Nitric oxide reactivities of the two globins of the foodborne pathogen Campylobacter jejuni: Roles in protection from nitrosative stress and analysis of potential reductants

Nitric Oxide - Biology and Chemistry

Volumn 34, Issue , 2013, Pages 65-75

  Tinajero Trejo, Mariana ^a   Vreugdenhil, Angie ^b,c   Sedelnikova, Svetlana E ^a   Davidge, Kelly S ^a,d   Poole, Robert K ^a  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

^b UNIVERSITY OF AMSTERDAM   (Netherlands)

^c ROSWELL PARK CANCER INSTITUTE   (United States)

^d UNIVERSITY OF NOTTINGHAM   (United Kingdom)

Author keywords

Bacterial haemoglobin; Campylobacter jejuni; Escherichia coli; Heterologous expression; Nitrosative stress; Reductase

Indexed keywords

ARABINOSE; CELL EXTRACT; FLAVORUBREDOXIN REDUCTASE; HEMOGLOBIN; HYDROGEN PEROXIDE; NITRIC OXIDE; OXIDOREDUCTASE; REACTIVE NITROGEN SPECIES; REDUCING AGENT; SINGLE DOMAIN HEMOGLOBIN; TRUNCATED HEMOGLOBIN; UBIQUINONE; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GROWTH; BACTERIAL MEMBRANE; BACTERIAL STRAIN; BACTERIUM CULTURE; BACTERIUM MUTANT; BREATHING RATE; CAMPYLOBACTER JEJUNI; CELL MUTANT; CELL SUSPENSION; DELETION MUTANT; DETOXIFICATION; ELECTRON TRANSPORT; ESCHERICHIA COLI; GENE DELETION; GENOTYPE; HETEROLOGOUS EXPRESSION; IMMUNOBLOTTING; NITROSATIVE STRESS; NONHUMAN; OXIDATIVE STRESS; OXYGEN CONSUMPTION; PHENOTYPE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN PURIFICATION; RESPIRATORY CHAIN; UPREGULATION;

BACTERIA (MICROORGANISMS); CAMPYLOBACTER; CAMPYLOBACTER JEJUNI; ESCHERICHIA COLI;

(Z)-1-[2-(2-AMINOETHYL)-N-(2-AMMONIOETHYL)AMINO]DIAZEN-1-IUM-1,2-DIOLATE; 1-(HYDROXYL-NNO-AZOXY)-L-PROLINE; BACTERIAL HAEMOGLOBIN; CAMPYLOBACTER JEJUNI; CAMPYLOBACTER SINGLE DOMAIN HAEMOGLOBIN; CAMPYLOBACTER TRUNCATED HAEMOGLOBIN; CGB; CTB; DETA NONOATE; E. COLI FLAVORUBREDOXIN PROTEIN; E. COLI FLAVORUBREDOXIN REDUCTASE; ESCHERICHIA COLI; FLAVOHAEMOGLOBIN; GSNO; HETEROLOGOUS EXPRESSION; HMP; NITRIC OXIDE SYNTHASE; NITROSATIVE STRESS; NITROSATIVE STRESS SENSING REGULATOR; NORR; NORV; NORW; NOS; NSSR; PROLI NONOATE; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN SPECIES; REDUCTASE; RNS; ROS; S-NITROSOGLUTATHIONE; TRANSCRIPTIONAL REGULATOR OF NORVW GENES IN E. COLI;

ANAEROBIOSIS; BACTERIAL PROTEINS; CAMPYLOBACTER JEJUNI; DIHYDROPTERIDINE REDUCTASE; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; HEMEPROTEINS; NAD; NADH, NADPH OXIDOREDUCTASES; NITRIC OXIDE; NITROSATION; OXIDATION-REDUCTION; S-NITROSOGLUTATHIONE; STRESS, PHYSIOLOGICAL; TRANS-ACTIVATORS; TRUNCATED HEMOGLOBINS;

