How Escherichia coli tolerates profuse hydrogen peroxide formation by a catabolic pathway

Journal of Bacteriology

Volumn 195, Issue 20, 2013, Pages 4569-4579

  Kumar, Sripriya Ravindra ^a,b   Imlay, James A ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARBON; CATALASE; GLUCOSE; HYDROGEN PEROXIDE; NITROGEN; PHENETHYLAMINE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE;

ARTICLE; AUTOOXIDATION; BACTERIAL GROWTH; CARBON SOURCE; CATABOLISM; CELL MEMBRANE; CELL STRESS; CYTOPLASM; ENZYME ACTIVITY; ESCHERICHIA COLI; EUKARYOTIC CELL; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; REGULON; STOICHIOMETRY;

CARBON; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; HYDROGEN PEROXIDE; MUTATION; NITROGEN; OXIDATION-REDUCTION; PHENETHYLAMINES; REGULON; REPRESSOR PROTEINS; STRESS, PHYSIOLOGICAL;

EID: 84885438576     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.00737-13     Document Type: Article

References (64)

1. Seaver LC, Imlay JA. 2004. Are respiratory enzymes the primary sources of intracellular hydrogen peroxide? J. Biol. Chem. 279:48742-48750.
2. Jang S, Imlay JA. 2007. Micromolar intracellular hydrogen peroxide disrupts metabolism by damaging iron-sulfur enzymes. J. Biol. Chem. 282:929-937.
3. Sobota JM, Imlay JA. 2011. Iron enzyme ribulose-5-phosphate 3-epimerase in Escherichia coli is rapidly damaged by hydrogen peroxide but can be protected by manganese. Proc. Natl. Acad. Sci. U. S. A. 108:5402-5407.
4. Anjem A, Imlay JA. 2012. Mononuclear iron enzymes are primary targets of hydrogen peroxide stress. J. Biol. Chem. 287:15544-15556.
5. - mutants of Escherichia coli. Proc. Natl. Acad. Sci. U. S. A. 102:9317-9322.
6. Massey V, Strickland S, Mayhew SG, Howell LG, Engel PC, Matthews RG, Schuman M, Sullivan PA. 1969. The production of superoxide anion radicals in the reaction of reduced flavins and flavoproteins with molecular oxygen. Biochem. Biophys. Res. Commun. 36:891-897.
7. Grinblat L, Sreider CM, Stoppani AO. 1991. Superoxide anion production by lipoamide dehydrogenase redox-cycling: effect of enzyme modifiers. Biochem. Int. 23:83-92.
8. Messner KR, Imlay JA. 1999. The identification of primary sites of superoxide and hydrogen peroxide formation in the aerobic respiratory chain and sulfite reductase complex of Escherichia coli. J. Biol. Chem. 274:10119-10128.
9. Messner KR, Imlay JA. 2002. Mechanism of superoxide and hydrogen peroxide formation by fumarate reductase, succinate dehydrogenase, and aspartate oxidase. J. Biol. Chem. 277:42563-42571.
10. Korshunov S, Imlay JA. 2010. Two sources of endogenous hydrogen peroxide in Escherichia coli. Mol. Microbiol. 75:1389-1401.
11. Seaver LC, Imlay JA. 2001. Alkyl hydroperoxide reductase is the primary scavenger of endogenous hydrogen peroxide in Escherichia coli. J. Bacteriol. 183:7173-7181.
12. Link AJ, Robison K, Church GM. 1997. Comparing the predicted and observed properties of proteins encoded in the genome of Escherichia coli K-12. Electrophoresis 18:1259-1313.
13. Imlay JA. 2013. The molecular mechanisms and physiological consequences of oxidative stress: lessons from a model bacterium. Nat. Rev. Microbiol. 11:443-454.
14. Rankin LD, Bodenmiller DM, Partridge JD, Nishino SF, Spain JC, Spiro S. 2008. Escherichia coli NsrR regulates a pathway for the oxidation of 3-nitrotyramine to 4-hydroxy-3-nitrophenylacetate. J. Bacteriol. 190: 6170-6177.
15. Hamana K, Niitsu M. 1999. Production of 2-phenylethylamine by decarboxylation of L-phenylalanine in alkaliphilic Bacillus cohnii. J. Gen. Appl. Microbiol. 45:149-153.
16. Galgano F, Suzzi G, Favati F, Caruso M, Martuscelli M, Gardini F, Salzano G. 2001. Biogenic amines during ripening in semicotto caprino cheese: role of enterococci. Int. J. Food Sci. Technol. 36:153-160.
17. González de Llano D, Cuesta P, Rodríguez A. 1998. Biogenic amine production by wild lactococcal and leuconostoc strains. Lett. Appl. Microbiol. 26:270-274.
18. Pessione E, Pessione A, Lamberti C, Coisson DJ, Riedel K, Mazzoli R, Giunta C. 2009. First evidence of a membrane-bound, tyramine and β-phenylethylamine producing tyrosine decarboxylase in Enterococcus faecalis: a two-dimensional electrophoresis proteomic study. Proteomics 9:2695-2710.
