Iron enzyme ribulose-5-phosphate 3-epimerase in Escherichia coli is rapidly damaged by hydrogen peroxide but can be protected by manganese

Proceedings of the National Academy of Sciences of the United States of America

Volumn 108, Issue 13, 2011, Pages 5402-5407

  Sobota, Jason M ^a   Imlay, James A ^a  

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

Author keywords

Hydroxyl radical; MntH; Oxidative damage; OxyR

Indexed keywords

HYDROGEN PEROXIDE; MANGANESE; PENTOSE PHOSPHATE; RIBULOSE PHOSPHATE; RIBULOSEPHOSPHATE 3 EPIMERASE; UNCLASSIFIED DRUG;

BACTERIAL STRAIN; CONFERENCE PAPER; ENZYME ACTIVITY; ENZYME INACTIVATION; ESCHERICHIA COLI; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; PRIORITY JOURNAL;

ESCHERICHIA COLI;

EID: 79953896180     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1100410108     Document Type: Article

References (45)

1. Loew O (1900) A new enzyme of general occurrence in organisms. Science 11: 701-702.
2. Glass GA, et al. (1986) The respiratory burst oxidase of human neutrophils. Further studies of the purified enzyme. J Biol Chem 261:13247-13251. (Pubitemid 17006903)
3. Mehdy MC (1994) Active oxygen species in plant defense against pathogens. Plant Physiol 105:467-472.
4. 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.
5. Lee JW, Helmann JD (2006) The PerR transcription factor senses H2O2 by metalcatalysed histidine oxidation. Nature 440:363-367.
6. Choi H, et al. (2001) Structural basis of the redox switch in the OxyR transcription factor. Cell 105:103-113. (Pubitemid 32323920)
7. Zheng M, et al. (2001) DNA microarray-mediated transcriptional profiling of the Escherichia coli response to hydrogen peroxide. J Bacteriol 183:4562-4570. (Pubitemid 32646006)
8. Seaver LC, Imlay JA (2001) Alkyl hydroperoxide reductase is the primary scavenger of endogenous hydrogen peroxide in Escherichia coli. J Bacteriol 183:7173-7181. (Pubitemid 33121851)
9. Park S, You X, Imlay JA (2005) Substantial DNA damage from submicromolar intracellular hydrogen peroxide detected in Hpx- mutants of Escherichia coli. Proc Natl Acad Sci USA 102:9317-9322. (Pubitemid 40923561)
10. Rai P, Cole TD, Wemmer DE, Linn S (2001) Localization of Fe(2+) at an RTGR sequence within a DNA duplex explains preferential cleavage by Fe(2+) and H2O2. J Mol Biol 312:1089-1101. (Pubitemid 32980328)
11. 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.
12. Jang S, Imlay JA (2007) Micromolar intracellular hydrogen peroxide disrupts metabolism by damaging iron-sulfur enzymes. J Biol Chem 282:929-937. (Pubitemid 47076541)
13. Kuo CF, Mashino T, Fridovich I (1987) α, β- Dihydroxyisovalerate dehydratase. A superoxide-sensitive enzyme. J Biol Chem 262:4724-4727.
14. Gardner PR, Fridovich I (1991) Superoxide sensitivity of the Escherichia coli 6-phosphogluconate dehydratase. J Biol Chem 266:1478-1483. (Pubitemid 21908327)
15. Gardner PR, Fridovich I (1991) Superoxide sensitivity of the Escherichia coli aconitase. J Biol Chem 266:19328-19333. (Pubitemid 21908236)
16. Liochev SI, Fridovich I (1992) Fumarase C, the stable fumarase of Escherichia coli, is controlled by the soxRS regulon. Proc Natl Acad Sci USA 89:5892-5896.
17. Flint DH, Tuminello JF, Emptage MH (1993) The inactivation of Fe-S cluster containing hydro-lyases by superoxide. J Biol Chem 268:22369-22376. (Pubitemid 23318282)
18. Jang S, Imlay JA (2010) Hydrogen peroxide inactivates the Escherichia coli Isc ironsulphur assembly system, and OxyR induces the Suf system to compensate. Mol Microbiol 78:1448-1467.
19. Varghese S, Wu A, Park S, Imlay KRC, Imlay JA (2007) Submicromolar hydrogen peroxide disrupts the ability of Fur protein to control free-iron levels in Escherichia coli. Mol Microbiol 64:822-830. (Pubitemid 46653221)
20. 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. (Pubitemid 28164882)
21. Ilari A, Ceci P, Ferrari D, Rossi GL, Chiancone E (2002) Iron incorporation into Escherichia coli Dps gives rise to a ferritin-like microcrystalline core. J Biol Chem 277: 37619-37623.
