Early Events in the Pathogenesis of Enteric Fever in Mice

  • David E. Briles
  • Nancy E. Dunlap
  • Edward Swords
  • William H. BenjaminJr.
Part of the NATO ASI Series book series (NSSA, volume 245)


Salmonella typhimurium is the best studied of the salmonella which cause mouse typhoid (enteric fever). The portal of entry of salmonella that cause enteric fevers in the mouse and in other species is normally oral. However, the organisms quickly enter the lymph and blood, and most of the organisms that survive blood clearance become lodged in the spleen and liver where they grow and cause disease (Carter and Collins, 1974; Carter and Collins, 1974). Although salmonella which cause enteric fevers have been described as facultative intracellular parasites that resides within macrophages, there is controversy over the major location of S. typhimurium multiplication in vivo (Benjamin, et al, 1990; Carroll et al, 1979; Dunlap et al, 1991; Guo et al, 1986; Schurr et al, 1989).


Visceral Leishmaniasis Post Infection Enteric Fever Blood Clearance Natural Resistance 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Benjamin, W. H., Jr., Hall, P. and Briles, D. E., Salmonella typhimurium locus mviA regulates virulence in Ity s but not Ity r mice: functional mviA results in avirulence; mutant (nonfunctional) mviA results in virulence., J. Exp. Med. 174:1073 (1991).PubMedCrossRefGoogle Scholar
  2. Benjamin, W. H., Jr., Hall, P., Roberts, S. J. and Briles, D. E., The primary effect of the Ity locus is on the growth rate of Salmonella typhimurium that are relatively protected from killing, J. Immunol. 144:3143 (1990).PubMedGoogle Scholar
  3. Benjamin, W. H., Jr., Turnbough, C. L., Jr., Goguen, J. D., Posey, B. S. and Briles, D. E., Genetic mapping of novel virulence determents of Salmonella typhimurium to the region between trpD and supD., Microbial Pathogenesis. 1:115 (1986).PubMedCrossRefGoogle Scholar
  4. Benjamin, W. H., Jr., Turnbough, C. L., Jr., Posey, B. S. and Briles., D. E., The ability of Salmonella typhimurium to produce the siderophore enterobactin is not a virulence factor in mouse typhoid., Infect. Immun. 50:392 (1985).PubMedGoogle Scholar
  5. Bradley, D. J., Taylor, B. A., Blackwell, J., Evans, E. P. and Freeman, J., Regulation of Leishmania populations within the host III Mapping of the locus controlling susceptibility to visceral leishmaniasis in the mouse., Clin. Exp. Immunol. 37:7 (1979).PubMedGoogle Scholar
  6. Briles, D. E., Benjamin, W. H., Jr., Williams, C. A. and Davie, J. M., A genetic locus responsible for salmonella susceptibility in BSVS mice is not responsible for the limited T-dependent immune responsiveness of BSVS mice., J. Immunol. 127:906 (1981).PubMedGoogle Scholar
  7. Briles, D. E., Lehmeyer, J. and Forman, C., Phagocytosis and killing of Salmonella typhimurium by peritoneal exudate cells., Infect. Immun. 33:380 (1981).PubMedGoogle Scholar
  8. Carrol, M. E. W., Jackett, P. S., Aber, V. R. and Lowrie, D. B., Phagolysosome formation, cyclic adenosine 3’:5’-monophosphate and the fate of Salmonella typhimurium within mouse peritoneal macrophages., J. Gen. Micro. 110:421 (1979).CrossRefGoogle Scholar
  9. Carter, P. B. and Collins, F. M., The route of enteric infection in normal mice, J. Exp. Med. 139:1189 (1974).PubMedCrossRefGoogle Scholar
  10. Carter, P. B. and Collins, J. M., Growth of typhoid and paratyphoid bacilli in intravenously infected mice., Infect. Immun. 10:816 (1974).PubMedGoogle Scholar
  11. Collins, F. M. and Mackaness, G. B., Delayed hypersensitivity and arthus reactivity in relation to host resistance in salmonella-infected mice., J. Immunol. 101:830 (1968).PubMedGoogle Scholar
  12. Colwell, D. E., Michalek, S. M., Briles, D. E., Jirillo, E. and McGhee, J. R., Monoclonal antibodies to salmonella lipopolysaccharide: Anti-O-polysaccharide antibodies protect C3H mice against challenge with virulent Salmonella typhimurium., J. Immunol. 133:950 (1984).PubMedGoogle Scholar
  13. Dunlap, N. E., Benjamin, W. H., Jr., McCall, R. D., Tilden, A. B. and Briles, D. E., A “safe site” for Salmonella typhimurium is within splenic cells during the early phase of infection in mice., Microbial Pathogenesis. 10:297 (1991).PubMedCrossRefGoogle Scholar
