Examination of the Staphylococcus aureus nitric oxide reductase (saNOR) reveals its contribution to modulating intracellular NO levels and cellular respiration

Molecular Microbiology

Volumn 96, Issue 3, 2015, Pages 651-669

  Lewis, A M ^a   Matzdorf, S S ^a   Endres, J L ^b   Windham, I H ^b   Bayles, K W ^b   Rice, K C ^a  

^a UNIVERSITY OF FLORIDA   (United States)

^b UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NITRIC OXIDE; NITRIC OXIDE REDUCTASE; OXYGEN; NITRIC-OXIDE REDUCTASE; OXIDOREDUCTASE;

ARTICLE; BACTERIUM CULTURE; BACTERIUM MUTANT; BIOFILM; CELL LEVEL; CELL RESPIRATION; CELL SUBPOPULATION; CONTROLLED STUDY; DETOXIFICATION; GENE EXPRESSION REGULATION; GENETIC COMPLEMENTATION; GROWTH REGULATION; MEMBRANE POTENTIAL; NITROSATIVE STRESS; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; STAPHYLOCOCCUS AUREUS; WILD TYPE; ENZYMOLOGY; GENE DELETION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; OXIDATION REDUCTION REACTION; PHYSIOLOGICAL STRESS;

STAPHYLOCOCCUS AUREUS;

GENE DELETION; GENETIC COMPLEMENTATION TEST; NITRIC OXIDE; OXIDATION-REDUCTION; OXIDOREDUCTASES; STAPHYLOCOCCUS AUREUS; STRESS, PHYSIOLOGICAL;

EID: 84928420085     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12962     Document Type: Article

References (98)

