Mouse models to assess the efficacy of non-typhoidal Salmonella vaccines: Revisiting the role of host innate susceptibility and routes of challenge

Vaccine

Volumn 29, Issue 32, 2011, Pages 5094-5106

  Simon, Raphael ^a,b   Tennant, Sharon M ^a,b   Galen, James E ^a,b   Levine, Myron M ^a,b  

^a University of Maryland School of Medicine Center for Vaccine Development   (United States)

^b UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

Conjugate vaccine; Live attenuated vaccine; Mouse model; Salmonella Enteritidis; Salmonella Typhimurium; Vaccine efficacy

Indexed keywords

SALMONELLOSIS VACCINE;

AFRICA; BACTEREMIA; BACTERIAL MENINGITIS; BACTERIAL STRAIN; BACTERIAL VIRULENCE; CELLULAR IMMUNITY; DRUG EFFICACY; GASTROENTERITIS; HOST PATHOGEN INTERACTION; HUMORAL IMMUNITY; IMMUNIZATION; INFECTION SENSITIVITY; INNATE IMMUNITY; MOUSE STRAIN; NONHUMAN; PRIORITY JOURNAL; REVIEW; SALMONELLA ENTERICA; SALMONELLA ENTERITIDIS; SALMONELLA TYPHIMURIUM; SEROTYPE;

ANIMALS; DISEASE MODELS, ANIMAL; HOST-PATHOGEN INTERACTIONS; IMMUNITY, INNATE; MICE; SALMONELLA ENTERITIDIS; SALMONELLA INFECTIONS; SALMONELLA TYPHIMURIUM; SALMONELLA VACCINES;

EID: 79960324045     PISSN: 0264410X     EISSN: 18732518     Source Type: Journal    
DOI: 10.1016/j.vaccine.2011.05.022     Document Type: Review

References (118)

