Co-ordinate regulation of Salmonella typhimurium invasion genes by environmental and regulatory factors is mediated by control of hilA expression

Molecular Microbiology

Volumn 22, Issue 4, 1996, Pages 703-714

  Bajaj, Vivek ^a   Lucas, Robin L ^a   Hwang, Clara ^a   Lee, Catherine A ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BACTERIAL GENE; BACTERIAL VIRULENCE; GENE CONTROL; GENE EXPRESSION; GENE MUTATION; NONHUMAN; OSMOLARITY; PH; PRIORITY JOURNAL; SALMONELLA TYPHIMURIUM;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; SALMONELLA TYPHIMURIUM; TYPHIMURIUM;

EID: 0029828325     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2958.1996.d01-1718.x     Document Type: Article

References (62)

1. Alpuche-Aranda, C.M., Swanson, J.A., Loomis, W.P., and Miller, S.I. (1992) Salmonella typhimurium activates virulence gene transcription within acidified macrophage phagosomes. Proc Natl Acad Sci USA 89: 10079-10083.
2. Ausubel, F.M., Brent, R., Kingston, R.E., Moore, D.D., Seidman, J.G., Smith, J.A., and Struhl, K. (1995) Current Protocols In Molecular Biology. New York: John Wiley and Sons, Inc.
3. Bajaj, V., Hwang, C., and Lee, C.A. (1995) hilA is a novel ompR/toxR family member that activates the expression of Salmonella typhimurium invasion genes. Mol Microbiol 18: 715-727.
4. deBeer, E.J., Johnston, C.G., and Wilson, D.W. (1935) The composition of intestinal secretions. J Biol Chem 198: 113-120.
5. Behlau, I., and Miller, S.I. (1993) A PhoP repressed gene promotes Salmonella typhimurium invasion of epithelial cells. J Bacteriol 175: 4475-4484.
6. Bhriain, N.N., Dorman, C.J., and Higgins, C.F. (1989) An overlap between osmotic and anaerobic stress responses: a potential role for DNA supercoiling in the co-ordinate regulation of gene expression. Mol Microbiol 3: 933-942.
7. Carter, P.B., and Collins, F.M. (1974) The route of enteric infection in normal mice. J Exp Med 139: 1189-1203.
8. Chen, J.C., Bavoil, P., and Clark, V.L. (1991) Enhancement of the invasive ability of Neisseria gonorrhoeae by contact with HeclB, an adenocarcinoma endometrial cell line. Mol Microbiol 5: 1531-1538.
9. Collazo, C.M., Zierler, M.K., and Galán, J.E. (1995) Functional analysis of the Salmonella typhimurium invasion genes invI and invJ and identification of a target of the protein secretion apparatus encoded in the inv locus. Mol Microbiol 15: 25-38.
10. Cornelis, G.R., Iriarte, M., and Sory, M.-P. (1995) Environmental control of virulence functions and signal transduction in Yersinia enterocolitica. In Signal Transduction And Bacterial Virulence. Rappuoli, R., Scarlato, V., and Aricö, B. (eds). Austin, Texas: R.G. Landes Company, pp. 95-110.
11. Cotter, P.A., Akerley, B.J., and Miller, J.E. (1995) BvgAS dependent phenotypic modulation of Bordetella species. In Signal Transduction And Bacterial Virulence. Rappuoli, R., Scarlato, V., and Aricö, B. (eds). Austin, Texas: R.G. Landes Company, pp. 21-42.
12. Davis, R.W., Botstein, D., and Roth, J.R. (1980) Advanced Bacterial Genetics. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press.
13. Dell, C.L., Neely, M.N., and Olson, E.R. (1994) Altered pH and lysine signalling mutants of cadC, a gene encoding a membrane-bound transcriptional activator of the Escherichia coli cadBA operon. Mol Microbiol 14: 7-16.
14. Donaldson, Jr, R.M. (1978) The relation of enteric bacterial populations to gastrointestinal function and disease. In Gastrointestinal Disease: Pathophysiology, Diagnosis, and Management. Sleisenger, M.H., and Fordtran, J.S. (eds). Philadelphia: W.B. Saunders Company, pp. 79-92.
15. Dorman, C.J., Bhriain, N.N., and Higgins, C.F. (1990) DNA supercoiling and environmental regulation of virulence gene expression in Shigella flexneri. Nature 344: 789-792.
16. Dziejman, M., and Mekalanos, J.J. (1995) Two-component signal transduction and its role in the expression of bacterial virulence factors. In Two-component Signal Transduction. Hoch, J.A., and Silhavy, T.J. (eds). Washington DC: American Society for Microbiology, pp. 305-317.
17. Eichelberg, K., Kaniga, K., and Galán, J.E. (1996) Transcriptional regulation of Salmonella secreted virulence determinants. In The 96th General Meeting of the American Society for Microbiology. New Orleans, Los Angeles: American Society for Microbiology, p. 161.
