Protective and pathogenic roles of CD8+ T cells during malaria infection

Parasite Immunology

Volumn 28, Issue 1-2, 2006, Pages 15-24

  Hafalla, J C R ^a,b   Cockburn, I A ^b   Zavala, F ^b  

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

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

Author keywords

CD8+ T cell; Cerebral malaria; Liver stages; Plasmodium; Vaccine

Indexed keywords

ANTIINFLAMMATORY AGENT; ANTIMALARIAL AGENT; CHEMOKINE; EPITOPE; GLYCOLIPID; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; MONOCLONAL ANTIBODY; PLASMID DNA; PRIMAQUINE; PROTOZOAL PROTEIN; PROTOZOAL VACCINE; RECOMBINANT VACCINE; SUBUNIT VACCINE; YELLOW FEVER VACCINE; MALARIA VACCINE;

ANTIGEN PRESENTING CELL; ATTENUATION; BRAIN MALARIA; CD8+ T LYMPHOCYTE; CELL PROTECTION; CLINICAL TRIAL; EFFECTOR CELL; HUMAN; IMMUNOGENICITY; LIVER FUNCTION; MALARIA; MEMORY; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; REVIEW; RODENT; SPOROZOITE; ANIMAL; ANTIGEN PRESENTATION; ERYTHROCYTE; IMMUNOLOGICAL MEMORY; IMMUNOLOGY; LIVER; MOUSE; PARASITOLOGY; PLASMODIUM BERGHEI; PLASMODIUM YOELII; VIROLOGY;

RODENTIA;

ANIMALS; ANTIGEN PRESENTATION; CD8-POSITIVE T-LYMPHOCYTES; ERYTHROCYTES; HUMANS; IMMUNODOMINANT EPITOPES; IMMUNOLOGIC MEMORY; LIVER; MALARIA; MALARIA VACCINES; MICE; PLASMODIUM BERGHEI; PLASMODIUM YOELII;

EID: 33644863805     PISSN: 01419838     EISSN: 13653024     Source Type: Journal    
DOI: 10.1111/j.1365-3024.2006.00777.x     Document Type: Review

References (106)

