Abstract
Salmonella spp are Gram-negative bacteria capable of infecting a wide range of host species, including humans, domesticated and wild mammals, reptiles, birds and insects. The outcome of an encounter between Salmonella and its host is dependent upon multiple factors including the host genetic background. To facilitate the study of the genetic factors involved in resistance to this pathogen, mouse models of Salmonella infection have been developed and studied for years, allowing identification of several genes and pathways that may influence the disease outcome. In this review, we will cover some of the genes involved in mouse resistance to Salmonella that were identified through the study of congenic mouse strains, cloning of spontaneous mouse mutations, use of site-directed mutagenesis or quantitative trait loci analysis. In parallel, the relevant information pertaining to genes involved in resistance to Salmonella in humans will be discussed.
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References
Brenner FW, Villar RG, Angulo FJ, Tauxe R, Swaminathan B . Salmonella nomenclature J Clin Microbiol 2000 38: 2465–2467
Centers for Disease Control and Prevention. National Center for Infectious Diseases. Division of Bacterial and Mycotic Diseaseshttp://www.cdc.gov2001
Guard-Petter J . The chicken, the egg and Salmonella enteritidis Environ Microbiol 2001 3: 421–430
Troutt HF, Osburn BI . Meat from dairy cows: possible microbiological hazards and risks Rev Sci Tech 1997 16: 405–414
Schott 2nd HC, Ewart SL, Walker RD et al. An outbreak of salmonellosis among horses at a veterinary teaching hospital J Am Vet Med Assoc 2001 218: 1152–1159 1100
Walker RL, Madigan JE, Hird DW, Case JT, Villanueva MR, Bogenrief DS . An outbreak of equine neonatal salmonellosis J Vet Diagn Invest 1991 3: 223–227
Greenwood CM, Fujiwara TM, Boothroyd LJ et al. Linkage of tuberculosis to chromosome 2q35 loci, including NRAMP1, in a large aboriginal Canadian family Am J Hum Genet 2000 67: 405–416
Bellamy R, Beyers N, McAdam KP et al. Genetic susceptibility to tuberculosis in Africans: a genome-wide scan Proc Natl Acad Sci USA 2000 97: 8005–8009
Marquet S, Abel L, Hillaire D et al. Genetic localization of a locus controlling the intensity of infection by Schistosoma mansoni on chromosome 5q31–q33 Nat Genet 1996 14: 181–184
Pavia AT, Shipman LD, Wells JG et al. Epidemiologic evidence that prior antimicrobial exposure decreases resistance to infection by antimicrobial-sensitive Salmonella J Infect Dis 1990 161: 255–260
Giannella RA, Broitman SA, Zamcheck N . Influence of gastric acidity on bacterial and parasitic enteric infections. A perspective Ann Intern Med 1973 78: 271–276
Wong WY . Prevention and management of infection in children with sickle cell anaemia Paediatr Drugs 2001 3: 793–801
Mouy R, Fischer A, Vilmer E, Seger R, Griscelli C . Incidence, severity, and prevention of infections in chronic granulomatous disease J Pediatr 1989 114: 555–560
Jouanguy E, Doffinger R, Dupuis S, Pallier A, Altare F, Casanova JL . IL-12 and IFN-gamma in host defense against mycobacteria and salmonella in mice and men Curr Opin Immunol 1999 11: 346–351
Dorman SE, Holland SM . Interferon-gamma and interleukin-12 pathway defects and human disease Cytokine Growth Factor Rev 2000 11: 321–333
Sperber SJ, Schleupner CJ . Salmonellosis during infection with human immunodeficiency virus Rev Infect Dis 1987 9: 925–934
