The war between the malaria parasite and the immune system: Immunity, immunoregulation and immunopathology

Clinical and Experimental Immunology

Volumn 133, Issue 2, 2003, Pages 145-152

  Artavanis Tsakonas, K ^a,b   Tongren, J E ^a   Riley, E M ^a  

^a LONDON SCHOOL OF HYGIENE AND TROPICAL MEDICINE   (United Kingdom)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Human; Immunoregulation; Malaria; Parasitic protozoa

Indexed keywords

GAMMA INTERFERON; MALARIA VACCINE; TUMOR NECROSIS FACTOR ALPHA;

ANEMIA; ANTIMALARIAL ACTIVITY; BRAIN MALARIA; CAUSE OF DEATH; CHILDHOOD DISEASE; CLINICAL OBSERVATION; CONTROLLED STUDY; DENSITY; DISEASE MODEL; DISEASE SEVERITY; ENDEMIC DISEASE; FATALITY; FEVER; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IMMUNOMODULATION; IMMUNOPATHOLOGY; IMMUNOREGULATION; INFLAMMATION; NONHUMAN; PARASITE IMMUNITY; PLASMODIUM; PLASMODIUM FALCIPARUM; PLASMODIUM VIVAX; PRIORITY JOURNAL; REINFECTION; REVIEW; RISK ASSESSMENT;

ADULT; AGE FACTORS; CHILD; HUMANS; IMMUNITY, NATURAL; INTERFERON TYPE II; MALARIA; MALARIA, CEREBRAL; MODELS, IMMUNOLOGICAL;

EID: 0042667124     PISSN: 00099104     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2249.2003.02174.x     Document Type: Review

References (69)