1. Schofield L Villaquiran J Ferreira A Schellekens H Nussenzweig R Nussenzweig V Gamma interferon, CD8+ T cells and antibodies required for immunity to malaria sporozoites Nature 1987 330 664 666
2. Weiss WR Sedegah M Beaudoin RL Miller LH Good MF CD8+ T cells (cytotoxic/suppressors) are required for protection in mice immunized with malaria sporozoites Proc Natl Acad Sci USA 1988 85 573 576
3. Romero P Maryanski JL Corradin G Nussenzweig RS Nussenzweig V Zavala F Cloned cytotoxic T cells recognize an epitope in the circumsporozoite protein and protect against malaria Nature 1989 341 323 326
4. Rodrigues MM Cordey AS Arreaza G et al. CD8+ cytolytic T cell clones derived against the Plasmodium yoelii circumsporozoite protein protect against malaria Int Immunol 1991 3 579 585
5. Weiss WR Berzofsky JA Houghten RA Sedegah M Hollindale M Hoffman SL A T cell clone directed at the circumsporozoite protein which protects mice against both Plasmodium yoelii and Plasmodium berghei J Immunol 1992 149 2103 2109
6. Rodrigues M Nussenzweig RS Romero P Zavala F The in vivo cytotoxic activity of CD8+ T cell clones correlates with their levels of expression of adhesion molecules J Exp Med 1992 175 895 905
7. Ferreira A Schofield L Enea V et al. Inhibition of development of exoerythrocytic forms of malaria parasites by gamma-interferon Science 1986 232 881 884
8. Schofield L Ferreira A Altszuler R Nussenzweig V Nussenzweig RS Interferon-gamma inhibits the intrahepatocytic development of malaria parasites in vitro J Immunol 1987 139 2020 2025
9. Nussler AK Renia L Pasquetto V Miltgen F Matile H Mazier D In vivo induction of the nitric oxide pathway in hepatocytes after injection with irradiated malaria sporozoites, malaria blood parasites or adjuvants Eur J Immunol 1993 23 882 887
10. Seguin MC Klotz FW Schneider I et al. Induction of nitric oxide synthase protects against malaria in mice exposed to irradiated Plasmodium berghei infected mosquitoes: involvement of interferon gamma and CD8+ T cells J Exp Med 1994 180 353 358
11. Renggli J Hahne M Matile H Betschart B Tschopp J Corradin G Elimination of P. berghei liver stages is independent of Fas (CD95/Apo-I) or perforin-mediated cytotoxicity Parasite Immunol 1997 19 145 148
12. Doolan DL Hoffman SL The complexity of protective immunity against liver-stage malaria J Immunol 2000 165 1453 1462
13. Morrot A Zavala F Effector and memory CD8+ T cells as seen in immunity to malaria Immunol Rev 2004 201 291 303
14. Sano G Hafalla JC Morrot A Abe R Lafaille JJ Zavala F Swift development of protective effector functions in naive CD8(+) T cells against malaria liver stages J Exp Med 2001 194 173 180
15. Busch DH Pilip Pamer EG Evolution of a complex T cell receptor repertoire during primary and recall bacterial infection J Exp Med 1998 188 61 70
16. Flynn KJ Belz GT Altman JD Ahmed R Woodland DL Doherty PC Virus-specific CD8+ T cells in primary and secondary influenza pneumonia Immunity 1998 8 683 691
17. Murali-Krishna K Altman JD Suresh M Sourdive D Zajac A Ahmed R In vivo dynamics of anti-viral CD8 T cell responses to different epitopes. An evaluation of bystander activation in primary and secondary responses to viral infection Adv Exp Med Biol 1998 452 123 142
18. Belz GT Altman JD Doherty PC Characteristics of virus-specific CD8(+) T cells in the liver during the control and resolution phases of influenza pneumonia Proc Natl Acad Sci USA 1998 95 13812 13817
19. Masopust D Vezys V Marzo AL Lefrancois L Preferential localization of effector memory cells in nonlymphoid tissue Science 2001 291 2413 2417
20. Masopust D Vezys V Usherwood EJ et al. Activated primary and memory CD8 T cells migrate to nonlymphoid tissues regardless of site of activation or tissue of origin J Immunol 2004 172 4875 4882
21. Carvalho LH Sano G Hafalla JC Morrot A Curotto de Lafaille MA Zavala F IL-4-secreting CD4+ T cells are crucial to the development of CD8+ T-cell responses against malaria liver stages Nat Med 2002 8 166 170
22. Hafalla JC Sano G Carvalho LH Morrot A Zavala F Short-term antigen presentation and single clonal burst limit the magnitude of the CD8(+) T cell responses to malaria liver stages Proc Natl Acad Sci USA 2002 99 11819 11824
