The roles of Tyr(CD1) and Trp(G8) in mycobacterium tuberculosis truncated hemoglobin O in ligand binding and on the heme distal site architecture

Biochemistry

Volumn 46, Issue 41, 2007, Pages 11440-11450

  Ouellet, Hugues ^a,c   Milani, Mario ^b   LaBarre, Marie ^c   Bolognesi, Martino ^b   Couture, Manon ^c   Guertin, Michel ^c,d  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF MILAN   (Italy)

^c UNIVERSITÉ LAVAL   (Canada)

^d Pavillon Marchand ^*  (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING AND STABILIZATION; LIGAND BINDING; MYCOBACTERIUM TUBERCULOSIS; RESONANCE RAMAN;

BACTERIA; BINDING SITES; DISEASES; HEMOGLOBIN; LIGANDS; RAMAN SPECTROSCOPY; X RAY CRYSTALLOGRAPHY;

CRYSTAL STRUCTURE;

HAPTOGLOBIN O; HEME; HEMOGLOBIN; TYROSINE; UNCLASSIFIED DRUG;

ARTICLE; CRYSTAL STRUCTURE; DISSOCIATION; LIGAND BINDING; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PROTEIN INTERACTION; RAMAN SPECTROMETRY; SITE DIRECTED MUTAGENESIS; SPECTROPHOTOMETRY; X RAY CRYSTALLOGRAPHY;

AMINO ACID SUBSTITUTION; BACTERIAL PROTEINS; BINDING SITES; CRYSTALLOGRAPHY, X-RAY; DNA PRIMERS; HEME; HEMOGLOBINS; HYDROGEN BONDING; LIGANDS; MUTAGENESIS; SPECTRUM ANALYSIS, RAMAN; TRUNCATED HEMOGLOBINS; TRYPTOPHAN; TYROSINE;

MYCOBACTERIUM TUBERCULOSIS;

EID: 35348845951     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi7010288     Document Type: Article

References (47)

