All Stressed Out. Salmonella Pathogenesis and Reactive Nitrogen Species

Advances in Microbial Physiology

Volumn 56, Issue , 2009, Pages 1-28

  Prior, K ^a   Hautefort, I ^b   Hinton, J C D ^c   Richardson, D J ^a   Rowley, G ^a  

^a UNIVERSITY OF EAST ANGLIA   (United Kingdom)

^b INSTITUTE OF FOOD RESEARCH   (United Kingdom)

^c TRINITY COLLEGE DUBLIN   (Ireland)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOCHROME C NITRITE REDUCTASE; FLAVOHEMOGLOBIN; FLAVORUBREDOXIN; HEMPA; NITRATE REDUCTASE; NITRATE REDUCTASE NAP; NITRATE REDUCTASE NR Z; NITRIC OXIDE; NITRIC OXIDE REDUCTASE; NITRITE REDUCTASE; REACTIVE NITROGEN SPECIES; UNCLASSIFIED DRUG; VIRULENCE FACTOR;

ANTIBIOTIC RESISTANCE; BOOK; DETOXIFICATION; DISEASE COURSE; GASTROENTERITIS; HOST; HOST RESISTANCE; HUMAN; INNATE IMMUNITY; MACROPHAGE; NITROGEN METABOLISM; NONHUMAN; PATHOGENESIS; SALMONELLA; STOMACH ACID; STOMACH PH; TYPHOID FEVER; ANIMAL; ENZYMOLOGY; HUMORAL IMMUNITY; IMMUNOLOGY; METABOLISM; PATHOGENICITY; SALMONELLA ENTERICA SUBSP. ENTERICA SEROVAR TYPHIMURIUM; SALMONELLOSIS;

ANIMALIA; BACTERIA (MICROORGANISMS); MAMMALIA; SALMONELLA;

ANIMALS; HUMANS; IMMUNITY, HUMORAL; NITRIC OXIDE; NITRITE REDUCTASES; REACTIVE NITROGEN SPECIES; SALMONELLA INFECTIONS; SALMONELLA TYPHIMURIUM;

EID: 77957104811     PISSN: 00652911     EISSN: None     Source Type: Book Series    
DOI: 10.1016/S0065-2911(09)05601-X     Document Type: Chapter

References (119)

1. Abergel C., Monchois V., Byrne D., Chenivesse S., Lembo F., Lazzaroni J.C., Claverie J.M. Structure and evolution of the Ivy protein family, unexpected lysozyme inhibitors in Gram-negative bacteria. Proc. Natl. Acad. Sci. USA 2007, 104:6394-6399.
2. Adak G.K., Meakins S.M., Yip H., Lopman B.A., O'Brien S.J. Disease risks from foods, England and Wales, 1996-2000. Emerg. Infect. Dis. 2005, 11:365-372.
3. Ansaldi M., Theraulaz L., Baraquet C., Panis G., Mejean V. Aerobic TMAO respiration in Escherichia coli. Mol. Microbiol. 2007, 66:484-494.
4. Backhed F., Ley R.E., Sonnenburg J.L., Peterson D.A., Gordon J.I. Host-bacterial mutualism in the human intestine. Science 2005, 307:1915-1920.
5. Bamford V.A., Angove H.C., Seward H.E., Thomson A.J., Cole J.A., Butt J.N., Hemmings A.M., Richardson D.J. Structure and spectroscopy of the periplasmic cytochrome c nitrite reductase from Escherichia coli. Biochemistry 2002, 41:2921-2931.
6. Bang I.S., Liu L., Vazquez-Torres A., Crouch M.L., Stamler J.S., Fang F.C. Maintenance of nitric oxide and redox homeostasis by the Salmonella flavohemoglobin hmp. J. Biol. Chem. 2006, 281:28039-28047.
7. Benjamin N., O'Driscoll F., Dougall H., Duncan C., Smith L., Golden M., McKenzie H. Stomach NO synthesis. Nature 1994, 368:502.
8. Berg D.T., Gupta A., Richardson M.A., O'Brien L.A., Calnek D., Grinnell B.W. Negative regulation of inducible nitric-oxide synthase expression mediated through transforming growth factor Β-dependent modulation of transcription factor TCF11. J. Biol. Chem. 2007, 282:36837-36844.
