Review of the series "disease of the year 2011: Toxoplasmosis" pathophysiology of toxoplasmosis

Ocular Immunology and Inflammation

Volumn 19, Issue 5, 2011, Pages 297-306

  Subauste, Carlos S ^a   Ajzenberg, Daniel ^b,c   Kijlstra, Aize ^d,e  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b DUPUYTREN UNIVERSITY HOSPITAL   (France)

^c UNIVERSITY OF LIMOGES   (France)

^d WAGENINGEN UNIVERSITY   (Netherlands)

^e MAASTRICHT UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Genetics; Immunology; Parasite; Retinitis; Uveitis

Indexed keywords

FAS LIGAND; GAMMA INTERFERON; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 6; MAJOR HISTOCOMPATIBILITY ANTIGEN; MESSENGER RNA; MONOCLONAL ANTIBODY; NITRIC OXIDE SYNTHASE INHIBITOR; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR RECEPTOR;

AUTOPHAGY; BACTERIAL STRAIN; CHORIORETINITIS; CLINICAL TRIAL (TOPIC); COHORT ANALYSIS; CONCURRENT INFECTION; CONGENITAL TOXOPLASMOSIS; DISEASE COURSE; DISEASE PREDISPOSITION; DNA SEQUENCE; ELECTRORETINOGRAM; GENETIC POLYMORPHISM; GENETIC SUSCEPTIBILITY; GENOTYPE; HLA SYSTEM; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; HYPER IGM SYNDROME; IMMUNE RESPONSE; IMMUNOPATHOGENESIS; MICROBIAL GENETICS; NONHUMAN; POLYMERASE CHAIN REACTION; POPULATION RESEARCH; PROTEIN EXPRESSION; RESTRICTION FRAGMENT LENGTH POLYMORPHISM; REVIEW; T LYMPHOCYTE; TOXOPLASMA GONDII; TOXOPLASMOSIS; WESTERN BLOTTING;

ANIMALS; ANTIGENS, PROTOZOAN; GENETIC PREDISPOSITION TO DISEASE; HIV INFECTIONS; HUMANS; MICE; TOXOPLASMA; TOXOPLASMOSIS;

EID: 80053632879     PISSN: 09273948     EISSN: 17445078     Source Type: Journal    
DOI: 10.3109/09273948.2010.605198     Document Type: Review

References (109)

