Of mice and women: Rodent models of placental malaria

Trends in Parasitology

Volumn 26, Issue 8, 2010, Pages 412-419

  Hviid, Lars ^a   Marinho, Claudio R F ^b   Staalsoe, Trine ^a   Penha Gonçalves, Carlos ^c  

^a Rigshospitalet   (Denmark)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

^c INSTITUTO GULBENKIAN DE CIÊNCIA   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

ERYTHROCYTE MEMBRANE PROTEIN 1; PARASITE ANTIGEN;

HUMAN; IMMUNITY; MALARIA; NONHUMAN; PATHOGENESIS; PLACENTA; PLASMODIUM FALCIPARUM; PREGNANCY; REVIEW; ANIMAL; DISEASE MODEL; FEMALE; GENETICS; IMMUNOLOGY; MALARIA FALCIPARUM; METABOLISM; MOUSE; PARASITOLOGY; PATHOGENICITY; PATHOLOGY; PLACENTA DISORDER; PREGNANCY COMPLICATION;

ANIMALS; ANTIGENS, PROTOZOAN; DISEASE MODELS, ANIMAL; FEMALE; HUMANS; MALARIA, FALCIPARUM; MICE; PLACENTA DISEASES; PLASMODIUM FALCIPARUM; PREGNANCY; PREGNANCY COMPLICATIONS, PARASITIC;

MURINAE; MUS; PLASMODIUM FALCIPARUM; RODENTIA;

EID: 77955057678     PISSN: 14714922     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pt.2010.04.010     Document Type: Review

References (76)

