Regulating immunity to malaria

Parasite Immunology

Volumn 28, Issue 1-2, 2006, Pages 35-49

  Riley, E M ^a   Wahl, S ^b   Perkins, D J ^c   Schofield, L ^d  

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

^b NATIONAL INSTITUTE OF DENTAL AND CRANIOFACIAL RESEARCH   (United States)

^c UNIVERSITY OF PITTSBURGH GRADUATE SCHOOL OF PUBLIC HEALTH   (United States)

^d WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

Author keywords

Anti toxic immunity; Glycosylphosphatidylinositol; IL 10; Nitric oxide; Regulatory T cell; TGF beta

Indexed keywords

GAMMA INTERFERON; GLYCOSYLPHOSPHATIDYLINOSITOL; INTERLEUKIN 12; MALARIA VACCINE; TUMOR NECROSIS FACTOR ALPHA; CYTOKINE; NITRIC OXIDE;

CELLULAR IMMUNITY; CLINICAL TRIAL; GENETIC ANALYSIS; HUMAN; IMMUNE RESPONSE; IMMUNITY; IMMUNOSUPPRESSIVE TREATMENT; LEISHMANIA; MALARIA; MOLECULAR DYNAMICS; NONHUMAN; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; REVIEW; T LYMPHOCYTE; ANIMAL; GENETIC PREDISPOSITION; GENETICS; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY; PARASITOLOGY; PLASMODIUM; REGULATORY T LYMPHOCYTE;

PLASMODIUM FALCIPARUM; PROTOZOA;

ANIMALS; CYTOKINES; GENETIC PREDISPOSITION TO DISEASE; GLYCOSYLPHOSPHATIDYLINOSITOLS; HUMANS; IMMUNE TOLERANCE; MALARIA; NITRIC OXIDE; PLASMODIUM; T-LYMPHOCYTES, REGULATORY;

EID: 33644867314     PISSN: 01419838     EISSN: 13653024     Source Type: Journal    
DOI: 10.1111/j.1365-3024.2006.00775.x     Document Type: Review

References (148)