1. Tenter AM, Heckeroth AR, Weiss LM. Toxoplasma gondii: from animals to humans. Int J Parasitol. 2000;30:1217-1258.
2. Woods AC, Jacobs L, Wood RM. A study of the role of toxoplasmosis in adult chorioretinitis. Am J Ophthalmol. 1954;37:163-177.
3. McCannel CA, Holland GN, Helm CJ, Cornell PJ, Winston JV, Rimmer TG. Causes of uveitis in the general practice of ophthalmology. UCLA Community-Based Uveitis Study Group. Am J Ophthalmol. 1996;121:35-46. (Pubitemid 26026079)
4. Subauste CS, Montoya JG, Remington JS. AIDS-associated toxoplasmosis. In: Volberding PA, Sande MA, Greene WC, Lange JMA, eds. Global HIV/AIDS Medicine. Philadelphia, PA: Saunders Elsevier; 2008:399-413.
5. Mets MB, Holfels E, Boyer KM, et al. Eye manifestations of congenital toxoplasmosis. Am J Ophthalmol. 1997;123:1-16. (Pubitemid 27044555)
6. Glasner PD, Silveira C, Kruszon-Moran D, et al. An unusually high prevalence of ocular toxoplasmosis in southern Brazil. Am J Ophthalmol. 1992;114:136-144.
7. Gilbert RE, Stanford MR. Is ocular toxoplasmosis caused by prenatal or postnatal infection? B. J Ophthalmol. 2000;84:224-226. (Pubitemid 30251670)
8. Friedmann CT, Knox DL. Variations in recurrent active toxoplasmic retinochoroiditis. Arch Ophthalmol. 1969;81: 481-493.
9. Pavesio CE, Lightman S. Toxoplasma gondii and ocular toxoplasmosis: pathogenesis. Br J Ophthalmol. 1996;80: 1099-1107. (Pubitemid 27010848)
10. Holland GN. Ocular toxoplasmosis: a global reassessment, part I: epidemiology and course of disease. Am J Ophthalmol. 2003;136:973-988. (Pubitemid 37485762)
11. Zimmerman LE. Ocular pathology of toxoplasmosis. Surv Ophthalmol. 1961;6:832-838.
12. Norose K, Mun H-S, Aosai F, et al. IFN-γ-regulated Toxoplasma gondii distribution and load in the murine eye. Invest Ophthalmol Vis Sci,. 2003;44:4375-4381. (Pubitemid 37186272)
13. Lambert H, Hitziger N, Dellacasa I, Svensson M, Barragan A. Induction of dendritic cell migration upon Toxoplasma gon-dii infection potentiates parasite dissemination. Cell Microbiol. 2006;8:1611-1623. (Pubitemid 44350020)
14. Courret N, Darche S, Sonigo P, Milon G, Buzoni-Gatel D, Tardieux I. CD11c-and CD11b-expressing mouse leukocytes transport single Toxoplasma gondii tachyzoites to the brain. Blood. 2006;107:309-316. (Pubitemid 43053557)
15. Smith JR, Franc DT, Carter NS, Zamora D, Planck SR, Rosenbaum JT. Susceptibility of retinal vascular endothe-lium to infection with Toxoplasma gondii tachyzoites. Invest Ophthalmol Vis Sci,. 2004;45:1157-1161. (Pubitemid 38869021)
16. Meenken C, Rothova A, de Waal LP, van der Horst AR, Mesman BJ, Kijlstra A. HLA typing in congenital toxoplas-mosis. Br J Ophthalmol. 1995;79:494-497.
17. Jamieson SE, de Roubaix L-A, Cortina-Borja M, et al. Genetic and epigenetic factors at COL2A1 and ABCA4 infuence clinical outcome in congenital toxoplasmosis. Plos One. 2008;3:e2285.
18. Jamieson SE, Peixoto-Rangel AL, Hargrave AC, et al. Evidence for associations between the purinergic receptor P2X7 (P2RX7) and toxoplasmosis. Genes Immun. 2010;11: 374-383.
19. Cordeiro CA, Moreira PR, Andrade MS, et al. Interleukin-10 gene polymorphism (-1082G/A) is associated with toxo-plasmic retinochoroiditis. Invest Ophthalmol. Vis. Sci,. 2008;49: 1979-1982.
20. Albuquerque MC, Aleixo AL, Benchimol EI, et al. The IFN-gamma +874T/A gene polymorphism is associated with retinochoroiditis toxoplasmosis susceptibility. Mem Inst Oswaldo Cruz. 2009;104:451-455.
21. Yamamoto JH, Vallochi AL, Silveira C, et al. Discrimination between patients with acquired toxoplasmosis and congenital toxoplasmosis on the basis of the immune response to parasite antigens. J Infect Dis. 2000;181: 2018-2022. (Pubitemid 30416166)