1. Altschul, S.F., Gish, W., Miller, W., Myers, E.W., and Lipman, D.J. (1990) Basic local alignment search tool. J Mol Biol 215: 403-410.
2. Amaral, M.M., Coelho, L.R., Flores, R.P., Souza, R.R., Silva-Carvalho, M.C., Teixeira, L.A., etal. (2005) The predominant variant of the Brazilian epidemic clonal complex of methicillin-resistant Staphylococcus aureus has an enhanced ability to produce biofilm and to adhere to and invade airway epithelial cells. J Infect Dis 192: 801-810.
3. Andersson, J.A., Cervin, A., Lindberg, S., Uddman, R., and Cardell, L.O. (2002) The paranasal sinuses as reservoirs for nitric oxide. Acta Otolaryngol 122: 861-865.
4. Anisimova, M., and Gascuel, O. (2006) Approximate likelihood-ratio test for branches: a fast, accurate, and powerful alternative. Syst Biol 55: 539-552.
5. Arai, H., and Iiyama, K. (2013) Role of nitric oxide-detoxifying enzymes in the virulence of Pseudomonas aeruginosa against the silkworm, Bombyx mori. Biosci Biotechnol Biochem 77: 198-200.
6. Barraud, N., Hassett, D.J., Hwang, S.H., Rice, S.A., Kjelleberg, S., and Webb, J.S. (2006) Involvement of nitric oxide in biofilm dispersal of Pseudomonas aeruginosa. J Bacteriol 188: 7344-7353.
7. Baty, A.M., 3rd, Eastburn, C.C., Techkarnjanaruk, S., Goodman, A.E., and Geesey, G.G. (2000) Spatial and temporal variations in chitinolytic gene expression and bacterial biomass production during chitin degradation. Appl Environ Microbiol 66: 3574-3585.
8. Bose, J.L., Lehman, M.K., Fey, P.D., and Bayles, K.W. (2012) Contribution of the Staphylococcus aureus Atl AM and GL murein hydrolase activities in cell division, autolysis, and biofilm formation. PLoS ONE 7: e42244.
9. Brown, G.C., McBride, A.G., Fox, E.J., McNaught, K.S., and Borutaite, V. (1997) Nitric oxide and oxygen metabolism. Biochem Soc Trans 25: 901-904.
10. Bruckner, R. (1997) Gene replacement in Staphylococcus carnosus and Staphylococcus xylosus. FEMS Microbiol Lett 151: 1-8.
11. Busch, A., Strube, K., Friedrich, B., and Cramm, R. (2005) Transcriptional regulation of nitric oxide reduction in Ralstonia eutropha H16. Biochem Soc Trans 33: 193-194.
12. Cals-Grierson, M.M., and Ormerod, A.D. (2004) Nitric oxide function in the skin. Nitric Oxide 10: 179-193.
13. Cassat, J.E., Dunman, P.M., McAleese, F., Murphy, E., Projan, S.J., and Smeltzer, M.S. (2005) Comparative genomics of Staphylococcus aureus musculoskeletal isolates. J Bacteriol 187: 576-592.
14. Castresana, J. (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17: 540-552.
15. Chai, Y., Chu, F., Kolter, R., and Losick, R. (2008) Bistability and biofilm formation in Bacillus subtilis. Mol Microbiol 67: 254-263.
16. Chen, F.J., Lauderdale, T.L., Wang, L.S., and Huang, I.W. (2013) Complete genome sequence of Staphylococcus aureus Z172, a vancomycin-intermediate and daptomycin-nonsusceptible methicillin-resistant strain isolated in Taiwan. Genome Announc 1: e01011-13.
17. Cheung, A.L., Nast, C.C., and Bayer, A.S. (1998) Selective activation of sar promoters with the use of green fluorescent protein transcriptional fusions as the detection system in the rabbit endocarditis model. Infect Immun 66: 5988-5993.
18. Chevenet, F., Brun, C., Banuls, A.L., Jacq, B., and Christen, R. (2006) TreeDyn: towards dynamic graphics and annotations for analyses of trees. BMC Bioinformatics 7: 439.
19. Chua, K., Seemann, T., Harrison, P.F., Davies, J.K., Coutts, S.J., Chen, H., etal. (2010) Complete genome sequence of Staphylococcus aureus strain JKD6159, a unique Australian clone of ST93-IV community methicillin-resistant Staphylococcus aureus. J Bacteriol 192: 5556-5557.
20. Costa, M.O., Beltrame, C.O., Ferreira, F.A., Botelho, A.M., Lima, N.C., Souza, R.C., etal. (2013) Complete genome sequence of a variant of the methicillin-resistant Staphylococcus aureus ST239 lineage, strain BMB9393, displaying superior ability to accumulate ica-independent biofilm. Genome Announc 1: e00576-13.