18. Ernst, R.K., Dombroski, D.M., and Merrick, J.M. (1990) Anaerobiosis, type 1 fimbriae, and growth phase are factors that affect invasion of HEp-2 cells by Salmonella typhimurium. Infect Immun 58: 2014-2016.
19. Francis, C.L., Ryan, T.A., Jones, B.J., Smith, S.J., and Falkow, S. (1993) Ruffles induced by Salmonella and other stimuli direct macropinocytosis of bacteria. Nature 364: 639-642.
20. Galán, J.E. (1996) Molecular genetic bases of Salmonella entry into host cells. Mol Microbiol 20: 263-271.
21. Galán, J.E., and Curtiss, III, R. (1989) Cloning and molecular characterization of genes whose products allow Salmonella typhimurium to penetrate tissue culture cells. Proc Natl Acad Sci USA 86: 6383-6387.
22. Galán, J.E., and Curtiss, III, R. (1990) Expression of Salmonella typhimurium genes required for invasion is regulated by changes in DNA supercoiling. Infect Immun 58: 1879-1885.
23. 2+ as an extracellular signal: environmental regulation of Salmonella virulence. Cell 84: 165-174.
24. Ginocchio, C.C., Olmsted, S.B., Wells, C.L, and Galán, J.E. (1994) Contact with epithelial cells induces the formation of surface appendages on Salmonella typhimurium. Cell 76: 717-724.
25. Higgins, C.F., Dorman, C.J., Stirling, D.A., Waddell, L., Booth, I.R., May, G., and Bremer, E. (1988) A physiological role for DNA supercoiling in the osmotic regulation of gene expression in S. typhimurium and E. coli. Cell 52: 569-584.
26. Hueck, C.J., Hantman, M.J., Bajaj, V., Johnston, C., Lee, C.A., and Miller, S.I. (1995) Salmonella typhimurium secreted invasion determinants are homologous to Shigella lpa proteins. Mol Microbiol 18: 479-490.
27. Igo, M.M., Ninfa, A.J., and Silhavy, T.J. (1989a) A bacterial environmental sensor that functions as a protein kinase and stimulates transcriptional activation. Genes Dev 3: 598-605.
28. Igo, M.M., Ninfa, A.J., Stock, J.B., and Silhavy, T.J. (1989b) Phosphorylation and dephosphorylation of a bacterial transcriptional activator by a transmembrane receptor. Genes Dev 3: 1725-1734.
29. Jones, B.D., and Falkow, S. (1994) Identification and characterization of a Salmonella typhimurium oxygen-regulated gene required for bacterial internalization. Infect Immun 62: 3745-3752.
30. Jones, B.D., Ghori, N., and Falkow, S. (1994) Salmonella typhimurium initiates murine infection by penetrating and destroying the specialized epithelial M cells of the Peyer's patches. J Exp Med 180: 15-23.
31. Jones, B.D., Paterson, J.F., Hall, A., and Falkow, S. (1993) Salmonella typhimurium induces membrane ruffling by a growth factor-receptor-independent mechanism. Proc Natl Acad Sci USA 90: 10390-10394.
32. Kaniga, K., Bossio, J.C., and Galán, J.E. (1994) The Salmonella typhimurium invasion genes invF and invG encode homologues of the araC and pulD family of proteins. Mol Microbiol 13: 555-568.
33. Kaniga, K., Tucker, S.C., Trollinger, D., and Galán, J.E. (1995) Homologues of the Shigella invasins lpaB and lpaC are required for Salmonella typhimurium entry into cultured cells. J Bacteriol 177: 3965-3971.
34. Karem, K., and Foster, J.W. (1993) The influence of DNA topology on the environmental regulation of a pH-regulated locus in Salmonella typhimurium. Mol Microbiol 10: 75-86.
35. Lee, C.A., and Falkow, S. (1990) The ability of Salmonella to enter mammalian cells is affected by bacterial growth state. Proc Natl Acad Sci USA 87: 4304-4308.
36. Lee, C.A., Jones, B.D., and Falkow, S. (1992) Identification of a Salmonella typhimurium invasion locus by selection for hyperinvasive mutants. Proc Natl Acad Sci USA 89:1847-1851.
37. Li, J., Ochman, H., Groisman, E.A., Fidelma Boyd, E., Solomon, F., Nelson, K., and Selander, R.K. (1995) Relationship between evolutionary rate and cellular location among the Inv/Spa invasion proteins of Salmonella enterica. Proc Natl Acad Sci USA 92: 7252-7256.
38. Lin, F.-R., Wang, X.-M., Hsu, H.S., Mumaw, V.R., and Nakoneczna, I. (1987) Electron microscopic studies on the location of bacterial proliferation in the liver in murine salmonellosis. Br J Exp Path 68: 539-550.
39. Lodge, J., Fear, J., Busby, S., Gunasekaran, P., and Kamini, N.R. (1992) Broad host range plasmids carrying the Escherichia coli lactose and galactose operons. FEMS Microbiol Lett 95: 271-276.