1. Ivanoff B., Levine M.M., Lambert P.H. Vaccination against typhoid fever: present status. Bull World Health Organ 1994, 72(6):957-971.
2. Preliminary FoodNet data on the incidence of infection with pathogens transmitted commonly through food-10 states, 2009. MMWR Morb Mortal Wkly Rep 2010;59(April (14)):418-22.
3. Vugia D.J., Samuel M., Farley M.M., Marcus R., Shiferaw B., Shallow S. Invasive Salmonella infections in the United States, FoodNet, 1996-1999: incidence, serotype distribution, and outcome. Clin Infect Dis 2004, 38(April (Suppl 3)):149-156.
4. Berkley J.A., Lowe B.S., Mwangi I., Williams T., Bauni E., Mwarumba S., et al. Bacteremia among children admitted to a rural hospital in Kenya. N Engl J Med 2005, 352(January (1)):39-47.
5. Mandomando I., Macete E., Sigauque B., Morais L., Quinto L., Sacarlal J., et al. Invasive non-typhoidal Salmonella in Mozambican children. Trop Med Int Health 2009, 14(December (12)):1467-1474.
6. Brent A.J., Oundo J.O., Mwangi I., Ochola L., Lowe B., Berkley J.A. Salmonella bacteremia in Kenyan children. Pediatr Infect Dis J 2006, 25(March (3)):230-236.
7. Graham S.M., Walsh A.L., Molyneux E.M., Phiri A.J., Molyneux M.E. Clinical presentation of non-typhoidal Salmonella bacteraemia in Malawian children. Trans R Soc Trop Med Hyg 2000, 94(May-June (3)):310-314.
8. Kariuki S., Revathi G., Kariuki N., Kiiru J., Mwituria J., Hart C.A. Characterisation of community acquired non-typhoidal Salmonella from bacteraemia and diarrhoeal infections in children admitted to hospital in Nairobi, Kenya. BMC Microbiol 2006, 6:101.
9. Ikumapayi U.N., Antonio M., Sonne-Hansen J., Biney E., Enwere G., Okoko B., et al. Molecular epidemiology of community-acquired invasive non-typhoidal Salmonella among children aged 2-29 months in rural Gambia and discovery of a new serovar, Salmonella enterica Dingiri. J Med Microbiol 2007, 56(November (Pt 11)):1479-1484.
10. Lepage P., Bogaerts J., Van Goethem C., Ntahorutaba M., Nsengumuremyi F., Hitimana D.G., et al. Community-acquired bacteraemia in African children. Lancet 1987, 1(June (8548)):1458-1461.
11. O'Dempsey T.J., McArdle T.F., Lloyd-Evans N., Baldeh I., Laurence B.E., Secka O., et al. Importance of enteric bacteria as a cause of pneumonia, meningitis and septicemia among children in a rural community in The Gambia, West Africa. Pediatr Infect Dis J 1994, 13(February (2)):122-128.
12. Walsh A.L., Phiri A.J., Graham S.M., Molyneux E.M., Molyneux M.E. Bacteremia in febrile Malawian children: clinical and microbiologic features. Pediatr Infect Dis J 2000, 19(April (4)):312-318.
13. Sigauque B., Roca A., Mandomando I., Morais L., Quinto L., Sacarlal J., et al. Community-acquired bacteremia among children admitted to a rural hospital in Mozambique. Pediatr Infect Dis J 2009, 28(February (2)):108-113.
14. Tennant S.M., Diallo S., Levy H., Livio S., Sow S.O., Tapia M., et al. Identification by PCR of non-typhoidal Salmonella enterica serovars associated with invasive infections among febrile patients in Mali. PLoS Negl Trop Dis 2010, 4(3):pe621.
15. Enwere G., Biney E., Cheung Y.B., Zaman S.M., Okoko B., Oluwalana C., et al. Epidemiologic and clinical characteristics of community-acquired invasive bacterial infections in children aged 2-29 months in The Gambia. Pediatr Infect Dis J 2006, 25(August (8)):700-705.
16. Kingsley R.A., Msefula C.L., Thomson N.R., Kariuki S., Holt K.E., Gordon M.A., et al. Epidemic multiple drug resistant Salmonella Typhimurium causing invasive disease in sub-Saharan Africa have a distinct genotype. Genome Res 2009, 19(December (12)):2279-2287.
17. Kariuki S., Revathi G., Gakuya F., Yamo V., Muyodi J., Hart C.A. Lack of clonal relationship between non-Typhi Salmonella strain types from humans and those isolated from animals living in close contact. FEMS Immunol Med Microbiol 2002, 33(July (3)):165-171.
18. Carter P.B., Collins F.M. The route of enteric infection in normal mice. J Exp Med 1974, 139(May (5)):1189-1203.
