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. 2004 Apr 15;6(2):81–91. doi: 10.1016/0882-4010(89)90011-9

Modulation of resistance to Salmonella typhimurium infection in mice by mouse hepatitis virus (MHV)

Michael T Fallon 1,, Trenton R Schoeb 1, William H Benjamin Jr 2, JRussell Lindsey 1, David E Briles 2
PMCID: PMC7127339  PMID: 2541308

Abstract

Prior infection of mice with a field strain of mouse hepatitis virus (MHV) increased the early resistance of euthymic mice to virulent Salmonella typhimurium strain SR-11 infections (as defined by significantly fewer salmonella colony-forming units (cfu) present in spleens and livers 4 days after salmonella infection). This increase in salmonella resistance was observed when the interval between MHV and salmonella infections was 6 days, but not at 3, 10, or 14 day intervals. The mouse lty locus, which controls the number of intracellular salmonella, had a significant effect on the ability of MHV to induce resistance to salmonella. MHV caused an increase in resistance to salmonella in ltys (salmonella susceptible) mice at all doses of salmonella tested (100 to 10000 cfu). In the ltyr (salmonella resistant) mice tested the beneficial effect of MHV on salmonella resistance was small and when observed, was only present at salmonella doses of 10000 cfu or greater. Neither the Lpsd nor Xid mutations affected the ability of MHV to increase resistance to salmonella infection. In contrast to euthymic mice, MHV infection greatly decreased the resistance of athymic (nude) mice to salmonella infection. Since the Nu locus does not affect the resistance of mice to salmonella (at 4 days post salmonella infection), these results indicate that MHV infection and the nude phenotype interact to increase susceptibility to salmonella.

These findings re-emphasize the importance of keeping laboratory mice used in research free of MHV and other immunomodulatory pathogens.

Keywords: mouse hepatitis virus (MHV), Salmonella typhimurium, host resistance, Ity, athymic (nude) mice

Footnotes

This work was supported in part by grants RR00463 and RR07003 from the Animal Resources Branch, Division of Research Resources, National Institutes of Health (NIH), and grant AI 15986 from the National Institute for Allergy and Infectious Disease, NIH.

