Suppression of lethal Plasmodium yoelii malaria following protective immunization requires antibody-, IL-4-, and IFN-γ-dependent responses induced by vaccination and/or challenge infection

Journal of Immunology

Volumn 180, Issue 1, 2008, Pages 444-453

  Petritus, Patricia M ^a   Burns Jr , James M ^a  

^a DREXEL UNIVERSITY COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGEN; EPITOPE; GAMMA INTERFERON; IMMUNOGLOBULIN G; INTERLEUKIN 4; MALARIA VACCINE; MEROZOITE SURFACE PROTEIN 8; PARASITE ANTIBODY; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; MEROZOITE SURFACE PROTEIN 8, PLASMODIUM; PARASITE ANTIGEN; PROTOZOAL PROTEIN; PROTOZOON ANTIBODY;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN SPECIFICITY; ARTICLE; BAGG ALBINO MOUSE; C57BL 6 MOUSE; CONTROLLED STUDY; CORRELATION ANALYSIS; CYTOKINE PRODUCTION; DRUG EFFICACY; DRUG MECHANISM; IMMUNE RESPONSE; IMMUNITY; IMMUNIZATION; LETHALITY; MALE; MOUSE; NONHUMAN; PASSIVE IMMUNIZATION; PLASMODIUM YOELII; PLASMODIUM YOELII INFECTION; PREDICTION; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROVOCATION TEST; SPECIES DIFFERENCE; VACCINATION; ANIMAL; BLOOD; C57BL MOUSE; GENETICS; IMMUNOLOGY; MALARIA; METABOLISM; MOUSE MUTANT;

ANIMALS; ANTIBODIES, PROTOZOAN; ANTIGENS, PROTOZOAN; INTERFERON TYPE II; INTERLEUKIN-4; MALARIA; MALARIA VACCINES; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, MUTANT STRAINS; PLASMODIUM YOELII; PROTOZOAN PROTEINS; TRANSFORMING GROWTH FACTOR BETA; VACCINATION;

EID: 40449140820     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.180.1.444     Document Type: Article

References (68)

1. Hay, S. I., C. A. Guerra, A. J. Tatem, A. M. Noor, and R. W. Snow. 2004. The global distribution and population at risk of malaria: past, present, and future. Lancet 4: 327-336.
2. Warrell, D. A., G. D. Turner, and N. Francis. 2002. Pathology and pathophysiology of human malaria. In Essential Malariology, 4th Ed. D. A. Warrell and H. M. Gillis, eds. Oxford University Press, New York, pp. 236-251.
3. Hviid, L. 2005. Naturally acquired immunity to Plasmodium falciparum malaria in Africa. Acta Trop. 95: 270-275.
4. Schofield, L., and I. Mueller. 2006. Clinical immunity to malaria. Curr. Mol. Med. 6: 205-221.
5. Richie, T. L., and A. Saul. 2002. Progress and challenges for malaria vaccines. Nature 415: 694-701.
6. Mahanty, S., A. Saul, and L. H. Miller. 2003. Progress in the development of recombinant and synthetic blood-stage malaria vaccines. J. Exp. Biol. 206: 3781-3788.
7. Galinsky, M. R., A. R. Dluzewski, and J. W. Barnwell. 2005. A mechanistic approach to merozoite invasion of red blood cells: merozoite biogenesis, rupture, and invasion of erythrocytes. In Molecular Approaches to Malaria, I. W. Sherman, ed. ASM Press, Washington DC, pp. 113-168.
8. Triglia, T., J. Healer, S. R. Caruana, A. N. Hodder, R. F. Anders, B. S. Crabb, and A. F. Cowman. 2000. Apical membrane antigen 1 plays a central role in erythrocyte invasion by Plasmodium species. Mol. Microbiol. 38: 706-718.
9. 19 across distantly related Plasmodium species. Nat. Med. 6: 91-95.
10. Chappel, J. A., and A. A. Holder. 1993. Monoclonal antibodies that inhibit Plasmodium falciparum invasion in vitro recognize the first growth factor-like domain of merozoite surface protein-1. Mol. Biochem. Parasitol. 60: 303-311.