22. Ayanru JO. The problem of uveitis in Bendel State of Nigeria: experience in Benin City. Br J Ophthalmol. 1977;61: 655-659. (Pubitemid 8216842)
23. Ronday MJ, Stilma JS, Barbe RF, et al. Aetiology of uveitis in Sierra Leone, West Africa. Br J Ophthalmol. 1996;80:956-961. (Pubitemid 26413696)
24. Gilbert RE, Freeman K, Lago EG, et al. Ocular sequelae of congenital toxoplasmosis in Brazil compared with Europe. PLoS Negl Trop Dis. 2008;2:e277.
25. Gilbert RE, Stanford MR, Jackson H, Holliman RE, Sanders MD. Incidence of acute symptomatic toxoplasma retinochor-oiditis in south London according to country of birth. BMJ. 1995;310:1037-1040.
26. de la Torre A, Gonzales G, Diaz-Ramirez J, Gomez-Marin JE. Screening by ophthalmoscopy for toxoplasma retin-ochoroiditis in Colombia. Am J Ophthalmol. 2007;143: 354-356. (Pubitemid 46136162)
27. Ajzenberg D, Cogne N, Paris L, et al. Genotype of 86 Toxoplasma gondii isolates associated with human congenital toxoplasmosis, and correlation with clinical fndings. J Infect Dis. 2002;186:684-689. (Pubitemid 34925541)
28. Halos L, Thebault A, Aubert D, et al. An innovative survey underlining the signifcant level of contamination by Toxoplasma gondii of ovine meat consumed in France. Int J Parasitol. 2010;40:193-200.
29. Ajzenberg D, Yera H, Marty P, et al. Genotype of 88 Toxoplasma gondii isolates associated with toxoplasmosis in immunocompromised patients and correlation with clinical fndings. J Infect Dis. 2009;199:1155-1167.
30. Elbez-Rubinstein A, Ajzenberg D, Darde ML, et al. Congenital toxoplasmosis and reinfection during pregnancy: case report, strain characterization, experimental model of reinfection and review. J Infect Dis. 2009;199: 280-285.
31. Howe DK, Sibley LD. Toxoplasma gondii comprises three clonal lineages: correlation of parasite genotypes with human disease. J Infect Dis. 1995;172:1561-1566.
32. Dubey J P, Quirk T, Pitt JA, et al. Isolation and genetic characterization of Toxoplasma gondii from racoons (Procyon lotor), cats (Felis domesticus), striped skunk (Mephitis mephitis), black bear (Ursus americanus), and cougar (Puma concolor). from Canada. J Parasitol. 2008;94:42-45. (Pubitemid 351415427)
33. Dubey JP, Sundar N, Hill D, et al. High prevalence and abundant atypical genotypes of Toxoplasma gondii isolated from lambs destined for human consumption in the USA. Int J Parasitol. 2008;38:999-1006.
34. Ajzenberg D, Banuls AL, Su C, et al. Genetic diversity, clon-ality and sexuality in Toxoplasma gondii. Int J Parasitol. 2004;34:1185-1196. (Pubitemid 39222052)
35. Khan A, Fux B, Su C, et al. Recent transcontinental sweep of Toxoplasma gondii driven by a single mono-morphic chromosome. Proc Natl Acad Sci USA. 2007;104: 14872-14877. (Pubitemid 350003235)
36. Pena HF, Gennari SM, Dubey JP, Su C. Population structure and mosue-virulence of Toxoplasma gondii in Brazil. Int J Parasitol. 2008;38:561-569. (Pubitemid 351273219)
37. Velmurugan GV, Dubey JP, Su C. Genotyping studies of Toxoplasma gondii isolates from Africa revealed that the archetypal clonal lineages predominate as in North America and Europe. Vet Parasitol. 2008;155:314-318.
38. Mercier A, Devillard S, Ngoubangoye B, et al. Additional haplogroups of Toxoplasma gondii out of Africa: population structure and mosue virulence of strains from Gabon. PLoS Negl Trop Dis. 2010;4:e876.
39. Neves ES, Bicudo LN, Curi AL, et al. Acute acquired toxo-plasmosis: clinical-laboratorial aspects and ophthalmologic evaluation in a cohort of immunocompetent patients. Mem Inst Oswaldo Cruz. 2009;104:393-396.
