The immunological challenge to developing a vaccine to the blood stages of malaria parasites

Immunological Reviews

Volumn 201, Issue , 2004, Pages 254-267

  Good, Michael F ^a,c   Stanisic, Danielle ^a   Xu, Huji ^a   Elliott, Salenna ^b   Wykes, Michelle ^a  

^a QIMR BERGHOFER MEDICAL RESEARCH INSTITUTE   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c ROYAL BRISBANE AND WOMEN'S HOSPITAL   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

MALARIA VACCINE; PARASITE ANTIGEN;

ANTIGENIC VARIATION; APOPTOSIS; CELL FUNCTION; CELLULAR IMMUNITY; DENDRITIC CELL; EFFECTOR CELL; HUMAN; IMMUNE RESPONSE; LIFE CYCLE; MALARIA; MEMORY CELL; MODULATION TRANSFER FUNCTION; NONHUMAN; PASSIVE IMMUNIZATION; PLASMODIUM; PRIORITY JOURNAL; REVIEW;

ANIMALS; ANTIGENS, PROTOZOAN; CHILD, PRESCHOOL; DRUG DESIGN; ERYTHROCYTES; HUMANS; INFANT; MALARIA; MALARIA VACCINES; MALARIA, FALCIPARUM; MICE; PLASMODIUM CHABAUDI; PLASMODIUM FALCIPARUM;

EID: 4844219516     PISSN: 01052896     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.0105-2896.2004.00178.x     Document Type: Review

References (138)

1. Davey S. Gaps in access to new vaccines. In: Geyer EM, ed. State of the World's Vaccines and Immunization. Geneva: World Health Organization 2002:7-8.
2. Riley EM, Wagner GE, Akanmori BD, Koram KA. Do maternally acquired antibodies protect infants from malaria infection? Parasite Immunol 2001;23:51-59.
3. Bruce-Chwatt LJ. Essential Malariology. London: William Heinemann Medical Books Ltd, 1985.
4. Stevenson MM, Riley EM. Innate immunity to malaria. Nat Rev Immunol 2004;4: 169-180.
5. Schofield L, Hewitt MC, Evans K, Siomos MA, Seeberger PH. Synthetic GPI as a candidate anti-toxic vaccine in a model of malaria. Nature 2002;418:785-789.
6. Marsh K, Howard RJ. Antigens induced on erythrocytes by P. falciparum: expression of diverse and conserved determinants. Science 1986;231:150-153.
7. Newbold CI, Pinches R, Roberts DJ, Marsh K. Plasmodium falciparum: the human agglutinating antibody response to the infected red cell surface is predominantly variant specific. Exp Parasitol 1992;75:281-292.
8. Baruch DI, et al. Cloning the P. falciparum gene encoding PfEMP1, a malarial variant antigen and adherence receptor on the surface of parasitized human erythrocytes. Cell 1995;82:77-87.
9. Su XZ, et al. The large diverse gene family var encodes proteins involved in cytoadherence and antigenic variation of Plasmodium falciparum-infected erythrocytes. Cell 1995;82:89-100.
10. Smith JD, et al. Switches in expression of Plasmodium falciparum var genes correlate with changes in antigenic and cytoadherent phenotypes of infected erythrocytes. Cell 1995;82:101-110.
11. Roberts DJ, et al. Rapid switching to multiple antigenic and adhesive phenotypes in malaria. Nature 1992;357:689-692.
12. Miller LH, Good MF, Milon G. Malaria pathogenesis. Science 1994;264:1878-1883.
13. Holder AA, et al. Merozoite surface protein 1, immune evasion, and vaccines against asexual blood stage malaria. Parasitologia 1999;41:409-114.
14. Miller LH, Roberts T, Shahabuddin M, McCutchan TF. Analysis of sequence diversity in the Plasmodium falciparum merozoite surface protein-1 (MSP-1). Mol Biochem Parasitol 1993;59:1-14.
15. Jongwutiwes S, Tanabe K, Kanbara H. Sequence conservation in the C-terminal part of the precursor to the major merozoite surface proteins (MSP1) of Plasmodium falciparum from field isolates. Mol Biochem Parasitol 1993;59:95-100.