1. Milani, M., Savard, P. Y., Ouellet, H., Ascenzi, P., Guertin, M., and Bolognesi, M. (2003) A TyrCD1/TrpG8 hydrogen bond network and a TyrB10/TyrCD1 covalent link shape the heme distal site of Mycobacterium tuberculosis hemoglobin O, Proc. Natl. Acad. Sci. U.S.A. 100, 5766-5771.
2. Ouellet, H., Juszczak, L., Dantsker, D., Samuni, U., Ouellet, Y. H., Savard, P. Y., Wittenberg, J. B., Wittenberg, B. A., Friedman, J. M., and Guertin, M. (2003) Reactions of Mycobacterium tuberculosis truncated hemoglobin O with ligands reveal a novel ligand-inclusive hydrogen bond network, Biochemistry 42, 5764-5774.
3. Ouellet, H., Ouellet, Y., Richard, C., Labarre, M., Wittenberg, B., Wittenberg, J., and Guertin, M. (2002) Truncated hemoglobin HbN protects Mycobacterium bovis from nitric oxide, Proc. Natl. Acad. Sci. U.S.A. 99, 5902-5907.
4. Herold, S., Exner, M., and Nauser, T. (2001) Kinetic and mechanistic studies of the NO*-mediated oxidation of oxymyoglobin and oxyhemoglobin, Biochemistry 40, 3385-3395.
5. Eich, R. F., Li, T., Lemon, D. D., Doherty, D. H., Curry, S. R., Aitken, J. F., Mathews, A. J., Johnson, K. A., Smith, R. D., Phillips, G. N., Jr., and Olson, J. S. (1996) Mechanism of NO-induced oxidation of myoglobin and hemoglobin, Biochemistry 35, 6976-6983.
6. Ouellet, H., Ranguelova, K., Labarre, M., Wittenberg, J. B., Wittenberg, B. A., Magliozzo, R. S., and Guertin, M. (2007) Reaction of Mycobacterium tuberculosis truncated hemoglobin O with hydrogen peroxide: evidence for peroxidatic activity and formation of protein-based radicals, J. Biol. Chem. 282, 7491-7503.
7. Vuletich, D. A., and Lecomte, J. T. (2006) A phylogenetic and structural analysis of truncated hemoglobins, J. Mol. Evol. 62, 196-210.
8. Vinogradov, S. N., Hoogewijs, D., Bailly, X., Arredondo-Peter, R., Guertin, M., Gough, J., Dewilde, S., Moens, L., and Vanfleteren, J. R. (2005) Three globin lineages belonging to two structural classes in genomes from the three kingdoms of life, Proc. Natl. Acad. Sci. U.S.A. 102, 11385-11389.
9. Wittenberg, J. B., Bolognesi, M., Wittenberg, B. A., and Guertin, M. (2002) Truncated hemoglobins: a new family of hemoglobins widely distributed in bacteria, unicellular eukaryotes, and plants, J. Biol. Chem. 277, 871-874.
10. Giangiacomo, L., Ilari, A., Boffi, A., Morea, V., and Chiancone, E. (2005) The truncated oxygen-avid hemoglobin from Bacillus subtilis: X-ray structure and ligand binding properties, J. Biol. Chem. 280, 9192-9202.
11. Bonamore, A., Ilari, A., Giangiacomo, L., Bellelli, A., Morea, V., and Boffi, A. (2005) A novel thermostable hemoglobin from the actinobacterium Thermobifida fusca, FEBS J. 272, 4189-4201.
12. Ilari, A., Kjelgaard, P., von Wachenfeldt, C., Catacchio, B., Chiancone, E., and Boffi, A. (2007) Crystal structure and ligand binding properties of the truncated hemoglobin from Geobacillus stearothermophilus, Arch. Biochem. Biophys. 457, 85-94.
13. Watts, R. A., Hunt, P. W., Hvitved, A. N., Hargrove, M. S., Peacock, W. J., and Dennis, E. S. (2001) A hemoglobin from plants homologous to truncated hemoglobins of microorganisms, Proc. Natl. Acad. Sci. U.S.A. 98, 10119-10124.
14. Bolognesi, M., Bordo, D., Rizzi, M., Tarricone, C., and Ascenzi, P. (1997) Nonvertebrate hemoglobins: structural bases for reactivity, Prog. Biophys. Mol. Biol. 68, 29-68.
15. Milani, M., Pesce, A., Ouellet, Y., Dewilde, S., Friedman, J., Ascenzi, P., Guertin, M., and Bolognesi, M. (2004) Heme-ligand tunneling in group I truncated hemoglobins, J. Biol. Chem. 279, 21520-21525.
16. 2 diffusion to the heme, EMBO J. 20, 3902-3909.
17. Hargrove, M. S., and Olson, J. S. (1996) The stability of holomyoglobin is determined by heme affinity, Biochemistry 35, 11310-11318.
18. Ouellet, Y., Milani, M., Couture, M., Bolognesi, M., and Guertin, M. (2006) Ligand interactions in the distal heme pocket of Mycobacterium tuberculosis truncated hemoglobin N: roles of TyrB10 and GlnE11 residues, Biochemistry 45, 8770-8781.
19. (1994) Collaborative Computational Project, Number 4 (CCP4). The CCP4 suite. Programs for protein crystallography, Acta Crystallogr., Sect. D: Biol. Crystallogr. 50, 760-763.
20. Steller, I., Bolotovsky, R., and Rossmann, M. (1997) An Algorithm for Automatic Indexing of Oscillation Images using Fourier Analysis, J. Appl. Crystallogr. 30, 1036-1040.
21. Murshudov, G. N., Vagin, A. A., and Dodson, E. J. (1997) Refinement of macromolecular structures by the maximum-likelihood method, Acta Crystallogr., Sect. D: Biol. Crystallogr. 53, 240-255.
22. Berman, H. M., Westbrook, J., Feng, Z., Gilliland, G., Bhat, T. N., Weissig, H., Shindyalov, I. N., and Bourne, P. E. (2000) The Protein Data Bank, Nucleic Acids Res. 28, 235-242.
23. Mukai, M., Savard, P. Y., Ouellet, H., Guertin, M., and Yeh, S. R. (2002) Unique ligand-protein interactions in a new truncated hemoglobin from Mycobacterium tuberculosis, Biochemistry 41, 3897-3905.
