Immunological responses against Salmonella enterica serovar Typhimurium Braun lipoprotein and lipid A mutant strains in Swiss-Webster mice: Potential use as live-attenuated vaccines

Microbial Pathogenesis

Volumn 44, Issue 3, 2008, Pages 224-237

  Liu, Tie ^a   König, Rolf ^a   Sha, Jian ^a   Agar, Stacy L ^a   Tseng, Chien Te K ^a   Klimpel, Gary R ^a   Chopra, Ashok K ^a  

^a University of Texas Medical Branch School of Medicine   (United States)

Author keywords

Immune responses; Mouse model; Salmonella Typhimurium; Vaccine

Indexed keywords

HERMES ANTIGEN; IMMUNOGLOBULIN G; IMMUNOGLOBULIN G2A; INTERLEUKIN 6; LIPID A; LIPOPROTEIN; LIVE VACCINE;

ACYLATION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN EXPRESSION; ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; CD4+ T LYMPHOCYTE; CELL PROLIFERATION; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE RELEASE; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; GENE DELETION; GENE MUTATION; GENETIC CODE; HUMORAL IMMUNITY; IMMUNE RESPONSE; IMMUNOGLOBULIN BLOOD LEVEL; MOUSE; NONHUMAN; OUTCOME ASSESSMENT; PRIORITY JOURNAL; SALMONELLA ENTERICA; SALMONELLA TYPHIMURIUM; SEROTYPE; SURVIVAL RATE; T LYMPHOCYTE ACTIVATION;

ANIMALS; BACTERIAL VACCINES; LIPID A; LIPOPROTEINS; MICE; SALMONELLA INFECTIONS; SALMONELLA TYPHIMURIUM; VACCINES, ATTENUATED;

ANIMALIA; MUS; SALMONELLA ENTERICA SUBSP. ENTERICA SEROVAR TYPHIMURIUM; SALMONELLA TYPHIMURIUM;

EID: 38549141239     PISSN: 08824010     EISSN: 10961208     Source Type: Journal    
DOI: 10.1016/j.micpath.2007.09.005     Document Type: Article

References (70)