Fernandez Guerrero ML, Ramos JM, Nunez A, de Gorgolas M . Focal infections due to non-typhi Salmonella in patients with AIDS: report of 10 cases and review Clin Infect Dis 1997 25: 690–697
Aragon A, Duran Perez-Navarro A . Familial Salmonella-triggered reactive arthritis Br J Rheumatol 1996 35: 908–909
Caron J, Loredo-Osti JC, Laroche L, Skamene E, Morgane K, Malo D . Identification of genetic loci controlling bacterial clearance in experimental Salmonella enteritidis infection: an unexpected role of Nramp 1 (Slc11a1) in the persistence of infection in mice Genes Immun 2002 3: 196–204
Sebastiani G, Olien L, Gauthier S et al. Mapping of genetic modulators of natural resistance to infection with Salmonella typhimurium in wild-derived mice Genomics 1998 47: 180–186
Mastroeni P, Harrison JA, Hormaeche CE . Natural resistance and acquired immunity to Salmonella Fundam Clin Immunol 1994 2: 83–95
Richter-Dahlfors A, Buchan AM, Finlay BB . Murine salmonellosis studied by confocal microscopy: Salmonella typhimurium resides intracellularly inside macrophages and exerts a cytotoxic effect on phagocytes in vivo J Exp Med 1997 186: 569–580
Salcedo SP, Noursadeghi M, Cohen J, Holden DW . Intracellular replication of Salmonella typhimurium strains in specific subsets of splenic macrophages in vivo Cell Microbiol 2001 3: 587–597
O'Brien AD, Scher I, Formal SB . Effect of silica on the innate resistance of inbred mice to Salmonella typhimurium infection Infect Immun 1979 25: 513–520
Hormaeche CE, Harrington KA . Natural resistance to Salmonellae in mice: control by genes within the major histocompatibility complex J Infect Dis 1985 152: 1050–1056
Nauciel C . Role of CD4+ T cells and T-independant mechanisms in acquired resistance to Salmonella typhimurium infection J Immunol 1990 145: 1265–1269
O'Brien AD, Metcalf ES . Control of early Salmonella typhimurium growth in innately Salmonella-resistant mice does not require functional T lymphocytes J Immunol 1982 129: 1349–1351
O'Brien AD, Scher I, Campbell GH, MacDermott RP, Formal SB . Susceptibility of CBA/N mice to infection with Salmonella typhimurium: influence of the x-linked gene controlling B lymphocyte function J Immunol 1979 123: 720–724
Plant J, Glynn AA . Genetics of resistance to infection with Salmonella typhimurium in mice J Infect Dis 1976 133: 72–78
Robson HG, Vas SI . Resistance of inbred mice to Salmonella typhimurium J Infect Dis 1972 126: 378–386
Allcock RJN, Martin AM, Price P . The mouse as a model for the effects of MHC genes on human disease Immunol Today 2000 7: 328–332
Nauciel C, Ronco E, Pla M . Influence of different regions of the H-2 complex on the rate of clearance of Salmonella typhimurium Infect Immun 1990 58: 573–574
Hess J, Ladel C, Miko D, Kaufmann SHE . Salmonella typhimurium aroA− infection in gene-targeted immunodeficient mice J Immunol 1996 156: 3321–3326
Chapes SK, Beharka AA . Salmonella infections in the absence of the major histocompatibility complex II J Leukoc Biol 1998 63: 297–304
Nauciel C, Ronco E, Guenet JL, Pla M . Role of H-2 and non-H-2 genes in control of bacterial clearance from the spleen in Salmonella typhimurium-infected mice Infect Immun 1988 56: 2407–2411
Lo WF, Ong H, Metcalf ES, Soloski MJ . 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: 5398–5406
Dunstan SJ, Stephens HA, Blackwell JM 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: 261–268
Dulphy N, Peyrat MA, Tieng V et al. Common intra-articular T cell expansions in patients with reactive arthritis: identical beta-chain junctional sequences and cytotoxicity toward HLA-B27 J Immunol 1999 162: 3830–3839