23. Hafalla JC Morrot A Sano G Milon G Lafaille JJ Zavala F Early self-regulatory mechanisms control the magnitude of CD8+ T cell responses against liver stages of murine malaria J Immunol 2003 171 964 970
24. Guebre-Xabier M Schwenk R Krzych U Memory phenotype CD8(+) T cells persist in livers of mice protected against malaria by immunization with attenuated Plasmodium berghei sporozoites Eur J Immunol 1999 29 3978 3986
25. Berenzon D Schwenk RJ Letellier L Guebre-Xabier M Williams J Krzych U Protracted protection to Plasmodium berghei malaria is linked to functionally and phenotypically heterogeneous liver memory CD8+ T cells J Immunol 2003 171 2024 2034
26. Hoffman SL Isenbarger D Long GW et al. Sporozoite vaccine induces genetically restricted T cell elimination of malaria from hepatocytes Science 1989 244 1078 1081
27. Pradel G Frevert U Malaria sporozoites actively enter and pass through rat Kupffer cells prior to hepatocyte invasion Hepatology 2001 33 1154 1165
28. Marshall DR Turner SJ Belz GT et al. Measuring the diaspora for virus-specific CD8+ T cells Proc Natl Acad Sci USA 2001 98 6313 6318
29. Jung S Unutmaz D Wong P et al. In vivo depletion of CD11c(+) dendritic cells abrogates priming of CD8(+) T cells by exogenous cell-associated antigens Immunity 2002 17 211 220
30. Klotz FW Scheller LF Seguin MC et al. Co-localization of inducible-nitric oxide synthase and Plasmodium berghei in hepatocytes from rats immunized with irradiated sporozoites J Immunol 1995 154 3391 3395
31. Scheller LF Azad AF Maintenance of protective immunity against malaria by persistent hepatic parasites derived from irradiated sporozoites Proc Natl Acad Sci USA 1995 92 4066 4068
32. Kaech SM Hemby S Kersh E Ahmed R Molecular and functional profiling of memory CD8 T cell differentiation Cell 2002 111 837 851
33. Franke ED Sette A Sacci J Jr. Southwood S Corradin G Hoffman SL A subdominant CD8(+) cytotoxic T lymphocyte (CTL) epitope from the Plasmodium yoelii circumsporozoite protein induces CTLs that eliminate infected hepatocytes from culture Infect Immun 2000 68 3403 3411
34. Khusmith S Sedegah M Hoffman SL Complete protection against Plasmodium yoelii by adoptive transfer of a CD8+ cytotoxic T-cell clone recognizing sporozoite surface protein 2 Infect Immun 1994 62 2979 2983
35. Doolan DL Sedegah M Hedstrom RC Hobart P Charoenvit Y Hoffman SL Circumventing genetic restriction of protection against malaria with multigene DNA immunization: CD8+ cell-, interferon gamma-, and nitric oxide-dependent immunity J Exp Med 1996 183 1739 1746
36. Hetttihewa LM Immunization of retrovirus-transfected dendritic cells induces specific cytotoxic T lymphocytes for two distinct malarial peptides presented by Kd molecule Int Immunopharmacol 2003 3 1401 1411
37. Belnoue E Costa FT Frankenberg T et al. Protective T cell immunity against malaria liver stage after vaccination with live sporozoites under chloroquine treatment J Immunol 2004 172 2487 2495
38. Aggarwal A Kumar S Jaffe R Hone D Gross M Sadoff J Oral Salmonella: malaria circumsporozoite recombinants induce specific CD8+ cytotoxic T cells J Exp Med 1990 172 1083 1090
39. Sedegah M Chiang CH Weiss WR et al. Recombinant pseudorabies virus carrying a plasmodium gene: herpesvirus as a new live viral vector for inducing T- and B-cell immunity Vaccine 1992 10 578 584
40. Li S Rodrigues M Rodriguez D et al. Priming with recombinant influenza virus followed by administration of recombinant vaccinia virus induces CD8+ T-cell-mediated protective immunity against malaria Proc Natl Acad Sci USA 1993 90 5214 5218
41. Rodrigues M Li S Murata K et al. Influenza and vaccinia viruses expressing malaria CD8+ T and B cell epitopes. Comparison of their immunogenicity and capacity to induce protective immunity J Immunol 1994 153 4636 4648
42. Sedegah M Hedstrom R Hobart P Hoffman SL Protection against malaria by immunization with plasmid DNA encoding circumsporozoite protein Proc Natl Acad Sci USA 1994 91 9866 9870
43. Renggli J Valmori D Romero JF et al. CD8+ T-cell protective immunity induced by immunization with Plasmodium berghei CS protein-derived synthetic peptides: evidence that localization of peptide-specific CTLs is crucial for protection against malaria Immunol Lett 1995 46 199 205
