Skip to main content
NCBI home page
Infection and Immunity logoLink to Infection and Immunity
. 1989 Jun;57(6):1647–1655. doi: 10.1128/iai.57.6.1647-1655.1989

Immunological and nonimmunological control of severity of Trypanosoma musculi infections in C3H and C57BL/6 inbred mice.

J W Albright 1, J F Albright 1
PMCID: PMC313334  PMID: 2785960

Abstract

Studies concerned with the mechanisms responsible for relative resistance or susceptibility of strains of inbred mice to Trypanosoma musculi infections are presented. Treatment with 400 rads of ionizing radiation, silica dust, or trypan blue (reticuloendothelial blocking agents) rendered C3H mice unable to control the initial maximum level of parasite growth, and the mice died of overwhelming infections. In contrast, similarly treated C57BL/6 (relatively resistant) mice controlled initial trypanosome growth as well as controls; however, the duration of infection, preceding eventual cure, was approximately doubled. Combined treatment with trypan blue and 400 rads of radiation resulted in much higher initial levels of infection in C57BL/6 mice, and about half of the mice died; the remaining mice eventually recovered after a prolonged course of infection. These results indicate that a nonimmunological mechanism, which controls initial infection, and an immunological mechanism cooperate to limit T. musculi infections in normal mice. We present results that suggest that both mechanisms are less effective in C3H than in C57BL/6 mice. The initial control of infection presumably reflects the activity of some type(s) of phagocytic effector cell; we show, however, that the initial control of infection is not an attribute of the liver Kupffer cells. Identification and characterization of the cells capable of controlling initial infection could lead to procedures for enhancing their function and, thus, to enhanced resistance to, and elimination of, trypanosome infections.

