Bacterial nitric oxide detoxification prevents host cell S-nitrosothiol formation: A novel mechanism of bacterial pathogenesis

FASEB Journal

Volumn 24, Issue 1, 2010, Pages 286-295

  Laver, Jay R ^a   Stevanin, Tânia M ^a   Messenger, Sarah L ^a   Lunn, Amy Dehn ^a   Lee, Margaret E ^a   Moir, James W B ^b   Poole, Robert K ^a   Read, Robert C ^a  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

^b UNIVERSITY OF YORK   (United Kingdom)

Author keywords

Infection; Macrophage; Nitrosative stress; S nitrosylation

Indexed keywords

FLAVOHEMOGLOBIN; GAMMA INTERFERON; LIPOPOLYSACCHARIDE; NITRIC OXIDE; NITRIC OXIDE REDUCTASE; S NITROSOTHIOL; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BACTERIAL INFECTION; CELL DAMAGE; DETOXIFICATION; ESCHERICHIA COLI; HOST CELL; MACROPHAGE; MOUSE; NEISSERIA MENINGITIDIS; NITROSATIVE STRESS; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; SALMONELLA ENTERICA;

ANIMALS; BACTERIA; CELL LINE; ESCHERICHIA COLI K12; HOST-PATHOGEN INTERACTIONS; INTERFERON-GAMMA, RECOMBINANT; LIPOPOLYSACCHARIDES; MACROPHAGES; METABOLIC DETOXICATION, DRUG; MICE; NEISSERIA MENINGITIDIS, SEROGROUP B; NITRIC OXIDE; OXIDOREDUCTASES; S-NITROSOTHIOLS; SALMONELLA TYPHIMURIUM;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; EUKARYOTA; MURINAE; NEISSERIA MENINGITIDIS; SALMONELLA ENTERICA;

EID: 75149137411     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.08-128330     Document Type: Article

References (71)