44. Franke ED Corradin G Hoffman SL Induction of protective CTL responses against the Plasmodium yoelii circumsporozoite protein by immunization with peptides J Immunol 1997 159 3424 3433
45. Wang HH Rogers WO Kang YH Sedegah M Hoffman SL Partial protection against malaria by immunization with Leishmania enriettii expressing the Plasmodium yoelii circumsporozoite protein Mol Biochem Parasitol 1995 69 139 148
46. Charest H Sedegah M Yap GS et al. Recombinant attenuated Toxoplasma gondii expressing the Plasmodium yoelii circumsporozoite protein provides highly effective priming for CD8+ T cell-dependent protective immunity against malaria J Immunol 2000 165 2084 2092
47. Lanar DE Tine JA de Taisne C et al. Attenuated vaccinia virus-circumsporozoite protein recombinants confer protection against rodent malaria Infect Immun 1996 64 1666 1671
48. Rodrigues EG Zavala F Eichinger D Wilson JM Tsuji M Single immunizing dose of recombinant adenovirus efficiently induces CD8+ T cell-mediated protective immunity against malaria J Immunol 1997 158 1268 1274
49. Tsuji M Bergmann CC Takita-Sonoda Y et al. Recombinant Sindbis viruses expressing a cytotoxic T-lymphocyte epitope of a malaria parasite or of influenza virus elicit protection against the corresponding pathogen in mice J Virol 1998 72 6907 6910
50. Gilbert SC Schneider J Plebanski M et al. Ty virus-like particles, DNA vaccines and Modified Vaccinia Virus Ankara; comparisons and combinations Biol Chem 1999 380 299 303
51. Oliveira-Ferreira J Miyahira Y Layton GT et al. Immunogenicity of Ty-VLP bearing a CD8(+) T cell epitope of the CS protein of P. yoelii: enhanced memory response by boosting with recombinant vaccinia virus Vaccine 2000 18 1863 1869
52. Tao D Barba-Spaeth G Rai U Nussenzweig V Rice CM Nussenzweig RS Yellow fever 17D as a vaccine vector for microbial CTL epitopes: protection in a rodent malaria model J Exp Med 2005 201 201 209
53. Murata K Garcia-Sastre A Tsuji M et al. Characterization of in vivo primary and secondary CD8+ T cell responses induced by recombinant influenza and vaccinia viruses Cell Immunol 1996 173 96 107
54. Schneider J Gilbert SC Blanchard TJ et al. Enhanced immunogenicity for CD8+ T cell induction and complete protective efficacy of malaria DNA vaccination by boosting with modified vaccinia virus Ankara Nat Med 1998 4 397 402
55. Sedegah M Jones TR Kaur M et al. Boosting with recombinant vaccinia increases immunogenicity and protective efficacy of malaria DNA vaccine Proc Natl Acad Sci USA 1998 95 7648 7653
56. Bruna-Romero O Gonzalez-Aseguinolaza G Hafalla JC Tsuji M Nussenzweig RS Complete, long-lasting protection against malaria of mice primed and boosted with two distinct viral vectors expressing the same plasmodial antigen Proc Natl Acad Sci USA 2001 98 11491 11496
57. Gilbert SC Schneider J Hannan CM et al. Enhanced CD8 T cell immunogenicity and protective efficacy in a mouse malaria model using a recombinant adenoviral vaccine in heterologous prime-boost immunisation regimes Vaccine 2002 20 1039 1045
58. Sedegah M Brice GT Rogers WO et al. Persistence of protective immunity to malaria induced by DNA priming and poxvirus boosting: characterization of effector and memory CD8(+)-T-cell populations Infect Immun 2002 70 3493 3499
59. Gonzalez-Aseguinolaza G Nakaya Y Molano A et al. Induction of protective immunity against malaria by priming-boosting immunization with recombinant cold-adapted influenza and modified vaccinia Ankara viruses expressing a CD8+-T-cell epitope derived from the circumsporozoite protein of Plasmodium yoelii J Virol 2003 77 11859 11866
60. Anderson RJ Hannan CM Gilbert SC et al. Enhanced CD8+ T cell immune responses and protection elicited against Plasmodium berghei malaria by prime boost immunization regimens using a novel attenuated fowlpox virus J Immunol 2004 172 3094 3100
61. Zavala F Rodrigues M Rodriguez D Rodriguez JR Nussenzweig RS Esteban M A striking property of recombinant poxviruses: efficient inducers of in vivo expansion of primed CD8(+) T cells Virology 2001 280 155 159
