Skip to main content
NCBI home page
Infection and Immunity logoLink to Infection and Immunity
. 1983 Feb;39(2):726–735. doi: 10.1128/iai.39.2.726-735.1983

Enhancement of Natural Resistance to Influenza Virus in Lipopolysaccharide-Responsive and -Nonresponsive Mice by Propionibacterium acnes

J David Gangemi 1, James A Hightower 2, Ronnie A Jackson 1, Michael H Maher 1, Marcia G Welsh 2, M Michael Sigel 1
PMCID: PMC348010  PMID: 6832817

Abstract

Lipopolysaccharide-responsive C3H/HeN mice were rendered resistant to a mouse-adapted strain of influenza (Aichi, H3N2) virus when Propionibacterium acnes was given either intranasally or intraperitoneally several days before virus infection. The time of P. acnes treatment was important since no protection was demonstrated when this agent was given either on the same day as or several days after virus challenge. In contrast, lipopolysaccharide-nonresponsive C3H/HeJ mice were not protected when P. acnes was administered intranasally at any time before infection; however, protection was demonstrated when P. acnes was given by the intraperitoneal route. Depending on the route of inoculation, P. acnes induced several distinctive immunological responses in the lungs of both C3H/HeN and C3H/HeJ mice. Intranasal inoculation was more effective in activating pulmonary macrophages in C3H/HeN than in C3H/HeJ mice. In contrast, intraperitoneal inoculation activated pulmonary natural killer cells in both mouse lines but did not activate pulmonary macrophages.

