Functional immunoassays using an in-vitro malaria liver-stage infection model: where do we go from here?

Trends in Parasitology

Volumn 25, Issue 11, 2009, Pages 525-533

  House, Brent L ^a   Hollingdale, Michael R ^a,b   Sacci Jr , John B ^c   Richie, Thomas L ^a  

^a WALTER REED ARMY INSTITUTE OF RESEARCH   (United States)

^b Clinical Research Management Inc   (United States)

^c UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MALARIA VACCINE;

HEPATITIS; HUMAN; IMMUNOASSAY; IN VITRO STUDY; LIVER CELL; MALARIA; PLASMODIUM FALCIPARUM; REVIEW; SPOROZOITE;

HUMANS; IMMUNOASSAY; LIVER; MALARIA, FALCIPARUM; PLASMODIUM FALCIPARUM; SPOROZOITES;

ANIMALIA; PLASMODIUM FALCIPARUM;

EID: 70350004211     PISSN: 14714922     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pt.2009.08.004     Document Type: Review

References (87)

1. Epstein J.E., et al. Malaria vaccines: are we getting closer?. Curr. Opin. Mol. Ther. 9 (2007) 12-24
2. Menard R., et al. Plasmodium pre-erythrocytic stages: what's new?. Trends Parasitol. 24 (2008) 564-569
3. Vekemans J., and Ballou W.R. Plasmodium falciparum malaria vaccines in development. Expert Rev. Vacc. 7 (2008) 223-240
4. Clyde D.F. Immunization of man against falciparum and vivax malaria by use of attenuated sporozoites. Am. J. Trop. Med. Hyg. 24 (1975) 397-401
5. Rieckmann K.H., et al. Use of attenuated sporozoites in the immunization of human volunteers against falciparum malaria. Bull. World Health Organ. 57 suppl 1 (1979) 261-265
6. Abdulla S., et al. Safety and immunogenicity of RTS,S/AS02D malaria vaccine in infants. N. Engl. J. Med. 359 (2008) 2533-2544
7. Hugel F.U., et al. Release of malaria circumsporozoite protein into the host cell cytoplasm and interaction with ribosomes. Mol. Biochem. Parasitol. 81 (1996) 151-170
8. Hollingdale M.R., et al. Inhibition of entry of Plasmodium falciparum and P. vivax sporozoites into cultured cells; an in vitro assay of protective antibodies. J. Immunol. 132 (1984) 909-913
9. Kester K.E., et al. A phase I/IIa safety, immunogenicity, and efficacy bridging randomized study of a two-dose regimen of liquid and lyophilized formulations of the candidate malaria vaccine RTS,S/AS02A in malaria-naive adults. Vaccine 25 (2007) 5359-5366
10. Tarun A.S., et al. Protracted sterile protection with Plasmodium yoelii pre-erythrocytic genetically attenuated parasite malaria vaccines is independent of significant liver-stage persistence and is mediated by CD8+ T cells. J. Infect. Dis. 196 (2007) 608-616
11. Pinder M., et al. Cellular immunity induced by the recombinant Plasmodium falciparum malaria vaccine, RTS,S/AS02, in semi-immune adults in The Gambia. Clin Exp. Immunol. 135 (2004) 286-293
12. Sun P., et al. Protective immunity induced with malaria vaccine, RTS,S, is linked to Plasmodium falciparum circumsporozoite protein-specific CD4+ and CD8+ T cells producing IFN-gamma. J. Immunol. 171 (2003) 6961-6967
13. Tsuji M., and Zavala F. T cells as mediators of protective immunity against liver stages of Plasmodium. Trends Parasitol. 19 (2003) 88-93
14. Hoffman S.L., et al. Protection of humans against malaria by immunization with radiation-attenuated Plasmodium falciparum sporozoites. J. Infect. Dis. 185 (2002) 1155-1164
15. Frevert U., and Nardin E. Cellular effector mechanisms against Plasmodium liver stages. Cell. Microbiol. 10 (2008) 1956-1967
16. Vanderberg J.P., 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
17. Kappe S.H., et al. The Plasmodium sporozoite journey: a rite of passage. Trends Parasitol. 19 (2003) 135-143
18. Sinnis P., and Zavala F. The skin stage of malaria infection: biology and relevance to the malaria vaccine effort. Future Microbiol. 3 (2008) 275-278
19. Hollingdale M.R. Biology and immunology of sporozoite invasion of liver cells and exoerythrocytic development of malaria parasites. Prog. Allergy 41 (1988) 15-48
20. Mazier D., et al. Complete development of hepatic stages of Plasmodium falciparum in vitro. Science 227 (1985) 440-442