1. Weatherall DJ Miller LH Baruch DI et al. Malaria and the red cell Hematology (Am Soc Hematol Educ Program) 2002 1 35 57
2. Mackinnon MJ Read AF Virulence in malaria: an evolutionary viewpoint Phil Trans R Soc Lond B Biol Sci 2004 359 965 986
3. Deitsch KW Hviid L Variant surface antigens, virulence genes and the pathogenesis of malaria Trends Parasitol 2004 20 562 566
4. Fortin A Stevenson MM Gros P Susceptibility to malaria as a complex trait: huge pressure from a tiny creature Hum Mol Genet 2002 11 2469 2478
5. Artavanis-Tsakonas K Tongren E Riley E The war between the malaria parasite and the immune system: immunity, immunoregulation and immunopathology Clin Exp Immunol 2003 133 145 152
6. Mahanty S Saul A Miller LH Progress in the development of recombinant and synthetic blood-stage malaria vaccines J Exp Biol 2003 206 3781 3788
7. Schwartz R T cell anergy Annu Rev Immunol 2003 21 305 334
8. Sakaguchi S Naturally arising CD4+ regulatory T cells for immunologic self-tolerance and negative control of immune responses Annu Rev Immunol 2004 22 531 562
9. Wahl SM Vazquez N Chen W Regulatory T cells and transcription factors: gatekeepers in allergic inflammation Curr Opin Immunol 2004 16 768 774
10. Schwartz RH Natural regulatory T cells and self-tolerance Nat Immunol 2005 6 327 330
11. Sakaguchi S Naturally arising Foxp3-expressing CD25+CD4+ regulatory T cells in immunological tolerance to self and non-self Nat Immunol 2005 6 345 352
12. Mills KH McGuirk P Antigen-specific regulatory T cells - their induction and role in infection Semin Immunol 2004 16 107 117
13. Thornton AM Shevach EM Suppressor effector function of CD4+CD25+ immunoregulatory T cells is antigen nonspecific J Immunol 2000 164 183 190
14. McHugh RS Whitters MJ Piccirillo CA et al. CD4 (+) CD25 (+) immunoregulatory T cells: gene expression analysis reveals a functional role for the glucocorticoid-induced TNF receptor Immunity 2002 16 311 323
15. Chen W Jin W Wahl SM Engagement of cytotoxic T lymphocyte-associated antigen 4 (CTLA-4) induces transforming growth factor b (TGF-b) production by murine CD4+ T cells J Exp Med 1998 188 1849 1857
16. Fontenot JD Gavin MA Rudensky AY Foxp3 programs the development and function of CD4+CD25+ regulatory T cells Nat Immunol 2003 4 330 336
17. Khattri R Cox T Yasayko S Ramsdell F An essential role for Scurfin in CD4+CD25+ T regulatory cells Nat Immunol 2003 4 337 342
18. Hori S Nomura T Sakaguchi S Control of regulatory T cell development by the transcription factor Foxp3 Science 2003 299 1057 1061
19. Chen W Wahl S TGF-beta: the missing link in CD4 (+) CD25 (+) regulatory T cell-mediated immunosuppression Cytokine Growth Factor Rev 2003 14 85 89
20. Nakamura K Kitani A Fuss I et al. TGF-beta 1 plays an important role in the mechanism of CD4+CD25+ regulatory T cell activity in both humans and mice J Immunol 2004 172 834 842
21. Wahl SM Chen W Transforming growth factor-beta-induced regulatory T cells referee inflammatory and autoimmune diseases Arthritis Res Ther 2005 7 62 68
22. Piccirillo CA Letterio JJ Thornton AM et al. CD4 (+) CD25 (+) regulatory T cells can mediate suppressor function in the absence of transforming growth factor beta1 production and responsiveness J Exp Med 2002 196 237 246
23. Read S Powrie F CD4 (+) regulatory T cells Curr Opin Immunol 2001 13 644 649
24. Thornton AM Shevach EM CD4+CD25+ immunoregulatory T cells suppress polyclonal T cell activation in vitro by inhibiting interleukin 2 production J Exp Med 1998 188 287 296
25. Brunkow ME Jeffery EW Hjerrild KA et al. Disruption of a new forkhead/winged-helix protein, scurfin, results in the fatal lymphoproliferative disorder of the scurfy mouse Nat Genet 2001 27 68 73