9. Bertero M.G., Rothery R.A., Boroumand N., Palak M., Blasco F., Ginet N., Weiner J.H., Strynadka N.C. Structural and biochemical characterization of a quinol binding site of Escherichia coli nitrate reductase A. J. Biol. Chem. 2005, 280:14836-14843.
10. Blasco F., Iobbi C., Ratouchniak J., Bonnefoy V., Chippaux M. Nitrate reductases of Escherichia coli: sequence of the second nitrate reductase and comparison with that encoded by the narGHJI operon. Mol. Gen. Genet. 1990, 222:104-111.
11. Bodenmiller D.M., Spiro S. The yjeB (nsrR) gene of Escherichia coli encodes a nitric oxide-sensitive transcriptional regulator. J. Bacteriol. 2006, 188:874-881.
12. Bonnefoy V., Demoss J.A. Nitrate reductases in Escherichia coli. Antonie Van Leeuwenhoek 1994, 66:47-56.
13. Borisov V.B., Forte E., Konstantinov A.A., Poole R.K., Sarti P., Giuffre A. Interaction of the bacterial terminal oxidase cytochrome bd with nitric oxide. FEBS Lett. 2004, 576:201-204.
14. Bourret T.J., Porwollik S., McClelland M., Zhao R., Greco T., Ischiropoulos H., Vazquez-Torres A. Nitric oxide antagonizes the acid tolerance response that protects Salmonella against innate gastric defenses. PLoS ONE 2008, 3:e1833.
15. Bryan N.S. Nitrite in nitric oxide biology: cause or consequence? A systems-based review. Free Radic. Biol. Med. 2006, 41:691-701.
16. Burlat B., Gwyer J.D., Poock S., Clarke T., Cole J.A., Hemmings A.M., Cheesman M.R., Butt J.N., Richardson D.J. Cytochrome c nitrite reductase: from structural to physicochemical analysis. Biochem. Soc. Trans. 2005, 33:137-140.
17. Busse R., Mulsch A. Induction of nitric oxide synthase by cytokines in vascular smooth muscle cells. FEBS Lett. 1990, 275:87-90.
18. Outbreak of Salmonella serotype Saintpaul infections associated with multiple raw produce items-United States, MMWR Morb. Mortal Wkly. Rep 2008, 57(34):929-934. Centers for Disease Control and Prevention (CDC).
19. 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.
20. Chakravortty D., Hensel M. Inducible nitric oxide synthase and control of intracellular bacterial pathogens. Microbes Infect. 2003, 5:621-627.
21. Chang L., Wei L.I., Audia J.P., Morton R.A., Schellhorn H.E. Expression of the Escherichia coli NRZ nitrate reductase is highly growth phase dependent and is controlled by RpoS, the alternative vegetative sigma factor. Mol. Microbiol. 1999, 34:756-766.
22. Chen L.M., Hobbie S., Galan J.E. Requirement of CDC42 for Salmonella-induced cytoskeletal and nuclear responses. Science 1996, 274:2115-2118.
23. Clarke T.A., Kemp G.L., Wonderen J.H., Doyle R.M., Cole J.A., Tovell N., Cheesman M.R., Butt J.N., Richardson D.J., Hemmings A.M. Role of a conserved glutamine residue in tuning the catalytic activity of Escherichia coli cytochrome c nitrite reductase. Biochemistry 2008, 47:3789-3799.
24. Clegg S.J., Jia W., Cole J.A. Role of the Escherichia coli nitrate transport protein, NarU, in survival during severe nutrient starvation and slow growth. Microbiology 2006, 152:2091-2100.
25. Constantinidou C., Hobman J.L., Griffiths L., Patel M.D., Penn C.W., Cole J.A., Overton T.W. A reassessment of the FNR regulon and transcriptomic analysis of the effects of nitrate, nitrite, NarXL, and NarQP as Escherichia coli K12 adapts from aerobic to anaerobic growth. J. Biol. Chem. 2006, 281:4802-4815.
26. Crawford M.J., Goldberg D.E. Regulation of the Salmonella typhimurium flavohemoglobin gene. A new pathway for bacterial gene expression in response to nitric oxide. J. Biol. Chem. 1998, 273:34028-34032.