References

  • 1.Mills EL. Viral infections predisposing to bacterial infections. Annu Rev Med. 1984;35:469–479. doi: 10.1146/annurev.me.35.020184.002345. [DOI] [PubMed] [Google Scholar]
  • 2.Jakab GJ. Interactions between Sendai virus and bacterial pathogens in the lung: A review. Lab Anim Sci. 1981;31:170–177. [PubMed] [Google Scholar]
  • 3.Loosli CG. Influenza and the interaction of viruses and bacteria in respiratory infections. Medicine (Baltimore) 1973;52:369–384. doi: 10.1097/00005792-197309000-00001. [DOI] [PubMed] [Google Scholar]
  • 4.Young LS, LaForce M, Head JJ, Fealy BS, Bennet JV. A simultaneous outbreak of meningococcal and influenza infections. N Engl J Med. 1972;287:5–9. doi: 10.1056/NEJM197207062870102. [DOI] [PubMed] [Google Scholar]
  • 5.Gardner ID. Effect of influenza virus infection on susceptibility to bacteria in mice. J Infect Dis. 1980;142:704–707. doi: 10.1093/infdis/142.5.704. [DOI] [PubMed] [Google Scholar]
  • 6.Hormaeche CE. The in vivo division and death rate of Salmonella typhimurium in the spleens of naturally resistant and susceptible mice measured by the superinfecting phage technique of Meynell. Immunology. 1980;41:973–979. [PMC free article] [PubMed] [Google Scholar]
  • 7.Briles DE, Benjamin W, Jr, Posey B, Michalek SM, McGhee JR. Independence of macrophage activation and expression of the alleles of the lty (immunity to typhimurium) locus. Microbial Pathogenesis. 1986;1:33–41. doi: 10.1016/0882-4010(86)90029-x. [DOI] [PubMed] [Google Scholar]
  • 8.Lissner CR, Swanson RN, O'Brien AD. Genetic control of the innate resistance of mice to Salmonella typhimurium: expression of the lty gene in peritoneal and splenic macrophages in vitro. J Immunol. 1983;131:3006–3013. [PubMed] [Google Scholar]
  • 9.Potter M, O'Brien AD, Skamene E, Gross P, Forget A, Kongshavn PAL, Wax JS. A BALB/c congenic strain of mice that carries a genetic locus (ltyr) controlling resistance to intracellular parasites. Infect Immun. 1983;40:1234–1235. doi: 10.1128/iai.40.3.1234-1235.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 10.O'Brien AD. Influence of host genes on resistance of inbred mice to lethal infection with Salmonella typhimurium. In: Briles DE, editor. Curr Top Microbiol, Vol. 124: Genetic Control of the Susceptibility to Bacterial Infection. 1986. pp. 37–48. [PubMed] [Google Scholar]
  • 11.Boorman GA, Luster MI, Dean JH. Peritoneal macrophage alterations caused by naturally occurring mouse hepatitis virus. Am J Pathol. 1982;106:110–117. [PMC free article] [PubMed] [Google Scholar]
  • 12.Taguchi F, Yamada A, Fujiwara K. Resistance to highly virulent mouse hepatitis virus acquired by mice after low-virulence infection: Enhanced antiviral activity of macrophages. Infect Immun. 1980;29:42–49. doi: 10.1128/iai.29.1.42-49.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 13.Sheets P, Shah KV, Bang FB. 3rd edn. Vol. 159. 1978. Mouse hepatitis virus (MHV) infection in thymectomized C3H mice; pp. 34–38. (Proc Soc Exp Biol Med). [DOI] [PubMed] [Google Scholar]
  • 14.Cheers CM, Waller R. Activated macrophages in congenitally athymic ‘nude’ mice. J Immunol. 1975;115:844–847. [PubMed] [Google Scholar]
  • 15.Shultz LD, Sidman CL. Genetically determined murine models of immunodeficiency. Annu Rev Immunol. 1987;5:367–403. doi: 10.1146/annurev.iy.05.040187.002055. [DOI] [PubMed] [Google Scholar]
  • 16.Hochnadel JF, Keller KF. Protective effects of passively transferred immune T- and B-lymphocytes in mice injected with Salmonella typhimurium. J Infect Dis. 1977;135:813–827. doi: 10.1093/infdis/135.5.813. [DOI] [PubMed] [Google Scholar]
  • 17.Chander R, Sainis KB, Lewis NF. Role of thymus-derived lymphocytes in acquired immunity to salmonellosis in mice. Microbiol Immunol. 1986;30:1299–1306. doi: 10.1111/j.1348-0421.1986.tb03062.x. [DOI] [PubMed] [Google Scholar]
  • 18.Bang FB, Warwick A. 3rd edn. Vol. 46. 1960. Mouse macrophages as host cells for the mouse hepatitis virus and the genetic basis of their susceptibility; pp. 1065–1075. (Proc Natl Acad Sci USA). [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 19.Taguchi F, Hirano N, Kiuchi Y, Fujiwara K. Difference in response to mouse hepatitis virus among susceptible mouse strains. Jpn J Microbiol. 1976;20:293–302. doi: 10.1111/j.1348-0421.1976.tb00991.x. [DOI] [PubMed] [Google Scholar]
  • 20.Knobler RL, Linthicum DS, Cohn M. Host genetic regulation of acute MHV-4 viral encephalomyelitis and acute autoimmune encephalomyelitis in (BALBcKe × SJLJ) recombinant-inbred mice. J Neuroimmunol. 1985;8:15–28. doi: 10.1016/S0165-5728(85)80044-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 21.Lindsey JR. 3rd edn. Institute for Laboratory Animal Resources, National Research Council, National Academy of Sciences; Washington, DC: 1988. (Guide to Infectious Diseases of Mice and Rats). (in press) [Google Scholar]
  • 22.Dempsey WL, Smith AL, Morahan PS. Effect of inapparent murine hepatitis virus infections on macrophages and host resistance. J Leukocyte Biol. 1986;39:559–565. doi: 10.1002/jlb.39.5.559. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 23.Carrano VA, Barthold SW, Beck DS, Smith AL. Alteration of viral respiratory infections by prior infection with mouse hepatitis virus. Lab Anim Sci. 1984;34:573–576. [PubMed] [Google Scholar]
  • 24.Plant J, Glynn AA. Locating salmonella resistance gene on mouse chromosome 1. Clin Exp Immunol. 1979;37:1–6. [PMC free article] [PubMed] [Google Scholar]
  • 25.Casebolt DB, Spalding DM, Schoeb TR, Lindsey JR. Suppression of immune response induction in Peyer's patch lymphoid cells from mice infected with mouse hepatitis virus. Cell Immunol. 1987;109:97–103. doi: 10.1016/0008-8749(87)90295-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 26.Bruning JL, Kintz BL. 3rd edn. Scott, Foresman and Company; Glenview: 1987. pp. 127–129. (Computational Handbook of Statistics). [Google Scholar]

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