1. Stamler, J. S., Jaraki, O., Osborne, J., Simon, D. I., Keaney, J., Vita, J., Singel, D., Valeri, C. R., and Loscalzo, J. (1992) Nitric oxide circulates in mammalian plasma primarily as an S-nitroso adduct of serum albumin. Proc. Natl. Acad. Sci. U. S. A. 89, 7674-7677
2. Mannick, J. B., and Schonhoff, C. M. (2002) Nitrosylation: the next phosphorylation? Arch. Biochem. Biophys. 408, 1-6
3. Hara, M. R., and Snyder, S. H. (2006) Nitric. oxide-GAPDH-Siah: A novel cell death cascade. Cell. Mol. Neurobiol. 26, 527-538
4. Kim, Y. M., Talanian, R. V., and Billiar, T. R. (1997) Nitric oxide inhibits apoptosis by preventing increases in caspase-3-like activity via two distinct mechanisms J. Biol. Chem. 272, 31138-31148
5. Li, J., Billiar, T. R., Talanian, R. V., and Kim, Y. M. (1997) Nitric oxide reversibly inhibits seven members of the caspase family via S-nitrosylation Biochem. Biophys. Res. Commun. 240, 419-424
6. Mannick, J. B., Miao, X. Q., and Stamler, J. S. (1997) Nitric oxide inhibits Fas-induced apoptosis. J. Biol. Chem. 272, 24125-24128
7. Lander, H. M., Hajjar, D. P., Hempstead, B. L., Mirza, U. A., Chait, B. T., Campbell, S., and Quilliam, L. A. (1997) A molecular redox switch on p21(ras). Structural basis for the nitric oxide-p21(ras) interaction. J. Biol. Chem. 272, 4323-4326
8. Jaffrey, S. R., Erdjument-Bromage, H., Ferris, C. D., Tempst, P., and Snyder, S. H. (2001) Protein S-nitrosylation: a physiological signal for neuronal nitric oxide. Nat. Cell Biol. 3, 193-197
9. Marshall, H. E., and Stamler, J. S. (2001) Inhibition of NF-kappa B by S-nitrosylation. Biochemistry 40, 1688-1693
10. Rabkin, S. W., and Klassen, S. S. (2007) Nitric oxide differentially regulates the gene expression of caspase genes but not some autophagic genes. Nitric Oxide 16, 339-347
11. Reynaert, N. L., Ckless, K., Korn, S. H., Vos, N., Guala, A. S., Wouters, E. F., van der Vliet, A., and Janssen-Heininger, Y. M. (2004) Nitric oxide represses inhibitory kappaB kinase through S-nitrosylation. Proc. Natl. Acad. Sci. U. S. A. 101, 8945-8950
12. Gow, A. J., Chen, Q., Hess, D. T., Day, B. J., Ischiropoulos, H., and Stamler, J. S. (2002) Basal and stimulated protein S-nitrosylation in multiple cell types and tissues. J. Biol. Chem. 277, 9637-9640
13. Hoffmann, J., Dimmeler, S., and Haendeler, J. (2003) Shear stress increases the amount of S-nitrosylated molecules in endothelial cells: important role for signal transduction FEBS Lett. 551, 153-158
14. Sun, J. H., Xin, C. L., Eu, J. P., Stamler, J. S., and Meissner, G. (2001) Cysteine-3635 is responsible for skeletal muscle ryanodine receptor modulation by NO Proc. Natl. Acad. Sci. U. S. A. 98, 11158-11162
15. Padgett, C. M., and Whorton, A. R. (1995) S-nitrosoglutathione reversibly inhibits GAPDH by S-nitrosylation. Am. J. Physiol. 269, 739-749
16. Fang, M., Jaffrey, S. R., Sawa, A., Ye, K., Luo, X., and Snyder, S. H. (2000) Dexras1: a G protein specifically coupled to neuronal nitric oxide synthase via CAPON. Neuron 28, 183-193
17. Iwakiri, Y., Satoh, A., Chatterjee, S., Toomre, D. K., Chalouni, C. M., Fulton, D., Groszmann, R. J., Shah, V. H., and Sessa, W. C. (2006) Nitric oxide synthase generates nitric oxide locally to regulate compartmentalized protein S-nitrosylation and protein trafficking. Proc. Natl. Acad. Sci. U. S. A. 103, 19777-19782
18. Hess, D. T., Matsumoto, A., Kim, S. O., Marshall, H. E., and Stamler, J. S. (2005) Protein S-nitrosylation:. purview and parameters. Nat. Rev. Mol. Cell. Biol. 6, 150-166
19. Singh, R. J., Hogg, N., Joseph, J., and Kalyanaraman, B. (1996) Mechanism of nitric oxide release from S-nitrosothiols. J. Biol. Chem. 271, 18596-18603