Full text

PDF
1647

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Albright J. F., Albright J. W. Natural resistance to animal parasites. Contemp Top Immunobiol. 1984;12:1–52. doi: 10.1007/978-1-4684-4571-8_1. [DOI] [PubMed] [Google Scholar]
  2. Albright J. W., Albright J. F. Differences in resistance to Trypanosoma musculi infection among strains of inbred mice. Infect Immun. 1981 Aug;33(2):364–371. doi: 10.1128/iai.33.2.364-371.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Albright J. W., Albright J. F., Dusanic D. G. Mechanisms of trypanosome-mediated suppression of humoral immunity in mice. Proc Natl Acad Sci U S A. 1978 Aug;75(8):3923–3927. doi: 10.1073/pnas.75.8.3923. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Albright J. W., Albright J. F. The availability of purines influences both the number of parasites and the splenocyte levels of purine-metabolizing enzymes in trypanosome-infected mice. Infect Immun. 1988 Apr;56(4):831–835. doi: 10.1128/iai.56.4.831-835.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Albright J. W., Albright J. F. The decline of immunological resistance of aging mice to Trypanosoma musculi. Mech Ageing Dev. 1982 Dec;20(4):315–330. doi: 10.1016/0047-6374(82)90099-9. [DOI] [PubMed] [Google Scholar]
  6. Albright J. W., Matusewicz N. M., Albright J. F. Aging of the murine immune system is reflected by declining ability to generate antibodies that promote elimination of Trypanosoma musculi. J Immunol. 1988 Aug 15;141(4):1318–1325. [PubMed] [Google Scholar]
  7. Anderson L. W., Banks K. L. Early course of infection in susceptible and resistant strains of mice, using [3H]uridine-labeled Trypanosoma brucei subsp. brucei. Infect Immun. 1982 May;36(2):525–530. doi: 10.1128/iai.36.2.525-530.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Brooks B. O., Wassom D. L., Cypess R. H. Kinetics of immunoglobulin M and G responses of nude and normal mice to Trypanosoma musculi. Infect Immun. 1982 May;36(2):667–671. doi: 10.1128/iai.36.2.667-671.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Cornford E. M., Freeman B. J., MacInnis A. J. Physiological relationships and circadian periodicities in rodent trypanosomes. Trans R Soc Trop Med Hyg. 1976;70(3):238–243. doi: 10.1016/0035-9203(76)90047-x. [DOI] [PubMed] [Google Scholar]
  10. DESOWITZ R. S., WATSON H. J. C. Studies on Trypanosoma vivax. III. Observations on the maintenance of a strain in white rats. Ann Trop Med Parasitol. 1952 May;46(1):92–100. [PubMed] [Google Scholar]
  11. De Gee A. L., Levine R. F., Mansfield J. M. Genetics of resistance to the African trypanosomes. VI. Heredity of resistance and variable surface glycoprotein-specific immune responses. J Immunol. 1988 Jan 1;140(1):283–288. [PubMed] [Google Scholar]
  12. Dempsey W. L., Mansfield J. M. Lymphocyte function in experimental African trypanosomiasis. V. Role of antibody and the mononuclear phagocyte system in variant-specific immunity. J Immunol. 1983 Jan;130(1):405–411. [PubMed] [Google Scholar]
  13. Desai B. B., Albright J. W., Albright J. F. Cooperative action of complement component C3 and phagocytic effector cells in innate murine resistance to Trypanosoma lewisi. Infect Immun. 1987 Feb;55(2):358–363. doi: 10.1128/iai.55.2.358-363.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Ferrante A. The role of the macrophage in immunity to Trypanosoma musculi. Parasite Immunol. 1986 Mar;8(2):117–127. doi: 10.1111/j.1365-3024.1986.tb00838.x. [DOI] [PubMed] [Google Scholar]
  15. Gillis S., Ferm M. M., Ou W., Smith K. A. T cell growth factor: parameters of production and a quantitative microassay for activity. J Immunol. 1978 Jun;120(6):2027–2032. [PubMed] [Google Scholar]
  16. Greenblatt H. C., Potter T. A., Rosenstreich D. L. Genetic control of natural resistance to Trypanosoma rhodesiense: transfer of resistance with bone marrow or spleen cells. J Infect Dis. 1985 May;151(5):911–916. doi: 10.1093/infdis/151.5.911. [DOI] [PubMed] [Google Scholar]
  17. Harel-Bellan A., Joskowicz M., Fradelizi D., Eisen H. Modification of T-cell proliferation and interleukin 2 production in mice infected with Trypanosoma cruzi. Proc Natl Acad Sci U S A. 1983 Jun;80(11):3466–3469. doi: 10.1073/pnas.80.11.3466. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Inverso J. A., De Gee A. L., Mansfield J. M. Genetics of resistance to the African trypanosomes. VII. Trypanosome virulence is not linked to variable surface glycoprotein expression. J Immunol. 1988 Jan 1;140(1):289–293. [PubMed] [Google Scholar]
  19. Kraal G., Janse M., Claassen E. Marginal metallophilic macrophages in the mouse spleen: effects of neonatal injections of MOMA-1 antibody on the humoral immune response. Immunol Lett. 1988 Feb;17(2):139–144. doi: 10.1016/0165-2478(88)90082-x. [DOI] [PubMed] [Google Scholar]