19. Haraga A., Ohlson M.B., Miller S.I. Salmonellae interplay with host cells. Nat Rev Microbiol 2008, 6(January (1)):53-66.
20. Collins F.M. Recall of immunity in mice vaccinated with Salmonella Enteritidis or Salmonella Typhimurium. J Bacteriol 1968, 95(June (6)):2014-2021.
21. Jarvelainen H.A., Galmiche A., Zychlinsky A. Caspase-1 activation by Salmonella. Trends Cell Biol 2003, 13(April (4)):204-209.
22. Watson K.G., Holden D.W. Dynamics of growth and dissemination of Salmonella in vivo. Cell Microbiol 2010, 12(October (10)):1389-1397.
23. Valdez Y., Ferreira R.B., Finlay B.B. Molecular mechanisms of Salmonella virulence and host resistance. Curr Top Microbiol Immunol 2009, 337:93-127.
24. Jones B.D., Ghori N., Falkow S. Salmonella Typhimurium initiates murine infection by penetrating and destroying the specialized epithelial M cells of the Peyer's patches. J Exp Med 1994, 180(July (1)):15-23.
25. Vazquez-Torres A., Jones-Carson J., Baumler A.J., Falkow S., Valdivia R., Brown W., et al. Extraintestinal dissemination of Salmonella by CD18-expressing phagocytes. Nature 1999, 401(October (6755)):804-808.
26. Collins F.M., Carter P.B. Comparative immunogenicity of heat-killed and living oral Salmonella vaccines. Infect Immun 1972, 6(October (4)):451-458.
27. Collins F.M. Effect of specific immune mouse serum on the growth of Salmonella Enteritidis in mice preimmunized with living or ethyl alcohol-killed vaccines. J Bacteriol 1969, 97(February (2)):676-683.
28. Collins F.M. Effect of specific immune mouse serum on the growth of Salmonella Enteritidis in nonvaccinated mice challenged by various routes. J Bacteriol 1969, 97(February (2)):667-675.
29. Chatfield S.N., Strugnell R.A., Dougan G. Live Salmonella as vaccines and carriers of foreign antigenic determinants. Vaccine 1989, 7(December(6)):495-498.
30. Zhang X., Kelly S.M., Bollen W.S., Curtiss R. Characterization and immunogenicity of Salmonella Typhimurium SL1344 and UK-1 Δcrp and Δcdt deletion mutants. Infect Immun 1997, 65(December (12)):5381-5387.
31. Curtiss R., Wanda S.Y., Gunn B.M., Zhang X., Tinge S.A., Ananthnarayan V., et al. Salmonella enterica serovar Typhimurium strains with regulated delayed attenuation in vivo. Infect Immun 2009, 77(March (3)):1071-1082.
32. Heithoff D.M., Sinsheimer R.L., Low D.A., Mahan M.J. An essential role for DNA adenine methylation in bacterial virulence. Science 1999, 284(May (5416)):967-970.
33. Heithoff D.M., Enioutina E.Y., Daynes R.A., Sinsheimer R.L., Low D.A., Mahan M.J. Salmonella DNA adenine methylase mutants confer cross-protective immunity. Infect Immun 2001, 69(November (11)):6725-6730.
34. Pasetti M.F., Levine M.M., Sztein M.B. Animal models paving the way for clinical trials of attenuated Salmonella enterica serovar Typhi live oral vaccines and live vectors. Vaccine 2003, 21(January (5-6)):401-418.
35. Galen J.E., Pasetti M.F., Tennant S., Ruiz-Olvera P., Sztein M.B., Levine M.M. Salmonella enterica serovar Typhi live vector vaccines finally come of age. Immunol Cell Biol 2009, 87(July (5)):400-412.
36. Matsui H., Suzuki M., Isshiki Y., Kodama C., Eguchi M., Kikuchi Y., et al. Oral immunization with ATP-dependent protease-deficient mutants protects mice against subsequent oral challenge with virulent Salmonella enterica serovar Typhimurium. Infect Immun 2003, 71(January (1)):30-39.
37. Miller S.I., Loomis W.P., Alpuche-Aranda C., Behlau I., Hohmann E. The PhoP virulence regulon and live oral Salmonella vaccines. Vaccine 1993, 11(2):122-125.
38. McFarland W.C., Stocker B.A. Effect of different purine auxotrophic mutations on mouse-virulence of a Vi-positive strain of Salmonella dublin and of two strains of Salmonella Typhimurium. Microb Pathog 1987, 3(August (2)):129-141.
39. Watson D.C., Robbins J.B., Szu S.C. Protection of mice against Salmonella Typhimurium with an O-specific polysaccharide-protein conjugate vaccine. Infect Immun 1992, 60(November (11)):4679-4686.
