Defense mechanisms against oxidative stress in Coxiella burnetii: Adaptation to a unique intracellular niche

Advances in Experimental Medicine and Biology

Volumn 984, Issue , 2012, Pages 39-63

  Mertens, Katja ^a   Samuel, James E ^b  

^a FEDERAL RESEARCH INSTITUTE FOR ANIMAL HEALTH   (Germany)

^b TEXAS A M COLLEGE OF MEDICINE   (United States)

Author keywords

Fur regulon; Oxidative stress; OxyR regulon; ROS and RNS scavenging enzymes; SOS response

Indexed keywords

ACID PHOSPHATASE; CATALASE; DEFENSIN; DNA; INDUCIBLE NITRIC OXIDE SYNTHASE; IRON; NITRIC OXIDE; PEROXIREDOXIN; PROTEINASE; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SUPEROXIDE; SUPEROXIDE DISMUTASE;

ADAPTIVE IMMUNITY; ARTICLE; BACTERIAL REPRODUCTION; BACTERIAL STRAIN; BACTERIAL SURVIVAL; BACTERIAL VIRULENCE; CELL DAMAGE; CELL VACUOLE; COXIELLA BURNETII; DNA DAMAGE; DNA RECOMBINATION; DNA REPAIR; ENDOCYTOSIS; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME RELEASE; ESCHERICHIA COLI; EXCISION REPAIR; GENOMIC INSTABILITY; HOST PATHOGEN INTERACTION; HOST RESISTANCE; IRON BALANCE; METABOLIC REGULATION; NITROSATIVE STRESS; NONHUMAN; OXIDATIVE STRESS; PARASITOPHOROUS VACUOLE; PHAGOCYTOSIS; PHAGOLYSOSOME; PHAGOSOME; PRIORITY JOURNAL;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; COXIELLA BURNETII; DNA DAMAGE; DNA REPAIR; HUMANS; OXIDATIVE STRESS; PHAGOSOMES;

BACTERIA (MICROORGANISMS); COXIELLA BURNETII;

EID: 84863745713     PISSN: 00652598     EISSN: None     Source Type: Book Series    
DOI: 10.1007/978-94-007-4315-1_3     Document Type: Article

References (117)