EID: 84885179793     PISSN: 10898603     EISSN: 10898611     Source Type: Journal    
DOI: 10.1016/j.niox.2013.06.002     Document Type: Article

References (77)

1. P.R. Gardner, A.M. Gardner, L.A. Martin, A.L. Salzman, Nitric oxide dioxygenase: an enzymic function for flavohemoglobin, Proc. Natl. Acad. Sci. U.S.A. 95 (1998) 10378-10383. (Pubitemid 28413075)
2. P.R. Gardner, A.M. Gardner, L.A. Martin, Y. Dou, T. Li, J.S. Olson, H. Zhu, A.F. Riggs, Nitric-oxide dioxygenase activity and function of flavohemoglobins. sensitivity to nitric oxide and carbon monoxide inhibition, J. Biol. Chem. 275 (2000) 31581-31587.
3. P.R. Gardner, A.M. Gardner, W.T. Brashear, T. Suzuki, A.N. Hvitved, K.D. Setchell, J.S. Olson, Hemoglobins dioxygenate nitric oxide with high fidelity, J. Inorg. Biochem. 100 (2006) 542-550.
4. M.T. Forrester, M.W. Foster, Protection from nitrosative stress: a central role for microbial flavohemoglobin, Free Radic. Biol. Med. 52 (2012) 1620-1633.
5. A. Hausladen, A.J. Gow, J.S. Stamler, Nitrosative stress: metabolic pathway involving the flavohemoglobin, Proc. Natl. Acad. Sci. U.S.A. 95 (1998) 14100-14105. (Pubitemid 28549327)
6. A. Hausladen, A. Gow, J.S. Stamler, Flavohemoglobin denitrosylase catalyzes the reaction of a nitroxyl equivalent with molecular oxygen, Proc. Natl. Acad. Sci. U.S.A. 98 (2001) 10108-10112. (Pubitemid 32802982)
7. P.R. Gardner, G. Costantino, A.L. Salzman, Constitutive and adaptive detoxification of nitric oxide in Escherichia coli. Role of nitric-oxide dioxygenase in the protection of aconitase, J. Biol. Chem. 273 (1998) 26528-26533. (Pubitemid 28471662)
8. E. Hernandez-Urzua, C.E. Mills, G.P. White, M.L. Contreras-Zentella, E. Escamilla, S.G. Vasudevan, J. Membrillo-Hernandez, R.K. Poole, Flavohemoglobin Hmp, but not its individual domains, confers protection from respiratory inhibition by nitric oxide in Escherichia coli, J. Biol. Chem. 278 (2003) 34975-34982. (Pubitemid 37102258)
9. A.M. Gardner, P.R. Gardner, Flavohemoglobin detoxifies nitric oxide in aerobic, but not anaerobic, Escherichia coli. Evidence for a novel inducible anaerobic nitric oxide-scavenging activity, J. Biol. Chem. 277 (2002) 8166-8171. (Pubitemid 34968271)
10. M.I. Hutchings, N. Mandhana, S. Spiro, The NorR protein of Escherichia coli activates expression of the flavorubredoxin gene norV in response to reactive nitrogen species, J. Bacteriol. 184 (2002) 4640-4643. (Pubitemid 34832595)
11. C.E. Mills, S. Sedelnikova, B. Soballe, M.N. Hughes, R.K. Poole, Escherichia coli flavohaemoglobin (Hmp) with equistoichiometric FAD and haem contents has a low affinity for dioxygen in the absence or presence of nitric oxide, Biochem. J. 353 (2001) 207-213. (Pubitemid 32096927)
12. C.R. Friedman, J. Neimann, H.C. Wegener, R.V. Tauxe, Epidemiology of Campylobacter jejuni infections in the United States and other industrialized nations, in: I. Nachamkin, M.J. Blaser (Eds.), Campylobacter, ASM Press, Washington, D.C., 2000, pp. 121-138.
