Hostname: page-component-586b7cd67f-gb8f7 Total loading time: 0 Render date: 2024-11-25T18:03:19.419Z Has data issue: false hasContentIssue false
  • English
  • Français

Manipulation of the immune response in parasitic infections

Published online by Cambridge University Press:  23 August 2011

J.G. Howard
J.G. Howard
Affiliation:
Biomedical Research Division, The Wellcome Research Laboratories, Beckenham, Kent, BR3 3BS
Get access Rights & Permissions [Opens in a new window]

Extract

The following brief survey considers various manoeuvres which can be applied to manipulate the immune response to parasitic infections in vivo. The examples quoted largely concern malaria, babesiosis, schistosomiasis and leishmaniasis, predominantly in inbred mouse strains. Since my own relevant research experience has been restricted to leishmaniasis, this will receive undue emphasis, although it does illustrate particularly well points I wish to stress. The types of intervention described do not all provide the precision of interpretation with which they are sometimes credited. Thus, effects of immunosuppression or T-cell depletion alone can usually only implicate the specific immune response (in its broad sense) in shaping the natural history and outcome of an infection or in underlying the effect of prophylactic immunization. Nevertheless, more precise delineation of lymphocyte subset involvement can be obtained by cell replacement studies in some of these models or by exclusion of antibody. The outcomes of these approaches have been (or are) predictable in most cases. More fascinating, however, are the various instances which will be stressed where totally unpredicted and contrary observations have been made which led (or may lead) to fresh insight into the disease. These serendipitous findings illustrate at the same time the value of applying the manoeuvres, even though they imply that the logical immunologist cannot yet always outsmart the parasite by design.

Type
Research Article
Information
Parasitology , Volume 88 , Issue 4: Symposia of the British Society for Parasitology Volume 21: Parasite evasion of the immune response , August 1984 , pp. 665 - 675
Copyright
Copyright © Cambridge University Press 1984

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Alexander, J. (1978). Effect of cyclophosphamide treatment on the course of Mycobacterium lepraemurium infection and development of delayed-type hypersensitivity reactions in C57BL and BALB/c mice. Clinical and Experimental Immunology 34, 52–8.Google ScholarPubMed
Allison, A. C., Christensen, J., Clark, I. A., Elford, B. C. & Euoui, E. M. (1979). The role of the spleen in protection against murine babesia infections. In Tropical Diseases Research Series: 1 (W.H.O.), pp. 151–82. Basel: Schwabe.Google Scholar
Bazin, H., Capron, A., Capron, M., Joseph, M., Dessaint, J.-P. & Pauwels, R. (1980). Effect of neonatal injection of anti-µi antibodies on immunity to schistosomes (S. mansoni) in the rat. Journal of Immunology 124, 2373–7.CrossRefGoogle Scholar
Belehu, A., Poulter, L. W. & Turk, J. L. (1976). Modification of cutaneous leishmaniasis in the guinea-pig by cyclophosphamide. Clinical and Experimental Immunology 24, 125–32.Google ScholarPubMed
Bout, D., Dupas, H., Carlier, Y., Afchain, D. & Capron, A. (1977). High resistance induced by young live bacillus Calmette-Guérin (BCG) to Schistosoma mansoni infection in mice. Annales d'Immunologie 128, 811–16.Google Scholar
Brown, I. N., Allison, A. C. & Taylor, R. B. (1968). Plasmodium berghei infections in thymectomized rats. Nature, London 219, 292–3.CrossRefGoogle ScholarPubMed