11. Kumar, S., A. Yadava, D. B. Keister, J. H. Tian, M. Ohl, K. A. Perdue-Greenfield, L. H. Miller, and D. C. Kaslow. 1995. Immunogenicity and in vivo efficacy of recombinant Plasmodium falciparum merozoite surface protein-1 in Aotus monkeys. Mol. Med. 1: 325-332.
12. Chang, S. P., S. E. Case, W. L. Gosnell, A. Hashimoto, K. J. Kramer, L. Q. Tam, C. Q. Hashiro, C. M. Nikaido, H. L. Gibson, C. T. Lee-Ng, et al. 1996. A recombinant baculovirus 42-kilodalton C-terminal fragment of Plasmodium falciparum merozoite surface protein 1 protects Aotus monkeys against malaria. Infect. Immun. 64: 253-261.
13. 19 are a major component of the invasion-inhibitory response in individuals immune to malaria. J. Exp. Med. 193: 1403-1412.
14. Darko, C. A., E. Angov, W. E. Collins, E. S. Bergmann-Leitner, A. S. Girouard, S. L. Hitt, J. S. McBride, C. L. Diggs, A. A. Holder, C. A. Long, et al. 2005. The clinical grade 42 kilodalton fragment of merozoite surface protein 1 of Plasmodium falciparum strain FVO expressed in Escherichia coli protects Aotus nancymai against challenge with homologous erythrocytic stage parasites. Infect. Immun. 73: 287-297.
15. Singh, S., K. Miura, H. Zhou, O. Muratova, B. Keegan, A. Miles, L. B. Martin, A. J. Saul, L. H. Miller, and C. A. Long. 2006. Immunity to recombinant Plasmodium falciparum merozoite surface protein 1 (MSP1): protection in Aotus nancymai monkeys strongly correlates with anti-MSP1 antibody titer and in vitro parasite-inhibitory activity. Infect. Immun. 74: 4573-4580.
16. Burns, J. M., Jr., W. R. Majarian, J. F. Young, T. M. Daly, and C. A. Long. 1989. A protective monoclonal antibody recognizes an epitope in the C-terminal cysteine-rich domain in the precursor of the major merozoite surface antigen of the rodent malarial parasite Plasmodium yoelii. J. Immunol. 143: 2670-2676.
17. Daly, T. M., and C. A. Long. 1995. Humoral response to a carboxyl-terminal region of the merozoite surface protein-1 plays a predominant role in controlling blood-stage infection in rodent malaria. J. Immunol. 155: 236-243.
18. Hirunpetcharat, C., P. Vukovic, X. Q. Liu, D. C. Kaslow, L. H. Miller, and M. F. Good. 1999. Absolute requirement for an active immune response involving B cells and Th cells in immunity to Plasmodium yoelii passively acquired with antibodies to the 19-kDa carboxyl-terminal fragment of merozoite surface protein-1. J. Immunol. 162: 7309-7314.
19. Burns, J. M., Jr., P. R. Flaherty, M. M. Romero, and W. P. Weidanz. 2003. Immunization against Plasmodium chabaudi malaria using combined formulations of apical membrane antigen-1 and merozoite surface protein-1. Vaccine 21: 1843-1852.
20. Burns, J. M., Jr., P. R. Flaherty, P. Nanavati, and W. P. Weidanz. 2004. Protection against Plasmodium chabaudi malaria induced by immunization with apical membrane antigen-1 and merozoite surface protein-1 in the absence of IFN-γ or IL-4. Infect. Immun. 72: 5605-5612.
21. Crewther, P. E., M. L. Matthew, R. H. Flegg, and R. Anders. 1996. Protective immune responses to apical membrane antigen 1 of Plasmodium chabaudi involve recognition of strain-specific epitopes. Infect. Immun. 64: 3310-3317.
22. Anders, R. A., P. E. Crewther, S. Edwards, M. Margetts, M. L. Matthew, B. Pollock, and D. Pye. 1997. Immunization with recombinant AMA-1 protects mice against infection with Plasmodium chabaudi. Vaccine 16: 240-247.
