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T cell-dependent elimination of dividing Trypanosoma grosi from the bloodstream of Mongolian jirds

Published online by Cambridge University Press:  03 March 2004

H. SATO ,
K. ISHITA ,
A. OSANAI ,
M. YAGISAWA ,
H. KAMIYA  and
M. ITO
H. SATO
Affiliation:
Department of Parasitology, Hirosaki University School of Medicine, Hirosaki 036-8562, Japan
K. ISHITA
Affiliation:
Department of Parasitology, Hirosaki University School of Medicine, Hirosaki 036-8562, Japan
A. OSANAI
Affiliation:
Department of Parasitology, Hirosaki University School of Medicine, Hirosaki 036-8562, Japan
M. YAGISAWA
Affiliation:
Department of Parasitology, Hirosaki University School of Medicine, Hirosaki 036-8562, Japan
H. KAMIYA
Affiliation:
Department of Parasitology, Hirosaki University School of Medicine, Hirosaki 036-8562, Japan
M. ITO
Affiliation:
Laboratory of Immunology, Central Institute for Experimental Animals, Kawasaki 216-0001, Japan
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Abstract

Mongolian jirds, Meriones unguiculatus, are susceptible to infection with Trypanosoma grosi, which naturally parasitizes Apodemus spp. The present study investigated T cell dependence of elimination of T. grosi from the bloodstream of jirds by in vivo T cell depletion using a monoclonal antibody (HUSM-M.g.15). In T cell-depleted jirds, elimination of T. grosi, particularly the dividing forms, from the bloodstream was significantly delayed, occurring at around week 3 p.i. The kinetics of serum levels of IgM and IgG specific to trypanosomes in T cell-depleted and control immunocompetent jirds were different; peak levels of IgM were noted on days 6–8 p.i. around the time of peak parasitaemia (day 6 p.i.) in immunocompetent jirds, whereas the serum levels began to increase abruptly after day 10 p.i., peaking at around day 18 p.i. in T cell-depleted jirds. Similarly, serum IgG increased after day 6 p.i. in immunocompetent jirds, in contrast to after day 12 p.i. in T cell-depleted jirds, and the level increased steadily even after disappearance of parasitaemia. Our findings indicate that T cells play a major role at least in the ‘first crisis’ during elimination of dividing T. grosi from the bloodstream.

Keywords

Trypanosoma grosiMeriones unguiculatuseliminationT cellparasitaemiahumoral immune response
Type
Research Article
Information
Parasitology , Volume 128 , Issue 3 , March 2004 , pp. 295 - 304
Copyright
2004 Cambridge University Press