Full text

PDF
726

Selected References

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

  1. Adlam C., Broughton E. S., Scott M. T. Enhanced resistance of mice to infection with bacteria following pre-treatment with Corynebacterium parvum. Nat New Biol. 1972 Feb 16;235(59):219–220. doi: 10.1038/newbio235219a0. [DOI] [PubMed] [Google Scholar]
  2. Adlam C., Scott M. T. Lympho-reticular stimulatory properties of Corynebacterium parvum and related bacteria. J Med Microbiol. 1973 Aug;6(3):261–274. doi: 10.1099/00222615-6-3-261. [DOI] [PubMed] [Google Scholar]
  3. Allison A. C. On the role of mononuclear phagocytes in immunity against viruses. Prog Med Virol. 1974;18(0):15–31. [PubMed] [Google Scholar]
  4. Armerding D., Rossiter H. Induction of natural killer cells by herpes-simplex virus type 2 in resistant and sensitive inbred mouse strains. Immunobiology. 1981;158(4):369–379. doi: 10.1016/S0171-2985(81)80007-1. [DOI] [PubMed] [Google Scholar]
  5. Bancroft G. J., Shellam G. R., Chalmer J. E. Genetic influences on the augmentation of natural killer (NK) cells during murine cytomegalovirus infection: correlation with patterns of resistance. J Immunol. 1981 Mar;126(3):988–994. [PubMed] [Google Scholar]
  6. Boraschi D., Meltzer M. S. Defective tumoricidal capacity of macrophages from A/J mice. II. Comparison of the macrophage cytotoxic defect of A/J mice with that of lipid A-unresponsive C3H/HeJ mice. J Immunol. 1979 Apr;122(4):1592–1597. [PubMed] [Google Scholar]
  7. Bradley D. J. Regulation of Leishmania populations within the host. II. genetic control of acute susceptibility of mice to Leishmania donovani infection. Clin Exp Immunol. 1977 Oct;30(1):130–140. [PMC free article] [PubMed] [Google Scholar]
  8. Brener Z., Cardoso J. E. Nonspecific resistance against Trypanosoma cruzi enhanced by Corynebacterium parvum. J Parasitol. 1976 Aug;62(4):645–646. [PubMed] [Google Scholar]
  9. Budzko D. B., Casals J., Waksman B. H. Enhanced resistance against Junin virus infection induced by Corynebacterium parvum. Infect Immun. 1978 Mar;19(3):893–897. doi: 10.1128/iai.19.3.893-897.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Castro J. E. The effect of Corynebacterium parvum on the structure and function of the lymphoid system in mice. Eur J Cancer. 1974 Feb;10(2):115–120. doi: 10.1016/0014-2964(74)90062-0. [DOI] [PubMed] [Google Scholar]
  11. Chedid L., Parant M., Damais C., Parant F., Juy D., Galelli A. Failure of endotoxin to increase nonspecific resistance to infection of lipopolysaccharide low-responder mice. Infect Immun. 1976 Mar;13(3):722–727. doi: 10.1128/iai.13.3.722-727.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Ching C., Lopez C. Natural killing of herpes simplex virus type 1-infected target cells: normal human responses and influence of antiviral antibody. Infect Immun. 1979 Oct;26(1):49–56. doi: 10.1128/iai.26.1.49-56.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Clark I. A., Cox F. E., Allison A. C. Protection of mice against Babesia spp. and Plasmodium spp. with killed Corynebacterium parvum. Parasitology. 1977 Feb;74(1):9–18. doi: 10.1017/s003118200004748x. [DOI] [PubMed] [Google Scholar]
  14. Collins F. M., Scott M. T. Effect of Corynebacterium parvum treatment on the growth of Salmonella enteritidis in mice. Infect Immun. 1974 May;9(5):863–869. doi: 10.1128/iai.9.5.863-869.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. DOUGHERTY R. M., GROUPE V. Studies on nonspecific acquired resistance to viral toxicity in mice. Proc Soc Exp Biol Med. 1957 Jul;95(3):593–596. doi: 10.3181/00379727-95-23303. [DOI] [PubMed] [Google Scholar]
  16. Gangemi J. D., Ghaffar A., Trauger R. L., Sigel M. M. Natural killer cell activation in lipopolysaccharide-responsive and -non responsive mice by viral and bacterial agents. J Reticuloendothel Soc. 1980 May;27(5):525–533. [PubMed] [Google Scholar]
  17. Gidlund M., Orn A., Wigzell H., Senik A., Gresser I. Enhanced NK cell activity in mice injected with interferon and interferon inducers. Nature. 1978 Jun 29;273(5665):759–761. doi: 10.1038/273759a0. [DOI] [PubMed] [Google Scholar]
  18. Glode L. M., Jacques A., Mergenhagen S. E., Rosenstreich D. L. Resistance of macrophages from C3H/HeJ mice to the in vitro cytotoxic effects of endotoxin. J Immunol. 1977 Jul;119(1):162–166. [PubMed] [Google Scholar]
  19. HALPERN B. N., PREVOT A. R., BIOZZI G., STIFFEL C., MOUTON D., MORARD J. C., BOUTHILLIER Y., DECREUSEFOND C. STIMULATION DE L'ACTIVIT'E PHAGOCYTAIRE DU SYST'EME R'ETICULOENDOTH'ELIAL PROVOQU'EE PAR CORYNEBACTERIUM PARVUM. J Reticuloendothel Soc. 1964 Jan;1:77–96. [PubMed] [Google Scholar]
  20. Haller O., Arnheiter H., Gresser I., Lindenmann J. Genetically determined, interferon-dependent resistance to influenza virus in mice. J Exp Med. 1979 Mar 1;149(3):601–612. doi: 10.1084/jem.149.3.601. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Haller O., Arnheiter H., Lindenmann J., Gresser I. Host gene influences sensitivity to interferon action selectively for influenza virus. Nature. 1980 Feb 14;283(5748):660–662. doi: 10.1038/283660a0. [DOI] [PubMed] [Google Scholar]
