dubey J.P., Blixt J.A., and Prokop K. Time lapse video microscopy and ultrastructure of penetrating sporozoites, types 1 and 2 parasitophorous vacuoles, and the transformation of sporozoites to tachyzoites of the VEG strain of Toxoplasma gondii. J Parasitol 83 (1997) 565-574
25. Ishino T., Chinzei Y., and Yuda M. 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 (2005) 199-208
26. Kaiser K., Camargo N., Coppens I., Morrisey J.M., Vaidya A.B., and Kappe S.H. A member of a conserved Plasmodium protein family with membrane-attack complex/perforin (MACPF)-like domains localizes to the micronemes of sporozoites. Mol Biochem Parasitol 133 (2004) 15-26
27. Ishino T., Yano K., Chinzei Y., and Yuda M. Cell-passage activity is required for the malarial parasite to cross the liver sinusoidal cell layer. PLoS Biol 2 (2004) 77-84
28. Kariu T., Ishino T., Yano K., Chinzei Y., and Yuda M. CelTOS, a novel malarial protein that mediates transmission to mosquito and vertebrate hosts. Mol Microbiol 59 (2006) 1369-1379
29. Matuschewski K., Ross J., Brown S.M., Kaiser K., Nussenzweig V., and Kappe S.H. Infectivity-associated changes in the transcriptional repertoire of the malaria parasite sporozoite stage. J Biol Chem 277 (2002) 41948-41953
30. Bhanot P., Schauer K., Coppens I., and Nussenzweig V. A surface phospholipase is involved in the migration of Plasmodium sporozoites through cells. J Biol Chem 280 (2005) 6752-6760
31. Sinnis P., and Nardin E. Sporozoite antigens: biology and immunology of the circumsporozoite protein and thrombospondin related anonymous protein. In: Perlmann P., and Troye-Blomberg M. (Eds). Malaria immunology (2002), S. Karger Press, Basel, Switzerland 70-96
32. Mota M.M., Hafalla J.C.R., and Rodriguez A. Migration through host cells activates Plasmodium sporozoites for infection. Nat Med 8 (2002) 1318-1322
33. Frevert U., Engelmann S., Zougbede S., Stange J., Ng B., Matuschewski K., et al. Intravital observation of Plasmodium berghei sporozoite infection of the liver. PLoS Biol 3 (2005) e192
34. Carrolo M., Giordano S., Cabrita-Santos L., Corso S., Vigario A., Silva S., et al. Hepatocyte growth factor and its receptor are required for malaria infection. Nat Med 9 (2003) 1363-1369
35. Cerami C., Frevert U., Sinnis P., Takacs B., Clavijo P., Santos M.J., et al. The basolateral domain of the hepatocyte plasma membrane bears receptors for the circumsporozoite protein of Plasmodium falciparum sporozoites. Cell 70 (1992) 1021-1035
36. Cerami C., Frevert U., Sinnis P., Takacs B., and Nussenzweig V. Rapid clearance of malaria circumsporozoite protein (CS) by hepatocytes. J Exp Med 179 (1994) 695-701
37. Frevert U., Sinnis P., Cerami C., Shreffler W., Takacs B., and Nussenzweig V. Malaria circumsporozoite protein binds to heparan sulfate proteoglycans associated with the surface membrane of hepatocytes. J Exp Med 177 (1993) 1287-1298
38. Pinzon-Ortiz C., Friedman J., Esko J., and Sinnis P. The binding of the circumsporozoite protein to cell surface heparan sulfate proteoglycans is required for Plasmodium sporozoite attachment to cells. J Biol Chem 276 (2001) 26784-26791
39. Pradel G., Garapaty S., and Frevert U. Proteoglycans mediate malaria sporozoite targeting to the liver. Mol Micro 45 (2002) 637-651
40. Sinnis P., Willnow T.E., Briones M.R.S., Herz J., and Nussenzweig V. Remnant lipoproteins inhibit malaria sporozoite invasion of hepatocytes. J Exp Med 184 (1996) 945-954
41. Sinnis P., Clavijo P., Fenyo D., Chait B., Cerami C., and Nussenzweig V. Structural and functional properties of region II-plus of the malaria circumsporozoite protein. J Exp Med 180 (1994) 297-306
42. Rathore D., Sacci J.B., de la Vega P., and McCutchan TF. Binding and invasion of liver cells by Plasmodium falciparum sporozoites. J Biol Chem 277 (2002) 7092-7098
43. Lyon M., Deakin J.A., and Gallagher J.T. Liver heparan sulfate structure. J Biol Chem 269 (1994) 11208-11215
44. Gressner A.M., and Schafer S. Comparison of sulfated glycosaminoglycan and hyaluronate synthesis and secretion in cultured hepatocytes, fat storing cells and Kupffer cells. J Clin Chem Clin Biochem 27 (1989) 141-149
45. Wake K. Perisinusoidal stellate cells, their related structure in and around the liver sinusoids and vitamin A-storing cells in extrahepatic organs. Int Rev Cytol 66 (1980) 303-353