21. Davis, K.L., Martin, E., Turko, I.V., and Murad, F. (2001) Novel effects of nitric oxide. Annu Rev Pharmacol Toxicol 41: 203-236.
22. Dereeper, A., Guignon, V., Blanc, G., Audic, S., Buffet, S., Chevenet, F., etal. (2008) Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res 36: W465-W469.
23. Dereeper, A., Audic, S., Claverie, J.M., and Blanc, G. (2010) BLAST-EXPLORER helps you building datasets for phylogenetic analysis. BMC Evol Biol 10: 8.
24. Edgar, R.C. (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32: 1792-1797.
25. Falsetta, M.L., Bair, T.B., Ku, S.C., Vanden Hoven, R.N., Steichen, C.T., McEwan, A.G., etal. (2009) Transcriptional profiling identifies the metabolic phenotype of gonococcal biofilms. Infect Immun 77: 3522-3532.
26. Falsetta, M.L., McEwan, A.G., Jennings, M.P., and Apicella, M.A. (2010) Anaerobic metabolism occurs in the substratum of gonococcal biofilms and may be sustained in part by nitric oxide. Infect Immun 78: 2320-2328.
27. Franceschini, A., Szklarczyk, D., Frankild, S., Kuhn, M., Simonovic, M., Roth, A., etal. (2013) STRING v9.1: protein-protein interaction networks, with increased coverage and integration. Nucleic Acids Res 41: D808-D815.
28. Francis, K.P., Joh, D., Bellinger-Kawahara, C., Hawkinson, M.J., Purchio, T.F., and Contag, P.R. (2000) Monitoring bioluminescent Staphylococcus aureus infections in living mice using a novel luxABCDE construct. Infect Immun 68: 3594-3600.
29. Garcia-Alvarez, L., Holden, M.T., Lindsay, H., Webb, C.R., Brown, D.F., Curran, M.D., etal. (2011) Meticillin-resistant Staphylococcus aureus with a novel mecA homologue in human and bovine populations in the UK and Denmark: a descriptive study. Lancet Infect Dis 11: 595-603.
30. Gillaspy, A.F., Hickmon, S.G., Skinner, R.A., Thomas, J.R., Nelson, C.L., and Smeltzer, M.S. (1995) Role of the accessory gene regulator (agr) in pathogenesis of staphylococcal osteomyelitis. Infect Immun 63: 3373-3380.
31. Golding, G.R., Bryden, L., Levett, P.N., McDonald, R.R., Wong, A., Graham, M.R., etal. (2012) Whole-genome sequence of livestock-associated ST398 methicillin-resistant Staphylococcus aureus isolated from humans in Canada. J Bacteriol 194: 6627-6628.
32. Goncalves, V.L., Nobre, L.S., Vicente, J.B., Teixeira, M., and Saraiva, L.M. (2006) Flavohemoglobin requires microaerophilic conditions for nitrosative protection of Staphylococcus aureus. FEBS Lett 580: 1817-1821.
33. Groicher, K.H., Firek, B.A., Fujimoto, D.F., and Bayles, K.W. (2000) The Staphylococcus aureus lrgAB operon modulates murein hydrolase activity and penicillin tolerance. J Bacteriol 182: 1794-1801.
34. Guerout-Fleury, A.M., Shazand, K., Frandsen, N., and Stragier, P. (1995) Antibiotic-resistance cassettes for Bacillus subtilis. Gene 167: 335-336.
35. Guinane, C.M., Ben Zakour, N.L., Tormo-Mas, M.A., Weinert, L.A., Lowder, B.V., Cartwright, R.A., etal. (2010) Evolutionary genomics of Staphylococcus aureus reveals insights into the origin and molecular basis of ruminant host adaptation. Genome Biol Evol 2: 454-466.
36. Guindon, S., and Gascuel, O. (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52: 696-704.
37. Gustafsson, L.E., Leone, A.M., Persson, M.G., Wiklund, N.P., and Moncada, S. (1991) Endogenous nitric oxide is present in the exhaled air of rabbits, guinea pigs and humans. Biochem Biophys Res Commun 181: 852-857.
38. Hanahan, D. (1983) Studies on transformation of Escherichia coli with plasmids. J Mol Biol 166: 557-580.
39. 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 USA 98: 10108-10112.
40. Hendriks, J., Oubrie, A., Castresana, J., Urbani, A., Gemeinhardt, S., and Saraste, M. (2000) Nitric oxide reductases in bacteria. Biochim Biophys Acta 1459: 266-273.
41. Holden, M.T., Feil, E.J., Lindsay, J.A., Peacock, S.J., Day, N.P., Enright, M.C., etal. (2004) Complete genomes of two clinical Staphylococcus aureus strains: evidence for the rapid evolution of virulence and drug resistance. Proc Natl Acad Sci USA 101: 9786-9791.