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References

REFERENCES

ALBRIGHT, J. W. & ALBRIGHT, J. F. (1991). Rodent trypanosomes: their conflict with the immune system of the host. Parasitology Today 7, 137–140.CrossRefGoogle Scholar
ALBRIGHT, J. W., PIERANTONI, M. & ALBRIGHT, J. F. (1990). Immune and nonimmune regulation of the population of Trypanosoma musculi in infected host mice. Infection and Immunity 58, 1757–1762.Google Scholar
BROOKS, B. O. & REED, N. D. (1977). Thymus dependency of Trypanosoma musculi elimination from mice. Journal of the Reticuloendothelial Society 22, 605–608.Google Scholar
DESBIENS, C. & VIENS, P. (1981). Trypanosoma musculi in CBA mice: trypanocidal mechanism eliminating dividing forms. Parasitology 83, 109–113.CrossRefGoogle Scholar
DUSANIC, D. G. (1975). Trypanosoma musculi infections in complement-deficient mice. Experimental Parasitology 37, 205–210.CrossRefGoogle Scholar
FERRANTE, A. (1986). The role of the macrophage in immunity to Trypanosoma musculi. Parasite Immunology 8, 117–127.CrossRefGoogle Scholar
HANSON, W. L. & CHAPMAN, W. L., Jr. (1974). Comparison of the effects of neonatal thymectomy on Plasmodium berghei, Trypanosoma lewisi and Trypanosoma cruzi infection in the albino rat. Zeitschrift für Parasitenkunde 44, 227–238.CrossRefGoogle Scholar
HOARE, C. A. (1972). The Trypanosomes of Mammals. Blackwell Scientific Publications, Oxford.
HORII, Y., KHAN, A. I. & NAWA, Y. (1993). Persistent infection of Strongyloides venezuelensis and normal expulsion of Nippostrongylus brasiliensis in Mongolian gerbil, Meriones unguiculatus, with reference to the cellular responses in the intestinal mucosa. Parasite Immunology 15, 175–179.CrossRefGoogle Scholar
HOUSE, R. V. & DEAN, J. H. (1988 a). Trypanosoma musculi: characterization of the T-lymphocyte dependency of immunity by selective immunomodulation of the mouse, Mus musculus. Experimental Parasitology 67, 104–115.Google Scholar
HOUSE, R. V. & DEAN, J. H. (1988 b). Adoptive cell transfer studies to examine the role of T lymphocytes in immunity to Trypanosoma musculi. Journal of Parasitology 74, 819–827.Google Scholar
JARVINEN, J. A. & DALMASSO, A. P. (1977). Trypanosoma musculi infections in normocomplementemic, C5-deficient, and C3-depleted mice. Infection and Immunity 16, 557–563.Google Scholar
KAMIYA, M. & SATO, H. (1990). Complete life cycle of the canid tapeworm, Echinococcus multilocularis, in laboratory rodents. FASEB Journal 4, 3334–3339.CrossRefGoogle Scholar
KHAN, A. I., HORII, Y. & NAWA, Y. (1993). Defective mucosal immunity and normal systemic immunity of Mongolian gerbils, Meriones unguiculatus, to reinfection with Strongyloides venezuelensis. Parasite Immunology 15, 565–571.CrossRefGoogle Scholar
KONGSHAVN, P. A. L., SHAW, K., GHADIRIAN, E. & ULCZAK, O. (1990). Failure to demonstrate a major role for Kupffer cells and radiosensitive leukocytes in immunoglobulin-mediated elimination of Trypanosoma musculi. Infection and Immunity 58, 1971–1978.Google Scholar
KRAMPITZ, H. E. (1961). Kritisches zur Taxonomie und Systematik parasitischer Säugetier-Trypanosomen mit besonderer Beachtung einiger die in Wühlmäusen verbreiteten spezifischen Formen. Zeitschrift für Tropenmedizin und Parasitologie 12, 117–137.Google Scholar
MARUYAMA, H., KOBAYASHI, T., TSUCHIYA, K., HORII, Y. & NAWA, Y. (1994). Sensitive enzyme-linked immunosorbent assay (ELISA) method to measure parasite-specific antibodies of Mongolian gerbils. Japanese Journal of Parasitology 43, 351–357.Google Scholar
MOHANTY, M. C. & RABINDRAN, B. (2002). Deficiency of antibody responses to T-independent antigens in gerbils – Meriones unguiculatus. Developmental and Comparative Immunology 26, 385–391.CrossRefGoogle Scholar
MÜHLPFORDT, H. (1969). Die Entwicklung von Trypanosoma lewisi in Meriones unguiculatus bei zusätzlicher Bartonella-Infection. Zeitschrift für Tropenmedizin und Parasitologie 20, 136–144.Google Scholar
NOYES, H. A., AMBROSE, P., BARKER, F., BEGON, M., BENNET, M., BOWN, K. J. & KEMP, S. J. (2002). Host specificity of Trypanosoma (Herpetosoma) species: evidence that bank voles (Clethrionomys glareolus) carry only one T. (H.) evotomys 18S rRNA genotype but wood mice (Apodemus sylvaticus) carry at least two polyphyletic parasites. Parasitology 124, 185–190.Google Scholar
POULIOT, P., VIENS, P. & TARGETT, G. A. T. (1977). T-lymphocytes and the transfer of immunity to Trypanosoma musculi in mice. Clinical and Experimental Immunology 27, 507–511.Google Scholar