16. Blackman MJ, Heidrich HG, Donachie S, McBride JS, Holder AA. A single fragment of a malaria merozoite surface protein remains on the parasite during red cell invasion and is the target of invasion-inhibiting antibodies. J Exp Med 1990;172:379-382.
17. Riley EM, et al. Naturally acquired cellular and humoral immune responses to the major merozoite surface antigen (PfMSP1) of Plasmodium falciparum are associated with reduced malaria morbidity. Parasite Immunol 1992;14:321-337.
18. Branch OH, et al. A longitudinal investigation of IgG and IgM antibody responses to the merozoite surface protein-1 19-kiloDalton domain of Plasmodium falciparum in pregnant women and infants: associations with febrile illness, parasitemia, and anemia. Am J Trop Med Hyg 1998;58:211-219.
19. Egan AF, Burghaus P, Druilhe P, Holder AA, Riley EM. Human antibodies to the 19kDa C-terminal fragment of Plasmodium falciparum merozoite surface protein 1 inhibit parasite growth in vitro. Parasite Immunol 1999;21:133-139.
20. Dodoo D, et al. Levels of antibody to conserved parts of Plasmodium falciparum merozoite surface protein 1 in Ghanaian children are not associated with protection from clinical malaria. Infect Immun 1999;67:2131-2137.
21. Okech BA, et al. Fine specificity of serum antibodies to Plasmodium falciparum merozoite surface protein, PfMSP-1 (19), predicts protection from malaria infection and high-density parasitemia. Infect Immun 2004;72:1557-1567.
22. O'Donnell RA, et al. Antibodies against merozoite surface protein (MSP)-1(19) are a major component of the invasion-inhibitory response in individuals immune to malaria. J Exp Med 2001;193:1403-1412.
23. Phillips RS, Trigg PI, Scott-Finnigan TJ, Bartholomew RK. Culture of Plasmodium falciparum in vitro: a subculture technique used for demonstrating antiplasmodial activity in serum from some Gambians, resident in an endemic malarious area. Parasitology 1972;65:525-535.
24. Cohen S, Mc GI, Carrington S. Gamma-globulin and acquired immunity to human malaria. Nature 1961;192:733-737.
25. Bouharoun-Tayoun H, Attanath P, Sabchareon A, Chongsuphajaisiddhi T, Druilhe P. Antibodies that protect humans against Plasmodium falciparum blood stages do not on their own inhibit parasite growth and invasion in vitro, but act in cooperation with monocytes. J Exp Med 1990;172:1633-1641.
26. Oeuvray C, Theisen M, Rogier C, Trape JF, Jepsen S, Druilhe P. Cytophilic immunoglobulin responses to Plasmodium falciparum glutamate-rich protein are correlated with protection against clinical malaria in Dielmo. Senegal Infect Immun 2000;68:2617-2620.
27. Soe S, Theisen M, Roussilhon C, Aye KS, Druilhe P. Association between protection against clinical malaria and antibodies to merozoite surface antigens in an area of hyperendemicity in Myanmar: complementarity between responses to merozoite surface protein 3 and the 220-kilodalton glutamate-rich protein. Infect Immun 2004;72:247-252.
28. Grun JL, Weidanz WP. Antibody-independent immunity to reinfection malaria in B-cell-deficient mice. Infect Immun 1983;41:1197-1204.
29. van der Heyde HC, Huszar D, Woodhouse C, Manning DD, Weidanz WP. The resolution of acute malaria in a definitive model of B cell deficiency, the JHD mouse. J Immunol 1994;152:4557-4562.
30. von der Weid T, Honarvar N, Langhorne J. Gene-targeted mice lacking B cells are unable to eliminate a blood stage malaria infection. J Immunol 1996;156:2510-2516.
31. Brake DA, Long CA, Weidanz WP. Adoptive protection against Plasmodium chabaudi adami malaria in athymic nude mice by a cloned T cell line. J Immunol 1988;140:1989-1993.
32. Taylor-Robinson AW, Phillips RS, Severn A, Moncada S, Liew FY. The role of TH1 and TH2 cells in a rodent malaria infection. Science 1993;260:1931-1934.
33. Amante FH, Good MF. Prolonged Th1-like response generated by a Plasmodium yoelii-specific T cell done allows complete clearance of infection in reconstituted mice. Parasite Immunol 1997;19:111-126.