Bryceson, A. D. M., Preston, P. M., Bray, R. S. & Dumonde, D. C. (1972). Experimental cutaneous leishmaniasis. II. Effects of immunosuppression and antigenic competition on the course of infection with Leishmania enriettii in the guinea-pig. Clinical and Experimental Immunology 10, 305–35.Google ScholarPubMed
Bryceson, A. D. M. & Turk, J. L. (1971). The effect of prolonged treatment with antilymphocyte serum on the course of infections with BCG and Leishmania enriettii in the guinea-pig. Journal of Pathology 104, 153–65.CrossRefGoogle ScholarPubMed
Byram, J. E. & Von Lichtenberg, F. (1977). Altered schistosome granuloma formation in nude mice. American Journal of Tropical Medicine and Hygiene 26, 944–56.CrossRefGoogle ScholarPubMed
Chen, D. H., Tigelaar, R. E. & Weinbaum, P. I. (1977). Immunity to sporozoite-induced Manipulation of the immune response 673 malaria infection in mice. I. The effect of immunization of T and B cell-deficient mice. Journal of Immunology 118, 1322–7.CrossRefGoogle Scholar
Cioli, D. & Dennert, G. (1976). The course of Schistosoma mansoni infection in thymectomized rats. Journal of Immunology 117, 59–65.CrossRefGoogle ScholarPubMed
Cioli, D., Malorni, W., De Martino, C. & Dennert, G. (1980). A study of Schistosoma mansoni reinfection in thymectomized rats. Cellular Immunology 53, 246–56.CrossRefGoogle ScholarPubMed
Civil, R. H., Warren, K. S. & Mahmoud, A. A. F. (1978). Conditions for bacille Calmette-Guerin-induced resistance to infection with Schistosoma mansoni in mice. Journal of Infectious Diseases 137, 550–5.CrossRefGoogle ScholarPubMed
Clark, I. A. & Allison, A. C. (1974). Babesia microti and Plasmodium berghei yoelii infections in nude mice. Nature, London 252, 328–9.CrossRefGoogle ScholarPubMed
Clark, I. A., Allison, A. C. & Cox, F. E. (1976). Protection of mice against Babesia and Plasmodium with BCG. Nature, London 259, 309–11.CrossRefGoogle ScholarPubMed
Clark, I. A., Cox, F. E. G. & Allison, A. C. (1977). Protection of mice against Babesia spp. and Plasmodium spp. with killed Corynebacterium parvum. Parasitology 74, 9–18.CrossRefGoogle ScholarPubMed
Clark, I. A. & Hunt, N. H. (1983). Evidence for reactive oxygen intermediates causing hemolysis and parasite death in malaria. Infection and Immunity 39, 1–6.CrossRefGoogle ScholarPubMed
Domingo, E. O., Cowan, R. B. T. & Wakren, K. S. (1967). The inhibition of granuloma formation around Schistosoma mansoni eggs. I. Immunosuppressive drugs. American Journal of Tropical Medicine and Hygiene 16, 284–92.CrossRefGoogle ScholarPubMed
Domingo, E. O. & Warren, K. S. (1967). The inhibition of granuloma formation around Schistosoma mansoni eggs. II. Thymectomy. American Journal of Pathology 51, 757–67.Google ScholarPubMed
Freeman, R. R., Trejdosiewicz, A. J. & Cross, G. A. M. (1980). Protective monoclonal antibodies recognizing stage-specific merozoite antigens of a rodent malaria parasite. Nature, London 284, 366–8.CrossRefGoogle ScholarPubMed
Gravely, S. M. & Kreier, J. P. (1976). Adoptive transfer of immunity to Plasmodium berghei with immune T and B lymphocytes. Infection and Immunity 14, 184–90.CrossRefGoogle ScholarPubMed
Grun, J. L. & Weidanz, W. P. (1981). Immunity to Plasmodium chabaudi adami in the B-cell-deficient mouse. Nature, London 290, 143–5.CrossRefGoogle ScholarPubMed
Herman, R. & Farrell, J. P. (1977). Effects of cyclophosphamide on visceral leishmaniasis in the mouse. Protozoology 24, 429–36.CrossRefGoogle ScholarPubMed