13. J.O. Lundberg, E. Weitzberg, J.A. Cole, N. Benjamin, Nitrate, bacteria and human health, Nat. Rev. Microbiol. 2 (2004) 593-602. (Pubitemid 39200033)
14. K.T. Elvers, G. Wu, N.J. Gilberthorpe, R.K. Poole, S.F. Park, Role of an inducible single-domain hemoglobin in mediating resistance to nitric oxide and nitrosative stress in Campylobacter jejuni and Campylobacter coli, J. Bacteriol. 186 (2004) 5332-5341. (Pubitemid 39038135)
15. C. Lu, M. Mukai, Y. Lin, G. Wu, R.K. Poole, S.R. Yeh, Structural and functional properties of a single domain hemoglobin from the food-borne pathogen Campylobacter jejuni, J. Biol. Chem. 282 (2007) 25917-25928. (Pubitemid 47372797)
16. M. Shepherd, P.V. Bernhardt, R.K. Poole, Globin-mediated nitric oxide detoxification in the foodborne pathogenic bacterium Campylobacter jejuni proceeds via a dioxygenase or denitrosylase mechanism, Nitric Oxide 25 (2011) 229-233.
17. K.T. Elvers, S.M. Turner, L.M. Wainwright, G. Marsden, J. Hinds, J.A. Cole, R.K. Poole, C.W. Penn, S.F. Park, 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. 57 (2005) 735-750. (Pubitemid 41025956)
18. J.B. Wittenberg, M. Bolognesi, B.A. Wittenberg, M. Guertin, Truncated hemoglobins: a new family of hemoglobins widely distributed in bacteria, unicellular eukaryotes, and plants, J. Biol. Chem. 277 (2002) 871-874. (Pubitemid 34968827)
19. C. Lu, T. Egawa, L.M. Wainwright, R.K. Poole, S.R. Yeh, Structural and functional properties of a truncated hemoglobin from a food-borne pathogen Campylobacter jejuni, J. Biol. Chem. 282 (2007) 13627-13636. (Pubitemid 47100515)
20. L.M. Wainwright, Y. Wang, S.F. Park, S.R. Yeh, R.K. Poole, Purification and spectroscopic characterization of Ctb, a group III truncated hemoglobin implicated in oxygen metabolism in the food-borne pathogen Campylobacter jejuni, Biochemistry 45 (2006) 6003-6011. (Pubitemid 43727092)
21. A. Bolli, C. Ciaccio, M. Coletta, M. Nardini, M. Bolognesi, A. Pesce, M. Guertin, P. Visca, P. Ascenzi, Ferrous Campylobacter jejuni truncated hemoglobin P displays an extremely high reactivity for cyanide - a comparative study, FEBS J. 275 (2008) 633-645. (Pubitemid 351160957)
22. M. Nardini, A. Pesce, M. Labarre, C. Richard, A. Bolli, P. Ascenzi, M. Guertin, M. Bolognesi, Structural determinants in the group III truncated hemoglobin from Campylobacter jejuni, J. Biol. Chem. 281 (2006) 37803-37812. (Pubitemid 46043310)
23. A.D. Frey, J. Farres, C.J. Bollinger, P.T. Kallio, Bacterial hemoglobins and flavohemoglobins for alleviation of nitrosative stress in Escherichia coli, Appl. Environ. Microbiol. 68 (2002) 4835-4840. (Pubitemid 35154789)
24. C. Avila-Ramirez, M. Tinajero-Trejo, K.S. Davidge, C.E. Monk, D.J. Kelly, R.K. Poole, Do Globins in microaerophilic Campylobacter jejuni confer nitrosative stress tolerance under oxygen limitation?, Antioxid Redox Signal. 18 (2013) 424-431.
25. L. Davis, K. Young, V. DiRita, Genetic manipulation of Campylobacter jejuni, Current protocols in microbiology (2008). 8A 2 1-8A 2 17, Chapter 8.