27. Crump J.A., Luby S.P., Mintz E.D. The global burden of typhoid fever. Bull. World Health Organ. 2004, 82:346-353.
28. Cruz-Garcia C., Murray A.E., Klappenbach J.A., Stewart V., Tiedje J.M. Respiratory nitrate ammonification by Shewanella oneidensis MR-1. J. Bacteriol. 2007, 189:656-662.
29. Darwin K.H., Miller V.L. Molecular basis of the interaction of Salmonella with the intestinal mucosa. Clin. Microbiol. Rev. 1999, 12:405-428.
30. Detweiler C.S., Cunanan D.B., Falkow S. Host microarray analysis reveals a role for the Salmonella response regulator phoP in human macrophage cell death. Proc. Natl. Acad. Sci. USA 2001, 98:5850-5855.
31. Elvers K.T., Turner S.M., Wainwright L.M., Marsden G., Hinds J., Cole J.A., Poole R.K., Penn C.W., Park S.F. NssR, a member of the Crp-Fnr superfamily from Campylobacter jejuni, regulates a nitrosative stress-responsive regulon that includes both a single-domain and a truncated haemoglobin. Mol. Microbiol. 2005, 57:735-750.
32. Eriksson S., Lucchini S., Thompson A., Rhen M., Hinton J.C. Unravelling the biology of macrophage infection by gene expression profiling of intracellular Salmonella enterica. Mol. Microbiol. 2003, 47:103-118.
33. Everest P., Wain J., Roberts M., Rook G., Dougan G. The molecular mechanisms of severe typhoid fever. Trends Microbiol. 2001, 9:316-320.
34. Fang F.C. Perspectives series: host/pathogen interactions. Mechanisms of nitric oxide-related antimicrobial activity. J. Clin. Invest. 1997, 99:2818-2825.
35. Fang F.C. Antimicrobial reactive oxygen and nitrogen species: concepts and controversies. Nat. Rev. Microbiol. 2004, 2:820-832.
36. Faucher S.P., Porwollik S., Dozois C.M., McClelland M., Daigle F. Transcriptome of Salmonella enterica serovar Typhi within macrophages revealed through the selective capture of transcribed sequences. Proc. Natl. Acad. Sci. USA 2006, 103:1906-1911.
37. Fedtke I., Kamps A., Krismer B., Gotz F. The nitrate reductase and nitrite reductase operons and the narT gene of Staphylococcus carnosus are positively controlled by the novel two-component system NreBC. J. Bacteriol. 2002, 184:6624-6634.
38. Fink S.L., Cookson B.T. Pyroptosis and host cell death responses during Salmonella infection. Cell Microbiol. 2007, 9:2562-2570.
39. Foster J.W. Salmonella acid shock proteins are required for the adaptive acid tolerance response. J. Bacteriol. 1991, 173:6896-6902.
40. Foster J.W. Escherichia coli acid resistance: tales of an amateur acidophile. Nat. Rev. Microbiol. 2004, 2:898-907.
41. Gardner P.R. Nitric oxide dioxygenase function and mechanism of flavohemoglobin, hemoglobin, myoglobin and their associated reductases. J. Inorg. Biochem. 2005, 99:247-266.
42. Gardner A.M., Gardner P.R. Flavohemoglobin detoxifies nitric oxide in aerobic, but not anaerobic, Escherichia coli. Evidence for a novel inducible anaerobic nitric oxide-scavenging activity. J. Biol. Chem. 2002, 277:8166-8171.
43. Gardner P.R., Gardner A.M., Martin L.A., Salzman A.L. Nitric oxide dioxygenase: an enzymic function for flavohemoglobin. Proc. Natl. Acad. Sci. USA 1998, 95:10378-10383.
44. Gardner A.M., Helmick R.A., Gardner P.R. Flavorubredoxin, an inducible catalyst for nitric oxide reduction and detoxification in Escherichia coli. J. Biol. Chem. 2002, 277:8172-8177.
45. Geddes K., Cruz F., Heffron F. Analysis of cells targeted by Salmonella type III secretion in vivo. PLoS Pathog. 2007, 3:e196.
46. Gilberthorpe N.J., Lee M.E., Stevanin T.M., Read R.C., Poole R.K. NsrR: a key regulator circumventing Salmonella enterica serovar Typhimurium oxidative and nitrosative stress in vitro and in IFN-gamma-stimulated J774.2 macrophages. Microbiology 2007, 153:1756-1771.