Holder, A. A. & Freeman, R. R. (1981). Immunization against blood-stage rodent malaria using purified parasite antigens. Nature, London 294, 361–4.CrossRefGoogle ScholarPubMed
Hormaeche, C. E. (1979). The natural resistance of radiation chimeras to S. typhimurium C5. Immunology 37, 329–32.Google ScholarPubMed
Howard, J. G. (1983). Host immunity to leishmaniasis. In Leishmaniasis (ed. Chang, K.-P. and Bray, R. S.). Amsterdam: Elsevier/North-Holland Biomedical Press (in the Press).Google Scholar
Howard, J. G., Hale, C. & Liew, F. Y. (1980a). Immunological regulation of experimental cutaneous leishmaniasis. III. Nature and significance of specific suppression of cell-mediated immunity in mice highly susceptible to Leishmania tropica. Journal of Experimental Medicine 152, 594–607.CrossRefGoogle ScholarPubMed
Howard, J. G., Hale, C. & Liew, F. Y. (1980b). Genetically-determined susceptibility to Leishmania tropica infection is expressed by haematopoietic donor cells in mouse radiation chimaeras. Nature, London 288, 161–2.CrossRefGoogle ScholarPubMed
Howard, J. G., Hale, C. & Liew, F. Y. (1981). Immunological regulation of experimental cutaneous leishmaniasis. IV. Prophylactic effect of irradiation as a result of abrogation of suppressor T cell generation in mice genetically susceptible to Leishmania tropica. Journal of Experimental Medicine 153, 557–68.CrossRefGoogle ScholarPubMed
Howard, J. G., Liew, F. Y., Hale, C. & Nicklin, S. (1984). Prophylactic immunization against experimental leishmaniasis. II. Further characterization of the protective immunity against fatal Leishmania tropica infection induced by irradiated promastigotes. Journal of Immunology 132, 450–5.CrossRefGoogle ScholarPubMed
Howard, J. G., Nicklin, S., Hale, C. & Liew, F. Y. (1982). Prophylactic immunization against experimental leishmaniasis. I. Protection induced in mice genetically vulnerable to fatal Leishmania tropica infection. Journal of Immunology 129, 2206–12.CrossRefGoogle ScholarPubMed
Inchley, C. J. & Howard, J. G. (1969). The immunogenicity of phagocytosed T4 bacteriophage: cell replacement studies with splenectomized and irradiated mice. Clinical and Experimental Immunology 5, 189–98.Google ScholarPubMed
Irvin, A. D., Young, E. R., Osborn, G. D. & Francis, L. M. A. (1981). A comparison of Babesia infections in intact, surgically splenectomised, and congenitally asplenic (Dh/+ ) mice. International Journal for Parasitology 11, 251–5.CrossRefGoogle ScholarPubMed
Jaroslow, B. N. (1955). The effect of X-irradiation on immunity of the mouse to Trypanosoma duttoni. Journal of Infectious Diseases 96, 242–9.CrossRefGoogle ScholarPubMed
Kongshavn, P. A. L., Sadarangani, C. & Skamene, E. (1980). Genetically-determined differences in anti-bacterial activity of macrophages are expressed in the environment in which the macrophage precursors mature. Cellular Immunology 53, 341–9.CrossRefGoogle Scholar
Liew, F. Y., Hale, C. & Howard, J. G. (1982). Immunologic regulation of experimental cutaneous leishmaniasis. V. Characterisation of effector and specific suppressor T cells. Journal of Immunology 128, 1917–22.CrossRefGoogle ScholarPubMed
Liew, F. Y., Howard, J. G. & Hale, C. (1984). Prophylactic immunization against experimental leishmaniasis. III. Protection against fatal Leishmania tropica infection induced by irradiated promastigotes involves Lyt-l+2− T cells which do not mediate cutaneous DTH. Journal of Immunology 132, 456–61.CrossRefGoogle Scholar
