Harbouring in the brain: A focus on immune evasion mechanisms and their deleterious effects in malaria and human African trypanosomiasis

International Journal for Parasitology

Volumn 36, Issue 5, 2006, Pages 529-540

  Bisser, S ^a,c   Ouwe Missi Oukem Boyer, O N ^a   Toure, F S ^a   Taoufiq, Z ^b   Bouteille, B ^c   Buguet, A ^d   Mazier, D ^b  

^a CENTRE INTERNATIONAL DE RECHERCHES MÉDICALES DE FRANCEVILLE   (Gabon)

^b PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

^c UNIVERSITÉ DE LIMOGES   (France)

^d UNIVERSITÉ LYON 1   (France)

Author keywords

Blood brain barrier; Central nervous system; Cerebral malaria; Late stage trypanosomiasis; Pladmodium; Trypanosoma

Indexed keywords

ARGININE; CYTOKINE; GAMMA INTERFERON; INTERLEUKIN 10; NITRIC OXIDE; TUMOR NECROSIS FACTOR ALPHA;

DISEASE CONTROL; DISEASE TRANSMISSION; DISEASE TREATMENT; EPIDEMIC; EPIDEMIOLOGY; INFECTIOUS DISEASE; MALARIA; NERVOUS SYSTEM; PROTOZOAN;

AFRICAN TRYPANOSOMIASIS; AMINO ACID DEFICIENCY; APOPTOSIS; BLOOD BRAIN BARRIER; BRAIN MALARIA; CENTRAL NERVOUS SYSTEM INFECTION; CLINICAL FEATURE; COMPARATIVE STUDY; DISEASE ASSOCIATION; ENDOTHELIUM CELL; HOST PARASITE INTERACTION; HUMAN; IMMUNE RESPONSE; MALARIA; MENINGOENCEPHALITIS; NEUROLOGIC DISEASE; NONHUMAN; OUTCOME ASSESSMENT; PARASITE SURVIVAL; PLASMODIUM FALCIPARUM; PROGNOSIS; REVIEW; TRYPANOSOMA BRUCEI;

ANIMALS; BLOOD-BRAIN BARRIER; CENTRAL NERVOUS SYSTEM PROTOZOAL INFECTIONS; HOST-PARASITE INTERACTIONS; HOST-PARASITE RELATIONS; HUMANS; MALARIA, CEREBRAL; MENINGOENCEPHALITIS; PLASMODIUM FALCIPARUM; TRYPANOSOMA BRUCEI GAMBIENSE; TRYPANOSOMA BRUCEI RHODESIENSE; TRYPANOSOMIASIS, AFRICAN;

AFRICA;

PLASMODIUM FALCIPARUM; PROTOZOA; TRYPANOSOMA; TRYPANOSOMA BRUCEI;

EID: 33646344203     PISSN: 00207519     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ijpara.2006.02.001     Document Type: Review

References (132)