40. Carme B, Demar M, Ajzenberg D, Darde ML. Severe acquired toxoplasmosis caused by wild cycle of Toxoplasma gondii, French Guiana. Emerg Infect Dis. 2009;15:656-658.
41. Delhaes L, Ajzenberg D, Sicot B, et al. Severe congenital toxoplasmosis due to a Toxoplasma gondii strain with an atypical genotype: case report and review. Prenat Diagn. 2010;30:902-905.
42. Bowie WR, King AS, Werker DH, et al. Outbreak of toxoplasmosis associated with municipal drinking water: The BC Toxoplasma Investigation Team. Lancet. 1997;350:173-177. (Pubitemid 27303624)
43. Vallochi AL, Muccioli C, Martins MC, Silveira C, Belfort RJ, Rizzo LV. The genotype of Toxoplasma gondii strains causing ocular toxoplasmosis in humans in Brazil. Am J Ophthalmol. 2005;139:350-351. (Pubitemid 40288286)
44. Khan A, Jordan C, Muccioli C, et al. Genetic divergence of Toxoplasma gondii strains associated with ocular toxoplas-mosis, Brazil. Emerg. Infect. Dis. 2006;12:942-949. (Pubitemid 43848416)
45. Fekkar A, Ajzenberg D, B. B, et al. Direct genotyping of Toxoplasma gondii in ocular fuid samples from 20 patients with ocular toxoplasmosis: predominance of type II in France. J Clin Microbiol. 2011:Epub ahead of print.
46. Grigg ME, Ganatra J, Boothroyd JC. T.P.M. Unusual abundance of atypical strains associated with human ocular toxo-plasmosis. J Infect Dis. 2001;184:633-639. (Pubitemid 32783556)
47. Silveira C, Vallochi AL, Rodrigues da Silva U, et al. Toxoplasma gondii in the peripheral blood of patients with acute and chronic toxoplasmosis. Br J Ophthalmol. 2010:Epub ahead of print.
48. Switaj K, Master A, Borkowski PK, Skrzypczak M, Wojciechowicz J, Zaborowski P. Association of ocular tox-oplasmosis with type I Toxoplasma gondii strains: direct genotyping from peripheral blood samples. J Clin Microbiol. 2006;44:4262-4264. (Pubitemid 44737288)
49. Nowakowska D, Colon I, Remington JS, et al. Genotyping of Toxoplasma gondii by multiplex PCR and peptide-based serological testing of samples from infants in Poland diagnosed with congenital toxoplasmosis. J Clin Microbiol. 2006;44:1382-1389.
50. Morisset S, Peyron F, Lobry JR, et al. Serotyping of Toxoplasma gondii: striking homogeneous pattern between symptomatic and asymptomatic infections within Europe and South America. Microbes Infect. 2008;10:742-747.
51. Hu MS, Schwartzman JD, Lepage AC, Khan IA, Kasper LH. Experimental ocular toxoplasmosis induced in naive and preinfected mice by intracameral inoculation. Ocul Immunol Infamm. 1999;7:17-26. (Pubitemid 29328929)
52. Hu MS, Schwartzman JD, Yeaman GR, et al. Fas-FasL interaction involved in pathogenesis of ocular toxoplasmosis in mice. Infect Immun. 1999;67:928-935. (Pubitemid 29059238)
53. Lu F, Huang S, Kasper LH. CD4+ T cells in the patho-genesis of murine ocular toxoplasmosis. Infect Immun. 2004;72:4966-4972. (Pubitemid 39223379)
54. Charles E, Callegan MC, Blander IJ. The SAG1 Toxoplasma gondii surface protein is not required for acute ocular toxo-plasmosis in mice. Infect Immun. 2007;75:2079-2083. (Pubitemid 46559479)
55. Tedesco RC, Smith RL, Corte-Real S, Calabrese KS. Ocular toxoplasmosis in mice: comparison of two routes of infection. Parasitology. 2005;131:303-307. (Pubitemid 41277729)
56. McMenamin PG, Dutton GN, Hay J, S. C. The ultrastructural pathology of congenital murine toxoplasmic retinochoroidi-tis, part I: The localization and morphology of Toxoplasma cysts in the retina. Ex. Eye Res. 1986;43:529-543. (Pubitemid 17178505)