Longenecker, B. M., Breitenbach, R. P., Congdon, L. L. & Farmer, J. N. (1969). Natural and acquired antibodies to Plasmodium lophurae in intact and bursaless chickens. I. Agglutination and passive immunity studies. Journal of Parasitology 55, 418–25.CrossRefGoogle ScholarPubMed
Mcdonald, V. & Phillips, R. S. (1978). Plasmodium chabaudi in mice. Adoptive transfer of immunity with enriched populations of spleen T and B lymphocytes. Immunology 34, 821–30.Google ScholarPubMed
Maddison, S. E., Chandler, F. W., Mcdougal, J. S., Slemenda, S. B. & Kagan, I. G. (1978). Schistosoma mansoni infection in intact and B cell deficient mice: the effect of pretreatment with BCG in these experimental models. American Journal of Tropical Medicine and Hygiene 27, 966–75.CrossRefGoogle Scholar
Mitchell, G. F. (1977). Studies on immune responses to parasite antigens in mice. V. Different susceptibilities of hypothymic and intact mice to Babesia rodhaini. International Archives of Allergy and Applied Immunology 53, 385–8.CrossRefGoogle ScholarPubMed
Mitchell, G. F., Curtis, J. M., Handman, E. & Mckenzie, I. F.C. (1980), Cutaneous leishmaniasis in mice: disease patterns in reconstituted nude mice of several genotypes infected with Leishmania tropica. Australian Journal of Experimental Biology and Medical Science 58, 521–32.CrossRefGoogle ScholarPubMed
Mitchell, G. F., Curtis, J. M., Scollay, R. G. & Handman, E. (1981). Resistance and abrogation of resistance to cutaneous leishmaniasis in reconstituted BALB/c nude mice. Australian Journal of Experimental Biology and Medical Science 59, 539–54.CrossRefGoogle ScholarPubMed
Nussenzweig, R. S. (1967). Increased nonspecific resistance to malaria produced by administration of killed Corynebacterium parvum. Experimental Parasitology 21, 224–31.CrossRefGoogle Scholar
Phillips, R. S. (1970). Plasmodium berghei: passive transfer of immunity by antisera and cells. Experimental Parasitology 27, 479–95.CrossRefGoogle ScholarPubMed
Phillips, S. M., Reid, W. A., Doughty, B. L. & Bentley, A. G. (1980). The immunologic modulation of morbidity in schistosomiasis. Studies in athymic mice and in vitro granuloma formation. American Journal of Tropical Medicine and Hygiene 29, 820–31.CrossRefGoogle ScholarPubMed
Potocnjak, P., Yoshida, N., Nussenzweig, R. S. & Nussenzweig, V. (1980). Monovalent fragments (Fab) of monoclonal antibodies to a sporozoite surface antigen (Pb44) protect mice against malarial infection. Journal of Experimental Medicine 151, 1504–13.CrossRefGoogle ScholarPubMed
Preston, P. M., Carter, R. L., Leuchars, E., Da Vies, A. J. S. & Dumonde, D. C. (1972). Experimental cutaneous leishmaniasis. III. Effects of thymectomy on the course of infection of CBA mice with Leishmania tropica. Clinical and Experimental Immunology 10, 337–57.Google Scholar
Rank, R. G. & Weidanz, W. P. (1976). Nonsterilizing immunity in avian malaria: an antibody independent phenomenon. Proceedings of the Society for Experimental Biology and Medicine 151, 257–9.CrossRefGoogle ScholarPubMed
Rosenberg, Y. J. & Evans, C. B. (1979). Resistance of mice suppressed for IgM production to Babesia microti infection. Nature, London 281, 302–4.CrossRefGoogle ScholarPubMed
Rosenstreich, D. L., Weinblatt, A. C. & O'Brien, A. D. (1982). Genetic control of resistance to infection in mice. CRC Critical Reviews in Immunology 3, 263–330.Google ScholarPubMed
Rowley, D. A. (1950). Effect of splenectomy on the formation of circulating antibody in the adult male albino rat. Journal of Immunology 64, 289–95.CrossRefGoogle ScholarPubMed