40. Carter P.B., Collins F.M. Assessment of typhoid vaccines by using the intraperitoneal route of challenge. Infect Immun 1977, 17(September (3)):555-560.
41. Srinivasan A., McSorley S.J. Activation of Salmonella-specific immune responses in the intestinal mucosa. Arch Immunol Ther Exp (Warsz) 2006, 54(January-February (1)):25-31.
42. Moon J.J., McSorley S.J. Tracking the dynamics of Salmonella specific T cell responses. Curr Top Microbiol Immunol 2009, 334:179-198.
43. Angerman C.R., Eisenstein T.K. Comparative efficacy and toxicity of a ribosomal vaccine, acetone-killed cells, lipopolysaccharide, and a live cell vaccine prepared from Salmonella Typhimurium. Infect Immun 1978, 19(February (2)):575-582.
44. Eisenstein T.K., Angerman C.R. Immunity to experimental Salmonella infection: studies on the protective capacity and immunogenicity of lipopolysaccharide, acetone-killed cells, and ribosome-rich extracts of Salmonella Typhimurium in C3H/HeJ and CD-1 mice. J Immunol 1978, 121(September (3)):1010-1014.
45. Eisenstein T.K., Deakins L.W., Killar L., Saluk P.H., Sultzer B.M. Dissociation of innate susceptibility to Salmonella infection and endotoxin responsiveness in C3HeB/FeJ mice and other strains in the C3H lineage. Infect Immun 1982, 36(May (2)):696-703.
46. Eisenstein T.K., Killar L.M., Sultzer B.M. Immunity to infection with Salmonella Typhimurium: mouse-strain differences in vaccine- and serum-mediated protection. J Infect Dis 1984, 150(September (3)):425-435.
47. Killar L.M., Eisenstein T.K. Immunity to Salmonella Typhimurium infection in C3H/HeJ and C3H/HeNCrlBR mice: studies with an aromatic-dependent live S. Typhimurium strain as a vaccine. Infect Immun 1985, 47(March (3)):605-612.
48. Collins F.M. Immunity to enteric infection in mice. Infect Immun 1970, 1(March (3)):243-250.
49. Hormaeche C.E. Genetics of natural resistance to Salmonellae in mice. Immunology 1979, 37(June (2)):319-327.
50. Hormaeche C.E. Natural resistance to Salmonella Typhimurium in different inbred mouse strains. Immunology 1979, 37(June (2)):311-318.
51. Hormaeche C.E., Maskell D.J., Harrington K., Joysey H., Brock J. Mechanisms of natural resistance to mouse typhoid. Bull Eur Physiopathol Respir 1983, 19(March-April (2)):137-142.
52. Collins F.M. Salmonellosis in orally infected specific pathogen-free C57B1 mice. Infect Immun 1972, 5(February (2)):191-198.
53. Plant J., Glynn A.A. Genetics of resistance to infection with Salmonella Typhimurium in mice. J Infect Dis 1976, 133(January (1)):72-78.
54. Robson H.G., Vas S.I. Resistance of inbred mice to Salmonella Typhimurium. J Infect Dis 1972, 126(October (4)):378-386.
55. Vidal S.M., Malo D., Vogan K., Skamene E., Gros P. Natural resistance to infection with intracellular parasites: isolation of a candidate for Bcg. Cell 1993, 73(May (3)):469-485.
56. Cellier M.F., Courville P., Campion C. Nramp1 phagocyte intracellular metal withdrawal defense. Microbes Infect 2007, 9(Novemeber-December (14-15)):1662-1670.
57. Eisenstein T.K., Killar L.M., Stocker B.A., Sultzer B.M. Cellular immunity induced by avirulent Salmonella in LPS-defective C3H/HeJ mice. J Immunol 1984, 133(August (2)):958-961.
58. Poltorak A., He X., Smirnova I., Liu M.Y., Van Huffel C., Du X., et al. Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science 1998, 282(December (5396)):2085-2088.
59. Qureshi S.T., Lariviere L., Leveque G., Clermont S., Moore K.J., Gros P., et al. Endotoxin-tolerant mice have mutations in Toll-like receptor 4 (Tlr4). J Exp Med 1999, 189(February (4)):615-625.
60. Talbot S., Totemeyer S., Yamamoto M., Akira S., Hughes K., Gray D., et al. Toll-like receptor 4 signalling through MyD88 is essential to control Salmonella enterica serovar Typhimurium infection, but not for the initiation of bacterial clearance. Immunology 2009, 128(December (4)):472-483.
61. Wick M.J. Living in the danger zone: innate immunity to Salmonella. Curr Opin Microbiol 2004, 7(February (1)):51-57.