23. Stowers, A. W., M. C. Kennedy, B. P. Keegan, A. Saul, C. A. Long, and L. H. Miller. 2002. Vaccination of monkeys with recombinant P. falciparum apical membrane antigen 1 confers protection against blood-stage malaria. Infect. Immun. 70: 6961-6967.
24. Collins, W. E., D. Pye, P. E. Crewther, K. L. Vandenberg, G. G. Galland, A. J. Sulzer, D. J. Kemp, S. J. Edwards, R. L. Coppel, J. S. Sullivan, et al. 1994. Protective immunity induced in squirrel monkeys with recombinant apical membrane antigen-1 of Plasmodium fragile. Am. J. Trop. Med. Hyg. 51: 711-719.
25. Grun, J. L., and W. P. Weidanz. 1981. Immunity to Plasmodium chabaudi adami in the B cell deficient mouse. Nature 290: 143-145.
26. HD mouse. J. Immunol. 152: 4557-4562.
27. Von der Weid, T., N. Honarvar, and J. Langhorne. 1996. Gene-targeted mice lacking B cells are unable to eliminate a blood stage malaria infection. J. Immunol. 156: 2510-2516.
28. Stevenson, M. M., J. J. Lyanga, and E. Skamene. 1982. Murine malaria: genetic control of resistance to Plasmodium chabaudi. Infect. Immun. 38: 80-88.
29. Hoffman, E. J., W. P. Weidanz, and C. A. Long. 1984. Susceptibility if CXB recombinant inbred mice to murine malaria. Infect. Immun. 43: 981-985.
30. Taylor, D. W., E. Pacheco, C. B. Evans, and R. Asofsky. 1988. Inbred mice infected with Plasmodium yoelii differ in their antimalarial immunoglobulin isotype response. Parasite Immunol. 10: 33-46.
31. Shear, H. L., R. Srinivasan, T. Nolan, and C. Ng. 1989. Role of IFN-γ in lethal and non-lethal malaria in susceptible and resistant murine hosts. J. Immunol. 143: 2038-2044.
32. De Souza, J. B., K. H. Williamson, T. Otani, and J. H. L. Playfair. 1997. Early γ interferon responses in lethal and nonlethal murine blood-stage malaria. Infect. Immun. 65: 1593-1598.
33. Wykes, M. N., X. Q. Liu, L. Beattie, D. I. Stanisic, K. J. Stacey, M. J. Smyth, R. Thomas, and M. F. Good. 2007. Plasmodium strain determines dendritic cell function essential for survival from malaria. PLoS Pathog. 3: e96.
34. Othoro, C., A. A. Lal, B. Nahlen, D. Koech, A. S. S. Orago, and V. Udhayakumar. 1999. A low IL-10: TNF-α ratio is associated with malaria anemia in children residing in a holoendemic malaria region in western Kenya. J. Infect. Dis. 179: 279-282.
35. Dodoo, D., F. M. Omer, J. Todd, B. D. Akanmori, K. A. Korman, and E. M. Riley. 2001. Absolute levels and ratios of proinflammatory and anti-inflammatory cytokine production in vitro predict clinical immunity to Plasmodium falciparum malaria. J. Infect. Dis. 185: 971-979.
36. Omer, F. M., J. B. De Souza, and E. M. Riley. 2003. Differential induction of TGF-β regulates proinflammatory cytokine production and determines the outcome of lethal and non-lethal Plasmodium yoelii infections. J. Immunol. 171: 5430-5436.
37. Good, M. F., H. Xu, M. Wykes, and C. R. Engwerda. 2005. Development and regulation of cell-mediated immune responses to the blood stages of malaria: implications for vaccine research. Annu. Rev. Immunol. 23: 69-99.
38. Burns, J. M., Jr., C. C. Belk, and P. D. Dunn. 2000. A protective glycosylphosphatidylinositol-anchored membrane protein of Plasmodium yoelii trophozoites and merozoites contains two epidermal growth factor-like domains. Infect. Immun. 68: 6189-6195.
39. Black, C. G., T. Wu, L. Wang, A. R. Hibbs, and R. L. Coppel. 2001. Merozoite surface protein 8 of Plasmodium falciparum contains two epidermal growth factor-like domains. Mol. Biochem. Parasitol. 114: 217-226.
40. Shi, Q., A. Cernetich, T. M. Daly, G. Galvan, A. B. Vaidya, L. W. Bergman, and J. M. Burns, Jr. 2005. Alteration in host cell tropism limits the efficacy of immunization with a surface protein of malaria merozoites. Infect. Immun. 73: 6363-6371.
41. 19) and T helper epitopes of tetanus toxoid. Vaccine 18: 531-539.
42. Ockenhouse, C. F., E. Angov, K. E. Kester, C. Diggs, L. Soisson, J. F. Cummings, A. V. Stewart, D. R. Palmer, B. Mahajan, U. Krzych, et al. 2006. Phase I safety and immunogenicity trial of FMP1/AS02A, a Plasmodium falciparum MSP-1 asexual blood stage vaccine. Vaccine 24: 3009-3017.
43. 42) vaccines for Plasmodium falciparum malaria. PLoS Clin. Trials. 2: e12.
44. Malkin, E. M., D. J. Diemert, J. H. McArthur, J. R. Perreault, A. P. Miles, B. K. Giersing, G. E. Mullen, A. Orcutt, O. Muratova, M. Awkal, et al. 2005. Phase 1 clinical trial of apical membrane antigen 1: an asexual blood-stage vaccine for Plasmodium falciparum. Infect. Immun. 73: 3677-3685.
45. Polhemus, M., A. J. Magill, J. F. Cummings, K. E. Kester, C. F. Ockenhouse, D. E. Lanar, S. Dutta, A. Barbosa, L. Soisson, C. L. Diggs, et al. 2007. Phase I does escalation safety and immunogenicity trial of Plasmodium falciparum apical membrane antigen (AMA-1) FMP2.1, adjuvanted with AS02A, in malaria-naïve adults at the Walter Reed Army Institute of Research. Vaccine 25: 4203-4212.
46. Sacks, D., and N. Noben-Trauth. 2002. The immunology of susceptibility and resistance to Leishmania major in mice. Nat. Rev. Immunol. 2: 845-858.
47. Smythies, L. E., K. B. Waites, J. R. Lindsey, P. R. Harris, P. Ghiara, and P. D. Smith. 2000. Helicobacter pylori-induced mucosal inflammation is Th1 mediated and exacerbated in IL-4, but not IFN-γ, gene-deficient mice. J. Immunol. 165: 1022-1029.
48. Pereira, V. R., V. M. Lorena, M. Nakazawa, C. F. Luna, E. D. Silva, A. G. Ferreira, M. A. Krieger, S. Goldenberg, M. B. Soares, E. M. Coutinho, et al. 2005. Humoral and cellular immune responses in BALB/c and C57BL/6 mice immunized with cytoplasmic (CRA) and flagellar (FRA) recombinant repetitive antigens, in acute experimental Trypanosoma cruzi infection. Parasitol. Res. 96: 154-161.
49. Rotman, H. L., T. M. Daly, R. Clynes, and C. A. Long. 1998. Fc receptors are not required for antibody-mediated protection against lethal malaria challenge in a mouse model. J. Immunol. 161: 1908-1912.
50. Vukovic, P., P. M. Hogarth, N. Barnes, D. C. Kaslow, and M. G. Good. 2000. Immunoglobulin G3 antibodies specific for the 19-kilodalton carboxyl-terminal fragment of Plasmodium yoelii merozoite surface protein 1 transfer protection to mice deficient in FcγRI receptors. Infect. Immun. 68: 3019-3022.
51. Bouharoun-Tayoun, H., and P. Druilhe. 1992. Plasmodium falciparum malaria: evidence for an isotype imbalance which may be responsible for delayed acquisition of protective immunity. Infect. Immun. 60: 1473-1481.
52. Groux, H., and J. Gysin. 1990. Opsonization as an effector mechanism in human protection against asexual blood stages of Plasmodium falciparum: functional role of IgG subclass. Res. Immunol. 141: 529-542.