Lo WF, Woods AS, DeCloux A, Cotter RJ, Metcalf ES, Soloski MJ . Molecular mimicry mediated by MHC class Ib molecules after infection with gram-negative pathogens Nat Med 2000 6: 215–218
Plant J, Glynn AA . Locating salmonella resistance gene on mouse chromosome 1 Clin Exp Immunol 1979 37: 1–6
Bradley DJ . Letter: genetic control of natural resistance to Leishmania donovani Nature 1974 250: 353–354
Forget A, Skamene E, Gros P, Miailhe AC, Turcotte R . Differences in response among inbred mouse strains to infection with small doses of Mycobacterium bovis BCG Infect Immun 1981 32: 42–47
Plant JE, Blackwell JM, O'Brien AD, Bradley DJ, Glynn AA . Are the Lsh and Ity disease resistance genes at one locus on mouse chromosome 1? Nature 1982 297: 510–511
Skamene E, Gros P, Forget A, Kongshavn PA, St Charles C, Taylor BA . Genetic regulation of resistance to intracellular pathogens Nature 1982 297: 506–509
Vidal SM, Malo D, Vogan K, Skamene E, Gros P . Natural resistance to infection with intracellular parasites: isolation of a candidate for Bcg Cell 1993 73: 469–485
Vidal S, Tremblay ML, Govoni G et al. The Ity/Lsh/Bcg locus: natural resistance to infection with intracellular parasites is abrogated by disruption of the Nramp1 gene J Exp Med 1995 182: 655–666
Lissner CR, Swanson RN, O'Brian AD . 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 1983 131: 3006–3013
Gros P, Skamene E, Forget A . Cellular mechanisms of genetically controlled host resistance to Mycobacterium bovis (BCG) J Immunol 1983 131: 1966–1972
Gros P, Skamene E, Forget A . Genetic control of natural resistance to Mycobacterium bovis (BCG) in mice J Immunol 1981 127: 2417–2421
Gros P, Malo D . A reverse genetics approach to Bcg/Ity/Lsh gene cloning Res Immunol 1989 140: 774–777
Blackwell JM . The macrophage resistance gene Lsh/Ity/Bcg Res Immunol 1989 140: 767–769
Schurr E, Skamene E, Forget A, Gros P . Linkage analysis of the Bcg gene on mouse chromosome 1 J Immunol 1989 142: 4507–4513
Malo D, Vidal S, Lieman JH, Ward DC, Gros P . Physical delineation of the minimal chromosomal segment encompassing the murine host resistance locus Bcg Genomics 1993 17: 667–675
Malo D, Vidal SM, Hu J, Skamene E, Gros P . High-resolution linkage map in the vicinity of the host resistance locus Bcg Genomics 1993 16: 655–663
Forbes JR, Gros P . Divalent-metal transport by NRAMP proteins at the interface of host–pathogen interactions Trends Microbiol 2001 9: 397–403
Malo D, Vogan K, Vidal S et al. Haplotype mapping and sequence analysis of the mouse Nramp gene predict susceptibility to infection with intracellular parasites Genomics 1994 23: 51–61
Vidal SM, Pinner E, Lepage P, Gauthier S, Gros P . Natural resistance to intracellular infections: Nramp1 encodes a membrane phosphoglycoprotein absent in macrophages from susceptible (Nramp1 D169) mouse strains J Immunol 1996 157: 3559–3568
Govoni G, Vidal S, Gauthier S, Skamene E, Malo D, Gros P . The Bcg/Ity/Lsh locus: genetic transfer of resistance to infections in C57BL/6J mice transgenic for the Nramp1 Gly169 allele Infect Immun 1996 64: 2923–2929
Brumell JH, Perrin AJ, Goosney DL, Finlay BB . Microbial pathogenesis: new niches for salmonella Curr Biol 2002 12: R15-R17
Gruenheid S, Pinner E, Desjardins M, Gros P . Natural resistance to infection with intracellular pathogens: the Nramp1 protein is recruited to the membrane of the phagosome J Exp Med 1997 185: 717–730
