Catalysis and oxygen binding of Ec DOS: A haem-based oxygen-sensor enzyme from Escherichia coli

Journal of Biochemistry

Volumn 148, Issue 6, 2010, Pages 693-703

  Kobayashi, Kazuo ^a   Tanaka, Atsunari ^b,c   Takahashi, Hiroto ^b   Igarashi, Jotaro ^b   Ishitsuka, Yukako ^b   Yokota, Nao ^b   Shimizu, Toru ^b  

^a OSAKA UNIVERSITY   (Japan)

^b TOHOKU UNIVERSITY   (Japan)

^c WISTAR INSTITUTE   (United States)

Author keywords

allosteric control; haem enzyme; O2 binding; oxygen sensor; phosphodiesterase; pulse radiolysis

Indexed keywords

DIMER; LIGAND; OXYGEN; PHOSPHODIESTERASE;

ALLOSTERISM; ARTICLE; CATALYSIS; ELECTRON BEAM; ENZYME ACTIVITY; ENZYME KINETICS; ESCHERICHIA COLI; MOLECULE; NONHUMAN; PULSE RADIOLYSIS; SENSOR;

BACTERIAL PROTEINS; BIOCATALYSIS; CATALYTIC DOMAIN; CLONING, MOLECULAR; ESCHERICHIA COLI; HEME; KINETICS; LIGANDS; MUTAGENESIS, SITE-DIRECTED; OXIDATION-REDUCTION; OXYGEN; PHOSPHORIC DIESTER HYDROLASES; PROTEIN BINDING; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, TERTIARY; PROTEIN SUBUNITS; PULSE RADIOLYSIS;

ESCHERICHIA COLI;

EID: 78649912237     PISSN: 0021924X     EISSN: 17562651     Source Type: Journal    
DOI: 10.1093/jb/mvq103     Document Type: Article

References (44)

