Ultrafast ligand dynamics in the heme-based GAF sensor domains of the histidine kinases DosS and DosT from Mycobacterium tuberculosis

Biochemistry

Volumn 51, Issue 1, 2012, Pages 159-166

  Vos, Marten H ^a,b   Bouzhir Sima, Latifa ^a,b   Lambry, Jean Christophe ^a,b   Luo, Hao ^c   Eaton Rye, Julian J ^c   Ioanoviciu, Alexandra ^d   De Montellano, Paul R Ortiz ^d   Liebl, Ursula ^a,b  

^a LABORATOIRE D OPTIQUE ET BIOSCIENCES   (France)

^b INSERM   (France)

^c UNIVERSITY OF OTAGO   (New Zealand)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CO REBINDING; HEME POCKETS; HISTIDINE KINASE; INITIAL PHASIS; INITIAL PROCESS; LIGAND BINDING; LIGAND DISSOCIATION; M. TUBERCULOSIS; MOLECULAR DYNAMICS SIMULATIONS; MYCOBACTERIUM TUBERCULOSIS; PICOSECONDS; SENSOR DOMAINS; TIME-RESOLVED ABSORPTION; TIME-SCALES; TRANSCRIPTIONAL REGULATOR; ULTRA-FAST;

AMINO ACIDS; DISSOCIATION; DYNAMICS; ENZYMES; HYDROGEN BONDS; LIGANDS; MOLECULAR DYNAMICS; PROTEINS; SENSORS; TUBES (COMPONENTS);

PORPHYRINS;

BACTERIAL PROTEIN; PROTEIN DOSS; PROTEIN DOST; PROTEIN HISTIDINE KINASE; UNCLASSIFIED DRUG;

ABSORPTION SPECTROSCOPY; ARTICLE; ENZYME ANALYSIS; ENZYME STRUCTURE; MOLECULAR DYNAMICS; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN;

BACTERIAL PROTEINS; BIOSENSING TECHNIQUES; CRYSTALLOGRAPHY, X-RAY; HEMEPROTEINS; HYDROGEN BONDING; LIGANDS; MOLECULAR DYNAMICS SIMULATION; MYCOBACTERIUM TUBERCULOSIS; PROTAMINE KINASE; PROTEIN BINDING; PROTEIN KINASES; PROTEIN STRUCTURE, TERTIARY; SIGNAL TRANSDUCTION; TYROSINE;

MYCOBACTERIUM TUBERCULOSIS;

EID: 84856856163     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi201467c     Document Type: Article

References (32)