Cuellar-Mata P, Jabado N, Liu J et al. Nramp1 modifies the fusion of Salmonella typhimurium containing vacuoles with cellular endomembranes in macrophages J Biol Chem 2002 277: 2258–2265
Jabado N, Jankowski A, Dougaparsad S, Picard V, Grinstein S, Gros P . Natural resistance to intracellular infections: natural resistance-associated macrophage protein 1 (Nramp1) functions as a pH-dependent manganese transporter at the phagosomal membrane J Exp Med 2000 192: 1237–1247
Cellier MF, Bergevin I, Boyer E, Richer E . Polyphyletic origins of bacterial Nramp transporters Trends Genet 2001 17: 365–370
Alcais A, Sanchez FO, Thuc NV et al. Granulomatous reaction to intradermal injection of lepromin (Mitsuda reaction) is linked to the human NRAMP1 gene in Vietnamese leprosy sibships J Infect Dis 2000 181: 302–308
Bellamy R, Ruwende C, Corrah T, McAdam KP, Whittle HC, Hill AV . Variations in the NRAMP1 gene and susceptibility to tuberculosis in West Africans N Engl J Med 1998 338: 640–644
Abel L, Sanchez FO, Oberti J et al. Susceptibility to leprosy is linked to the human NRAMP1 gene J Infect Dis 1998 177: 133–145
Dunstan SJ, Ho VA, Duc CM et al. Typhoid fever and genetic polymorphisms at the natural resistance-associated macrophage protein 1 J Infect Dis 2001 183: 1156–1160
Hu J, Bumstead N, Barrow P et al. Resistance to salmonellosis in the chicken is linked to NRAMP1 and TNC Genome Res 1997 7: 693–704
Bumstead N, Barrow PA . Genetics of resistance to Salmonella typhimurium in newly hatched chicks Br Poult Sci 1988 29: 521–529
Rietschel ET, Kirikae T, Schade FU et al. Bacterial endotoxin: molecular relationships of structure to activity and function FASEB J 1994 8: 217–225
Medzhitov R . Toll-like receptors and innate immunity Nat Rev Immunol 2001 1: 135–145
Sultzer BM . Genetic control of leucocyte responses to endotoxin Nature 1968 219: 1253–1254
Sultzer BM . Genetic factors in leucocyte responses to endotoxin: further studies in mice J Immunol 1969 103: 32–38
O'Brien AD, Rosenstreich DL, Scher I, Campbell GH, MacDermott RP, Formal SB . Genetic control of susceptibility to Salmonella typhimurium in mice: role of the LPS gene J Immunol 1980 124: 20–24
McAdam KPWJ, Ryan JL . C57BL/10/CR mice: nonresponders to activation by the lipid A moiety of a bacterial lipopolysaccharide J Immunol 1978 120: 249–253
Vogel SN, Hansen CT, Rosenstreich DL . Characterization of a congenitally LPS-resistant athymic mouse strain J Immunol 1979 122: 619–622
Bihl F, Lariviere L, Qureshi ST, Flaherty L, Malo D . LPS-hyporesponsiveness of mnd mice is associated with a mutation in Toll-like receptor 4 Genes Immun 2001 2: 56–59
Coutinho A, Tommaso M . Genetic basis for unresponsiveness to lipopolysaccharide in C57BL/10Cr mice Immunogenetics 1978 7: 17–24
Watson J, Riblet R . Genetic control of responses to bacterial lipopolysaccharides in mice. I. Evidence for a single gene that influences mitogenic and immunogenic respones to lipopolysaccharides J Exp Med 1974 140: 1147–1161
Watson J, Riblet R, Taylor BA . The response of recombinant inbred strains of mice to bacterial lipopolysaccharides J Immunol 1977 118: 2088–2093
Watson J, Kelly K, Largen M, Taylor BA . The genetic mapping of a defective LPS response gene in C3H/HeJ mice J Immunol 1978 120: 422–424
Qureshi ST, Lariviere L, Sebastiani G et al. A high-resolution map in the chromosomal region surrounding the Lps locus Genomics 1996 31: 283–294
Poltorak A, Smirnova I, He X et al. Genetic and physical mapping of the Lps locus: identification of the toll-4 receptor as a candidate gene in the critical region Blood Cells Mol Dis 1998 24: 340–355
