Immunological control of congenital toxoplasmosis in the murine model

Immunology Letters

Volumn 115, Issue 2, 2008, Pages 83-89

  Menzies, Fiona M ^a   Henriquez, Fiona L ^b   Roberts, Craig W ^a  

^a UNIVERSITY OF STRATHCLYDE   (United Kingdom)

^b UNIVERSITY OF THE WEST OF SCOTLAND   (United Kingdom)

Author keywords

Congenital; Pregnancy; Toxoplasma gondii; Toxoplasmosis; Vaccine

Indexed keywords

GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; MIFEPRISTONE; TOXOPLASMA GONDII VACCINE;

ABORTION; CONGENITAL TOXOPLASMOSIS; DISEASE TRANSMISSION; DRUG EFFICACY; FETUS DEATH; HUMAN; IMMUNE RESPONSE; INNATE IMMUNITY; NATURAL KILLER CELL; NONHUMAN; PREGNANCY OUTCOME; PRIORITY JOURNAL; REVIEW; T LYMPHOCYTE; TOXOPLASMA GONDII;

ABORTION, SPONTANEOUS; ANIMALS; DISEASE MODELS, ANIMAL; DISEASE TRANSMISSION, VERTICAL; FEMALE; HUMANS; IMMUNITY, NATURAL; MICE; MICE, INBRED BALB C; PREGNANCY; PREGNANCY COMPLICATIONS, PARASITIC; PROTOZOAN VACCINES; TOXOPLASMA; TOXOPLASMOSIS, CONGENITAL;

EID: 37749007430     PISSN: 01652478     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.imlet.2007.10.009     Document Type: Review

References (80)

