Nitric oxide antagonizes the acid tolerance response that protects Salmonella against innate gastric defenses

PLoS ONE

Volumn 3, Issue 3, 2008, Pages

  Bourret, Travis J ^a   Porwollik, Steffen ^b   McClelland, Michael ^b   Zhao, Rui ^a   Greco, Todd ^c   Ischiropoulos, Harry ^c   Vázquez Torres, Andrés ^a  

^a UNIVERSITY OF COLORADO   (United States)

^b SIDNEY KIMMEL CANCER CENTER   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; FERRIC UPTAKE REGULATOR; NITRIC OXIDE; NITRIC OXIDE DONOR; PROTEIN PHOPQ; REACTIVE NITROGEN SPECIES; SPERMINE; SPERMINE NONOATE; ACID;

ACID TOLERANCE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBACTERIAL ACTIVITY; ARTICLE; BACTERIAL GROWTH; BACTERIAL IMMUNITY; BACTERIAL SURVIVAL; BACTERIAL VIRULENCE; CONTROLLED STUDY; GENETIC TRANSCRIPTION; HOST RESISTANCE; INNATE IMMUNITY; MOUSE; NONHUMAN; PROTECTION; REGULON; RNA TRANSLATION; SALMONELLA; SALMONELLOSIS; SIGNAL TRANSDUCTION; STOMACH PH; ADAPTATION; ANIMAL; C57BL MOUSE; DNA MICROARRAY; IMMUNOLOGY; MICROBIOLOGY; PATHOGENICITY; PHYSIOLOGY; PLASMID; SALMONELLA ENTERICA; STOMACH; VIRULENCE;

SALMONELLA;

ACIDS; ADAPTATION, PHYSIOLOGICAL; ANIMALS; IMMUNITY, NATURAL; MICE; MICE, INBRED C57BL; NITRIC OXIDE; NITRIC OXIDE DONORS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PLASMIDS; SALMONELLA ENTERICA; STOMACH; VIRULENCE;

EID: 46649109551     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0001833     Document Type: Article

References (71)