46. Vanderberg J.P. Clearance of malaria sporozoites. Parasitol Today 11 (1995) 24
47. Meis J.F.G.M., Verhave J.P., Jap P.H.K., and Neuwissen J.H.E.T. An ultrastructural study on the role of Kupffer cells in the process of infection by Plasmodium berghei sporozoites in rats. Parasitology 86 (1983) 231-242
48. Pradel G., and Frevert U. Malaria sporozoites actively enter and pass through rat Kupffer cells prior to hepatocytes invasion. Hepatology 33 (2001) 1154-1165
49. Baer K., Roosevelt M., Clarkson A.B., van Rooijen N., Schnieder T., and Frevert U. Kupffer cells are obligatory for Plasmodium yoelii sporozoite infection of the liver. Cell Micro 9 (2007) 397-412
50. Dobrowolski J.M., and Sibley L.D. Toxoplasma invasion of mammalian cells is powered by the actin cytoskeleton of the parasite. Cell 84 (1996) 933-939
51. Kappe S., Bruderer T., Gantt S., Fujioka H., Nussenzweig V., and Menard R. Conservation of a gliding motility and cell invasion machinery in Apicomplexan parasites. J Cell Biol 147 (1999) 937-943
52. Sultan A.A., Thathy V., Frevert U., Robson K.J.H., Crisanti A., Nussenzweig V., et al. TRAP is necessary for gliding motility and infectivity of Plasmodium sporozoites. Cell 90 (1997) 511-522
53. Carruthers V.B., and Sibley L.D. Sequential protein secretion from three distinct organelles of Toxoplasma gondii accompanies invasion of human fibroblasts. Eur J Cell Biol 73 (1997) 114-123
54. Carruthers V.B., and Sibley L.D. Mobilization of intracellular calcium stimulates microneme discharge in Toxoplasma gondii. Mol Micro 31 (1999) 421-428
55. Carruthers V.B. Armed and dangerous: Toxoplasma gondii uses an arsenal of secretory proteins to infect host cells. Parasitol Int 48 (1999) 1-10
56. Soldati D., Dubremetz J.F., and Lebrun M. Microneme proteins: structural and functional requirements to promote adhesion and invasion by the apicomplexan parasite Toxoplasma gondii. Int J Parasitol 31 (2001) 1293-1302
57. Gantt S., Persson C., Rose K., Birkett A.J., Abagyan R., and Nussenzweig V. Antibodies against thrombospondin-related anonymous protein do not inhibit Plasmodium sporozoite infectivity in vivo. Infect Immun 68 (2000) 3667-3673
58. Binder E.M., and Kim K. Location, location, location: trafficking and function of secreted proteases of Toxoplasma and Plasmodium. Traffic 5 (2004) 914-924
59. Dowse T., and Soldati D. Host cell invasion by the Apicomplexans: the significance of microneme protein proteolysis. Curr Opin Microbiol 7 (2004) 388-396
60. Carruthers V.B., and Blackman M.J. A new release on life: emerging concepts in proteolysis and parasite invasion. Mol Microbiol 55 (2005) 1617-1630
61. Bannister L.H., and Dluzewski A.R. The ultrastructure of red cell invasion in malaria interactions: a review. Blood Cells 16 (1990) 257-292
62. Sinnis P., and Sim B.K.L. Cell invasion by the vertebrate stages of Plasmodium. Trends Microbiol 5 (1997) 52-58
63. Coppi A., Pinzon-Ortiz C., Hutter C., and Sinnis P. Proteolytic processing of the Plasmodium circumsporozoite protein is required for cell invasion. J Exp Med 201 (2005) 27-33
64. Robson K.J.H., Hall J.R.S., Jennings M.W., Harris T.J.R., Marsh K., Newbold C.I., et al. A highly conserved amino-acid sequence in thrombospondin, properdin and in proteins from sporozoites and blood stages of a human malaria parasite. Nature 335 (1988) 79-82
65. Peterson M.G., Marshall V.M., Smythe J.A., Crewther P.E., Lew A., Silva A., et al. Integral membrane protein located in the apical complex of Plasmodium falciparum. Mol Cell Biol 9 (1989) 3151-3154
66. Menard R. The journey of the malaria sporozoite through its hosts: two parasite proteins lead the way. Microb Infect 2 (2000) 633-642
67. Wengelnik K., Spaccapelo R., Naitza S., Robson K.J.H., Janse C.J., Bistoni F., et al. 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 (1999) 5195-5204
68. Matuschewski K., Nunes A.C., Nussenzweig V., and Menard R. Plasmodium sporozoite invasion into insect and mammalian cells is directed by the same dual binding system. EMBO J 21 (2002) 1597-1606
69. Silvie O., Franetich J., Charrin S., Mueller M.S., Siau A., Bodescot M., et al. A role for apical membrane antigen 1 during invasion of hepatocytes by Plasmodium falciparum sporozoites. J Biol Chem 279 (2004) 9490-9496