20. Liu, L., Hausladen, A., Zeng, M., Que, L., Heitman, J., and Stamler, J. S. (2001) A metabolic enzyme for S-nitrosothiol conserved from bacteria to humans. Nature 410, 490-494
21. Benhar, M., Forrester, M. T., Hess, D. T., and Stamler, J. S. (2008) Regulated protein denitrosylation by cytosolic and mitochondrial thioredoxins. Science 320, 1050-1054
22. Busch, T., Kuhlen, R., Knorr, M., Kelly, K., Lewandowski, K., Rossaint, R., Falke, K. J., and Gerlach, H. (2000) Nasal, pulmonary and autoinhaled nitric oxide at rest and during moderate exercise. Intensive Care Med. 26, 391-399
23. Gerlach, H., Rossaint, R., Pappert, D., Knorr, M., and Falke, K. J. (1994) Autoinhalation of nitric oxide after endogenous synthesis in nasopharynx. Lancet 343, 518-519
24. Kimberly, B., Nejadnik, B., Giraud, G. D., and Holden, W. E. (1996) Nasal contribution to exhaled nitric oxide at rest and during breathholding in humans. Am. J. Resp. Crit. Care Med. 153, 829-836
25. Rock, J. D., Mahnane, M. R., Anjum, M. F., Shaw, J. G., Read, R. C., and Moir, J. W. (2005) The pathogen Neisseria meningitidis requires oxygen, but supplements growth by denitrification. Nitrite nitric oxide and oxygen control respiratory flux at genetic and metabolic levels. Mol. Microbiol. 58, 800-809
26. Anjum, M. F., Stevanin, T. M., Read, R. C., and Moir, J. W. (2002) Nitric oxide metabolism in Neisseria meningitidis. J. Bacteriol. 184, 2987-2993
27. Stevanin, T. M., Moir, J. W., and Read, R. C. (2005) Nitric oxide detoxification systems enhance survival of Neisseria meningitidis in human macrophages and in nasopharyngeal mucosa. Infect. Immun. 73, 3322-3329
28. Stevanin, T. M., Laver, J. R., Poole, R. K., Moir, J. W., and Read, R. C. (2007) Metabolism of nitric oxide by Neisseria meningitidis modifies release of NO-regulated cytokines and chemokines by human macrophages. Microbes Infect. 9, 981-987
29. Tunbridge, A. J., Stevanin, T. M., Lee, M., Marriott, H. M., Moir, J. W., Read, R. C., and Dockrell, D. H. (2006) Inhibition of macrophage apoptosis by Neisseria meningitidis requires nitric oxide detoxification mechanisms. Infect. Immun. 74, 729-733
30. Heurlier, K., Thomson, M. J., Aziz, N., and Moir, J. W. (2008) The nitric oxide (NO)-sensing repressor NsrR of Neisseria meningitidis has a compact regulon of genes involved in NO synthesis and detoxification. J. Bacteriol. 190, 2488-2495
31. Hardison, R. C. (1996) A brief history of hemoglobins: plant, animal, protist, and bacteria. Proc. Natl. Acad. Sci. U. S. A. 93, 5675-5679
32. Zhu, H., and Riggs, A. F. (1992) Yeast flavohemoglobin is an ancient protein related to globins and a reductase family. Proc. Natl. Acad. Sci. U. S. A. 89, 5015-5019
33. Hernandez-Urzua, E., Mills, C. E., White, G. P., Contreras-Zentella, M. L., Escamilla, E., Vasudevan, S. G., Membrillo-Hernandez, J., and Poole, R. K. (2003) Flavohemoglobin Hmp, but not its individual domains, confers protection from respiratory inhibition by nitric oxide in Escherichia coli. J. Biol. Chem. 278, 34975-34982
34. Poole, R. K., Ioannidis, N., and Orii, Y. (1994) Reactions of the Escherichia coli flavohaemoglobin (Hmp) with oxygen and reduced nicotinamide adenine dinucleotide: evidence for oxygen switching of flavin oxidoreduction and a mechanism for oxygen sensing. Proc. Biol. Sci. 255, 251-258
35. Hausladen, A., Gow, A., and Stamler, J. S. (2001) Flavohemoglobin denitrosylase catalyzes the reaction of a nitroxyl equivalent with molecular oxygen. Proc. Natl. Acad. Sci. U. S. A. 98, 10108-10112
36. Poole, R. K., and Hughes, M. N. (2000) New functions for the ancient globin family: bacterial responses to nitric oxide and nitrosative stress. Mol. Microbiol. 36, 775-783
