Activation of the OxyR transcription factor by reversible disulfide bond formation

Science

Volumn 279, Issue 5357, 1998, Pages 1718-1721

  Zheng, Ming ^a   Åslund, Fredrik ^b   Storz, Gisela ^a  

^a EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYSTEINE; DISULFIDE; GLUTATHIONE; GLUTATHIONE REDUCTASE; GLUTATHIONE SYNTHASE; HYDROGEN PEROXIDE; THIOREDOXIN; THIOREDOXIN REDUCTASE; TRANSCRIPTION FACTOR;

AMINO ACID SUBSTITUTION; ARTICLE; CONTROLLED STUDY; DISULFIDE BOND; ESCHERICHIA COLI; GENE CONTROL; GENE EXPRESSION; MASS SPECTROMETRY; NONHUMAN; OXIDATION; OXIDATION REDUCTION POTENTIAL; PRIORITY JOURNAL;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; BACTERIAL PROTEINS; BASE SEQUENCE; CYSTEINE; DISULFIDES; DNA-BINDING PROTEINS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; GLUTATHIONE; GLUTATHIONE DISULFIDE; GLUTATHIONE REDUCTASE; HYDROGEN PEROXIDE; MOLECULAR SEQUENCE DATA; OXIDATION-REDUCTION; OXIDATIVE STRESS; OXIDOREDUCTASES; PROTEINS; REPRESSOR PROTEINS; SIGNAL TRANSDUCTION; THIOREDOXIN; TRANSCRIPTION FACTORS;

ESCHERICHIA COLI;

EID: 0032513362     PISSN: 00368075     EISSN: None     Source Type: Journal    
DOI: 10.1126/science.279.5357.1718     Document Type: Article

References (43)