19. Kurtis CRP, Knowles PF, Parsons MR, Gaule TG, Phillips SEV, McPherson MJ. 2011. Tyrosine 381 in E. coli copper amine oxidase influences substrate specificity. J. Neural Transm. 118:1043-1053.
20. Parrott S, Jones S, Cooper RA. 1987. 2-Phenylethylamine catabolism of Escherichia coli K12. J. Gen. Microbiol. 133:347-351.
21. Ferrández A, Miñambres B, García B, Olivera ER, Luengo JM, García JL, Díaz E. 1998. Catabolism of phenylacetic acid in Escherichia coli. Characterization of a new aerobic hybrid pathway. J. Biol. Chem. 273: 25974-25986.
22. Teufel R, Mascaraque V, Ismail W, Voss M, Perera J, Eisenreich W, Haehnel W, Fuchs G. 2010. Bacterial phenylalanine and phenylacetate catabolic pathway revealed. Proc. Natl. Acad. Sci. U. S. A. 107:14390-14395.
23. Ferrández A, García JL, Díaz E. 2000. Transcriptional regulation of the divergent paa catabolic operons for phenylacetic acid degradation in Escherichia coli. J. Biol. Chem. 275:12214-12222.
24. Fic E, Bonarek P, Gorecki A, Kedracka-Krok S, Mikolajczak J, Polit A, Wasylewski Z. 2009. cAMP receptor protein from Escherichia coli as a model of signal transduction in proteins-a review. J. Mol. Microbiol. Biotechnol. 17:1-11.
25. Azakami H, Yamashita M, Roh J, Suzuki H, Kumagai H, Murooka Y. 1994. Nucleotide sequence of the gene for monoamine oxidase (maoA) from Escherichia coli. J. Ferment. Bioeng. 77:315-319.
26. Storz G, Imlay JA. 1999. Oxidative stress. Curr. Opin. Microbiol. 2:188-194.
27. Christman MF, Storz G, Ames BN. 1989. OxyR, a positive regulator of hydrogen peroxide-inducible genes in Escherichia coli and Salmonella typhimurium, is homologous to a family of bacterial regulatory proteins. Proc. Natl. Acad. Sci. U. S. A. 86:3484-3488.
28. Jacobson FS, Morgan RW, Christman MF, Ames BN. 1989. An alkyl hydroperoxide reductase from Salmonella typhimurium involved in the defense of DNA against oxidative damage. Purification and properties. J. Biol. Chem. 264:1488-1496.
29. Altuvia S, Almiron M, Huisman G, Kolter R, Storz G. 1994. The dps promoter is activated by OxyR during growth and by IHF and sigma S in stationary phase. Mol. Microbiol. 13:265-272.
30. Anjem A, Varghese S, Imlay JA. 2009. Manganese import is a key element of the OxyR response to hydrogen peroxide in Escherichia coli. Mol. Microbiol. 72:844-858.
31. Liu Y, Bauer SC, Imlay JA. 2011. The YaaA protein of the Escherichia coli OxyR regulon lessens hydrogen peroxide toxicity by diminishing the amount of intracellular unincorporated iron. J. Bacteriol. 193:2186-2196.
32. Jang S, Imlay JA. 2010. Hydrogen peroxide inactivates the Escherichia coli Isc iron-sulphur assembly system, and OxyR induces the Suf system to compensate. Mol. Microbiol. 78:1448-1467.
33. Miller JH. 1972. Experiments in molecular genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
34. 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.
35. Haldimann A, Wanner BL. 2001. Conditional-replication, integration, excision, and retrieval plasmid-host systems for gene structure-function studies of bacteria. J. Bacteriol. 183:6384-6393.
36. Kullik I, Stevens J, Toledano MB, Storz G. 1995. Mutational analysis of the redox-sensitive transcriptional regulator OxyR: regions important for DNA binding and multimerization. J. Bacteriol. 177:1285-1291.
37. Weski J, Ehrmann M. 2012. Genetic analysis of 15 protein folding factors and proteases of the Escherichia coli cell envelope. J. Bacteriol. 194:3225-3233.
38. Imlay JA, Fridovich I. 1991. Assay of metabolic superoxide production in Escherichia coli. J. Biol. Chem. 266:6957-6965.
39. Oliver DB. 1996. Periplasm. In Neidhardt FC, Curtiss R, III, Ingraham JL, Lin ECC, Low KB, Magasanik B, ReznikoffWS, Riley M, Schaechter M, Umbarger HE (ed), Escherichia coli and Salmonella: cellular and molecular biology, 2nd ed, vol 1. ASM Press, Washington, DC.
40. Neidhardt FC, Ingraham JL, Schaechter M. 1990. Physiology of the bacterial cell: a molecular approach. Sinauer Associates, Inc., Sunderland, MA.