1. Abolarin M.O., Evans D.A., Tovey D.G., and Ormerod W.E. Cryptic stage of sleeping-sickness trypanosome developing in choroid plexus epithelial cells. Br. Med. J. 285 (1982) 1380-1382
2. Adams S., Brown H., and Turner G. Breaking down the blood-brain barrier: signaling a path to cerebral malaria?. Trends Parasitol. 18 (2002) 360-366
3. Amani V., Vigario A.M., Belnoue E., Marussig M., Fonseca L., Mazier D., and Renia L. Involvement of IFN-gamma receptor-medicated signaling in pathology and anti-malarial immunity induced by Plasmodium berghei infection. Eur. J. Immunol. 30 (2000) 1646-1655
4. Amevigbe M.D., Jauberteau-Marchan M.O., Bouteille B., Doua F., Breton J.C., Nicolas J.A., and Dumas M. Human African trypanosomiasis: presence of antibodies to galactocerebrosides. Am. J. Trop. Med. Hyg. 47 (1992) 652-662
5. Anonymous. World Development Report 1993-Investing in Health. Commun. Dis. Rep. CDR Wkly 3 (1993) 137
6. Anonymous. Control and surveillance of African trypanosomiasis. Report of a WHO Expert Committee. World Health Organ. Tech. Rep. Ser. 881 I-VI (1998) 1-14
7. Anonymous. Severe falciparum malaria. World Health Organization, communicable diseases cluster. Trans. R. Soc. Trop. Med. Hyg. 94 Suppl. 1 (2000) S1-S90
8. Artavanis-Tsakonas K., Eleme K., McQueen K.L., Cheng N.W., Parham P., Davis D.M., and Riley E.M. Activation of a subset of human NK cells upon contact with Plasmodium falciparum-infected erythrocytes. J. Immunol. 171 (2003) 5396-5405
9. Artavanis-Tsakonas K., Tongren J.E., and Riley E.M. The war between the malaria parasite and the immune system: immunity, immunoregulation and immunopathology. Clin. Exp. Immunol. 133 (2003) 145-152
10. Ayed Z., Brindel I., Bouteille B., Van Meirvenne N., Doua F., Houinato D., Dumas M., and Jauberteau M.O. Detection and characterization of autoantibodies directed against neurofilament proteins in human African trypanosomiasis. Am. J. Trop. Med. Hyg. 57 (1997) 1-6
11. Bakhiet M., Olsson T., Edlund C., Hojeberg B., Holmberg K., Lorentzen J., and Kristensson K. A trypanosoma brucei brucei-derived factor that triggers CD8+ lymphocytes to interferon-gamma secretion: purification, characterization and protective effects in vivo by treatment with a monoclonal antibody against the factor. Scand. J. Immunol. 37 (1993) 165-178
12. Bouteille B., Keita M., Enanga B., and Mezui Me Ndong J. Experimental models for new chemotherapeutic approaches to human African trypanosomiasis. In: Dumas M., Bouteille B., and Buguet A. (Eds). Progress in Human African Trypanosomiasis, Sleeping Sickness (1999), Springer, Paris 289-300
13. Brenier-Pinchart M.P., Pelloux H., Derouich-Guergour D., and Ambroise-Thomas P. Chemokines in host-protozoan-parasite interactions. Trends Parasitol. 17 (2001) 292-296
14. Brown H., Hien T.T., Day N., Mai N.T., Chuong L.V., Chau T.T., Loc P.P., Phu N.H., Bethell D., Farrar J., Gatter K., White N., and Turner G. Evidence of blood-brain barrier dysfunction in human cerebral malaria. Neuropathol. Appl. Neurobiol. 25 (1999) 331-340
15. Brown H., Turner G., Rogerson S., Tembo M., Mwenechanya J., Molyneux M., and Taylor T. Cytokine expression in the brain in human cerebral malaria. J. Infect. Dis. 180 (1999) 1742-1746
16. Brown H., Rogerson S., Taylor T., Tembo M., Mwenechanya J., Molyneux M., and Turner G. Blood-brain barrier function in cerebral malaria in malawian children. Am. J. Trop. Med. Hyg. 64 (2001) 207-213
17. Brunet L.R. Nitric oxide in parasitic infections. Int. Immunopharmacol. 1 (2001) 1457-1467
18. Buguet A., Vincendeau P., Bouteille B., Burlet S., and Cespuglio R. Nitric oxide in murine malaria: divergent roles in blood and brain suggested by voltametric measures. Trans. R. Soc. Trop. Med. Hyg. 93 (1999) 663-664
19. Buguet A., Banzet S., Bouteille B., Vincendeau P., Tapie P., Doua F., Bogui P., and Cespuglio R. NO is a cornerstone in sleeping sickness: voltametric assessment in mouse and man. In: Moravec J., Takeda N., and Singal P.K. (Eds). Adaptation Biology and Medicine vol. 3 (2002), Narosa Publishing House, New Dehli, India 222-230