1. Dubey J.P. Sources of Toxoplasma gondii infection in pregnancy. BMJ 321 (2000) 127-212
2. Montoya J.G., and Liesenfeld O. Toxoplasmosis. Lancet 363 (2004) 1965-1976
3. Sensini A. Toxoplasma gondii infection in pregnancy: opportunities and pitfalls of serological diagnosis. Clin Microbiol Infect 12 (2006) 504-512
4. Dunn D., Wallon M., Peyron F., Peterson E., Peckham C., and Gilbert R. Mother-to-child transmission of toxoplasmosis: risk estimates for clinical counselling. Lancet 353 (1999) 1829-1833
5. Wallon M., Liou C., Garner P., and Peyron F. Congenital toxoplasmosis: systematic review of efficacy of treatment in pregnancy. BMJ 318 (1999) 1511-1514
6. Tenter A.M., Heckeroth A.J., and Weiss L.M. Toxoplasma gondii: from animals to humans. Int J Parasitol 30 (2000) 1217-1258
7. Pelloux H., Brenier-Pinchart M.P., and Fricker-Hidalgo H. Protozoan infections in humans: congenital toxoplasmosis. Eur J Protistol 39 (2003) 444-448
8. Bennett R., Christiansen K., and Clifton-Hadley R. Preliminary estimates of the direct costs associated with endemic diseases of livestock in Great Britain. Prev Vet Med 39 (1999) 155-171
9. Guerina N.G., Hsu H.W., Meissner C., Maguire J.H., Lynfield R., Stechenberg B., et al. Neonatal serologic screening and early treatment for congenital Toxoplasma gondii infection. N Engl J Med 330 (1994) 1858-1863
10. Roberts C.W., and Alexander J. Studies on a murine model of congenital toxoplasmosis: vertical disease transmission only occurs in BALB/c mice infected for the first time during pregnancy. Parasitology 104 (1992) 19-23
11. Beverley J.K. Congenital transmission of toxoplasmosis through successive generations of mice. Nature 183 (1959) 1348-1349
12. Remington J.S. Experiments on the transmission of toxoplasmosis. Surv Ophthalmol 6 (1961) 856-876
13. De Roever-Bonnet H. Congenital toxoplasma infections in mice and hamsters infected with avirulent and virulent strains. Trop Geogr Med 21 (1969) 443-450
14. Freyre A., Falcon J., Mendez J., Rodrigues A., Correa L., and Gonzalez M. Refinement of the mouse model of congenital toxoplasmosis. Exp Parasitol 113 (2006) 154-160
15. Jones T.C., and Erb P. H-2 complex-linked resistance in murine toxoplasmosis. J Infect Dis 151 (1985) 739-740
16. Innes E.A. Toxoplasmosis: comparative species susceptibility and host immune response. Comp Immunol Microbiol Infect Dis 20 (1997) 131-138
17. Alexander J., Scharton-Kersten T.M., Yap G., Roberts C.W., Liew F.Y., and Sher A. Mechanisms of innate resistance to Toxoplasma gondii infection. Phil Trans R Soc Lond 52 (1997) 1355-1359
18. Liesenfeld O. Immune responses to Toxoplasma gondii in the gut. Immunobiology 201 (1999) 229-239
19. Jones L.A., Alexander J., and Roberts C.W. Ocular toxoplasmosis: in the storm of the eye. Parasite Immunol 28 (2006) 635-642
20. Yap G.S., Shaw M.H., Ling Y., and Sher A. Genetic analysis of host resistance to intracellular pathogens: lessons from studies of Toxoplasma gondii infection. Microbes Infect 8 (2006) 1117-1118
21. Debierre-Grockiego F., Campos M.A., Azzouz N., Schidt J., Bieker U., Resende M.G., et al. Activation of TLR2 and TLR4 by glycosylphosphatidylinositols derived from Toxoplasma gondii. J Immunol 179 (2007) 1129-1137
22. Mun H.S., Aosai F., Norose K., Piao L.X., Fang H., Akira S., et al. Toll-like receptor 4 mediates tolerance in macrophages stimulated with Toxoplasma gondii-derived heat shock protein 70. Infect Immun 73 (2005) 4634-4642
23. Aosai F., Rodriguez Pena M.S., Mun H.S., Fang H., Mitsunaga T., Norose K., et al. Toxoplasma gondii-derived heat shock protein 70 stimulates maturation of murine bone marrow-derived dendritic cells via Toll-like receptor 4. Cell Stress Chaperones 11 (2006) 13-22
24. Aliberti J., Valenzuela J.G., Carruthers V.B., Hieny S., Andersen J., Charest H., et al. Molecular mimicry of a CCR5 binding-domain in the microbial activation of dendritic cells. Nat Immunol 4 (2003) 485-490