21. Mellouk S., et al. In vitro and in vivo results suggesting that anti-sporozoite antibodies do not totally block Plasmodium falciparum sporozoite infectivity. N. Engl. J. Med. 315 (1986) 648
22. Mazier D., et al. Effect of antibodies to recombinant and synthetic peptides on P. falciparum sporozoites in vitro. Science 231 (1986) 156-159
23. Mellouk S., et al. Evaluation of an in vitro assay aimed at measuring protective antibodies against sporozoites. Bull. World Health Organ. 68 Suppl (1990) 52-59
24. Vanderberg J., et al. Protective immunity induced by the injection of x-irradiated sporozoites of Plasmodium berghei. V. In vitro effects of immune serum on sporozoites. Mil. Med. 21 (1969) 527-537
25. Vanderberg J.P. Studies on the motility of Plasmodium sporozoites. J. Protozool. 21 (1974) 527-537
26. Hollingdale M.R., et al. In vitro cultivation of the exoerythrocytic stage of Plasmodium berghei from sporozoites. Science 213 (1981) 1021-1022
27. Hollingdale M.R., and Leland P. Detection of exoerythrocytic stages of Plasmodium berghei in fixed liver tissue and cultured cells by an immunoperoxidase antibody technique. Trans. R. Soc. Trop. Med. Hyg. 76 (1982) 624-626
28. Hollingdale M.R., et al. Serological reactivity of in vitro cultured exoerythrocytic stages of Plasmodium berghei in indirect immunofluorescent or immunoperoxidase antibody tests. Am. J. Trop. Med. Hyg. 32 (1983) 24-30
29. Aikawa M., et al. Ultrastructure of in vitro cultured exoerythrocytic stage of Plasmodium berghei in a hepatoma cell line. Am. J. Trop. Med. Hyg. 33 (1984) 792-799
30. Potocnjak P., et al. Monovalent fragments (Fab) of monoclonal antibodies to a sporozoite surface antigen (Pb44) protect mice against malarial infection. J. Exp. Med. 151 (1980) 1504-1513
31. Hollingdale M.R., et al. Antibodies to the protective antigen of Plasmodium berghei sporozoites prevent entry into cultured cells. J. Immunol. 128 (1982) 1929-1930
32. Stewart M.J., et al. Plasmodium berghei sporozoite invasion is blocked in vitro by sporozoite-immobilizing antibodies. Infect. Immun. 51 (1986) 859-864
33. Hollingdale M.R., et al. In vitro cultivation of the exoerythrocytic stage of Plasmodium berghei in a hepatoma cell line. Am. J. Trop. Med. Hyg. 32 (1983) 682-684
34. Hollingdale M.R., et al. In vitro culture of two populations (dividing and nondividing) of exoerythrocytic parasites of Plasmodium vivax. Am. J. Trop. Med. Hyg. 34 (1985) 216-222
35. Herrington D., et al. Successful immunization of humans with irradiated malaria sporozoites: humoral and cellular responses of the protected individuals. Am. J. Trop. Med. Hyg. 45 (1991) 539-547
36. Karnasuta C., et al. Complete development of the liver stage of Plasmodium falciparum in a human hepatoma cell line. Am. J. Trop. Med. Hyg. 53 (1995) 607-611
37. Silvie O., et al. Malaria sporozoite: migrating for a living. Trends Mol. Med. 10 (2004) 97-100 discussion 100-1001
38. Hollingdale M.R., et al. Plasmodium falciparum: elicitation by peptides and recombinant circumsporozoite proteins of circulating mouse antibodies inhibiting sporozoite invasion of hepatoma cells. Exp. Parasitol. 63 (1987) 345-351
39. Zavala F., et al. Immunoradiometric assay to measure the in vitro penetration of sporozoites of malaria parasites into hepatoma cells. J. Immunol. 134 (1985) 1202-1205
40. Gwadz R.W., et al. Preliminary studies on vaccination of rhesus monkeys with irradiated sporozoites of Plasmodium knowlesi and characterization of surface antigens of these parasites. Bull. World Health Organ. 57 suppl 1 (1979) 165-173
41. Kumar K.A., et al. Quantitative Plasmodium sporozoite neutralization assay (TSNA). J. Immunol. Meth. 292 (2004) 157-164
42. Ballou W.R., et al. Immunogenicity of synthetic peptides from circumsporozoite protein of Plasmodium falciparum. Science 228 (1985) 996-999
