Insights into the immunopathogenesis of malaria using mouse models

Expert Reviews in Molecular Medicine

Volumn 8, Issue 6, 2006, Pages 1-22

  Lamb, Tracey J ^a   Brown, Douglas E ^a   Potocnik, Alexandre J ^a   Langhorne, Jean ^a  

^a NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN E; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 12; INTERLEUKIN 12P40; INTERLEUKIN 13; INTERLEUKIN 1BETA; INTERLEUKIN 23; INTERLEUKIN 4; LEUKOCYTE ANTIGEN; MALARIA VACCINE; TUMOR NECROSIS FACTOR ALPHA;

ANEMIA; BRAIN MALARIA; CACHEXIA; CELL ACTIVATION; CELL DAMAGE; CELL SPECIFICITY; CORRELATION ANALYSIS; CYTOKINE PRODUCTION; DISEASE SEVERITY; ENDOTHELIUM CELL; ERYTHROCYTE DEFORMABILITY; GENETIC POLYMORPHISM; GENETIC VARIABILITY; HEMOLYSIS; HOST PARASITE INTERACTION; HOST RESISTANCE; HUMAN; IMMUNE RESPONSE; IMMUNOPATHOGENESIS; IMMUNOPATHOLOGY; INFLAMMATION; MALARIA; MEDICAL RESEARCH; NONHUMAN; PARASITE VIRULENCE; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; REVIEW; RISK ASSESSMENT; SIGNAL TRANSDUCTION; TH2 CELL; THERMOREGULATION; UPREGULATION;

ANEMIA; ANIMALS; DISEASE MODELS, ANIMAL; HOST-PARASITE RELATIONS; HUMANS; MALARIA; MICE; PLASMODIUM;

ANIMALIA; PLASMODIUM FALCIPARUM;

EID: 33645233847     PISSN: 14623994     EISSN: 14623994     Source Type: Journal    
DOI: 10.1017/S1462399406010581     Document Type: Review

References (174)

1. WHO (2006) Roll Back Malaria. http://mosquito.who.int/cmc_upload/0/000/ 015/372/RBMInfosheet_1.htm
2. Snow, R.W. et al. (1999) Estimating mortality, morbidity and disability due to malaria among Africa's non-pregnant population. Bull World Health Organ 77, 624-640, PubMed: 10516785
3. Engwerda, C. et al. (2005) Experimental models of cerebral malaria. Curr Top Microbiol Immunol 297, 103-143, PubMed: 16265904
4. Craig, A. and Scherf, A. (2001) Molecules on the surface of the Plasmodium falciparum infected erythrocyte and their role in malaria pathogenesis and immune evasion. Mol Biochem Parasitol 115, 129-143, PubMed: 11420100
5. Maeno, Y. et al. (2000) IgE deposition in brain microvessels and on parasitized erythrocytes from cerebral malaria patients. Am J Trop Med Hyg 63, 128-132, PubMed: 11388503
6. Rowe, J.A. et al. (1997) P. falciparum rosetting mediated by a parasite-variant erythrocyte membrane protein and complement-receptor 1. Nature 388, 292-295, PubMed: 9230440
7. Cockburn, I.A. et al. (2004) A human complement receptor 1 polymorphism that reduces Plasmodium falciparum rosetting confers protection against severe malaria. Proc Natl Acad Sci U S A 101, 272-277, PubMed: 14694201
8. Rowe, J.A. et al. (2002) Short report: Positive correlation between rosetting and parasitemia in Plasmodium falciparum clinical isolates. Am J Trop Med Hyg 66, 458-460, PubMed: 12201576
9. WHO (1990) Severe and complicated malaria. World Health Organization, Division of Control of Tropical Diseases. Trans R Soc Trop Med Hyg 84 Suppl 2, 1-65, PubMed: 2219249
10. Turner, G. (1997) Cerebral malaria. Brain Pathol 7, 569-582, PubMed: 9034566
11. Taylor, T.E. et al. (2004) Differentiating the pathologies of cerebral malaria by postmortem parasite counts. Nat Med 10, 143-145, PubMed: 14745442
12. Grau, G.E. et al. (2003) Platelet accumulation in brain microvessels in fatal pediatric cerebral malaria. J Infect Dis 187, 461-466, PubMed: 12552430
13. Patnaik, J.K. et al. (1994) Vascular clogging, mononuclear cell margination, and enhanced vascular permeability in the pathogenesis of human cerebral malaria. Am J Trop Med Hyg 51, 642-647, PubMed: 7985757
14. Clark, I.A. et al. (2003) Tissue distribution of migration inhibitory factor and inducible nitric oxide synthase in falciparum malaria and sepsis in African children. Malar J 2, 6, PubMed: 12716455
15. English, M. and Newton, C.R. (2002) Malaria: Pathogenicity and disease. Chem Immunol 80, 50-69, PubMed: 12058651
16. Anstey, N.M. et al. (2002) Pulmonary manifestations of uncomplicated falciparum and vivax malaria: Cough, small airways obstruction, impaired gas transfer, and increased pulmonary phagocytic activity. J Infect Dis 185, 1326-1334, PubMed: 12001051