20. Buguet A., Bisser S., Josenando T., Chapotot F., and Cespuglio R. Sleep structure: a new diagnostic tool for stage determination in sleeping sickness. Acta Trop. 93 (2005) 107-117
21. Carter J.A., Ross A.J., Neville B.G., Obiero E., Katana K., Mung'ala-Odera V., Lees J.A., and Newton C.R. Developmental impairments following severe falciparum malaria in children. Trop. Med. Int. Health 10 (2005) 3-10
22. Chakravorty S.J., and Craig A. The role of ICAM-1 in Plasmodium falciparum cytoadherence. Eur. J. Cell Biol. 84 (2005) 15-27
23. Chen Q., Fernandez V., Sundstrom A., Schlichtherle M., Datta S., Hagblom P., and Wahlgren M. Developmental selection of var gene expression in Plasmodium falciparum. Nature 394 (1998) 392-395
24. Clark I.A., and Cowden W.B. Why is the pathology of falciparum worse than that of vivax malaria?. Parasitol. Today 15 (1999) 458-461
25. Cross G.A. Antigenic variation in trypanosomes: secrets surface slowly. Bioessays 18 (1996) 283-291
26. Darji A., Sileghem M., Heremans H., Brys L., and De Baetselier P. Inhibition of T-cell responsiveness during experimental infections with trypanosoma brucei: active involvement of endogenous gamma interferon. Infect. Immun. 61 (1993) 3098-3102
27. Daulouede S., Bouteille B., Moynet D., De Baetselier P., Courtois P., Lemesre J.L., Buguet A., Cespuglio R., and Vincendeau P. Human macrophage tumor necrosis factor (TNF)-alpha production induced by trypanosoma brucei gambiense and the role of TNF-alpha in parasite control. J. Infect. Dis. 183 (2001) 988-991
28. de Souza J.B., and Riley E.M. Cerebral malaria: the contribution of studies in animal models to our understanding of immunopathogenesis. Microbes Infect. 4 (2002) 291-300
29. Deininger M.H., Kremsner P.G., Meyermann R., and Schluesener H.J. Differential cellular accumulation of transforming growth factor-beta1, -beta2, and -beta3 in brains of patients who died with cerebral malaria. J. Infect. Dis. 181 (2000) 2111-2115
30. Deitsch K.W., Calderwood M.S., and Wellems T.E. Cooperative silencing elements in var genes. Nature 412 (2001) 875-876
31. Dobbie M.S., Hurst R.D., Klein N.J., and Surtees R.A. Upregulation of intercellular adhesion molecule-1 expression on human endothelial cells by tumour necrosis factor-alpha in an in vitro model of the blood-brain barrier. Brain Res. 830 (1999) 330-336
32. Dobbie M., Crawley J., Waruiru C., Marsh K., and Surtees R. Cerebrospinal fluid studies in children with cerebral malaria: an excitotoxic mechanism?. Am. J. Trop. Med. Hyg. 62 (2000) 284-290
33. Dondorp A.M., Kager P.A., Vreeken J., and White N.J. Abnormal blood flow and red blood cell deformability in severe malaria. Parasitol. Today 16 (2000) 228-232
34. Dondorp A.M., Nyanoti M., Kager P.A., Mithwani S., Vreeken J., and Marsh K. The role of reduced red cell deformability in the pathogenesis of severe falciparum malaria and its restoration by blood transfusion. Trans. R. Soc. Trop. Med. Hyg. 96 (2002) 282-286
35. Dondorp A.M., Pongponratn E., and White N.J. Reduced microcirculatory flow in severe falciparum malaria: pathophysiology and electron-microscopic pathology. Acta Trop. 89 (2004) 309-317
36. Donelson J.E., Hill K.L., and El-Sayed N.M. Multiple mechanisms of immune evasion by African trypanosomes. Mol. Biochem. Parasitol. 91 (1998) 51-66
37. Dumas M., and Bisser S. Clinical aspects of human African trypanosomiasis. In: Dumas M., Bouteille B., and Buguet A. (Eds). Progress in Human African Trypanosomiasis, Sleeping Sickness (1999), Springer, Paris 215-234
38. Enanga B., Burchmore R.J., Stewart M.L., and Barrett M.P. Sleeping sickness and the brain. Cell. Mol. Life Sci. 59 (2002) 845-858
39. Engelhardt B., and Ransohoff R.M. The ins and outs of T-lymphocyte trafficking to the CNS: anatomical sites and molecular mechanisms. Trends Immunol. 26 (2005) 485-495