1. Aamodt RM, Falnes PO, Johansen RF, Seeberg E, Bjoras M (2004) The Bacillus subtilis counterpart of the mammalian 3-methyladenine DNA glycosylase has hypoxanthine and 1, N6-ethenoadenine as preferred substrates. J Biol Chem 279:13601-13606
2. Akporiaye ET, Baca OG (1983) Superoxide anion production and superoxide dismutase and catalase activities in Coxiella burnetii . J Bacteriol 154:520-523
3. Akporiaye ET, Stefanovich D, Tsosie V, Baca G (1990) Coxiella burnetii fails to stimulate human neutrophil superoxide anion production. Acta Virol 34:64-70
4. Albakri QA, Stuehr DJ (1996) Intracellular assembly of inducible NO synthase is limited by nitric oxide-mediated changes in heme insertion and availability. J Biol Chem 271:5414-5421
5. Anderson AD, Kruszon-Moran D, Loftis AD, McQuillan G, Nicholson WL, Priestley RA, Candee AJ, Patterson NE, massung RF (2009) Seroprevalence of Q fever in the United States, 2003-2004. Am J Trop Med Hyg 81:691-694
6. Baca OG, Paretsky D (1983) Q fever and Coxiella burnetii: a model for host-parasite interactions. Microbiol Rev 47:127-149
7. Baca OG, Roman MJ, Glew RH, Christner RF, Buhler JE, Aragon AS (1993) Acid phosphatase activity in Coxiella burnetii: a possible virulence factor. Infect Immun 61:4232-4239
8. Badwey JA, Curnutte JT, Robinson JM, Lazdins JK, Briggs RT, Karnovsky MJ, Karnovsky ML (1980) Comparative aspects of oxidative metabolism of neutrophils from human blood and guinea pig peritonea: magnitude of the respiratory burst, dependence upon stimulating agents, and localization of the oxidases. J Cell Physiol 105:541-545
9. Baek KJ, Thiel BA, Lucas S, Stuehr DJ (1993) macrophage nitric oxide synthase subunits. Puri fication, characterization, and role of prosthetic groups and substrate in regulating their association into a dimeric enzyme. J Biol Chem 268:21120-21129
10. Baker LM, Raudonikiene A, Hoffman PS, Poole LB (2001) Essential thioredoxin-dependent peroxiredoxin system from Helicobacter pylori: genetic and kinetic characterization. J Bacteriol 183:1961-1973
11. Bandyopadhyay P, Steinman HM (1998) Legionella pneumophila catalase-peroxidases: cloning of the katB gene and studies of KatB function. J Bacteriol 180:5369-5374
12. Bandyopadhyay P, Steinman HM (2000) Catalase-peroxidases of Legionella pneumophila: cloning of the katA gene and studies of KatA function. J Bacteriol 182:6679-6686
13. Battistoni A (2003) Role of prokaryotic Cu, Zn superoxide dismutase in pathogenesis. Biochem Soc Trans 31:1326-1329
14. Beare PA, Unsworth N, Andoh M, Voth DE, Omsland A, Gilk SD, Williams KP, Sobral BW, Kupko JJ 3rd, Porcella SF, Samuel JE, Heinzen RA (2009) Comparative genomics reveal extensive transposon-mediated genomic plasticity and diversity among potential effector proteins within the genus Coxiella . Infect Immun 77:642-656
15. Beron W, Gutierrez MG, Rabinovitch M, Colombo MI (2002) Coxiella burnetii localizes in a Rab7-labeled compartment with autophagic characteristics. Infect Immun 70:5816-5821
16. Beyenbach KW, Wieczorek H (2006) The V-type H + ATPase: molecular structure and function, physiological roles and regulation. J Exp Biol 209:577-589
17. Bogdan C (2001) Nitric oxide and the immune response. Nat Immunol 2:907-916
18. Boschi-Muller S, Olry A, Antoine M, Branlant G (2005) The enzymology and biochemistry of methionine sulfoxide reductases. Biochim Biophys Acta 1703:231-238