17. Maitland, K. and Marsh, K. (2004) Pathophysiology of severe malaria in children. Acta Trop 90, 131-140, PubMed: 15177139
18. Mackintosh, C.L., Beeson, J.G. and Marsh, K. (2004) Clinical features and pathogenesis of severe malaria. Trends Parasitol 20, 597-603, PubMed: 15522670
19. English, M. et al. (1997) Acidosis in severe childhood malaria. Qjm 90, 263-270, PubMed: 9307760
20. Maguire, G.P. et al. (2005) Lung injury in uncomplicated and severe falciparum malaria: A longitudinal study in papua, Indonesia. J Infect Dis 192, 1966-1974, PubMed: 16267769
21. Maitland, K., Bejon, P. and Newton, C.R. (2003) Malaria. Curr Opin Infect Dis 16, 389-395, PubMed: 14501990
22. Bojang, K.A. et al. (1997) Management of severe malarial anaemia in Gambian children. Trans R Soc Trop Med Hyg 91, 557-561, PubMed: 9463667
23. Jakeman, G.N. et al. (1999) Anaemia of acute malaria infections in non-immune patients primarily results from destruction of uninfected erythrocytes. Parasitology 119 (Pt 2), 127-133, PubMed: 10466119
24. Snow, R.W. et al. (2005) The global distribution of clinical episodes of Plasmodium falciparum malaria. Nature 434, 214-217, PubMed: 15759000
25. Beale, G.H., Carter, R. and Walliker, D. (1978) Genetics. In Rodent Malaria (Killick-Kendrick, R. and Peters, W., eds), pp. 213-245, Academic Press Inc., London
26. Landau, I. and Boulard, Y. (1978) Life cycles and morphology. In Rodent Malaria (Killick-Kendrick, R. and Peters, W., eds), pp. 53-84, Academic Press Inc., London
27. Kern, P. et al. (1989) Elevated tumor necrosis factor alpha and interleukin-6 serum levels as markers for complicated Plasmodium falciparum malaria. Am J Med 87, 139-143, PubMed: 2667356
28. Lyke, K.E. et al. (2004) Serum levels of the proinflammatory cytokines interleukin-1 beta (IL-1beta), IL-6, IL-8, IL-10, tumor necrosis factor alpha, and IL-12(p70) in Malian children with severe Plasmodium falciparum malaria and matched uncomplicated malaria or healthy controls. Infect Immun 72, 5630-5637, PubMed: 15385460
29. Mshana, R.N. et al. (1991) 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 Lab Immunol 34, 131-139, PubMed: 1667945
30. Malaguarnera, L. et al. (2002) Plasma levels of interleukin-12 (IL-12), interleukin-18 (IL-18) and transforming growth factor beta (TGF-beta) in Plasmodium falciparum malaria. Eur Cytokine Netw 13, 425-430, PubMed: 12517727
31. Chaiyaroj, S.C. et al. (2004) Reduced levels of transforming growth factor-beta1, interleukin-12 and increased migration inhibitory factor are associated with severe malaria. Acta Trop 89, 319-327, PubMed: 14744558
32. Kojima, S. et al. (2004) A potential role of interleukin 18 in severe falciparum malaria. Acta Trop 89, 279-284, PubMed: 14744554
33. Artavanis-Tsakonas, K. and Riley, E.M. (2002) Innate immune response to malaria: Rapid induction of IFN-gamma from human NK cells by live Plasmodium falciparum-infected erythrocytes. J Immunol 169, 2956-2963, PubMed: 12218109
34. Baratin, M. et al. (2005) Natural killer cell and macrophage cooperation in MyD88-dependent innate responses to Plasmodium falciparum. Proc Natl Acad Sci U S A 102, 14747-14752, PubMed: 16203971
35. Artavanis-Tsakonas, K. et al. (2003) Activation of a subset of human NK cells upon contact with Plasmodium falciparum-infected erythrocytes. J Immunol 171, 5396-5405, PubMed: 14607943
36. Goodier, M.R. et al. (1995) Cytokine profiles for human V gamma 9+ T cells stimulated by Plasmodium falciparum. Parasite Immunol 17, 413-423, PubMed: 7501422
37. Jones, S.M., Goodier, M.R. and Langhorne, J. (1996) The response of gamma delta T cells to Plasmodium falciparum is dependent on activated CD4+ T cells and the recognition of MHC class I molecules. Immunology 89, 405-412, PubMed: 8958054
38. Thuma, P.E. et al. (1996) Serum neopterin, interleukin-4, and interleukin-6 concentrations in cerebral malaria patients and the effect of iron chelation therapy. Am J Trop Med Hyg 54, 164-168, PubMed: 8619442
39. Perlmann, H. et al. (1994) IgE elevation and IgE anti-malarial antibodies in Plasmodium falciparum malaria: Association of high IgE levels with cerebral malaria. Clin Exp Immunol 97, 284-292, PubMed: 8050178