  22. Herberman R. B., Nunn M. E., Holden H. T., Staal S., Djeu J. Y. Augmentation of natural cytotoxic reactivity of mouse lymphoid cells against syngeneic and allogeneic target cells. Int J Cancer. 1977 Apr 15;19(4):555–564. doi: 10.1002/ijc.2910190417. [DOI] [PubMed] [Google Scholar]
  23. Ivins B. E., Wyrick P. B. Response of C3H/HeJ and C3H/HeN mice and their peritoneal macrophages to the toxicity of Chlamydia psittaci elementary bodies. Infect Immun. 1978 Nov;22(2):620–622. doi: 10.1128/iai.22.2.620-622.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Kirchner H., Hirt H. M., Munk K. Protection against herpes simplex virus infection in mice by Corynebacterium parvum. Infect Immun. 1977 Apr;16(1):9–11. doi: 10.1128/iai.16.1.9-11.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Kirchner H., Hirt H. M., Rosenstreich D. L., Mergenhagen S. E. Resistance of C3H/HeJ mice to lethal challenge with herpes simplex virus. Proc Soc Exp Biol Med. 1978 Jan;157(1):29–32. doi: 10.3181/00379727-157-39983. [DOI] [PubMed] [Google Scholar]
  26. Kirchner H., Scott M. T., Hirt H. M., Munk K. Protection of mice against viral infection by Corynebacterium parvum and Bordetella pertussis. J Gen Virol. 1978 Oct;41(1):97–104. doi: 10.1099/0022-1317-41-1-97. [DOI] [PubMed] [Google Scholar]
  27. Kobayashi F., Nagoya T., Koshi T., Saino Y. Biphasic protection against bacterial infection in mice induced by vaccination of Propionibacterium acnes. Infect Immun. 1980 Feb;27(2):391–396. doi: 10.1128/iai.27.2.391-396.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. LINDENMANN J., LANE C. A., HOBSON D. THE RESISTANCE OF A2G MICE TO MYXOVIRUSES. J Immunol. 1963 Jun;90:942–951. [PubMed] [Google Scholar]
  29. Lindenmann J., Deuel E., Fanconi S., Haller O. Inborn resistance of mice to myxoviruses: macrophages express phenotype in vitro. J Exp Med. 1978 Feb 1;147(2):531–540. doi: 10.1084/jem.147.2.531. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. MIMS C. A. ASPECTS OF THE PATHOGENESIS OF VIRUS DISEASES. Bacteriol Rev. 1964 Mar;28:30–71. doi: 10.1128/br.28.1.30-71.1964. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Morahan P. S., Kern E. R., Glasgow L. A. Immunomodulator-induced resistance against herpes simplex virus. Proc Soc Exp Biol Med. 1977 Apr;154(4):615–620. doi: 10.3181/00379727-154-39730. [DOI] [PubMed] [Google Scholar]
  32. Morahan P. S., Morse S. S., McGeorge M. G. Macrophage extrinsic antiviral activity during herpes simplex virus infection. J Gen Virol. 1980 Feb;46(2):291–300. doi: 10.1099/0022-1317-46-2-291. [DOI] [PubMed] [Google Scholar]
  33. O'Neill G. J., Henderson D. C., White R. G. The role of anaerobic coryneforms on specific and non-specific immunological reactions. I. Effect on particle clearance and humoral and cell-mediated immunological responses. Immunology. 1973 Jun;24(6):977–995. [PMC free article] [PubMed] [Google Scholar]
  34. Puccetti P., Santoni A., Riccardi C., Herberman R. B. Cytotoxic effector cells with the characteristics of natural killer cells in the lungs of mice. Int J Cancer. 1980 Jan 15;25(1):153–158. doi: 10.1002/ijc.2910250121. [DOI] [PubMed] [Google Scholar]
  35. Ruco L. P., Meltzer M. S. Defective tumoricidal capacity of macrophages from C3H/HeJ mice. J Immunol. 1978 Jan;120(1):329–334. [PubMed] [Google Scholar]
  36. Shayegani M., Lief F. S., Mudd S. Specific and nonspecific cell-mediated resistance to influenza virus in mice. Infect Immun. 1974 Jun;9(6):991–998. doi: 10.1128/iai.9.6.991-998.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Spencer J. C., Ganguly R., Waldman R. H. Nonspecific protection of mice against influenza virus infection by local or systemic immunization with Bacille Calmette-Guérin. J Infect Dis. 1977 Aug;136(2):171–175. doi: 10.1093/infdis/136.2.171. [DOI] [PubMed] [Google Scholar]
  38. Starr S. E., Visintine A. M., Tomeh M. O., Nahmias A. J. Effects of immunostimulants on resistance of newborn mice to herpes simplex type 2 infection. Proc Soc Exp Biol Med. 1976 May;152(1):57–60. doi: 10.3181/00379727-152-39327. [DOI] [PubMed] [Google Scholar]
  39. Stinnett J. D., Morris M. J., Alexander J. W. Macrophage activation and increased resistance to infection in immunosuppressed mice treated with Corynebacterium parvum vaccine or pyran copolymer. J Reticuloendothel Soc. 1979 May;25(5):525–531. [PubMed] [Google Scholar]
  40. Welsh R. M., Jr Mouse natural killer cells: induction specificity, and function. J Immunol. 1978 Nov;121(5):1631–1635. [PubMed] [Google Scholar]
  41. Wood P. R., Clark I. A. Genetic control of Propionibacterium acnes-induced protection of mice against Babesia microti. Infect Immun. 1982 Jan;35(1):52–57. doi: 10.1128/iai.35.1.52-57.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Woodruff M. F., Ghaffar A., Whitehead V. L. Modification of the effect of C. parvum on macrophage activity and tumour growth by X-irradiation. Int J Cancer. 1976 May 15;17(5):652–658. doi: 10.1002/ijc.2910170515. [DOI] [PubMed] [Google Scholar]
  43. Wyde P. R., Peavy D. L., Cate T. R. Morphological and cytochemical characterization of cells infiltrating mouse lungs after influenza infection. Infect Immun. 1978 Jul;21(1):140–146. doi: 10.1128/iai.21.1.140-146.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]

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

RESOURCES