25. Combe C.L., Curiel T.J., Moretto M.M., and Khan I.A. NK cells help to induce CD8(+)-T-cell immunity against Toxoplasma gondii in the absence of CD4(+) T cells. Infect Immun 73 (2005) 4913-4921
26. Gazzinelli R., Xu Y., Hieny S., Cheever A., and Sher A. Simultaneous depletion of CD4+ and CD8+ T lymphocytes is required to reactivate chronic infection with Toxoplasma gondii. J Immunol 149 (1982) 175-180
27. Nickdel M.B., Lyons R.E., Roberts F., Brombacher F., Hunter C.A., Alexander J., et al. Intestinal pathology during acute toxoplasmosis is IL-4 dependent and unrelated to parasite burden. Parasite Immunol 26 (2004) 75-82
28. Villard O., Candolfi E., Despringre J.L., Derouin F., Marcellin L., Viville S., et al. Protective effect of low doses of an anti-IL-4 monoclonal antibody in a murine model of acute toxoplasmosis. Parasite Immunol 17 (1995) 233-236
29. Roberts C.W., Ferguson D.J., Jebbari H., Satoskar A., Bluethmann H., and Alexander J. Different roles for interleukin-4 during the course of Toxoplasma gondii infection. Infect Immun 64 (1996) 897-904
30. Suzuki Y., Yang Q., Yang S., Nguyen N., Lim S., Liesenfeld O., et al. IL-4 is protective against development of toxoplasmic encephalitis. J Immunol 157 (1996) 2564-2569
31. Alexander J., Jebbari H., Bluethmann H., Brombacher F., and Roberts C.W. The role of IL-4 in adult acquired and congenital toxoplamosis. Int J Parasitol 28 (1998) 113-120
32. Gazzinelli R.T., Wysocka M., Hieny S., Scharton-Kersten T., Cheever A., Kuhn R., 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-gamma and TNF-alpha. J Immunol 157 (1996) 798-805
33. Croy B.A., Gambel P., Rossant J., and Wegmann T.G. Characterisation of murine decidual natural killer (NK) cells and their relevance to the success of pregnancy. Cell Immunol 93 (1985) 315-326
34. Bulmer J.N., Smith J., Morrison L., and Wells M. Maternal and fetal cellular relationships in the human placental basal plate. Placenta 9 (1988) 237-246
35. King A., Burrows T., Verma S., Hiby S., and Loke Y.W. Human uterine lymphocytes. Hum Reprod Update 4 (1998) 480-484
36. Kaitu'u-Lino T.J., Morison N.B., and Salamonsen L.A. Neutrophil depletion retards endometrial repair in a mouse model. Cell Tissue Res 328 (2007) 197-206
37. Miller L., Alley E.W., Murphy W.J., Russell S.W., and Hunt J.S. Progesterone inhibits inducible nitric oxide synthase gene expression and nitric oxide production in murine macrophages. J Leukoc Biol 59 (1996) 442-450
38. Miller L., and Hunt J.S. Sex steroid hormones and macrophage function. Life Sci 59 (1996) 1-14
39. Chao T.C., Chao H.H., Chen M.F., Greager J.A., and Walter R.J. Female sex hormones modulate the function of LPS-treated macrophages. Am J Reprod Immunol 44 (2000) 310-318
40. Hamano N., Terada N., Maesako K., Numata T., and Konno A. Effect of sex hormones on eosinophilic inflammation in nasal mucosa. Allergy Asthma Proc 19 (1998) 263-269
41. Silva H., Tchernitchin A.N., and Tchernitchin N.N. Low doses of estradiol-17 alpha degranulate blood eosinophil leucocytes and high doses alter homeostatic mechanisms. Med Sci Res 25 (1997) 201-204
42. Vliagoftis H., Dimitriadou V., Boucher W., Rozniecki J.J., Correia I., Raam S., et al. Estradiol augments while tamoxifen inhibits rat mast-cell secretion. Int Arch Allergy Immunol 98 (1992) 398-409
43. Baley J.E., and Schacter B.Z. Mechanisms of diminished natural killer cell activity in pregnant women and neonates. J Immunol 134 (1985) 3042-3048
44. Furukawa K., Itoh K., Okamura K., Kumagai K., and Suzuki M. Changes in NK cell activity during the oestrous cycle and pregnancy in mice. J Reprod Immunol 6 (1984) 353-363
45. Toder V., Nebel L., Elrad H., Blank M., Durdana A., and Gleicher N. Studies of natural killer cells in pregnancy. II. The immunoregulatory effect of pregnancy substances. J Clin Lab Immunol 14 (1984) 129-133