40. Kwiatkowski, D. et al. (1990) TNF concentration in fatal cerebral, non-fatal cerebral, and uncomplicated Plasmodium falciparum malaria. Lancet 336, 1201-1204, PubMed: 1978068
41. McGuire, W. et al. (1994) Variation in the TNF-alpha promoter region associated with susceptibility to cerebral malaria. Nature 371, 508-510, PubMed: 7935762
42. Knight, J.C. et al. (1999) A polymorphism that affects OCT-1 binding to the TNF promoter region is associated with severe malaria. Nat Genet 22, 145-150, PubMed: 10369255
43. Heddini, A. (2002) Malaria pathogenesis: A jigsaw with an increasing number of pieces. Int J Parasitol 32, 1587-1598, PubMed: 12435443
44. Krishna, S. et al. (1994) Lactic acidosis and hypoglycaemia in children with severe malaria: Pathophysiological and prognostic significance. Trans R Soc Trop Med Hyg 88, 67-73, PubMed: 8154008
45. McGuire, W. et al. (1998) Levels of tumour necrosis factor and soluble TNF receptors during malaria fever episodes in the community. Trans R Soc Trop Med Hyg 92, 50-53, PubMed: 9692151
46. Kwiatkowski, D. et al. (1993) Anti-TNF therapy inhibits fever in cerebral malaria. Q J Med 86, 91-98, PubMed: 8329024
47. Langhorne, J., Quin, S.J. and Sanni, L.A. (2002) Mouse models of blood-stage malaria infections: Immune responses and cytokines involved in protection and pathology. Chem Immunol 80, 204-228, PubMed: 12058640
48. Peyron, F. et al. (1994) High levels of circulating IL-10 in human malaria. Clin Exp Immunol 95, 300-303, PubMed: 8306505
49. Kurtzhals, J.A. et al. (1998) Low plasma concentrations of interleukin 10 in severe malarial anaemia compared with cerebral and uncomplicated malaria. Lancet 351, 1768-1772, PubMed: 9635949
50. Nussenblatt, V et al. (2001) Anemia and interleukin-10, tumor necrosis factor alpha, and erythropoietin levels among children with acute, uncomplicated Plasmodium falciparum malaria. Clin Diagn Lab Immunol 8, 1164-1170, PubMed: 11687458
51. Othoro, C. et al. (1999) 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 179, 279-282, PubMed: 9841855
52. Dodoo, D. et al. (2002) 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, PubMed: 11920322
53. Li, C. et al. (2003) Pathology of Plasmodium chabaudi chabaudi infection and mortality in interleukin-10-deficient mice are ameliorated by anti-tumor necrosis factor alpha and exacerbated by anti-transforming growth factor beta antibodies. Infect Immun 71, 4850-4856, PubMed: 12933825
54. Omer, F.M. and Riley, E.M. (1998) Transforming growth factor beta production is inversely correlated with severity of murine malaria infection. J Exp Med 188, 39-48, PubMed: 9653082
55. Omer, F.M., de Souza, J.B. and Riley, E.M. (2003) Differential induction of TGF-beta regulates proinflammatory cytokine production and determines the outcome of lethal and nonlethal Plasmodium yoelii infections. J Immunol 171, 5430-5436, PubMed: 14607947
56. Walther, M. et al. (2005) Upregulation of TGF-beta, FOXP3, and CD4+CD25+ regulatory T cells correlates with more rapid parasite growth in human malaria infection. Immunity 23, 287-296, PubMed: 16169501
57. Hisaeda, H. et al. (2004) Escape of malaria parasites from host immunity requires CD4+ CD25+ regulatory T cells. Nat Med 10, 29-30, PubMed: 14702631
58. Langhorne, J. et al. (2004) Dendritic cells, proinflammatory responses, and antigen presentation in a rodent malaria infection. Immunol Rev 201, 35-47, PubMed: 15361231
59. Korbel, D.S., Finney, O.C. and Riley, E.M. (2004) Natural killer cells and innate immunity to protozoan pathogens. Int J Parasitol 34, 1517-1528, PubMed: 15582528
60. O'Neill, L.A. (2004) TLRs: Professor Mechnikov, sit on your hat. Trends Immunol 25, 687-693, PubMed: 15530840
61. Pichyangkul, S. et al. (2004) Malaria blood stage parasites activate human plasmacytoid dendritic cells and murine dendritic cells through a Toll-like receptor 9-dependent pathway. J Immunol 172, 4926-4933, PubMed: 15067072
62. Krishnegowda, G. et al. (2005) Induction of proinflammatory responses in macrophages by the glycosylphosphatidylinositols of Plasmodium falciparum: Cell signaling receptors, glycosylphosphatidylinositol (GPI) structural requirement, and regulation of GPI activity. J Biol Chem 280, 8606-8616, PubMed: 15623512