47. Gilberthorpe N.J., Poole R.K. Nitric oxide homeostasis in Salmonella typhimurium: roles of respiratory nitrate reductase and flavohemoglobin. J. Biol. Chem. 2008.
48. Gobert A.P., McGee D.J., Akhtar M., Mendz G.L., Newton J.C., Cheng Y., Mobley H.L., Wilson K.T. Helicobacter pylori arginase inhibits nitric oxide production by eukaryotic cells: a strategy for bacterial survival. Proc. Natl. Acad. Sci. USA 2001, 98:13844-13849.
49. Gomes C.M., Giuffre A., Forte E., Vicente J.B., Saraiva L.M., Brunori M., Teixeira M. A novel type of nitric-oxide reductase. Escherichia coli flavorubredoxin. J. Biol. Chem. 2002, 277:25273-25276.
50. Gow A.J., Stamler J.S. Reactions between nitric oxide and haemoglobin under physiological conditions. Nature 1998, 391:169-173.
51. Green S.J., Nacy C.A., Meltzer M.S. Cytokine-induced synthesis of nitrogen oxides in macrophages: a protective host response to Leishmania and other intracellular pathogens. J. Leukoc. Biol. 1991, 50:93-103.
52. Greenacre E.J., Lucchini S., Hinton J.C., Brocklehurst T.F. The lactic acid-induced acid tolerance response in Salmonella enterica serovar Typhimurium induces sensitivity to hydrogen peroxide. Appl. Environ. Microbiol. 2006, 72:5623-5625.
53. Griffith O.W., Stuehr D.J. Nitric oxide synthases: properties and catalytic mechanism. Ann. Rev. Physiol. 1995, 57:707-736.
54. Haque A., Bowe F., Fitzhenry R.J., Frankel G., Thomson M., Heuschkel R., Murch S., Stevens M.P., Wallis T.S., Phillips A.D., Dougan G. Early interactions of Salmonella enterica serovar Typhimurium with human small intestinal epithelial explants. Gut 2004, 53:1424-1430.
55. Haraga A., Ohlson M.B., Miller S.I. Salmonellae interplay with host cells. Nat. Rev. Microbiol. 2008, 6:53-66.
56. Hardt W.D., Chen L.M., Schuebel K.E., Bustelo X.R., Galan J.E. S. typhimurium encodes an activator of Rho GTPases that induces membrane ruffling and nuclear responses in host cells. Cell 1998, 93:815-826.
57. Hausladen A., Gow A.J., Stamler J.S. Nitrosative stress: metabolic pathway involving the flavohemoglobin. Proc. Natl. Acad. Sci. USA 1998, 95:14100-14105.
58. Hautefort I., Thompson A., Eriksson-Ygberg S., Parker M.L., Lucchini S., Danino V., Bongaerts R.J., Ahmad N., Rhen M., Hinton J.C. During infection of epithelial cells Salmonella enterica serovar Typhimurium undergoes a time-dependent transcriptional adaptation that results in simultaneous expression of three type 3 secretion systems. Cell Microbiol. 2007.
59. Health Protection Agency (HPA). (2008) Health Protection Agency. In: Health Protection Agency; Infectious Diseases, Epidemiology and Surveillance, Salmonella, Disease Statistics. http://www.hpa.nhs.uk/web/HPAweb&HPAwebStandard/HPAweb_C/1195733760280.
60. Hernandez L.D., Pypaert M., Flavell R.A., Galan J.E. A Salmonella protein causes macrophage cell death by inducing autophagy. J. Cell Biol. 2003, 163:1123-1131.
61. Hutchings M.I., Mandhana N., Spiro S. The NorR protein of Escherichia coli activates expression of the flavorubredoxin gene norV in response to reactive nitrogen species. J. Bacteriol. 2002, 184:4640-4643.
62. Jepson M.A., Clark M.A. The role of M cells in Salmonella infection. Microbes Infect. 2001, 3:1183-1190.
63. Jepson B.J., Mohan S., Clarke T.A., Gates A.J., Cole J.A., Butler C.S., Butt J.N., Hemmings A.M., Richardson D.J. Spectropotentiometric and structural analysis of the periplasmic nitrate reductase from Escherichia coli. J. Biol. Chem. 2007, 282:6425-6437.
64. Jones S.A., Chowdhury F.Z., Fabich A.J., Anderson A., Schreiner D.M., House A.L., Autieri S.M., Leatham M.P., Lins J.J., Jorgensen M., Cohen P.S., Conway T. Respiration of Escherichia coli in the mouse intestine. Infect. Immun. 2007, 75:4891-4899.