26. Bennett CL Christie J Ramsdell F et al. The immune dysregulation, polyendocrinopathy, enteropathy, X-linked syndrome (IPEX) is caused by mutations of FOXP3 Nat Genet 2001 27 20 21
27. Wildin RS Ramsdell F Peake J et al. X-linked neonatal diabetes mellitus, enteropathy and endocrinopathy syndrome is the human equivalent of mouse scurfy Nat Genet 2001 27 18 20
28. Khattri R Cox T Yasayko SA Ramsdell F An essential role for Scurfin in CD4+CD25+ T regulatory cells Nat Immunol 2003 4 337 342
29. Chen W Jin W Hardegen N et al. Conversion of peripheral CD4+CD25- naive T cells to CD4+CD25+ regulatory T cells by TGF-beta induction of transcription factor Foxp3 J Exp Med 2003 198 1875 1886
30. Kursar M Kohler A Kaufmann SH Mittrucker HW Depletion of CD4+ T cells during immunization with nonviable Listeria monocytogenes causes enhanced CD8+ T cell-mediated protection against listeriosis J Immunol 2004 172 3167 3172
31. Toka FN Suvas S Rouse BT CD4+ CD25+ T cells regulate vaccine-generated primary and memory CD8+ T-cell responses against herpes simplex virus type 1 J Virol 2004 78 13082 13089
32. Kullberg MC Jankovic D Gorelick PL et al. Bacteria-triggered CD4 (+) T regulatory cells suppress Helicobacter hepaticus-induced colitis J Exp Med 2002 196 505 515
33. Rivas L Moreno J Canavate C Alvar J Virulence and disease in leishmaniasis: what is relevant for the patient? Trends Parasitol 2004 20 297 301
34. Scott P Artis D Uzonna J Zaph C The development of effector and memory T cells in cutaneous leishmaniasis: the implications for vaccine development Immunol Rev 2004 201 318 338
35. Sacks D Anderson C Re-examination of the immunosuppressive mechanisms mediating non-cure of Leishmania infection in mice Immunol Rev 2004 201 225 238
36. Belkaid Y The role of CD4 (+) CD25 (+) regulatory T cells in Leishmania infection Expert Opin Biol Ther 2003 3 875 885
37. Belkaid Y Hoffmann KF Mendez S et al. The role of interleukin (IL)-10 in the persistence of Leishmania major in the skin after healing and the therapeutic potential of anti-IL-10 receptor antibody for sterile cure J Exp Med 2001 194 1497 1506
38. Belkaid Y Piccirillo CA Mendez S Shevach EM Sacks DL. CD4+CD25+ regulatory T cells control Leishmania major persistence and immunity Nature 2002 420 502 507
39. Rogers KA Titus RG The human cytokine response to Leishmania major early after exposure to the parasite in vitro J Parasitol 2004 90 557 563
40. Antonelli LR Dutra WO Almeida RP Bacellar O Gollob KJ Antigen specific correlations of cellular immune responses in human leishmaniasis suggests mechanisms for immunoregulation Clin Exp Immunol 2004 136 341 348
41. Anderson CF Mendez S Sacks DL Nonhealing infection despite Th1 polarization produced by a strain of Leishmania major in C57BL/6 mice J Immunol 2005 174 2934 2941
42. Mendez S Reckling SK Piccirillo CA Sacks D Belkaid Y Role for CD4(+) CD25(+) regulatory T cells in reactivation of persistent leishmaniasis and control of concomitant immunity J Exp Med 2004 200 201 210
43. Greenwood BM Bradley-Moore AM Palit A Bryceson ADM Immunosuppression in children with malaria Lancet 1972 i 169 172
44. Struik S Riley E Does malaria suffer from lack of memory? Immunol Rev 2004 201 268 290
45. Kossodo S Monso C Juillard P Velu T Goldman M Grau GE Interleukin-10 modulates susceptibility in experimental cerebral malaria Immunology 1997 91 536 540
46. Li C Corraliza I Langhorne J A defect in interleukin-10 leads to enhanced malarial disease in Plasmodium chabaudi chabaudi infection in mice Infect Immun 1999 67 4435 4442
47. Li C Sanni LA Omer FM Riley EM Langhorne J Pathology and mortality of Plasmodium chabaudi chabaudi infection in IL-10-deficient mice is ameliorated by anti-TNF-α and exacerbated by anti-TGF-β antibodies Infection and Immunity 2003