RANK, R. G., ROBERTS, D. W. & WEIDANZ, W. P. (1977). Chronic infection with Trypanosoma musculi in congenitally athymic nude mice. Infection and Immunity 16, 715–716.Google Scholar
SATO, H. & KAMIYA, H. (2001). Defect of protective immunity to Schistosoma mansoni infection in Mongolian gerbils involves limited recruitment of dendritic cells in the vaccinated skin. Parasite Immunology 23, 627–632.CrossRefGoogle Scholar
SATO, H., CHISTY, M. & KAMIYA, H. (2000). Anti-Thy-1 monoclonal antibody-induced glomerulonephritis in Mongolian gerbils. Comparative Medicine 50, 603–608.Google Scholar
SATO, H., IHAMA, Y. & KAMIYA, H. (2000). Survival of destrobilated adults of Taenia crassiceps in T cell-depleted Mongolian gerbils. Parasitology Research 86, 284–289.CrossRefGoogle Scholar
SATO, H., INABA, T. & KAMIYA, H. (1997). Production of murine monoclonal antibodies to guinea pig leukocytes and immunohistochemistry of guinea pig skin exposed to Schistosoma mansoni. Hybridoma 16, 529–536.CrossRefGoogle Scholar
SATO, H., CHISTY, M., NARGIS, M., INABA, T., YAGISAWA, M. & KAMIYA, H. (2001). Monoclonal antibodies reactive with dendritic cells of Mongolian gerbils. Comparative Medicine 51, 234–238.Google Scholar
SATO, H., ISHITA, K., MATSUO, K., INABA, T., KAMIYA, H. & ITO, M. (2003). Persistent infection of Mongolian jirds with a non-pathogenic trypanosome, Trypanosoma (Herpetosoma) grosi. Parasitology 127, 357–363.CrossRefGoogle Scholar
SEBEK, Z. (1978). Blood parasites of small mammals in western Hungary. Parasitologia Hungarica 11, 17–22.Google Scholar
SEBEK, Z., SIXL, W., STUNZNER, D., VALOVA, M., HUBALEK, Z. & TROGER, H. (1980). The blood parasites of wild small mammals in Steinermark and Burgenland, Austria. Folia Parasitologica 27, 295–301 (in German with English summary).Google Scholar
TARGETT, G. A. T. & VIENS, P. (1975). The immunological response of CBA mice to Trypanosoma musculi: elimination of the parasite from the blood. International Journal for Parasitology 5, 231–234.CrossRefGoogle Scholar
TARGETT, G. A. T., LEUCHARS, E., DAVIES, A. J. S. & VIENS, P. (1981). Thymus graft reconstitution of T cell-deprived mice infected with Trypanosoma musculi. Parasite Immunology 3, 353–358.CrossRefGoogle Scholar
TRUDEL, L., DESBIENS, C., VIENS, P. & TARGETT, G. A. T. (1982). Ablastin and the control of Trypanosoma musculi infections in mice. Parasite Immunology 4, 149–156.CrossRefGoogle Scholar
VARGAS, F. D. C., VIENS, P. & KONGSHAVN, P. A. L. (1984). Trypanosoma musculi infection in B-cell-deficient mice. Infection and Immunity 44, 162–167.Google Scholar
VIENS, P. (1985). Immunology of nonpathogenic trypanosomes of rodents. In Immunology and Pathogenesis of Trypanosomiasis (ed. Tizard, I.), pp. 201–223. CRC Press, Boca Raton, Florida.
VIENS, P., POULIET, P. & TARGETT, G. A. T. (1973). Cell-mediated immunity during the infection of CBA mice with Trypanosoma musculi. Canadian Journal of Microbiology 19, 105–106.Google Scholar
VIENS, P., TARGETT, G. A. T., LEUCHARDS, E. & DAVIES, A. J. S. (1974). The immunological response of CBA mice to Trypanosoma musculi: I. Initial control of the infection and the effect of T cell deprivation. Clinical and Experimental Immunology 16, 279–294.Google Scholar
VIENS, P., TARGETT, G. A. T., WILSON, V. C. L. C. & EDWARDS, C. I. (1972). The persistence of Trypanosoma (Herpetosoma) musculi in the kidneys of immune CBA mice. Transactions of the Royal Society of Tropical Medicine and Hygiene 66, 669–670.CrossRefGoogle Scholar
VINCENDEAU, P., DAERON, M. & DAULOUEDE, S. (1986). Identification of antibody classes and Fc receptors responsible for phagocytosis of Trypanosoma musculi by mouse macrophages. Infection and Immunity 53, 600–605.Google Scholar
VINCENDEAU, P., DAULOUEDE, S. & VEYRET, B. (1989). Role of hypochlorous acid in Trypanosoma musculi killing by phagocytes. Parasitology 98, 253–257.CrossRefGoogle Scholar
WECHSLER, D. S. & KONGSHAVN, P. A. L. (1985). Characterization of antibodies mediating protection and cure of Trypanosoma musculi infection in mice. Infection and Immunity 48, 787–794.Google Scholar
WECHSLER, D. S. & KONGSHAVN, P. A. L. (1988). Further characterization of the curative antibodies in Trypanosoma musculi infection. Infection and Immunity 56, 2379–2384.Google Scholar
WILSON, V. C. L. C., VIENS, P., TARGETT, G. A. T. & EDWARDS, C. I. (1973). Comparative studies on the persistence of Trypanosoma (Herpetosoma) musculi and T. (H.) lewisi in immune hosts. Transactions of the Royal Society of Tropical Medicine and Hygiene 67, 271–272.Google Scholar