  14. Eisenstein, T., Killar, L. and Sultzer, B., Immunity to Infection with Salmonella typhimurium: mouse-strain differences in vaccine-and serum-mediated protection, J. Infect. Dis. 150:425 (1984).PubMedCrossRefGoogle Scholar
  15. Fields, P. I., Groisman, E. A. and Heffron, F., A Salmonella locus that controls resistance to microbicidal proteins from phagocytic cells, Science. 243:1059 (1989).PubMedCrossRefGoogle Scholar
  16. Fields, P. I., Swanson, R. V., Haidaris, C. G. and Heffron, F., Mutants of Salmonella typhimurium that cannot survive within the macrophage are avirulent, Proc. Natl. Acad. Sci. (USA) 83:5189 (1986).CrossRefGoogle Scholar
  17. Fridovich, I., The biology of oxygen radicals., Science. 201:875 (1975).CrossRefGoogle Scholar
  18. Guo, Y.-N., Hsu, H. S., Mumaw, V. R. and Nakoneczna, I., Electronmicroscopy studies on the bacterial action of inflammatory leukocytes in murine salmonellosis, J. Med. Microbiol. 21:151 (1986).PubMedCrossRefGoogle Scholar
  19. Hart, P. D., Armstrong, J. A., Brown, C. A. and Draper, P., Ultrastructural study of the behavior of macrophages toward parasitic mycobacteria, Infect. Immun. 5:803 (1972).PubMedGoogle Scholar
  20. Hormaeche, C. E., The natural resistance of radiation chimeras to S. typhimurium C5., Immunology. 37:329 (1979).PubMedGoogle Scholar
  21. Hormaeche, C. E., Natural resistance to Salmonella typhimurium in different inbred mouse strains., Immunology 37:311 (1979).PubMedGoogle Scholar
  22. Hormaeche, C. E., The in vivo division and death rates of S. typhimurium in the spleens of naturally resistant and susceptible mice measured by the superinfecting phage technique of Meynell., Immunology 41:973 (1980).PubMedGoogle Scholar
  23. Hormaeche, C. E., Brock, J. and Pettifor, R. A. 1980. Natural resistance to mouse typhoid: Possible role of the macrophage, in Genetic control of natural resistance to infection and malignancy, edited by Skamene et al. New York: Academic Press, 121.CrossRefGoogle Scholar
  24. Kim, K., Kim, I. H., Rhee, S. G. and Stadtman, E. R., The isolation and purification of a specific “protector” protein which inhibits enzyme activation by a thiol/Fe(III)/O2 mixed-function oxydation system., J. Biol. Chem. 263:4704 (1988).PubMedGoogle Scholar
  25. Krishnapillia, V., Uridinediphosphogalactose-4-epimerase deficiency in Salmonella typhimurium and its correction by plasmid-borne galactose genes of Escherichia coli K-12: Effects on mouse virulence, phagocytosis, and serum sensitivity., Infect. Immun. 4:177 (1971).Google Scholar
  26. Lane, F. C. and Unanue, E. R., Requirment of thymus (T) lymphocytes for resistance to listeriosis., J. Exp. Med. 135:1104(1972).PubMedCrossRefGoogle Scholar
  27. Lin, F. R., Hsu, H. S., Mumaw, V. R. and Moncure, C. W., Confirmation of destruction of salmonellae within murine peritoneal exudate cells by immunocytochemical technique., Immunology 67:394 (1989).PubMedGoogle Scholar
  28. Lin, F. R., X. M. Wang, H. S. Hsu, V. R. Mumaw and Nakoneczna, I., Electron microscopic studies on the location of bacterial proliferation in the liver in murine salmonelosis, Br. J. Exp. Pathol. 68:539 (1987).PubMedGoogle Scholar
  29. Lissner, C. R., Swanson, R. N. and O’Brien, A. D., Genetic control of the innate resistance of mice to Salmonella typhimurium: expression of the Ity gene in peritoneal and splenic macrophages isolated in vitro., J. Immunol. 131:3006 (1983).PubMedGoogle Scholar
  30. Lowrie, D. B., Abner, V. R. and Carrol, M. E. W., Division and death rates of Salmonella typhimurium inside macrophages: Use of penicillin as a probe, J. Gen. Microbiol. 110:409 (1979).PubMedCrossRefGoogle Scholar
  31. Miller, S. I., Rulkkinen, W. S., Selsted, M. E. and Mekalanos, J. J., A characterization of defensin resistance phenotypes associated with mutations in the phoP virulence regulon of Salmonella typhimurium., Infect. Immun. 58:3706 (1990).PubMedGoogle Scholar
  32. Muotiala, A., Hovi, M. and Mäkelä, P. H., Protective immunity in mouse salmonellosis: comparison of smooth and rough live and killed vaccines., Microbial Pathogenesis 6:51 (1989).PubMedCrossRefGoogle Scholar
  33. Nakoneczna, I. and Hsu, H. S., The comparative histopathology of primary and secondary lesions in murine salmonellosis., Br. J. Exp. Pathol. 61:76 (1980).PubMedGoogle Scholar