63. Adachi, K. et al. (2001) Plasmodium berghei infection in mice induces liver injury by an IL-12-and toll-like receptor/myeloid differentiation factor 88-dependent mechanism. J Immunol 167, 5928-5934, PubMed: 11698470
64. Schofield, L. and Hackett, F. (1993) Signal transduction in host cells by a glycosylphosphatidylinositol toxin of malaria parasites. J Exp Med 177, 145-153, PubMed: 8418196
65. Coban, C. et al. (2005) Toll-like receptor 9 mediates innate immune activation by the malaria pigment hemozoin. J Exp Med 201, 19-25, PubMed: 15630134
66. Yarovinsky, F. et al. (2005) TLR11 activation of dendritic cells by a protozoan profilin-like protein. Science 308, 1626-1629, PubMed: 15860593
67. Hoebe, K. et al. (2005) CD36 is a sensor of diacylglycerides. Nature 433, 523-527, PubMed: 15690042
68. Cross, C.E. and Langhorne, J. (1998) Plasmodium chabaudi chabaudi (AS): inflammatory cytokines and pathology in an erythrocytic-stage infection in mice. Exp Parasitol 90, 220-229, PubMed: 9806866
69. Cordeiro, R.S. et al. (1983) Plasmodium berghei: Physiopathological changes during infections in mice. Ann Trop Med Parasitol 77, 455-465, PubMed: 6362586
70. Amani, V. et al. (1998) Cloned lines of Plasmodium berghei ANKA differ in their abilities to induce experimental cerebral malaria. Infect Immun 66, 4093-4099, PubMed: 9712753
71. Sherry, B.A. et al. (1995) Malaria-specific metabolite hemozoin mediates the release of several potent endogenous pyrogens (TNF, MIP-1 alpha, and MIP-1 beta) in vitro, and altered thermoregulation in vivo. J Inflamm 45, 85-96, PubMed: 7583361
72. Piguet, P.F., Kan, C.D. and Vesin, C. (2002) Role of the tumor necrosis factor receptor 2 (TNFR2) in cerebral malaria in mice. Lab Invest 82, 1155-1166, PubMed: 12218076
73. Li, C. and Langhorne, J. (2000) Tumor necrosis factor alpha p55 receptor is important for development of memory responses to blood-stage malaria infection. Infect Immun 68, 5724-5730, PubMed: 10992477
74. Wajant, H., Pfizenmaier, K. and Scheurich, P. (2003) Tumor necrosis factor signaling. Cell Death Differ 10, 45-65, PubMed: 12655295
75. Leon, L.R. (2002) InviteS review: Cytokine regulation of fever: studies using gene knockout mice. J Appl Physiol 92, 2648-2655, PubMed: 12015385
76. Utsuyama, M. and Hirokawa, K. (2002) Differential expression of various cytokine receptors in the brain after stimulation with LPS in young and old mice. Exp Gerontol 37, 411-420, PubMed: 11772528
77. de Souza, J.B. and Riley, E.M. (2002) Cerebral malaria: The contribution of studies in animal models to our understanding of immunopathogenesis. Microbes Infect 4, 291-300, PubMed: 11909739
78. Bauer, P.R. et al. (2002) Regulation of endothelial cell adhesion molecule expression in an experimental model of cerebral malaria. Microcirculation 9, 463-470, PubMed: 12483543
79. Franke-Fayard, B. et al. (2005) Murine malaria parasite sequestration: CD36 is the major receptor, but cerebral pathology is unlinked to sequestration. Proc Natl Acad Sci U S A 102, 11468-11473, PubMed: 16051702
80. Belnoue, E. et al. (2003) CCR5 deficiency decreases susceptibility to experimental cerebral malaria. Blood 101, 4253-4259, PubMed: 12560237
81. Pais, T.F. and Chatterjee, S. (2005) Brain macrophage activation in murine cerebral malaria precedes accumulation of leukocytes and CD8+ T cell proliferation. J Neuroimmunol 163, 73-83, PubMed: 15885309
82. Curfs, J.H. et al. (1993) Tumour necrosis factor-alpha and macrophages in Plasmodium berghei-induced cerebral malaria. Parasitology 107 (Pt 2) 125-134, PubMed: 8414666
83. Belnoue, E. et al. (2002) On the pathogenic role of brain-sequestered alphabeta CD8+ T cells in experimental cerebral malaria. J Immunol 169, 6369-6375, PubMed: 12444144
84. Hanum, P.S., Hayano, M. and Kojima, S. (2003) Cytokine and chemokine responses in a cerebral malaria-susceptible or -resistant strain of mice to Plasmodium berghei ANKA infection: Early chemokine expression in the brain. Int Immunol 15, 633-640, PubMed: 12697663
85. Piguet, P.F. et al. (2001) Role of CD40-CVD40L in mouse severe malaria. Am J Pathol 159, 733-742, PubMed: 11485931