42. Holden, M.T., Lindsay, J.A., Corton, C., Quail, M.A., Cockfield, J.D., Pathak, S., etal. (2010) Genome sequence of a recently emerged, highly transmissible, multi-antibiotic- and antiseptic-resistant variant of methicillin-resistant Staphylococcus aureus, sequence type 239 (TW). J Bacteriol 192: 888-892.
43. Holden, M.T., Hsu, L.Y., Kurt, K., Weinert, L.A., Mather, A.E., Harris, S.R., etal. (2013) A genomic portrait of the emergence, evolution, and global spread of a methicillin-resistant Staphylococcus aureus pandemic. Genome Res 23: 653-664.
44. Howden, B.P., Seemann, T., Harrison, P.F., McEvoy, C.R., Stanton, J.A., Rand, C.J., etal. (2010) Complete genome sequence of Staphylococcus aureus strain JKD6008, an ST239 clone of methicillin-resistant Staphylococcus aureus with intermediate-level vancomycin resistance. J Bacteriol 192: 5848-5849.
45. Justino, M.C., Almeida, C.C., Teixeira, M., and Saraiva, L.M. (2007) Escherichia coli di-iron YtfE protein is necessary for the repair of stress-damaged iron-sulfur clusters. J Biol Chem 282: 10352-10359.
46. Kakishima, K., Shiratsuchi, A., Taoka, A., Nakanishi, Y., and Fukumori, Y. (2007) Participation of nitric oxide reductase in survival of Pseudomonas aeruginosa in LPS-activated macrophages. Biochem Biophys Res Commun 355: 587-591.
47. 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 Respir Crit Care Med 153: 829-836.
48. Kinkel, T.L., Roux, C.M., Dunman, P.M., and Fang, F.C. (2013) The Staphylococcus aureus SrrAB two-component system promotes resistance to nitrosative stress and hypoxia. MBio 4: e00696-13.
49. Kohler, C., von Eiff, C., Liebeke, M., McNamara, P.J., Lalk, M., Proctor, R.A., etal. (2008) A defect in menadione biosynthesis induces global changes in gene expression in Staphylococcus aureus. J Bacteriol 190: 6351-6364.
50. Kreiswirth, B.N., Lofdahl, S., Betley, M.J., O'Reilly, M., Schlievert, P.M., Bergdoll, M.S., and Novick, R.P. (1983) The toxic shock syndrome exotoxin structural gene is not detectably transmitted by a prophage. Nature 305: 709-712.
51. Kussell, E., and Leibler, S. (2005) Phenotypic diversity, population growth, and information in fluctuating environments. Science 309: 2075-2078.
52. Larkin, M.A., Blackshields, G., Brown, N.P., Chenna, R., McGettigan, P.A., McWilliam, H., etal. (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23: 2947-2948.
53. Lewis, M.E., Corker, H.A., Gollan, B., and Poole, R.K. (2008) A survey of methods for the purification of microbial flavohemoglobins. Methods Enzymol 436: 169-186.
54. Li, Y., Cao, B., Zhang, Y., Zhou, J., Yang, B., and Wang, L. (2011) Complete genome sequence of Staphylococcus aureus T0131, an ST239-MRSA-SCCmec type III clone isolated in China. J Bacteriol 193: 3411-3412.
55. Lidstrom, M.E., and Konopka, M.C. (2010) The role of physiological heterogeneity in microbial population behavior. Nat Chem Biol 6: 705-712.
56. Livak, K.J., and Schmittgen, T.D. (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25: 402-408.
57. Loisel-Meyer, S., Jimenez de Bagues, M.P., Basseres, E., Dornand, J., Kohler, S., Liautard, J.P., and Jubier-Maurin, V. (2006) Requirement of norD for Brucella suis virulence in a murine model of in vitro and in vivo infection. Infect Immun 74: 1973-1976.
58. Lowy, F.D. (1998) Staphylococcus aureus infections. N Engl J Med 339: 520-532.
59. Luong, T.T., and Lee, C.Y. (2007) Improved single-copy integration vectors for Staphylococcus aureus. J Microbiol Methods 70: 186-190.
60. Malone, C.L., Boles, B.R., Lauderdale, K.J., Thoendel, M., Kavanaugh, J.S., and Horswill, A.R. (2009) Fluorescent reporters for Staphylococcus aureus. J Microbiol Methods 77: 251-260. doi: 10.1016/j.mimet.2009.02.011; Epub 2009 Mar 1013.
61. Mann, E.E., Rice, K.C., Boles, B.R., Endres, J.L., Ranjit, D., Chandramohan, L., etal. (2009) Modulation of eDNA release and degradation affects Staphylococcus aureus biofilm maturation. PLoS ONE 4: e5822.