19. Brennan RE, Russell K, Zhang G, Samuel JE (2004) Both inducible nitric oxide synthase and NADPH oxidase contribute to the control of virulent phase I Coxiella burnetii infections. Infect Immun 72:6666-6675
20. Briggs HL, Pul N, Seshadri R, Wilson MJ, Tersteeg C, Russell-Lodrigue KE, Andoh M, Baumler AJ, Samuel JE (2008) A limited role for iron regulation in Coxiella burnetii pathogenesis. Infect Immun 76(5):2189-2201
21. Bylund J, Brown KL, Movitz C, Dahlgren C, Karlsson A (2010) Intracellular generation of superoxide by the phagocyte NADPH oxidase: how, where, and what for? Free Radic Biol Med 49(12):1834-1845
22. Cabusora L, Sutton E, Fulmer A, Forst CV (2005) Differential network expression during drug and stress response. Bioinformatics 21:2898-2905
23. Callahan LA, Nethery D, Stofan D, Dimarco A, Supinski G (2001) Free radical-induced contractile protein dysfunction in endotoxin-induced sepsis. Am J Respir Cell Mol Biol 24:210-217
24. Cantwell AM, Bubeck SS, Dube PH (2010) YopH inhibits early pro-in flammatory cytokine responses during plague pneumonia. BMC Immunol 11:29
25. Carmel-Harel O, Storz G (2000) Roles of the glutathione- and thioredoxin-dependent reduction systems in the Escherichia coli and Saccharomyces cerevisiae responses to oxidative stress. Annu Rev Microbiol 54:439-461
26. Chelikani P, Fita I, Loewen PC (2004) Diversity of structures and properties among catalases. Cell Mol Life Sci 61:192-208
27. Chen C, Banga S, Mertens K, Weber MM, Gorbaslieva I, Tan Y, Luo ZQ, Samuel JE (2010) Large-scale identi fication and translocation of type IV secretion substrates by Coxiella burnetii . Proc Natl Acad Sci USA 107(50):21755-21760
28. Cirillo SL, Subbian S, Chen B, Weisbrod TR, Jacobs WR Jr, Cirillo JD (2009) Protection of Mycobacterium tuberculosis from reactive oxygen species conferred by the mel2 locus impacts persistence and dissemination. Infect Immun 77:2557-2567
29. Davis AS, Vergne I, master SS, Kyei GB, Chua J, Deretic V (2007) Mechanism of inducible nitric oxide synthase exclusion from mycobacterial phagosomes. PLoS Pathog 3:e186
30. de Jong MF, Sun YH, den Hartigh AB, van Dijl JM, Tsolis RM (2008) Identi fication of VceA and VceC, two members of the VjbR regulon that are translocated into macrophages by the Brucella type IV secretion system. Mol Microbiol 70:1378-1396
31. Demple B, Harrison L (1994) Repair of oxidative damage to DNA: enzymology and biology. Annu Rev Biochem 63:915-948
32. Ennis DG, Little JW, Mount DW (1993) Novel mechanism for UV sensitivity and apparent UV nonmutability of recA432 mutants: persistent LexA cleavage following SOS induction. J Bacteriol 175:7373-7382
33. Enserink M (2010) Infectious diseases. Questions abound in Q-fever explosion in the Netherlands. Science 327:266-267
34. Fang FC, Degroote ma, Foster JW, Baumler AJ, Ochsner U, Testerman T, Bearson S, Giard J-C, Xu Y, Campbell G, Laessig T (1999) Virulent Salmonella typhimurium has two periplasmic Cu, Zn-superoxide dismutases. Proc Natl Acad Sci 96:7502-7507
35. Franzon VL, Arondel J, Sansonetti PJ (1990) Contribution of superoxide dismutase and catalase activities to Shigella flexneri pathogenesis. Infect Immun 58:529-535
36. Friedberg EC, Walker GC, Siede W, Wood RD, Schultz RA, Ellenberger T (2006) DNA repair and mutagenesis. American Society of Microbiology Press, Washington, DC
37. Fujikura Y, Kudlackova P, Vokurka M, Krijt J, Melkova Z (2009) The effect of nitric oxide on vaccinia virus-encoded ribonucleotide reductase. Nitric Oxide 20:114-121