40. Engstler M., Thilo L., Weise F., Grunfelder C.G., Schwarz H., Boshart M., and Overath P. Kinetics of endocytosis and recycling of the GPI-anchored variant surface glycoprotein in Trypanosoma brucei. J. Cell Sci. 117 (2004) 1105-1115
41. Gachot B., and Vachon F. Physiopathology of cerebral malaria. Presse Med. 24 (1995) 642-646
42. Gatton M.L., Peters J.M., Fowler E.V., and Cheng Q. Switching rates of plasmodium falciparum var genes: faster than we thought?. Trends Parasitol. 19 (2003) 202-208
43. Gimenez F., Barraud de Lagerie S., Fernandez C., Pino P., and Mazier D. Tumor necrosis factor alpha in the pathogenesis of cerebral malaria. Cell. Mol. Life Sci. 60 (2003) 1623-1635
44. Girard M., Bisser S., Courtioux B., Vermot-Desroches C., Bouteille B., Wijdenes J., Preud'homme J.L., and Jauberteau M.O. In vitro induction of microglial and endothelial cell apoptosis by cerebrospinal fluids from patients with human African trypanosomiasis. Int. J. Parasitol. 33 (2003) 713-720
45. Girard M., Giraud S., Courtioux B., Jauberteau-Marchan M.O., and Bouteille B. Endothelial cell activation in the presence of African trypanosomes. Mol. Biochem. Parasitol. 139 (2005) 41-49
46. Gitau E.N., and Newton C.R. Review article: blood-brain barrier in falciparum malaria. Trop. Med. Int. Health 10 (2005) 285-292
47. Gobert A.P., Daulouede S., Lepoivre M., Boucher J.L., Bouteille B., Buguet A., Cespuglio R., Veyret B., and Vincendeau P. l-Arginine availability modulates local nitric oxide production and parasite killing in experimental trypanosomiasis. Infect. Immun. 68 (2000) 4653-4657
48. Grab D.J., Nikolskaia O., Kim Y.V., Lonsdale-Eccles J.D., Ito S., Hara T., Fukuma T., Nyarko E., Kim K.J., Stins M.F., Delannoy M.J., Rodgers J., and Kim K.S. African trypanosome interactions with an in vitro model of the human blood-brain barrier. J. Parasitol. 90 (2004) 970-979
49. Grau G.E., Mackenzie C.D., Carr R.A., Redard M., Pizzolato G., Allasia C., Cataldo C., Taylor T.E., and Molyneux M.E. Platelet accumulation in brain microvessels in fatal pediatric cerebral malaria. J. Infect. Dis. 187 (2003) 461-466
50. Greenwood B.M., and Whittle H.C. The pathogenesis of sleeping sickness. Trans. R. Soc. Trop. Med. Hyg. 74 (1980) 716-725
51. Hebert M.J., Gullans S.R., Mackenzie H.S., and Brady H.R. Apoptosis of endothelial cells is associated with paracrine induction of adhesion molecules: evidence for an interleukin-1beta-dependent paracrine loop. Am. J. Pathol. 152 (1998) 523-532
52. Helbok R., Dent W., Nacher M., Treeprasertsuk S., Krudsood S., Wilairatana P., Silachamroon U., Looareesuwan S., and Schmutzhard E. Use of the multi-organ dysfunction score as a tool to discriminate different levels of severity in uncomplicated Plasmodium falciparum malaria. Am. J. Trop. Med. Hyg. 68 (2003) 372-375
53. Helbok R., Dent W., Nacher M., Lackner P., Treeprasertsuk S., Krudsood S., Wilairatana P., Silachamroon U., Looareesuwan S., and Schmutzhard E. The use of the multi-organ-dysfunction score to discriminate different levels of severity in severe and complicated Plasmodium falciparum malaria. Am. J. Trop. Med. Hyg. 72 (2005) 150-154
54. Hill K.L., Hutchings N.R., Grandgenett P.M., and Donelson J.E. T lymphocyte-triggering factor of african trypanosomes is associated with the flagellar fraction of the cytoskeleton and represents a new family of proteins that are present in several divergent eukaryotes. J. Biol. Chem. 275 (2000) 39369-39378
55. Hunt N.H., and Grau G.E. Cytokines: accelerators and brakes in the pathogenesis of cerebral malaria. Trends Immunol. 24 (2003) 491-499
56. Hutchings N.R., Donelson J.E., and Hill K.L. Trypanin is a cytoskeletal linker protein and is required for cell motility in African trypanosomes. J. Cell Biol. 156 (2002) 867-877
