Association of malaria-induced murine pregnancy failure with robust peripheral and placental cytokine responses

Infection and Immunity

Volumn 77, Issue 11, 2009, Pages 4998-5006

  Poovassery, Jayakumar ^a,b   Moore, Julie M ^a  

^a UNIVERSITY OF GEORGIA   (United States)

^b UNIVERSITY OF IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; HEMOZOIN; INTERLEUKIN 10; INTERLEUKIN 1BETA; TUMOR NECROSIS FACTOR; TUMOR NECROSIS FACTOR RECEPTOR 2;

ABORTION; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL CULTURE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE ASSOCIATION; ERYTHROCYTE; FEMALE; FETUS WASTAGE; GIANT CELL; HISTOPATHOLOGY; IMMUNE RESPONSE; IMMUNOPATHOGENESIS; MALARIA; MOUSE; NONHUMAN; PHAGOCYTOSIS; PLACENTA; PLASMA; PLASMODIUM CHABAUDI; PREGNANCY; PREGNANCY DISORDER; PRIORITY JOURNAL; SPLEEN; TROPHOBLAST; TUMOR NECROSIS;

ANIMALS; CYTOKINES; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; MALARIA; MICE; MICE, INBRED C57BL; PLACENTA; PLASMODIUM CHABAUDI; PREGNANCY; PREGNANCY COMPLICATIONS, PARASITIC;

EID: 70350463864     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00617-09     Document Type: Article

References (45)