1. Molineaux L. Plasmodium falciparum malaria. some epidemiological implications of parasite and host diversity. Ann Trop Med Parasitol 1996; 90:379-93.
2. Yipp BG, Baruch DI, Brady C et al. Recombinant PfEMP1 peptide inhibits and reverses cytoadherence of clinical Plasmodium falciparum isolates in vivo. Blood 2003; 101:331-7.
3. Smith JD, Craig AG, Kriek N et al. Identification of a Plasmodium falciparum intercellular adhesion molecule-1 binding domain: a parasite adhesion trait implicated in cerebral malaria. Proc Natl Acad Sci USA 2000; 97:1766-71.
4. Bull PC, Marsh K. The role of antibodies to Plasmodium falciparum-infected-erythrocyte surface antigens in naturally acquired immunity to malaria. Trends Microbiol 2002; 10:55-8.
5. 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; 75:281-92.
6. Guevara Patino JA, Holder AA, McBride JS, Blackman MJ. Antibodies that inhibit malaria merozoite surface protein-1 processing and erythrocyte invasion are blocked by naturally acquired human antibodies. J Exp Med 1997; 186:1689-99.
7. Oeuvray C, Bouharoun-Tayoun H, Gras-Masse H et al. Merozoite surface protein-3: a malaria protein inducing antibodies that promote Plasmodium falciparum killing by cooperation with blood monocytes. Blood 1994; 84:1594-602.
8. Fritsche G, Larcher C, Schennach H, Weiss G. Regulatory interactions between iron and nitric oxide metabolism for immune defense against Plasmodium falciparum infection. J Infect Dis 2001; 183:1388-94.
9. Tsuji M, Zavala F. T cells as mediators of protective immunity against liver stages of Plasmodium. Trends Parasitol 2003; 19:88-93
10. Brunet LR. Nitric oxide in parasitic infections. Int Immunopharmacol 2001; 1:1457-67.
11. Balmer P, Phillips HM, Maestre AE, McMonagle FA, Phillips RS. The effect of nitric oxide on the growth of Plasmodium falciparum. P. chabaudi and P berghei in vitro. Parasite Immunol 2000; 22:97-106
12. Al Yaman FM, Mokela D, Genton B, Rockett KA, Alpers MP, Clark IA. Association between serum levels of reactive nitrogen intermediates and coma in children with cerebral malaria in Papua New Guinea. Trans R Soc Trop Med Hyg 1996; 90:270-3
13. Favre N, Ryffel B, Rudin W. Parasite killing in murine malaria does not require nitric oxide production. Parasitology 1999; 118:139-43
14. Favre N, Ryffel B, Rudin W. The development of murine cerebral malaria does not require nitric oxide production. Parasitology 1999; 118:135-8
15. Grau GE, Taylor TE, Molyneux ME et al. Tumor necrosis factor and disease severity in children with falciparum malaria. N Engl J Med 1989; 320:1586-91
16. Kwiatkowski D, Hill AV, Sambou I et al. TNF concentration in fatal cerebral, non-fatal cerebral, and uncomplicated Plasmodium falciparum malaria. Lancet 1990; 336:1201-4.
17. Kurtzhals JA, Adabayeri V, Goka BQ et al. Low plasma concentrations of interleukin 10 in severe malarial anaemia compared with cerebral and uncomplicated malaria. Lancet 1998; 351:1768-72
18. Engwerda CR, Mynott TL, Sawhney S, De Souza JB, Bickle QD, Kaye PM. Locally up-regulated lymphotoxin alpha, not systemic tumor necrosis factor alpha, is the principle mediator of murine cerebral malaria. J Exp Med 2002; 195:1371-7
19. Anstey NM, Weinberg JB, Hassanali MY et al. Nitric oxide in Tanzanian children with malaria. inverse relationship between malaria severity and nitric oxide production/nitric oxide synthase type 2 expression. J Exp Med 1996; 184:557-67
20. Kern P, Hemmer CJ, Van Damme J, Gruss HJ, Dietrich M. Elevated tumor necrosis factor alpha and interleukin-6 serum levels as markers for complicated Plasmodium falciparum malaria. Am J Med 1989; 87:139-43
21. Day NP, Hien TT, Schollaardt T et al. The prognostic and pathophysiologic role of pro- and antiinflammatory cytokines in severe malaria. J Infect Dis 1999; 180:1288-97
22. Amani V, Vigario AM, Belnoue E et al. Involvement of IFN-gamma receptor-medicated signaling in pathology and anti-malarial immunity induced by Plasmodium berghei infection. Eur J Immunol 2000; 30:1646-55
23. Su Z, Stevenson MM. Central role of endogenous gamma interferon in protective immunity against blood-stage Plasmodium chabaudi AS infection. Infect Immun 2000; 68:4399-406
24. Meding SJ, Cheng SC, Simon-Haarhaus B, Langhorne J. Role of gamma interferon during infection with Plasmodium chabaudi chabaudi. Infect Immun 1990; 58:3671-8