26. C.E. Monk, B.M. Pearson, F. Mulholland, H.K. Smith, R.K. Poole, Oxygen- and NssR-dependent globin expression and enhanced iron acquisition in the response of Campylobacter to nitrosative stress, J. Biol. Chem. 283 (2008) 28413-28425.
27. J. Parkhill, B.W. Wren, K. Mungall, J.M. Ketley, C. Churcher, D. Basham, T. Chillingworth, R.M. Davies, T. Feltwell, S. Holroyd, K. Jagels, A.V. Karlyshev, S. Moule, M.J. Pallen, C.W. Penn, M.A. Quail, M.A. Rajandream, K.M. Rutherford, A.H.M. vanVliet, S. Whitehead, B.G. Barrell, The genome sequence of the foodborne pathogen Campylobacter jejuni reveals hypervariable sequences, Nature 403 (2000) 665-668. (Pubitemid 30104008)
28. J.L. Pickford, L. Wainwright, G. Wu, R.K. Poole, Expression and purification of Cgb and Ctb, the NO-inducible globins of the foodborne bacterial pathogen C. jejuni, Methods Enzymol. 436 (2008) 289-302.
29. R.K. Poole, H.D. Williams, J.A. Downie, F. Gibson, Mutations affecting the cytochrome d-containing oxidase complex of Escherichia coli K12: identification and mapping of a fourth locus, cydD, J. Gen. Microbiol. 135 (1989) 1865-1874.
30. L.M. Wainwright, K.T. Elvers, S.F. Park, R.K. Poole, A truncated haemoglobin implicated in oxygen metabolism by the microaerophilic food-borne pathogen Campylobacter jejuni, Microbiology 151 (2005) 4079-4091. (Pubitemid 41829988)
31. T. Baba, T. Ara, M. Hasegawa, Y. Takai, Y. Okumura, M. Baba, K.A. Datsenko, M. Tomita, B.L. Wanner, H. Mori, Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection, Mol. Syst. Biol. 2 (2006) (2006) 0008.
32. K.A. Datsenko, B.L. Wanner, One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products, Proc. Natl. Acad. Sci. U.S.A. 97 (2000) 6640-6645. (Pubitemid 30412767)
33. A.M. Gardner, R.A. Helmick, P.R. Gardner, Flavorubredoxin, an inducible catalyst for nitric oxide reduction and detoxification in Escherichia coli, J. Biol. Chem. 277 (2002) 8172-8177. (Pubitemid 34968272)
34. M. Bekker, S. de Vries, A. Ter Beek, K.J. Hellingwerf, M.J. de Mattos, Respiration of Escherichia coli can be fully uncoupled via the nonelectrogenic terminal cytochrome bd-II oxidase, J. Bacteriol. 191 (2009) 5510-5517.
35. A.I. Shestopalov, A.V. Bogachev, R.A. Murtazina, M.B. Viryasov, V.P. Skulachev, Aeration-dependent changes in composition of the quinone pool in Escherichia coli. Evidence of post-transcriptional regulation of the quinone biosynthesis, FEBS Lett. 404 (1997) 272-274. (Pubitemid 27113466)
36. R.K. Poole, B.A. Haddock, Energy-linked reduction of nicotinamide- adenine dinucleotide in membranes derived from normal and various respiratory-deficient mutant strains of Escherichia coli K12, Biochem. J. 144 (1974) 77-85.
37. M.A.K. Markwell, S.M. Haas, L.L. Bieber, N.E. Tolbert, A modification of the Lowry procedure to simplify protein determination in membrane and lipoprotein samples, Anal. Biochem. 87 (1978) 206-210. (Pubitemid 9050428)
38. H. Corker, R.K. Poole, Nitric oxide formation by Escherichia coli. Dependence on nitrite reductase, the NO-sensing regulator Fnr, and flavohemoglobin Hmp, J. Biol. Chem. 278 (2003) 31584-31592. (Pubitemid 37048336)