1. Rodgers, K. R. (1999) Heme-based sensors in biological systems. Curr. Opin. Chem. Biol. 3, 158-167
2. Chan, M. K. (2000) CooA, CAP and allostery. Nat. Struct. Biol. 7, 822-824
3. Aono, S. and Nakajima, H. (1999) Structure and function of CooA, a novel transcriptional regulator containing a b-type heme as a CO sensor. Coord. Chem. Rev. 190-192, 267-282
4. Gilles-Gonzalez, M.-A. and Gonzalez, G. (2005) Heme-based sensors: defining characteristics, recent developments, and regulatory hypotheses. J. Inorg. Biochem. 99, 1-22
5. Uchida, T. and Kitagawa, T. (2005) Mechanism for transduction of the ligand-binding signal in heme-based gas sensory proteins revealed by resonance Raman spectroscopy. Acc. Chem. Res. 38, 662-670
6. Sasakura, Y., Yoshimura-Suzuki, T., Kurokawa, H., and Shimizu, T. (2006) Structure-function relationships of EcDOS, a heme-regulated phosphodiesterase from Escherichia coli. Acc. Chem. Res. 39, 37-43
7. Delgado-Nixon, V. M., Gonzalez, G., and Gilles-Gonzalez, M. A. (2000) Dos, a heme-binding PAS protein from Escherichia coli, is a direct oxygen sensor. Biochemistry 39, 2685-2691
8. Sasakura, Y., Hirata, S., Sugiyama, S., Suzuki, S., Taguchi, S., Watanabe, M., Matsui, T., Sagami, I., and Shimizu, T. (2002) Characterization of a direct oxygen sensor heme protein from E. coli: effects of the heme redox states and mutations at the heme binding site on catalysis and structure. J. Biol. Chem. 277, 23821-23827
9. Mendez-Oritz, M. M., Hyodo, M., Hayakawa, Y., and Membrillo-Hernandez, J. (2006) Genome-wide transcriptional profile of Escherichia coli in response to high levels of the second messenger 3', 5-cyclic diguanylic acid. J. Biol. Chem. 281, 8090-8099
10. Schmidt, A. J., Ryjenkov, D. A., and Gomelsky, M. (2005) The ubiquitous protein domain EAL is a cyclic diguanylate-specific phosphodiesterase: enzymatically active and inactive EAL domains. J. Bacteriol. 187, 4774-4781
11. 2 and CO binding. Chem. Lett. 35, 970-971
12. Tanaka, A., Takahashi, H., and Shimizu, T. (2007) Critical role of the heme axial ligand, Met95, in locking catalysis of the phosphodiesterase from Escherichia coli (Ec DOS) toward cyclic diGMP. J. Biol. Chem. 282, 21301-21307
13. Huang, S. H., Rio, D. C., and Marletta, M. A. (2007) Ligand binding and inhibition of an oxygen-sensitive soluble guanylate cyclase, Gyc-88E, from Drosophila. Biochemistry 46, 15115-15122
14. Kurokawa, H., Lee, D. S., Watanabe, M., Sagami, I., Mikami, B., Raman, C. S., and Shimizu, T. (2005) A redox-controlled molecular switch revealed by the crystal structure of a bacterial heme PAS sensor. J. Biol. Chem. 279, 20186-20193
15. Park, H. J., Suquet, C., Satterlee, J. D., and Kang, C. (2004) Insights into signal transduction involving PAS domain oxygen-sensing heme proteins from the X-ray crystal structure of Escherichia coli Dos heme domain (Ec DosH). Biochemistry 43, 2738-2746
16. Land, E. J. and Swallow, A. J. (1971) One-electron reactions in biochemical systems as studied by pulse radiolysis: V. Cytochrome. c. Arch. Biochem. Biophys. 145, 365-372
17. Kobayashi, K. and Hayashi, K. (1981) One-electron reduction in oxyform of hemoproteins. J. Biol. Chem. 256, 12350-12354
18. cam. J. Biol. Chem. 262, 5445-5447
19. Nakajima, H., Nakagawa, E., Kobayashi, K., Tagawa, S., and Aono, S. (2001) Ligand-switching intermediates for the CO-sensing transcriptional activator CooA measured by pulse radiolysis. J. Biol. Chem. 276, 37895-37899
20. Kobayashi, K., Koppenhofer, A., Ferguson, S. J., and Tagawa, S. (1997) Pulse radiolysis studies on cytochrome cd1 nitrite reductase from Thiosphaera pantotropha: evidence for a fast intramolecular electron transfer from c-heme to d1-heme. Biochemistry 36, 13611-13616
21. Rollema, H. S., Scholberg, H. P. F., de Bruin, S. H., and Raap, I. A. (1976) The kinetics of carbon monoxide binding to partially reduced methemoglobin. Biochem. Biophys. Res. Commun. 71, 997-1003
22. Ilan, Y. A., Samuni, A., Chevion, M., and Czapski, G. (1978) Quaternary states of methemoglobin and its valence-hybrid: a pulse radiolysis study. J. Biol. Chem. 253, 82-86
23. Chevion, M., Ilan, Y. A., Samuni, A., Navok, T., and Czapski, G. (1979) Quaternary structure of methemoglobin: pulse radiolysis study of the binding of oxygen to the valence hybrid. J. Biol. Chem. 254, 6370-6374
24. Raap, A., van Leeuwen, J. W., van Eck-Schouten, T., Rollema, H. S., and de Bruin, S. H. (1977) Heterogeneity in the kinetics of oxygen binding to partially reduced human methemoglobin. Eur. J. Biochem. 81, 619-626
25. Kobayashi, K. and Hayashi, K. (1990) Reduction of the oxy form in hemoproteins to the ferryl form. J. Am. Chem. Soc. 112, 6051-6053 (Pubitemid 20271843)