25. Luty AJ, Lell B, Schmidt-Ott R et al. Interferon-gamma responses are associated with resistance to reinfection with Plasmodium falciparum in young African children. J Infect Dis 1999; 179:980-8
26. Torre D, Giola M, Speranza F, Matteelli A, Basilico C, Biondi G. Serum levels of interleukin-18 in patients with uncomplicated Plasmodium falciparum malaria. Eur Cytokine Netw 2001; 12:361-4
27. Torre D, Speranza F, Giola M, Matteelli A, Tambini R, Biondi G. Role of Th1 and Th2 cytokines in immune response to uncomplicated Plasmodium falciparum malaria. Clin Diagn Laboratory Immunol 2002; 9:348-51
28. Winkler S, Willheim M, Baier K et al. Frequency of cytokine-producing T cells in patients of different age groups with Plasmodium falciparum malaria. J Infect Dis 1999; 179:209-16
29. Riley EM, Jakobsen PH, Allen SJ et al. Immune response to soluble exoantigens of Plasmodium falciparum may contribute to both pathogenesis and protection in clinical malaria: evidence from a longitudinal, prospective study of semi-immune African children. Eur J Immunol 1991; 21:1019-25
30. Mshana RN, Boulandi J, Mshana NM, Mayombo J, Mendome G. Cytokines in the pathogenesis of malaria: levels of IL-I beta, IL-4, IL-6, TNF-alpha and IFN-gamma in plasma of healthy individuals and malaria patients in a holoendemic area. J Clin Laboratory Immunol 1991; 34:131-9
31. Rhee MS, Akanmori BD, Waterfall M, Riley EM. Changes in cytokine production associated with acquired immunity to Plasmodium falciparum malaria. Clin Exp Immunol 2001; 126:503-10
32. Chizzolini C, Grau GE, Geinoz A, Schrijvers D. T lymphocyte interferon-gamma production induced by Plasmodium falciparum antigen is high in recently infected non-immune and low in immune subjects. Clin Exp Immunol 1990; 79:95-9
33. Erunkulu OA, Hill AV, Kwiatkowski DP et al. Severe malaria in Gambian children is not due to lack of previous exposure to malaria. Clin Exp Immunol 1992; 89:296-300
34. Riley EM. Is T-cell priming required for initiation of pathology in malaria infections? Immunol Today 1999; 20:228-33
35. Sanni LA, Thomas SR, Tattam BN et al. Dramatic changes in oxidative tryptophan metabolism along the kynurenine pathway in experimental cerebral and noncerebral malaria. Am J Pathol 1998; 152:611-9.
36. Medana IM, Hien TT, Day NP et al. The clinical significance of cerebrospinal fluid levels of kynurenine pathway metabolites and lactate in severe malaria. J Infect Dis 2002; 185:650-6
37. Baird JK, Masbar S, Basri H, Tirtokusumo S, Subianto B, Hoffman SL. Age-dependent susceptibility to severe disease with primary exposure to Plasmodium falciparum. J Infect Dis 1998; 178:592-5
38. Dick S, Waterfall M, Currie J, Maddy A, Riley E. Naive human alpha beta T cells respond to membrane-associated components of malaria-infected erythrocytes by proliferation and production of interferon-gamma. Immunology 1996; 88:412-20
39. Waterfall M, Black A, Riley E. Gamma delta+ T cells preferentially respond to live rather than killed malaria parasites. Infect Immun 1998; 66:2393-8
40. Currier J, Sattabongkot J, Good MF. 'Natural' T cells responsive to malaria. evidence implicating immunological cross-reactivity in the maintenance of TCR alpha beta+ malaria-specific responses from non-exposed donors. Int Immunol 1992; 4:985-94
41. Goodier MR, Lundqvist C, Hammarstrom ML, Troye-Blomberg M, Langhorne J. Cytokine profiles for human V gamma 9+ T cells stimulated by Plasmodium falciparum. Parasite Immunol 1995; 17:413-23
42. Zevering Y, Amante F, Smillie A et al. High frequency of malaria-specific T cells in non-exposed humans. Eur J Immunol 1992; 22:689-96
43. Fell AH, Currier J, Good MF. Inhibition of Plasmodium falciparum growth in vitro by CD4+ and CD8+ T cells from non-exposed donors. Parasite Immunol 1994; 16:579-86
44. De Souza JB, Williamson KH, Otani T, Playfair JH. Early gamma interferon responses in lethal and nonlethal murine blood-stage malaria. Infect Immun 1997; 65:1593-8
45. Choudhury HR, Sheikh NA, Bancroft GJ, Katz DR, De Souza JB. Early nonspecific immune responses and immunity to blood-stage non-lethal Plasmodium yoelii malaria. Infect Immun 2000; 68:6127-32
46. Schofield L, Hackett F. Signal transduction in host cells by a glycosylphosphatidylinositol toxin of malaria parasites. J Exp Med 1993; 177:145-53