39. J. Membrillo-Hernandez, N. Ioannidis, R.K. Poole, The flavohaemoglobin (HMP) of Escherichia coli generates superoxide in vitro and causes oxidative stress in vivo, FEBS Lett. 382 (1996) 141-144. (Pubitemid 26092947)
40. G. Wu, H. Corker, Y. Orii, R.K. Poole, Escherichia coli Hmp, an "oxygen-binding flavohaemoprotein", produces superoxide anion and self-destructs, Arch. Microbiol. 182 (2004) 193-203. (Pubitemid 39361996)
41. R. Hilton, R. Armstrong, Stat Note 16. Fitting a regression line to data, Microbiologist, (2009) 40-42.
42. P.T. Kallio, D.J. Kim, P.S. Tsai, J.E. Bailey, Intracellular expression of Vitreoscilla hemoglobin alters Escherichia coli energy metabolism under oxygen-limited conditions, Eur. J. Biochem. 219 (1994) 201-208. (Pubitemid 24053634)
43. C.Y. Lu, T. Egawa, L.M. Wainwright, R.K. Poole, S.-R. Yeh, Structural and functional properties of a truncated hemoglobin from a food-borne pathogen Campylobacter jejuni, J. Biol. Chem. 282 (2007) 13627-13636. (Pubitemid 47100515)
44. N.J. Gilberthorpe, M.E. Lee, T.M. Stevanin, R.C. Read, R.K. Poole, NsrR: a key regulator circumventing Salmonella enterica serovar Typhimurium oxidative and nitrosative stress in vitro and in IFN-gamma-stimulated J774.2 macrophages, Microbiology 153 (2007) 1756-1771. (Pubitemid 46952506)
45. S. McLean, L.A.H. Bowman, R.K. Poole, Peroxynitrite stress is exacerbated by flavohaemoglobin-derived oxidative stress in Salmonella Typhimurium and is relieved by nitric oxide, Microbiology 156 (2010) 3556-3565.
46. C. Lu, M. Mukai, Y. Lin, G. Wu, R.K. Poole, S.-R. Yeh, Structural and functional properties of a single-domain hemoglobin from the food-borne pathogen Campylobacter jejuni, J. Biol. Chem. 282 (2007) 25917-25928. (Pubitemid 47372797)
47. R.J. Jackson, K.T. Elvers, L.J. Lee, M.D. Gidley, L.M. Wainwright, J. Lightfoot, S.F. Park, R.K. Poole, Oxygen reactivity of both respiratory oxidases in Campylobacter jejuni: the cydAB genes encode a cyanide-resistant, lowaffinity oxidase that is not of the cytochrome bd type, J. Bacteriol. 189 (2007) 1604-1615. (Pubitemid 46446122)
48. S.O. Kim, Y. Orii, D. Lloyd, M.N. Hughes, R.K. Poole, Anoxic function for the Escherichia coli flavohaemoglobin (Hmp): reversible binding of nitric oxide and reduction to nitrous oxide, FEBS Lett. 445 (1999) 389-394. (Pubitemid 29117250)
49. M.C. Justino, J.B. Vicente, M. Teixeira, L.M. Saraiva, New genes implicated in the protection of anaerobically grown Escherichia coli against nitric oxide, J. Biol. Chem. 280 (2005) 2636-2643. (Pubitemid 40189367)
50. S. Spiro, Nitric oxide-sensing mechanisms in Escherichia coli, Biochem. Soc. Trans. 34 (2006) 200-202. (Pubitemid 43235572)
51. A.M. Gardner, C.R. Gessner, P.R. Gardner, Regulation of the nitric oxide reduction operon (norRVW) in Escherichia coli. Role of NorR and sigma54 in the nitric oxide stress response, J. Biol. Chem. 278 (2003) 10081-10086. (Pubitemid 36800264)