  20. LINCICOME D. R. Growth of Trypanosoma lewisi in the heterologous mouse host. Exp Parasitol. 1958 Jan;7(1):1–13. doi: 10.1016/0014-4894(58)90002-x. [DOI] [PubMed] [Google Scholar]
  21. Levine R. F., Mansfield J. M. Genetics of resistance to the African trypanosomes. III. Variant-specific antibody responses of H-2-compatible resistant and susceptible mice. J Immunol. 1984 Sep;133(3):1564–1569. [PubMed] [Google Scholar]
  22. MAKINODAN T., KASTENBAUM M. A., PETERSON W. J. Radiosensitivity of spleen cells from normal and preimmunized mice and its significance to intact animals. J Immunol. 1962 Jan;88:31–37. [PubMed] [Google Scholar]
  23. Macaskill J. A., Holmes P. H., Jennings F. W., Urquhart G. M. Immunological clearance of 75Se-labelled Trypanosoma brucei in mice. III. Studies in animals with acute infections. Immunology. 1981 Aug;43(4):691–698. [PMC free article] [PubMed] [Google Scholar]
  24. Macaskill J. A., Holmes P. H., Whitelaw D. D., McConnell I., Jennings F. W., Urquhart G. M. Immunological clearance of 75Se-labelled Trypanosoma brucei in mice. II. Mechanisms in immune animals. Immunology. 1980 Aug;40(4):629–635. [PMC free article] [PubMed] [Google Scholar]
  25. Mitchell L. A., Pearson T. W. Antibody responses in resistant and susceptible inbred mice infected with Trypanosoma congolense. Immunology. 1986 Feb;57(2):297–303. [PMC free article] [PubMed] [Google Scholar]
  26. Morrison W. I., Murray M. The role of humoral immune responses in determining susceptibility of A/J and C57BL/6 mice to infection with Trypanosoma congolense. Parasite Immunol. 1985 Jan;7(1):63–79. doi: 10.1111/j.1365-3024.1985.tb00479.x. [DOI] [PubMed] [Google Scholar]
  27. Murray M., Morrison W. I., Whitelaw D. D. Host susceptibility to African trypanosomiasis: trypanotolerance. Adv Parasitol. 1982;21:1–68. doi: 10.1016/s0065-308x(08)60274-2. [DOI] [PubMed] [Google Scholar]
  28. Nusrat A. R., Wright S. D., Aderem A. A., Steinman R. M., Cohn Z. A. Properties of isolated red pulp macrophages from mouse spleen. J Exp Med. 1988 Oct 1;168(4):1505–1510. doi: 10.1084/jem.168.4.1505. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Pinder M., Chassin P., Fumoux F. Mechanisms of self-cure from Trypanosoma congolense infection in mice. J Immunol. 1986 Feb 15;136(4):1427–1434. [PubMed] [Google Scholar]
  30. Pinder M. Trypanosoma congolense: genetic control of resistance to infection in mice. Exp Parasitol. 1984 Apr;57(2):185–194. doi: 10.1016/0014-4894(84)90079-1. [DOI] [PubMed] [Google Scholar]
  31. Reinitz D. M., Mansfield J. M. Independent regulation of B cell responses to surface and subsurface epitopes of African trypanosome variable surface glycoproteins. J Immunol. 1988 Jul 15;141(2):620–626. [PubMed] [Google Scholar]
  32. Roelants G. E. Natural resistance to African trypanosomiasis. Parasite Immunol. 1986 Jan;8(1):1–10. doi: 10.1111/j.1365-3024.1986.tb00828.x. [DOI] [PubMed] [Google Scholar]
  33. Samarawickrema N. A., Howell M. J. Interactions between peritoneal cells and Trypanosoma musculi in mice. Int J Parasitol. 1988 Feb;18(1):69–73. doi: 10.1016/0020-7519(88)90038-0. [DOI] [PubMed] [Google Scholar]
  34. Tanaka S., Suzuki T., Nishioka K. Assay of classical and alternative pathway activities of murine complement using antibody-sensitized rabbit erythrocytes. J Immunol Methods. 1986 Feb 12;86(2):161–170. doi: 10.1016/0022-1759(86)90448-5. [DOI] [PubMed] [Google Scholar]
  35. Tarleton R. L., Kuhn R. E. Restoration of in vitro immune responses of spleen cells from mice infected with Trypanosoma cruzi by supernatants containing interleukin 2. J Immunol. 1984 Sep;133(3):1570–1575. [PubMed] [Google Scholar]
  36. Vincendeau P., Daëron M., Daulouede S. Identification of antibody classes and Fc receptors responsible for phagocytosis of Trypanosoma musculi by mouse macrophages. Infect Immun. 1986 Sep;53(3):600–605. doi: 10.1128/iai.53.3.600-605.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Wakelin D. Genetic control of susceptibility and resistance to parasitic infection. Adv Parasitol. 1978;16:219–308. doi: 10.1016/s0065-308x(08)60575-8. [DOI] [PubMed] [Google Scholar]
  38. Wechsler D. S., Kongshavn P. A. Further characterization of the curative antibodies in Trypanosoma musculi infection. Infect Immun. 1988 Sep;56(9):2379–2384. doi: 10.1128/iai.56.9.2379-2384.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Wechsler D. S., Kongshavn P. A. Heat-labile IgG2a antibodies affect cure of Trypanosoma musculi infection in C57BL/6 mice. J Immunol. 1986 Nov 1;137(9):2968–2972. [PubMed] [Google Scholar]
  40. Whitelaw D. D., Macaskill J. A., Holmes P. H., Jennings F. W., Urquhart G. M. Genetic resistance to Trypanosoma congolense infections in mice. Infect Immun. 1980 Mar;27(3):707–713. doi: 10.1128/iai.27.3.707-713.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Infection and Immunity are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES