Skip to main content
Infection and Immunity logoLink to Infection and Immunity
. 1997 Jul;65(7):2725–2731. doi: 10.1128/iai.65.7.2725-2731.1997

Effects of neutrophil, natural killer cell, and macrophage depletion on murine Clostridium piliforme infection.

R A Van Andel 1, R R Hook Jr 1, C L Franklin 1, C L Besch-Williford 1, N van Rooijen 1, L K Riley 1
PMCID: PMC175384  PMID: 9199442

Abstract

Clostridium piliforme infection (Tyzzer's disease) induces enterohepatic disease in many domestic and laboratory animals. Murine susceptibility to Tyzzer's disease varies with host strain, age, and immune status However, little is known about the role of the immune system in control of this disease. To investigate the role of host immunity in Tyzzer's disease, mice were depleted of either neutrophils, natural killer cells, or macrophages by antibody administration or chemotherapy. After depletion, DBA/2 mice, which are naturally susceptible to C. piliforme, or naturally resistant C57BL/6 mice were inoculated intravenously with C. piliforme. Animals were euthanized 3 days postinoculation and evaluated for gross and histologic lesions and hepatic bacterial load. In juvenile DBA/2 or C57BL/6 mice, depletion of either neutrophils or natural killer cells increased severity of disease. In adult mice, depletion of natural killer cells significantly increased severity of Tyzzer's disease in the resistant (C57BL/6) but not in the susceptible (DBA/2) strain. Macrophage depletion did not alter the course of infection in either mouse strain. These studies indicate an important role for neutrophils and natural killer cells in the pathogenesis of murine Tyzzer's disease. The role of macrophages in murine C. piliforme infection will require further evaluation.

Full Text

The Full Text of this article is available as a PDF (664.8 KB).

Selected References

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

  1. Belluardo N., Mudó G., Campisi A., Vanella A., Russo J., Bindoni M. Crossfostering and early development of natural killer cytotoxic activity in various inbred mouse strains. Physiol Behav. 1993 May;53(5):951–957. doi: 10.1016/0031-9384(93)90274-j. [DOI] [PubMed] [Google Scholar]
  2. Berra A., Rodriguez A., Heiligenhaus A., Pazos B., Van Rooijen N., Foster C. S. The role of macrophages in the pathogenesis of HSV-1 induced chorioretinitis in BALB/c mice. Invest Ophthalmol Vis Sci. 1994 Jun;35(7):2990–2998. [PubMed] [Google Scholar]
  3. Burch R. M., Noronha-Blob L., Bator J. M., Lowe V. C., Sullivan J. P. Mice treated with a leumedin or antibody to Mac-1 to inhibit leukocyte sequestration survive endotoxin challenge. J Immunol. 1993 Apr 15;150(8 Pt 1):3397–3403. [PubMed] [Google Scholar]
  4. Conlan J. W., Dunn P. L., North R. J. Leukocyte-mediated lysis of infected hepatocytes during listeriosis occurs in mice depleted of NK cells or CD4+ CD8+ Thy1.2+ T cells. Infect Immun. 1993 Jun;61(6):2703–2707. doi: 10.1128/iai.61.6.2703-2707.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Conlan J. W., North R. J. Neutrophils are essential for early anti-Listeria defense in the liver, but not in the spleen or peritoneal cavity, as revealed by a granulocyte-depleting monoclonal antibody. J Exp Med. 1994 Jan 1;179(1):259–268. doi: 10.1084/jem.179.1.259. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Czuprynski C. J., Brown J. F., Maroushek N., Wagner R. D., Steinberg H. Administration of anti-granulocyte mAb RB6-8C5 impairs the resistance of mice to Listeria monocytogenes infection. J Immunol. 1994 Feb 15;152(4):1836–1846. [PubMed] [Google Scholar]
  7. Dussault I., Miller S. C. Stimulation of natural killer cell numbers but not function in leukemic infant mice: a system primed in infancy allows survival in adulthood. Nat Immun. 1993 Mar-Apr;12(2):66–78. [PubMed] [Google Scholar]
  8. Franklin C. L., Kinden D. A., Stogsdill P. L., Riley L. K. In vitro model of adhesion and invasion by Bacillus piliformis. Infect Immun. 1993 Mar;61(3):876–883. doi: 10.1128/iai.61.3.876-883.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Fries A. S. Studies on Tyzzer's disease: acquired immunity against infection and activation of infection by immunosuppressive treatment. Lab Anim. 1979 Apr;13(2):143–147. doi: 10.1258/002367779780943486. [DOI] [PubMed] [Google Scholar]
  10. Han Y., van Rooijen N., Cutler J. E. Binding of Candida albicans yeast cells to mouse popliteal lymph node tissue is mediated by macrophages. Infect Immun. 1993 Aug;61(8):3244–3249. doi: 10.1128/iai.61.8.3244-3249.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Harshan K. V., Gangadharam P. R. In vivo depletion of natural killer cell activity leads to enhanced multiplication of Mycobacterium avium complex in mice. Infect Immun. 1991 Aug;59(8):2818–2821. doi: 10.1128/iai.59.8.2818-2821.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Heremans H., Dillen C., van Damme J., Billiau A. Essential role for natural killer cells in the lethal lipopolysaccharide-induced Shwartzman-like reaction in mice. Eur J Immunol. 1994 May;24(5):1155–1160. doi: 10.1002/eji.1830240522. [DOI] [PubMed] [Google Scholar]
  13. Kawamura S., Taguchi F., Fujiwara K. Plaque formation by Tyzzer's organism in primary monolayer culture of mouse hepatocytes. Microbiol Immunol. 1983;27(5):415–424. doi: 10.1111/j.1348-0421.1983.tb00600.x. [DOI] [PubMed] [Google Scholar]
  14. Laskay T., Röllinghoff M., Solbach W. Natural killer cells participate in the early defense against Leishmania major infection in mice. Eur J Immunol. 1993 Sep;23(9):2237–2241. doi: 10.1002/eji.1830230928. [DOI] [PubMed] [Google Scholar]
  15. Livingston R. S., Franklin C. L., Besch-Williford C. L., Hook R. R., Jr, Riley L. K. A novel presentation of Clostridium piliforme infection (Tyzzer's disease) in nude mice. Lab Anim Sci. 1996 Feb;46(1):21–25. [PubMed] [Google Scholar]
  16. Motzel S. L., Riley L. K. Bacillus piliformis flagellar antigens for serodiagnosis of Tyzzer's disease. J Clin Microbiol. 1991 Nov;29(11):2566–2570. doi: 10.1128/jcm.29.11.2566-2570.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Pope B. L., Chourmouzis E., Sigindere J., MacIntyre J. P., Capetola R. J., Lau C. Y. In vivo activation of natural killer cells and priming of IL-2 responsive cytolytic cells by loxoribine (7-allyl-8-oxoguanosine). Cell Immunol. 1993 Apr 1;147(2):302–312. doi: 10.1006/cimm.1993.1071. [DOI] [PubMed] [Google Scholar]