38. Gort AS, Imlay JA (1998) Balance between endogenous superoxide stress and antioxidant defenses. J Bacteriol 180:1402-1410
39. Grzesiuk E, Gozdek A, Tudek B (2001) Contribution of E. coli AlkA, TagA glycosylases and UvrABC-excinuclease in MMS mutagenesis. Mutat Res 480-481:77-84
40. Gupta S, Chatterji D (2005) Stress responses in mycobacteria. IUBMB Life 57:149-159
41. Gutierrez MG, Vazquez CL, Munafo DB, Zoppino FC, Beron W, Rabinovitch M, Colombo MI (2005) Autophagy induction favours the generation and maturation of the Coxiella -replicative vacuoles. Cell Microbiol 7:981-993
42. Hackstadt T (1986) Antigenic variation in the phase I lipopolysaccharide of Coxiella burnetii isolates. Infect Immun 52:337-340
43. Hackstadt T, Williams JC (1981) Biochemical stratagem for obligate parasitism of eukaryotic cells by Coxiella burnetii . Proc Natl Acad Sci USA 78:3240-3244
44. Hassett DJ, Cohen MS (1989) Bacterial adaptation to oxidative stress: implications for pathogenesis and interaction with phagocytic cells. FASEB J 3:2574-2582
45. Heinzen RA, Frazier ME, mallavia LP (1990) Nucleotide sequence of Coxiella burnetii superoxide dismutase. Nucleic Acids Res 18:6437
46. Heinzen RA, Frazier ME, mallavia LP (1992) Coxiella burnetii superoxide dismutase gene: cloning, sequencing, and expression in Escherichia coli . Infect Immun 60:3814-3823
47. Heinzen RA, Scidmore ma, Rockey DD, Hackstadt T (1996) Differential interaction with endocytic and exocytic pathways distinguish parasitophorous vacuoles of Coxiella burnetii and Chlamydia trachomatis . Infect Immun 64:796-809
48. Hendrix LR, Samuel JE, mallavia LP (1991) Differentiation of Coxiella burnetii isolates by analysis of restriction-endonuclease-digested DNA separated by SDS-PAGE. J Gen Microbiol 137:269-276
49. Hicks LD, Raghavan R, Battisti JM, Minnick MF (2010) A DNA-binding peroxiredoxin of Coxiella burnetii is involved in countering oxidative stress during exponential-phase growth. J Bacteriol 192:2077-2084
50. Hill J, Samuel JE (2010) Coxiella burnetii acid phosphatase: inhibiting the release of reactive oxygen intermediates in polymorphonuclear leukocytes. Infect Immun 79(1):414-420
51. Hillas PJ, del Alba FS, Oyarzabal J, Wilks A, Ortiz De Montellano PR (2000) The AhpC and AhpD antioxidant defense system of Mycobacterium tuberculosis . J Biol Chem 275:18801-18809
52. Hisert KB, Kirksey ma, Gomez JE, Sousa AO, Cox JS, Jacobs WR Jr, Nathan CF, McKinney JD (2004) Identi fication of Mycobacterium tuberculosis counterimmune (cim) mutants in immunode ficient mice by differential screening. Infect Immun 72:5315-5321
53. Howe D, mallavia LP (1999) Coxiella burnetii infection increases transferrin receptors on J774A. 1 cells. Infect Immun 67:3236-3241
54. Howe D, mallavia LP (2000) Coxiella burnetii exhibits morphological change and delays phagolysosomal fusion after internalization by J774A.1 cells. Infect Immun 68:3815-3821
55. Howe D, Barrows LF, Lindstrom NM, Heinzen RA (2002) Nitric oxide inhibits Coxiella burnetii replication and parasitophorous vacuole maturation. Infect Immun 70:5140-5147
56. Hubber A, Roy CR (2010) Modulation of host cell function by Legionella pneumophila type IV effectors. Annu Rev Cell Dev Biol 26:261-283
57. Imlay JA (2008) Cellular defenses against superoxide and hydrogen peroxide. Annu Rev Biochem 77:755-776
58. Imlay JA, Linn S (1988) DNA damage and oxygen radical toxicity. Science 240:1302-1309
59. Imlay JA, Chin SM, Linn S (1988) Toxic DNA damage by hydrogen peroxide through the Fenton reaction in vivo and in vitro. Science 240:640-642