86. Lou, J. et al. (1998) Differential reactivity of brain microvascular endothelial cells to TNF reflects the genetic susceptibility to cerebral malaria. Eur J Immunol 28, 3989-4000, PubMed: 9862335
87. Engwerda, C.R. et al. (2002) Locally up-regulated lymphotoxin alpha, not systemic tumor necrosis factor alpha, is the principle mediator of murine cerebral malaria. J Exp Med 195, 1371-1377, PubMed: 12021316
88. Sanni, L.A. et al. (1999) Are reactive oxygen species involved in the pathogenesis of murine cerebral malaria? J Infect Dis 179, 217-222, PubMed: 9841842
89. Potter, S.M. et al. (2005) Phagocyte-derived reactive oxygen species do not influence the progression of murine blood-stage malaria infections. Infect Immun 73, 4941-4947, PubMed: 16041008
90. Favre, N., Ryffel, B. and Rudin, W. (1999) The development of murine cerebral malaria does not require nitric oxide production. Parasitology 118 (Pt 2), 135-138, PubMed: 10028526
91. Favre, N. et al. (1999) Role of ICAM-1 (CD54) in the development of murine cerebral malaria. Microbes Infect 1, 961-968, PubMed: 10617927
92. Sun, G. et al. (2003) Inhibition of platelet adherence to brain microvasculature protects against severe Plasmodium berghei malaria. Infect Immun 71, 6553-6561, PubMed: 14573677
93. Mackinnon, M.J., Walker, P.R. and Rowe, J.A. (2002) Plasmodium chabaudi: rosetting in a rodent malaria model. Exp Parasitol 101, 121-128, PubMed: 12427466
94. Nitcheu, J. et al. (2003) Perforin-dependent brain-infiltrating cytotoxic CD8+ T lymphocytes mediate experimental cerebral malaria pathogenesis. J Immunol 170, 2221-2228, PubMed: 12574396
95. Yanez, D.M. et al. (1996) Participation of lymphocyte subpopulations in the pathogenesis of experimental murine cerebral malaria. J Immunol 157, 1620-1624, PubMed: 8759747
96. Nussenzweig, V.S., Cochrane, A.H. and Lustig, H.J. (1978) Immunological responses. In Rodent Malaria (Killick-Kendrick, R. and Peters, W., eds), pp. 247-307, Academic Press Inc., London
97. Gilks, C.F., Walliker, D. and Newbold, C.I. (1990) Relationships between sequestration, antigenic variation and chronic parasitism in Plasmodium chabaudi chabaudi - a rodent malaria model. Parasite Immunol 12, 45-64, PubMed: 2314922
98. Cox, J., Semoff, S. and Hommel, M. (1987) Plasmodium chabaudi: A rodent malaria model for in-vivo and in-vitro cytoadherence of malaria parasites in the absence of knobs. Parasite Immunol 9, 543-561, PubMed: 3684327
99. Desowitz, R.S. and Barnwell, J.W. (1976) Plasmodium berghei: Deep vascular sequestration of young forms in the heart and kidney of the white rat. Ann Trop Med Parasitol 70, 475-476, PubMed: 793548
100. Coquelin, F. et al. (1999) Final stage of maturation of the erythrocytic schizonts of rodent Plasmodium in the lungs. C R Acad Sci III 322, 55-62, PubMed: 10047954
101. Mota, M.M. et al. (2000) Plasmodium chabaudi-infected erythrocytes adhere to CD36 and bind to microvascular endothelial cells in an organ-specific way. Infect Immun 68, 4135-4144, PubMed: 10858230
102. Vuong, P.N. et al. (1999) Development of irreversible lesions in the brain, heart and kidney following acute and chronic murine malaria infection. Parasitology 119 (Pt 6), 543-553, PubMed: 10633915
103. Eiam-Ong, S. (2003) Malarial nephropathy. Semin Nephrol 23, 21-33, PubMed: 12563598
104. Sinniah, R., Rui-Mei, L. and Kara, A. (1999) Up-regulation of cytokines in glomerulonephritis associated with murine malaria infection. Int J Exp Pathol 80, 87-95, PubMed: 10469263
105. Rui-Mei, L., Kara, A.U. and Sinniah, R. (1998) Dysregulation of cytokine expression in tubulointerstitial nephritis associated with murine malaria. Kidney Int 53, 845-852, PubMed: 9551390
106. Suzuki, Y. et al. (2003) Pre-existing glomerular immune complexes induce polymorphonuclear cell recruitment through an Fc receptor-dependent respiratory burst: Potential role in the perpetuation of immune nephritis. J Immunol 170, 3243-3253, PubMed: 12626583
107. Rencricca, N.J. and Coleman, R.M. (1979) Altered erythropoiesis during the course of virulent murine malaria. Proc Soc Exp Biol Med 162, 424-428, PubMed: 390536
