Activity of the tetrapyrrole regulator CrtJ is controlled by oxidation of a redox active cysteine located in the DNA binding domain

Molecular Microbiology

Volumn 85, Issue 4, 2012, Pages 734-746

  Cheng, Zhuo ^a   Wu, Jiang ^a   Setterdahl, Aaron ^a   Reddie, Khalilah ^b   Carroll, Kate ^c   Hammad, Loubna A ^a   Karty, Jonathan A ^a   Bauer, Carl E ^a  

^a INDIANA UNIVERSITY   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

^c SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; CYSTEINE; HYDROGEN PEROXIDE; OXYGEN; PROTEIN CRTJ; REGULATOR PROTEIN; SERINE; SULFENIC ACID DERIVATIVE; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; ARTICLE; BINDING AFFINITY; CHEMICAL MODIFICATION; CONTROLLED STUDY; DNA BINDING MOTIF; GENE EXPRESSION; HELIX TURN HELIX MOTIF; IN VIVO STUDY; LIQUID CHROMATOGRAPHY; MUTATION; NONHUMAN; OXIDATION; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN MOTIF; REDUCTION; RHODOBACTER CAPSULATUS; TANDEM MASS SPECTROMETRY;

BACTERIAL PROTEINS; CHROMATOGRAPHY, LIQUID; CYSTEINE; DNA; DNA-BINDING PROTEINS; HELIX-TURN-HELIX MOTIFS; HYDROGEN PEROXIDE; MODELS, BIOLOGICAL; OXIDATION-REDUCTION; OXYGEN; PROTEIN BINDING; RHODOBACTER CAPSULATUS; TANDEM MASS SPECTROMETRY; TETRAPYRROLES; TRANSCRIPTION FACTORS;

RHODOBACTER CAPSULATUS;

EID: 84864824413     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2012.08135.x     Document Type: Article

References (34)