62. Weiss WR Ishii KJ Hedstrom RC et al. A plasmid encoding murine granulocyte-macrophage colony-stimulating factor increases protection conferred by a malaria DNA vaccine J Immunol 1998 161 2325 2332
63. Bruna-Romero O Schmieg J Del Val M Buschle M Tsuji M The dendritic cell-specific chemokine, dendritic cell-derived CC chemokine 1, enhances protective cell-mediated immunity to murine malaria J Immunol 2003 170 3195 3203
64. Gonzalez-Aseguinolaza G Van Kaer L Bergmann CC et al. Natural killer T cell ligand alpha-galactosylceramide enhances protective immunity induced by malaria vaccines J Exp Med 2002 195 617 624
65. Hill AV Allsopp CE Kwiatkowski D et al. Common west African HLA antigens are associated with protection from severe malaria Nature 1991 352 595 600
66. Hill AV Elvin J Willis AC et al. Molecular analysis of the association of HLA-B53 and resistance to severe malaria Nature 1992 360 434 439
67. Yate SNR Snow R Allsopp CE et al. HLV associated differential susceptibility to severe malaria in children from Kilifi, Kenya in 6th Malaria Meeting of the British Society of Parasitology Liverpool, UK 1994
68. Aidoo M Lalvani A Gilbert SC et al. Cytotoxic T-lymphocyte epitopes for HLA-B53 and other HLA types in the malaria vaccine candidate liver-stage antigen 3 Infect Immun 2000 68 227 232
69. Connelly M King CL Bucci K et al. T-cell immunity to peptide epitopes of liver-stage antigen 1 in an area of Papua New Guinea in which malaria is holoendemic Infect Immun 1997 65 5082 5087
70. Doolan DL Khamboonruang C Beck HP Houghten RA Good MF Cytotoxic T lymphocyte (CTL) low-responsiveness to the Plasmodium falciparum circumsporozoite protein in naturally-exposed endemic populations: analysis of human CTL response to most known variants Int Immunol 1993 5 37 46
71. Plebanski M Aidoo M Whittle HC Hill AV Precursor frequency analysis of cytotoxic T lymphocytes to pre-erythrocytic antigens of Plasmodium falciparum in West Africa J Immunol 1997 158 2849 2855
72. Sedegah M Belmonte M Epstein JE 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
73. Wizel B Houghten RA Parker KC et al. Irradiated sporozoite vaccine induces HLA-B8-restricted cytotoxic T lymphocyte responses against two overlapping epitopes of the Plasmodium falciparum sporozoite surface protein 2 J Exp Med 1995 182 1435 1445
74. John CC Moormann AM Sumba PO Ofulla AV Pregibon DC Kazura JW Gamma interferon responses to Plasmodium falciparum liver-stage antigen 1 and thrombospondin-related adhesive protein and their relationship to age, transmission intensity, and protection against malaria Infect Immun 2004 72 5135 5142
75. Kester KE McKinney DA Tornieporth N et al. Efficacy of recombinant circumsporozoite protein vaccine regimens against experimental Plasmodium falciparum malaria J Infect Dis 2001 183 640 647
76. Stoute JA Kester KE Krzych U et al. Long-term efficacy and immune responses following immunization with the RTS,S malaria vaccine J Infect Dis 1998 178 1139 1144
77. Stoute JA Slaoui M Heppner DG et al. A preliminary evaluation of a recombinant circumsporozoite protein vaccine against Plasmodium falciparum malaria. RTS,S Malaria Vaccine Evaluation Group N Engl J Med 1997 336 86 91
78. Sun P Schwenk R White K 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 2003 171 6961 6967
79. Alonso PL Sacarlal J Aponte JJ et al. Efficacy of the RTS,S/AS02A vaccine against Plasmodium falciparum infection and disease in young African children: randomised controlled trial Lancet 2004 364 1411 1420
80. Bojang KA Milligan PJ Pinder M et al. Efficacy of RTS,S/AS02 malaria vaccine against Plasmodium falciparum infection in semi-immune adult men in The Gambia: a randomised trial Lancet 2001 358 1927 1934
81. McConkey SJ Reece WH Moorthy VS 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
82. Wang R Epstein J Charoenvit Y et al. Induction in humans of CD8+ and CD4+ T cell and antibody responses by sequential immunization with malaria DNA and recombinant protein J Immunol 2004 172 5561 5569
83. BenMohamed L Thomas A Druilhe P Long-term multiepitopic cytotoxic-T-lymphocyte responses induced in chimpanzees by combinations of Plasmodium falciparum liver-stage peptides and lipopeptides Infect Immun 2004 72 4376 4384