108. Yap, G.S. and Stevenson, M.M. (1994) Blood transfusion alters the course and outcome of Plasmodium chabaudi AS infection in mice. Infect Immun 62, 3761-3765, PubMed: 8063391
109. Chang, K.H., Tam, M. and Stevenson, M.M. (2004) Modulation of the course and outcome of blood-stage malaria by erythropoietin-induced reticulocytosis. J Infect Dis 189, 735-743, PubMed: 14767829
110. Chang, K.H., Tam, M. and Stevenson, M.M. (2004) Inappropriately low reticulocytosis in severe malarial anemia correlates with suppression in the development of late erythroid precursors. Blood 103, 3727-3735, PubMed: 14739226
111. Burgmann, H. et al. (1996) Serum levels of erythropoietin in acute Plasmodium falciparum malaria. Am J Trop Med Hyg 54, 280-283, PubMed: 8600766
112. Abdalla, S. et al. (1980) The anaemia of P. falciparum malaria. Br J Haematol 46, 171-183, PubMed: 7000157
113. Srichaikul, T., Panikbutr, N. and Jeumtrakul, P. (1967) Bone-marrow changes in human malaria. Ann Trop Med Parasitol 61, 40-51, PubMed: 6051537
114. Price, R.N. et al. (2001) Factors contributing to anemia after uncomplicated falciparum malaria. Am J Trop Med Hyg 65, 614-622, PubMed: 11716124
115. Evans, K.J. et al. (2006) Severe malarial anemia of low parasite burden in rodent models results from accelerated clearance of uninfected erythrocytes. Blood 107, 1192-1199, PubMed: 16210332
116. Wickramasinghe, S.N. et al. (1987) The bone marrow in human cerebral malaria: Parasite sequestration within sinusoids. Br J Haematol 66, 295-306, PubMed: 3304391
117. Shi, Q. et al. (2005) Alteration in host cell tropism limits the efficacy of immunization with a surface protein of malaria merozoites. Infect Immun 73, 6363-6371, PubMed: 16177307
118. del Portillo, H.A. et al. (2004) Variant genes and the spleen in Plasmodium vivax malaria. Int J Parasitol 34, 1547-1554, PubMed: 15582531
119. Weiss, L., Johnson, J. and Weidanz, W. (1989) Mechanisms of splenic control of murine malaria: Tissue culture studies of the erythropoietic interplay of spleen, bone marrow, and blood in lethal (strain 17XL) Plasmodium yoelii malaria in BALB/c mice. Am J Trop Med Hyg 41, 135-143, PubMed: 2774062
120. Silverman, P.H., Schooley, J.C. and Mahlmann, L.J. (1987) Murine malaria decreases hemopoietic stem cells. Blood 69, 408-413, PubMed: 3801660
121. Yap, G.S. and Stevenson, M.M. (1992) Plasmodium chabaudi AS: erythropoietic responses during infection in resistant and susceptible mice. Exp Parasitol 75, 340-352, PubMed: 1426136
122. Miller, K.L. et al. (1989) Tumor necrosis factor alpha and the anemia associated with murine malaria. Infect Immun 57, 1542-1546, PubMed: 2707858
123. Yap, G.S. and Stevenson, M.M. (1994) Inhibition of in vitro erythropoiesis by soluble mediators in Plasmodium chabaudi AS malaria: lack of a major role for interleukin 1, tumor necrosis factor alpha, and gamma interferon. Infect Immun 62, 357-362, PubMed: 8300197
124. Linke, A. et al. (1996) Plasmodium chabaudi chabaudi: Differential susceptibility of gene-targeted mice deficient in IL-10 to an erythrocytic-stage infection. Exp Parasitol 84, 253-263, PubMed: 8932775
125. Mohan, K. and Stevenson, M.M. (1998) Dyserythropoiesis and severe anaemia associated with malaria correlate with deficient interleukin-12 production. Br J Haematol 103, 942-949, PubMed: 9886304
126. Mohan, K. and Stevenson, M.M. (1998) Interleukin-12 corrects severe anemia during blood-stage Plasmodium chabaudi AS in susceptible A/J mice. Exp Hematol 26, 45-52, PubMed: 9430513
127. Martiney, J.A. et al. (2000) Macrophage migration inhibitory factor release by macrophages after ingestion of Plasmodium chabaudi-infected erythrocytes: Possible role in the pathogenesis of malarial anemia. Infect Immun 68, 2259-2267, PubMed: 10722628
128. Villeval, J.L., Lew, A. and Metcalf, D. (1990) Changes in hemopoietic and regulator levels in mice during fatal or nonfatal malarial infections. I. Erythropoietic populations. Exp Parasitol 71, 364-374, PubMed: 2146141
129. Abdalla, S.H., Wickramasinghe, S.N. and Weatherall, D.J. (1984) The deoxyuridine suppression test in severe anaemia following Plasmodium falciparum malaria. Trans R Soc Trop Med Hyg 78, 60-63, PubMed: 6369652