43. Young J.F., et al. Expression of Plasmodium falciparum circumsporozoite proteins in Escherichia coli for potential use in a human malaria vaccine. Science 228 (1985) 958-962
44. Ballou W.R., et al. Safety and efficacy of a recombinant DNA Plasmodium falciparum sporozoite vaccine. Lancet 1 (1987) 1277-1281
45. Herrington D.A., et al. Safety and immunogenicity in man of a synthetic peptide malaria vaccine against Plasmodium falciparum sporozoites. Nature 328 (1987) 257-259
46. Nudelman S., et al. Dual action of anti-sporozoite antibodies in vitro. J. Immunol. 143 (1989) 996-1000
47. Kester K.E., et al. Phase 2a trial of 0, 1, and 3 month and 0, 7, and 28 day immunization schedules of malaria vaccine RTS,S/AS02 in malaria-naive adults at the Walter Reed Army Institute of Research. Vaccine 26 (2008) 2191-2202
48. Okitsu S.L., et al. A virosomal malaria Peptide vaccine elicits a long-lasting sporozoite-inhibitory antibody response in a phase 1a clinical trial. PLoS ONE 2 (2007) e1278
49. Rickman L.S., et al. Use of adjuvant containing mycobacterial cell-wall skeleton, monophosphoryl lipid A, and squalane in malaria circumsporozoite protein vaccine. Lancet 337 (1991) 998-1001
50. Fries L.F., et al. Liposomal malaria vaccine in humans: a safe and potent adjuvant strategy. Proc. Natl. Acad. Sci. U. S. A. 89 (1992) 358-632
51. Bathurst I.C., et al. Muramyl peptide adjuvants for Plasmodium falciparum and Plasmodium vivax circumsporozoite vaccines in rodent model systems. Biotechnol. Ther 3 (1992) 15-34
52. Brown A.E., et al. Safety, immunogenicity and limited efficacy study of a recombinant Plasmodium falciparum circumsporozoite vaccine in Thai soldiers. Vaccine 12 (1994) 102-108
53. Gordon D.M., et al. Safety, immunogenicity, and efficacy of a recombinantly produced Plasmodium falciparum circumsporozoite protein-hepatitis B surface antigen subunit vaccine. J. Infect. Dis. 171 (1995) 1576-1585
54. Zavala F., et al. Rationale for development of a synthetic vaccine against Plasmodium falciparum malaria. Science 228 (1985) 1436-1440
55. Hollingdale M.R., et al. Activity of human volunteer sera to candidate Plasmodium falciparum circumsporozoite protein vaccines in the inhibition of sporozoite invasion assay of human hepatoma cells and hepatocytes. Trans. R. Soc. Trop. Med. Hyg. 84 (1990) 325-329
56. Sedegah M., et al. Protection against malaria by immunization with plasmid DNA encoding circumsporozoite protein. Proc. Natl. Acad. Sci. U. S. A. 91 (1994) 9866-9870
57. Sedegah M., et al. Improving protective immunity induced by DNA-based immunization: priming with antigen and GM-CSF-encoding plasmid DNA and boosting with antigen-expressing recombinant poxvirus. J. Immunol. 164 (2000) 5905-5912
58. Franke E.D., et al. Pan DR binding sequence provides T-cell help for induction of protective antibodies against Plasmodium yoelii sporozoites. Vaccine 17 (1999) 1201-1205
59. Daubersies P., et al. Protection against Plasmodium falciparum malaria in chimpanzees by immunization with the conserved pre-erythrocytic liver-stage antigen 3. Nat. Med. 6 (2000) 1258-1263
60. Millet P., et al. Inhibitory activity against Plasmodium vivax sporozoites induced by plasma from Saimiri monkeys immunized with circumsporozoite recombinant proteins or irradiated sporozoites. Am. J. Trop. Med. Hyg. 45 (1991) 44-48
61. Rogers W.O., et al. Characterization of the gene encoding sporozoite surface protein 2, a protective Plasmodium yoelii sporozoite antigen. Mol. Biochem. Parasitol. 53 (1992) 45-51
62. Wang R., et al. Protection against malaria by Plasmodium yoelii sporozoite surface protein 2 linear peptide induction of CD4+ T cell- and IFN-gamma-dependent elimination of infected hepatocytes. J. Immunol. 157 (1996) 4061-4067
63. Brahimi K., et al. Human antibodies against Plasmodium falciparum liver-stage antigen 3 cross-react with Plasmodium yoelii pre-erythrocytic-stage epitopes and inhibit sporozoite invasion in vitro and in vivo. Infect. Immun. 69 (2001) 3845-3852