48. Omer FM Riley EM TGFbeta production is inversely correlated with severity of murine malaria infection J Exp Med 1998 188 39 48
49. Omer F de Souza J Riley E Differential induction of TGF-beta regulates proinflammatory cytokine production and determines the outcome of lethal and nonlethal Plasmodium yoelii infections J Immunol 2003 171 5430 5436
50. Jacobs T Graefe SE Niknafs S Gaworski I Fleischer B Murine malaria is exacerbated by CTLA-4 blockade J Immunol 2002 169 2323 2329
51. Jacobs T Plate T Gaworski I Fleischer B CTLA-4-dependent mechanisms prevent T cell induced-liver pathology during the erythrocyte stage of Plasmodium berghei malaria Eur J Immunol 2004 34 972 980
52. Long TT Nakazawa S Onizuka S Huaman MC Kanbara H Influence of CD4+CD25+ T cells on Plasmodium berghei NK65 infection in BALB/c mice Int J Parasitol 2003 33 175 183
53. Hisaeda H Maekawa Y Iwakawa D et al. Escape of malaria parasites from host immunity requires CD4(+) CD25(+) regulatory T cells Nat Med 2004 10 29 30
54. Omer F de Souza J Corran P Sultan AA Riley E Activation of transforming growth factor-β by parasite-derived metalloproteases and a thrombospondin-like molecule J Exp Med 2003
55. Rhee M Riley E Changes in cytokine production associated with acquired immunity to Plasmodium falciparum malaria Clin Exp Immunol 2001 126 503 510
56. Day NPJ 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 1297
57. Perkins D Weinberg J Kremsner P Reduced interleukin-12 and transforming growth factor-β1 in severe childhood malaria: relationship of cytokine balance with disease severity J Infect Dis 2000 182 988 992
58. May J Lell B Luty A Meyer C Kremsner P Plasma interleukin-10: Tumor necrosis factor (TNF)-alpha ratio is associated with TNF promoter variants and predicts malarial complications J Infect Dis 2000 182 1570 1573
59. Luty A Perkins D Lell B et al. Low interleukin-12 activity in severe Plasmodium falciparum malaria Infection Immunity 2000 68 3905 3915
60. Kurtzhals JAL Adabayeri V Goka BQ et al. Low concentrations of interleukin 10 in severe malarial anaemia compared with cerebral and uncomplicated malaria Lancet 1998 351 1768 1772
61. Othoro C Lal A Nahlen B Koech D Orago A 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 179 279 282
62. Dodoo D Omer F Todd J Akanmori B Koram K Riley E Absolute levels and ratios of pro-inflammatory and anti-inflammatory cytokine production in vitro predict clinical immunity to P. falciparum malaria J Infect Dis 2002 185 971 979
63. Playfair JHL Taverne J Bate CAW de Souza JB The malaria vaccine: antiparasite or antidisease? Immunol Today 1990 11 25 27
64. Jakobsen PH Bate CAW Taverne J Playfair JHL Malaria: toxins, cytokines and disease Parasite Immunol 1995 17 223 231
65. Schofield L Hackett F Signal transduction in host cells by a glycophosphatidylinositol toxin of malaria parasites J Exp Med 1993 177 145 153
66. Krishnegowda G Hajjar AM Zhu J et al. 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 2005 280 8606 8616
67. Zhu J Krishnegowda G Gowda DC Induction of proinflammatory responses in macrophages by the glycosylphosphatidylinositols of Plasmodium falciparum: the requirement of extracellular signal-regulated kinase, p38, c-Jun N-terminal kinase and NF-kappaB pathways for the expression of proinflammatory cytokines and nitric oxide J Biol Chem 2005 280 8617 8627
68. Schofield L Novakovic S Gerold P Schwartz RT McConville MJ Tachado SD Glycophosphatidylinositol toxin of Plasmodium falciparum upregulates intercellular adhesion molecule-1, vascular cell adhesion molecule-1 and E-selectin expression in vascular endothelial cells and increases leukocyte and parasite cytoadherence via tyrosine kinase-dependent signal transduction J Immunol 1996 156 1886 1896