130. Clark, I.A. and Chaudhri, G. (1988) Tumour necrosis factor may contribute to the anaemia of malaria by causing dyserythropoiesis and erythrophagocytosis. Br J Haematol 70, 99-103, PubMed: 3179231
131. Mackinnon, M.J. et al. (2000) Quantifying genetic and nongenetic contributions to malarial infection in a Sri Lankan population. Proc Natl Acad Sci U S A 97, 12661-12666, PubMed: 11035799
132. Marsh, K. and Snow, R.W. (1999) Malaria transmission and morbidity. Parassitologia 41, 241-246, PubMed: 10697862
133. Snow, R.W. et al. (1997) Relation between severe malaria morbidity in children and level of Plasmodium falciparum transmission in Africa. Lancet 349, 1650-1654, PubMed: 9186382
134. Min-Co, G. and Gros, P. (2005) Erythrocyte variants and the nature of their malaria protective effect. Cell Microbiol 7, 753-763, PubMed: 15888079
135. Fortin, A. et al. (1997) Genetic control of blood parasitaemia in mouse malaria maps to chromosome 8. Nat Genet 17, 382-383, PubMed: 9398835
136. Foote, S.J. et al. (1997) Mouse loci for malaria-induced mortality and the control of parasitaemia. Nat Genet 17, 380-381, PubMed: 9398834
137. Burt, R.A. et al. (1999) Temporal expression of an H2-linked locus in host response to mouse malaria. Immunogenetics 50, 278-285, PubMed: 10630291
138. Stevenson, M.M. et al. (1995) IL-12-induced protection against blood-stage Plasmodium chabaudi AS requires IFN-gamma and TNF-alpha and occurs via a nitric oxide-dependent mechanism. J Immunol 155, 2545-2556, PubMed: 7650384
139. Stevenson, M.M. et al. (1992) Macrophage activation during Plasmodium chabaudi AS infection in resistant C57BL/6 and susceptible A/J mice. Infect Immun 60, 1193-1201, PubMed: 1311705
140. Sam, H. and Stevenson, M.M. (1999) Early IL-12 p70, but not p40, production by splenic macrophages correlates with host resistance to blood-stage Plasmodium chabaudi AS malaria. Clin Exp Immunol 117, 343-349, PubMed: 10444268
141. Mohan, K., Moulin, P. and Stevenson, M.M. (1997) Natural killer cell cytokine production, not cytotoxicity, contributes to resistance against blood-stage Plasmodium chabaudi AS infection. J Immunol 159, 4990-4998, PubMed: 9366426
142. Tsutsui, N. and Kamiyama, T. (1999) Transforming growth factor beta-induced failure of resistance to infection with blood-stage Plasmodium chabaudi in mice. Infect Immun 67, 2306-2311, PubMed: 10225888
143. Gardner, J.P. et al. (1996) Variant antigens and endothelial receptor adhesion in Plasmodium falciparum. Proc Natl Acad Sci U S A 93, 3503-3508, PubMed: 8622966
144. Luxemburger, C. et al. (1997) The epidemiology of severe malaria in an area of low transmission in Thailand. Trans R Soc Trop Med Hyg 91, 256-262, PubMed: 9231189
145. Smith, T. et al. (2001) Prospective risk of morbidity in relation to malaria infection in an area of high endemicity of multiple species of Plasmodium. Am J Trop Med Hyg 64, 262-267, PubMed: 11463113
146. Maitland, K. et al. (1996) The interaction between Plasmodium falciparum and P. vivax in children on Espiritu Santo island, Vanuatu. Trans R Soc Trop Med Hyg 90, 614-620, PubMed: 9015495
147. Ofosu-Okyere, A. et al. (2001) Novel Plasmodium falciparum clones and rising clone multiplicities are associated with the increase in malaria morbidity in Ghanaian children during the transition into the high transmission season. Parasitology 123, 113-123, PubMed: 11510676
148. Mackinnon, M.J. and Read, A.F. (1999) Genetic relationships between parasite virulence and transission in the rodent malaria Plasmodium chabaudi. Evolution 53, 689-703
149. Allan, R.J. et al. (1995) Strain variation in tumor necrosis factor induction by parasites from children with acute falciparum malaria. Infect Immun 63, 1173-1175, PubMed: 7890368
150. Rowe, J.A. et al. (1998) Implications of mycoplasma contamination in Plasmodium falciparum cultures and methods for its detection and eradication. Mol Biochem Parasitol 92, 177-180, PubMed: 9574920
151. Robben, P.M. et al. (2004) Production of IL-12 by macrophages infected with Toxoplasma gondii depends on the parasite genotype. J Immunol 172, 3686-3694, PubMed: 15004172