1. Kaufmann S.H., Raupach B., and Finlay B.B. Introduction: microbiology and immunology: lessons learned from Salmonella. Microbes Infect 3 (2001) 1177-1181
2. Kabra S.K., Madhulika, Talati A., Soni N., Patel S., and Modi R.R. Multidrug-resistant typhoid fever. Trop Doct 30 (2000) 195-197
3. Pang T., Levine M.M., Ivanoff B., Wain J., and Finlay B.B. Typhoid fever-important issues still remain. Trends Microbiol 6 (1998) 131-133
4. Jones B.D., Ghori N., and Falkow S. Salmonella Typhimurium initiates murine infection by penetrating and destroying the specialized epithelial M cells of the Peyer's patches. J Exp Med 180 (1994) 15-23
5. Glauser M.P., Zanetti G., Baumgartner J.D., and Cohen J. Septic shock: pathogenesis. Lancet 338 (1991) 732-736
6. Braun V., and Hantke K. Biochemistry of bacterial cell envelopes. Annu Rev Biochem 43 (1974) 89-121
7. Juncker A.S., Willenbrock H., Von Heijne G., Brunak S., Nielsen H., and Krogh A. Prediction of lipoprotein signal peptides in Gram-negative bacteria. Protein Sci 12 (2003) 1652-1662
8. Hayashi S., and Wu H.C. Lipoproteins in bacteria. J Bioenerg Biomembr 22 (1990) 451-471
9. Sha J., Fadl A.A., Klimpel G.R., Niesel D.W., Popov V.L., and Chopra A.K. The two murein lipoproteins of Salmonella enterica serovar Typhimurium contribute to the virulence of the organism. Infect Immun 72 (2004) 3987-4003
10. Neidhardt F., Ingraham J., Low K., Magasanik B., Schaechter M., and Umbarger H. Escherichia coli and Salmonella typhimurium: cellular and molecular biology (1987), American Society for Microbiology, Washington, DC
11. Guo L., Lim K.B., Gunn J.S., Bainbridge B., Darveau R.P., Hackett M., et al. Regulation of lipid A modifications by Salmonella Typhimurium virulence genes phoP-phoQ. Science 276 (1997) 250-253
12. Clementz T., Zhou Z., and Raetz C.R. Function of the Escherichia coli msbB gene, a multicopy suppressor of htrB knockouts, in the acylation of lipid A. Acylation by MsbB follows laurate incorporation by HtrB. J Biol Chem 272 (1997) 10353-10360
13. Post D.M., Ketterer M.R., Phillips N.J., Gibson B.W., and Apicella M.A. The msbB mutant of Neisseria meningitis strain NMB has a defect in lipooligosaccharide assembly and transport to the outer membrane. Infect Immun 71 (2003) 647-655
14. Khan S.A., Everest P., Servos S., Foxwell N., Zahringer U., Brade H., et al. A lethal role for lipid A in Salmonella infections. Mol Microbiol 29 (1998) 571-579
15. Low K.B., Ittensohn M., Le T., Platt J., Sodi S., Amoss M., et al. Lipid A mutant Salmonella with suppressed virulence and TNFα induction retain tumor-targeting in vivo. Nat Biotechnol 17 (1999) 37-41
16. Evans M.E., and Pollack M. Effect of antibiotic class and concentration on the release of lipopolysaccharide from Escherichia coli. J Infect Dis 167 (1993) 1336-1343
17. Dofferhoff A.S., Nijland J.H., de Vries-Hospers H.G., Mulder P.O., Weits J., and Bom V.J. Effects of different types and combinations of antimicrobial agents on endotoxin release from gram-negative bacteria: an in vitro and in vivo study. Scand J Infect Dis 23 (1991) 745-754
18. Gately M.K., Renzetti L.M., Magram J., Stern A.S., Adorini L., Gubler U., et al. The interleukin-12/interleukin-12-receptor system: role in normal and pathologic immune responses. Annu Rev Immunol 16 (1998) 495-521
19. Aliprantis A.O., Yang R.B., Mark M.R., Suggett S., Devaux B., Radolf J.D., et al. Cell activation and apoptosis by bacterial lipoproteins through toll-like receptor-2. Science 285 (1999) 736-739
20. Zhang H., Peterson J.W., Niesel D.W., and Klimpel G.R. Bacterial lipoprotein and lipopolysaccharide act synergistically to induce lethal shock and proinflammatory cytokine production. J Immunol 159 (1997) 4868-4878
21. Means T.K., Golenbock D.T., and Fenton M.J. The biology of toll-like receptors. Cytokine Growth Factor Rev 11 (2000) 219-232
22. Chow J.C., Young D.W., Golenbock D.T., Christ W.J., and Gusovsky F. Toll-like receptor-4 mediates lipopolysaccharide-induced signal transduction. J Biol Chem 274 (1999) 10689-10692
23. Fadl A.A., Sha J., Klimpel G.R., Olano J.P., Niesel D.W., and Chopra A.K. Murein lipoprotein is a critical outer membrane component involved in Salmonella enterica serovar Typhimurium systemic infection. Infect Immun 73 (2005) 1081-1096
24. Brightbill H.D., Libraty D.H., Krutzik S.R., Yang R.B., Belisle J.T., Bleharski J.R., et al. Host defense mechanisms triggered by microbial lipoproteins through toll-like receptors. Science 285 (1999) 732-736