  18. Qian Q., Jutila M. A., Van Rooijen N., Cutler J. E. Elimination of mouse splenic macrophages correlates with increased susceptibility to experimental disseminated candidiasis. J Immunol. 1994 May 15;152(10):5000–5008. [PubMed] [Google Scholar]
  19. Riley L. K., Besch-Williford C., Waggie K. S. Protein and antigenic heterogeneity among isolates of Bacillus piliformis. Infect Immun. 1990 Apr;58(4):1010–1016. doi: 10.1128/iai.58.4.1010-1016.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Rogers H. W., Unanue E. R. Neutrophils are involved in acute, nonspecific resistance to Listeria monocytogenes in mice. Infect Immun. 1993 Dec;61(12):5090–5096. doi: 10.1128/iai.61.12.5090-5096.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Shpitz B., Chambers C. A., Singhal A. B., Hozumi N., Fernandes B. J., Roifman C. M., Weiner L. M., Roder J. C., Gallinger S. High level functional engraftment of severe combined immunodeficient mice with human peripheral blood lymphocytes following pretreatment with radiation and anti-asialo GM1. J Immunol Methods. 1994 Feb 28;169(1):1–15. doi: 10.1016/0022-1759(94)90119-8. [DOI] [PubMed] [Google Scholar]
  22. Sjöstedt A., Conlan J. W., North R. J. Neutrophils are critical for host defense against primary infection with the facultative intracellular bacterium Francisella tularensis in mice and participate in defense against reinfection. Infect Immun. 1994 Jul;62(7):2779–2783. doi: 10.1128/iai.62.7.2779-2783.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Smith A. L., Rose M. E., Wakelin D. The role of natural killer cells in resistance to coccidiosis: investigations in a murine model. Clin Exp Immunol. 1994 Aug;97(2):273–279. doi: 10.1111/j.1365-2249.1994.tb06080.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Smith K. J., Skelton H. G., Hilyard E. J., Hadfield T., Moeller R. S., Tuur S., Decker C., Wagner K. F., Angritt P. Bacillus piliformis infection (Tyzzer's disease) in a patient infected with HIV-1: confirmation with 16S ribosomal RNA sequence analysis. J Am Acad Dermatol. 1996 Feb;34(2 Pt 2):343–348. doi: 10.1016/s0190-9622(07)80005-3. [DOI] [PubMed] [Google Scholar]
  25. Takagaki Y., Fujiwara K. Bacteremia in experimental Tyzzer's disease of mice. Jpn J Microbiol. 1968 Jun;12(2):129–143. doi: 10.1111/j.1348-0421.1968.tb00377.x. [DOI] [PubMed] [Google Scholar]
  26. Tepper R. I., Coffman R. L., Leder P. An eosinophil-dependent mechanism for the antitumor effect of interleukin-4. Science. 1992 Jul 24;257(5069):548–551. doi: 10.1126/science.1636093. [DOI] [PubMed] [Google Scholar]
  27. Van Rooijen N. The liposome-mediated macrophage 'suicide' technique. J Immunol Methods. 1989 Nov 13;124(1):1–6. doi: 10.1016/0022-1759(89)90178-6. [DOI] [PubMed] [Google Scholar]
  28. Veazey R. S., 2nd, Paulsen D. B., Schaeffer D. O. Encephalitis in gerbils due to naturally occurring infection with Bacillus piliformis (Tyzzer's disease). Lab Anim Sci. 1992 Oct;42(5):516–518. [PubMed] [Google Scholar]
  29. Vreden S. G., Sauerwein R. W., Verhave J. P., Van Rooijen N., Meuwissen J. H., Van Den Broek M. F. Kupffer cell elimination enhances development of liver schizonts of Plasmodium berghei in rats. Infect Immun. 1993 May;61(5):1936–1939. doi: 10.1128/iai.61.5.1936-1939.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Waggie K. S., Ganaway J. R., Wagner J. E., Spencer T. H. Experimentally induced Tyzzer's disease in Mongolian gerbils (Meriones unguiculatus). Lab Anim Sci. 1984 Feb;34(1):53–57. [PubMed] [Google Scholar]
  31. Waggie K. S., Hansen C. T., Ganaway J. R., Spencer T. S. A study of mouse strains susceptibility to Bacillus piliformis (Tyzzer's disease): the association of B-cell function and resistance. Lab Anim Sci. 1981 Apr;31(2):139–142. [PubMed] [Google Scholar]
  32. Waggie K. S., Thornburg L. P., Grove K. J., Wagner J. E. Lesions of experimentally induced Tyzzer's disease in Syrian hamsters, guineapigs, mice and rats. Lab Anim. 1987 Apr;21(2):155–160. doi: 10.1177/002367728702100213. [DOI] [PubMed] [Google Scholar]
  33. Wike D. A., Tallent G., Peacock M. G., Ormsbee R. A. Studies of the rickettsial plaque assay technique. Infect Immun. 1972 May;5(5):715–722. doi: 10.1128/iai.5.5.715-722.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Young J. K., Baker D. C., Burney D. P. Naturally occurring Tyzzer's disease in a puppy. Vet Pathol. 1995 Jan;32(1):63–65. doi: 10.1177/030098589503200110. [DOI] [PubMed] [Google Scholar]
  35. van Rooijen N., Poppema A. Efficacy of various water-soluble chelator molecules in the liposome-mediated macrophage "suicide" technique. J Pharmacol Toxicol Methods. 1992 Dec;28(4):217–221. doi: 10.1016/1056-8719(92)90007-n. [DOI] [PubMed] [Google Scholar]

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

RESOURCES