53. Garraud, O., S. Mahanty, and R. Perraut. 2003. Malaria-specific antibodies in immune individuals: a key source of information for vaccine design. Trends Immunol. 24: 30-35.
54. McIntosh, R. S., J. Shi, R. M. Jennings, J. C. Chappel, T. F. de Koning-Ward, T. Smoth, J. Green, M. van Egmond, J. H. W. Leusen, M. Lazarou, et al. 2007. The importance of human FcγRI in mediating protection to malaria. PLoS Pathog. 3: e72.
55. White, W. I., C. B. Evans, and D. W. Taylor. 1991. Antimalarial antibodies of the immunoglobulin G2a isotype modulate parasitemias in mice infected with Plasmodium yoelii. Infect. Immun. 59: 3547-3554.
56. Hunter, R. L., M. R. Kidd, M. R. Olsen, P. S. Patterson, and A. A. Lal. 1995. Induction of long-lasting immunity to Plasmodium yoelii malaria with whole blood-stage antigens and copolymer adjuvants. J. Immunol. 154: 1762-1769.
57. Matsumoto, S., H. Yukitake, H. Kanbara, H. Yamada, A. Kitamura, and T. Yamada. 2001. Mycobacterium bovis bacillus Calmette-Guérin induces protective immunity against infection by Plasmodium yoelii at blood-stage depending on shifting immunity toward Th1 type and inducing protective IgG2a after the parasite infection. Vaccine 19: 779-787.
58. Langhorne, J., C. B. Evans, R. Asofsky, and D. W. Taylor. 1984. Immunoglobulin isotype distribution of malaria-specific antibodies produced during infection with Plasmodium chabaudi adami and Plasmodium yoelii. Cell. Immunol. 87: 452-461.
59. Su, Z., and M. M. Stevenson. 2002. IL-12 is required for antibody-mediated protective immunity against blood-stage Plasmodium chabaudi AS malaria infection in mice. J. Immunol. 168: 1348-1355.
60. Nimmerjahn, F., and J. V. Ravetch. 2005. Divergent immunoglobulin G subclass activity through selective Fc receptor binding. Science 310: 1510-1512.
61. Van der Heyde, H. C., B. Pepper, J. Batchelder, F. Cigel, and W. P. Weidanz. 1997. The time course of selected malarial infections in cytokine-deficient mice. Exp. Parasitol. 85: 206-213.
62. Su, Z., and M. M. Stevenson. 2000. Central role of endogenous γ interferon in protectivie immunity against blood-stage Plasmodium chabaudi AS infection. Infect. Immun. 68: 4399-4406.
63. Batchelder, J. M., J. M. Burns, Jr., F. K. Cigel, H. Lieberg, D. D. Manning, B. J. Pepper, D. M. Yanez, H. van der Heyde, and W. P. Weidanz. 2003. Plasmodium chabaudi: IFN-γ but not IL-2 is essential for the expression of cell-mediated immunity against blood-stage parasites in mice. Exp. Parasitol. 105: 159-166.
64. Matsumoto, S., H. Yukitake, H. Kanbara, and T. Yamada. 1998. Recombinant Mycobacterium bovis bacillus Calmette-Guérin secreting merozoite surface protein 1 (MSP1) induces protection against rodent malaria parasite infection depending on MSP-1-stimulated interferon-γ and parasite specific antibodies. J. Exp. Med. 188: 845-854.
65. Perry, J. A., A. Rush, R. J. Wilson, C. S. Olver, and A. C. Avery. 2004. Dendritic cells from malaria-infected mice are fully functional APC. J. Immunol. 172: 475-482.
66. Tsutsui, N., and T. Kamiyama. 1999. Transforming growth factor β-induced failure of resistance to infection with blood-stage Plasmodium chabaudi in mice. Infect. Immun. 67: 2306-2311.
67. + regulatory T cells correlates with more rapid parasite growth in human malaria infection. Immunity 23: 287-296.
68. Clark, I. A., and W. B. Cowden. 2003. The pathophysiology of falciparum malaria. Pharmacol. Ther. 99: 221-260.