1. B. Halliwell and J. M. C. Gutteridge, Free Radicals in Biology and Medicine (Clarendon Press, Oxford, 1989).
2. D. J. Jamieson and G. Storz, in Oxidative Stress and the Molecular Biology of Antioxidant Defenses, J. G. Scandalios, Ed. (Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, 1997), pp. 91-115; B. González-Flecha and B. Demple, in Reactive Oxygen Species in Biological Systems: An Interdisciplinary Approach, D. L. Gilbert and C. A. Colton, Eds. (Plenum, New York, in press).
3. D. J. Jamieson and G. Storz, in Oxidative Stress and the Molecular Biology of Antioxidant Defenses, J. G. Scandalios, Ed. (Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, 1997), pp. 91-115; B. González-Flecha and B. Demple, in Reactive Oxygen Species in Biological Systems: An Interdisciplinary Approach, D. L. Gilbert and C. A. Colton, Eds. (Plenum, New York, in press).
4. G. E. Schultz and R. H. Schirmer, Principles of Protein Structure (Springer-Verlag, New York, 1979); J. M. Thornton, J. Mol. Biol. 151, 261 (1981); C. Branden and J. Tooze, Introduction to Protein Structure (Garland, New York, 1991).
5. G. E. Schultz and R. H. Schirmer, Principles of Protein Structure (Springer-Verlag, New York, 1979); J. M. Thornton, J. Mol. Biol. 151, 261 (1981); C. Branden and J. Tooze, Introduction to Protein Structure (Garland, New York, 1991).
6. G. E. Schultz and R. H. Schirmer, Principles of Protein Structure (Springer-Verlag, New York, 1979); J. M. Thornton, J. Mol. Biol. 151, 261 (1981); C. Branden and J. Tooze, Introduction to Protein Structure (Garland, New York, 1991).
7. H. F. Gilbert, Adv. Enzymol. Relat. Areas Mol. Biol. 63, 69 (1990).
8. C. Hwang, A. J. Sinskey, H. F. Lodish, Science 257, 1496 (1992).
9. A. I. Derman, W. A. Prinz, D. Belin, J. Beckwith, ibid. 262, 1744 (1993); W. A. Prinz, F. Åslund, A. Holmgren, J. Beckwith, J. Biol. Chem. 272, 15661 (1997).
10. A. I. Derman, W. A. Prinz, D. Belin, J. Beckwith, ibid. 262, 1744 (1993); W. A. Prinz, F. Åslund, A. Holmgren, J. Beckwith, J. Biol. Chem. 272, 15661 (1997).
11. F. Åslund, K. D. Berndt, A. Holmgren, J. Biol. Chem. 272, 30780 (1997).
12. S. Altuvia, D. Weinstein-Fischer, A. Zhang, L. Postow, G. Storz, Cell 90, 43 (1997).
13. G. Storz, L. A. Tartaglia, B. N. Ames, Science 248, 189 (1990).
14. M. B. Toledano et al., Cell 78, 897 (1994).
15. Two samples of OxyR (15 μM) were analyzed by the Chemical Analysis Laboratory at the University of Georgia. No transition metals were detected at a sensitivity of ≤5 pM.
16. I. Kullik, M. B. Toledano, L. A. Tartaglia, G. Storz, J. Bacteriol. 177, 1275 (1995).
17. Escherichia coli (J04553, residues 191-208), LLMLEDGHCLRDQAMGFC; Erwinia carotovora (U74302), LLMLEDGHCLRDQAMGFC; Haemophilus influenzae (U49355), MLMLDDGHCLRNQALDYC; Xanthomonas campestris (U94336), LLLLEDGHCLRDQALDVC; Mycobacterium leprae (L01095), LLLLDEGHCLRDQTLDIC; Acinetobacter calcoaceticus (X88895), LMLLEEGHCLRDHALSAC (26).
18. M. Zheng, F. Åslund, G. Storz, data not shown.
19. We carried out 5,5′-dithiobis-(2-nitrobenzoic acid) and 2-nitro-5-thiosulfobenzoate titrations under denaturing conditions as described [P. W. Riddles, R. L. Blakeley, B. Zerner, Anal. Biochem. 94, 75 (1979); T. W. Thannhauser, Y. Konishi, H. A. Scheraga, ibid. 138, 181 (1984)]. For reduced OxyFMC→A, 1.8 equivalents of -SH and 0.1 equivalents of S-S were detected, whereas 0.2 equivalents of -SH and 0.9 equivalents of S-S were detected for the oxidized protein.
20. We carried out 5,5′-dithiobis-(2-nitrobenzoic acid) and 2-nitro-5-thiosulfobenzoate titrations under denaturing conditions as described [P. W. Riddles, R. L. Blakeley, B. Zerner, Anal. Biochem. 94, 75 (1979); T. W. Thannhauser, Y. Konishi, H. A. Scheraga, ibid. 138, 181 (1984)]. For reduced OxyFMC→A, 1.8 equivalents of -SH and 0.1 equivalents of S-S were detected, whereas 0.2 equivalents of -SH and 0.9 equivalents of S-S were detected for the oxidized protein.
21. Mass spectrometry (MALDI-TOF) of oxidized, denatured OxyR revealed a major peak at 34.3 ± 0.1 kD and a minor peak at 17.1 ± 0.1 kD, corresponding to the singly- and doubly-charged OxyR monomer (theoretical mass of 34.28 kD), respectively.
22. J. L. Kice, Adv. Phys. Org. Chem. 17, 65 (1980); A. Claiborne, H. Miller, D. Parsonage, R. P. Ross, FASEB J. 7, 1483 (1993).
23. J. L. Kice, Adv. Phys. Org. Chem. 17, 65 (1980); A. Claiborne, H. Miller, D. Parsonage, R. P. Ross, FASEB J. 7, 1483 (1993).
24. F. A. Davis and R. L. Billmers, J. Am. Chem. Soc. 103, 7016 (1981); H. R. Ellis and L. B. Poole, Biochemistry 36, 13349 (1997).
25. F. A. Davis and R. L. Billmers, J. Am. Chem. Soc. 103, 7016 (1981); H. R. Ellis and L. B. Poole, Biochemistry 36, 13349 (1997).
26. 2O] [(17); E. Block and J. O'Connor, J. Am. Chem. Soc. 96, 3929 (1974); F. A. Davis, L. A. Jenkins, R. L. Billmers, J. Org. Chem. 51, 1033 (1986)].
27. 2O] [(17); E. Block and J. O'Connor, J. Am. Chem. Soc. 96, 3929 (1974); F. A. Davis, L. A. Jenkins, R. L. Billmers, J. Org. Chem. 51, 1033 (1986)].