Qureshi ST, Lariviere L, Leveque G et al. Endotoxin-tolerant mice have mutations in Toll-like receptor 4 (Tlr4) J Exp Med 1999 189: 615–625
Poltorak A, He X, Smirnova I et al. Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene Science 1998 282: 2085–2088
Poltorak A, Smirnova I, Clisch R, Beutler B . Limits of a deletion spanning Tlr4 in C57BL/10ScCr mice J Endotoxin Res 2000 6: 51–56
Hoshino K, Takeuchi O, Kawai T et al. Cutting edge: Toll-like receptor 4 (TLR4)-deficient mice are hyporesponsive to lipopolysaccharide: evidence for TLR4 as the Lps gene product J Immunol 1999 162: 3749–3752
Aderem A, Ulevitch RJ . Toll-like receptors in the induction of the innate immune response Nature 2000 406: 782–787
Hoffmann JA, Reichhart JM . Drosophila innate immunity: an evolutionary perspective Nat Immunol 2002 3: 121–126
da Silva Correia J, Ulevitch RJ . MD-2 and TLR4 N-linked glycosylations are important for a functional lipopolysaccharide receptor J Biol Chem 2002 277: 1845–1854
Lien E, Means TK, Heine H et al. Toll-like receptor 4 imparts ligand-specific recognition of bacterial lipopolysaccharide J Clin Invest 2000 105: 497–504
Poltorak A, Ricciardi-Castagnoli P, Citterio S, Beutler B . Physical contact between lipopolysaccharide and toll-like receptor 4 revealed by genetic complementation Proc Natl Acad Sci USA 2000 97: 2163–2167
Horng T, Barton GM, Medzhitov R . TIRAP: an adapter molecule in the Toll signaling pathway Nat Immunol 2001 2: 835–841
Fitzgerald KA, Palsson-McDermott EM, Bowie AG et al. Mal (MyD88-adapter-like) is required for Toll-like receptor-4 signal transduction Nature 2001 413: 78–83
Takeuchi O, Hoshino K, Kawai T et al. Differential roles of TLR2 and TLR4 in recognition of gram-negative and gram-positive bacterial cell wall components Immunity 1999 11: 443–451
Medzhitov R, Preston-Hurlburt P, Janeway Jr CA . A human homologue of the Drosophila Toll protein signals activation of adaptive immunity Nature 1997 388: 394–397
Schnare M, Barton GM, Holt AC, Takeda K, Akira S, Medzhitov R . Toll-like receptors control activation of adaptive immune responses Nat Immunol 2001 2: 947–950
Scher I . The CBA/N mouse strain: an experimental model illustrating the influence of the X-chromosome on immunity Adv Immunol 1982 33: 1–71
Nahm MH, Paslay JW, Davie JM . Unbalanced X chromosome mosaicism in B cells of mice with X-linked immunodeficiency J Exp Med 1983 158: 920–931
O’Brien AD, Scher I, Metcalf ES . Genetically conferred defect in anti-Salmonella antibody formation renders CBA/N mice innately susceptible to Salmonella typhimurium infection J Immunol 1981 126: 1368–1372
Thomas JD, Sideras P, Smith CI, Vorechovsky I, Chapman V, Paul WE . Colocalization of X-linked agammaglobulinemia and X-linked immunodeficiency genes Science 1993 261: 355–358
Ochs HD, Smith CI . X-linked agammaglobulinemia. A clinical and molecular analysis Medicine (Baltimore) 1996 75: 287–299
Vetrie D, Vorechovsky I, Sideras P et al. The gene invoved in X-linked agammaglobulinaemia is a member of the src family of protein-tyrosine kinases Nature 1993 361: 226–232
Tsukada S, Saffran DC, Rawlings DJ et al. Deficient expression of a B cell cytoplasmic tyrosine kinase in human X-linked agammaglobulinemia Cell 1993 72: 279–290
Rawlings DJ, Saffran DC, Tsukada S et al. Mutation of unique region of Bruton's tyrosine kinase in immunodeficient XID mice Science 1993 261: 358–361
