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The vertical transmission following the reactivation of a Neospora caninum chronic infection does not seem to be due to an alteration of the systemic immune response in pregnant CBA/Ca mice

Published online by Cambridge University Press:  01 March 2004

C. RETTIGNER ,
F. DE MEERSCHMAN ,
C. FOCANT ,
A. VANDERPLASSCHEN  and
B. LOSSON
C. RETTIGNER
Affiliation:
Laboratory of Parasitology and Pathology of Parasitic Diseases, Faculty of Veterinary Medicine, Department of Infectious and Parasitic Diseases, University of Liège, Boulevard de Colonster, 20, 4000, Liège, Belgium
F. DE MEERSCHMAN
Affiliation:
Laboratory of Parasitology and Pathology of Parasitic Diseases, Faculty of Veterinary Medicine, Department of Infectious and Parasitic Diseases, University of Liège, Boulevard de Colonster, 20, 4000, Liège, Belgium
C. FOCANT
Affiliation:
Laboratory of Parasitology and Pathology of Parasitic Diseases, Faculty of Veterinary Medicine, Department of Infectious and Parasitic Diseases, University of Liège, Boulevard de Colonster, 20, 4000, Liège, Belgium
A. VANDERPLASSCHEN
Affiliation:
Immunology-Vaccinology, Faculty of Veterinary Medicine, Department of Infectious and Parasitic Diseases, University of Liège, B436 Boulevard de Colonster, 20, 4000, Liège, Belgium
B. LOSSON
Affiliation:
Laboratory of Parasitology and Pathology of Parasitic Diseases, Faculty of Veterinary Medicine, Department of Infectious and Parasitic Diseases, University of Liège, Boulevard de Colonster, 20, 4000, Liège, Belgium
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Abstract

The factors responsible for the reactivation of a Neospora caninum latent infection are unknown, but it is postulated that the maternal immune response could be altered during pregnancy. The immune response was investigated in N. caninum chronically infected mice during successive pregnancies as well as in non-pregnant infected mice and mice infected when pregnant. Vertical transmission was demonstrated in chronically infected mice after the first pregnancy but the rate of fœtal infection fell after further pregnancies. Non-pregnant chronically infected mice showed a marked specific proliferative response and an IgG2a isotype preferential secretion. During the course of the first pregnancy, no significant modification of the immune response was recorded. After 2 successive pregnancies, the specific cellular response showed a significant fall whereas Th2 cytokine mRNA expression was noted. At the same time, IgG1 secretion increased to reach the IgG2a level. At the third delivery, a partial restoration of the proliferative response was observed. The reactivation of N. caninum chronic infection during pregnancy does not seem to be consecutive to an immunodepression. Nevertheless, pregnancy could favour parasite multiplication in utero after an occasional spontaneous release of bradyzoites.

Keywords

Neospora caninumreactivationpregnancyimmunitychronic infectiontransmission
Type
Research Article
Information
Parasitology , Volume 128 , Issue 2 , February 2004 , pp. 149 - 160
Copyright
2004 Cambridge University Press