65. Jormakka M., Richardson D., Byrne B., Iwata S. Architecture of NarGH reveals a structural classification of Mo-bisMGD enzymes. Structure 2004, 12:95-104.
66. Kindt T.J., Goldsby R.A., Osborne B.A. Kuby Immunology 2007, W.H. Freeman and Company, New York.
67. Levy M.N., Koeppen B.M., Stanton B.A. Berne and Levy, Principles of Physiology 2005, Elsevier Mosby.
68. Lundberg J.O., Weitzberg E., Cole J.A., Benjamin N. Nitrate, bacteria and human health. Nat. Rev. Microbiol. 2004, 2:593-602.
69. Lupp C., Robertson M.L., Wickham M.E., Sekirov I., Champion O.L., Gaynor E.C., Finlay B.B. Host-mediated inflammation disrupts the intestinal microbiota and promotes the overgrowth of Enterobacteriaceae. Cell Host Microbe 2007, 2:119-129.
70. Maggini S., Wintergerst E.S., Beveridge S., Hornig D.H. Selected vitamins and trace elements support immune function by strengthening epithelial barriers and cellular and humoral immune responses. Br. J. Nutr. 2007, 98(Suppl 1):S29-S35.
71. Marletta M.A. Nitric oxide synthase: aspects concerning structure and catalysis. Cell 1994, 78:927-930.
72. Maskell D.J. Salmonella Infections; Clinical, Immunological and Molecular Aspects 2005, Cambridge University Press, Cambridge.
73. Mastroeni P., Vazquez-Torres A., Fang F.C., Xu Y., Khan S., Hormaeche C.E., Dougan G. 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, 192:237-248.
74. McGhie E.J., Brawn L.C., Hume P.J., Humphreys D., Koronakis V. Salmonella takes control: effector-driven manipulation of the host. Curr. Opin. Microbiol. 2009, 12:117-124.
75. Michel T., Feron O. Nitric oxide synthases: which, where, how, and why?. J. Clin. Invest. 1997, 100:2146-2152.
76. Mills P.C., Rowley G., Spiro S., Hinton J.C., Richardson D.J. A combination of cytochrome c nitrite reductase (NrfA) and flavorubredoxin (NorV) protects Salmonella enterica serovar Typhimurium against killing by NO in anoxic environments. Microbiology 2008, 154:1218-1228.
77. Moncada S., Higgs A., Furchgott R. International Union of Pharmacology Nomenclature in Nitric Oxide Research. Pharmacol Rev. 1997, 49:137-142.
78. Mumy K.L., McCormick B.A. Events at the host-microbial interface of the gastrointestinal tract. II. Role of the intestinal epithelium in pathogen-induced inflammation. Am. J. Physiol. Gastrointest. Liver Physiol. 2005, 288:G854-G859.
79. Murphy C., Carroll C., Jordan K.N. The effect of different media on the survival and induction of stress responses by Campylobacter jejuni. J. Microbiol. Methods 2005, 62:161-166.
80. Nathan C., Xie Q.W. Nitric oxide synthases: roles, tolls, and controls. Cell 1994, 78:915-918.
81. Nelson D.L., Cox M.M. Lehninger, Principles of Biochemistry 2004, W.H.Freeman and Co.
82. Parry C.M., Hien T.T., Dougan G., White N.J., Farrar J.J. Typhoid fever. N. Engl. J. Med. 2002, 347:1770-1782.
83. Philpott D.J., Girardin S.E. The role of Toll-like receptors and Nod proteins in bacterial infection. Mol. Immunol. 2004, 41:1099-1108.
84. Pittman M.S., Elvers K.T., Lee L., Jones M.A., Poole R.K., Park S.F., Kelly D.J. Growth of Campylobacter jejuni on nitrate and nitrite: electron transport to NapA and NrfA via NrfH and distinct roles for NrfA and the globin Cgb in protection against nitrosative stress. Mol. Microbiol. 2007, 63:575-590.
85. Poock S.R., Leach E.R., Moir J.W., Cole J.A., Richardson D.J. Respiratory detoxification of nitric oxide by the cytochrome c nitrite reductase of Escherichia coli. J. Biol. Chem. 2002, 277:23664-23669.