34. Luty AJ, et al. Interferon-gamma responses are associated with resistance to reinfection with Plasmodium falciparum in young African children. J Infect Dis 1999;179:980-988.
35. Pombo DJ, et al. Immunity to malaria after administration of ultra-low doses of red cells infected with Plasmodium falciparum. Lancet 2002;360:610-617.
36. van der Heyde HC, Elloso MM, Chang WL, Kaplan M, Manning DD, Weidanz WP. Gamma delta T cells function in cell-mediated immunity to acute blood-stage Plasmodium chabaudi adami malaria. J Immunol 1995;154:3985-3990.
37. Seixas EM, Langhorne J. gammadelta T cells contribute to control of chronic parasitemia in Plasmodium chabaudi infections in mice. J Immunol 1999;162:2837-2841.
38. Su Z, Stevenson MM. Central role of endogenous gamma interferon in protective immunity against blood-stage Plasmodium chabaudi AS infection. Infect Immun 2000;68:4399-4406.
39. Favila-Castillo L, Monroy-Ostria A, Kobayashi E, Hirunpetcharat C, Kamada N, Good MF. Protection of rats against malaria by a transplanted immune spleen. Parasite Immunol 1996;18:325-331.
40. Makobongo MO, et al. The purine salvage enzyme hypoxanthine guanine xanthine phosphoribosyl transferase is a major target antigen for cell-mediated immunity to malaria. Proc Natl Acad Sci USA 2003;100:2628-2633.
41. Shahabuddin M, et al. Localisation of hypoxanthine phosphoribosyl transferase in the malaria parasite Plasmodium falciparum. Exp Parasitol 1992;74:11-19.
42. Wipasa J, Hirunpetcharat C, Mahakunkijcharoen Y, Xu H, Elliott S, Good MF. Identification of T cell epitopes on the 33-kDa fragment of Plasmodium yoelii merozoite surface protein 1 and their antibody-independent protective role in immunity to blood stage malaria. J Immunol 2002;169:944-951.
43. + T cells acting independently of antibody contribute to protective immunity to Plasmodium chabaudi infection after apical membrane antigen 1 immunization. J Immunol 2000;165:389-396.
44. Chandramohan D, Greenwood BM. Is there an interaction between human immunodeficiency virus and Plasmodium falciparum? Int J Epidemiol 1998;27:296-301.
45. Whitworth J, et al. Effect of HIV-1 and increasing immunosuppression on malaria parasitaemia and clinical episodes in adults in rural Uganda: a cohort study. Lancet 2000;356:1051-1056.
46. Verhoef H, Veenemans J, West CE. HIV-1 infection and malaria parasitaemia. Lancet 2001;357:232-233.
47. French N, Nakiyingi J, Lugada E, Watera C, Whitworth JA, Gilks CF. Increasing rates of malarial fever with deteriorating immune status in HIV-1-infected Ugandan adults. Aids 2001;15:899-906.
48. Grimwade K, French N, Mbatha DD, Zungu DD, Dedicoat M, Gilks CF. Childhood malaria in a region of unstable transmission and high human immunodeficiency virus prevalence. Pediatr Infect Dis J 2003;22:1057-1063.
49. Beeson JG, Brown GV. Plasmodium falciparum-infected erythrocytes demonstrate dual specificity for adhesion to hyaluronic acid and chondroitin sulfate A and have distinct adhesive properties. J Infect Dis 2004;189:169-179.
50. Fried M, Duffy PE. Adherence of Plasmodium falciparum to chondroitin sulfate A in the human placenta. Science 1996;272:1502-1504.
51. Beeson JG, et al. Adhesion of Plasmodium falciparum-infected erythrocytes to hyaluronic acid in placental malaria. Nat Med 2000;6:86-90.
52. Fried M, Nosten F, Brockman A, Brabin BJ, Duffy PE. Maternal antibodies block malaria. Nature 1998;395:851-852.
53. Steketee RW, et al. Impairment of a pregnant woman's acquired ability to limit Plasmodium falciparum by infection with human immunodeficiency virus type-1. Am J Trop Med Hyg 1996;55:42-49.