1. Giannella RA, Broitman SA, Zamcheck N (1972) Gastric acid barrier to ingested microorganisms in man: studies in vivo and in vitro. Gut 13: 251-256.
2. Cook GC (1985) Infective gastroenteritis and its relationship to reduced gastric acidity. Scand J Gastroenterol Suppl 111: 17-23.
3. Buchin PJ, Andriole VT, Spiro HM (1980) Salmonella infections and hypochlorhydria. J Clin Gastroenterol 2: 133-138.
4. Holt P (1985) Severe salmonella infection in patients with reduced gastric acidity. Practitioner 229: 1027-1030.
5. Stockbruegger RW (1985) Bacterial overgrowth as a consequence of reduced gastric acidity. Scand J Gastroenterol Suppl 111: 7-16.
6. Canani RB, Cirillo P, Roggero P, Romano C, Malamisura B, et al. (2006) Therapy with gastric acidity inhibitors increases the risk of acute gastroenteritis and community-acquired pneumonia in children. Pediatrics 117: e817-820.
7. Cunningham R, Dale B, Undy B, Gaunt N (2003) Proton pump inhibitors as a risk factor for Clostridium difficile diarrhoea. J Hosp Infect 54: 243-245.
8. Puzniak L, Teutsch S, Powderly W, Polish L (2004) Has the epidemiology of nosocomial candidemia changed? Infect Control Hosp Epidemiol 25: 628-633.
9. Reynaert H, Fernandes E, Bourgain C, Smekens L, Devis G (1995) Proton-pump inhibition and gastric giardiasis: a causal or casual association? J Gastroenterol 30: 775-778.
10. Benjamin N, O'Driscoll F, Dougall H, Duncan C, Smith L, et al. (1994) Stomach NO synthesis. Nature 368: 502.
11. Spiegelhalder B, Eisenbrand G, Preussmann R (1976) Influence of dietary nitrate on nitrite content of human saliva: possible relevance to in vivo formation of N-nitroso compounds. Food Cosmet Toxicol 14: 545-548.
12. Tannenbaum SR, Weisman M, Fett D (1976) The effect of nitrate intake on nitrite formation in human saliva. Food Cosmet Toxicol 14: 549-552.
13. Duncan C, Dougall H, Johnston P, Green S, Brogan R, et al. (1995) Chemical generation of nitric oxide in the mouth from the enterosalivary circulation of dietary nitrate. Nat Med 1: 546-551.
14. Dykhuizen RS, Frazer R, Duncan C, Smith CC, Golden M, et al. (1996) Antimicrobial effect of acidified nitrite on gut pathogens: importance of dietary nitrate in host defense. Antimicrob Agents Chemother 40: 1422-1425.
15. Xu J, Xu X, Verstraete W (2001) The bactericidal effect and chemical reactions of acidified nitrite under conditions simulating the stomach. J Appl Microbiol 90: 523-529.
16. Fite A, Dykhuizen R, Litterick A, Golden M, Leifert C (2004) Effects of ascorbic acid, glutathione, thiocyanate, and iodide on antimicrobial activity of acidified nitrite. Antimicrob Agents Chemother 48: 655-658.
17. Small P, Blankenhorn D, Welty D, Zinser E, Slonczewski JL (1994) Acid and base resistance in Escherichia coli and Shigella flexneri: role of rpoS and growth pH. J Bacteriol 176: 1729-1737.
18. Foster JW (2004) Escherichia coli acid resistance: tales of an amateur acidophile. Nat Rev Microbiol 2: 898-907.
19. Dressman JB, Berardi RR, Dermentzoglou LC, Russell TL, Schmaltz SP, et al. (1990) Upper gastrointestinal (GI) pH in young, healthy men and women. Pharm Res 7: 756-761.
20. Foster JW, Hall HK (1990) Adaptive acidification tolerance response of Salmonella typhimurium. J Bacteriol 172: 771-778.
21. Foster JW (1993) The acid tolerance response of Salmonella typhimurium involves transient synthesis of key acid shock proteins. J Bacteriol 175: 1981-1987.
22. Lee IS, Lin J, Hall HK, Bearson B, Foster JW (1995) The stationary-phase sigma factor sigma S (RpoS) is required for a sustained acid tolerance response in virulent Salmonella typhimurium. Mol Microbiol 17: 155-167.
23. Hall HK, Foster JW (1996) The role of fur in the acid tolerance response of Salmonella typhimurium is physiologically and genetically separable from its role in iron acquisition. J Bacteriol 178: 5683-5691.
24. Bearson BL, Wilson L, Foster JW (1998) A low pH-inducible, PhoPQ-dependent acid tolerance response protects Salmonella typhimurium against inorganic acid stress. J Bacteriol 180: 2409-2417.