1. Steketee R.W., et al. The burden of malaria in pregnancy in malaria-endemic areas. Am. J. Trop. Med. Hyg. 2001, 64:28-35.
2. Duffy P.E., Desowitz R.S. Pregnancy malaria throughout history: dangerous labors. Malaria in Pregnancy. Deadly Parasite, Susceptible Host 2001, 1-25. Taylor & Francis. P.E. Duffy, M. Fried (Eds.).
3. Fried M., Duffy P.E. Adherence of Plasmodium falciparum to chondroitin sulphate A in the human placenta. Science 1996, 272:1502-1504.
4. Kraemer S.M., Smith J.D. A family affair: var genes, PfEMP1 binding, and malaria disease. Curr. Opin. Microbiol. 2006, 9:374-380.
5. Salanti A., et al. Selective upregulation of a single distinctly structured var gene in CSA-adhering Plasmodium falciparum involved in pregnancy-associated malaria. Mol. Microbiol. 2003, 49:179-191.
6. Salanti A., et al. Evidence for the involvement of VAR2CSA in pregnancy-associated malaria. J. Exp. Med. 2004, 200:1197-1203.
7. Tuikue Ndam N.G., et al. High level of var2csa transcription by Plasmodium falciparum isolated from the placenta. J. Infect. Dis. 2005, 192:331-335.
8. Chotivanich K., et al. The adhesion receptors of P. vivax-infected red cells. Exp. Parasitol. 2003, 105:33-34.
9. Neres R., et al. Pregnancy outcome and placenta pathology in Plasmodium berghei infected mice reproduce the pathogenesis of severe malaria in pregnant women. PLoS ONE 2008, 3:e1608.
10. Mackenstedt U., et al. Comparative morphology of human and animal malaria parasites. I. Host-parasite interface. Parasitol. Res. 1989, 75:528-535.
11. Hall N., et al. A comprehensive survey of the Plasmodium life cycle by genomic, transcriptomic, and proteomic analyses. Science 2005, 307:82-86.
12. Oduola A.M., et al. Effects of malaria (Plasmodium berghei) on the maternal-fetal relationship in mice. J. Protozool. 1982, 29:77-81.
13. Hioki A., et al. Influence of pregnancy on the course of malaria in mice infected with Plasmodium berghei. J. Protozool. 1990, 37:163-167.
14. Desowitz R.S., et al. Characterization of a model of malaria in the pregnant host: Plasmodium berghei in the white rat. Am. J. Trop. Med. Hyg. 1989, 41:630-634.
15. Tegoshi T., et al. Placental pathology in Plasmodium berghei-infected rats. Am. J. Trop. Med. Hyg. 1992, 47:643-651.
16. Vinayak V.K., et al. Influence of malarial infection on the maternal-foetal relationship in pregnant mice. Aust. J. Exp. Biol. Med. Sci. 1986, 64:223-227.
17. Oduola A.M., et al. Plasmodium berghei: histology, immunocytochemistry, and ultrastructure of the placenta in rodent malaria. Exp. Parasitol. 1986, 62:181-193.
18. Poovassery J., Moore J.M. Murine malaria infection induces fetal loss associated with accumulation of Plasmodium chabaudi AS-infected erythrocytes in the placenta. Infect. Immun. 2006, 74:2839-2848.
19. Cox J., et al. Plasmodium chabaudi: a rodent malaria model for in-vivo and in-vitro cytoadherence of malaria parasites in the absence of knobs. Parasite Immunol. 1987, 9:543-561.
20. Gilks C.F., et al. Relationships between sequestration, antigenic variation and chronic parasitism in Plasmodium chabaudi chabaudi - a rodent malaria model. Parasite Immunol. 1990, 12:45-64.
21. Shapiro S.S., Sherman M.I. Sulfated mucopolysaccharides of midgestation embryonic and extraembryonic tissues of the mouse. Arch. Biochem. Biophys. 1974, 162:272-280.
22. Su Z., Stevenson M.M. Central role of endogenous gamma interferon in protective immunity against blood-stage Plasmodium chabaudi AS infection. Infect. Immun. 2000, 68:4399-4406.
23. Su Z., Stevenson M.M. IL-12 is required for antibody-mediated protective immunity against blood-stage Plasmodium chabaudi AS malaria infection in mice. J. Immunol. 2002, 168:1348-1355.
24. Poovassery J., Moore J.M. Association of malaria-induced murine pregnancy failure with robust peripheral and placental cytokine responses. Infect. Immun. 2009, 77:4998-5006.
25. Li C., et al. Pathology of Plasmodium chabaudi chabaudi infection and mortality in interleukin-10-deficient mice are ameliorated by anti-tumor necrosis factor alpha and exacerbated by anti-transforming growth factor β antibodies. Infect. Immun. 2003, 71:4850-4856.