54. Kemp DJ, Coppel RL, Cowman AF, Saint RB, Brown GV, Anders RF. Expression of Plasmodium falciparum blood-stage antigens in Escherichia coli: detection with antibodies from immune humans. Proc Natl Acad Sci USA 1983;80:3787-3791.
55. Ellis J, et al. Cloning and expression in E. coli of the malarial sporozoite surface antigen gene from Plasmodium knowlesi. Nature 1983;302:536-538.
56. Ballou WR, et al. Safety and efficacy of a recombinant DNA Plasmodium falciparum sporozoite vaccine. Lancet 1987;1:1277-1281.
57. Herrington DA, et al. Safety and immunogenicity in man of a synthetic peptide malaria vaccine against Plasmodium falciparum sporozoites. Nature 1987;328:257-259.
58. Genton B, et al. A recombinant blood-stage malaria vaccine reduces Plasmodium falciparum density and exerts selective pressure on parasite populations in a phase 1-2b trial in Papua New Guinea. J Infect Dis 2002;185:820-827.
59. Moreno A, Patarroyo ME. Malaria vaccines. Curr Opin Immunol 1995;7:607-611.
60. Nosten F, et al. Randomised double-blind placebo-controlled trial of SPf66 malaria vaccine in children in northwestern Thailand. Shoklo Spf66 Malaria Vaccine Trial Group. Lancet 1996;348:701-707.
61. Bojang KA, et al. Follow-up of Gambian children recruited to a pilot safety and immunogenicity study of the malaria vaccine SPf66. Parasite Immunol 1997;19:579-581.
62. Chauhan VS, Bhardwaj D. Current status of malaria vaccine development. Adv Biochem Eng Biotechnol 2003;84:143-182.
63. Reeder JC. Towards a malaria vaccine for Papua New Guinea. P N G Med J 2001;44:17-23.
64. Wipasa J, Elliott S, Xu H, Good MF. Immunity to asexual blood stage malaria and vaccine approaches. Immunol Cell Biol 2002;80:401-414.
65. Moorthy V, Hill AV. Malaria vaccines. Br Med Bull 2002;62:59-72.
66. Greenwood B, Alonso P. Malaria vaccine trials. Chem Immunol 2002;80:366-395.
67. Schofield L. Antidisease vaccines. Chem Immunol 2002;80:322-342.
68. Good MF. Towards a blood-stage vaccine for malaria: are we following all the leads? Nat Rev Immunol 2001;1:117-125.
69. Richie TL, Saul A. Progress and challenges for malaria vaccines. Nature 2002;415:694-701.
70. Urban BC, et al. Plasmodium falciparum-infected erythrocytes modulate the maturation of dendritic cells. Nature 1999;400:73-77.
71. Urban BC, Willcox N, Roberts DJ. A role for CD36 in the regulation of dendritic cell function. Proc Natl Acad Sci USA 2001;98:8750-8755.
72. Ocana-Morgner C, Mota MM, Rodriguez A. Malaria blood stage suppression of liver stage immunity by dendritic cells. J Exp Med 2003;197:143-151.
73. Perry JA, Rush A, Wilson RJ, Olver CS, Avery AC. Dendritic cells from malaria-infected mice are fully functional APC. J Immunol 2004;172:475-482.
74. Seixas E, Cross C, Quin S, Langhorne J. Direct activation of dendritic cells by the malaria parasite, Plasmodium chabaudi chabaudi. Eur J Immunol 2001;31:2970-2978.
75. Schwarzer E, Alessio M, Ulliers D, Arese P. Phagocytosis of the malarial pigment, hemozoin, impairs expression of major histocompatibility complex class II antigen, CD54, and CD11c in human monocytes. Infect Immun 1998;66:1601-1606.
76. Randolph GJ, Sanchez-Schmitz G, Liebman RM, Schakel K. The CD16(+) (FcgammaRIII(+)) subset of human monocytes preferentially becomes migratory dendritic cells in a model tissue setting. J Exp Med 2002;196:517-527.
77. Randolph GJ, Inaba K, Robbiani DF, Steinman RM, Muller WA. Differentiation of phagocytic monocytes into lymph node dendritic cells in vivo. Immunity 1999;11:753-761.
78. Randolph GJ, Beaulieu S, Lebecque S, Steinman RM, Muller WA. Differentiation of monocytes into dendritic cells in a model of transendothelial trafficking. Science 1998;282:480-483.