70. Muller H.M., Reckman I., Hollingdale M.R., Bujard H., Robson K.J.H., and Crisanti A. Thrombospondin related anonymous protein (TRAP) of Plasmodium falciparum binds specifically to sulfated glycoconjugates and to HepG2 hepatoma cells suggesting a role for this molecule in sporozoite invasion of hepatocytes. EMBO J 12 (1993) 2881-2889
71. Robson K.J.H., Frevert U., Reckmann I., Cowan G., Beier J., Scragg I.G., et al. Thrombospondin-related adhesive protein (TRAP) of Plasmodium falciparum: expression during sporozoite ontogeny and binding to human hepatocytes. EMBO J 14 (1995) 3883-3894
72. McCormick C.J., Tuckwell D.S., Crisanti A., Humphries M.J., and Hollingdale M.R. Identification of heparin as a ligand for the A-domain of Plasmodium falciparum thrombospondin-related adhesion protein. Mol Biochem Parasitol 100 (1999) 111-124
73. Florens L., Washburn M.P., Raine J.D., Anthony R.M., Grainger M., Haynes J.D., et al. A proteomic view of the Plasmodium falciparum life cycle. Nature 419 (2002) 520-526
74. Howell S.A., Withers-Martinez C., Kocken C.H.M., Thomas A.W., and Blackman M.J. Proteolytic processing and primary structure of Plasmodium falciparum apical membrane antigen-1. J Biol Chem 276 (2001) 31311-31320
75. Ishino T., Chinzei Y., and Yuda M. Two proteins with 6-cys motifs are required for malarial parasites to commit to infection of the hepatocyte. Mol Micro 58 (2005) 1264-1275
76. van Dijk M.R., Douradinha B., Franke-Fayard B., Heussler V., van Dooren M.W., van Schaijk B., et al. Genetically attenuated, P36p-deficient malarial sporozoites induce protective immunity and apoptosis of infected liver cells. Proc Natl Acad Sci U S A 102 (2005) 12194-12199
77. Gruner A.C., Snounou G., Fuller K., Jarra W., Renia L., and Preiser P.R. The Py235 proteins: glimpses into the versatility of a malaria multigene family. Microb Infect 6 (2004) 864-873
78. Freeman R.R., Trejdosiewicz A.J., and Cross G.A. Protective monoclonal antibodies recognizing stage-specific merozoite antigens of a rodent malaria parasite. Nature 284 (1980) 366-368
79. Holder A.A., and Freeman R.R. Immunization against blood-stage rodent malaria using purified parasite antigens. Nature 294 (1981) 361-364
80. Preiser P.R., Khan S., Costa F.T., Jarra W., Belnoue E., Ogun S., et al. Stage-specific transcription of distinct repertoires of a multigene family during Plasmodium life cycle. Science 295 (2002) 342-345
81. Chattopadhyay R., Rathore D., Fujioka H., Kumar S., de la Vega P., Haynes D., et al. PfSPATR, a Plasmodium falciparum protein containing an altered thrombospondin type I repeat domain is expressed at several stages of the parasite life cycle and is the target of inhibitory antibodies. J Biol Chem 278 (2003) 25977-25981
82. Gruner A.C., Brahimi K., Letourneur F., Renia L., Eling W., Snounou G., et al. Expression of the erythrocyte-binding antigen 175 in sporozoites and in liver stages of Plasmodium falciparum. J Infect Dis 184 (2001) 892-897
83. Pasquetto V., Fidock D.A., Gras H., Badell E., Eling W., Ballou W.R., et al. Plasmodium falciparum sporozoite invasion is inhibited by naturally acquired or experimentally induced polyclonal antibodies to the STARP antigen. Eur J Immunol 27 (1997) 2502-2513
84. Gruner A.C., Brahimi K., Eling W., Konings R., Meis J., Aikawa M., et al. The Plasmodium falciparum knob-associated PfEMP3 antigen is also expressed at pre-erythrocytic stages and induces antibodies which inhibit sporozoite invasion. Mol Biochem Parasitol (2001) 253-261
85. Silvie O., Rubinstein E., Franetich J., Prenant M., Belnoue E., Renia L., et al. Hepatocyte CD81 is required for Plasmodium falciparum and Plasmodium yoelii sporozoite infectivity. Nat Med 9 (2003) 93-96
86. Silvie O., Franetich J.F., Boucheix C., Rubinstein E., and Mazier D. Alternative invasion pathways for Plasmodium berghei sporozoites. Int J Parasitol 37 (2007) 173-182
87. Silvie O., Greco C., Franetich J.F., Dubart-Kupperschmitt A., Hannoun L., van Gemert G.J., et al. Expression of human CD81 differently affects host cell susceptibility to malaria sporozoites depending on the Plasmodium species. Cell Microbiol 8 (2006) 1134-1146