24. Spiro, T. G., and Li, X. Y. (1988) Resonance Raman spectroscopy of metalloporphyrins, in Biological Applications of Raman Spectroscopy, John Wiley & Sons, New York.
25. Wang, J., Caughey, W. S., and Rousseau, D. L. (1996) Resonance Raman scattering: A probe of heme protein-bound nitric oxide, Methods Nitric Oxide Res., 427-454.
26. Spiro, T. G., and Wasbotten, I. H. (2005) CO as a vibrational probe of heme protein active sites, J. Inorg. Biochem. 99, 34-44.
27. Pesce, A., Nardini, M., Ascenzi, P., Geuens, E., Dewilde, S., Moens, L., Bolognesi, M., Riggs, A. F., Hale, A., Deng, P., Nienhaus, G. U., Olson, J. S., and Nienhaus, K. (2004) Thr-E11 regulates O2 affinity in Cerebratulus lacteus mini-hemoglobin, J. Biol. Chem. 279, 33662-33672.
28. Fe-O2 Raman bands for oxymyoglobin mutants, J. Am. Chem. Soc. 118, 7845-7846.
29. Springer, B. A., Sligar, S. G., Olson, J. S., and Phillips, G. N., Jr. (1994) Mechanisms of ligand recognition in myoglobin, Chem. Rev. 94, 699-714.
30. Zhao, X., Vyas, K., Nguyen, B. D., Rajarathnam, K., La Mar, G. N., Li, T., Phillips, G. N., Jr., Eich, R. F., Olson, J. S., Ling, J., and Bocian, D. F. (1995) A double mutant of sperm whale myoglobin mimics the structure and function of elephant myoglobin, J. Biol. Chem. 270, 20763-20774.
31. Crumpton, M. J., and Polson, A. (1965) A comparison of the conformation of sperm whale metmyoglobin with that of apomyoglobin, J. Mol. Biol. 11, 722-729.
32. Kawahara, K., Kirshner, A. G., and Tanford, C. (1965) Dissociation of human CO-hemoglobin by urea, guanidine hydrochloride, and other reagents, Biochemistry 4, 1203-1213.
33. 2 stretching modes in oxyhemoglobins, Proc. Natl. Acad. Sci. U.S.A. 98, 479-484.
34. Yeh, S. R., Couture, M., Ouellet, Y., Guertin, M., and Rousseau, D. L. (2000) A cooperative oxygen binding hemoglobin from Mycobacterium tuberculosis. Stabilization of heme ligands by a distal tyrosine residue, J. Biol. Chem. 275, 1679-1684.
35. Lu, C., Egawa, T., Wainwright, L. M., Poole, R. K., and Yeh, S. R. (2007) Structural and functional properties of a truncated hemoglobin from a food-borne pathogen Campylobacter jejuni, J. Biol. Chem., submitted.
36. Vojtechovsky, J., Chu, K., Berendzen, J., Sweet, R. M., and Schlichting, I. (1999) Crystal structures of myoglobin-ligand complexes at near-atomic resolution, Biophys. J. 77, 2153-2174.
37. Rohlfs, R. J., Mathews, A. J., Carver, T. E., Olson, J. S., Springer, B. A., Egeberg, K. D., and Sligar, S. G. (1990) The effects of amino acid substitution at position E7 (residue 64) on the kinetics of ligand binding to sperm whale myoglobin, J. Biol. Chem. 265, 3168-3176.
38. Olson, J. S., and Phillips, G. N., Jr. (1996) Kinetic pathways and barriers for ligand binding to myoglobin, J. Biol. Chem. 271, 17596.
39. 2, NO and CO by electrostatic interactions with the bound ligands, J. Biol. Inorg. Chem. 2, 544-552.
40. 2 entry into and exit from myoglobin, J. Biol. Chem. 276, 5177-5188.
41. Goldbeck, R. A., Bhaskaran, S., Ortega, C., Mendoza, J. L., Olson, J. S., Soman, J., Kliger, D. S., and Esquerra, R. M. (2006) Water and ligand entry in myoglobin: assessing the speed and extent of heme pocket hydration after CO photodissociation, Proc. Natl. Acad. Sci. U.S.A. 103, 1254-1259.
42. Nardini, M., Pesce, A., Labarre, M., Richard, C., Bolli, A., Ascenzi, P., Guertin, M., and Bolognesi, M. (2006) Structural determinants in the group III truncated hemoglobin from Campylobacter jejuni, J. Biol. Chem. 281, 37803-37812.
43. Couture, M., Das, T. K., Lee, H. C., Peisach, J., Rousseau, D. L., Wittenberg, B. A., Wittenberg, J. B., and Guertin, M. (1999) Chlamydomonas chloroplast ferrous hemoglobin. Heme pocket structure and reactions with ligands, J. Biol. Chem. 274, 6898-6910.
44. Couture, M., Das, T. K., Savard, P. Y., Ouellet, Y., Wittenberg, J. B., Wittenberg, B. A., Rousseau, D. L., and Guertin, M. (2000) Structural investigations of the hemoglobin of the cyanobacterium Synechocystis PCC6803 reveal a unique distal heme pocket, Eur. J. Biochem. 267, 4770-4780.
45. Das, T. K., Weber, R. E., Dewilde, S., Wittenberg, J. B., Wittenberg, B. A., Yamauchi, K., Van Hauwaert, M. L., Moens, L., and Rousseau, D. L. (2000) Ligand binding in the ferric and ferrous states of Paramecium hemoglobin, Biochemistry 39, 14330-14340.
46. Couture, M., Yeh, S. R., Wittenberg, B. A., Wittenberg, J. B., Ouellet, Y., Rousseau, D. L., and Guertin, M. (1999) A cooperative oxygen-binding hemoglobin from Mycobacterium tuberculosis, Proc. Natl. Acad. Sci. U.S.A. 96, 11223-11228.
47. Potterton, L., McNicholas, S., Krissinel, E., Gruber, J., Cowtan, K., Emsley, P., Murshudov, G. N., Cohen, S., Perrakis, A., and Noble, M. (2004) Developments in the CCP4 molecular-graphics project, Acta Crystallogr., Sect. D: Biol. Crystallogr. 60, 2288-2294.