62. Matsumoto, Y., Tosha, T., Pisliakov, A.V., Hino, T., Sugimoto, H., Nagano, S., etal. (2012) Crystal structure of quinol-dependent nitric oxide reductase from Geobacillus stearothermophilus. Nat Struct Mol Biol 19: 238-245.
63. Miller, W.G., and Lindow, S.E. (1997) An improved GFP cloning cassette designed for prokaryotic transcriptional fusions. Gene 191: 149-153.
64. Moormeier, D.E., Endres, J.L., Mann, E.E., Sadykov, M.R., Horswill, A.R., Rice, K.C., etal. (2013) Use of microfluidic technology to analyze gene expression during Staphylococcus aureus biofilm formation reveals distinct physiological niches. Appl Environ Microbiol 79: 3413-3424. doi: 10.1128/AEM.00395-13; Epub 02013 Mar 00322.
65. Moormeier, D.E., Bose, J.L., Horswill, A.R., and Bayles, K.W. (2014) Temporal and stochastic control of Staphylococcus aureus biofilm development. MBio 5: e1341-e1314.
66. Moreno-Vivian, C., Cabello, P., Martinez-Luque, M., Blasco, R., and Castillo, F. (1999) Prokaryotic nitrate reduction: molecular properties and functional distinction among bacterial nitrate reductases. J Bacteriol 181: 6573-6584.
67. Munch, R., Hiller, K., Grote, A., Scheer, M., Klein, J., Schobert, M., and Jahn, D. (2005) Virtual Footprint and PRODORIC: an integrative framework for regulon prediction in prokaryotes. Bioinformatics 21: 4187-4189.
68. Nienaber, J.J., Sharma Kuinkel, B.K., Clarke-Pearson, M., Lamlertthon, S., Park, L., Rude, T.H., etal. (2011) Methicillin-susceptible Staphylococcus aureus endocarditis isolates are associated with clonal complex 30 genotype and a distinct repertoire of enterotoxins and adhesins. J Infect Dis 204: 704-713.
69. Novo, D., Perlmutter, N.G., Hunt, R.H., and Shapiro, H.M. (1999) Accurate flow cytometric membrane potential measurement in bacteria using diethyloxacarbocyanine and a ratiometric technique. Cytometry 35: 55-63.
70. Overton, T.W., Justino, M.C., Li, Y., Baptista, J.M., Melo, A.M., Cole, J.A., and Saraiva, L.M. (2008) Widespread distribution in pathogenic bacteria of di-iron proteins that repair oxidative and nitrosative damage to iron-sulfur centers. J Bacteriol 190: 2004-2013.
71. Panaro, M.A., Brandonisio, O., Acquafredda, A., Sisto, M., and Mitolo, V. (2003) Evidences for iNOS expression and nitric oxide production in the human macrophages. Curr Drug Targets Immune Endocr Metabol Disord 3: 210-221.
72. Park, M.K., Myers, R.A., and Marzella, L. (1992) Oxygen tensions and infections: modulation of microbial growth, activity of antimicrobial agents, and immunologic responses. Clin Infect Dis 14: 720-740.
73. Patton, T.G., Rice, K.C., Foster, M.K., and Bayles, K.W. (2005) The Staphylococcus aureus cidC gene encodes a pyruvate oxidase that affects acetate metabolism and cell death in stationary phase. Mol Microbiol 56: 1664-1674.
74. Patton, T.G., Yang, S.J., and Bayles, K.W. (2006) The role of proton motive force in expression of the Staphylococcus aureus cid and lrg operons. Mol Microbiol 59: 1395-1404.
75. Rice, K.C., Mann, E.E., Endres, J.L., Weiss, E.C., Cassat, J.E., Smeltzer, M.S., and Bayles, K.W. (2007) The cidA murein hydrolase regulator contributes to DNA release and biofilm development in Staphylococcus aureus. Proc Natl Acad Sci USA 104: 8113-8118.
76. Richardson, A.R., Dunman, P.M., and Fang, F.C. (2006) The nitrosative stress response of Staphylococcus aureus is required for resistance to innate immunity. Mol Microbiol 61: 927-939.
77. Richardson, A.R., Libby, S.J., and Fang, F.C. (2008) A nitric oxide-inducible lactate dehydrogenase enables Staphylococcus aureus to resist innate immunity. Science 319: 1672-1676.
78. Sapp, A.M., Mogen, A.B., Almand, E.A., Rivera, F.E., Shaw, L.N., Richardson, A.R., and Rice, K.C. (2014) Contribution of the nos-pdt operon to virulence phenotypes in methicillin-sensitive Staphylococcus aureus. PLoS ONE 9: e108868.