62. Fierer J., Swancutt M.A., Heumann D., Golenbock D. The role of lipopolysaccharide binding protein in resistance to Salmonella infections in mice. J Immunol 2002, 168(June (12)):6396-6403.
63. Harrison J.A., Villarreal-Ramos B., Mastroeni P., Demarco de Hormaeche R., Hormaeche C.E. Correlates of protection induced by live Aro-Salmonella Typhimurium vaccines in the murine typhoid model. Immunology 1997, 90(April (4)):618-625.
64. McSorley S.J., Cookson B.T., Jenkins M.K. Characterization of CD4+ T cell responses during natural infection with Salmonella Typhimurium. J Immunol 2000, 164(January (2)):986-993.
65. Hormaeche C.E., Mastroeni P., Harrison J.A., Demarco de Hormaeche R., Svenson S., Stocker B.A. Protection against oral challenge three months after i. v. immunization of BALB/c mice with live Aro Salmonella Typhimurium and Salmonella Enteritidis vaccines is serotype (species)-dependent and only partially determined by the main LPS O antigen. Vaccine 1996, 14(March (4)):251-259.
66. Mastroeni P., Villarreal-Ramos B., 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 1993, 61(September (9)):3981-3984.
67. Mastroeni P., Simmons C., Fowler R., Hormaeche C.E., Dougan G. Igh-6(-/-) (B-cell-deficient) mice fail to mount solid acquired resistance to oral challenge with virulent Salmonella enterica serovar Typhimurium and show impaired Th1 T-cell responses to Salmonella antigens. Infect Immun 2000, 68(January (1)):46-53.
68. McSorley S.J., Jenkins M.K. Antibody is required for protection against virulent but not attenuated Salmonella enterica serovar Typhimurium. Infect Immun 2000, 68(June (6)):3344-3348.
69. Collins F.M. Immunogenicity of living and heat-killed Salmonella pullorum vaccines. Infect Immun 1973, 7(May (5)):735-742.
70. Collins F.M. Effect of adjuvant on immunogenicity of a heat-killed Salmonella vaccine. J Infect Dis 1972, 126(July (1)):69-76.
71. Matsui K., Arai T. Protective immunity induced by porin in experimental mouse salmonellosis. Microbiol Immunol 1989, 33(9):699-708.
72. Matsui K., Arai T. Protective immunities induced by porins from mutant strains of Salmonella Typhimurium. Microbiol Immunol 1990, 34(11):917-927.
73. Jazani N.H., Worobec E., Shahabi S., Nejad G.B. Conjugation of tetanus toxoid with Salmonella Typhimurium PTCC 1735 O-specific polysaccharide and its effects on production of opsonizing antibodies in a mouse model. Can J Microbiol 2005, 51(April (4)):319-324.
74. Gil-Cruz C., Bobat S., Marshall J.L., Kingsley R.A., Ross E.A., Henderson I.R., et al. The porin OmpD from nontyphoidal Salmonella is a key target for a protective B1b cell antibody response. Proc Natl Acad Sci U S A 2009, 106(June (24)):9803-9808.
75. Udhayakumar V., Muthukkaruppan V.R. Protective immunity induced by outer membrane proteins of Salmonella Typhimurium in mice. Infect Immun 1987, 55(March (3)):816-821.
76. Muthukkumar S., Muthukkaruppan V.R. Mechanism of protective immunity induced by porin-lipopolysaccharide against murine salmonellosis. Infect Immun 1993, 61(July (7)):3017-3025.
77. Kita E., Nishi K., Emoto M., Katsui N., Yasui K., Kashiba S. Analysis of immunity to infection with Salmonella Typhimurium in outbred mice I. Requirement of the antibody to non-O antigen for protection in mice that are not protected by the RNA-rich vaccine. Immunology 1987, 61(August (4)):535-541.
78. Kuusi N., Nurminen M., Saxen H., Valtonen M., Makela P.H. Immunization with major outer membrane proteins in experimental salmonellosis of mice. Infect Immun 1979, 25(September (3)):857-862.
79. Ornellas E.P., Roantree R.J., Steward J.P. The specificity and importance of humoral antibody in the protection of mice against intraperitoneal challenge with complement-sensitive and complement-resistant Salmonella. J Infect Dis 1970, 121(February (2)):113-123.
80. Svenson S.B., Nurminen M., Lindberg A.A. Artificial Salmonella vaccines: O-antigenic oligosaccharide-protein conjugates induce protection against infection with Salmonella Typhimurium. Infect Immun 1979, 25(September (3)):863-872.