37. Kim, S. O., Orii, Y., Lloyd, D., Hughes, M. N., and Poole, R. K. (1999) Anoxic function for the Escherichia coli flavohaemoglobin (Hmp): reversible binding of nitric oxide and reduction to nitrous oxide. FEBS Lett. 445, 389-394
38. Membrillo-Hernandez, J., Coopamah, M. D., Channa, A., Hughes, M. N., and Poole, R. K. (1998) A novel mechanism for upregulation of the Escherichia coli K-12 hmp (flavohaemoglobin) gene by the "NO releaser", S-nitrosoglutathione: nitrosation of homocysteine and modulation of MetR binding to the glyA-hmp intergenic region. Mol. Microbiol. 29, 1101-1112
39. Stevanin, T. M., Ioannidis, N., Mills, C. E., Kim, S. O., Hughes, M. N., and Poole, R. K. (2000)Flavohemoglobin Hmp affords inducible protection for Escherichia coli respiration, catalyzed by cytochromes bo' or bd, from nitric oxide. J. Biol. Chem. 275, 35868-35875
40. Stevanin, T. M., Read, R. C., and Poole, R. K. (2007) The hmp gene encoding the NO-inducible flavohaemoglobin in Escherichia coli confers a protective advantage in resisting killing within macrophages, but not in vitro: links with swarming motility. Gene 398, 62-68
41. Bang, I. S., Liu, L., Vazquez-Torres, A., Crouch, M. L., Stamler, J. S., and Fang, F. C. (2006) Maintenance of nitric oxide and redox homeostasis by the Salmonella flavohemoglobin hmp. J. Biol. Chem. 281, 28039-28047
42. Gilberthorpe, N. J., Lee, M. E., Stevanin, T. M., Read, R. C., and Poole, R. K. (2007) NsrR: a key regulator circumventing Salmonella enterica serovar Typhimurium oxidative and nitrosative stress in vitro and in IFN-γ-stimulated J774.2 macrophages. Microbiology 153, 1756-1771
43. Stevanin, T. M., Poole, R. K., Demoncheaux, E. A., and Read, R. C. (2002) Flavohemoglobin Hmp protects Salmonella enterica serovar typhimurium from nitric oxide-related killing by human macrophages. Infect. Immun. 70, 4399-4405
44. Chen, B., Keshive, M., and Deen, W.M. (1998) Diffusion and reaction of nitric oxide in suspension cell cultures. Biophys. J. 75, 745-754
45. Eu, J. P., Liu, L., Zeng, M., and Stamler, J. S. (2000) An apoptotic model for nitrosative stress. Biochemistry 39, 1040-1047
46. Zhang, Y., and Hogg, N. (2004) Formation and stability of S-nitrosothiols in RAW 264.7 cells. Am. J. Physiol. Lung Cell Mol Physiol. 287, L467-L474
47. Laver, J. R., Stevanin, T. M., and Read, R. C. (2008) Chemiluminescence quantification of NO and its derivatives in liquid samples. Methods Enzymol. 436, 113-127
48. Miles, A. A., and Misra, S. S. (1938) The estimation of the bactericidal power of the blood. J. Hygiene 38, 732-749
49. Fang, K., Ragsdale, N. V., Carey, R. M., MacDonald, T., and Gaston, B. (1998) Reductive assays for S-nitrosothiols: implications for measurements in biological systems Biochem. Biophys. Res. Commun. 252, 535-540
50. Boehm, U., Klamp, T., Groot, M., and Howard, J. C. (1997) Cellular responses to interferon-gamma. Annu. Rev. Immunol. 15, 749-795
51. Rock, J. D., Thomson, M. J., Read, R. C., and Moir, J. W. (2007) Regulation of denitrification genes in Neisseria meningitidis by nitric oxide and the repressor NsrR. J. Bacteriol. 189, 1138-1144
52. Farres, J., Rechsteiner, M. P., Herold, S., Frey, A. D., and Kallio, P. T. (2005) Ligand binding properties of bacterial hemoglobins and flavohemoglobins. Biochemistry 44, 4125-4134
53. Broniowska, K. A., Zhang, Y., and Hogg, N. (2006) Requirement of transmembrane transport for S-nitrosocysteine-dependent modification of intracellular thiols. J. Biol. Chem. 281, 33835-33841