69. Tachado SD Gerold P Schwarz R Novakovic S McConville M Schofield L Signal transduction in macrophages by glycosylphosphatidylinositols of Plasmodium, Trypanosoma, and Leishmania: activation of protein tyrosine kinases and protein kinase C by inositolglycan and diacylglycerol moieties Proc Natl Acad Sci USA 1997 94 4022 4027
70. Schofield L Hewitt M Evans K Siomos M Seeberger P Synthetic GPI as a candidate anti-toxic vaccine in a model of malaria Nature 2002 418 785 789
71. Naik R Branch O Woods A 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 1576
72. Boutlis CS Gowda DC Naik RS et al. Antibodies to Plasmodium falciparum glycosylphosphatidylinositols: inverse association with tolerance of parasitemia in Papua New Guinean children and adults Infect Immun 2002 70 5052 5057
73. de Souza J Todd J Krishegowda G Gowda D Kwiatkowski D Riley E Prevalence and boosting of antibodies to P. falciparum glycosylphosphatidylinositols (GPI) and evaluation of their association with protection from mild and severe clinical malaria Infection Immunity 2002 70 5045 5051
74. Suguitan AL Jr. Gowda DC Fouda G et al. Lack of an association between antibodies to Plasmodium falciparum glycosylphosphatidylinositols and malaria-associated placental changes in Cameroonian women with preterm and full-term deliveries Infect Immun 2004 72 5267 5273
75. Perraut R Diatta B Marrama L et al. Differential antibody responses to Plasmodium falciparum glycosylphosphatidylinositol anchors in patients with cerebral and mild malaria Microbes Infect 2005
76. Hudson Keenihan SN Ratiwayanto S Soebianto S et al. Age-dependent impairment of IgG responses to glycosylphosphatidylinositol with equal exposure to Plasmodium falciparum among Javanese migrants to Papua, Indonesia Am J Trop Med Hyg 2003 69 36 41
77. Boutlis CS Fagan PK Gowda DC et al. Immunoglobulin G (IgG) responses to Plasmodium falciparum glycosylphosphatidylinositols are short-lived and predominantly of the IgG3 subclass J Infect Dis 2003 187 862 865
78. Coban C Ishii KJ Kawai T et al. Toll-like receptor 9 mediates innate immune activation by the malaria pigment hemozoin J Exp Med 2005 201 19 25
79. Pichyangkul S Saengkrai P Webster HK Plasmodium falciparum pigment induces monocytes to release high levels of tumour necrosis factor-α and interleukin-1β Am J Trop Med Hyg 1994 51 430 435
80. Sherry BA Alava G Tracey KJ Martiney J Cerami A Slater AF 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 1995 45 85 96
81. Mordmuller B Turrini F Long H Kremsner PG Arese P Neutrophils and monocytes from subjects with the Mediterranean G6PD variant: effect of Plasmodium falciparum hemozoin on G6PD activity, oxidative burst and cytokine production Eur Cytokine Netw 1998 9 239 245
82. Biswas S Karmarkar MG Sharma YD Antibodies detected against Plasmodium falciparum haemozoin with inhibitory properties to cytokine production FEMS Microbiol Lett 2001 194 175 179
83. Jaramillo M Gowda DC Radzioch D Olivier M Hemozoin increases IFN-gamma-inducible macrophage nitric oxide generation through extracellular signal-regulated kinase- and NF-kappa B-dependent pathways J Immunol 2003 171 4243 4253
84. Keller CC Kremsner PG Hittner JB Misukonis MA Weinberg JB Perkins DJ Elevated nitric oxide production in children with malarial anemia: hemozoin-induced nitric oxide synthase type 2 transcripts and nitric oxide in blood mononuclear cells Infect Immun 2004 72 4868 4873
85. Skorokhod OA Alessio M Mordmuller B Arese P Schwarzer E Hemozoin (malarial pigment) inhibits differentiation and maturation of human monocyte-derived dendritic cells: a peroxisome proliferator-activated receptor-gamma-mediated effect J Immunol 2004 173 4066 4074