60. Jones SA, Chowdhury FZ, Fabich AJ, Anderson A, Schreiner DM, House AL, Autieri SM, Leatham MP, Lins JJ, Jorgensen M, Cohen PS, Conway T (2007) Respiration of Escherichia coli in the mouse intestine. Infect Immun 75:4891-4899
61. Juedes MJ, Wogan GN (1996) Peroxynitrite-induced mutation spectra of pSP189 following replication in bacteria and in human cells. Mutat Res 349:51-61
62. Kana BD, Weinstein EA, Avarbock D, Dawes SS, Rubin H, Mizrahi V (2001) Characterization of the cydAB -encoded cytochrome bd oxidase from Mycobacterium smegmatis . J Bacteriol 183:7076-7086
63. Korshunov SS, Imlay JA (2002) A potential role for periplasmic superoxide dismutase in blocking the penetration of external superoxide into the cytosol of Gram-negative bacteria. Mol Microbiol 43:95-106
64. Kowalczykowski SC, Dixon DA, Eggleston AK, Lauder SD, Rehrauer WM (1994) Biochemistry of homologous recombination in Escherichia coli . Microbiol Rev 58:401-465
65. Leblanc JJ, Davidson RJ, Hoffman PS (2006) Compensatory functions of two alkyl hydroperoxide reductases in the oxidative defense system of Legionella pneumophila . J Bacteriol 188:6235-6244
66. Leblanc JJ, Brassinga AK, Ewann F, Davidson RJ, Hoffman PS (2008) An ortholog of OxyR in Legionella pneumophila is expressed postexponentially and negatively regulates the alkyl hydroperoxide reductase ( ahpC2D ) operon. J Bacteriol 190:3444-3455
67. Li YP, Curley G, Lopez M, Chavez M, Glew R, Aragon A, Kumar H, Baca OG (1996) Proteintyrosine phosphatase activity of Coxiella burnetii that inhibits human neutrophils. Acta Virol 40:263-272
68. Lindgren H, Stenmark S, Chen W, Tarnvik A, Sjostedt A (2004) Distinct roles of reactive nitrogen and oxygen species to control infection with the facultative intracellular bacterium Francisella tularensis . Infect Immun 72:7172-7182
69. masse E, Salvail H, Desnoyers G, Arguin M (2007) Small RNAs controlling iron metabolism. Curr Opin Microbiol 10:140-145
70. master SS, Springer B, Sander P, Boettger EC, Deretic V, Timmins GS (2002) Oxidative stress response genes in Mycobacterium tuberculosis: role of ahpC in resistance to peroxynitrite and stage-speci fic survival in macrophages. Microbiology 148:3139-3144
71. maurin M, Raoult D (1999) Q fever. Clin Microbiol Rev 12:518-553
72. mayer B, Hemmens B (1997) Biosynthesis and action of nitric oxide in mammalian cells. Trends Biochem Sci 22:477-481
73. McCaul TF, Williams JC (1981) Developmental cycle of Coxiella burnetii: structure and morphogenesis of vegetative and sporogenic differentiations. J Bacteriol 147:1063-1076
74. Mertens K, Lantsheer L, Ennis DG, Samuel JE (2008) Constitutive SOS expression and damageinducible AddAB-mediated recombinational repair systems for Coxiella burnetii as potential adaptations for survival within macrophages. Mol Microbiol 69:1411-1426
75. Mongkolsuk S, Helmann JD (2002) Regulation of inducible peroxide stress responses. Mol Microbiol 45:9-15
76. Nathan C, Shiloh MU (2000) Reactive oxygen and nitrogen intermediates in the relationship between mammalian hosts and microbial pathogens. Proc Natl Acad Sci USA 97:8841-8848
77. Ohno Y, Hirai K, Kanoh T, Uchino H, Ogawa K (1982) Subcellular localization of H2O2 production in human neutrophils stimulated with particles and an effect of cytochalasin-B on the cells. Blood 60:253-260
78. Omsland A, Cockrell DC, Fischer ER, Heinzen RA (2008) Sustained axenic metabolic activity by the obligate intracellular bacterium Coxiella burnetii . J Bacteriol 190:3203-3212