28. C. T. Privalle and I. Fridovich, J. Biol. Chem. 265, 21966 (1990); A. Hausladen, C. T. Privalle, T. Keng, J. DeAngelo, J. S. Stamler, Cell 86, 719 (1996).
29. C. T. Privalle and I. Fridovich, J. Biol. Chem. 265, 21966 (1990); A. Hausladen, C. T. Privalle, T. Keng, J. DeAngelo, J. S. Stamler, Cell 86, 719 (1996).
30. I. Kullik, J. Stevens, M. B. Toledano, G. Storz, J. Bacteriol. 177, 1285 (1995).
31. o is the standard potential of GSH [-240 mV (7)], R is the gas constant, T is the temperature, n is the number of electrons transferred (eight electrons in the case of OxyR), and F is the Faraday constant.
32. OxyR reduction by thioredoxin reductase and thioredoxin was carried out essentially the same as the reduction described in Fig. 2B, except that 10 μg/ml E. coli thioredoxin reductase (lmco) and 10 μME. coli thioredoxin (lmco) were used in place of glutathione reductase, Grx1, and GSH.
33. The OxyR-regulated transcription start was mapped to an A residue 23 nucleotides upstream of the AUG. The extent of the OxyR DNase I footprint on both strands is underlined, and the matches to the OxyR binding site consensus (10) are capitalized on the following sequences. Top strand: 5′-gtgtttaacagttATAGcTtttAgCaATtaatgcaAcAGgTtaaAcCTActttcagcgaa; bottom strand: 3′-cacaaattgtcaaTATCgAaaaTcGtTAattacgtTgTCcAattTgGATgaaagtcgctt. The same transcription start and OxyR binding site were recently identified [K. Tao, J. Bacteriol. 179, 5967 (1997)].
34. H. Ding, E. Hidalgo, B. Demple, J. Biol. Chem. 271, 33173 (1996); P. Gaudu and B. Weiss, Proc. Natl. Acad. Sci. U.S.A. 93, 10094 (1996); E. Hidalgo, H. Ding, B. Demple, Cell 88, 121 (1997).
35. H. Ding, E. Hidalgo, B. Demple, J. Biol. Chem. 271, 33173 (1996); P. Gaudu and B. Weiss, Proc. Natl. Acad. Sci. U.S.A. 93, 10094 (1996); E. Hidalgo, H. Ding, B. Demple, Cell 88, 121 (1997).
36. H. Ding, E. Hidalgo, B. Demple, J. Biol. Chem. 271, 33173 (1996); P. Gaudu and B. Weiss, Proc. Natl. Acad. Sci. U.S.A. 93, 10094 (1996); E. Hidalgo, H. Ding, B. Demple, Cell 88, 121 (1997).
37. Single-letter abbreviations for the amino acid residues are as follows: A, Ala; C, Cys; D, Asp; E, Glu; F, Phe; G, Gly; H, His; I, Ile; K, Lys; L, Leu; M, Met; N, Asn; P, Pro; Q, Gln; R, Arg; S, Ser; T, Thr; V, Val; W, Trp; and Y, Tyr.
38. N. K. Davis, S. Greer, M. C. Jones-Mortimer, R. N. Perham, J. Gen. Microbiol. 128, 1631 (1982); J. T. Greenberg and B. Demple, J. Bacteriol. 168, 1026 (1986); M. Russel and A. Holmgren, Proc. Natl. Acad. Sci. U.S.A. 85, 990 (1988); M. Russel and P. Model, in Thioredoxin and Glutaredoxin Systems: Structure and Function, A. Holmgren, C. I. Brändén, H. Jörnvall, B.-M. Sjöberg, Eds. (Raven Press, New York, 1986), pp. 331-337.
39. N. K. Davis, S. Greer, M. C. Jones-Mortimer, R. N. Perham, J. Gen. Microbiol. 128, 1631 (1982); J. T. Greenberg and B. Demple, J. Bacteriol. 168, 1026 (1986); M. Russel and A. Holmgren, Proc. Natl. Acad. Sci. U.S.A. 85, 990 (1988); M. Russel and P. Model, in Thioredoxin and Glutaredoxin Systems: Structure and Function, A. Holmgren, C. I. Brändén, H. Jörnvall, B.-M. Sjöberg, Eds. (Raven Press, New York, 1986), pp. 331-337.
40. N. K. Davis, S. Greer, M. C. Jones-Mortimer, R. N. Perham, J. Gen. Microbiol. 128, 1631 (1982); J. T. Greenberg and B. Demple, J. Bacteriol. 168, 1026 (1986); M. Russel and A. Holmgren, Proc. Natl. Acad. Sci. U.S.A. 85, 990 (1988); M. Russel and P. Model, in Thioredoxin and Glutaredoxin Systems: Structure and Function, A. Holmgren, C. I. Brändén, H. Jörnvall, B.-M. Sjöberg, Eds. (Raven Press, New York, 1986), pp. 331-337.
41. N. K. Davis, S. Greer, M. C. Jones-Mortimer, R. N. Perham, J. Gen. Microbiol. 128, 1631 (1982); J. T. Greenberg and B. Demple, J. Bacteriol. 168, 1026 (1986); M. Russel and A. Holmgren, Proc. Natl. Acad. Sci. U.S.A. 85, 990 (1988); M. Russel and P. Model, in Thioredoxin and Glutaredoxin Systems: Structure and Function, A. Holmgren, C. I. Brändén, H. Jörnvall, B.-M. Sjöberg, Eds. (Raven Press, New York, 1986), pp. 331-337.
42. J. S. Stamler and J. Loscalzo, Anal. Chem. 64, 779 (1992).
43. We thank C. Wu and C. Klee for the use of the MALDI mass spectrophotometer and Pharmacia Smart system, C. Vinson for use of the spectropolarimeter, L. Poole and J. Beckwith (grant GM-41883) for experiments conducted by M.Z. and F.A. in their laboratories, and J. Bushweller, B. Demple, A. Eisenstark, A. Holmgren, and M. Russel for E. coli strains, plasmids, and purified Grx1. We also appreciate the advice of J. Beckwith, L. Poole, and W. Prinz, and the editorial comments of J. Beckwith, C. Dismukes, R. Klausner, L. Poole, C. Wu, Y.-L. Wu, and M. Zhong. Supported by the intramural program of the National Institute of Child Health and Human Development and grants from the American Cancer Society (M.Z.), the Karolinska Institute (F.A.), and the Wennergren Foundation (F.A.).