86. Deshpande P Shastry P Modulation of cytokine profiles by malaria pigment-hemozoin: role of IL-10 in suppression of proliferative responses of mitogen stimulated human PBMC Cytokine 2004 28 205 213
87. Schwarzer E Turrini F Ulliers D Giribaldi G Ginsburg H Arese P Impairment of macrophage functions after ingestion of Plasmodium falciparum-infected erythrocytes or isolated malarial pigment J Exp Med 1992 176 1033 1041
88. Schwarzer E Kuhn H Valente E Arese P Malaria-parasitized erythrocytes and hemozoin nonenzymatically generate large amounts of hydroxy fatty acids that inhibit monocyte functions Blood 2003 101 722 728
89. Morakote N Justus DE Immunosuppression in malaria: effect of hemozoin produced by Plasmodium berghei and Plasmodium falciparum Int Arch Allergy Appl Immunol 1988 86 28 34
90. Scorza T Magez S Brys L De Baetselier P Hemozoin is a key factor in the induction of malaria-associated immunosuppression Parasite Immunol 1999 21 545 554
91. Giribaldi G Ulliers D Schwarzer E Roberts I Piacibello W Arese P Hemozoin- and 4-hydroxynonenal-mediated inhibition of erythropoiesis. Possible role in malarial dyserythropoiesis and anemia Haematologica 2004 89 492 493
92. Egan TJ Mavuso WW Ncokazi KK The mechanism of beta-hematin formation in acetate solution. Parallels between hemozoin formation and biomineralization processes Biochemistry 2001 40 204 213
93. Nathan C Xie QW Nitric oxide synthases: roles, tolls, and controls Cell 1994 78 915 918
94. Geller DA Billiar TR Molecular biology of nitric oxide synthases Cancer Metastasis Rev 1998 17 7 23
95. Stevenson MM Tam MF Wolf SF Sher A IL-12-induced protection against blood-stage Plasmodium chabaudi AS requires IFNγ and TNFα and occurs via a nitric oxide-dependent mechanism J Immunol 1995 155 2545 2556
96. Jacobs P Radzioch D Stevenson MM In vivo regulation of nitric oxide production by tumor necrosis factor alpha and gamma interferon, but not by interleukin-4, during blood stage malaria in mice Infection Immunity 1996 64 44 49
97. Rockett KA Awburn MM Cowden WB Clark IA Killing of Plasmodium falciparum in vitro by nitric oxide derivatives Infection Immunity 1991 59 3280 3283
98. Nussler A Drapier JC Renia L et al. 1-arginine-dependent destruction of intrahepatic malaria parasites in response to tumor necrosis factor and/or interleukin 6 stimulation Eur J Immunol 1991 21 227 230
99. Gyan B Troye-Blomberg M Perlmann P Björkman A Human monocytes cultured with and without interferon-gamma inhibit Plasmodium falciparum parasite growth in vitro via secretion of reactive nitrogen intermediates Parasite Immunol 1994 16 371 375
100. Kremsner PG Neifer S Chaves MF Rudolph R Bienzle U Interferon-g induced lethality in the late phase of Plasmodium vinckei malaria despite effective parasite clearance by chloroquine European J Immunol 1992 22 2873 2878
101. Weinberg JB Nitric oxide production and nitric oxide synthase type 2 expression by human mononuclear phagocytes: a review Mol Med 1998 4 557 591
102. 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 184 557 567
103. Kremsner PG Winkler X Wilding E et al. High plasma levels of nitrogen oxides are associated with severe disease and correlate with rapid parasitological and clinical cure in Plasmodium falciparum malaria Trans Royal Soc Trop Med Hyg 1996 90 44 47
104. Perkins DJ Kremsner PG Schmid D Misukonis MA Kelly MA Weinberg JB Blood mononuclear cell nitric oxide production and plasma cytokine levels in healthy Gabonese children with prior mild or severe malaria Infect Immun 1999 67 4977 4981
105. 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 90 270 273
106. al-Yaman F Awburn MM Clark IA Serum creatinine levels and reactive nitrogen intermediates in children with cerebral malaria in Papua New Guinea Trans R Soc Trop Med Hyg 1997 91 303 305