26. Suzuki, S., Kohzuma, T., Deligeer, Yamaguchi, K., Nakamura, N., Shidara, S., Kobayashi, K., and Tagawa, S. (1994) Pulse radiolysis studies on nitrite reductase from Achromobacter cycloclastes IAM 1013: evidence for intramolecular electron transfer from Type 1 Cu to Type 2 Cu. J. Am. Chem. Soc. 116, 11145-11146
27. Kobayashi, K., Tagawa, S., Daff, S., Sagami, I., and Shimizu, T. (2001) Rapid calmodulin-dependent interdomain electron transfer in neuronal nitric-oxide synthase measured by pulse radiolysis. J. Biol. Chem. 276, 39864-39871
28. Kobayashi, K. and Tagawa, S. (2003) Direct observation of guanine radical cation deprotonation in duplex DNA using pulse radiolysis. J. Am. Chem. Soc. 125, 10213-10218
29. Kobayashi, K., Mostafa, G., Tagawa, S., and Yamada, M. (2005) Transient formation of a neutral ubisemiquinone radical and subsequent intramolecular electron transfer to pyrroloquinoline quinone in the Escherichia coli membrane-integrated glucose dehydrogenase. Biochemistry 44, 13567-13572
30. Mustafa, G., Ishikawa, Y., Kobayashi, K., Migita, C. T., Elias, M. D., Nakamura, S., Tagawa, S., and Yamada, M. (2008) Amino acid residues interacting with both the bound quinone and coenzyme, pyrroloquinoline quinone, in Escherichia coli membrane-bound glucose dehydrogenas. J. Biol. Chem. 283, 22215-22221
31. 60 γ-ray irradiated solutions. J. Am. Chem. Soc. 86, 5343-5344
32. Yokota, N., Araki, Y., Kurokawa, H., Ito, O., Igarashi, J., and Shimizu, T. (2006) Critical roles of Leu99 and Leu115 at the heme distal side in auto-oxidation and the redox potential of a heme-regulated phosphodiesterase from Escherichia coli. FEBS J. 273, 1210-1223
33. 2. Biochemistry 47, 8874-8884
34. Gonzalez, G., Dioum, E. M., Bertolucci, CM., Tomita, T., Ikeda-Saito, M., Cheesman, M. R., Watmough, N. J., and Gilles-Gonzalez, M.-A. (2002) Nature of the displaceable heme-axial residue in the EcDos protein, a heme-based sensor from Escherichia coli. Biochemistry 41, 8414-8421
35. Taguchi, S., Matsui, T., Igarashi, J., Sasakura, Y., Araki, Y., Ito, O., Sugiyama, S., Sagami, I., and Shimizu, T. (2004) Binding of oxygen and carbon monoxide to a heme-regulated phosphodiesterase from Escherichia coli: kinetics and infrared spectra of the full-length wild-type enzyme, isolated PAS domain and Met95 mutants. J. Biol. Chem. 279, 3340-3347
36. Yoshimura, T., Sagami, I., Sasakura, I., and Shimizu, T. (2003) Relationships between heme incorporation, tetramer formation, and catalysis of a heme-regulated phosphodiesterase from Escherichia coli: a study of deletion and site-directed mutants. J. Biol. Chem. 278, 53105-53111
37. Lechauve, C., Bouzhir-Sima, L., Yamashita, T., Marden, M. C., Vos, M. H., Liebl, U., and Kiger, L. (2009) Heme ligand binding properties and intradimer interactions in the full-length sensor protein DOS from Escherichia coli and its isolated heme domain. J. Biol. Chem. 284, 36146-36159
38. Miksanova, M., Igarashi, J., Minami, M., Sagami, I., Yamauchi, S., Kurokawa, H., and Shimizu, T. (2006) Characterization of heme-regulated eIF2α kinase: roles of the N-terminal domain in the oligomeric state, heme binding, catalysis and inhibition. Biochemistry 45, 9894-9905
39. Gilles-Gonzalez, M. A. and Gonzalez, G. (2004) Signal transduction by heme-containing PAS-domain proteins. J. Appl. Phys. 96, 774-783
40. Tuckerman, J. R., Gonzalez, G., Sousa, E. H. S., Wan, X., Saito, J. A., Alam, M., and Gillez-Gonzalez, M. A. (2009) An oxygen-sensing diguanylate cyclase and phosphodiesterase couple for c-di-GMP control. Biochemistry 48, 9764-9774
41. El-Mashtoly, S. F., Nakashima, S., Tanaka, A., Shimizu, T., and Kitagawa, T. (2008) Roles of Arg97 and Phe113 in regulation of distal ligand binding to heme in the sensor domain of Ec DOS protein: resonance Raman and mutation study. J. Biol. Chem. 283, 19000-19010
42. Liebl, U., Bouzhir-Shima, L., Negrerie, M., Martin, J.-L., and Vos, M. H. (2002) Ultrafast ligand rebinding in the heme domain of the oxygen sensors FixL and Dos: general regulatory implications for heme-based sensors. Proc. Natl Acad. Sci. USA 99, 12771-12776
43. Liebl, U., Bouzhir-Shima, L., Kinger, L., Marden, M. C., Lambry, J.-C., Negrerie, M., and Vos, M. H. (2003) Ligand binding dynamics to the heme domain of the oxygen sensor Dos from Escherichia coli. Biochemistry 42, 6527-6535
44. Yamashita, T., Bouzhir-Shima, L., Lambry, J-C., Liebl, U., and Vos, M. H. (2008) Ligand dynamics and early signaling events in the heme domain of the sensor protein Dos from Escherichia coli. J. Biol. Chem. 283, 2344-2352