26. Poovassery J.S., et al. Malaria-induced murine pregnancy failure: distinct roles for IFN-γ and TNF. J. Immunol. 2009, 183:5342-5349.
27. Pavia C.S., Niederbuhl C.J. Immunization and protection against malaria during murine pregnancy. Am. J. Trop. Med. Hyg. 1991, 44:176-182.
28. Clark I.A., Chaudhri G. Tumor necrosis factor in malaria-induced abortion. Am. J. Trop. Med. Hyg. 1988, 39:246-249.
29. H2 phenomenon ?. Immunol. Today 1993, 14:353-356.
30. Van Zon A.A., Eling W.M. Depressed malarial immunity in pregnant mice. Infect. Immun. 1980, 28:630-632.
31. Eling W. Survival of parasites in mice immunized against Plasmodium berghei. Tropenmed. Parasitol. 1978, 29:204-209.
32. Marinho C.R., et al. Recrudescent Plasmodium berghei from pregnant mice displays enhanced binding to the placenta and induces protection in multigravida. PLoS ONE 2009, 4:e5630.
33. Megnekou R., et al. Variant-specific immunity to Plasmodium berghei in pregnant mice. Infect. Immun. 2009, 77:1827-1834.
34. Van Zon A.A., Eling W.M. Pregnancy associated recrudescence in murine malaria (Plasmodium berghei). Tropenmed. Parasitol. 1980, 31:402-408.
35. Van Zon A.A., et al. Pregnancy-induced recrudescences strengthen malarial immunity in mice infected with Plasmodium berghei. Parasitology 1985, 91:9-17.
36. Nosten F., et al. Malaria in pregnancy and the endemicity spectrum: what can we learn?. Trends Parasitol. 2004, 20:425-432.
37. Desai M., et al. Epidemiology and burden of malaria in pregnancy. Lancet Infect. Dis. 2007, 7:93-104.
38. Pichyangkul S., et al. Plasmodium falciparum pigment induces monocytes to release high levels of tumor necrosis factor-α and interleukin-1β. Am. J. Trop. Med. Hyg. 1994, 51:430-435.
39. Veenstra van Nieuwenhoven A.L., et al. The immunology of successful pregnancy. Hum. Reprod. Update 2003, 9:347-357.
40. Mengistu G., et al. Outcomes of pregnancy in severe malaria with emphasis on neurological manifestations in Gondar Hospital northwest Ethiopia. Ethiop. Med. J. 2006, 44:321-330.
41. Poespoprodjo J.R., et al. Adverse pregnancy outcomes in an area where multidrug-resistant Plasmodium vivax and Plasmodium falciparum infections are endemic. Clin. Infect. Dis. 2008, 46:1374-1381.
42. McGready R., et al. The effects of Plasmodium falciparum and P. vivax infections on placental histopathology in an area of low malaria transmission. Am. J. Trop. Med. Hyg. 2004, 70:398-407.
43. McGregor I.A., Smith D.A. A health, nutrition and parasitological survey in a rural village (Keneba) in west Kiang, Gambia. Trans. R. Soc. Trop. Med. Hyg. 1952, 46:403-427.
44. Walter P.R., et al. Placental pathologic changes in malaria. A histologic and ultrastructural study. Am. J. Pathol. 1982, 109:330-342.
45. Beeson J.G., et al. Selective accumulation of mature asexual stages of Plasmodium falciparum-infected erythrocytes in the placenta. Infect. Immun. 2002, 70:5412-5415.
46. Rogerson S.J., et al. Malaria in pregnancy: pathogenesis and immunity. Lancet Infect. Dis. 2007, 7:105-117.
47. Fievet N., et al. Plasmodium falciparum induces a Th1/Th2 disequilibrium, favoring the Th1-type pathway, in the human placenta. J. Infect. Dis. 2001, 183:1530-1534.
48. Suguitan A.L., et al. Malaria-associated cytokine changes in the placenta of women with pre-term deliveries in Yaounde, Cameroon. Am. J. Trop. Med. Hyg. 2003, 69:574-581.
49. Nosten F., et al. Malaria during pregnancy in an area of unstable endemicity. Trans. R. Soc. Trop. Med. Hyg. 1991, 85:424-429.
50. Shulman C.E., et al. A community randomized controlled trial of insecticide-treated bednets for the prevention of malaria and anaemia among primigravid women on the Kenyan coast. Trop. Med. Int. Health 1998, 3:197-204.
51. Beeson J.G., et al. Plasmodium falciparum isolates from infected pregnant women and children are associated with distinct adhesive and antigenic properties. J. Infect. Dis. 1999, 180:464-472.
52. Ricke C.H., et al. Plasma antibodies from malaria-exposed pregnant women recognize variant surface antigens on Plasmodium falciparum-infected erythrocytes in a parity-dependent manner and block parasite adhesion to chondroitin sulphate A. J. Immunol. 2000, 165:3309-3316.