1. World Health Organization (2010) Global Tuberculosis Control.
2. Wayne, L. G., and Sohaskey, C. D. (2001) Nonreplicating persistence of Mycobaterium tuberculosis. Annu. Rev. Microbiol. 55, 139-163.
3. Nathan, C., and Shiloh, M. U. (2000) Reactive oxygen and nitrogen intermediates in the relationship between mammalian hosts and microbial pathogens. Proc. Natl. Acad. Sci. U. S. A. 97, 8841-8848. (Pubitemid 30626635)
4. Sherman, D. R., Voskuil, M., Schnappinger, D., Liao, R., Harrell, M. I., and Schoolnik, G. K. (2001) Regulation of the Mycobacterium tuberculosis hypoxic response gene encoding a-Crystallin. Proc. Natl. Acad. Sci. U. S. A. 98, 7534-7539. (Pubitemid 32567983)
5. Roberts, D. M., Liao, R. P., Wisedchaisri, G., Hol, W. G. J., and Sherman, D. R. (2004) Two Sensor Kinases Contribute to the Hypoxic Response of Mycobacterium tuberculosis. J. Biol. Chem. 279, 23082-23087. (Pubitemid 38685612)
6. Sardiwal, S., Kendall, S. L., Movahedzadeh, F., Rison, S. C. G., Stoker, N. G., and Djordjevic, S. (2005) A GAF Domain in the Hypoxia/NO-inducible Mycobacterium tuberculosis DosS Protein Binds Haem. J. Mol. Biol. 353, 929-936. (Pubitemid 41503261)
7. Sousa, E. H. S., Tuckerman, J. R., Gonzalez, G., and Gilles-Gonzalez, M. A. (2007) DosT and DevS are oxygen-switched kinases in Mycobacterium tuberculosis. Protein Sci. 16, 1708-1719. (Pubitemid 47195697)
8. Honaker, R. W., Leistikow, R. L., Bartek, I. L., and Voskuil, M. I. (2009) Unique Roles of DosT and DosS in DosR Regulon Induction and Mycobacterium tuberculosis Dormancy. Infect. Immun. 77, 3258-3263.
9. Kim, M.-J., Park, K.-J., Ko, I.-J., Kim, Y. M., and Oh, J.-I. (2010) Different Roles of DosS and DosT in the Hypoxic Adaptation of Mycobacteria. J. Bacteriol. 192, 4868-4875.
10. Ioanoviciu, A., Yukl, E. T., Moënne-Loccoz, P., and Ortiz de Montellano, P. R. (2007) DevS, a Heme-Containing Two-Component Oxygen Sensor of Mycobacterium tuberculosis. Biochemistry 46, 4250-4260. (Pubitemid 46559392)
11. Ioanoviciu, A., Meharenna, Y. T., Poulos, T. L., and Ortiz de Montellano, P. R. (2009) DevS Oxy Complex Stability Identifies This Heme Protein as a Gas Sensor in Mycobacterium tuberculosis Dormancy. Biochemistry 48, 5839-5848.
12. Kumar, A., Toledo, J. C., Patel, R. P., Lancaster, J. R., and Steyn, A. J. C. (2007) Mycobacterium tuberculosis DosS is a redox sensor and DosT is a hypoxia sensor. Proc. Natl. Acad. Sci. U. S. A. 104, 11568-11573. (Pubitemid 47175053)
13. Yukl, E. T., Ioanoviciu, A., Sivaramakrishnan, S., Nakano, M. M., Ortiz de Montellano, P. R., and Moënne-Loccoz, P. (2011) Nitric Oxide Dioxygenation Reaction in DevS and the Initial Response to Nitric Oxide in Mycobacterium tuberculosis. Biochemistry 50, 1023-1028.
14. Cho, H. Y., Cho, H. J., Kim, Y. M., Oh, J. I., and Kang, B. S. (2009) Structural Insight into the Heme-based Redox Sensing by DosS from Mycobacterium tuberculosis. J. Biol. Chem. 284, 13057-13067.
15. Podust, L. M., Ioanoviciu, A., and Ortiz de Montellano, P. R. (2008) 2.3 Ã X-ray Structure of the Heme-Bound GAF Domain of Sensory Histidine Kinase DosT of Mycobacterium tuberculosis. Biochemistry 47, 12523-12531.
16. Yukl, E. T., Ioanoviciu, A., Nakano, M. M., Ortiz de Montellano, P. R., and Moënne-Loccoz, P. (2008) A Distal Tyrosine Residue Is Required for Ligand Discrimination in DevS from Mycobacterium tuberculosis. Biochemistry 47, 12532-12539.
17. Vos, M. H. (2008) Ultrafast dynamics of ligands within heme proteins. Biochim. Biophys. Acta 1777, 15-31.
18. Négrerie, M., Bouzhir-Sima, L., Martin, J.-L., and Liebl, U. (2001) Control of nitric oxide dynamics by guanylate cyclase in its activated state. J. Biol. Chem. 276, 46815-46821.
19. Kumazaki, S., Nakajima, H., Sakaguchi, T., Nakagawa, E., Shinahara, H., Yoshihara, K., and Aono, S. (2000) Dissociation and recombination between ligands and heme in a CO-sensing transcriptional activator CooA. J. Biol. Chem. 275, 38378-38383. (Pubitemid 32009161)
20. Jasaitis, A., Hola, K., Bouzhir-Sima, L., Lambry, J.-C., Balland, V., Vos, M. H., and Liebl, U. (2006) Role of distal arginine in early sensing intermediates in the heme domain of the oxygen sensor FixL. Biochemistry 45, 6018-6026. (Pubitemid 43727094)
21. Kruglik, S. G., Jasaitis, A., Hola, K., Yamashita, T., Liebl, U., Martin, J.-L., and Vos, M. H. (2007) Subpicosecond Oxygen Trapping in the Heme Pocket of the Oxygen Sensor FixL Observed by Time-Resolved Resonance Raman Spectroscopy. Proc. Natl. Acad. Sci. U. S. A. 104, 7408-7413. (Pubitemid 47185919)
22. 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.
23. Liebl, U., Bouzhir-Sima, L., Négrerie, 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. U. S. A. 99, 12771-12776.
24. Liebl, U., Bouzhir-Sima, L., Kiger, L., Marden, M. C., Lambry, J.-C., Négrerie, 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. (Pubitemid 36665828)
25. Yamashita, T., Bouzhir-Sima, L., Lambry, J.-C., Liebl, U., and Vos, M. H. (2008) Ligand dynamics and early signalling events in the heme domain of the sensor protein Dos from Escherichia coli. J. Biol. Chem. 283, 2344-2352.
26. Silkstone, G., Jasaitis, A., Wilson, M. T., and Vos, M. H. (2007) Ligand dynamics in an electron-transfer protein: picosecond geminate recombination of carbon monoxide to heme in mutant forms of cytochrome c. J. Biol. Chem. 282, 1638-1649. (Pubitemid 47076704)
27. Brooks, B. R., Bruccoleri, R. E., Olafson, B. D., Swaminathan, S., and Karplus, M. (1983) CHARMM: A Program for Macromolecular Energy, Minimization, and Dynamics Calculations. J. Comput. Chem. 4, 187-212.
28. Petrich, J. W., Poyart, C., and Martin, J.-L. (1988) Photophysics and reactivity of heme proteins: a femtosecond absorption study of hemoglobin, myoglobin and protoheme. Biochemistry 27, 4049-4060.
29. Gilles-Gonzalez, M. A., Gonzalez, G., Perutz, M. F., Kiger, L., Marden, M. C., and Poyart, C. (1994) Heme-based sensors, exemplified by the kinase FixL, are a new class of heme protein with distinctive ligand binding and autoxidation. Biochemistry 33, 8067-8073. (Pubitemid 24223828)
30. Ye, X., Yu, A., and Champion, P. M. (2006) Dynamics of Nitric Oxide Rebinding and Escape in Horseradish Peroxidase. J. Am. Chem. Soc. 128, 1444-1445. (Pubitemid 43214845)
31. Ye, X., Demidov, A., and Champion, P. M. (2002) Measurements of the Photodissociation Quantum Yields of MbNO and MbO2 and the Vibrational Relaxation of the Six-Coordinate Heme Species. J. Am. Chem. Soc. 124, 5914-5924. (Pubitemid 34533531)
32. Pettersen, E. F., Goddard, T. D., Huang, C. C., Couch, G. S., Greenblatt, D. M., Meng, E. C., and Ferrin, T. E. (2004) UCSF Chimera?A visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605-1612.