52. A. Giuffre, T. Moschetti, B. Vallone, M. Brunori, Is neuroglobin a signal transducer?, IUBMB Life 60 (2008) 410-413
53. G.B. Cox, J.A. Downie, Isolation and characterization of mutants of Escherichia coli K-12 affected in oxidative phosphorylation of quinone biosynthesis, Methods Enzymol. 56 (1979) 106-117.
54. R.K. Poole, W.J. Ingledew, Pathways of electrons to oxygen, in: Escherichia coli and Salmonella typhimurium, Cellular and Molecular Biology, American Society for Microbiology, Washington D. C., 1987.
55. K.W. Park, K.J. Kim, A.J. Howard, B.C. Stark, D.A. Webster, Vitreoscilla hemoglobin binds to subunit I of cytochrome bo ubiquinol oxidases, J. Biol. Chem. 277 (2002) 33334-33337. (Pubitemid 34984855)
56. R. Pathania, N.K. Navani, G. Rajamohan, K.L. Dikshit, Mycobacterium tuberculosis hemoglobin HbO associates with membranes and stimulates cellular respiration of recombinant Escherichia coli, J. Biol. Chem. 277 (2002) 15293-15302. (Pubitemid 34967790)
57. R.P. Dikshit, K.L. Dikshit, Y.X. Liu, D.A. Webster, The bacterial hemoglobin from Vitreoscilla can support the aerobic growth of Escherichia coli lacking terminal oxidases, Arch. Biochem. Biophys. 293 (1992) 241-245.
58. S. Korshunov, J.A. Imlay, Detection and quantification of superoxide formed within the periplasm of Escherichia coli, J. Bacteriol. 188 (2006) 6326-6334. (Pubitemid 44448575)
59. P. Sharma, M.J. Teixeira de Mattos, K.J. Hellingwerf, M. Bekker, On the function of the various quinone species in Escherichia coli, FEBS J. 279 (2012) 3364-3373.
60. K. Kita, K. Konishi, Y. Anraku, Purification and properties of two terminal oxidase complexes of Escherichia coli aerobic respiratory chain, Methods Enzymol. 126 (1986) 94-113.
61. G. Wu, H.D. Williams, M. Zamanian, F. Gibson, R.K. Poole, Isolation and characterization of Escherichia coli mutants affected in aerobic respiration: the cloning and nucleotide sequence of ubiG. Identification of an Sadenosylmethionine- binding motif in protein, RNA, and small-molecule methyltransferases, J. Gen. Microbiol. 138 (1992) 2101-2112.
62. G.H. Wu, H.D. Williams, F. Gibson, R.K. Poole, Mutants of Escherichia-coli affected in respiration - the cloning and nucleotide sequence of ubia, encoding the membrane-bound p-hydroxybenzoate - octaprenyltransferase, J. Gen. Microbiol. 139 (1993) 1795-1805. (Pubitemid 23258606)
63. M. Shepherd, V. Barynin, C. Lu, P.V. Bernhardt, G. Wu, S.R. Yeh, T. Egawa, S.E. Sedelnikova, D.W. Rice, J.L. Wilson, R.K. Poole, The single-domain globin from the pathogenic bacterium Campylobacter jejuni: novel D-helix conformation, proximal hydrogen bonding that influences ligand binding, and peroxidaselike redox properties, J. Biol. Chem. 285 (2010) 12747-12754.
64. C.Y. Lu, M. Mukai, Y. Lin, G.H. Wu, R.K. Poole, S.R. Yeh, Structural and functional properties of a single domain hemoglobin from the food-borne pathogen Campylobacter jejuni, J. Biol. Chem. 282 (2007) 25917-25928. (Pubitemid 47372797)