57. Imbert P., Gerardin P., Rogier C., Ka A.S., Jouvencel P., Brousse V., and Guyon P. Severe falciparum malaria in children: a comparative study of 1990 and 2000 WHO criteria for clinical presentation, prognosis and intensive care in Dakar, Senegal. Trans. R. Soc. Trop. Med. Hyg. 96 (2002) 278-281
58. Jensen A.T., Magistrado P., Sharp S., Joergensen L., Lavstsen T., Chiucchiuini A., Salanti A., Vestergaard L.S., Lusingu J.P., Hermsen R., Sauerwein R., Christensen J., Nielsen M.A., Hviid L., Sutherland C., Staalsoe T., and Theander T.G. Plasmodium falciparum associated with severe childhood malaria preferentially expresses PfEMP1 encoded by group A var genes. J. Exp. Med. 199 (2004) 1179-1190
59. Kaiser, K., Texier, A., Ferrandiz, J., Buguet, A., Meiller, A., Latour, C., Peyron, F., Cespuglio, R., Picot, S., 2006. Recombinant Human Erythropoietin prevents the death of mice during cerebral malaria. J. Infect. Dis. 193 (7), 987-95.
60. Keita M., Vincendeau P., Buguet A., Cespuglio R., Vallat J.M., Dumas M., and Bouteille B. Inducible nitric oxide synthase and nitrotyrosine in the central nervous system of mice chronically infected with Trypanosoma brucei brucei. Exp. Parasitol. 95 (2000) 19-27
61. Kennedy P.G. Human African trypanosomiasis of the CNS: current issues and challenges. J. Clin. Invest. 113 (2004) 496-504
62. Khonde N., Pepin J., Niyonsenga T., Milord F., and De Wals P. Epidemiological evidence for immunity following Trypanosoma brucei gambiense sleeping sickness. Trans. R. Soc. Trop. Med. Hyg. 89 (1995) 607-611
63. Kilunga Kubata B., Eguchi N., Urade Y., Yamashita K., Mitamura T., Tai K., Hayaishi O., and Horii T. Plasmodium falciparum produces prostaglandins that are pyrogenic, somnogenic, and immunosuppressive substances in humans. J. Exp. Med. 188 (1998) 1197-1202
64. Kristensson K., and Bentivoglio M. Pathology of African trypanosomiasis. In: Dumas M., Bouteille B., and Buguet A. (Eds). Progress in Human African Trypanosomiasis, Sleeping Sickness (1999), Springer, Paris 157-182
65. Kristensson K., Mhlanga J.D., and Bentivoglio M. Parasites and the brain: neuroinvasion, immunopathogenesis and neuronal dysfunctions. Curr. Top. Microbiol. Immunol. 265 (2002) 227-257
66. Lejon V., Lardon J., Kenis G., Pinoges L., Legros D., Bisser S., N'Siesi X., Bosmans E., and Buscher P. Interleukin (IL)-6, IL-8 and IL-10 in serum and CSF of Trypanosoma brucei gambiense sleeping sickness patients before and after treatment. Trans R. Soc. Trop. Med. Hyg. 96 (2002) 329-333
67. Lonsdale-Eccles J.D., and Grab D.J. Trypanosome hydrolases and the blood-brain barrier. Trends Parasitol. 18 (2002) 17-19
68. Lopansri B.K., Anstey N.M., Weinberg J.B., Stoddard G.J., Hobbs M.R., Levesque M.C., Mwaikambo E.D., and Granger D.L. Low plasma arginine concentrations in children with cerebral malaria and decreased nitric oxide production. Lancet 361 (2003) 676-678
69. Lou J., Lucas R., and Grau G.E. Pathogenesis of cerebral malaria: recent experimental data and possible applications for humans. Clin. Microbiol. Rev. 14 (2001) 810-820
70. Lucas R., Magez S., Songa B., Darji A., Hamers R., and de Baetselier P. A role for TNF during African trypanosomiasis: involvement in parasite control, immunosuppression and pathology. Res. Immunol. 144 (1993) 370-376
71. MacDonald S.M., Bhisutthibhan J., Shapiro T.A., Rogerson S.J., Taylor T.E., Tembo M., Langdon J.M., and Meshnick S.R. Immune mimicry in malaria: Plasmodium falciparum secretes a functional histamine-releasing factor homolog in vitro and in vivo. Proc. Natl Acad. Sci. USA 98 (2001) 10829-10832
72. Mackintosh C.L., Beeson J.G., and Marsh K. Clinical features and pathogenesis of severe malaria. Trends Parasitol. 20 (2004) 597-603
73. MacLean L., Odiit M., and Sternberg J.M. Nitric oxide and cytokine synthesis in human African trypanosomiasis. J. Infect. Dis. 184 (2001) 1086-1090