107. Agbenyega T Angus B Bedu-Addo G et al. Plasma nitrogen oxides and blood lactate concentrations in Ghanaian children with malaria Trans R Soc Trop Med Hyg 1997 91 298 302
108. Taylor AM Day NP Sinh DX et al. Reactive nitrogen intermediates and outcome in severe adult malaria Trans R Soc Trop Med Hyg 1998 92 170 175
109. Kun J Mordmuller B Perkins D et al. Nitric oxide synthase 2 Lambarene (G-954C), increased nitric oxide production, and protection against malaria J Infect Dis 2001 184 330 336
110. Shami PJ Weinberg JB Differential effects of nitric oxide on erythroid and myeloid colony growth from CD34+ human bone marrow cells Blood 1996 87 977 982
111. Reykdal S Abboud C Liesveld J Effect of nitric oxide production and oxygen tension on progenitor preservation in ex vivo culture Exp Hematol 1999 27 441 450
112. Kwiatkowski D Genetic dissection of the molecular pathogenesis of severe infection Intensive Care Med 2000 26 Suppl. 1 S89 S97
113. Burgner D Xu W Rockett K et al. Inducible nitric oxide synthase polymorphism and fatal cerebral malaria Lancet 1998 352 1193 1194
114. Kun JF Mordmuller B Lell B Lehman LG Luckner D Kremsner PG Polymorphism in promoter region of inducible nitric oxide synthase gene and protection against malaria Lancet 1998 351 265 266
115. Parikh S Dorsey G Rosenthal PJ Host polymorphisms and the incidence of malaria in Ugandan children Am J Trop Med Hyg 2004 71 750 753
116. Levesque MC Hobbs MR Anstey NM et al. Nitric oxide synthase type 2 promoter polymorphisms, nitric oxide production, and disease severity in Tanzanian children with malaria J Infect Dis 1999 180 1994 2002
117. Hobbs M Udhayakumar V Levesque M et al. A new NOS2 promoter polymorphism associated with increased nitric oxide production and protection from severe malaria in Tanzanian and Kenyan children Lancet 2002 360 1468 1475
118. Burgner D Usen S Rockett K et al. Nucleotide and haplotypic diversity of the NOS2A promoter region and its relationship to cerebral malaria Hum Genet 2003 112 379 386
119. Modiano D Petrarca V Sirima BS et al. Different response to Plasmodium falciparum malaria in West African sympatric ethnic groups Proc Natl Acad Sci USA 1996 93 13206 13211
120. Dolo A Modiano D Maiga B et al. Difference in susceptibility to malaria between two sympatric ethnic groups in Mali Am J Trop Med Hyg 2005 72 243 248
121. Luoni G Verra F Arca B et al. Antimalarial antibody levels and IL4 polymorphism in the Fulani of West Africa Genes Immun 2001 2 411 414
122. Bolad A Farouk SE Israelsson E et al. Distinct interethnic differences in immunoglobulin G class/subclass and immunoglobulin M antibody responses to malaria antigens but not in immunoglobulin g responses to nonmalarial antigens in sympatric tribes living in West Africa Scand J Immunol 2005 61 380 386
123. Farouk SE Dolo A Bereczky S et al. Different antibody- and cytokine-mediated responses to Plasmodium falciparum parasite in two sympatric ethnic tribes living in Mali Microbes Infect 2005 7 110 117
124. Bryceson AD Fleming AF Edington GM Splenomegaly in Northern Nigeria Acta Trop 1976 33 185 214
125. Greenwood BM Groenendaal F Bradley AK et al. Ethnic differences in the prevalence of splenomegaly and malaria in The Gambia Ann Trop Med Parasitol 1987 81 345 354
126. Schofield L McConville M Hansen D et al. CD1d-restricted immunoglobulin G formation to GPI-anchored antigens mediated by NKT cells Science 1999 283 225 229
127. Fischer K Scotet E Niemeyer M et al. Mycobacterial phosphatidylinositol mannoside is a natural antigen for CD1d-restricted T cells Proc Natl Acad Sci USA 2004 101 10685 10690