79. Omsland A, Cockrell DC, Howe D, Fischer ER, Virtaneva K, Sturdevant DE, Porcella SF, Heinzen RA (2009) Host cell-free growth of the Q fever bacterium Coxiella burnetii . Proc Natl Acad Sci USA 106:4430-4434
80. Ouellet H, Ouellet Y, Richard C, Labarre M, Wittenberg B, Wittenberg J, Guertin M (2002) Truncated hemoglobin HbN protects Mycobacterium bovis from nitric oxide. Proc Natl Acad Sci USA 99:5902-5907
81. Pagan-Ramos E, master SS, Pritchett CL, Reimschuessel R, Trucksis M, Timmins GS, Deretic V (2006) Molecular and physiological effects of mycobacterial oxyR inactivation. J Bacteriol 188:2674-2680
82. Park SH, Lee HW, Cao W (2010) Screening of nitrosative stress resistance genes in Coxiella burnetii: involvement of nucleotide excision repair. Microb Pathog 49:323-329
83. Pollock JD, Williams DA, Gifford ma, Li LL, Du X, Fisherman J, Orkin SH, Doerschuk CM, Dinauer MC (1995) Mouse model of X-linked chronic granulomatous disease, an inherited defect in phagocyte superoxide production. Nat Genet 9:202-209
84. Poole LB (2005) Bacterial defenses against oxidants: mechanistic features of cysteine-based peroxidases and their flavoprotein reductases. Arch Biochem Biophys 433:240-254
85. Posey JE, Gherardini FC (2000) Lack of a role for iron in the Lyme disease pathogen. Science 288:1651-1653
86. Qiu H, Kuolee R, Harris G, Chen W (2009) Role of NADPH phagocyte oxidase in host defense against acute respiratory Acinetobacter baumannii infection in mice. Infect Immun 77:1015-1021
87. Rosner JL, Storz G (1997) Regulation of bacterial responses to oxidative stress. Curr Top Cell Regul 35:163-177
88. Roux CM, Booth NJ, Bellaire BH, Gee JM, Roop RM 2nd, Kovach ME, Tsolis RM, Elzer PH, Ennis DG (2006) RecA and RadA proteins of Brucella abortus do not perform overlapping protective DNA repair functions following oxidative burst. J Bacteriol 188:5187-5195
89. Sadosky AB, Wilson JW, Steinman HM, Shuman HA (1994) The iron superoxide dismutase of Legionella pneumophila is essential for viability. J Bacteriol 176:3790-3799
90. Saha AK, Dowling JN, Lamarco KL, Das S, Remaley AT, Olomu N, Pope MT, Glew RH (1985) Properties of an acid phosphatase from Legionella micdadei which blocks superoxide anion production by human neutrophils. Arch Biochem Biophys 243:150-160
91. Saha AK, Dowling JN, Pasculle AW, Glew RH (1988) Legionella micdadei phosphatase catalyzes the hydrolysis of phosphatidylinositol 4,5-bisphosphate in human neutrophils. Arch Biochem Biophys 265:94-104
92. Samuel JE, Frazier ME, mallavia LP (1985) Correlation of plasmid type and disease caused by Coxiella burnetii . Infect Immun 49:775-779
93. Sauer JD, Shannon JG, Howe D, Hayes SF, Swanson MS, Heinzen RA (2005) Speci ficity of Legionella pneumophila and Coxiella burnetii vacuoles and versatility of Legionella pneumophila revealed by coinfection. Infect Immun 73:4494-4504
94. Schell ma (1993) Molecular biology of the LysR family of transcriptional regulators. Annu Rev Microbiol 47:597-626
95. Schellhorn HE (1995) Regulation of hydroperoxidase (catalase) expression in Escherichia coli . FEMS Microbiol Lett 131:113-119
96. Sekeyova Z, Roux V, Raoult D (1999) Intraspecies diversity of Coxiella burnetii as revealed by com1 and mucZ sequence comparison. FEMS Microbiol Lett 180:61-67
97. Sexton JA, Vogel JP (2002) Type IVB secretion by intracellular pathogens. Traf fic 3:178-185