74. MacLean L., Chisi J.E., Odiit M., Gibson W.C., Ferris V., Picozzi K., and Sternberg J.M. Severity of human African trypanosomiasis in East Africa is associated with geographic location, parasite genotype, and host inflammatory cytokine response profile. Infect. Immun. 72 (2004) 7040-7044
75. MacPherson G.G., Warrell M.J., White N.J., Looareesuwan S., and Warrell D.A. Human cerebral malaria. A quantitative ultrastructural analysis of parasitized erythrocyte sequestration. Am. J. Pathol. 119 (1985) 385-401
76. Magez S., Stijlemans B., Radwanska M., Pays E., Ferguson M.A., and De Baetselier P. The glycosyl-inositol-phosphate and dimyristoylglycerol moieties of the glycosylphosphatidylinositol anchor of the trypanosome variant-specific surface glycoprotein are distinct macrophage-activating factors. J. Immunol. 160 (1998) 1949-1956
77. Maneerat Y., Pongponratn E., Viriyavejakul P., Punpoowong B., Looareesuwan S., and Udomsangpetch R. Cytokines associated with pathology in the brain tissue of fatal malaria. Southeast Asian J. Trop. Med. Public Health 30 (1999) 643-649
78. Maneerat Y., Viriyavejakul P., Punpoowong B., Jones M., Wilairatana P., Pongponratn E., Turner G.D., and Udomsangpetch R. Inducible nitric oxide synthase expression is increased in the brain in fatal cerebral malaria. Histopathology 37 (2000) 269-277
79. Marsh K., Marsh V.M., Brown J., Whittle H.C., and Greenwood B.M. Plasmodium falciparum: the behavior of clinical isolates in an in vitro model of infected red blood cell sequestration. Exp. Parasitol. 65 (1988) 202-208
80. Masocha W., Robertson B., Rottenberg M.E., Mhlanga J., Sorokin L., and Kristensson K. Cerebral vessel laminins and IFN-gamma define Trypanosoma brucei brucei penetration of the blood-brain barrier. J. Clin. Invest. 114 (2004) 689-694
81. May J., Lell B., Luty A.J., Meyer C.G., and Kremsner P.G. Plasma interleukin-10:Tumor necrosis factor (TNF)-alpha ratio is associated with TNF promoter variants and predicts malarial complications. J. Infect. Dis. 182 (2000) 1570-1573
82. Medana I.M., Day N.P., Salahifar-Sabet H., Stocker R., Smythe G., Bwanaisa L., Njobvu A., Kayira K., Turner G.D., Taylor T.E., and Hunt N.H. Metabolites of the kynurenine pathway of tryptophan metabolism in the cerebrospinal fluid of Malawian children with malaria. J. Infect. Dis. 188 (2003) 844-849
83. Mhlanga J.D., Bentivoglio M., and Kristensson K. Neurobiology of cerebral malaria and African sleeping sickness. Brain Res. Bull. 44 (1997) 579-589
84. Morgan G.W., Hall B.S., Denny P.W., Carrington M., and Field M.C. The kinetoplastida endocytic apparatus. part I: a dynamic system for nutrition and evasion of host defences. Trends Parasitol. 18 (2002) 491-496
85. Mturi N., Musumba C.O., Wamola B.M., Ogutu B.R., and Newton C.R. Cerebral malaria: optimising management. CNS Drugs 17 (2003) 153-165
86. Mulenga C., Mhlanga J.D., Kristensson K., and Robertson B. Trypanosoma brucei brucei crosses the blood-brain barrier while tight junction proteins are preserved in a rat chronic disease model. Neuropathol. Appl. Neurobiol. 27 (2001) 77-85
87. Nagatake T., Hoang V.T., Tegoshi T., Rabbege J., Ann T.K., and Aikawa M. Pathology of falciparum malaria in Vietnam. Am. J. Trop. Med. Hyg. 47 (1992) 259-264
88. Newton C.R., and Warrell D.A. Neurological manifestations of falciparum malaria. Ann. Neurol. 43 (1998) 695-702
89. Newton C.R., Hien T.T., and White N. Cerebral malaria. J. Neurol. Neurosurg. Psychiatry 69 (2000) 433-441
90. Nitcheu J., Bonduelle O., Combadiere C., Tefit M., Seilhean D., Mazier D., and Combadiere B. Perforin-dependent brain-infiltrating cytotoxic CD8+T lymphocytes mediate experimental cerebral malaria pathogenesis. J. Immunol. 170 (2003) 2221-2228
91. Okomo-Assoumou M.C., Geffard M., Daulouede S., Chaugier C., Lemesre J.L., and Vincendeau P. Circulating antibodies directed against tryptophan-like epitopes in sera of patients with human African trypanosomiasis. Am. J. Trop. Med. Hyg. 52 (1995) 461-467