1. Bauer, C.E. (2001) Regulating synthesis of the purple bacterial photosystem. In Regulation of Photosynthesis. Aro, E., and Andersson, B. (eds). Dodrecht: Kluwer Academic Press, pp. 67-83.
2. Bauer, C.E., and Bird, T.H. (1996) Regulatory circuits controlling photosynthesis gene expression. Cell 85: 5-8.
3. Birkett, D.J., Price, N.C., Radda, G.K., and Salmon, A.G. (1970) The reactivity of SH groups with a fluorogenic reagent. FEBS Lett 6: 346-348.
4. Boyer, P.D. (1954) Spectrophotometric study of the reaction of protein sulfhydryl groups with organic mercurials. J Am Chem Soc 76: 4331-4337.
5. Carballal, S., Radi, R., Kirk, M.C., Barnes, S., Freeman, B.A., and Alvarez, B. (2003) Sulfenic acid formation in human serum albumin by hydrogen peroxide and peroxynitrite. Biochemistry 42: 9906-9914.
6. Charles, R.L., Schroder, E., May, G., Free, P., Gaffney, P.R., Wait, R., etal. (2007) Protein sulfenation as a redox sensor: proteomics studies using a novel biotinylated dimedone analogue. Mol Cell Proteomics 6: 1473-1484.
7. Cohen-Bazire, G., Sistrom, W.R., and Stanier, R.Y. (1957) Kinetic studies of pigment synthesis by non-sulfur purple bacteria. J Cell Physiol 49: 25-68.
8. Denu, J.M., and Tanner, K.G. (1998) Specific and reversible inactivation of protein tyrosine phosphatases by hydrogen peroxide: evidence for a sulfenic acid intermediate and implications for redox regulation. Biochemistry 37: 5633-5642.
9. Dong, C., Elsen, S., Swem, L.R., and Bauer, C.E. (2002) AerR, a second aerobic repressor of photosynthesis gene expression in Rhodobacter capsulatus. J Bacteriol 184: 2805-2814.
10. Ellis, H.R., and Poole, L.B. (1997) Novel application of 7-chloro-4-nitrobenzo-2-oxa-1, 3-diazole to identify cysteine sulfenic acid in the AhpC component of alkyl hydroperoxide reductase. Biochemistry 36: 15013-15018.
11. Elsen, S., Ponnampalam, S.N., and Bauer, C.E. (1998) CrtJ bound to distant binding sites interacts cooperatively to aerobically repress photopigment biosynthesis and light harvesting II gene expression in Rhodobacter capsulatus. J Biol Chem 273: 30762-30769.
12. Fuangthong, M., and Helmann, J.D. (2002) The OhrR repressor senses organic hydroperoxides by reversible formation of a cysteine-sulfenic acid derivative. Proc Natl Acad Sci USA 99: 6690-6695.
13. Hong, M., Fuangthong, M., Helmann, J.D., and Brennan, R.G. (2005) Structure of an OhrR-ohrA operator complex reveals the DNA binding mechanism of the MarR family. Mol Cell 20: 131-141.
14. Hunt, D.F., Yates, J.R., 3rd, Shabanowitz, J., Winston, S., and Hauer, C.R. (1986) Protein sequencing by tandem mass spectrometry. Proc Natl Acad Sci USA 83: 6233-6237.
15. Imhoff, J.F., Truper, H.G., and Pfennig, N. (1984) Rearrangement of the species and genera of the phototrophic 'purple nonsulfur bacteria'. Int J Syst Bacteriol 34: 340-343.
16. Jaubert, M., Zappa, S., Fardoux, J., Adriano, J.M., Hannibal, L., Elsen, S., etal. (2004) Light and redox control of photosynthesis gene expression in Bradyrhizobium: dual roles of two PpsR. J Biol Chem 279: 44407-44416.
17. Kim, S.O., Merchant, K., Nudelman, R., Beyer, W.F., Jr, Keng, T., DeAngelo, J., etal. (2002) OxyR: a molecular code for redox-related signaling. Cell 109: 383-396.
18. Kovacs, A.T., Rakhely, G., and Kovacs, K.L. (2005) The PpsR regulator family. Res Microbiol 156: 619-625.
19. Kullik, I., Toledano, M.B., Tartaglia, L.A., and Storz, G. (1995) Mutational analysis of the redox-sensitive transcriptional regulator OxyR: regions important for oxidation and transcriptional activation. J Bacteriol 177: 1275-1284.
20. Leonard, S.E., Reddie, K.G., and Carroll, K.S. (2009) Mining the thiol proteome for sulfenic acid modifications reveals new targets for oxidation in cells. ACS Chem Biol 4: 783-799.
21. Lin, W.S., Armstrong, D.A., and Gaucher, G.M. (1975) Formation and repair of papain sulfenic acid. Can J Biochem 53: 298-307.
22. Masuda, S., Dong, C., Swem, D., Setterdahl, A.T., Knaff, D.B., and Bauer, C.E. (2002) Repression of photosynthesis gene expression by formation of a disulfide bond in CrtJ. Proc Natl Acad Sci USA 99: 7078-7083.
23. Paulsen, C.E., and Carroll, K.S. (2009) Chemical dissection of an essential redox switch in yeast. Chem Biol 16: 217-225.
24. Penfold, R.J., and Pemberton, J.M. (1991) A gene from the photosynthetic gene cluster of Rhodobacter Sphaeroides Induces Trans suppression of bacteriochlorophyll and carotenoid levels in R. Sphaeroides and R. Capsulatus. Curr Microbiol 23: 259-263.
25. Ponnampalam, S.N., and Bauer, C.E. (1997) DNA binding characteristics of CrtJ. A redox-responding repressor of bacteriochlorophyll, carotenoid, and light harvesting-II gene expression in Rhodobacter capsulatus. J Biol Chem 272: 18391-18396.
26. Ponnampalam, S.N., Buggy, J.J., and Bauer, C.E. (1995) Characterization of an aerobic repressor that coordinately regulates bacteriochlorophyll, carotenoid, and light harvesting-II expression in Rhodobacter capsulatus. J Bacteriol 177: 2990-2997.
27. Poor, C.B., Chen, P.R., Duguid, E., Rice, P.A., and He, C. (2009) Crystal structures of the reduced, sulfenic acid, and mixed disulfide forms of SarZ, a redox active global regulator in Staphylococcus aureus. J Biol Chem 284: 23517-23524.
28. Reddie, K.G., and Carroll, K.S. (2008) Expanding the functional diversity of proteins through cysteine oxidation. Curr Opin Chem Biol 12: 746-754.
29. Reddie, K.G., Seo, Y.H., Muse Iii, W.B., Leonard, S.E., and Carroll, K.S. (2008) A chemical approach for detecting sulfenic acid-modified proteins in living cells. Mol Biosyst 4: 521-531.
30. Saurin, A.T., Neubert, H., Brennan, J.P., and Eaton, P. (2004) Widespread sulfenic acid formation in tissues in response to hydrogen peroxide. Proc Natl Acad Sci USA 101: 17982-17987.
31. Soonsanga, S., Lee, J.W., and Helmann, J.D. (2008) Oxidant-dependent switching between reversible and sacrificial oxidation pathways for Bacillus subtilis OhrR. Mol Microbiol 68: 978-986.
32. Torchinsky, Y.M. (1981) Properties of SH groups. Sulfhydryl reagents. In Sulfur in Proteins. Torchinsky, Y.M. (ed.). Oxford: Pergamon, p. 53.
33. Turell, L., Botti, H., Carballal, S., Ferrer-Sueta, G., Souza, J.M., Duran, R., etal. (2008) Reactivity of sulfenic acid in human serum albumin. Biochemistry 47: 358-367.
34. Zheng, M., Aslund, F., and Storz, G. (1998) Activation of the OxyR transcription factor by reversible disulfide bond formation. Science 279: 1718-1721.