54. Lancaster, Jr., J. R., and Gaston, B. (2004) NO and nitrosothiols: spatial confinement and free diffusion. Am. J. Physiol. Lung Cell Mol. Physiol. 287, L465-L466
55. Li, H., Marshall, Z. M., and Whorton, A. R. (1999) Stimulation of cystine uptake by nitric oxide: regulation of endothelial cell glutathione levels. Am. J. Physiol. 276, C803-C811
56. Li, S., and Whorton, A. R. (2007) Functional characterization of two S-nitroso-L-cysteine transporters, which mediate movement of NO equivalents into vascular cells. Am. J. Physiol. Cell Physiol. 292, C1263-C1271
57. James, J. H., Hasselgren, P. O., Hummel, R. P., 3rd, Warner, B. W., and Fischer, J. E. (1990) Effect of sepsis on amino acid transport system A and its response to insulin in incubated rat skeletal muscle. Metabolism 39, 335-340
58. Paige, J. S., Xu, G., Stancevic, B., and Jaffrey, S. R. (2008) Nitrosothiol reactivity profiling identifies S-nitrosylated proteins with unexpected stability. Chem. Biol. 15, 1307-1316
59. Mannick, J. B., Schonhoff, C., Papeta, N., Ghafourifar, P., Szibor, M., Fang, K., and Gaston, B. (2001) S-Nitrosylation of mitochondrial caspases. J. Cell Biol. 154, 1111-1116
60. Stamler, J. S., Toone, E. J., Lipton, S. A., Sucher, N. J. (1997) (S)NO. signals: translocation, regulation, and a consensus motif. Neuron 18, 691-696
61. Schonhoff, C. M., Matsuoka, M., Tummala, H., Johnson, M. A., Estevez, A. G., Wu, R., Kamaid, A., Ricart, K. C., Hashimoto, Y., Gaston, B., Macdonald, T. L., Xu, Z., and Mannick, J. B. (2006) S-nitrosothiol depletion in amyotrophic lateral sclerosis Proc. Natl. Acad. Sci. U. S. A. 103, 2404-2409
62. Chung, K. K., Thomas, B., Li, X., Pletnikova, O., Troncoso, J. C., Marsh, L., Dawson, V. L., and Dawson, T. M. (2004) S-nitrosylation of parkin regulates ubiquitination and compromises parkin's protective function. Science 304, 1328-1331
63. Fang, J., Nakamura, T., Cho, D. H., Gu, Z., and Lipton, S. A. (2007) S-nitrosylation of peroxiredoxin 2 promotes oxidative stress-induced neuronal cell death in Parkinson's disease Proc. Natl. Acad. Sci. U. S. A. 104, 18742-18747
64. Bizzozero, O. A., DeJesus, G., Bixler, H. A., and Pastuszyn, A. (2005) Evidence of nitrosative damage in the brain white matter of patients with multiple sclerosis. Neurochem. Res. 30, 139-149
65. Benhar, M., Forrester, M. T., and Stamler, J. S. (2006) Nitrosative stress in the ER: a new role for S-nitrosylation in neurodegenerative diseases. ACS Chem. Biol. 1, 355-358
66. Que, L. G., Liu, L., Yan, Y., Whitehead, G. S., Gavett, S. H., Schwartz, D. A., and Stamler, J. S. (2005) Protection from experimental asthma by an endogenous bronchodilator. Science 308, 1618-1621
67. Liu, L., Yan, Y., Zeng, M., Zhang, J., Hanes, M. A., Ahearn, G., McMahon, T. J., Dickfeld, T., Marshall, H. E., Que, L. G., and Stamler, J. S. (2004) Essential roles of S-nitrosothiols in vascular homeostasis and endotoxic shock. Cell 116, 617-628
68. Que, L. G., Yang, Z., Stamler, J. S., Lugogo, N. L., Kraft, M. (2009) S-Nitrosoglutathione reductase-an important regulator in human asthma. Am. J. Resp. Crit. Care Med. 180, 226-231
69. Darton, T., Guiver, M., Naylor, S., Jack, D. L., Kaczmarski, E. B., Borrow, R., and Read, R. C. (2009) Severity of meningococcal disease associated with genomic bacterial load. Clin. Infect. Dis. 48, 587-594
70. McGuinness, B. T., Clarke, I. N., Lambden, P. R., Barlow, A. K., Poolman, J. T., Jones, D. M., and Heckels, J. E. (1991) Point mutation in meningococcal por A gene associated with increased endemic disease Lancet 337, 514-517
71. Crawford, M. J., and Goldberg, D. E. (1998) Role for the Salmonella flavohemoglobin in protection from nitric oxide J. Biol. Chem. 273, 12543-12547