53. Duffy P.E., Fried M. Antibodies that inhibit Plasmodium falciparum adhesion to chondroitin sulfate A are associated with increased birth weight and the gestational age of newborns. Infect. Immun. 2003, 71:6620-6623.
54. Staalsoe T., et al. Variant surface antigen-specific IgG and protection against the clinical consequences of pregnancy-associated Plasmodium falciparum malaria. Lancet 2004, 363:283-289.
55. Ofori M.F., et al. Expression of variant surface antigens by Plasmodium falciparum parasites in the peripheral blood of clinically immune pregnant women indicates ongoing placental infection. Infect. Immun. 2003, 71:1584-1586.
56. Nguyen-Dinh P., et al. Rapid spontaneous postpartum clearance of Plasmodium falciparum parasitaemia in African women. Lancet 1988, 2:751-752.
57. Khunrae P., et al. Full-length recombinant Plasmodium falciparum VAR2CSA binds specifically to CSPG and induces potent parasite adhesion-blocking antibodies. J. Mol. Biol. 2010, 397:826-834.
58. Hviid L. Naturally acquired immunity to Plasmodium falciparum malaria in Africa. Acta Trop. 2005, 95:270-275.
59. Jacobs R., Warren M. Sequestration of schizonts in the deep tissues of mice infected with chloroquine-resistant Plasmodium berghei. Trans. R. Soc. Trop. Med. Hyg. 1967, 61:273-275.
60. Mota M.M., et al. Antibody recognition of rodent malaria parasite antigens exposed at the infected erythrocyte surface: specificity of immunity generated in hyperimmune mice. Infect. Immun. 2001, 69:2535-2541.
61. Srivastava A., et al. Full-length extracellular region of the var2CSA variant of PfEMP1 is required for specific, high-affinity binding to CSA. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:4884-4889.
62. Beeson J.G., et al. Adhesion of Plasmodium falciparum-infected erythrocytes to hyaluronic acid in placental malaria. Nat. Med. 2000, 6:86-90.
63. Flick K., et al. Role of non-immune IgG bound to PfEMP1 in placental malaria. Science 2001, 293:2098-2100.
64. Creasey A., et al. Nonspecific immunoglobulin M binding and chondroitin sulfate A binding are linked phenotypes of Plasmodium falciparum isolates implicated in malaria during pregnancy. Infect. Immun. 2003, 71:4767-4771.
65. Rasti N., et al. Nonimmune immunoglobulin binding and multiple adhesion characterize P. falciparum-infected erythrocytes of placental origin. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:13795-13800.
66. Muthusamy A., et al. Chondroitin sulfate proteoglycan but not hyaluronic acid is the receptor for the adherence of Plasmodium falciparum-infected erythrocytes in human placenta and IRBC adherence upregulates the receptor expression. Am. J. Pathol. 2007, 170:1989-2000.
67. Janssen C.S., et al. Plasmodium interspersed repeats: the major multigene superfamily of malaria parasites. Nucleic Acids Res. 2004, 32:5712-5720.
68. Cunningham D., et al. The pir multigene family of Plasmodium: antigenic variation and beyond. Mol. Biochem. Parasitol. 2010, 170:65-73.
69. Druilhe P., et al. The importance of models of infection in the study of disease resistance. Trends Microbiol. 2002, 10:S38-S46.
70. Giobbia M., et al. Late recrudescence of Plasmodium falciparum malaria in a pregnant woman: a case report. Int. J. Infect. Dis. 2005, 9:234-235.
71. Poilane I., et al. Découverte fortuite de paludisme à Plasmodium falciparum au cours de la grossesse: à propos de deux cas. Gynecol. Obstet. Fertil. 2009, 37:824-826.
72. Brabin B.J., et al. The sick placenta - The role of malaria. Placenta 2004, 25:359-378.
73. Fried M., et al. Maternal antibodies block malaria. Nature 1998, 395:851-852.
74. Archibald H.M. The influence of malarial infection of the placenta on the incidence of prematurity. Bull. World Health Organ. 1956, 15:842-845.
75. Cannon D.S. Malaria and prematurity in the western region of Nigeria. Br. Med. J. 1958, 2:877-878.
76. Diagne N., et al. Increased susceptibility to malaria during the early postpartum period. N. Engl. J. Med. 2000, 343:598-603.