Upregulation of cytokines is detected in the placentas of cattle infected with Neospora caninum and is more marked early in gestation when fetal death is observed

Infection and Immunity

Volumn 76, Issue 6, 2008, Pages 2352-2361

  Rosbottom, Anne ^a   Gibney, E Helen ^a,b   Guy, Catherine S ^a   Kipar, Anja ^b   Smith, Robert F ^b   Kaiser, Pete ^c   Trees, Alexander J ^a   Williams, Diana J L ^a  

^a LIVERPOOL SCHOOL OF TROPICAL MEDICINE   (United Kingdom)

^b UNIVERSITY OF LIVERPOOL   (United Kingdom)

^c INSTITUTE FOR ANIMAL HEALTH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 12P40; INTERLEUKIN 18; INTERLEUKIN 2; INTERLEUKIN 4; MESSENGER RNA; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CATTLE; CD4+ T LYMPHOCYTE; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENZYME LINKED IMMUNOSORBENT ASSAY; EXPERIMENTAL INFECTION; FEMALE; FETAL WELL BEING; FETUS; FETUS DEATH; GENE EXPRESSION; INFLAMMATORY INFILTRATE; LYMPHOCYTIC INFILTRATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PLACENTA; PLACENTA DISORDER; PREGNANCY; PRIORITY JOURNAL; PROTOZOAL INFECTION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TH1 CELL; TH2 CELL; TISSUE NECROSIS; ANIMAL; ANIMAL DISEASE; BREEDING; COCCIDIOSIS; GENE EXPRESSION REGULATION; GESTATIONAL AGE; METABOLISM; NEOSPORA; PARASITOLOGY; PATHOLOGY; PHYSIOLOGY; UPREGULATION;

ANIMALS; CATTLE; COCCIDIOSIS; CYTOKINES; FEMALE; FETAL DEATH; GENE EXPRESSION REGULATION; GESTATIONAL AGE; NEOSPORA; PLACENTA; PREGNANCY; PREGNANCY, ANIMAL; RNA, MESSENGER; UP-REGULATION;

EID: 46249103012     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.01780-06     Document Type: Article

References (48)