Rawlings DJ . Bruton's tyrosine kinase control a sustained calcium signal essential for B lineage development and function Clin Immunol 1999 91: 243–253
Chan VW, Mecklenbrauker I, Su I et al. The molecular mechanism of B cell activation by toll-like receptor protein RP-105 J Exp Med 1998 188: 93–101
Yang WC, Collette Y, Nunes JA, Olive D . Tec kinases: a family with multiple roles in immunity Immunity 2000 12: 373–382
Guo B, Kato RM, Garcia-Lloret M, Wahl MI, Rawlings DJ . Engagement of the human pre-B cell receptor generates a lipid raft-dependent calcium signaling complex Immunity 2000 13: 243–253
Fruman DA, Satterthwaite AB, Witte ON . Xid-like phenotypes: a B cell signalosome takes shape Immunity 2000 13: 1–3
Kang SW, Wahl MI, Chu J et al. PKCbeta modulates antigen receptor signaling via regulation of Btk membrane localization EMBO J 2001 20: 5692–5702
Baraldi E, Carugo KD, Hyvonen M et al. Structure of the PH domain from Bruton's tyrosine kinase in complex with inositol 1,3,4,5-tetrakisphosphate Struc Fold Des 1999 7: 449–460
Petro JB, Rahman SM, Ballard DW, Khan WN . Bruton's tyrosine kinase is required for activation of IkappaB kinase and nuclear factor kappaB in response to B cell receptor engagement J Exp Med 2000 191: 1745–1754
Bajpai UD, Zhang K, Teutsch M, Sen R, Wortis HH . Bruton's tyrosine kinase links the B cell receptor to nuclear factor kappaB activation J Exp Med 2000 191: 1735–1744
Fenton MJ, Golenbock DT . LPS-binding proteins and receptors J Leukoc Biol 1998 64: 25–32
Jack RS, Fan X, Bernheiden M et al. Lipopolysaccharide-binding protein is required to combat a murine gram-negative bacterial infection Nature 1997 389: 742–745
Heinrich JM, Bernheiden M, Minigo G et al. The essential role of lipopolysaccharide-binding protein in protection of mice against a peritoneal Salmonella infection involves the rapid induction of an inflammatory response J Immunol 2001 167: 1624–1628
Haziot A, Ferrero E, Kontgen F et al. Resistance to endotoxin shock and reduced dissemination of gram-negative bacteria in CD14-deficient mice Immunity 1996 4: 407–414
Bernheiden M, Heinrich JM, Minigo G et al. LBP, CD14, TLR4 and the murine innate immune response to a peritoneal Salmonella infection J Endotoxin Res 2001 7: 447–450
Haziot A, Hijiya N, Gangloff SC, Silver J, Goyert SM . Induction of a novel mechanism of accelerated bacterial clearance by lipopolysaccharide in CD14-deficient and Toll-like receptor 4-deficient mice J Immunol 2001 166: 1075–1078
Vazquez-Torres A, Fang FC . Oxygen-dependent anti-Salmonella activity of macrophages Trends Microbiol 2001 9: 29–33
Nathan C, Shiloh MU . Reactive oxygen and nitrogen intermediates in the relationship between mammalian hosts and microbial pathogens Proc Natl Acad Sci USA 2000 97: 8841–8848
Pollock JD, Williams DA, Gifford MA et al. Mouse model of X-linked chronic granulomatous disease, an inherited defect in phagocyte superoxide production Nat Genet 1995 9: 202–209
Mastroeni P, Vazquez-Torres A, Fang FC et al. Antimicrobial actions of the NADPH phagocyte oxidase and inducible nitric oxide synthase in experimental salmonellosis. II. Effects on microbial proliferation and host survival in vivo J Exp Med 2000 192: 237–247
Shiloh MU, MacMicking JD, Nicholson S et al. Phenotype of mice and macrophages deficient in both phagocyte oxidase and inducible nitric oxide synthase Immunity 1999 10: 29–38
MacMicking JD, Nathan C, Hom G et al. Altered responses to bacterial infection and endotoxic shock in mice lacking inducible nitric oxide synthase Cell 1995 81: 641–650