81. Kenny K., Herzberg M. Early antibody response in mice to either infection or immunization with Salmonella Typhimurium. J Bacteriol 1967, 93(March (3)):773-778.
82. Herzberg M., Nash P., Hino S. Degree of immunity induced by killed vaccines to experimental salmonellosis in mice. Infect Immun 1972, 5(January (1)):83-90.
83. Tabaraie B., Sharma B.K., Sharma P.R., Sehgal R., Ganguly N.K. Evaluation of Salmonella porins as a broad spectrum vaccine candidate. Microbiol Immunol 1994, 38(7):553-559.
84. Mastroeni P., Menager N. Development of acquired immunity to Salmonella. J Med Microbiol 2003, 52(June (Pt 6)):453-459.
85. Michetti P., Mahan M.J., Slauch J.M., Mekalanos J.J., Neutra M.R. Monoclonal secretory immunoglobulin A protects mice against oral challenge with the invasive pathogen Salmonella Typhimurium. Infect Immun 1992, 60(May (5)):1786-1792.
86. Michetti P., Porta N., Mahan M.J., Slauch J.M., Mekalanos J.J., Blum A.L., et al. Monoclonal immunoglobulin A prevents adherence and invasion of polarized epithelial cell monolayers by Salmonella Typhimurium. Gastroenterology 1994, 107(October (4)):915-923.
87. Eisenstein T.K. Intracellular pathogens: the role of antibody-mediated protection in Salmonella infection. Trends Microbiol 1998, 6(April (4)):135-136.
88. Casadevall A., Pirofski L.A. A reappraisal of humoral immunity based on mechanisms of antibody-mediated protection against intracellular pathogens. Adv Immunol 2006, 91:1-44.
89. Cunningham A.F., Gaspal F., Serre K., Mohr E., Henderson I.R., Scott-Tucker A., et al. Salmonella induces a switched antibody response without germinal centers that impedes the extracellular spread of infection. J Immunol 2007, 178(May (10)):6200-6207.
90. Roantree R.J., Rantz L.A. A study of the relationship of the normal bactericidal activity of human serum to bacterial infection. J Clin Invest 1960, 39(January (1)):72-81.
91. Souwer Y., Griekspoor A., Jorritsma T., de Wit J., Janssen H., Neefjes J., et al. B cell receptor-mediated internalization of Salmonella: a novel pathway for autonomous B cell activation and antibody production. J Immunol 2009, 182(June (12)):7473-7481.
92. Liang-Takasaki C.J., Saxen H., Makela P.H., Leive L. Complement activation by polysaccharide of lipopolysaccharide: an important virulence determinant of Salmonellae. Infect Immun 1983, 41(August (2)):563-569.
93. Jimenez-Lucho V.E., Joiner K.A., Foulds J., Frank M.M., Leive L. C3b generation is affected by the structure of the O-antigen polysaccharide in lipopolysaccharide from Salmonellae. J Immunol 1987, 139(August (4)):1253-1259.
94. Mittrucker H.W., Raupach B., Kohler A., Kaufmann S.H. Cutting edge: role of B lymphocytes in protective immunity against Salmonella Typhimurium infection. J Immunol 2000, 164(February (4)):1648-1652.
95. Mastroeni P., Villarreal-Ramos B., Hormaeche C.E. Role of T cells, TNF alpha and IFN gamma in recall of immunity to oral challenge with virulent Salmonellae in mice vaccinated with live attenuated aro-Salmonella vaccines. Microb Pathog 1992, 13(December (6)):477-491.
96. Lo W.F., Ong H., Metcalf E.S., Soloski M.J. T cell responses to Gram-negative intracellular bacterial pathogens: a role for CD8+ T cells in immunity to Salmonella infection and the involvement of MHC class Ib molecules. J Immunol 1999, 162(May (9)):5398-5406.
97. Collins F.M. Vaccines and cell-mediated immunity. Bacteriol Rev 1974, 38(December (4)):371-402.
98. Bergman M.A., Cummings L.A., Alaniz R.C., Mayeda L., Fellnerova I., Cookson B.T. CD4+-T-cell responses generated during murine Salmonella enterica serovar Typhimurium infection are directed towards multiple epitopes within the natural antigen FliC. Infect Immun 2005, 73(Novemeber (11)):7226-7235.
99. Bergman M.A., Cummings L.A., Barrett S.L., Smith K.D., Lara J.C., Aderem A., et al. CD4+ T cells and toll-like receptors recognize Salmonella antigens expressed in bacterial surface organelles. Infect Immun 2005, 73(March (3)):1350-1356.