152. Manca, C. et al. (2004) Differential monocyte activation underlies strain-specific Mycobacterium tuberculosis pathogenesis. Infect Immun 72, 5511-5514, PubMed: 15322056
153. Shear, H.L. et al. (1989) Role of IFN-gamma in lethal and nonlethal malaria in susceptible and resistant murine hosts. J Immunol 143, 2038-2044, PubMed: 2506274
154. Kobayashi, F. et al. (1996) Production of interleukin 10 during malaria caused by lethal and nonlethal variants of Plasmodium yoelii yoelii. Parasitol Res 82, 385-391, PubMed: 8738275
155. Jennings, V.M., Lal, A.A. and Hunter, R.L. (1998) Evidence for multiple pathologic and protective mechanisms of murine cerebral malaria. Infect Immun 66, 5972-5979, PubMed: 9826380
156. Mackinnon, M.J. and Read, A.F. (2004) Immunity promotes virulence evolution in a malaria model. PLoS Biol 2, E230, PubMed: 15221031
157. Gandon, S. et al. (2001) Imperfect vaccines and the evolution of pathogen virulence. Nature 414, 751-756, PubMed: 11742400
158. Dieckmann, U. et al., eds (2002) Adaptive Dynamics of Infectious Diseases: In Pursuit of Virulence Management (Cambridge Studies in Adaptive Dynamics), Cambridge University Press, Cambridge, UK
159. Maggio-Price, L., Brookoff, D. and Weiss, L. (1985) Changes in hematopoietic stem cells in bone marrow of mice with Plasmodium berghei malaria. Blood 66, 1080-1085, PubMed: 3902119
160. Asami, M. et al. (1992) A comparative study of the kinetic changes of hemopoietic stem cells in mice infected with lethal and non-lethal malaria. Int J Parasitol 22, 43-47, PubMed: 1563919
161. Sanni, L.A. et al. (2004) Cerebral edema and cerebral hemorrhages in interleukin-10-deficient mice infected with Plasmodium chabaudi. Infect Immun 72, 3054-3058, PubMed: 15102820
162. Chang, K.H. and Stevenson, M.M. (2004) Malarial anaemia: Mechanisms and implications of insufficient erythropoiesis during blood-stage malaria. Int J Parasitol 34, 1501-1516, PubMed: 15582527
163. Howard, R.J. and Mitchell, G.F. (1979) Accelerated clearance of uninfected red cells from Plasmodium berghei-infected mouse blood in normal mice. Aust J Exp Biol Med Sci 57, 455-457, PubMed: 548017
164. Hunter, K.W., Jr., Winkelstein, J.A. and Simpson, T.W. (1979) Serum opsonic activity in rodent malaria: Functional and immunochemical characteristics in vitro. J Immunol 123, 2582-2587, PubMed: 387873
165. Ubalee, R. et al. (2001) Strong association of a tumor necrosis factor-alpha promoter allele with cerebral malaria in Myanmar. Tissue Antigens 58, 407-410, PubMed: 11929592
166. McGuire, W. et al. (1999) Severe malarial anemia and cerebral malaria are associated with different tumor necrosis factor promoter alleles. J Infect Dis 179, 287-290, PubMed: 9841857
167. Kun, J.F. et al. (1998) Polymorphism in promoter region of inducible nitric oxide synthase gene and protection against malaria. Lancet 351, 265-266, PubMed: 9457101
168. Burgner, D. et al. (1998) Inducible nitric oxide synthase polymorphism and fatal cerebral malaria. Lancet 352, 1193-1194, PubMed: 9777841
169. Walley, A.J. et al. (2004) Interleukin-1 gene cluster polymorphisms and susceptibility to clinical malaria in a Gambian case-control study. Eur J Hum Genet 12, 132-138, PubMed: 14673470
170. Gyan, B. et al. (2002) Polymorphisms in interleukin-1beta and interleukin-1 receptor antagonist genes and malaria in Ghanaian children. Scand J Immunol 56, 619-622, PubMed: 12472674
171. Morahan, G. et al. (2002) A promoter polymorphism in the gene encoding interleukin-12 p40 (IL12B) is associated with mortality from cerebral malaria and with reduced nitric oxide production. Genes Immun 3, 414-418, PubMed: 12424623
172. Gyan, B.A. et al. (2004) Allelic polymorphisms in the repeat and promoter regions of the interleukin-4 gene and malaria severity in Ghanaian children. Clin Exp Immunol 138, 145-150, PubMed: 15373917
173. Ohashi, J. et al. (2003) A single-nucleotide substitution from C to T at position -1055 in the IL-13 promoter is associated with protection from severe malaria in Thailand. Genes Immun 4, 528-531, PubMed: 14551608
174. Hill, A.V. et al. (1991) Common west African HLA antigens are associated with protection from severe malaria. Nature 352, 595-600, PubMed: 1865923