79. Randolph GJ, Luther T, Albrecht S, Magdolen V, Muller WA. Role of tissue factor in adhesion of mononuclear phagocytes to and trafficking through endothelium in vitro. Blood 1998;92:4167-4177.
80. Ling IT, Ogun SA, Holder AA. The combined epidermal growth factor-like modules of Plasmodium yoelii Merozoite Surface Protein-1 are required for a protective immune response to the parasite. Parasite Immunol 1995;17:425-433.
81. Daly TM, Long CA. 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 1995;155:236-243.
82. Hirunpetcharat C, et al. Complete protective immunity induced in mice by immunization with the 19-kilodalton carboxyl-terminal fragment of the merozoite surface protein-1 (MSP1[19]) of Plasmodium yoelii expressed in Saccharomyces cerevisiae: correlation of protection with antigen-specific antibody titer, but not with effector CD4+ T cells. J Immunol 1997;159:3400-3411.
83. Tian JH, et al. Genetic regulation of protective immune response in congenic strains of mice vaccinated with a subunit malaria vaccine. J Immunol 1996;157:1176-1183.
84. Stanisic DI, Martin LB, Liu XQ, Jackson D, Cooper J, Good MF. Analysis of immunological nonresponsiveness to the 19-kilodalton fragment of merozoite surface Protein 1 of Plasmodium yoelii: rescue by chemical conjugation to diphtheria toxoid (DT) and enhancement of immunogenicity by prior DT vaccination. Infect Immun 2003;71:5700-5713.
85. Kumar S, et al. Immunogenicity and in vivo efficacy of recombinant Plasmodium falciparum merozoite surface protein-1 in Aotus monkeys. Mol Med 1995;1:325-332.
86. Daly TM, Burns JM Jr, Long CA. Comparison of the carboxy-terminal, cysteine-rich domain of the merozoite surface protein-1 from several strains of Plasmodium yoelii. Mol Biochem Parasitol 1992;52:279-282.
87. Burns JM Jr, Parke LA, Daly TM, Cavacini LA, Weidanz WP, Long CA. A protective monoclonal antibody recognizes a variant-specific epitope in the precursor of the major merozoite surface antigen of the rodent malarial parasite Plasmodium yoelii. J Immunol 1989;142:2835-2840.
88. Renia L, Ling IT, Marussig M, Miltgen F, Holder AA, Mazier D. Immunization with a recombinant C-terminal fragment of Plasmodium yoelii merozoite surface protein 1 protects mice against homologous but not heterologous P. yoelii sporozoite challenge. Infect Immun 1997;65:4419-4423.
89. Stowers AW, Kennedy MC, Keegan BP, Saul A, Long CA, Miller LH. Vaccination of monkeys with recombinant Plasmodium falciparum apical membrane antigen 1 confers protection against blood-stage malaria. Infect Immun 2002;70:6961-6967.
90. Marshall VM, Zhang L, Anders RF, Coppel RL. Diversity of the vaccine candidate AMA-1 of Plasmodium falciparum. Mol Biochem Parasitol 1996;77:109-113.
91. Cortes A, Mellombo M, Mueller I, Benet A, Reeder JC, Anders RF. Geographical structure of diversity and differences between symptomatic and asymptomatic infections for Plasmodium falciparum vaccine candidate AMA1. Infect Immun 2003;71:1416-1426.
92. Escalante AA, et al. Polymorphism in the gene encoding the apical membrane antigen-1 (AMA-1) of Plasmodium falciparum. X. Asembo Bay Cohort Project. Mol Biochem Parasitol 2001;113:279-287.
93. Polley SD, Conway DJ. Strong diversifying selection on domains of the Plasmodium falciparum apical membrane antigen 1 gene. Genetics 2001;158:1505-1512.
94. Oliveira DA, et al. Genetic conservation of the Plasmodium falciparum apical membrane antigen-1 (AMA-1). Mol Biochem Parasitol 1996;76:333-336.
95. Crewther PE, Matthew ML, Flegg RH, Anders RF. Protective immune responses to apical membrane antigen 1 of Plasmodium chabaudi involve recognition of strain-specific epitopes. Infect Immun 1996;64:3310-3317.