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References

REFERENCES

ATHANASSAKIS, I. & ICONOMIDOU, B. (1996). Cytokine production in the serum and spleen of mice from day 6 to 14 of gestation: cytokines/placenta/spleen/serum. Developmental Immunology 4, 247–255.Google Scholar
CHOI, B. C., POLGAR, K., XIAO, L. & HILL, J. A. (2000). Progesterone inhibits in-vitro embryotoxic Th1 cytokine production to trophoblast in women with recurrent pregnancy loss. Human Reproduction 15, 46–59.CrossRefGoogle Scholar
COLE, R. A., LINDSAY, D. S., BLAGBURN, B. L. & DUBEY, J. P. (1995). Vertical transmission of Neospora caninum in mice. Journal of Parasitology 81, 730–732.CrossRefGoogle Scholar
DUBEY, J. P., HATTEL, A. L., LINDSAY, D. S. & TOPPER, M. J. (1988). Neonatal Neospora caninum infection in dogs: Isolation of the causative agent and experimental transmission. Journal of American Veterinary Medical Association 193, 1259–1263.Google Scholar
EPERON, S., BRONNIMANN, K., HEMPHILL, A. & GOTTSTEIN, B. (1999). Susceptibility of B-cell deficient C57BL/6 (μMT) mice to Neospora caninum infection. Parasite Immunology 21, 225–236.CrossRefGoogle Scholar
GAZZINELLI, R., XU, Y., HIENY, S., CHEEVER, A. & SHER, A. (1992). Simultaneous depletion of CD4+ and CD8+ T lymphocytes is required to reactivate chronic infection with Toxoplasma gondii. Journal Immunology 149, 175–180.Google Scholar
GUY, C. S., WILLIAMS, D. J. L., KELLY, D. F., MacGARRY, J. W., GUY, F., BJORKMAN, C., SMITH, R. F. & TREES, A. J. (2001). Neospora caninum in persistently infected, pregnant cows: spontaneous transplacental infection is associated with an acute increase in maternal antibody. Veterinary Record 149, 443–449.CrossRefGoogle Scholar
HUNT, J. S. & JOHNSON, P. M. (1999). Immunology of reproduction. In Encyclopedia of Reproduction ( ed. Knobil, E. & Neill, J. D.), pp. 798–806. Academic Press, USA.
INNES, E. A., PANTON, W. R. M., SANDERSON, A., THOMSON, K. M., WASTLING, J. M., MALEY, S. & BUXTON, D. (1995). Induction of CD4+ and CD8+ T cell response in efferent lymph responding to Toxoplasma gondii infection: analysis of phenotype and function. Parasite Immunology 17, 151–160.CrossRefGoogle Scholar
INNES, E. A., WRIGHT, S. E., MALEY, S., RAE, A., SCHOCK, A., KIRVAR, E., BARTLEY HAMILTON, C., CAREY, I. M. & BUXTON, D. (2001). Protection against vertical transmission in bovine neosporosis. International Journal for Parasitology 31, 1523–1534.CrossRefGoogle Scholar
ITO, A., BEBO, B. F., MATEJUK, A., ZAMORA, A., SILVERMAN, M., FYFE-JOHNSON, A. & OFFNER, H. (2001). Estrogen treatment down-regulates TNF-alpha production and reduces the severity of experimental autoimmune encephalomyelitis in cytokine knockout mice. Journal of Immunology 167, 542–552.CrossRefGoogle Scholar
JENKINS, C., ROBERTS, J., WILSON, R., MACLEAN, M. A., SHILITO, J. & WALKER, J. J. (2000). Evidence of a Th1 type response associated with recurrent miscarriage. Fertility and Sterility 73, 1206–1208.CrossRefGoogle Scholar
JOSS, A., AKDIS, M., BLASER, K. & AKDIS, C. A. (2000). IL-10 directly acts on T cells by specifically altering the CD28 co-stimulation pathway. European Journal of Immunology 30, 1683–1690.3.0.CO;2-A>CrossRefGoogle Scholar
KANG, H., REMINGTON, J. S. & SUZUKI, Y. (2000). Decreased resistance of B cell-deficient mice to infection with Toxoplasma gondii despite unimpaired expression of IFN-gamma, TNF-alpha and inducible nitric oxide synthase. Journal of Immunology 164, 2629–2634.CrossRefGoogle Scholar
KHAN, I. M., SCHWARTZMAN, J. D., FONSEKA, S. & KASPER, L. H. (1997). Neospora caninum: role for immune cytokines in host immunity. Experimental Parasitology 85, 24–34.CrossRefGoogle Scholar
KOBAYASHI, A., KATAGIRI, S., KIMURA, T., OCHIAI, K. & UMEMURA, T. (2002). Steroid hormones do not reactivate Neospora caninum in ovariectomized mice. Journal of Veterinary Medical Science 64, 773–777.CrossRefGoogle Scholar
KRISHNAN, L., GUILBERT, L. J., RUSSELL, A. S., WEGMANN, T. G., MOSMANN, T. R. & BELOSEVIC, M. (1996 a). Pregnancy impairs resistance of C57BL/6 mice to Leishmania major infection and causes decreased antigen-specific IFN-gamma responses and increased production of T helper 2 cytokines. Journal of Immunology 156, 644–652.Google Scholar
KRISHNAN, L., GUILBERT, L. J., WEGMANN, T. G., BELOSEVIC, M. & MOSMANN, T. R. (1996 b). T helper 1 response against Leishmania major in pregnant C57BL/6 mice increases implantation failure and fetal resorptions. Journal of Immunology 156, 653–662.Google Scholar
LIDDELL, S., JENKINS, M. C., COLLICA, C. M. & DUBEY, J. P. (1999). Prevention of vertical transfer of Neospora caninum in Balb/c mice by vaccination. Journal of Parasitology 85, 1072–1075.CrossRefGoogle Scholar