40. MacBeth, K.J., and Lee, C.A. (1993) Prolonged inhibition of bacterial protein synthesis abolishes Salmonella invasion. Infect Immun 61: 1544-1546.
41. McCormick, B.A., Colgan S.P., Delp-Archer, C., Miller, S.I., and Madara, J.L. (1993) Salmonella typhimurium attachment to human intestinal epithelial monolayers: transcellular signalling to subepithelial neutrophils. J Cell Biol 123: 895-907.
42. McCormick, B.A., Hofman, P.M., Kim, J., Carnes, D.K., Miller, S.I., and Madara, J.L. (1995a) Surface attachment of Salmonella typhimurium to intestinal epithelia imprints the subepithelial matrix with gradients chemotactic for neutrophils. J Cell Biol 131: 1599-1608.
43. McCormick, B.A., Miller, S.I., Carnes, D., and Madara, J.L. (1995b) Transepithelial signaling to neutrophils by salmonellae: a novel virulence mechanism for gastroenteritis. Infect Immun 63: 2302-2309.
44. Mekalanos, J.J. (1992) Environmental signals controlling expression of virulence determinants in bacteria. J Bacteriol 174: 1-7.
45. Miller, J.H. (1972) Experiments In Molecular Genetics. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press.
46. Miller, S.I. (1991) PhoP/PhoQ: macrophage-specific modulators of Salmonella virulence? Mol Microbiol 5: 2073-2078.
47. Miller, S.I., and Mekalanos, J.J. (1990) Constitutive expression of the phoP regulon attenuates Salmonella virulence and survival within macrophages. J Bacteriol 172: 2485-2490.
48. Miller, S.I., Kukral, A.M., and Mekalanos, J.J. (1989) A two-component regulatory system (phoP phoQ) controls Salmonella typhimurium virulence. Proc Natl Acad Sci USA 86: 5054-5058.
49. Mills, D.M., Bajaj, V., and Lee, C.A. (1995) A 40kb chromosomal fragment encoding Salmonella typhimurium invasion genes is absent from the corresponding region of the Escherichia coli K-12 chromosome. Mol Microbiol 15: 749-759.
50. Nnalue, N.A., Shnyra, A., Hultenby, K., and Lindberg, A.A. (1992) Salmonella choleraesuis and Salmonella typhimurium associated with liver cells after intravenous inoculation of rats are localized mainly in Kupffer cells and multiply intracellularly. Infect Immun 60: 27758-27768.
51. Pace, J., Hayman, M.J., and Galán, J.E. (1993) Signal transduction and invasion of epithelial cells by S. typhimurium. Cell 72: 505-514.
52. Pegues, D.A., Hantman, M.J., Behlau, I., and Miller, S.I. (1995) PhoP/PhoQ transcriptional repression of Salmonella typhimurium invasion genes: evidence for a role in protein secretion. Mol Microbiol 17: 169-181.
53. Rosenshine, I., Ruschkowski, V., Foubister, V., and Finlay, B.B. (1994) Salmonella typhimurium invasion of epithelial cells: role of induced host cell tyrosine protein phosphorylation. Infect Immun 62: 4969-4974.
54. Russo, F.D., and Silhavy, T.J. (1991) EnvZ controls the concentration of phosphorylated OmpR to mediate osmoregulation of the porin genes. J Mol Biol 222: 567-580.
55. Sanderson, K.E., Hessel, A., and Rudd, K.E. (1995) Genetic map of Salmonella typhimurium, edn VIII. Microbiol Rev 59: 241-303.
56. Schiemann, D.A., and Shope, S.R. (1991) Anaerobic growth of Salmonella typhimurium results in increased uptake by Henle-407 epithelial and mouse peritoneal cells in vitro and repression of a major outer membrane protein. Infect Immun 59: 437-440.
57. Soncini, F.D., García-Véscovi, E., and Groisman, E.A. (1995) Transcriptional autoregulation of the Salmonella typhimurium phoPQ operon. J Bacteriol 177: 4364-4371.
58. Stibitz, S., Black, W., and Falkow, S. (1986) The construction of a cloning vector designed for gene replacement in Bordetella pertussis. Gene 50: 133-140.
59. Takeuchi, A. (1967) Electron microscope studies of experimental Salmonella infection. Penetration into the intestinal epithelium by Salmonella typhimurium. Am J Pathol 50: 109-136.
60. Tartera, C., and Metcalf, E.S. (1993) Osmolarity and growth phase overlap in regulation of Salmonella typhi adherence to and invasion of human intestinal cells. Infect Immun 61: 3084-3089.
61. Uhl, M.A., and Miller, J.F. (1996) Bordetella pertussis BvgAS virulence control system. In Two-component Signal Transduction. Hoch, J.A., and Silhavy, T.J. (eds). Washington DC: American Society for Microbiology, pp. 333-349.
62. Zierler, M.K., and Galán, J.E. (1995) Contact with epithelial cells stimulates secretion of Salmonella typhimurium invasion protein InvJ. Infect Immun 63: 4024-4028.