  34. O’Brien, A. D. and Metcalf, E. S., Control of early Salmonella typhimurium growth in innately salmonella-resistant mice does not require functional T-lymphocytes., J. Immunol. 129:1349 (1982).PubMedGoogle Scholar
  35. O’Brien, A. D. and Rosenstreich., D. L., Genetic control of the susceptibility of C3HeB/FeJ mice to Salmonella typhimurium is regulated by a locus distinct from known Salmonella response genes., J. Immunol. 131:2613(1983).PubMedGoogle Scholar
  36. O’Brien, A. D., Scher, I. and Formal., S. B., Effects of silica on the innate resistance of inbred mice to Salmonella typhimurium infection., Infect. Immun. 25:513 (1979).PubMedGoogle Scholar
  37. O’Brien, A. D., Taylor, B. A. and Rosenstreich, D. L., Genetic control of natural resistance to Salmonella typhimurium in mice during the late phase of infection, J. Immunol. 133:3313 (1984).PubMedGoogle Scholar
  38. Orm, I. M. and Collins, F. M., Protection against M. tuberculosis infection by adoptive immunotherapy, J. Exp. Med. 158:74 (1983).CrossRefGoogle Scholar
  39. Plant, J. and Glynn, A. A., Natural resistance to salmonella infection, delayed hypersensitivity and Ir genes in different strains of mice., Nature 248:345 (1974).PubMedCrossRefGoogle Scholar
  40. Plant, J. and Glynn, A. A., Genetics of resistance to infection with Salmonella typhimurium., J. Infect. Dis. 133:72 (1976).PubMedCrossRefGoogle Scholar
  41. Plant, J. and Glynn, A. A., Locating salmonella resistance gene on mouse chromosome 1., Clin. Exp. Immunol. 37:1 (1979).PubMedGoogle Scholar
  42. Plant, J. E., Blackwell, J. M., O’Brien, A. D., Bradley, D. J. and Glynn, A. A., Are the Lsh and Ity disease resistance genes at one locus on mouse chromosome 1?, Nature 297:510 (1982).PubMedCrossRefGoogle Scholar
  43. Robson, H. G. and Vas, S. I., Resistance of inbred mice to Salmonella typhimurium., J. Infect. Dis. 126:378 (1972).PubMedCrossRefGoogle Scholar
  44. Rowley, D. and Turner, J. K., Number of molecules of antibody required to promote phagocytosis of one bacterium., Nature. 1:496(1966).CrossRefGoogle Scholar
  45. Saxen, H., Mechanism of the protective action of anti-Salmonella IgM in experimental mouse salmonellosis., J. Gen. Microbiol. 130:2277 (1984).PubMedGoogle Scholar
  46. Schurr, E., Skamene, E., Forget, A. and Gros, P., Linkage analysis of the Bcg gene on mouse chromosome 1: Identification of a tightly linked marker, J. Immunol. 142:4507 (1989).PubMedGoogle Scholar
  47. Skamene, E., Genetic regulation of host resistance to bacterial infection., Rev. Infect. Dis. 5:S823 (1983).PubMedCrossRefGoogle Scholar
  48. Skamene, E., Gros, P., Forget, A., Kongshavn, P. A. L., Charles, C. S. and Taylor, B. A., Genetic regulation of resistance to intracellular pathogens., Nature 297:506 (1982).PubMedCrossRefGoogle Scholar
  49. Stinavage, P. S., Martin, L. E. and Spitznagel, J. K., A 59 kilodalton outer membrane protein of Salmonella typhimurium protects against oxidative intraleukocytic killing due to human neutrophils., Mole. Microbiol. 4:283 (1990).CrossRefGoogle Scholar
  50. Stocker, B. A. D. and Mäkelä, P. H., Genetic determination of bacterial virulence, with a special reference to Salmonella., Curr. Topic Microbiol. Immunol. 124:149 (1986).CrossRefGoogle Scholar
  51. Swanson, R. N. and O’Brien, A. D., Genetic control of the innate resistance of mice to Salmonella typhimurium: Ity gene is expressed in vivo by 24 hours after infection., J. Immunol. 131:3014 (1983).PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 1993

Authors and Affiliations

  • David E. Briles
    • 1
    • 2
    • 3
  • Nancy E. Dunlap
    • 1
    • 4
  • Edward Swords
    • 1
  • William H. BenjaminJr.
    • 1
    • 5
  1. 1.Department of MicrobiologyThe University of Alabama at BirminghamBirmingham, AlabamaUK
  2. 2.Department of PediatricsThe University of Alabama at BirminghamBirmingham, AlabamaUK
  3. 3.Department of Comparative MedicineThe University of Alabama at BirminghamBirmingham, AlabamaUK
  4. 4.Department of MedicineThe University of Alabama at BirminghamBirmingham, AlabamaUK
  5. 5.Department of PathologyThe University of Alabama at BirminghamBirmingham, AlabamaUK

Personalised recommendations