1. Aderka, D., H. Engelmann, Y. Maor, C. Brakebusch, and D. Wallach. 1992. Stabilization of the bioactivity of tumor necrosis factor by its soluble receptors. J. Exp. Med. 175:323-329.
2. Albieri, A., M. S. Hoshida, S. M. Gagioti, E. C. Leanza, I. Abrahamsohn, A. Croy, A. A. Ashkar, and E. Bevilacqua. 2005. Interferon-gamma alters the phagocytic activity of the mouse trophoblast. Reprod. Biol. Endocrinol. 3:34.
3. Ashkar, A. A., J. P. Di Santo, and B. A. Croy. 2000. Interferon gamma contributes to initiation of uterine vascular modification, decidual integrity, and uterine natural killer cell maturation during normal murine pregnancy. J. Exp. Med. 192:259-270.
4. Chang, K. H., M. Tam, and M. M. Stevenson. 2004. Modulation of the course and outcome of blood-stage malaria by erythropoietin-induced reticulocytosis. J. Infect. Dis. 189:735-743.
5. Chaouat, G., E. Menu, D. de Smedt, L. Khrihnan, L. Hui, A. Assal Meliani, J. Martal, R. Raghupathy, and T. G. Wegmann. 1996. The emerging role of IL-10 in pregnancy. Am. J. Reprod. Immunol. 35:325-329.
6. Clark, D. A., G. Chaouat, P. C. Arck, H. W. Mittruecker, and G. A. Levy. 1998. Cytokine-dependent abortion in CBA x DBA/2 mice is mediated by the procoagulant fgl2 prothombinase. J. Immunol. 160:545-549.
7. Clark, I. A., and G. Chaudhri. 1988. Tumor necrosis factor in malariainduced abortion. Am. J. Trop. Med. Hyg. 39:246-249.
8. Davison, B. B., F. B. Cogswell, G. B. Baskin, K. P. Falkenstein, E. W. Henson, and D. J. Krogstad. 2000. Placental changes associated with fetal outcome in the Plasmodium coatneyi/rhesus monkey model of malaria in pregnancy. Am. J. Trop. Med. Hyg. 63:158-173.
9. Davison, B. B., M. B. Kaack, L. B. Rogers, K. K. Rasmussen, T. A. Rasmussen, E. W. Henson, M. C. Henson, F. K. Parekh, and D. J. Krogstad. 2006. The role of soluble tumor necrosis factor receptor types I and II and tumor necrosis factor-alpha in malaria during pregnancy. J. Infect. Dis. 194:123-132.
10. Desai, M., F. O. Ter Kuile, F. Nosten, R. McGready, K. Asamoa, B. Brabin, and R. D. Newman. 2007. Epidemiology and burden of malaria in pregnancy. Lancet Infect. Dis. 7:93-104.
11. Francischetti, I. M. 2008. Does activation of the blood coagulation cascade have a role in malaria pathogenesis? Trends Parasitol. 24:258-263.
12. Fried, M., R. O. Muga, A. O. Misore, and P. E. Duffy. 1998. Malaria elicits type 1 cytokines in the human placenta: IFN-gamma and TNF-alpha associated with pregnancy outcomes. J. Immunol. 160:2523-2530. (Pubitemid 28119939)
13. Guleria, I., and J. W. Pollard. 2000. The trophoblast is a component of the innate immune system during pregnancy. Nat. Med. 6:589-593.
14. Haider, S., and M. Knofler. 2009. Human tumour necrosis factor: physiological and pathological roles in placenta and endometrium. Placenta 30: 111-123.
15. Haimovici, F., J. A. Hill, and D. J. Anderson. 1991. The effects of soluble products of activated lymphocytes and macrophages on blastocyst implantation events in vitro. Biol. Reprod. 44:69-75.
16. Ing, R., M. Segura, N. Thawani, M. Tam, and M. M. Stevenson. 2006. Interaction of mouse dendritic cells and malaria-infected erythrocytes: uptake, maturation, and antigen presentation. J. Immunol. 176:441-450. (Pubitemid 43023290)
17. Jacobs, P., D. Radzioch, and M. M. Stevenson. 1996. 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. Infect. Immun. 64:44-49.
18. Jacobs, P., D. Radzioch, and M. M. Stevenson. 1996. A Th1-associated increase in tumor necrosis factor alpha expression in the spleen correlates with resistance to blood-stage malaria in mice. Infect. Immun. 64:535-541.
19. Kern, P., C. J. Hemmer, H. Gallati, S. Neifer, P. Kremsner, M. Dietrich, and F. Porzsolt. 1992. Soluble tumor necrosis factor receptors correlate with parasitemia and disease severity in human malaria. J. Infect. Dis. 166:930-934.
20. Kohno, T., M. T. Brewer, S. L. Baker, P. E. Schwartz, M. W. King, K. K. Hale, C. H. Squires, R. C. Thompson, and J. L. Vannice. 1990. A second tumor necrosis factor receptor gene product can shed a naturally occurring tumor necrosis factor inhibitor. Proc. Natl. Acad. Sci. USA 87:8331-8335.
21. Krishnan, L., L. J. Guilbert, T. G. Wegmann, M. Belosevic, and T. R. Mosmann. 1996. 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. 156:653-662.
22. Langhorne, J., S. Gillard, B. Simon, S. Slade, and K. Eichmann. 1989. Frequencies of CD4 T cells reactive with Plasmodium chabaudi chabaudi: distinct response kinetics for cells with Th1 and Th2 characteristics during infection. Int. Immunol. 1:416-424.
23. Li, C., L. A. Sanni, F. Omer, E. Riley, and J. Langhorne. 2003. 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 beta antibodies. Infect. Immun. 71:4850-4856.