Umezawa K, Akaike T, Fujii S et al. Induction of nitric oxide synthesis and xanthine oxidase and their roles in the antimicrobial mechanism against Salmonella typhimurium infection in mice Infect Immun 1997 65: 2932–2940
Uchiya K, Barbieri MA, Funato K, Shah AH, Stahl PD, Groisman EA . A Salmonella virulence protein that inhibits cellular trafficking EMBO J 1999 18: 3924–3933
Vazquez-Torres A, Xu Y, Jones-Carson J et al. Salmonella pathogenicity island 2-dependent evasion of the phagocyte NADPH oxidase Science 2000 287: 1655–1658
Gallois A, Klein JR, Allen LA, Jones BD, Nauseef WM . Salmonella pathogenicity island 2-encoded type III secretion system mediates exclusion of NADPH oxidase assembly from the phagosomal membrane J Immunol 2001 166: 5741–5748
Chakravortty D, Hansen-Wester I, Hensel M . Salmonella pathogenicity island 2 mediates protection of intracellular salmonella from reactive nitrogen intermediates J Exp Med 2002 195: 1155–1166
Fiers W . Tumor necrosis factor. Characterization at the molecular, cellular and in vivo level FEBS Lett 1991 285: 199–212
Everest P, Roberts M, Dougan G . Susceptibility to Salmonella typhimurium infection and effectiveness of vaccination in mice deficient in the tumor necrosis factor alpha p55 receptor Infect Immun 1998 66: 3355–3364
Vazquez-Torres A, Fantuzzi G, Edwards 3rd CK, Dinarello CA, Fang FC . Defective localization of the NADPH phagocyte oxidase to Salmonella-containing phagosomes in tumor necrosis factor p55 receptor-deficient macrophages Proc Natl Acad Sci USA 2001 98: 2561–2565
Bao S, Beagley KW, France MP, Shen J, Husband AJ . Interferon-gamma plays a critical role in intestinal immunity against Salmonella typhimurium infection Immunology 2000 99: 464–472
Lengeling A, Pfeffer K, Balling R . The battle of two genomes: genetics of bacterial host/pathogen interactions in mice Mammalian Genome 2001 12: 261–271
Mastroeni P, Harrison JA, Robinson JH et al. Interleukin-12 is required for control of the growth of attenuated aromatic-compound-dependent salmonellae in BALB/c mice: role of gamma interferon and macrophage activation Infect Immun 1998 66: 4767–4776
Lehmann J, Bellmann S, Werner C, Schroder R, Schutze N, Alber G . IL-12p40-dependent agonistic effects on the development of protective innate and adaptive immunity against Salmonella enteritidis J Immunol 2001 167: 5304–5315
Picard C, Fieschi C, Altare F et al. Inherited interleukin-12 deficiency: IL12B genotype and clinical phenotype of 13 patients from six kindreds Am J Hum Genet 2002 70: 336–348
de Jong R, Altare F, Haagen IA et al. Severe mycobacterial and Salmonella infections in interleukin-12 receptor-deficient patients Science 1998 280: 1435–1438
Altare F, Durandy A, Lammas D et al. Impairment of mycobacterial immunity in human interleukin-12 receptor deficiency Science 1998 280: 1432–1435
Altare F, Lammas D, Revy P et al. Inherited interleukin 12 deficiency in a child with bacille Calmette–Guerin and Salmonella enteritidis disseminated infection J Clin Invest 1998 102: 2035–2040
Jouanguy E, Lamhamedi-Cherradi S, Altare F et al. Partial interferon-gamma receptor 1 deficiency in a child with tuberculoid bacillus Calmette–Guerin infection and a sibling with clinical tuberculosis J Clin Invest 1997 100: 2658–2664
Newport MJ, Huxley CM, Huston S et al. A mutation in the interferon-gamma-receptor gene and susceptibility to mycobacterial infection N Engl J Med 1996 335: 1941–1949