25. Bang IS, Kim BH, Foster JW, Park YK (2000) OmpR regulates the stationary-phase acid tolerance response of Salmonella enterica serovar Typhimurium. J Bacteriol 182: 2245-2252.
26. Datsenko KA, Wanner BL (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci U S A 97: 6640-6645.
27. Ellermeier CD, Janakiraman A, Slauch JM (2002) Construction of targeted single copy lac fusions using λ Red and FLP-mediated site-specific recombination in bacteria. Gene 290: 153-161.
28. Uzzau S, Figueroa-Bossi N, Rubino S, Bossi L (2001) Epitope tagging of chromosomal genes in Salmonella. Proc Natl Acad Sci U S A 98: 15264-15269.
29. Vogel HJ, Bonner DM (1956) Acetylornithinase of Escherichia coli: partial purification and some properties. J Biol Chem 218: 97-106.
30. Lee YH, Kim BH, Kim JH, Yoon WS, Bang SH, et al. (2007) CadC has a global translational effect during acid adaptation in Salmonella enterica serovar Typhimurium. J Bacteriol 189: 2417-2425.
31. Klose KE, Mekalanos JJ (1997) Simultaneous prevention of glutamine synthesis and high-affinity transport attenuates Salmonella typhimurium virulence. Infect Immun 65: 587-596.
32. van der Velden AW, Baumler AJ, Tsolis RM, Heffron F (1998) Multiple fimbrial adhesins are required for full virulence of Salmonella typhimurium in mice. Infect Immun 66: 2803-2808.
33. Wijburg OL, Uren TK, Simpfendorfer K, Johansen FE, Brandtzaeg P, et al. (2006) Innate secretory antibodies protect against natural Salmonella typhimurium infection. J Exp Med 203: 21-26.
34. Porwollik S, Frye J, Florea LD, Blackmer F, McClelland M (2003) A non-redundant microarray of genes for two related bacteria. Nucleic Acids Res 31: 1869-1876.
35. Tusher VG, Tibshirani R, Chu G (2001) Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci U S A 98: 5116-5121.
36. Miller JH (1972) Experiments in Molecular Genetics. Cold Spring Harbor Laboratory Press pp 352-355.
37. Bacon RT, Sofos JN, Kendall PA, Belk KE, Smith GC (2003) Comparative analysis of acid resistance between susceptible and multi-antimicrobial-resistant Salmonella strains cultured under stationary-phase acid tolerance-inducing and noninducing conditions. J Food Prot 66: 732-740.
38. D'Autreaux B, Touati D, Bersch B, Latour JM, Michaud-Soret I (2002) Direct inhibition by nitric oxide of the transcriptional ferric uptake regulation protein via nitrosylation of the iron. Proc Natl Acad Sci U S A 99: 16619-16624.
39. Zhou D, Harch WD, Galan JE (1999) Salmonella typhimurium encodes a putative iron transport system within the centisome 63 pathogenicity island. Infect Immun 67: 1974-1981.
40. Baumler AJ, Tsolis RM, van der Velden AW, Stojiljkovic I, Anic S, et al. (1996) Identification of a new iron regulated locus of Salmonella typhi. Gene 183: 207-213.
41. McCollister BD, Bourret TJ, Gill R, Jones-Carson J, Vazquez-Torres A (2005) Repression of SPI2 transcription by nitric oxide-producing, IFNγ-activated macrophages promotes maturation of Salmonella phagosomes. J Exp Med 202: 625-635.
42. Hung CR, Wang PS (2004) Gastric oxidative stress and hemorrhagic ulcer in Salmonella typhimurium-infected rats. Eur J Pharmacol 491: 61-68.
43. Leyer GJ, Johnson KA (1993) Acid adaptation induces cross-protection against environmental stresses in Salmonella typhimurium. Appl Environ Microbiol 59: 1842-1847.
44. Husain M, Bourret TJ, McCollister BD, Jones-Carson J, Laughlin J, et al. (2008) Nitric oxide evokes an adaptive response to oxidative stress by arresting respiration. J Biol Chem. In press.
45. Foster JW, Hall HK (1991) Inducible pH homeostasis and the acid tolerance response of Salmonella typhimurium. J Bacteriol 173: 5129-5135.
46. Prost LR, Daley ME, Le Sage V, Bader MW, Le Moual H, et al. (2007) Activation of the bacterial sensor kinase PhoQ by acidic pH. Mol Cell 26: 165-174.
47. Monsieurs P, De Keersmaecker S, Navarre WW, Bader MW, De Smet F, et al. (2005) Comparison of the PhoPQ regulon in Escherichia coli and Salmonella typhimurium. J Mol Evol 60: 462-474.
48. Zwir I, Shin D, Kato A, Nishino K, Latifi T, et al. (2005) Dissecting the PhoP regulatory network of Escherichia coli and Salmonella enterica. Proc Natl Acad Sci U S A 102: 2862-2867.