1. Andrianarivo, A. G., B. C. Barr, M. L. Anderson, J. D. Rowe, A. E. Packham, K. W. Sverlow, and P. A. Conrad. 2001. Immune responses in pregnant cattle and bovine fetuses following experimental infection with Neospora caninum. Parasitol. Res. 87:817-825.
2. Barber, E. M., M. Fazzari, and J. W. Pollard. 2005. Th1 cytokines are essential for placental immunity to Listeria monocytogenes. Infect. Immun. 73:6322-6331.
3. Barber, J. S., O. J. Holmdahl, M. R. Owen, F. Guy, A. Uggla, and A. J. Trees. 1995. Characterization of the first European isolate of Neospora caninum (Dubey, Carpenter, Speer, Topper, and Uggla). Parasitology 111(Pt. 5):563-568.
4. Bartley, P. M., E. Kirvar, S. Wright, C. Swales, I. Esteban-Redondo, D. Buxton, S. W. Maley, A. Schock, A. G. Rae, C. Hamilton, and E. A. Innes. 2004. Maternal and fetal immune responses of cattle inoculated with Neospora caninum at mid-gestation. J. Comp. Pathol. 130:81-91.
5. Baszler, T. V., M. T. Long, T. F. McElwain, and B. A. Mathison. 1999. Interferon-gamma and interleukin-12 mediate protection to acute Neospora caninum infection in BALB/c mice. Int. J. Parasitol. 29:1635-1646.
6. Bennett, W. A., S. Lagoo-Deenadayalan, N. S. Whitworth, M. N. Brackin, E. Hale, and B. D. Cowan. 1997. Expression and production of interleukin-10 by human trophoblast: relationship to pregnancy immunotolerance. Early Pregnancy 3:190-198.
7. Brown, W. C., A. C. Rice-Ficht, and D. M. Estes. 1998. Bovine type 1 and type 2 responses. Vet. Immunol. Immunopathol. 63:45-55.
8. Buxton, D., J. S. Gilmour, K. W. Angus, D. A. Blewett, and J. K. Miller. 1982. Perinatal changes in lambs infected with Toxoplasma gondii. Res. Vet. Sci. 32:170-176.
9. Chaouat, G., M. A. Assal, J. Martal, R. Raghupathy, J. F. Elliott, T. Mosmann, and T. G. Wegmann. 1995. IL-10 prevents naturally occurring fetal loss in the CBA x DBA/2 mating combination, and local defect in IL-10 production in this abortion-prone combination is corrected by in vivo injection of IFN-tau. J. Immunol. 154:4261-4268.
10. Chaouat, G., E. Menu, D. A. Clark, M. Dy, M. Minkowski, and T. G. Wegmann. 1990. Control of fetal survival in CBA x DBA/2 mice by lymphokine therapy. J. Reprod. Fertil. 89:447-458.
11. Dubey, J. P., and D. S. Lindsay. 1996. A review of Neospora caninum and neosporosis. Vet. Parasitol. 67:1-59.
12. Dungy, L. J., T. A. Siddiqi, and S. Khan. 1991. Transforming growth factor-β1 expression during placental development. Am. J. Obstet. Gynecol. 165:853-857.
13. Fest, S., A. C. Zenclussen, R. Joachim, E. Hagen, H. U. Demuth, and T. Hoffmann. 2006. Stress and substance P but not the substance P-metabolite SP5-11 trigger murine abortion by augmenting TNF-α levels at the fetomaternal interface. Scand. J. Immunol. 63:42-49.
14. Fried, M., R. O. Muga, A. O. Misore, and P. E. Duffy. 1998. Malaria elicits type 1 cytokines in the human placenta: IFN-γ and TNF-α associated with pregnancy outcomes. J. Immunol. 160:2523- 2530.
15. Gibney, E. H., A. Kipar, A. Rosbottom, C. S. Guy, R. F. Smith, U. Hetzel, A. J. Trees, and D. J. L. Williams. 2008. The extent of parasite-associated necrosis in the placenta and foetal tissues of cattle following N. caninum infection in early and late gestation correlates with foetal death. Int. J. Parasitol. 38:579-588.
16. + T lymphocytes, B cells and macrophages in fixed and paraffin embedded bovine tissue using a range of antigen recovery and signal amplification techniques. Vet. Immunol. Immunopathol. 71:321-334.
17. Innes, E. A., W. R. Panton, J. Marks, A. J. Trees, J. Holmdahl, and D. Buxton. 1995. Interferon gamma inhibits the intracellular multiplication of Neospora caninum, as shown by incorporation of 3H uracil. J. Comp. Pathol. 113:95-100.
18. Johnson, L., J. Gough, Y. Spencer, G. Hewinson, M. Vordermeier, and A. Wangoo. 2006. Immunohistochemical markers augment evaluation of vaccine efficacy and disease severity in bacillus Calmette-Guerin (BCG) vaccinated cattle challenged with Mycobacterium bovis. Vet. Immunol. Immunopathol. 111:219-229.
19. Khan, I. A., J. D. Schwartzman, S. Fonseka, and L. H. Kasper. 1997. Neospora caninum: role for immune cytokines in host immunity. Exp. Parasitol. 85:24-34.
20. Kim, S., D. S. Lee, K. Watanabe, H. Furuoka, H. Suzuki, and M. Watarai. 2005. Interferon-gamma promotes abortion due to Brucella infection in pregnant mice. BMC. Microbiol. 5:22.
21. King, A., P. P. Jokhi, S. K. Smith, A. M. Sharkey, and Y. W. Loke. 1995. Screening for cytokine mRNA in human villous and extravillous trophoblasts using the reverse-transcriptase polymerase chain reaction (RT-PCR). Cytokine 7:364-371.
22. Kipar, A., S. Bellmann, J. Kremendahl, K. Kohler, and M. Reinacher. 1998. Cellular composition, coronavirus antigen expression and production of specific antibodies in lesions in feline infectious peritonitis. Vet. Immunol. Immunopathol. 65:243-257.