65. C.Y. Lu, Y. Lin, R.K. Poole, S.R. Yeh, Ligand binding properties of hemoglobin Cgb from the food-borne pathogen Campylobacter jejuni, Biophys. J. (2007). 382A-382A.
66. M.S. Pittman, K.T. Elvers, L. Lee, M.A. Jones, R.K. Poole, S.F. Park, D.J. Kelly, 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. 63 (2007) 575-590. (Pubitemid 46058941)
67. H.K. Smith, M. Shepherd, C. Monk, J. Green, R.K. Poole, The NO-responsive hemoglobins of Campylobacter jejuni: concerted responses of two globins to NO and evidence in vitro for globin regulation by the transcription factor NssR, Nitric Oxide 25 (2011) 234-241.
68. A. Lama, S. Pawaria, K.L. Dikshit, Oxygen binding and NO scavenging properties of truncated hemoglobin, HbN, of Mycobacterium smegmatis, FEBS Lett. 580 (2006) 4031-4041. (Pubitemid 44037563)
69. R. Pathania, N.K. Navani, A.M. Gardner, P.R. Gardner, K.L. Dikshit, Nitric oxide scavenging and detoxification by the Mycobacterium tuberculosis haemoglobin, HbN in Escherichia coli, Mol. Microbiol. 45 (2002) 1303-1314. (Pubitemid 35015354)
70. C. Avila-Ramirez, M. Tinajero-Trejo, K.S. Davidge, C.E. Monk, D.J. Kelly, R.K. Poole, Do Globins in Microaerophilic Campylobacter jejuni Confer Nitrosative Stress Tolerance Under Oxygen Limitation?, Antioxidants redox signaling (2012)
71. S.I. Liochev, A. Hausladen, W.F. Beyer, I. Fridovich, NADPH: ferredoxin oxidoreductase acts as a paraquat diaphorase and is a member of the SoxRS regulon, Proc. Natl. Acad. Sci. U.S.A. 91 (1994) 1328-1331. (Pubitemid 24059004)
72. F. Trandafir, D. Hoogewijs, F. Altieri, P. Cervo, K. Ramser, S. Van Doorslaer, J.R. Vanfleteren, L. Moens, S. Dewilde, Neuroglobin and cytoglobin as potential enzyme or substrate, Gene 398 (2007) 103-113. (Pubitemid 47068899)
73. I. Gusarov, M. Starodubtseva, Z.Q. Wang, L. McQuade, S.J. Lippard, D.J. Stuehr, E. Nudler, Bacterial nitric-oxide synthases operate without a dedicated redox partner, J. Biol. Chem. 283 (2008) 13140-13147.
74. A.J. Grant, C. Coward, M.A. Jones, C.A. Woodall, P.A. Barrow, D.J. Maskell, Signature-tagged transposon mutagenesis studies demonstrate the dynamic nature of cecal colonization of 2-week-old chickens by Campylobacter jejuni, Appl. Environ. Microbiol. 71 (2005) 8031-8041. (Pubitemid 41803926)
75. K.W. Ramandeep, M. Hwang, K.J. Raje, B.C. Kim, K.L. Stark, D.A. Dikshit, Webster, Vitreoscilla hemoglobin. Intracellular localization and binding to membranes, J. Biol. Chem. 276 (2001) 24781-24789.
76. F.R. Blattner, G. Plunkett 3rd, C.A. Bloch, N.T. Perna, V. Burland, M. Riley, J. Collado-Vides, J.D. Glasner, C.K. Rode, G.F. Mayhew, J. Gregor, N.W. Davis, H.A. Kirkpatrick, M.A. Goeden, D.J. Rose, B. Mau, Y. Shao, The complete genome sequence of Escherichia coli K-12, Science 277 (1997) 1453-1462. (Pubitemid 27449228)
77. S.G. Vasudevan, W.L.F. Armarego, D.C. Shaw, P.E. Lilley, N.E. Dixon, R.K. Poole, Isolation and nucleotide sequence of the hmp gene that encodes a haemoglobin-like protein in Escherichia coli K-12, Mol. Gen. Genet. 226 (1991) 49-58.