86. Poole R.K., Anjum M.F., Membrillo-Hernandez J., Kim S.O., Hughes M.N., Stewart V. Nitric oxide, nitrite, and Fnr regulation of hmp (flavohemoglobin) gene expression in Escherichia coli K-12. J. Bacteriol. 1996, 178:5487-5492.
87. Poole R.K., D'Mello R., Hill S., Ioannidis N., Leung D., Wu G. The oxygen reactivity of bacterial respiratory haemoproteins: oxidases and globins. Biochim. Biophys. Acta 1994, 1187:226-231.
88. Popoff M.Y., Bockemuhl J., Gheesling L.L. Supplement 2001 (no. 45) to the Kauffmann-White scheme. Res. Microbiol. 2003, 154:173-174.
89. Potter L.C., Millington P., Griffiths L., Thomas G.H., Cole J.A. Competition between Escherichia coli strains expressing either a periplasmic or a membrane-bound nitrate reductase: does Nap confer a selective advantage during nitrate-limited growth?. Biochem. J. 1999, 344(Pt 1):77-84.
90. Pullan S.T., Gidley M.D., Jones R.A., Barrett J., Stevanin T.M., Read R.C., Green J., Poole R.K. Nitric oxide in chemostat-cultured Escherichia coli is sensed by Fnr and other global regulators: unaltered methionine biosynthesis indicates lack of S nitrosation. J. Bacteriol. 2007, 189:1845-1855.
91. Rahman S.H., Ammori B.J., Larvin M., McMahon M.J. Increased nitric oxide excretion in patients with severe acute pancreatitis: evidence of an endotoxin mediated inflammatory response?. Gut 2003, 52:270-274.
92. Raines K.W., Kang T.J., Hibbs S., Cao G.L., Weaver J., Tsai P., Baillie L., Cross A.S., Rosen G.M. Importance of nitric oxide synthase in the control of infection by Bacillus anthracis. Infect. Immun. 2006, 74:2268-2276.
93. Roos D., Winterbourn C.C. Immunology. Lethal weapons. Science 2002, 296:669-671.
94. Rychlik I., Barrow P.A. Salmonella stress management and its relevance to behaviour during intestinal colonisation and infection. FEMS Microbiol. Rev. 2005, 29:1021-1040.
95. Schreiber K., Krieger R., Benkert B., Eschbach M., Arai H., Schobert M., Jahn D. The anaerobic regulatory network required for Pseudomonas aeruginosa nitrate respiration. J. Bacteriol. 2007, 189:4310-4314.
96. Shea J.E., Hensel M., Gleeson C., Holden D.W. Identification of a virulence locus encoding a second type III secretion system in Salmonella typhimurium. Proc. Natl. Acad. Sci. USA 1996, 93:2593-2597.
97. Sohaskey C.D., Wayne L.G. Role of narK2X and narGHJI in hypoxic upregulation of nitrate reduction by Mycobacterium tuberculosis. J. Bacteriol. 2003, 185:7247-7256.
98. Spector M.P., Garcia del Portillo F., Bearson S.M., Mahmud A., Magut M., Finlay B.B., Dougan G., Foster J.W., Pallen M.J. The rpoS-dependent starvation-stress response locus stiA encodes a nitrate reductase (narZYWV) required for carbon-starvation-inducible thermotolerance and acid tolerance in Salmonella typhimurium. Microbiology 1999, 145(Pt 11):3035-3045.
99. Stecher B., Hardt W.D. The role of microbiota in infectious disease. Trends Microbiol. 2008, 16:107-114.
100. Stecher B., Robbiani R., Walker A.W., Westendorf A.M., Barthel M., Kremer M., Chaffron S., Macpherson A.J., Buer J., Parkhill J., Dougan G., von Mering C., Hardt W.D. Salmonella enterica serovar Typhimurium exploits inflammation to compete with the intestinal microbiota. PLoS Biol. 2007, 5:2177-2189.
101. Stevanin T.M., Poole R.K., Demoncheaux E.A., Read R.C. Flavohemoglobin Hmp protects Salmonella enterica serovar Typhimurium from nitric oxide-related killing by human macrophages. Infect. Immun. 2002, 70:4399-4405.
102. Stewart V., Berg B.L. Influence of nar (nitrate reductase) genes on nitrate inhibition of formate-hydrogen lyase and fumarate reductase gene expression in Escherichia coli K-12. J. Bacteriol. 1988, 170:4437-4444.