Jouanguy E, Lamhamedi-Cherradi S, Lammas D et al. A human IFNGR1 small deletion hotspot associated with dominant susceptibility to mycobacterial infection Nat Genet 1999 21: 370–378
Sebastiani G, Leveque G, Lariviere L et al. Cloning and characterization of the murine toll-like receptor 5 (Tlr5) gene: sequence and mRNA expression studies in Salmonella-susceptible MOLF/Ei mice Genomics 2000 64: 230–240
Sebastiani G, Blais V, Sancho V et al. Host immune response to Salmonella enterica serovar Typhimurium infection in mice derived from wild strains Infect Immun 2002 70: 1997–2009
Nathan C . Perspectives series: nitric oxide and nitric oxide synthases. Inducible nitric oxide synthase: what difference does it make? J Clin Invest 1997 100: 2417–2423
Gewirtz AT, Navas TA, Lyons S, Godowski PJ, Madara JL . Cutting edge: bacterial flagellin activates basolaterally expressed TLR5 to induce epithelial proinflammatory gene expression J Immunol 2001 167: 1882–1885
Hayashi F, Smith KD, Ozinsky A et al. The innate immune response to bacterial flagellin is mediated by Toll-like receptor 5 Nature 2001 410: 1099–1103
Wojciechowski W, DeSanctis J, Skamene E, Radzioch D . Attenuation of MHC class II expression in macrophages infected with Mycobacterium bovis bacillus Calmette–Guerin involves class II transactivator and depends on the Nramp1 gene J Immunol 1999 163: 2688–2696
Blackwell JM, Black GF, Sharples C, Soo SS, Peacock CS, Miller N . Roles of Nramp1, HLA, and a gene(s) in allelic association with IL-4, in determining T helper subset differentiation Microbes Infect 1999 1: 95–102
Fortin A, Cardon LR, Tam M, Skamene E, Stevenson MM, Gros P . Identification of a new malaria susceptibility locus (Char4) in recombinant congenic strains of mice Proc Natl Acad Sci USA 2001 98: 10 793–10 798
Fortin A, Belouchi A, Tam MF et al. Genetic control of blood parasitaemia in mouse malaria maps to chromosome 8 Nat Genet 1997 17: 382–383
Foote SJ, Burt RA, Baldwin TM et al. Mouse loci for malaria-induced mortality and the control of parasitaemia Nat Genet 1997 17: 380–381
Roberts LJ, Baldwin TM, Speed TP, Handman E, Foote SJ . Chromosomes X, 9, and the H2 locus interact epistatically to control Leishmania major infection Eur J Immunol 1999 29: 3047–3050
Lavebratt C, Apt AS, Nikonenko BV, Schalling M, Schurr E . Severity of tuberculosis in mice is linked to distal chromosome 3 and proximal chromosome 9 J Infect Dis 1999 180: 150–155
Kramnik I, Dietrich WF, Demant P, Bloom BR . Genetic control of resistance to experimental infection with virulent Mycobacterium tuberculosis Proc Natl Acad Sci USA 2000 97: 8560–8565
Boyartchuk VL, Broman KW, Mosher RE, D’Orazio SE, Starnbach MN, Dietrich WF . Multigenic control of Listeria monocytogenes susceptibility in mice Nat Genet 2001 27: 259–260
Mitsos LM, Cardon LR, Fortin A et al. Genetic control of susceptibility to infection with Mycobacterium tuberculosis in mice Genes Immun 2000 1: 467–477
Acknowledgements
We thank Ellen Bushman and Silvia Vidal for a critical reading of the manuscript. Danielle Malo is an investigator of the Canadian Institutes for Health Research and an International Research Scholar of the Howard Hughes Medical Institute.
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Roy, MF., Malo, D. Genetic regulation of host responses to Salmonella infection in mice. Genes Immun 3, 381–393 (2002). https://doi.org/10.1038/sj.gene.6363924
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DOI: https://doi.org/10.1038/sj.gene.6363924
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