57. Suzuki Y, Orellana MA, Schreiber RD, Remington JS. Interferon-γ: the major mediator of resistance against Toxoplasma gondii. Science. 1988;240:516-518.
58. Suzuki Y, Conley FK, Remington JS. Importance of endogenous IFN-γ for prevention of toxoplasmic encephalitis in mice. J Immunol. 1989;143:2045-2050. (Pubitemid 19241227)
59. Gazzinelli RT, Wysocka M, Hayashi S, et al. Parasite-induced IL-12 stimulates early IFN-γ synthesis and resistance during acute infection with Toxoplasma gondii. J Immunol. 1994;153:2533-2543. (Pubitemid 24278122)
60. Yap G, Pesin M, Sher A. IL-12 is required for the maintenance of IFN-γ production in T cells mediating chronic resistance to the intracellular pathogen, Toxoplasma gondii. J Immunol. 2000;165:628-631. (Pubitemid 30484726)
61. Gazzinelli RT, Brezin A, Li Q, Nussenblatt RB, Chan CC. Toxoplasma gondii: acquired ocular toxoplasmosis in the murine model, protective role of TNF-α and IFN-γ. Exp Parasitol. 1994;78:217-229. (Pubitemid 24176145)
62. Norose K, Aosai F, Mizota A, Yamamoto S, Mun H-,S, Yano A. Deterioration of visual function as examined by electroretino-grams in Toxoplasma gondii-infected IFN-γ-knockout mice. Invest Ophthalmol Vis. Sci,. 2005;46:317-321. (Pubitemid 40041214)
63. Lassoued S, Zabraniecki L, Marin F, Billey T. Toxoplasmic cho-rioretinitis and antitumor necrosis factor treatment in rheumatoid arthritis. Semin Arthritis Rheum. 2007;36:262-263. (Pubitemid 46177201)
64. Roberts F, Roberts CW, Ferguson DJP, McLeod R. Inhibition of nitric oxide production exacerbates chronic ocular toxo-plasmosis. Parasite Immunol. 2000;22:1-5. (Pubitemid 30098811)
65. Portillo J-,AC, Okenka G, Reed E, et al. The CD40-autophagy pathway is needed for host protection despite IFN-γ-dependent immunity and CD40 induces auto phagy via control of p21 levels. Plos One. 2010;e14472.
66. Shen DF, Mattheson DM, Tuaillon N, Suedekum BK, Buggage RR, Chan C-,C. Involvement of apoptosis and interferon-γ in murine toxoplasmosis. Invest Ophthalmol Vis Sci,. 2001;42:2031-2036. (Pubitemid 32726035)
67. Hayashi S, Chan C-,C, Gazzinelli RT, Pham NTH, Cheung MK, Roberge FG. Protective role of nitric oxide in ocular toxoplasmosis. Br J Ophthalmol. 1996;80:644-648. (Pubitemid 26258151)
68. Naginemi CN, Pardhasaradhi K, Martins MC, Detrick B, Hooks JJ. Mechanisms of interferon-induced inhibition of Toxoplasma gondii replication in human retinal pigment epithelial cells. Infect Immun. 1996;64:4188-4196. (Pubitemid 26318141)
69. Lyons RE, Anthony JP, Ferguson DJP, Alexander J, Roberts F, Roberts CW. Immunological studies of chronic ocular toxo-plasmosis: up-regulation of major histocompatibility complex class I and transforming growth factor β and a protective role for interleukin-6. Infect Immun. 2001;69:2589-2595. (Pubitemid 32239733)
70. Suzuki Y, Yang Q, Conley FK, Abrams JS, Remington JS. Antibody against interleikin-6 reduces infammation and numbers of cysts in brains of mice with toxoplasmic encephalitis. Infect Immun. 1994;62:2773-2778. (Pubitemid 24203959)
71. Jebbari H, Roberts CW, Ferguson DJP, Bluethmann H, Alexander J. A protective role for IL-6 during early infection with Toxoplasma gondii. Parasite Immunol. 1998;20:231-239. (Pubitemid 28255396)
72. Suzuki Y, Remington JS. Dual regulation of resistance against Toxoplasma gondii infection by Lyt-2+ and Lyt-1+, L3T4+ T cells in mice. J Immunol. 1988;140:3943-3946.
73. Gazzinelli R, Xu Y, Hieny S, Cheever A, Sher A. Simultaneous depletion of CD4+ and CD8+ T lymphocytes is required to reactivate chronic infection with Toxoplasma gondii. J Immunol. 1992;149:175-180.