22. Zhao G, et al. (2002) Iron and hydrogen peroxide detoxification properties of DNAbinding protein from starved cells. A ferritin-like DNA-binding protein of Escherichia coli. J Biol Chem 277:27689-27696. (Pubitemid 34966712)
23. Zheng M, Doan B, Schneider TD, Storz G (1999) OxyR and SoxRS regulation of fur. J Bacteriol 181:4639-4643. (Pubitemid 29357947)
24. 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.
25. Akana J, et al. (2006) D-Ribulose 5-phosphate 3-epimerase: Functional and structural relationships to members of the ribulose-phosphate binding (β/α)8-barrel superfamily. Biochemistry 45:2493-2503.
26. Rush JD, Maskos Z, Koppenol WH (1990) Distinction between hydroxyl radical and ferryl species. Methods Enzymol 186:148-156. (Pubitemid 20279952)
27. Murakami K, Tsubouchi R, Fukayama M, Ogawa T, Yoshino M (2006) Oxidative inactivation of reduced NADP-generating enzymes in E. coli: Iron-dependent inactivation with affinity cleavage of NADP-isocitrate dehydrogenase. Arch Microbiol 186:385-392. (Pubitemid 44705113)
28. (2+). J Bacteriol 184:3151-3158. (Pubitemid 34568923)
29. Seaver LC, Imlay JA (2001) Hydrogen peroxide fluxes and compartmentalization inside growing Escherichia coli. J Bacteriol 183:7182-7189. (Pubitemid 33121852)
30. Leichert LI, et al. (2008) Quantifying changes in the thiol redox proteome upon oxidative stress in vivo. Proc Natl Acad Sci USA 105:8197-8202. (Pubitemid 351904734)
31. Daly MJ, et al. (2007) Protein oxidation implicate as the perimary determinant of bacterial radioresistance. PLoS Biol 5:769-779. (Pubitemid 46631854)
32. Krisko A, Radman M (2010) Protein damage and death by radiation in Escherichia coli and Deinococcus radiodurans. Proc Natl Acad Sci USA 107:14373-14377.
33. Bosshard F, et al. (2010) Protein oxidation and aggregation in UVA-irradiated Escherichia coli cells as signs of accelerated cellular senescence. Environ Microbiol 12: 2931-2945.
34. Compan I, Touati D (1993) Interaction of six global transcription regulators in expression of manganese superoxide dismutase in Escherichia coli K-12. J Bacteriol 175:1687-1696. (Pubitemid 23084131)
35. Martin JE, Imlay JA (2011) The alternative aerobic ribonucleotide reductase of Escherichia coli, NrdEF, is a manganese-dependent enzyme that enables cell replication during periods of iron starvation. Mol Microbiol, in press.
36. Tseng HJ, Srikhanta Y, McEwan AG, Jennings MP (2001) Accumulation of manganese in Neisseria gonorrhoeae correlates with resistance to oxidative killing by superoxide anion and is independent of superoxide dismutase activity. Mol Microbiol 40: 1175-1186. (Pubitemid 32574984)
37. Seib KL, Tseng HJ, McEwan AG, Apicella MA, Jennings MP (2004) Defenses against oxidative stress in Neisseria gonorrhoeae and Neisseria meningitidis: Distinctive systems for different lifestyles. J Infect Dis 190:136-147. (Pubitemid 38858414)
38. Tseng HJ, McEwan AG, Paton JC, Jennings MP (2002) Virulence of Streptococcus pneumoniae: PsaA mutants are hypersensitive to oxidative stress. Infect Immun 70: 1635-1639. (Pubitemid 34163448)
39. Kehres DG, Zaharik ML, Finlay BB, Maguire ME (2000) The NRAMP proteins of Salmonella typhimurium and Escherichia coli are selective manganese transporters involved in the response to reactive oxygen. Mol Microbiol 36:1085-1100. (Pubitemid 30330680)
40. Daly MJ, et al. (2004) Accumulation of Mn(II) in Deinococcus radiodurans facilitates gamma-radiation resistance. Science 306:1025-1028. (Pubitemid 39482904)
41. Daly MJ, et al. (2010) Small-molecule antioxidant proteome-shields in Deinococcus radiodurans. PLoS ONE 5:e12570.
42. Runyen-Janecky L, Dazenski E, Hawkins S, Warner L (2006) Role and regulation of the Shigella flexneri sit and MntH systems. Infect Immun 74:4666-4672. (Pubitemid 44157254)
43. Horsburgh MJ, Wharton SJ, Karavolos M, Foster SJ (2002) Manganese: Elemental defence for a life with oxygen. Trends Microbiol 10:496-501. (Pubitemid 35284795)
44. Kehres DG, Maguire ME (2003) Emerging themes in manganese transport, biochemistry and pathogenesis in bacteria. FEMS Microbiol Rev 27:263-290. (Pubitemid 36694659)
45. Archibald F (1986) Manganese: its acquisition by and function in the lactic acid bacteria. Crit Rev Microbiol 13:63-109.