LONG, M. T., BASZLER, T. V. & MATHISON, B. A. (1998). Comparison of intracerebral parasite load, lesion development, and systemic cytokines in mouse strains infected with Neospora caninum. Journal of Parasitology 84, 316–320.CrossRefGoogle Scholar
LONG, M. T. & BASZLER, T. V. (2000). Neutralisation of maternal IL-4 modulates congenital protozoal transmission: comparaison of innate versus acquired immune responses. Journal of Immunology 164, 4768–4774.CrossRefGoogle Scholar
MIYAURA, H. & IWATA, M. (2002). Direct and indirect inhibition of Th1 development by progesterone and glucocorticoids. Journal of Immunology 168, 1087–1094.CrossRefGoogle Scholar
O'GARRA, A. (1998). Cytokines induce the development of functionally heterogeneous T helper cell subsets. Immunity 8, 275–283.CrossRefGoogle Scholar
PARÉ, J., THURMOND, M. C. & HIETALA, S. K. (1997). Neospora caninum antibodies in cows during pregnancy as a predictor of congenital infection and abortion. Journal of Parasitology 83, 82–87.CrossRefGoogle Scholar
PETERS, M., LUTKEFELS, E., HECKEROTH, A. R. & SCHARES, G. (2001). Immunohistological and ultrastructural evidence for Neospora caninum tissue cysts in skeletal musles of naturally infected dogs and cattle. International Journal for Parasitology 31, 1144–1148.CrossRefGoogle Scholar
QUINN, H. E., MILLER, M. D. C., RYCE, C., WINDSOR, P. A. & ELLIS, J. T. (2002). Characterization of an outbred pregnant mouse model of Neospora caninum infection. Journal of Parasitology 88, 691–696.CrossRefGoogle Scholar
RAGHUPATHY, R., MAKHSEED, M., AZIZIEH, F., OMU, A., GUPTA, M. & FARHAT, R. (2000). Cytokine production by maternal lymphocytes during normal human pregnancy and in unexplained recurrent spontaneous abortion. Human Reproduction 15, 713–718.CrossRefGoogle Scholar
RITTER, D. M., KERLIN, R., SIBERT, G. & BRAKE, D. (2002). Immune factors influencing the course of infection with Neospora caninum in the murine host. Journal of Parasitology 88, 271–280.CrossRefGoogle Scholar
ROBERTS, C. W., WALKER, W. & ALEXANDER, J. (2001). Sex-associated hormones and immunity to protozoan parasites. Clinical Microbiology Reviews 14, 476–488.CrossRefGoogle Scholar
SAITO, S. (2000). Cytokine network at the feto–maternal interface. Journal of Reproductive Immunology 47, 87–103.CrossRefGoogle Scholar
SCHARES, G., PETERS, M., WURM, R., BÄRWALD, A. & CONRATHS, F. J. (1998). The efficiency of vertical transmission of Neospora caninum in dairy cattle analysed by serological techniques. Veterinary Parasitology 80, 87–98.CrossRefGoogle Scholar
SHURIN, M. R., LU, L., KALINSKI, P., STEWART-AKERS, A. M. & LOTZE, M. T. (1999). Th1/Th2 balance in cancer, transplantation and pregnancy. Springer-Verlag, Berlin.CrossRef
STENLUND, S., KINDAHL, H., MAGNUSSON, U., UGGLA, A. & BJORKMAN, C. (1999). Serum antibody profile and reproductive performance during two consecutive pregnancies of cows naturally infected with Neospora caninum. Veterinary Parasitology 85, 227–234.CrossRefGoogle Scholar
TANAKA, T., HAMADA, T., INOUE, N., NAGASAWA, H., FUJISAKI, K., SUZUKI, N. & MIKAMI, T. (2000). The role of CD4+ or CD8+ T cells in the protective immune response of BALB/c mice to Neospora caninum infection. Veteterinary Parasitology 90, 183–191.CrossRefGoogle Scholar
THURMOND, M. C. & HIETALA, S. K. (1997). Effect of congenitally acquired Neospora caninum infection on risk of abortion and subsequent abortions in dairy cattle. American Journal of Veterinary Research 58, 1381–1385.Google Scholar
ULETT, G. C., KETHEESAN, N. & HIRST, R. G. (2000). Cytokine gene expression in innately susceptible BALB/c mice and relatively resistant C57BL/6 mice during infection with virulent Burkholderia pseudomallei. Infection and Immunity 68, 2034–2042.CrossRefGoogle Scholar
WEGMANN, T. G., LIN, H., GUILBERT, L. & MOSMANN, T. R. (1993). Bidirectional cytokine interactions in the maternal–fetal relationship: is successful pregnancy a Th2 phenomenon? Immunology Today 14, 353–356.Google Scholar
WILLIAMS, D. J. L., GUY, C. S., McGARRY, J. W., GUY, F., TASKER, L., SMITH, R. F., MacEACHERN, K., CRIPPS, P. J., KELLY, D. F. & TREES, A. J. (2000). Neospora caninum-associated abortion in cattle: the time of experimentally-induced parasitaemia during gestation determines fœtal survival. Parasitology 121, 347–358.CrossRefGoogle Scholar
YAP, G., PESIN, M. & SHER, A. (2000). Cutting edge: IL-12 is required for the maintenance of IFN-gamma production in T cells mediating chronic resistance to intracellular pathogen, Toxoplasma gondii. Journal of Immunology 165, 628–632.CrossRefGoogle Scholar