103. Stewart V., Lu Y., Darwin A.J. Periplasmic nitrate reductase (NapABC enzyme) supports anaerobic respiration by Escherichia coli K-12. J. Bacteriol. 2002, 184:1314-1323.
104. Ten Bruggencate S.J., Bovee-Oudenhoven I.M., Lettink-Wissink M.L., Katan M.B., Van Der Meer R. Dietary fructo-oligosaccharides and inulin decrease resistance of rats to Salmonella: protective role of calcium. Gut 2004, 53:530-535.
105. Tucker N.P., D'Autreaux B., Studholme D.J., Spiro S., Dixon R. DNA binding activity of the Escherichia coli nitric oxide sensor NorR suggests a conserved target sequence in diverse proteobacteria. J. Bacteriol. 2004, 186:6656-6660.
106. Tucker N.P., Hicks M.G., Clarke T.A., Crack J.C., Chandra G., Le Brun N.E., Dixon R., Hutchings M.I. The transcriptional repressor protein NsrR senses nitric oxide directly via a [2Fe-2S] cluster. PLoS ONE 2008, 3:e3623.
107. Tukel C., Raffatellu M., Chessa D., Wilson R.P., Akcelik M., Baumler A.J. Neutrophil influx during non-typhoidal salmonellosis: who is in the driver's seat?. FEMS Immunol. Med. Microbiol. 2006, 46:320-329.
108. Umezawa K., Akaike T., Fujii S., Suga M., Setoguchi K., Ozawa A., Maeda H. 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.
109. United States Department of Agriculture (USDA). (2007) Food Safety and Inspection Service, http://www.fsis.usda.gov/News_&_Events/NR_122007_01/index.asp.
110. Vazquez-Torres A., Jones-Carson J., Mastroeni P., Ischiropoulos H., Fang F.C. Antimicrobial actions of the NADPH phagocyte oxidase and inducible nitric oxide synthase in experimental salmonellosis. I. Effects on microbial killing by activated peritoneal macrophages in vitro. J. Exp. Med. 2000, 192:227-236.
111. Velge P., Cloeckaert A., Barrow P. Emergence of Salmonella epidemics: the problems related to Salmonella enterica serotype Enteritidis and multiple antibiotic resistance in other major serotypes. Vet Res. 2005, 36:267-288.
112. Wallis T.S., Galyov E.E. Molecular basis of Salmonella-induced enteritis. Mol. Microbiol. 2000, 36:997-1005.
113. Wang H., Gunsalus R.P. The nrfA and nirB nitrite reductase operons in Escherichia coli are expressed differently in response to nitrate than to nitrite. J. Bacteriol. 2000, 182:5813-5822.
114. Weller R., Pattullo S., Smith L., Golden M., Ormerod A., Benjamin N. Nitric oxide is generated on the skin surface by reduction of sweat nitrate. J. Invest. Dermatol. 1996, 107:327-331.
115. Wink D.A., Kasprzak K.S., Maragos C.M., Elespuru R.K., Misra M., Dunams T.M., Cebula T.A., Koch W.H., Andrews A.W., Allen J.S., et al. DNA deaminating ability and genotoxicity of nitric oxide and its progenitors. Science 1991, 254:1001-1003.
116. Winterbourn C.C., Hampton M.B., Livesey J.H., Kettle A.J. Modeling the reactions of superoxide and myeloperoxidase in the neutrophil phagosome: implications for microbial killing. J. Biol. Chem. 2006, 281:39860-39869.
117. van Wonderen J.H., Burlat B., Richardson D.J., Cheesman M.R., Butt J.N. The nitric oxide reductase activity of cytochrome c nitrite reductase from Escherichia coli. J. Biol. Chem. 2008, 283:9587-9594.
118. Xu J., Xu X., Verstraete W. The bactericidal effect and chemical reactions of acidified nitrite under conditions simulating the stomach. J. Appl. Microbiol. 2001, 90:523-529.
119. Zhang S., Kingsley R.A., Santos R.L., Andrews-Polymenis H., Raffatellu M., Figueiredo J., Nunes J., Tsolis R.M., Adams L.G., Baumler A.J. Molecular pathogenesis of Salmonella enterica serotype typhimurium-induced diarrhea. Infect. Immun. 2003, 71:1-12.