46. Toder V., Nebel L., and Gleicher N. Studies of natural killer cells in pregnancy. I. Analysis at the single cell level. J Clin Lab Immunol 14 (1984) 123-127
47. Coulam C.B., Goodman C., Roussev R.G., Thomason E.J., and Beaman K.D. Systemic CD561 cells can predict pregnancy outcome. Am J Reprod Immunol 33 (1995) 40-46
48. Szekeres-Bartho J., Varga P., and Pacsa A.S. Immunologic factors contributing to the initiation of labor-lymphocyte reactivity in term labor and threatened preterm delivery. Am J Obstet Gynecol 155 (1986) 108-112
49. Gendron R.L., and Baines M.G. Infiltrating decidual natural killer cells are associated with spontaneous abortion in mice. Cell Immunol 113 (1988) 261-267
50. Gendron R.L., Farookhi R., and Baines M.G. Resorption of CBA/J3 DBA/2 mouse conceptuses in CBA/J uteri correlates with failure if the feto-placental unit to suppress natural killer cell activity. J Reprod Fertil 89 (1990) 277-284
51. Gendron R.L. Lipopolysaccharide-induced fetal resorption in mice is associated with intrauterine production of tumour necrosis factor-alpha. J Reprod Fertil 90 (1990) 395-402
52. Szekeres-Bartho J., Par G., Dombay G., Smart Y.C., and Volgyi Z. The antiabortive effect of progesterone-induced blocking factor in mice is manifested by modulating NK activity. Cell Immunol 177 (1997) 194-199
53. Piccinni M.P., Giudizi M.G., Biagiotti R., Beloni L., Giannarini L., Sampognaro S., et al. Progesterone favors the development of human T-helper cells producing Th2-type cytokines and promotes both IL-4 production and membrane cd30 expression in established Th1 cell clones. J Immunol 155 (1995) 128-133
54. Lin Y., Zeng Y., Zeng S., and Wang T. Potential role of toll-like receptor 3 in a murine model of polyinosinic-polycytidylic acid-induced embryo resorption. Fertil Steril Suppl 1 (2006) 1125-1129
55. Zhang J., Wei H., Wu D., and Tian Z. Toll-like receptor 3 agonist induces impairment of uterine vascular remodeling and fetal losses in CBA x DBA/2 mice. J Reprod Immunol 74 (2007) 61-67
56. Fried M., and Muga R.O. Misore AO Duffy PE. Malaria elicits type 1 cytokines in the human placenta: IFN-gamma and TNF-alpha associated with pregnancy outcomes. J Immunol 160 (1998) 2523-2530
57. Quinn H.E., Ellis J.T., and Smith N.C. Neospora caninum: a cause of immune-mediated failure of pregnancy?. Trends Parasitol 18 (2003) 391-394
58. Krishnan L., Guilbert L.J., Wegmann T.G., Belosevic M., and Mosmann T.R. T helper 1 response against Leishmania major in pregnant C57BL/6 mice increases implantation failure and fetal resorptions. Correlation with increased IFN-gamma and TNF and reduced IL-10 production by placental cells. J Immunol 156 (1996) 653-662
59. Koch F., Stanzl U., Jennewein P., Janke K., Heufler C., Kampgen E., et al. High level IL-12 production by murine dendritic cells: upregulation via MHC class II and CD40 molecules and downregulation by IL-4 and IL-10. J Exp Med 184 (1996) 741-746
60. Lauw F.N., Caffrey D.R., and Golenbock D.T. Of mice and man: TLR11 (finally) finds profilin. Trends Immunol 26 (2005) 509-511
61. Yarovinsky F., Zhang D., Abdersen J.F., Bannerberg G.L., Serhan C.N., Hayden M.S., et al. TLR11 activation of dendritic cells by a protozoan profilin-like protein. Science 308 (2005) 1626-1629
62. Shiono Y., Mun H.S., He N., Nakazaki Y., Fang H., Furuya M., et al. Maternal-fetal transmission of Toxoplama gondii in interferon-γ deficient mice. Parasitol Int 56 (2007) 141-148
63. Khan I.A., Matsuura T., Fonseka S., and Kasper L.H. Production of nitric oxide (NO) is not essential for protection against acute Toxoplasma gondii infection in IRF-1-/- mice. J Immunol 156 (1996) 636-643
64. Ashkar A.A., Di Santo J.P., and Croy B.A. Interferon γ contributes to initiation of uterine vascular modification, decidual integrity, and uterine natural killer cell maturation during normal murine pregnancy. J Exp Med 192 (2000) 259-269