96. Kennedy MC, et al. In vitro studies with recombinant Plasmodium falciparum apical membrane antigen 1 (AMA1): production and activity of an AMA1 vaccine and generation of a multiallelic response. Infect Immun 2002;70:6948-6960.
97. Hirunpetcharat C, Vukovic P, Liu XQ, Kaslow DC, Miller LH, Good MF. 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 1999;162:7309-7314.
98. Akanmori BD, Afari EA, Sakatoku H, Nkrumah FK. A longitudinal study of malaria infection, morbidity and antibody titres in infants of a rural community in Ghana. Trans R Soc Trop Med Hyg 1995;89:560-561.
99. Campbell CC, Martinez JM, Collins WE. Seroepidemiological studies of malaria in pregnant women and newborns from coastal El Salvador. Am J Trop Med Hyg 1980;29:151-157.
100. Edozien JC, Gilles HM, Udezo IOK. Adult and cord blood gamma-globulin and immunity to malaria in Nigerians. Lancet 1962;ii:951-955.
101. McGregor IA. The passive transfer of human malarial immunity. Am J Trop Med Hyg 1964;13:237-239.
102. Siegrist CA, Lambert PH. Maternal immunity and infant responses to immunization: factors influencing infant responses. Dev Biol Stand 1998;95:133-139.
103. Siegrist CA, et al. Influence of maternal antibodies on vaccine responses: inhibition of antibody but not T cell responses allows successful early prime-boost strategies in mice. Eur J Immunol 1998;28:4138-4148.
104. Siegrist CA. Vaccination in the neonatal period and early infancy. Int Rev Immunol 2000;19:195-219.
105. Siegrist CA. Neonatal and early life vaccinology. Vaccine 2000;19:3331-3346.
106. Harte PG, De Souza JB, Playfair JH. Failure of malaria vaccination in mice born to immune mothers. Clin Exp Immunol 1982;49:509-516.
107. Harte PG, Playfair JH. Failure of malaria vaccination in mice born to immune mothers. II. Induction of specific suppressor cells by maternal IgG. Clin Exp Immunol 1983;51:157-164.
108. Adler S, Foner A. Transfer of antibodies to Plasmodium vinckei through milk of immune mice. Isr J Med Sci 1965;1:988-993.
109. Bruce-Chwatt L. Plasmodium berghei in the placenta of mice and rats: Transmission of specific immunity from mother rats to litters. Nature 1954;173:353-354.
110. Desowitz RS. Some factors influencing the induction, maintenance and degree of maternally transmitted protective immunity to malaria (Plasmodium berghei) Trans R Soc Trop Med Hyg 1973;67:238-244.
111. Harte PG, Rogers N, Targett GA, Playfair JH. Maternal inhibition of malaria vaccination in mice can be overcome by giving a second dose of vaccine. Immunology 1984;53:401-409.
112. Orjih AU, Cochrane AH, Nussenzweig RS. Active immunization and passive transfer of resistance against sporozoite-induced malaria in infant mice. Nature 1981;291:331-332.
113. Palmer TT. Plasmodium berghei infection in pregnant rats: effects on antibody response and course of infection in offspring. J Parasitol 1978;64:493-496.
114. Terry RJ. Transmission of antimalarial immunity (Plasmodium berghei) from mother rats to their young during lactation. Trans R Soc Trop Med Hyg 1956;50:41-53.
115. Sedegah M, et al. Successful induction of CD8 T cell-dependent protection against malaria by sequential immunization with DNA and recombinant poxvirus of neonatal mice born to immune mothers. J Immunol, 2003;171:3148-3153.
116. Stanisic DI, Martin L, Gatton M, Good MF. Inhibition of MSP1-19 specific antibody responses in neonatal pups by maternally derived MSP1-19 specific antibodies but not whole parasite specific antibodies. J Immunol 2004;172:5570-5581.
117. Stanisic DI, Martin LB, Good MF. The role of the 19-kDa region of merozoite surface protein 1 and whole-parasite-specific maternal antibodies in directing neonatal pups' responses to rodent malaria infection. J Immunol 2003;171:5461-5469.
118. + T cells adoptively transferred into recipient mice after challenge with homologous parasite. Proc Natl Acad Sci USA 1998;95:1715-1720.