100. Mastroeni P., Arena A., Costa G.B., Liberto M.C., Bonina L., Hormaeche C.E. Serum TNF alpha in mouse typhoid and enhancement of a Salmonella infection by anti-TNF alpha antibodies. Microb Pathog 1991, 11(July (1)):33-38.
101. Mittrucker H.W., Kohler A., Mak T.W., Kaufmann S.H. Critical role of CD28 in protective immunity against Salmonella Typhimurium. J Immunol 1999, 163(December (12)):6769-6776.
102. Ravindran R., Foley J., Stoklasek T., Glimcher L.H., McSorley S.J. Expression of T-bet by CD4 T cells is essential for resistance to Salmonella infection. J Immunol 2005, 175(October (7)):4603-4610.
103. Monack D.M., Bouley D.M., Falkow S. Salmonella Typhimurium persists within macrophages in the mesenteric lymph nodes of chronically infected Nramp1+/+ mice and can be reactivated by IFNgamma neutralization. J Exp Med 2004, 199(January (2)):231-241.
104. Alaniz R.C., Cummings L.A., Bergman M.A., Rassoulian-Barrett S.L., Cookson B.T. Salmonella Typhimurium coordinately regulates FliC location and reduces dendritic cell activation and antigen presentation to CD4+ T cells. J Immunol 2006, 177(September (6)):3983-3993.
105. Lalmanach A.C., Lantier F. Host cytokine response and resistance to Salmonella infection. Microbes Infect 1999, 1(July (9)):719-726.
106. Eckmann L., Kagnoff M.F. Cytokines in host defense against Salmonella. Microbes Infect 2001, 3(November-December (14-15)):1191-1200.
107. van de Vosse E., Hoeve M.A., Ottenhoff T.H. Human genetics of intracellular infectious diseases: molecular and cellular immunity against mycobacteria and Salmonellae. Lancet Infect Dis 2004, 4(December (12)):739-749.
108. van de Vosse E., van Dissel J.T., Ottenhoff T.H. Genetic deficiencies of innate immune signalling in human infectious disease. Lancet Infect Dis 2009, 9(November (11)):688-698.
109. Dunstan S.J., Stephens H.A., Blackwell J.M., Duc C.M., Lanh M.N., Dudbridge F., et al. Genes of the class II and class III major histocompatibility complex are associated with typhoid fever in Vietnam. J Infect Dis 2001, 183(January (2)):261-268.
110. Hormaeche C.E., Harrington K.A., Joysey H.S. Natural resistance to Salmonellae in mice: control by genes within the major histocompatibility complex. J Infect Dis 1985, 152(November (5)):1050-1056.
111. Svenson S.B., Lindberg A.A. Protection against mouse typhoid by artificial Salmonella vaccines. Scand J Infect Dis 1980, 24(Suppl 24):210-215.
112. Jorbeck H.J., Svenson S.B., Lindberg A.A. Artificial Salmonella vaccines: Salmonella Typhimurium O-antigen-specific oligosaccharide-protein conjugates elicit opsonizing antibodies that enhance phagocytosis. Infect Immun 1981, 32(May (2)):497-502.
113. Svenson S.B., Lindberg A.A. Artificial Salmonella vaccines: Salmonella Typhimurium O-antigen-specific oligosaccharide-protein conjugates elicit protective antibodies in rabbits and mice. Infect Immun 1981, 32(May (2)):490-496.
114. Colwell D.E., Michalek S.M., Briles D.E., Jirillo E., McGhee J.R. Monoclonal antibodies to Salmonella lipopolysaccharide: anti-O-polysaccharide antibodies protect C3H mice against challenge with virulent Salmonella Typhimurium. J Immunol 1984, 133(August (2)):950-957.
115. Levine M.M., Taylor D.N., Ferreccio C. Typhoid vaccines come of age. Pediatr Infect Dis J 1989, 8(June (6)):374-381.
116. Lin F.Y., Ho V.A., Khiem H.B., Trach D.D., Bay P.V., Thanh T.C., et al. The efficacy of a Salmonella Typhi Vi conjugate vaccine in two-to-five-year-old children. N Engl J Med 2001, 344(April (17)):1263-1269.
117. Mai N.L., Phan V.B., Vo A.H., Tran C.T., Lin F.Y., Bryla D.A., et al. Persistent efficacy of Vi conjugate vaccine against typhoid fever in young children. N Engl J Med 2003, 349(October (14)):1390-1391.
118. Szu S.C., Taylor D.N., Trofa A.C., Clements J.D., Shiloach J., Sadoff J.C., et al. Laboratory and preliminary clinical characterization of Vi capsular polysaccharide-protein conjugate vaccines. Infect Immun 1994, 62(October (10)):4440-4444.