65. Abou-Bacar A., Pfaff A.W., Letscher-Bru V., Filisetti D., Rajapakse R., Antoni E., et al. Role of gamma interferon and T cells in congenital Toxoplasma transmission. Parasite Immunol 26 (2004) 315-318
66. Luft B.J., and Remington J.S. Effect of pregnancy on augmentation of natural killer cell activity by Corynebacterium parvum and Toxoplasma gondii. J Immunol 132 (1984) 2375-2380
67. Lin H., Mosmann T.R., Guilbert L., Tuntipopipat S., and Wegmann T.G. Synthesis of T helper 2-type cytokines at the maternal-fetal interface. J Immunol 151 (1993) 4562-4573
68. Luft B.J., and Remington J.S. Effect of pregnancy on resistance to Listeria monocytogenes and Toxoplasma gondii infection in mice. Infect Immun 38 (1982) 1164-1171
69. Shirahata T., Muroya N., Ohta C., Goto H., and Nakane A. Correlation between increased susceptibility to primary Toxoplasma gondii infection and depressed production of gamma interferon in pregnant mice. Microbiol Immunol 36 (1992) 81-91
70. Shirahata T., Muroya N., Ohta C., Goto H., and Nakane A. Enhancement by recombinant human interleukin 2 of host resistance to Toxoplasma gondii infection in pregnant mice. Microbiol Immunol 37 (1993) 583-590
71. Thouvenin M., Candolfi E., Villard O., Klein J.P., and Kein T. Immune response in a murine model of congenital toxoplasmosis: increased susceptibility of pregnant mice and transplacental passage of Toxoplasma gondii are type 2-dependent. Parassitologia 39 (1997) 279-283
72. Kodjikian L., Hoigne I., Adam O., Jacquier P., Aebi-Ochsner C., Aebi C., et al. Vertical transmission of toxoplasmosis from a chronically infected immunocompetent woman. Pediatr Infect Dis J 23 (2004) 272-274
73. McLeod R., Frenkel J.K., Estes R.G., Mack D.G., Eisenhauer P.B., and Gibori G. Subcutaneous and intestinal vaccination with tachyzoites of Toxoplasma gondii and acquisition of immunity to peroral and congenital Toxoplasma challenge. J Immunol 140 (1988) 1632-1637
74. Mevelec M.N., Bout D., Desolme B., Marchand H., Magne R., Bruneel O., et al. Evaluation of protective effect of DNA vaccination with genes encoding antigens GRA4 and SAG1 associated with GM-CSF plasmid, against acute, chronical and congenital toxoplasmosis in mice. Vaccine 23 (2005) 4489-4499
75. Ismael A.B., Dimier-Poisson I., Lebrun M., Dubremetz J.F., Bout D., and Mevelec M.N. Mic1-3 knockout of Toxoplasma gondii is a successful vaccine against chronic and congenital toxoplasmosis in mice. J Infect Dis 194 (2006) 1176-1183
76. Roberts C.W., Brewer J.M., and Alexander J. Congenital toxoplasmosis in the BALB/c mouse: prevention of vertical disease transmission and fetal death by vaccination. Vaccine 12 (1994) 1389-1394
77. Elsaid M.A., Martins M.S., Frezard F., Braga E.M., and Vitor R.W.A. Vertical Toxoplasmosis in a Murine Model. Protection after immunization with Antigens of Toxoplasma gondii Incorporated into Liposomes. Mem Inst Oswaldo Cruz 96 (2001) 99-104
78. Letscher-Bru V., Pfaff A.W., Abou-Bacar A., Filisetti D., Antoni E., Villard O., et al. Vaccination with Toxoplasma gondii SAG-1 Protein is protective against Congenital Toxoplasmosis in BALB/c mice but not in CBA/J mice. Infect Immun 71 (2003) 6615-6619
79. Couper K.N., Nielsen H.V., Petersen E., Roberts F., Roberts C.W., and Alexander J. DNA vaccination with the immunodominant tachyzoite surface antigen (SAG-1) protects against adult acquired Toxoplasma gondii infection but does not prevent maternofoetal transmission. Vaccine 21 (2003) 2813-2820
80. Fux B., Ferreira A.M., Cassali G.D., Tafuri W.L., and Vitor R.W.A. Experimental toxoplasmosis in BALB/c mice. Prevention of vertical disease transmission by treatment and reproductive failure in chronic infection. Mem Inst Oswaldo Cruz 95 (2000) 121-126