119. Xu H, et al. The mechanism and significance of deletion of parasite-specific CD4(+) T cells in malaria infection. J Exp Med 2002;195:881-892.
120. Hayashi N, Liu D, Min B, Ben-Sasson SZ, Paul WE. Antigen challenge leads to in vivo activation and elimination of highly polarized TH1 memory T cells. Proc Natl Acad Sci USA 2002;99:6187-6191.
121. Wipasa J, Xu H, Stowers A, Good MF. Apoptotic deletion of Th cells specific for the 19-kDa carboxyl-terminal fragment of merozoite surface protein 1 during malaria infection. J Immunol 2001;167:3903-3909.
122. Ahlborg N, Ling IT, Howard W, Holder AA, Riley EM. Protective immune responses to the 42-kilodalton (kDa) region of Plasmodium yoelii merozoite surface protein 1 are induced by the C-terminal 19-kda region but not by the adjacent 33-kDa region. Infect Immun 2002;70:820-825.
123. Kumar A, Arora R, Kaur P, Chauhan VS, Sharma P. 'Universal' T helper cell determinants enhance immunogenicity of a Plasmodium falciparum merozoite surface antigen peptide. J Immunol 1992;148:1499-1505.
124. Ramasamy R, Wijesundere DA, Nagendran K, Ramasamy MS. Antibody and clinical responses in volunteers to immunization with malaria peptide-diptheria toxoid conjugates. Clin Exp Immunol 1995;99:168-174.
125. Herzenberg LA, Tokuhisa T. Carrier-priming leads to hapten-specific suppression. Nature 1980;285:664-667.
126. Schutze MP, Leclerc C, Jolivet M, Audibert F, Chedid L. Carrier-induced epitopic suppression, a major issue for future synthetic vaccines. J Immunol 1985;135:2319-2322.
127. Schutze MP, Leclerc C, Vogel FR, Chedid L. Epitopic suppression in synthetic vaccine models: analysis of the effector mechanisms. Cell Immunol 1987;104:79-90.
128. Schutze MP, Deriaud E, Przewlocki G, LeClerc C. Carrier-induced epitopic suppression is initiated through clonal dominance. J Immunol 1989;142:2635-2640.
129. Good MF, et al. Human T-cell recognition of the circumsporozoite protein of Plasmodium falciparum: immunodominant T-cell domains map to the polymorphic regions of the molecule. Proc Natl Acad Sci USA 1988;85:1199-1203.
130. Hughes AL. Circumsporozoite protein genes of malaria parasites (Plasmodium spp.): evidence for positive selection on immunogenic regions. Genetics 1991;127:345-353.
131. Verra F, Hughes AL. Natural selection on apical membrane antigen-1 of Plasmodium falciparum. Parassitologia 1999;41:93-95.
132. Sercarz EE, Lehmann PV, Ametani A, Benichou G, Miller A, Moudgil K. Dominance and crypticity of T cell antigenic determinants. Annu Rev Immunol 1993;11:729-766.
133. Amante FH, Crewther PE, Anders RF, Good MF. A cryptic T cell epitope on the apical membrane antigen 1 of Plasmodium chabaudi adami can prime for an anamnestic antibody response: implications for malaria vaccine design. J Immunol 1997;159:5535-5544.
134. Bretscher PA, Wei G, Menon JN, Bielefeldt-Ohmann H. Establishment of stable, cell-mediated immunity that makes 'susceptible' mice resistant to Leishmania major. Science 1992;257:539-542.
135. Shata MT, et al. Exposure to low infective doses of HCV induces cellular immune responses without consistently detectable viremia or seroconversion in chimpanzees. Virology 2003;314:601-616.
136. McConkey SJ, et al. Enhanced T-cell immunogenicity of plasmid DNA vaccines boosted by recombinant modified vaccinia virus Ankara in humans. Nat Med 2003;9:729-735.
137. Su Z, Tam MF, Jankovic D, Stevenson MM. Vaccination with novel immunostimulatory adjuvants against blood-stage malaria in mice. Infect Immun 2003;71:5178-5187.
138. Miller LH, Howard RJ, Carter R, Good MF, Nussenzweig V, Nussenzweig RS. Research toward malaria vaccines. Science 1986;234:1349-1356.