25. Fadl A.A., Sha J., Klimpel G.R., Olano J.P., Galindo C.L., and Chopra A.K. Attenuation of Salmonella enterica serovar Typhimurium by altering biological functions of murein lipoprotein and lipopolysaccharide. Infect Immun 73 (2005) 8433-8436
26. Sprent J. Immunological memory. Current Opin Immunol 9 (1997) 371
27. Eisenstein T.K., Killar L.M., Stocker B.A., and Sultzer B.M. Cellular immunity induced by avirulent Salmonella in LPS-defective C3H/HeJ mice. J Immunol 133 (1984) 958-961
28. Lee J.C., Gibson C.W., and Eisenstein T.K. Macrophage-mediated mitogenic suppression induced in mice of the C3H lineage by a vaccine strain of Salmonella typhimurium. Cell Immunol 91 (1985) 75-91
29. Akira S., Takeda K., and Kaisho T. Toll-like receptors: critical proteins linking innate and acquired immunity. Nat Immunol 2 (2001) 675
30. Mittrucker H.-W., Kohler A., and Kaufmann S.H.E. Characterization of the murine T-lymphocyte response to Salmonella enterica serovar Typhimurium infection. Infect Immun 70 (2002) 199-203
31. Kaufmann S.H. Immunity to intracellular bacteria. In: Paul W.E. (Ed). Fundamental immunology (2003), Lippincott-Raven, Philadelphia 1229-1261
32. Mizuno Y., Takada H., Nomura A., Jin C.H., Hattori H., Ihara K., et al. Th1 and Th1-inducing cytokines in Salmonella infection. Clin Exp Immunol 131 (2003) 111-117
33. Ugrinovic S., Menager N., Goh N., and Mastroeni P. Characterization and development of T-Cell immune responses in B-cell-deficient (Igh-6(-/-)) mice with Salmonella enterica serovar Typhimurium infection. Infect Immun 71 (2003) 6808-6819
34. Lalmanach A.C., and Lantier F. Host cytokine response and resistance to Salmonella infection. Microbes Infect 1 (1999) 719-726
35. Boehm U., Klamp T., Groot M., and Howard J.C. Cellular responses to interferon-gamma. Annu Rev Immunol 15 (1997) 749-795
36. Beutler B., and Cerami A. The biology of cachectin/TNF-a primary mediator of the host response. Annu Rev Immunol 7 (1989) 625-655
37. Beutler B., Milsark I.W., and Cerami A.C. Passive immunization against cachectin/tumor necrosis factor protects mice from lethal effect of endotoxin. Science 229 (1985) 869-871
38. Billiau A., and Dijkmans R. Interferon-γ mechanism of action and therapeutic potential. Biochem Pharmacol 40 (1990) 1433-1439
39. Heinzel F.P. The role of IFN-gamma in the pathology of experimental endotoxemia. J Immunol 145 (1990) 2920-2924
40. Kohler J., Heumann D., Garotta G., LeRoy D., Bailat S., Barras C., et al. IFN-γ involvement in the severity of gram-negative infections in mice. J Immunol 151 (1993) 916-921
41. Le J.M., and Vilcek J. Interleukin 6: a multifunctional cytokine regulating immune reactions and the acute phase protein response. Lab Invest 61 (1989) 588-602
42. Diehl S., Anguita J., Hoffmeyer A., Zapton T., Ihle J.N., Fikrig E., et al. Inhibition of Th1 differentiation by IL-6 is mediated by SOCS1. Immunity 13 (2000) 805-815
43. Rincon M., Anguita J., Nakamura T., Fikrig E., and Flavell R.A. Interleukin (IL)-6 directs the differentiation of IL-4-producing CD4+ T cells. J Exp Med 185 (1997) 461-469
44. Cherwinski H.M., Schumacher J.H., Brown K.D., and Mosmann T.R. Two types of mouse helper T cell clone: III. Further differences in lymphokine synthesis between Th1 and Th2 clones revealed by RNA hybridization, functionally monospecific bioassays, and monoclonal antibodies. J Exp Med 166 (1987) 1229-1244
45. Stevens T.L., Bossie A., Sanders V.M., Fernandez-Botran R., Coffman R.L., Mosmann T.R., et al. Regulation of antibody isotype secretion by subsets of antigen-specific helper T cells. Nature 334 (1988) 255-258
46. Collins F.M. Vaccines and cell-mediated immunity. Bacteriol Rev 38 (1974) 371-402
47. Galdiero M., De Martino L., Marcatili A., Nuzzo I., Vitiello M., and Cipollaro de l'Ero G. Th1 and Th2 cell involvement in immune response to Salmonella typhimurium porins. Immunology 94 (1998) 5-13
48. Guilloteau L., Buzoni-Gatel D., Bernard F., Lantier I., and Lantier F. Salmonella abortusovis infection in susceptible BALB/cby mice: importance of Lyt-2+ and L3T4+ T cells in acquired immunity and granuloma formation. Microb Pathog 14 (1993) 45-55
49. Mastroeni P., Villarreal-Ramos B., and Hormaeche C.E. Adoptive transfer of immunity to oral challenge with virulent salmonellae in innately susceptible BALB/c mice requires both immune serum and T cells. Infect Immun 61 (1993) 3981-3984
