The repeat region of the circumsporozoite protein is critical for sporozoite formation and maturation in Plasmodium

PLoS ONE

Volumn 9, Issue 12, 2014, Pages

  Ferguson, David J P ^a   Balaban, Amanda E ^b   Patzewitz, Eva Maria ^c   Wall, Richard J ^c   Hopp, Christine S ^b   Poulin, Benoit ^c   Mohmmed, Asif ^d   Malhotra, Pawan ^d   Coppi, Alida ^b,e   Sinnis, Photini ^b   Tewari, Rita ^c  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

^c UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^d INTERNATIONAL CENTRE FOR GENETIC ENGINEERING AND BIOTECHNOLOGY   (Italy)

^e REGENERON PHARMACEUTICALS INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CIRCUMSPOROZOITE PROTEIN; CIRCUMSPOROZOITE PROTEIN, PROTOZOAN; PROTOZOAL PROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; CONTROLLED STUDY; GENE MUTATION; MUTANT; NONHUMAN; OOCYST; PARASITE DEVELOPMENT; PLASMODIUM BERGHEI; POLYMERASE CHAIN REACTION; PROTEIN EXPRESSION; PROTEIN STRUCTURE; PULSED FIELD GEL ELECTROPHORESIS; SOUTHERN BLOTTING; SPOROZOITE; TANDEM REPEAT; WESTERN BLOTTING; WILD TYPE; ANIMAL; CHEMISTRY; GENE DELETION; GENETICS; GROWTH, DEVELOPMENT AND AGING; MALARIA; METABOLISM; PARASITOLOGY; ULTRASTRUCTURE;

ANIMALS; MALARIA; PLASMODIUM BERGHEI; PROTOZOAN PROTEINS; SEQUENCE DELETION; SPOROZOITES;

EID: 84914680452     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0113923     Document Type: Article

References (35)