49. Soncini FC, Garcia Vescovi E, Solomon F, Groisman EA (1996) Molecular basis of the magnesium deprivation response in Salmonella typhimurium: identification of PhoP-regulated genes. J Bacteriol 178: 5092-5099.
50. Bjorne H, Weitzberg E, Lundberg JO (2006) Intragastric generation of antimicrobial nitrogen oxides from saliva-physiological and therapeutic considerations. Free Radic Biol Med 41: 1404-1412.
51. Soncini FC, Vescovi EG, Groisman EA (1995) Transcriptional autoregulation of the Salmonella typhimurium phoPQ operon. J Bacteriol 177: 4364-4371.
52. Aiso T, Ohki R (2003) Instability of sensory histidine kinase mRNAs in Escherichia coli. Genes Cells 8: 179-187.
53. Adams P, Fowler R, Kinsella N, Howell G, Farris M, et al. (2001) Proteomic detection of PhoPQ- and acid-mediated repression of Salmonella motility. Proteomics 1: 597-607.
54. Eichelberg K, Galan JE (1999) Differential regulation of Salmonella typhimurium type III secreted proteins by pathogenicity island 1 (SPI-1)-encoded transcriptional activators InvF and hilA. Infect Immun 67: 4099-4105.
55. Llama-Palacios A, Lopez-Solanilla E, Poza-Carrion C, Garcia-Olmedo F, Rodriguez-Palenzuela P (2003) The Envinia chrysanthemi phoP-phoQ operon plays an important role in growth at low pH, virulence and bacterial survival in plant tissue. Mol Microbiol 49: 347-357.
56. Oyston PC, Dorrell N, Williams K, Li SR, Green M, et al. (2000) The response regulator PhoP is important for survival under conditions of macrophage-induced stress and virulence in Yersinia pestis. Infect Immun 68: 3419-3425.
57. 2+-responsive PhoP regulator in Yersinia pestis. FEMS Microbiol Lett 250: 85-95.
58. Butler CS, Seward HE, Greenwood C, Thomson AJ (1997) Fast cytochrome bo from Escherichia coli binds two molecules of nitric oxide at CuB. Biochemistry 36: 16259-16266.
59. Hori H, Tsubaki M, Mogi T, Anraku Y (1996) EPR study of NO complex of bd- type ubiquinol oxidase from Escherichia coli. J Biol Chem 271: 9254-9258.
60. Groisman EA, Parra-Lopez C, Salcedo M, Lipps CJ, Heffron F (1992) Resistance to host antimicrobial peptides is necessary for Salmonella virulence. Proc Natl Acad Sci U S A 89: 11939-11943.
61. Golubeva YA, Slauch JM (2006) Salmonella enterica serovar Typhimurium periplasmic superoxide dismutase SodCI is a member of the PhoPQ regulon and is induced in macrophages. J Bacteriol 188: 7853-7861.
62. Miller SI, Kukral AM, Mekalanos JJ (1989) A two-component regulatory system (phoP phoQ) controls Salmonella typhimurium virulence. Proc Natl Acad Sci U S A 86: 5054-5058.
63. Fields PI, Groisman EA, Heffron F (1989) A Salmonella locus that controls resistance to microbicidal proteins from phagocytic cells. Science 243: 1059-1062.
64. 3 enhances the nitrosative potential of IFNγ-primed macrophages in response to Salmonella. Immunobiol 212: 759-769.
65. Deiwick J, Nikolaus T, Erdogan S, Hensel M (1999) Environmental regulation of Salmonella pathogenicity island 2 gene expression. Mol Microbiol 31: 1759-1773.
66. Worley MJ, Ching KH, Heffron F (2000) Salmonella SsrB activates a global regulon of horizontally acquired genes. Mol Microbiol 36: 749-761.
67. Bijlsma JJ, Groisman EA (2005) The PhoP/PhoQ system controls the intramacrophage type three secretion system of Salmonella enterica. Mol Microbiol 57: 85-96.
68. Dorman CJ, Chatfield S, Higgins CF, Hayward C, Dougan G (1989) Characterization of porin and ompR mutants of a virulent strain of Salmonella typhimurium: ompR mutants are attenuated in vivo. Infect Immun 57: 2136-2140.
69. Stojiljkovic I, Baumler AJ, Heffron F (1995) Ethanolamine Utilization in Salmonella typhimurium: Nucleotide Sequence, Protein Expression, and Mutational Analysis of the cchA cchB eutE eutF eutG eutH Gene Cluster. J. Bacteriol 177: 1257-1366.
70. R cassettes with the option of Flp-catalyzed excision of the antibiotic-resistance determinant. Gene 158: 9-14.
71. Wang RF, Kushner SR (1991) Construction of versatile low-copy-number vectors for cloning, sequencing and gene expression in Escherichia coli. Gene 100: 195-199.