50. Paul C., Shalala K., Warren R., and Smith R. Adoptive transfer of murine host protection to salmonellosis with T-cell growth factor-dependent, Salmonella-specific T-cell lines. Infect Immun 48 (1985) 40-43
51. Whittle B.L., and Verma N.K. The immune response to a B-cell epitope delivered by Salmonella is enhanced by prior immunological experience. Vaccine 15 (1997) 1737-1740
52. Coynault C., and Norel F. Comparison of the abilities of Salmonella typhimurium rpoS, aroA and rpoS aroA strains to elicit humoral immune responses in BALB/c mice and to cause lethal infection in athymic BALB/c mice. Microb Pathog 26 (1999) 299-305
53. Brennan F.R., Oliver J.J., and Baird G.D. Differences in the immune responses of mice and sheep to an aromatic-dependent mutant of Salmonella typhimurium. J Med Microbiol 41 (1994) 20-28
54. Hoiseth S.K., and Stocker B.A. Aromatic-dependent Salmonella typhimurium are non-virulent and effective as live vaccines. Nature 291 (1981) 238-239
55. Mastroeni P., Chabalgoity J.A., Dunstan S.J., Maskell D.J., and Dougan G. Salmonella: immune responses and vaccines. Vet J 161 (2001) 132-164
56. Roberts M., Chatfield S.N., and Dougan G. Salmonella as carriers of heterologous antigens. In: O'Hagan D.T. (Ed). Novel delivery systems for oral vaccines (1994), CRC Press, Inc., Boca Raton, FL 27-58
57. Sigwart D.F., Stocker B.A., and Clements J.D. Effect of a purA mutation on efficacy of Salmonella live-vaccine vectors. Infect Immun 57 (1989) 1858-1861
58. O'Callaghan D., Maskell D., Liew F.Y., Easmon C.S., and Dougan G. Characterization of aromatic- and purine-dependent Salmonella typhimurium: attention, persistence, and ability to induce protective immunity in BALB/c mice. Infect Immun 56 (1988) 419-423
59. Curtiss III R., and Kelly S.M. Salmonella typhimurium deletion mutants lacking adenylate cyclase and cyclic AMP receptor protein are avirulent and immunogenic. Infect Immun 55 (1987) 3035-3043
60. Galan J.E., and Curtiss III R. Virulence and vaccine potential of phoP mutants of Salmonella typhimurium. Microb Pathog 6 (1989) 433-443
61. Zhang X., Kelly S.M., Bollen W.S., and Curtiss III R. Characterization and immunogenicity of Salmonella typhimurium SL1344 and UK-1 Δcrp and Δcdt deletion mutants. Infect Immun 65 (1997) 5381-5387
62. Khan S.A., Stratford R., Wu T., McKelvie N., Bellaby T., Hindle Z., et al. Salmonella typhi and S typhimurium derivatives harbouring deletions in aromatic biosynthesis and Salmonella Pathogenicity Island-2 (SPI-2) genes as vaccines and vectors. Vaccine 21 (2003) 538-548
63. Hensel M., Shea J.E., Waterman S.R., Mundy R., Nikolaus T., Banks G., et al. Genes encoding putative effector proteins of the type III secretion system of Salmonella pathogenicity island 2 are required for bacterial virulence and proliferation in macrophages. Mol Microbiol 30 (1998) 163-174
64. Shea J.E., Beuzon C.R., Gleeson C., Mundy R., and Holden D.W. Influence of the Salmonella typhimurium pathogenicity island 2 type III secretion system on bacterial growth in the mouse. Infect Immun 67 (1999) 213-219
65. Shea J.E., Hensel M., Gleeson C., and Holden D.W. Identification of a virulence locus encoding a second type III secretion system in Salmonella typhimurium. Proc Natl Acad Sci USA 93 (1996) 2593-2597
66. Angelakopoulos H., and Hohmann E.L. Pilot study of phoP/phoQ-deleted Salmonella enterica serovar Typhimurium expressing Helicobacter pylori urease in adult volunteers. Infect Immun 68 (2000) 2135-2141
67. Hindle Z., Chatfield S.N., Phillimore J., Bentley M., Johnson J., Cosgrove C.A., et al. Characterization of Salmonella enterica derivatives harboring defined aroC and Salmonella pathogenicity island 2 type III secretion system (ssaV) mutations by immunization of healthy volunteers. Infect Immun 70 (2002) 3457-3467
68. Ravindran R., Rusch L., Itano A., Jenkins M.K., and McSorley S.J. CCR6-dependent recruitment of blood phagocytes is necessary for rapid CD4 T cell responses to local bacterial infection. Proc Natl Acad Sci USA 104 (2007) 12075-12080
69. Hanna E.E., and Hale M. Deregulation of mouse antibody-forming cells in vivo in cell culture by streptococcal pyrogenic exotoxin. Infect Immun 11 (1975) 265-272
70. Julius M.H., Simpson E., and Herzenberg L.A. A rapid method for the isolation of functional thymus-derived murine lymphocytes. Eur J Immunol 3 (1973) 645-649