Sacks, D. L., Scott, P. A., Asofsky, R. & Sher, A. (1984). Cutaneous leishmaniasis in anti-IgM treated mice: enhanced resistance due to functional depletion of a B cell dependent T cell involved in the suppressor pathway. Journal of Immunology 132, 2072–7.CrossRefGoogle Scholar
Shaw, J. J. & Voller, A. (1968). Observations on the susceptibility of white mice to infection with Leishmania mexicana following whole-body X-irradiation. Annals of Tropical Medicine and Parasitology 62, 174–7.CrossRefGoogle ScholarPubMed
Singer, I. (1953). The effect of X-irradiation on infections with Plasmodium berghei in the white mouse. Journal of Infectious Diseases 92, 97–104.CrossRefGoogle ScholarPubMed
Skov, C. B. & Twohy, D. W. (1974). Cellular immunity to Leishmania donovani. I. The effect of T cell depletion on resistance to L. donovani in mice. Journal of Immunology 113, 2004–11.CrossRefGoogle Scholar
Smith, M. A., Clegg, J. A., Snary, D. & Trejdosiewicz, A. J. (1982). Passive immunization of mice against Schistosoma mansoni with an IgM monoclonal antibody. Parasitology 84, 83–91.CrossRefGoogle ScholarPubMed
Smrkovski, L. L. & Larson, C. I. (1977). Effect of treatment with BCG on the course of visceral leishmaniasis in BALB/c mice. Infection and Immunity 16, 249–57.CrossRefGoogle ScholarPubMed
Spitalny, G. L. & Nussenzweig, R. S. (1972). Effect of various routes of immunization and methods of parasite attenuation on the development of protection against sporozoite-induced rodent malaria. Proceedings of the Helminthological Society of Washington 39, 506–14.Google Scholar
Spitalny, G. L., Rivera-Ortiz, C.-I. & Nussenzweig, R. S. (1976). Plasmodium berghei: the spleen in sporozoite-induced immunity to mouse malaria. Experimental Parasitology 40, 179–88.CrossRefGoogle ScholarPubMed
Spitalny, G. L., Verhave, J. P., Meuwissen, J. H. E. Th. & Nussenzweig, R. S. (1977). Plasmodium berghei: T cell dependence of sporozoite-induced immunity in rodents. Experimental Parasitology 42, 73–81.CrossRefGoogle ScholarPubMed
Taverne, J., Dockrell, H. M. & Playfair, J. H. L. (1981). Endotoxin-induced serum factor kills malarial parasites in vitro. Infection and Immunity 33, 83–9.CrossRefGoogle ScholarPubMed
Verhave, J. P., Strickland, G. T., Jaffe, H. A. & Ahmed, A. (1978). Studies on the transfer of protective immunity with lymphoid cells from mice immune to malaria sporozoites. Journal of Immunology 121, 1031–3.CrossRefGoogle ScholarPubMed
Wakeljn, D. & Donachie, A. M. (1981). Genetic control of immunity to Trichinella spiralis. Donor bone marrow cells determine responses to infection in mouse radiation chimaeras. Immunology 43, 787–92.Google Scholar
Weinbaum, F. I., Evans, C. B. & Tioelaar, R. E. (1976). Immunity to Plasmodium berghei yoelii in mice. I. The course of infection in T cell and B cell deficient mice. Journal of Immunology 117, 1999–2005.CrossRefGoogle Scholar
Weintraub, J. & Weinbaum, F. I. (1977). The effect of BCG on experimental cutaneous leishmaniasis in mice. Journal of Immunology 118, 2288–90.CrossRefGoogle ScholarPubMed
Wells, R. A., Diggs, C. L. & Phillips, S. M. (1977). Cyclophosphamide-induced specific suppression of the protective immune response to rodent malaria. Journal of Immunology 118, 472–7.CrossRefGoogle ScholarPubMed
Wolf, R. E. (1974). Effects of antilymphocyte serum and splenectomy on resistance to Babesia microti infection in hamsters. Clinical Immunology and Immunopathology 2, 381–94.CrossRefGoogle ScholarPubMed
Young, A. S. & Cox, F. E. G. (1971). The effect of betamethasone on Babesia microti and B. rodhaini infections in rodents. Parasitology 63, 447–53.CrossRefGoogle Scholar