47. Mohan K, Moulin P, Stevenson MM. Natural killer cell cytokine production, not cytotoxicity, contributes to resistance against blood-stage Plasmodium chabaudi AS infection. J Immunol 1997; 159:4990-8
48. Scragg IG, Hensmann M, Bate CA, Kwiatkowski D. Early cytokine induction by Plasmodium falciparum is not a classical endotoxin-like process. Eur J Immunol 1999; 29:2636-44
49. Artavanis-Tsakonas K, Riley EM. Innate immune response to malaria. rapid induction of IFN-gamma from human NK cells by live Plasmodium falciparum-infected erythrocytes. J Immunol 2002; 169:2956-63
50. Hensmann M, Kwiatkowski D. Cellular basis of early cytokine response to Plasmodium falciparum. Infect Immun 2001; 69:2364-71
51. Carnaud C, Lee D, Donnars O et al. Cutting edge. Cross-talk between cells of the innate immune system: NKT cells rapidly activate NK cells. J Immunol 1999; 163:4647-50
52. Urban BC, Willcox N, Roberts DJ. A role for CD36 in the regulation of dendritic cell function. Proc Natl Acad Sci USA 2001; 98:8750-5
53. Ocana-Morgner C, Mota MM, Rodriguez A. Malaria blood stage suppression of liver stage immunity by dendritic cells. J Exp Med 2003; 197:143-51
54. Seixas E, Cross C, Quin S, Langhorne J. Direct activation of dendritic cells by the malaria parasite, Plasmodium chabaudi chabaudi. Eur J Immunol 2001; 31:2970-8
55. 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; 418:785-9
56. Naik RS, Branch OH, Woods AS et al. Glycosylphosphatidylinositol anchors of Plasmodium falciparum: molecular characterization and naturally elicited antibody response that may provide immunity to malaria pathogenesis. J Exp Med 2000; 192:1563-76
57. de Souza JB, Todd J, Krishegowda G, Gowda DC, Kwiatkowski D, Riley EM. Prevalence and boosting of antibodies to Plasmodium falciparum glycosylphosphatidylinositols and evaluation of their association with protection from mild and severe clinical malaria. Infect Immun 2002; 70:5045-51
58. Omer FM, Kurtzhals JA, Riley EM. Maintaining the immunological balance in parasitic infections: a role for TGF-beta? Parasitol Today 2000; 16:18-23
59. Linke A, Kuhn R, Muller W, Honarvar N, Li C, Langhorne J. Plasmodium chabaudi chabaudi, differential susceptibility of gene-targeted mice deficient in IL-10 to an erythrocytic-stage infection. Exp Parasitol 1996; 84:253-63
60. Omer FM, Riley EM. Transforming growth factor beta production is inversely correlated with severity of murine malaria infection. J Exp Med 1998; 188:39-48
61. Tsutsui N, Kamiyama T. Transforming growth factor beta-induced failure of resistance to infection with blood-stage Plasmodium chabaudi in mice. Infect Immun 1999; 67:2306-11
62. Othoro C, Lal AA, Nahlen B, Koech D, Orago AS, Udhayakumar V. A low interleukin-10 tumor necrosis factor-alpha ratio is associated with malaria anemia in children residing in a holoendemic malaria region in western Kenya. J Infect Dis 1999; 179:279-82
63. Udomsangpetch R, Chivapat S, Viriyavejakul P et al. Involvement of cytokines in the histopathology of cerebral malaria. Am J Trop Med Hyg 1997; 57:501-6.
64. Aikawa M, Iseki M, Barnwell JW, Taylor D, Oo MM, Howard RJ. The pathology of human cerebral malaria. Am J Trop Med Hyg 1990; 43:30-7
65. Tongren JE, Yang C, Collins WE, Sullivan JS, Lal AA, Xiao L. Expression of proinflammatory cytokines in four regions of the brain in Macaque mulatta (rhesus) monkeys infected with Ptasmodium coatneyi. Am J Trop Med Hyg 2000; 62:530-4
66. Rest JR. Cerebral malaria in inbred mice. I. A new model and its pathology. Trans R Soc Trop Med Hyg 1982; 76:410-5
67. Dodoo D, Omer FM, Todd J, Akanmori BD, Koram KA, Riley EM. Absolute levels and ratios of proinflammatory and anti-inflammatory cytokine production in vitro predict clinical immunity to Plasmodium falciparum malaria. J Infect Dis 2002; 185:971-9
68. Riley EM, Wagner GE, Akanmori BD, Koram KA. Do maternally acquired antibodies protect infants from malaria infection? Parasite Immunol 2001; 23:51-9
69. Collins WE, Jeffery GM. A retrospective examination of sporozoite-and trophozoite-induced infections with Plasmodium falciparum in patients previously infected with heterologous species of Plasmodium: effect on development of parasitologic and clinical immunity. Am J Trop Med Hyg 1999; 61:36-43.