79. Sau, S., Sun, J., and Lee, C.Y. (1997) Molecular characterization and transcriptional analysis of type 8 capsule genes in Staphylococcus aureus. J Bacteriol 179: 1614-1621.
80. Schenk, S., and Laddaga, R.A. (1992) Improved method for electroporation of Staphylococcus aureus. FEMS Microbiol Lett 73: 133-138.
81. Schijffelen, M.J., Boel, C.H., van Strijp, J.A., and Fluit, A.C. (2010) Whole genome analysis of a livestock-associated methicillin-resistant Staphylococcus aureus ST398 isolate from a case of human endocarditis. BMC Genomics 11: 376.
82. Schlag, S., Nerz, C., Birkenstock, T.A., Altenberend, F., and Gotz, F. (2007) Inhibition of staphylococcal biofilm formation by nitrite. J Bacteriol 189: 7911-7919.
83. Shafer, W.M., and Iandolo, J.J. (1979) Genetics of staphylococcal enterotoxin B in methicillin-resistant isolates of Staphylococcus aureus. Infect Immun 25: 902-911.
84. Shapiro, H.M., and Nebe-von-Caron, G. (2004) Multiparameter flow cytometry of bacteria. Methods Mol Biol 263: 33-44.
85. Shimizu, T., Tsutsuki, H., Matsumoto, A., Nakaya, H., and Noda, M. (2012) The nitric oxide reductase of enterohaemorrhagic Escherichia coli plays an important role for the survival within macrophages. Mol Microbiol 85: 492-512.
86. Shompole, S., Henon, K.T., Liou, L.E., Dziewanowska, K., Bohach, G.A., and Bayles, K.W. (2003) Biphasic intracellular expression of Staphylococcus aureus virulence factors and evidence for Agr-mediated diffusion sensing. Mol Microbiol 49: 919-927.
87. Snel, B., Lehmann, G., Bork, P., and Huynen, M.A. (2000) STRING: a web-server to retrieve and display the repeatedly occurring neighbourhood of a gene. Nucleic Acids Res 28: 3442-3444.
88. 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.
89. Sullivan, M.A., Yasbin, R.E., and Young, F.E. (1984) New shuttle vectors for Bacillus subtilis and Escherichia coli which allow rapid detection of inserted fragments. Gene 29: 21-26.
90. Throup, J.P., Zappacosta, F., Lunsford, R.D., Annan, R.S., Carr, S.A., Lonsdale, J.T., etal. (2001) The srhSR gene pair from Staphylococcus aureus: genomic and proteomic approaches to the identification and characterization of gene function. Biochemistry 40: 10392-10401.
91. Treangen, T.J., Maybank, R.A., Enke, S., Friss, M.B., Diviak, L.F., Karaolis, D.K., etal. (2014) Complete genome sequence of the quality control strain Staphylococcus aureus subsp. aureus ATCC 25923. Genome Announc 2: e01110-14.
92. Uhlemann, A.C., Porcella, S.F., Trivedi, S., Sullivan, S.B., Hafer, C., Kennedy, A.D., etal. (2012) Identification of a highly transmissible animal-independent Staphylococcus aureus ST398 clone with distinct genomic and cell adhesion properties. MBio 3: e00027-12.
93. Waheed, S.M., Ghosh, A., Chakravarti, R., Biswas, A., Haque, M.M., Panda, K., and Stuehr, D.J. (2010) Nitric oxide blocks cellular heme insertion into a broad range of heme proteins. Free Radic Biol Med 48: 1548-1558.
94. Worlitzsch, D., Tarran, R., Ulrich, M., Schwab, U., Cekici, A., Meyer, K.C., etal. (2002) Effects of reduced mucus oxygen concentration in airway Pseudomonas infections of cystic fibrosis patients. J Clin Invest 109: 317-325.
95. Wright, C.D., Mulsch, A., Busse, R., and Osswald, H. (1989) Generation of nitric oxide by human neutrophils. Biochem Biophys Res Commun 160: 813-819.
96. Yao, J., Zhong, J., Fang, Y., Geisinger, E., Novick, R.P., and Lambowitz, A.M. (2006) Use of targetrons to disrupt essential and nonessential genes in Staphylococcus aureus reveals temperature sensitivity of Ll.LtrB group II intron splicing. RNA 12: 1271-1281.
97. Yarwood, J.M., Bartels, D.J., Volper, E.M., and Greenberg, E.P. (2004) Quorum sensing in Staphylococcus aureus biofilms. J Bacteriol 186: 1838-1850.
98. Zhang, X., Hu, Q., Yuan, W., Shang, W., Cheng, H., Yuan, J., etal. (2013) First report of a sequence type 239 vancomycin-intermediate Staphylococcus aureus isolate in Mainland China. Diagn Microbiol Infect Dis 77: 64-68.