84. Daubersies P Thomas AW Millet P et al. Protection against Plasmodium falciparum malaria in chimpanzees by immunization with the conserved pre-erythrocytic liver-stage antigen 3 Nat Med 2000 6 1258 1263
85. Doolan DL Hoffman SL Southwood S Wentworth PA Sidney J Chesnut RW Keogh E Appella E Nutman TB Lal AA Gordon DM Olco A Sette A Dogenorate cytotoxic T-cell epitopes from P. falciparum restricted by multiple HLA-A and HLA-B supertype alleles Immunity 1997 7 97 112
86. Gilbert SC Plebanski M Gupta S et al. Association of malaria parasite population structure, HLA, and immunological antagonism Science 1998 279 1173 1177
87. Plebanski M Lee EA Hannan CM et al. Altered peptide ligands narrow the repertoire of cellular immune responses by interfering with T-cell priming Nat Med 1999 5 565 571
88. Kumar S Miller LH Cellular mechanisms in immunity to blood stage infection Immunol Lett 1990 25 109 114
89. Vinetz JM Kumar S Good MF Fowlkes BJ Berzofsky JA Miller LH Adoptive transfer of CD8+ T cells from immune animals does not transfer immunity to blood stage Plasmodium yoelii malaria J Immunol 1990 144 1069 1074
90. Podoba JE Stevenson MM CD4+ and CD8+ T lymphocytes both contribute to acquired immunity to blood-stage Plasmodium chabaudi AS Infect Immun 1991 59 51 58
91. Thumwood CM Hunt NH Clark IA Cowden WB Breakdown of the blood-brain barrier in murine cerebral malaria Parasitology 1988 96 579 589
92. Hearn J Rayment N Landon DN Katz DR de Souza JB Immunopathology of cerebral malaria: morphological evidence of parasite sequestration in murine brain microvasculature Infect Immun 2000 68 5364 5376
93. Finley RW Mackey LJ Lambert PH Virulent P. berghei malaria: prolonged survival and decreased cerebral pathology in cell-dependent nude mice J Immunol 1982 129 2213 2218
94. Imai Y Kamiyama T T lymphocyte-dependent development of cerebral symptoms in WM/Ms rats infected with Plasmodium berghei Ann Trop Med Parasitol 1994 88 83 85
95. Grau GE Piguet PF Engers HD Louis JA Vassalli P Lambert PH L3T4+ T lymphocytes play a major role in the pathogenesis of murine cerebral malaria J Immunol 1986 137 2348 2354
96. Yanez DM Manning DD Cooley AJ Weidanz WP van der Heyde HC Participation of lymphocyte subpopulations in the pathogenesis of experimental murine cerebral malaria J Immunol 1996 157 1620 1624
97. Hermsen C van de Wiel T Mommers E Sauerwein R Eling W Depletion of CD4+ or CD8+ T-cells prevents Plasmodium berghei induced cerebral malaria in end-stage disease Parasitology 1997 114 1 7 12
98. Boubou MI Collette A Voegtle D Mazier D Cazenave PA Pied S T cell response in malaria pathogenesis: selective increase in T cells carrying the TCR V (beta) 8 during experimental cerebral malaria Int Immunol 1999 11 1553 1562
99. Belnoue E Kayibanda M Vigario AM et al. On the pathogenic role of brain-sequestered alphabeta CD8+ T cells in experimental cerebral malaria J Immunol 2002 169 6369 6375
100. Nitcheu J Bonduelle O Combadiere C et al. Perforin-dependent brain-infiltrating cytotoxic CD8+ T lymphocytes mediate experimental cerebral malaria pathogenesis J Immunol 2003 170 2221 2228
101. Belnoue E Kayibanda M Deschemin JC et al. CCR5 deficiency decreases susceptibility to experimental cerebral malaria Blood 2003 101 4253 4259
102. Bagot S Nogueira F Collette A et al. Comparative study of brain CD8+ T cells induced by sporozoites and those induced by blood-stage Plasmodium berghei ANKA involved in the development of cerebral malaria Infect Immun 2004 72 2817 2826
103. Clark IA Awburn MM Whitten RO et al. Tissue distribution of migration inhibitory factor and inducible nitric oxide synthase in falciparum malaria and sepsis in African children Malaria J 2003 2 6
104. Brown HC Chau TT Mai NT et al. Blood-brain barrier function in cerebral malaria and CNS infections in Vietnam Neurology 2000 55 104 111
105. Medana IM Day NP Hien TT et al. Axonal injury in cerebral malaria Am J Pathol 2002 160 655 666
106. Collette A Bagot S Ferrandiz ME Cazenave PA Six A Pied S A profound alteration of blood TCRB repertoire allows prediction of cerebral malaria J Immunol 2004 173 4568 4575