74. Norose K, Kikumura A, Luster AD, Hunter CA, Harris TH. CXCL10 is required to maintain T cell populations and control parasite replication during chronic ocular toxoplasmosis. Invest Ophthalmol Vis Sci,. 2010;Epub ahead of print.
75. Subauste CS, Koniaris AH, Remington JS. Murine CD8+ cyto-toxic T lymphocytes lyse Toxoplasma gondii-infected cells. J Immunol. 1991;147:3955-3959.
76. Montoya JG, Lowe KE, Clayberger C, et al. Human CD4+ and CD8+ T lymphocytes are both cytotoxic to Toxoplasma gondii-infected cells. Infect Immun. 1996;64:176-181. (Pubitemid 26009356)
77. Denkers EY, Yap G, Scharton-Kersten T, et al. Perforin-mediated cytolysis plays a limited role in host resistance to Toxoplasma gondii. J Immunol. 1997;159:1903-1908. (Pubitemid 127484179)
78. Brown CR, McLeod R. Class I MHC genes and CD8+ T cells determine cyst number in Toxoplasma gondii infection. J Immunol. 1990;145:3438-3441.
79. Lu F, Huang S, Hu MS, Kasper LH. Experimental ocular toxo-plasmosis in genetically susceptible and resistant mice. Infect Immun. 2005;73:5160-5165. (Pubitemid 41105675)
80. van Kooten C, Banchereau J. CD40-CD40 ligand. J Leuk Biol. 2000;67:2-17. (Pubitemid 30046812)
81. Subauste CS. Primary immunodefciencies and susceptibility to parasitic infections. Parasite Immunol. 2006;28:567-575. (Pubitemid 44581382)
82. Reichmann G, Walker W, Villegas EN, et al. The CD40/CD40 ligand interaction is required for resistance to toxoplasmic encephalitis. Infect Immun. 2000;68:1312-1318. (Pubitemid 30108527)
83. Andrade RM, Wessendarp M, Gubbels MJ, Striepen B, Subauste CS. CD40 induces macrophage anti-Toxoplasma gondii activity by triggering autophagy-dependent fusion of pathogen-containing vacuoles and lysosomes. J Clin Invest. 2006;116:2366-2377. (Pubitemid 44330135)
84. Subauste CS. Autophagy and immunity against Toxoplasma gondii. Curr Topics Microbiol Immunol. 2009;335:251-265.
85. Liesenfeld O, Kosek J, Remington JS, Suzuki Y. Association of CD4+ T cell-dependent, interferon-γ-mediated necrosis of the small intestine with genetic susceptibility of mice to peroral infection with Toxoplasma gondii. J Exp Med. 1996;184:597-607. (Pubitemid 26324113)
86. Gazzinelli RT, Wysocka M, Hieny S, et al. In the absence of endogenous IL-10, mice acutely infected with Toxoplasma gondii succumb to a lethal immune response dependent on CD4+ T cells and accompanied by overproduction of IL-12, IFN-y, and TNF-a. J Immunol. 1996;157:798-805.
87. Suzuki Y, Sher A, Yap G, et al. IL-10 is required for prevention of necrosis in the small intestine and mortality in both genetically resistant BALB/c and susceptible C57BL/6 mice following peroral infection with Toxoplasma gondii. J Immunol. 2000;164:5375-5382. (Pubitemid 30305218)
88. Wilson EH, Wille-Reece U, Dzierszinski F, Hunter CA. A critical role for IL-10 in limiting infammation during toxoplasmic encephalitis. J Neuroimmunol. 2005;165:63-74. (Pubitemid 40984624)
89. Lu F, Huang S, Kasper LH. Interleukin-10 and pathogenesis of murine ocular toxoplasmosis. Infect Immun. 2003;71:7159-7163. (Pubitemid 37475349)
90. Charles E, Joshi S, Ash JD, et al. CD4 T-cell suppression by cells from Toxoplasma gondii-infected retinas is mediated by surface protein PD-L1. Infect Immun. 2010;78:3484-3492.
91. Stein-Streilein J. Immure regulation and the eye. Trends Immunol. 29:548-554.
92. Nagineni CN, Detrick B, Hooks JJ. Transforming growth factor-(3 expression in human retinal pigmented epithelial cells is enhanced by Toxoplasma gondii: a possible role in the immunopathogenesis of retinochoroiditis. Clin Exp Immunol. 2002;128:372-378. (Pubitemid 34534055)