128. Brigl M Brenner MB CD1: antigen presentation and T cell function Annu Rev Immunol 2004 22 817 890
129. Hansen D Siomos M Buckingham L Scalzo A Schofield L Regulation of murine cerebral malaria pathogenesis by CD1d-restricted NKT cells and the natural killer complex Immunity 2003 18 391 402
130. Scalzo AA Lyons PA Fitzgerald NA Forbes CA Yokoyama WM Shellam GR Genetic mapping of Cmv1 in the region of mouse chromosome 6 encoding the NK gene complex-associated loci Ly49 and musNKR-P1 Genomics 1995 27 435 441
131. Scalzo AA Brown MG Chu DT Heusel JW Yokoyama WM Forbes CA Development of intra-natural killer complex (NKC) recombinant and congenic mouse strains for mapping and functional analysis of NK cell regulatory loci Immunogenetics 1999 49 238 241
132. Hansen DS Siomos MA De Koning-Ward T Buckingham L Crabb BS Schofield L CD1d-restricted NKT cells contribute to malarial splenomegaly and enhance parasite-specific antibody responses Eur J Immunol 2003 33 2588 2598
133. Hansen DS Evans KJ D'Ombrain MC et al. The natural killer complex regulates severe malarial pathogenesis and influences acquired immune responses to Plasmodium berghei ANKA Infect Immun 2005 73 2288 2297
134. Sexton AC Good RT Hansen DS et al. Transcriptional profiling reveals suppressed erythropoiesis, up-regulated glycolysis, and interferon-associated responses in murine malaria J Infect Dis 2004 189 1245 1256
135. Yokoyama WM Plougastel BF Immune functions encoded by the natural killer gene complex Nat Rev Immunol 2003 3 304 316
136. Artavanis-Tsakonas K Riley EM Innate immune response to malaria: rapid induction of IFN-γ from human NK cells by live Plasmodium falciparum-infected erythrocytes J Immunol 2002 169 2956 2963
137. Artavanis-Tsakonas K Eleme K McQueen K Parham P Davis D Riley E Activation of a subset of human natural killer cells upon contact with Plasmodium falciparum-infected erythrocytes J Immunol 2003 171 5396 5405
138. Booth M Vennervald BJ Kenty L et al. Micro-geographical variation in exposure to Schistosoma mansoni and malaria, and exacerbation of splenomegaly in Kenyan school-aged children BMC Infect Dis 2004 4 13
139. Grimwade K French N Mbatha DD Zungu DD Dedicoat M Gilks CF HIV infection as a cofactor for severe falciparum malaria in adults living in a region of unstable malaria transmission in South Africa. AIDS 2004 18 547 554
140. Nacher M Interactions between worm infections and malaria Clin Rev Allergy Immunol 2004 26 85 92
141. Shapiro AE Tukahebwa EM Kasten J et al. Epidemiology of helminth infections and their relationship to clinical malaria in southwest Uganda Trans R Soc Trop Med Hyg 2005 99 18 24
142. Cooper PJ Espinel I Wieseman M et al. Human onchocerciasis and tetanus vaccination: impact on the postvaccination antitetanus antibody response Infect Immun 1999 67 5951 5957
143. Elias D Wolday D Akuffo H Petros B Bronner U Britton S Effect of deworming on human T cell responses to mycobacterial antigens in helminth-exposed individuals before and after bacille Calmette-Guerin (BCG) vaccination Clin Exp Immunol 2001 123 219 225
144. Nacher M Malaria vaccine trials in a wormy world Trends Parasitol 2001 17 563 565
145. Urban B Ferguson D Pain A et al. Plasmodium falciparum-infected erythrocytes modulate the maturation of dendritic cells Nature 1999 400 73 77
146. Baird JK Host age as a determinant of naturally acquired immunity to Plasmodium falciparum Parasitol Today 1995 11 105 111
147. Reyburn H Mbatia R Drakeley C et al. Association of transmission intensity and age with clinical manifestations and case fatality of severe Plasmodium falciparum malaria JAMA 2005 293 1461 1470
148. Riley EM Is T cell priming required for initiation of pathology in malaria infections? Immunol Today 1999 20 228 233