92. Owens T., Babcock A.A., Millward J.M., and Toft-Hansen H. Cytokine and chemokine inter-regulation in the inflamed or injured CNS. Brain Res. Brain Res. Rev. 48 (2005) 178-184
93. Paget-McNicol S., Gatton M., Hastings I., and Saul A. The Plasmodium falciparum var gene switching rate, switching mechanism and patterns of parasite recrudescence described by mathematical modelling. Parasitology 124 (2002) 225-235
94. Pays E. Antigenic variation in African trypanosomes. In: Dumas M., Bouteille B., and Buguet A. (Eds). Progress in Human African Trypanosomiasis, Sleeping Sickness (1999), Springer, Paris 31-52
95. Pays E. Regulation of antigen gene expression in Trypanosoma brucei. Trends Parasitol. 21 (2005) 517-520
96. Pentreath V.W. Cytokines and the blood-brain-barrier in human and experimental African trypanosomiasis. In: Dumas M., Bouteille B., and Buguet A. (Eds). Progress in Human African Trypanosomiasis, Sleeping Sickness (1999), Springer, Paris 105-118
97. Pentreath V.W., Owolabi A.O., and Doua F. Survival of Trypanosoma brucei brucei in cerebrospinal fluid. Ann. Trop. Med. Parasitol. 86 (1992) 29-34
98. Philip K.A., Dascombe M.J., Fraser P.A., and Pentreath V.W. Blood-brain barrier damage in experimental African trypanosomiasis. Ann. Trop. Med. Parasitol. 88 (1994) 607-616
99. Pino P., Vouldoukis I., Kolb J.P., Mahmoudi N., Desportes-Livage I., Bricaire F., Danis M., Dugas B., and Mazier D. Plasmodium falciparum-infected erythrocyte adhesion induces caspase activation and apoptosis in human endothelial cells. J. Infect. Dis. 187 (2003) 1283-1290
100. Pino P., Taoufiq Z., Nitcheu J., Vouldoukis I., and Mazier D. Blood-brain barrier breakdown during cerebral malaria: suicide or murder?. Thromb. Haemost. 94 (2005) 336-340
101. Pongponratn E., Turner G.D., Day N.P., Phu N.H., Simpson J.A., Stepniewska K., Mai N.T., Viriyavejakul P., Looareesuwan S., Hien T.T., Ferguson D.J., and White N.J. An ultrastructural study of the brain in fatal Plasmodium falciparum malaria. Am. J. Trop. Med. Hyg. 69 (2003) 345-359
102. Ransohoff R.M., Kivisakk P., and Kidd G. Three or more routes for leukocyte migration into the central nervous system. Nat. Rev. Immunol. 3 (2003) 569-581
103. Reist M., Marshall K.A., Jenner P., and Halliwell B. Toxic effects of sulphite in combination with peroxynitrite on neuronal cells. J. Neurochem. 71 (1998) 2431-2438
104. Rhind S.G., and Shek P.N. Cytokines in the pathogenesis of human African trypanosomiasis: antagonistic roles of TNF-α and IL-10. In: Dumas M., Bouteille B., and Buguet A. (Eds). Progress in Human African Trypanosomiasis, Sleeping Sickness (1999), Springer, Paris 119
105. Rivest S., Lacroix S., Vallieres L., Nadeau S., Zhang J., and Laflamme N. How the blood talks to the brain parenchyma and the paraventricular nucleus of the hypothalamus during systemic inflammatory and infectious stimuli. Proc. Soc. Exp. Biol. Med. 223 (2000) 22-38
106. Sacks D., and Sher A. Evasion of innate immunity by parasitic protozoa. Nat. Immunol. 3 (2002) 1041-1047
107. Sanni L.A. The role of cerebral oedema in the pathogenesis of cerebral malaria. Redox Rep. 6 (2001) 137-142
108. Scherf A., Hernandez-Rivas R., Buffet P., Bottius E., Benatar C., Pouvelle B., Gysin J., and Lanzer M. Antigenic variation in malaria: in situ switching, relaxed and mutually exclusive transcription of var genes during intra-erythrocytic development in Plasmodium falciparum. Eur. Mol. Biol. Org. 17 (1998) 5418-5426
109. Schleifer K.W., and Mansfield J.M. Suppressor macrophages in African trypanosomiasis inhibit T cell proliferative responses by nitric oxide and prostaglandins. J. Immunol. 151 (1993) 5492-5503
110. Schofield L., and Grau G.E. Immunological processes in malaria pathogenesis. Nat. Rev. Immunol. 5 (2005) 722-735
111. Schofield L., Novakovic S., Gerold P., Schwarz R.T., McConville M.J., and Tachado S.D. Glycosylphosphatidylinositol toxin of plasmodium up-regulates 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. 156 (1996) 1886-1896