24. Long, G. H., B. H. Chan, J. E. Allen, A. F. Read, and A. L. Graham. 2008. Experimental manipulation of immune-mediated disease and its fitness costs for rodent malaria parasites. BMC Evol. Biol. 8:128.
25. Lucchi, N. W., R. Koopman, D. S. Peterson, and J. M. Moore. 2006. Plasmodium falciparum-infected red blood cells selected for binding to cultured syncytiotrophoblast bind to chondroitin sulfate A and induce tyrosine phosphorylation in the syncytiotrophoblast. Placenta 27:384-394.
26. Lucchi, N. W., D. S. Peterson, and J. M. Moore. 2008. Immunologic activation of human syncytiotrophoblast by Plasmodium falciparum. Malaria J. 7:42.
27. Marzi, M., A. Vigano, D. Trabattoni, M. L. Villa, A. Salvaggio, E. Clerici, and M. Clerici. 1996. Characterization of type 1 and type 2 cytokine production profile in physiologic and pathologic human pregnancy. Clin. Exp. Immunol. 106:127-133.
28. Mohan, K., P. Moulin, and M. M. Stevenson. 1997. Natural killer cell cytokine production, not cytotoxicity, contributes to resistance against blood-stage Plasmodium chabaudi AS infection. J. Immunol. 159:4990-4998. (Pubitemid 127471037)
29. Moore, K. W., R. de Waal Malefyt, R. L. Coffman, and A. O'Garra. 2001. Interleukin-10 and the interleukin-10 receptor. Annu. Rev. Immunol. 19: 683-765.
30. Moormann, A. M., A. D. Sullivan, R. A. Rochford, S. W. Chensue, P. J. Bock, T. Nyirenda, and S. R. Meshnick. 1999. Malaria and pregnancy: placental cytokine expression and its relationship to intrauterine growth retardation. J. Infect. Dis. 180:1987-1993.
31. Neres, R., C. R. Marinho, L. A. Goncalves, M. B. Catarino, and C. Penha- Goncalves. 2008. Pregnancy outcome and placenta pathology in Plasmodium berghei ANKA infected mice reproduce the pathogenesis of severe malaria in pregnant women. PLoS One 3:e1608. (Pubitemid 351850774)
32. Ordi, J., M. R. Ismail, P. J. Ventura, E. Kahigwa, R. Hirt, A. Cardesa, P. L. Alonso, and C. Menendez. 1998. Massive chronic intervillositis of the placenta associated with malaria infection. Am. J. Surg. Pathol. 22: 1006-1011.
33. Pavia, C. S. 1983. Expression of cell-mediated antimicrobial immunity by mouse trophoblast monolayers. J. Infect. Dis. 147:1006-1010.
34. Piccinni, M. P., C. Scaletti, A. Vultaggio, E. Maggi, and S. Romagnani. 2001. Defective production of LIF, M-CSF and Th2-type cytokines by T cells at fetomaternal interface is associated with pregnancy loss. J. Reprod. Immunol. 52:35-43.
35. Platt, J. S., and J. S. Hunt. 1998. Interferon-gamma gene expression in cycling and pregnant mouse uterus: temporal aspects and cellular localization. J. Leuk. Biol. 64:393-400.
36. Poovassery, J., and J. M. Moore. 2006. Murine malaria infection induces fetal loss associated with accumulation of Plasmodium chabaudi AS-infected erythrocytes in the placenta. Infect. Immun. 74:2839-2848.
37. Poovassery, J., D. Sarr, G. Smith, T. Nagy, and J. M. Moore. Malariainduced murine pregnancy failure: distinct roles for IFN-γ and TNF. J. Immunol., in press.
38. Rockett, K. A., M. M. Awburn, E. J. Rockett, and I. A. Clark. 1994. Tumor necrosis factor and interleukin-1 synergy in the context of malaria pathology. Am. J. Trop. Med. Hyg. 50:735-742.
39. Rogerson, S. J., H. C. Brown, E. Pollina, E. T. Abrams, E. Tadesse, V. M. Lema, and M. E. Molyneux. 2003. Placental tumor necrosis factor alpha but not gamma interferon is associated with placental malaria and low birth weight in Malawian women. Infect. Immun. 71:267-270.
40. Stevenson, M. M., M. F. Tam, S. F. Wolf, and A. Sher. 1995. IL-12-induced protection against blood-stage Plasmodium chabaudi AS requires IFNgamma and TNF-alpha and occurs via a nitric oxide-dependent mechanism. J. Immunol. 155:2545-2556.
41. Su, Z., and M. M. Stevenson. 2000. Central role of endogenous gamma interferon in protective immunity against blood-stage Plasmodium chabaudi AS infection. Infect. Immun. 68:4399-4406.
42. Su, Z., and M. M. Stevenson. 2002. IL-12 is required for antibody-mediated protective immunity against blood-stage Plasmodium chabaudi AS malaria infection in mice. J. Immunol. 168:1348-1355. (Pubitemid 34094505)
43. Taylor-Robinson, A. W., and R. S. Phillips. 1998. Infective dose modulates the balance between Th1- and Th2-regulated immune responses during blood-stage malaria infection. Scandinavian J. Immunol. 48:527-534.
44. Wegmann, T. G., H. Lin, L. Guilbert, and T. R. Mosmann. 1993. Bidirectional cytokine interactions in the maternal-fetal relationship: is successful pregnancy a TH2 phenomenon? Immunol. Today 14:353-356.
45. Yui, J., M. Garcia-Lloret, T. G. Wegmann, and L. J. Guilbert. 1994. Cytotoxicity of tumour necrosis factor-alpha and gamma-interferon against primary human placental trophoblasts. Placenta 15:819-835.