23. 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-γ and TNF and reduced IL-10 production by placental cells. J. Immunol. 156:653-662.
24. Li, M. O., Y. Y. Wan, S. Sanjabi, A. K. Robertson, and R. A. Flavell. 2006. Transforming growth factor-beta regulation of immune responses. Annu. Rev. Immunol. 24:99-146.
25. Lin, H., T. R. Mosmann, L. Guilbert, S. Tuntipopipat, and T. G. Wegmann. 1993. Synthesis of T helper 2-type cytokines at the maternal-fetal interface. J. Immunol. 151:4562-4573.
26. Long, M. T., T. V. Baszler, and B. A. Mathison. 1998. Comparison of intracerebral parasite load, lesion development, and systemic cytokines in mouse strains infected with Neospora caninum. J. Parasitol. 84:316-320.
27. Maley, S. W., D. Buxton, C. N. Macaldowie, I. E. Anderson, S. E. Wright, P. M. Bartley, I. Esteban-Redondo, C. M. Hamilton, A. K. Storset, and E. A. Innes. 2006. Characterization of the immune response in the placenta of cattle experimentally infected with Neospora caninum in early gestation. J. Comp. Pathol. 135:130-141.
28. + T cells and immune sera from experimentally infected cattle. Parasite Immunol. 20:303-309.
29. 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.
30. Munson, L., A. Wilhite, V. F. Boltz, and J. E. Wilkinson. 1996. Transforming growth factor beta in bovine placentas. Biol. Reprod. 55:748-755.
31. Nagaeva, O., L. Jonsson, and L. Mincheva-Nilsson. 2002. Dominant IL-10 and TGF-β mRNA expression in γδT cells of human early pregnancy decidua suggests immunoregulatory potential. Am. J. Reprod. Immunol. 48:9-17.
32. Piccinni, M. P., L. Beloni, C. Livi, E. Maggi, G. Scarselli, and S. Romagnani. 1998. Defective production of both leukemia inhibitory factor and type 2 T-helper cytokines by decidual T cells in unexplained recurrent abortions. Nat. Med. 4:1020-1024.
33. Pyeon, D., K. L. O'Reilly, and G. A. Splitter. 1996. Increased interleukin-10 mRNA expression in tumor-bearing or persistently lymphocytotic animals infected with bovine leukemia virus. J. Virol. 70:5706-5710.
34. Quinn, H. E., J. T. Ellis, and N. C. Smith. 2002. Neospora caninum: a cause of immune-mediated failure of pregnancy? Trends Parasitol. 18:391-394.
35. Quinn, H. E., C. M. Miller, and J. T. Ellis. 2004. The cell-mediated immune response to Neospora caninum during pregnancy in the mouse is associated with a bias toward production of interleukin-4. Int. J. Parasitol. 34:723-732.
36. Raghupathy, R. 1997. Th1-type immunity is incompatible with successful pregnancy. Immunol. Today 18:478-482.
37. Rosbottom, A., C. S. Guy, E. H. Gibney, R. F. Smith, J. F. Valarcher, G. Taylor, and D. J. Williams. 2007. Peripheral immune responses in pregnant cattle following Neospora caninum infection. Parasite Immunol. 29:219-228.
38. Sollwedel, A., A. Z. Bertoja, M. L. Zenclussen, K. Gerlof, U. Lisewski, P. Wafula, B. Sawitzki, C. Woiciechowsky, H. D. Volk, and A. C. Zenclussen. 2005. Protection from abortion by heme oxygenase-1 up-regulation is associated with increased levels of Bag-1 and neuropilin-1 at the fetal-maternal interface. J. Immunol. 175:4875-4885.
39. + cytotoxic T lymphocytes. Infect. Immun. 71:3272-3279.
40. Tezabwala, B. U., P. M. Johnson, and R. C. Rees. 1989. Inhibition of pregnancy viability in mice following IL-2 administration. Immunology 67:115-119.
41. Trees, A. J., and D. J. Williams. 2005. Endogenous and exogenous transplacental infection in Neospora caninum and Toxoplasma gondii. Trends Parasitol. 21:558-561.
42. 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.
43. Williams, D. J., H. C. Davison, B. Helmick, J. McGarry, F. Guy, A. Otter, and A. J. Trees. 1999. Evaluation of a commercial ELISA for detecting serum antibody to Neospora caninum in cattle. Vet. Rec. 145:571-575.
44. Williams, D. J., C. S. Guy, J. W. McGarry, F. Guy, L. Tasker, R. F. Smith, K. MacEachern, P. J. Cripps, D. F. Kelly, and A. J. Trees. 2000. Neospora caninum-associated abortion in cattle: the time of experimentally-induced parasitaemia during gestation determines fetal survival. Parasitology 121(Pt. 4):347-358.
45. Williams, D. J., J. McGarry, F. Guy, J. Barber, and A. J. Trees. 1997. Novel ELISA for detection of Neospora-specific antibodies in cattle. Vet. Rec. 140:328-331.
46. Zenclussen, A. C., R. Joachim, E. Hagen, C. Peiser, B. F. Klapp, and P. C. Arck. 2002. Heme oxygenase is downregulated in stress-triggered and interleukin-12-mediated murine abortion. Scand. J. Immunol. 55:560-569.
47. Zenclussen, A. C., A. Sollwedel, A. Z. Bertoja, K. Gerlof, M. L. Zenclussen, C. Woiciechowsky, and H. D. Volk. 2005. Heme oxygenase as a therapeutic target in immunological pregnancy complications. Int. Immunopharmacol. 5:41-51.
48. Zenclussen, A. C., K. Gerlof, M. L. Zenclussen, S. Ritschel, A. Z. Bertoja, S. Fest, S. Hontsu, S. Ueha, K. Matshushima, J. Leber, and H. D. Volk. 2006. Regulatory T cells induce a privileged tolerant microenvironment at the fetal-maternal interface. Eur. J. Immunol. 36:82-94.