41. Beers RFJ, Sizer IW. 1952. A spectrophotometric method for measuring the breakdown of hydrogen peroxide by catalase. J. Biol. Chem. 195:133-140.
42. Choi H, Kim S, Mukhopadhyay P, Cho S, Woo J, Storz G, Ryu S. 2001. Structural basis of the redox switch in the OxyR transcription factor. Cell 105:103-113.
43. Aslund F, Zheng M, Beckwith J, Storz G. 1999. Regulation of the OxyR transcriptional factor by hydrogen peroxide and the cellular thioldisulfide status. Proc. Natl. Acad. Sci. U. S. A. 96:6161-6165.
44. Seaver LC, Imlay JA. 2001. Hydrogen peroxide fluxes and compartmentalization inside growing Escherichia coli. J. Bacteriol. 183:7182-7189.
45. Grant RA, Filman DJ, Finkel SE, Kolter R, Hogle JM. 1998. The crystal structure of Dps, a ferritin homolog that binds and protects DNA. Nat. Struct. Biol. 5:294-303.
46. Ilari A, Ceci P, Ferrari D, Rossi G, Chiancone E. 2002. Iron incorporation into E. coli Dps gives rise to a ferritin-like microcrystalline core. J. Biol. Chem. 277:37619-37623.
47. Kehres DG, Janakiraman A, Slauch JM, Maguire ME. 2002. Regulation of Salmonella enterica serovar Typhimurium mntH transcription byH2O2, Fe2, and Mn2. J. Bacteriol. 184:3151-3158.
48. Lee JH, Yeo WS, Roe JH. 2004. Induction of the sufA operon encoding Fe-S assembly proteins by superoxide generators and hydrogen peroxide: involvement of OxyR, IHF and an unidentified oxidant-responsive factor. Mol. Microbiol. 51:1745-1755.
49. Imlay JA, Linn S. 1986. Bimodal pattern of killing of DNA-repairdefective or anoxically grown Escherichia coli by hydrogen peroxide. J. Bacteriol. 166:519-527.
50. Hengge R. 2009. Proteolysis of sigmaS (RpoS) and the general stress response in Escherichia coli. Res. Microbiol. 160:667-676.
51. Ruiz N, Silhavy TJ. 2005. Sensing external stress: watchdogs of the Escherichia coli cell envelope. Curr. Opin. Microbiol. 8:122-126.
52. Depuydt M, Leonard SE, Vertommen D, Denoncin K, Morsomme P, Wahni K, Messens J, Carroll KS, Collet J-F. 2009. A periplasmic reducing system protects single cysteine residues from oxidation. Science 236: 1109-1111.
53. Wilmot CM, Murray JM, Alton G, Parsons MR, Convery MA, Blakeley V, Corner AS, Palcic MM, Knowles PF, McPherson MJ, Phillips SEV. 1997. Catalytic mechanism of the quinoenzyme amine oxidase from Escherichia coli: exploring the reductive half-reaction. Biochemistry 36:1608-1620.
54. Macomber L, Imlay JA. 2009. The iron-sulfur clusters of dehydratases are primary intracellular targets of copper toxicity. Proc. Natl. Acad. Sci. U. S. A. 106:8344-8349.
55. Fitzpatrick PF. 2010. Oxidation of amines by flavoproteins. Arch. Biochem. Biophys. 493:13-25.
56. Winterbourn CC, Hampton MB, Livesey JH, Kettle AJ. 2006. Modeling the reactions of superoxide and myeloperoxidase in the neutrophil phagosome. Implications for microbial killing. J. Biol. Chem. 281:39860-39869.
57. Nikaido H, Rosenberg EV. 1981. Effect of solute size on diffusion rates through the transmembrane pores of the outer membrane of Escherichia coli. J. Gen. Physiol. 77:121-135.
58. Jacobs NJ, Jacobs JM. 1978. Quinones as hydrogen carriers for a late step in anaerobic heme biosynthesis in Escherichia coli. Biochim. Biophys. Acta 544:540-546.
59. Wanders RJA, Waterham HR. 2006. Biochemistry of mammalian peroxisomes revisited. Annu. Rev. Biochem. 75:295-332.
60. Kerfeld CA, Heinhorst S, Cannon GC. 2010. Bacterial microcompartments. Annu. Rev. Microbiol. 64:391-408.
61. Winterbourn CC, Metodiewa D. 1999. Reactivity of biologically important thiol compounds with superoxide and hydrogen peroxide. Free Radic. Biol. Med. 27:322-328.
62. Jaakkola K, Kaunismaki K, Tohka S, Yegutkin G, Vanttinen E, Havia T, Pelliniemi LJ, Virolainen M, Jalkanen S, Salmi M. 1999. Human vascular adhesion protein-1 in smooth muscle cells. Am. J. Pathol. 155:1953-1965.
63. Hrycay E, Bandiera SM. 2012. The monooxygenase, peroxidase, and peroxygenase properties of cytochrome P450. Arch. Biochem. Biophys. 522:71-89.
64. Yamashita M, Azakami H, Yokoro N, Roh JH, Suzuki H, Kumagai H, Murooka Y. 1996. maoB, a gene that encodes a positive regulator of the monoamine oxidase gene (maoA) in Escherichia coli. J. Bacteriol. 178: 2941-2947.