112. Schultzberg M., Ambatsis M., Samuelsson E.B., Kristensson K., and van Meirvenne N. Spread of Trypanosoma brucei to the nervous system: early attack on circumventricular organs and sensory ganglia. J. Neurosci. Res. 21 (1988) 56-61
113. Scorza T., Magez S., Brys L., and De Baetselier P. Hemozoin is a key factor in the induction of malaria-associated immunosuppression. Parasite Immunol. 21 (1999) 545-554
114. Sein K.K., Maeno Y., Thuc H.V., Anh T.K., and Aikawa M. Differential sequestration of parasitized erythrocytes in the cerebrum and cerebellum in human cerebral malaria. Am. J. Trop. Med. Hyg. 48 (1993) 504-511
115. Sherman I.W., Eda S., and Winograd E. Cytoadherence and sequestration in Plasmodium falciparum: defining the ties that bind. Microbes Infect. 5 (2003) 897-909
116. Sternberg J.M. Human African trypanosomiasis: clinical presentation and immune response. Parasite Immunol. 26 (2004) 469-476
117. Sternberg J., and McGuigan F. Nitric oxide mediates suppression of T cell responses in murine Trypanosoma brucei infection. Eur. J. Immunol. 22 (1992) 2741-2744
118. Stiles J.K., Whittaker J., Sarfo B.Y., Thompson W.E., Powell M.D., and Bond V.C. Trypanosome apoptotic factor mediates apoptosis in human brain vascular endothelial cells. Mol. Biochem. Parasitol. 133 (2004) 229-240
119. Stoppini L., Buchs P.A., Brun R., Muller D., Duport S., Parisi L., and Seebeck T. Infection of organotypic slice cultures from rat central nervous tissue with Trypanosoma brucei brucei. Int. J. Med. Microbiol. 290 (2000) 105-113
120. Strazielle N., and Ghersi-Egea J.F. Choroid plexus in the central nervous system: biology and physiopathology. J. Neuropathol. Exp. Neurol. 59 (2000) 561-574
121. Szallies A., Kubata B.K., and Duszenko M. A metacaspase of Trypanosoma brucei causes loss of respiration competence and clonal death in the yeast Saccharomyces cerevisiae. FEBS: Fed. Eur. Biochem. Soc. Lett. 517 (2002) 144-150
122. Tizard I., Nielsen K.H., Seed J.R., and Hall J.E. Biologically active products from African trypanosomes. Microbiol. Rev. 42 (1978) 664-681
123. Turner G. Cerebral malaria. Brain Pathol. 7 (1997) 569-582
124. Udomsangpetch R., Chivapat S., Viriyavejakul P., Riganti M., Wilairatana P., Pongponratin E., and Looareesuwan S. Involvement of cytokines in the histopathology of cerebral malaria. Am. J. Trop. Med. Hyg. 57 (1997) 501-506
125. Urban B.C., and Roberts D.J. Malaria, monocytes, macrophages and myeloid dendritic cells: sticking of infected erythrocytes switches off host cells. Curr. Opin. Immunol. 14 (2002) 458-465
126. Urban B.C., and Roberts D.J. Inhibition of T cell function during malaria: implications for immunology and vaccinology. J. Exp. Med. 197 (2003) 137-141
127. Urban B.C., Ferguson D.J., Pain A., Willcox N., Plebanski M., Austyn J.M., and Roberts D.J. Plasmodium falciparum-infected erythrocytes modulate the maturation of dendritic cells. Nature 400 (1999) 73-77
128. Vincendeau P., Jauberteau-Marchan M.O., Daulouede S., and Ayed Z. Immunology of African trypanosomiasis. In: Dumas M., Bouteille B., and Buguet A. (Eds). Progress in Human African Trypanosomiasis, Sleeping Sickness (1999), Springer, Paris 137-156
129. Vincendeau P., Gobert A.P., Daulouede S., Moynet D., and Mossalayi M.D. Arginases in parasitic diseases. Trends Parasitol. 19 (2003) 9-12
130. Viswambharan H., Seebeck T., and Yang Z. Enhanced endothelial nitric oxide-synthase activity in mice infected with Trypanosoma brucei. Int. J. Parasit. 33 (2003) 1099-1104
131. Wassmer S.C., Combes V., and Grau G.E. Pathophysiology of cerebral malaria: role of host cells in the modulation of cytoadhesion. Ann. NY Acad. Sci. 992 (2003) 30-38
132. Wu Y., Wang X., Liu X., and Wang Y. Data-mining approaches reveal hidden families of proteases in the genome of malaria parasite. Genome Res. 13 (2003) 601-616