64. Shi Y.P., et al. Immunogenicity and in vitro protective efficacy of a recombinant multistage Plasmodium falciparum candidate vaccine. Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 1615-1620
65. Joshi M.B., et al. Immunogenicity of well-characterized synthetic Plasmodium falciparum multiple antigen peptide conjugates. Infect. Immun. 69 (2001) 4884-4890
66. Caro-Aguilar I., et al. Plasmodium vivax promiscuous T-helper epitopes defined and evaluated as linear peptide chimera immunogens. Infect. Immun. 70 (2002) 3479-3492
67. Zhou Z., et al. Development, characterization and immunogenicity of a multi-stage, multi-valent Plasmodium falciparum vaccine antigen (FALVAC-1A) expressed in Escherichia coli. Hum. Vaccin. 2 (2006) 14-23
68. do Rosario V., and Hollingdale M.R. Prevalence of anti-P. falciparum sporozoite antibodies in adults in the Amapa region of Brazil. Rev. Inst. Med. Trop. Sao Paulo 29 (1987) 63-66
69. Hollingdale M.R., et al. Age-dependent occurrence of protective anti-Plasmodium falciparum sporozoite antibodies in a holoendemic area of Liberia. Trans. R. Soc. Trop. Med. Hyg. 83 (1989) 322-324
70. Hoffman S.L., et al. Immunity to malaria and naturally acquired antibodies to the circumsporozoite protein of Plasmodium falciparum. N. Engl. J. Med. 315 (1986) 601-606
71. Hoffman S.L., et al. Naturally acquired antibodies to sporozoites do not prevent malaria: vaccine development implications. Science 237 (1987) 639-642
72. Silvie O., et al. A sporozoite asparagine-rich protein controls initiation of Plasmodium liver stage development. PLoS Pathog. 4 (2008) e1000086
73. Pied S., et al. IL-6 induced by IL-1 inhibits malaria pre-erythrocytic stages but its secretion is down-regulated by the parasite. J. Immunol. 148 (1992) 197-201
74. Ferreira A., et al. Inhibition of development of exoerythrocytic forms of malaria parasites by gamma-interferon. Science 232 (1986) 881-884
75. Nussler A., et al. TNF inhibits malaria hepatic stages in vitro via synthesis of IL-6. Int. Immunol. 3 (1991) 317-321
76. Weiss W.R., et al. Genetic restriction of protective immunity to Plasmodium yoelii sporozoites. Bull. World Health Organ. 68 Suppl (1990) 104-108
77. Carraz M., et al. Isolation and antimalarial activity of new morphinan alkaloids on Plasmodium yoelii liver stage. Bioorg. Med. Chem. 16 (2008) 6186-6192
78. Lazaro J.E., et al. Antimalarial activity of crambescidin 800 and synthetic analogues against liver and blood stage of Plasmodium sp. J. Antibiot. (Tokyo) 59 (2006) 583-590
79. Luke T.C., and Hoffman S.L. Rationale and plans for developing a non-replicating, metabolically active, radiation-attenuated Plasmodium falciparum sporozoite vaccine. J. Exp. Biol. 206 (2003) 3803-3808
80. Aly A.S., et al. Targeted deletion of SAP1 abolishes the expression of infectivity factors necessary for successful malaria parasite liver infection. Mol. Microbiol. 69 (2008) 152-163
81. Frevert U. Sneaking in through the back entrance: the biology of malaria liver stages. Trends Parasitol. 20 (2004) 417-424
82. Renia L., et al. Malaria sporozoite penetration. A new approach by double staining. J. Immunol. Meth. 112 (1988) 201-205
83. Hollingdale M.R., et al. In vitro infectivity of cryopreserved Plasmodium berghei sporozoites to cultured cells. Trans. R. Soc. Trop. Med. Hyg. 79 (1985) 206-208
84. Yalaoui S., et al. Hepatocyte permissiveness to Plasmodium infection is conveyed by a short and structurally conserved region of the CD81 large extracellular domain. PLoS Pathog. 4 (2008) e1000010
85. Yalaoui S., et al. Scavenger receptor BI boosts hepatocyte permissiveness to Plasmodium infection. Cell Host Microbe 4 (2008) 283-292
86. Hoffman S.L., et al. Sporozoite vaccine induces genetically restricted T cell elimination of malaria from hepatocytes. Science 244 (1989) 1078-1081
87. Khan Z.M., et al. Early hepatic stages of Plasmodium berghei: release of circumsporozoite protein and host cellular inflammatory response. Infect. Immun. 60 (1992) 264-270