98. Siemsen DW, Kirpotina LN, Jutila ma, Quinn MT (2009) Inhibition of the human neutrophil NADPH oxidase by Coxiella burnetii . Microbes Infect 11:671-679
99. St John G, Steinman HM (1996) Periplasmic copper-zinc superoxide dismutase of Legionella pneumophila: role in stationary-phase survival. J Bacteriol 178:1578-1584
100. Stein A, Saunders NA, Taylor AG, Raoult D (1993) Phylogenic homogeneity of Coxiella burnetii strains as determinated by 16S ribosomal RNA sequencing. FEMS Microbiol Lett 113: 339-344
101. Stenger S, Donhauser N, Thuring H, Rollinghoff M, Bogdan C (1996) Reactivation of latent leishmaniasis by inhibition of inducible nitric oxide synthase. J Exp Med 183:1501-1514
102. Stoenner HG, Lackman DB (1960) The biologic properties of Coxiella burnetii isolated from rodents collected in Utah. Am J Hyg 71:45-51
103. Storz G, Imlay JA (1999) Oxidative stress. Curr Opin Microbiol 2:188-194
104. Tanaka K, Handel K, Loewen PC, Takahashi H (1997) Identi fication and analysis of the rpoS - dependent promoter of katE , encoding catalase HPII in Escherichia coli . Biochim Biophys Acta 1352:161-166
105. Tautz L, Bruckner S, Sareth S, Alonso A, Bogetz J, Bottini N, Pellecchia M, Mustelin T (2005) Inhibition of Yersinia tyrosine phosphatase by furanyl salicylate compounds. J Biol Chem 280:9400-9408
106. Thiemermann C, Vane J (1990) Inhibition of nitric oxide synthesis reduces the hypotension induced by bacterial lipopolysaccharides in the rat in vivo. Eur J Pharmacol 182:591-595
107. Tlili A, Dupre-Crochet S, Erard M, Nubetae O (2011) Kinetic analysis of phagosomal production of reactive oxygen species. Free Radic Biol Med 50(3):438-447
108. Touati D (2000) Iron and oxidative stress in bacteria. Arch Biochem Biophys 373:1-6
109. Vazquez-Torres A, Xu Y, Jones-Carson J, Holden DW, Lucia SM, Dinauer MC, mastroeni P, Fang FC (2000) Salmonella pathogenicity island 2-dependent evasion of the phagocyte NADPH oxidase. Science 287:1655-1658
110. Via LE, Lin PL, Ray SM, Carrillo J, Allen SS, Eum SY, Taylor K, Klein E, manjunatha U, Gonzales J, Lee EG, Park SK, Raleigh JA, Cho SN, McMurray DN, Flynn JL, Barry CE 3rd (2008) Tuberculous granulomas are hypoxic in guinea pigs, rabbits, and nonhuman primates. Infect Immun 76:2333-2340
111. Vila-Del Sol V, Diaz-Munoz MD, Fresno M (2007) Requirement of tumor necrosis factor alpha and nuclear factor-kappaB in the induction by IFN-gamma of inducible nitric oxide synthase in macrophages. J Leukoc Biol 81:272-283
112. Voth DE, Heinzen RA (2009) Coxiella type IV secretion and cellular microbiology. Curr Opin Microbiol 12(1):74-80
113. Wang G, Alamuri P, Humayun MZ, Taylor DE, maier RJ (2005) The Helicobacter pylori MutS protein confers protection from oxidative DNA damage. Mol Microbiol 58:166-176
114. Wang G, Alamuri P, maier RJ (2006) The diverse antioxidant systems of Helicobacter pylori . Mol Microbiol 61:847-860
115. Webb JL, Harvey MW, Holden DW, Evans TJ (2001) macrophage nitric oxide synthase associates with cortical actin but is not recruited to phagosomes. Infect Immun 69:6391-6400
116. Weisburg WG, Dobson ME, Samuel JE, Dasch GA, mallavia LP, Baca O, mandelco L, Sechrest JE, Weiss E, Woese CR (1989) Phylogenetic diversity of the Rickettsiae . J Bacteriol 171:4202-4206
117. Wink DA, Kasprzak KS, maragos CM, Elespuru RK, Misra M, Dunams TM, Cebula TA, Koch WH, Andrews AW, Allen JS et al (1991) DNA deaminating ability and genotoxicity of nitric oxide and its progenitors. Science 254:1001-1003