93. Jones LA, Alexander J, Roberts CW. Ocular toxoplasmosis: in the storm of the eye. Parasite Immunol. 2006;28: 635-642. (Pubitemid 44722229)
94. Ohta K, Yamagami S, Taylor AW, Streilein JW. IL-6 antagonizes TGF-beta and abolishes immune privilege in eyes with endotoxin-induced uveitis. Invest Ophthalmol Vis Sci,. 2000;41:2591-2599. (Pubitemid 30624387)
95. Tedesco RC, Smith RL, Corte-Real S, Calabrese KS. Ocular toxoplasmosis: the role of retinal pigment epithelium migration in infection. Parasitol Res. 2004;92:467-472. (Pubitemid 38658341)
96. Naginemi CN, Detrick B, Hooks JJ. Toxoplasma gondii infection induces gene expression and secretion of interleukin 1 (IL-1), IL-6, granulocyte-macrophage ceolony-stimulating factor, and intercellular adhesion molecule 1 by human retinal epithelial cells. Infect Immun. 2000;68:407-410. (Pubitemid 30016727)
97. Kang H, Remington JS, Suzuki Y Decreased resistance of B cell-defcient mice to infection with Toxoplasma gondii despite unimpaired expression of IFN-y, TNF-a, and inducible nitric oxide synthase. J Immunol. 2000;164: 2629-2643.
98. Stumhofer JS, Laurence A, Wilson EH, et al. Interleukin 27 negatively regulates the development of interleukin 17-pro-ducing T helper cells during chronic infammation of the central nervous system. Nat Immunol. 2006;7:937-945. (Pubitemid 44263907)
99. Munoz M, Heimesaat MM, Danker K, et al. Interleukin (IL)-23 mediates Toxoplasma gondii-induced immu-nopathology in the gut via matrixmetalloproteinase-2 and IL-22 but independent of IL-17. J Exp Med. 2009;206:3047-3059.
100. Guiton R, Vasseur V, Charron S, et al. Interleukin 17 receptor signaling is deleterious during Toxoplasma gondii infection in susceptible BL6 mice. J Infect. Dis. 2010;202:427-435.
101. Nussenblatt RB, Mittal KK, Fuhrman S, Sharma SD, Palestine AG. Lymphocyte proliferative responses of patients with ocular toxoplasmosis to parasite and retinal antigens. Am J Ophthalmol. 1989;107:632-641. (Pubitemid 19140926)
102. Kijlstra A, Hoekzema R, vd Lelij A, Doekes G, Rothova A. Humoral and cellular immune reactions against retinal antigens in clinical disease. Curr Eye Res. 1990;9 Suppl.: 85-89. (Pubitemid 20295606)
103. Feron EJ, Klaren VN, Wierenga EA, Verjans GM, Kijlstra A. Characterization of Toxoplasma gondii-spe-cific T cells recovered from vitreous fluid of patients with ocular toxoplasmosis. Invest Ophthalmol Vis Sci, 2001;42:3228-3232. (Pubitemid 33740684)
104. Desmonts G. Defnitive serological diagnosis of ocular toxoplasmosis. Arch Ophthalmol. 1966;76:839-851.
105. Kijlstra A, Breebaart AC, Baarsma GS, et al. Aqueous chamber taps in toxoplasmic chorioretinitis. Doc Ophthalmol. 1986;64:53-58. (Pubitemid 17015155)
106. de Boer JH, Verhagen C, Bruinenberg M, et al. Serologic and polymerase chain reaction analysis of intraocular fuids in the diagnosis of infectious uveitis. Am J Ophthalmol. 1996;121:650-658. (Pubitemid 26183745)
107. Klaren VN, van Doornik CE, Ongkosuwito JV, Feron EJ, Kijlstra A. Differences between intraocular and serum antibody responses in patients with ocular toxoplasmosis. Am J Ophthalmol. 1998;126:698-706. (Pubitemid 28514242)
108. Ongkosuwito JV, Feron EJ, van Doornik CE, et al. Analysis of immunoregulatory cytokines in ocular fuid samples from patients with uveitis. Invest Ophthalmol Vis Sci. 1998;39:2659-2665. (Pubitemid 28558224)
109. Lahmar I, Abou-Bacar A, Abdelrahman T, et al. Cytokine profles in toxoplasmic and viral uveitis. J Infect Dis. 2009;199:1239-1249.