1. WHO (2013) World Malaria Report, 2013. (Geneva: World Health Organisation).
2. Aly AS, Vaughan AM, Kappe SH (2009) Malaria parasite development in the mosquito and infection of the mammalian host. Annu Rev Microbiol 63: 195-221.
3. Luke TC, Hoffman SL (2003) Rationale and plans for developing a non-replicating, metabolically active, radiation-attenuated Plasmodium falciparum sporozoite vaccine. J Exp Biol 206: 3803-3808.
4. Nussenzweig RS, Vanderberg J, Most H, Orton C (1967) Protective immunity produced by the injection of x-irradiated sporozoites of plasmodium berghei. Nature 216: 160-162.
5. Seder RA, Chang LJ, Enama ME, Zephir KL, Sarwar UN, et al. (2013) Protection against malaria by intravenous immunization with a nonreplicating sporozoite vaccine. Science 341: 1359-1365.
6. Sinnis P, Nardin E (2002) Sporozoite antigens: biology and immunology of the circumsporozoite protein and thrombospondin-related anonymous protein. Chem Immunol 80: 70-96.
7. Agnandji ST, Lell B, Fernandes JF, Abossolo BP, Methogo BG, et al. (2012) A phase 3 trial of RTS, S/AS01 malaria vaccine in African infants. N Engl J Med 367: 2284-2295.
8. Bejon P, White MT, Olotu A, Bojang K, Lusingu JP, et al. (2013) Efficacy of RTS, S malaria vaccines: individual-participant pooled analysis of phase 2 data. Lancet Infect Dis 13: 319-327.
9. Coppi A, Pinzon-Ortiz C, Hutter C, Sinnis P (2005) The Plasmodium circumsporozoite protein is proteolytically processed during cell invasion. J Exp Med 201: 27-33.
10. Dame JB, Williams JL, McCutchan TF, Weber JL, Wirtz RA, et al. (1984) Structure of the gene encoding the immunodominant surface antigen on the sporozoite of the human malaria parasite Plasmodium falciparum. Science 225: 593-599.
11. McCutchan TF, Kissinger JC, Touray MG, Rogers MJ, Li J, et al. (1996) Comparison of circumsporozoite proteins from avian and mammalian malarias: biological and phylogenetic implications. Proc Natl Acad Sci USA 93: 11889-11894.
12. Tewari R, Spaccapelo R, Bistoni F, Holder AA, Crisanti A (2002) Function of region I and II adhesive motifs of Plasmodium falciparum circumsporozoite protein in sporozoite motility and infectivity. J Biol Chem 277: 47613-47618.
13. Menard R, Sultan AA, Cortes C, Altszuler R, van Dijk MR, et al. (1997) Circumsporozoite protein is required for development of malaria sporozoites in mosquitoes. Nature 385: 336-340.
14. Thathy V, Fujioka H, Gantt S, Nussenzweig R, Nussenzweig V, et al. (2002) Levels of circumsporozoite protein in the Plasmodium oocyst determine sporozoite morphology. EMBO J 21: 1586-1596.
15. Coppi A, Natarajan R, Pradel G, Bennett BL, James ER, et al. (2011) The malaria circumsporozoite protein has two functional domains, each with distinct roles as sporozoites journey from mosquito to mammalian host. J Exp Med 208: 341-356.
16. Tewari R, Rathore D, Crisanti A (2005) Motility and infectivity of Plasmodium berghei sporozoites expressing avian Plasmodium gallinaceum circumsporozoite protein. Cell Microbiol 7: 699-707.
17. Wang Q, Fujioka H, Nussenzweig V (2005) Mutational analysis of the GPI-anchor addition sequence from the circumsporozoite protein of Plasmodium. Cell Microbiol 7: 1616-1626.
18. Wang Q, Fujioka H, Nussenzweig V (2005) Exit of Plasmodium sporozoites from oocysts is an active process that involves the circumsporozoite protein. PLoS Pathog 1: e9.
19. Sidjanski SP, Vanderberg JP, 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.
20. Coppi A, Tewari R, Bishop JR, Bennett BL, Lawrence R, et al. (2007) Heparan sulfate proteoglycans provide a signal to Plasmodium sporozoites to stop migrating and productively invade host cells. Cell Host Microbe 2: 316-327.
21. Espinosa DA, Yadava A, Angov E, Maurizio PL, Ockenhouse CF, et al. (2013) Development of a chimeric Plasmodium berghei strain expressing the repeat region of the P. vivax circumsporozoite protein for in vivo evaluation of vaccine efficacy. Infect Immun 81: 2882-2887.
22. Aldrich C, Magini A, Emiliani C, Dottorini T, Bistoni F, et al. (2012) Roles of the amino terminal region and repeat region of the Plasmodium berghei circumsporozoite protein in parasite infectivity. PLoS One 7: e32524.
23. Persson C, Oliveira GA, Sultan AA, Bhanot P, Nussenzweig V, et al. (2002) Cutting edge: a new tool to evaluate human pre-erythrocytic malaria vaccines: rodent parasites bearing a hybrid Plasmodium falciparum circumsporozoite protein. J Immunol 169: 6681-6685.
24. Janse CJ, Franke-Fayard B, Mair GR, Ramesar J, Thiel C, et al. (2006) High efficiency transfection of Plasmodium berghei facilitates novel selection procedures. Mol Biochem Parasitol 145: 60-70.
25. Yoshida N, Nussenzweig RS, Potocnjak P, Nussenzweig V, Aikawa M (1980) Hybridoma produces protective antibodies directed against the sporozoite stage of malaria parasite. Science 207: 71-73.
26. Sinden RE, Strong K (1978) An ultrastructural study of the sporogonic development of Plasmodium falciparum in Anopheles gambiae. Trans R Soc Trop Med Hyg 72: 477-491.
27. Vanderberg J, Rhodin J (1967) Differentiation of nuclear and cytoplasmic fine structure during sporogonic development of Plasmodium berghei. J Cell Biol 32: C7-10.
28. Proto WR, Coombs GH, Mottram JC (2013) Cell death in parasitic protozoa: regulated or incidental? Nat Rev Microbiol 11: 58-66.
29. Tucker R (2004) The thrombospondin type 1 repeat superfamily. Int J Biochem Cell Biol 36: 969-974.
30. Leung-Hagestejin C, Spence AM, Stern BD, Zhou Y, Su MW, Hedgecock EM, and Culotti JG (1992) UNC-5, a transmembrane protein with immunoglobulin and throm- bospondin type I domains, guides cell and pioneer axon migrations in C. elegans. Cell 71: 289-299.
31. Klar A, Baldassare M, Jessell TM (1992) F-Spondin: a gene expressed at high levels in the floor plate encodes a secreted protein that promotes neural cell adhesion and neurite extension. Cell 69: 95-110.
32. Sinden RE, Garnham PCC (1973) A comparative study of the ultrastructure of Plasmodium sporozoites within the oocyst and salivary glands, with particular reference to the incidence of the micropore. Trans Roy Soc trop Med Hyg 67: 631-637.
33. Godson GN, Ellis J, Svec P, Schlesinger DH, Nussenzweig V (1983) Identification and chemical synthesis of a tandemly repeated immunogenic region of Plasmodium knowlesi circumsporozoite protein. Nature 305: 29-33.
34. Aly AS, Matuschewski K (2005) A malarial cysteine protease is necessary for Plasmodium sporozoite egress from oocysts. J Exp Med 202: 225-230.
35. Guttery DS, Poulin B, Ferguson DJ, Szoor B, Wickstead B, et al. (2012) A unique protein phosphatase with kelch-like domains (PPKL) in Plasmodium modulates ookinete differentiation, motility and invasion. PLoS Pathog 8: e1002948.