Purification and spectroscopic characterization of Ctb, a group III truncated hemoglobin implicated in oxygen metabolism in the food-borne pathogen Campylobacter jejuni

Biochemistry

Volumn 45, Issue 19, 2006, Pages 6003-6011

  Wainwright, Laura M ^a   Wang, Yinghua ^b   Park, Simon F ^c   Yeh, Syun Ru ^b   Poole, Robert K ^a  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

^b ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^c UNIVERSITY OF SURREY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA; BIODIVERSITY; DETOXIFICATION; GENES; HEMOGLOBIN; METABOLISM; PATHOLOGY; RAMAN SCATTERING;

FOOD-BORNE BACTERIAL PATHOGEN; OPTICAL SPECTRA; RAMAN ANALYSIS; TRUNCATED HEMOGLOBIN (CTB);

MICROORGANISMS;

BACTERIAL PROTEIN; CARBON MONOXIDE; FERRIC ION; FERROUS ION; HEMOGLOBIN; HISTIDINE; LIGAND; MONOMER; OXIDOREDUCTASE; OXYGEN; PROTEIN CTB; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; TRYPTOPHAN; TYROSINE; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL METABOLISM; CAMPYLOBACTER JEJUNI; CGB GENE; CTB GENE; DETOXIFICATION; MOLECULAR STABILITY; MUTANT; NONHUMAN; NUCLEOTIDE SEQUENCE; OXYGEN TRANSPORT; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN PURIFICATION; RAMAN SPECTROMETRY; SPECTRAL SENSITIVITY;

AMINO ACID SEQUENCE; BASE SEQUENCE; CAMPYLOBACTER JEJUNI; DNA PRIMERS; HEMOGLOBINS; MOLECULAR SEQUENCE DATA; OXYGEN; SEQUENCE HOMOLOGY, AMINO ACID; SPECTRUM ANALYSIS, RAMAN;

BACTERIA (MICROORGANISMS); CAMPYLOBACTER JEJUNI;

EID: 33646589058     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi052247k     Document Type: Article

References (53)

1. 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.
2. Wu, G., Wainwright, L. M., and Poole, R. K. (2005) Microbial globins, Adv. Microb. Physiol. 47, 255-310.
3. Membrillo-Hernández, J., Coopamah, M. D., Anjum, M. F., Stevanin, T. M., Kelly, A., Hughes, M. N., and Poole, R. K. (1999) The flavohemoglobin of Escherichia coli confers resistance to a nitrosating agent, a "nitric oxide releaser," and paraquat and is essential for transcriptional responses to oxidative stress, J. Biol. Chem. 274, 748-754.
4. Crawford, M. J., and Goldberg, D. E. (1998) Role for the Salmonella flavohemoglobin in protection from nitric oxide, J. Biol. Chem. 273, 12543-12547.
5. Liu, L. M., Zeng, M., Hausladen, A., Heitman, J., and Stomler, J. S. (2000) Protection from nitrosative stress by yeast flavohemoglobin, Proc. Natl. Acad. Sci. U.S.A. 97, 4672-4676.
6. Poole, R. K., and Hughes, M. N. (2000) New functions for the ancient globin family: bacterial responses to nitric oxide and nitrosative stress, Mol. Microbiol. 36, 775-783.
7. Gardner, P. R., Gardner, A. M., Brashear, W. T., Suzuki, T., Hvitved, A. N., Setchell, K. D. R., and Olson, J. S. (2006) Hemoglobins dioxygenate nitric oxide with high fidelity, J. Inorg. Biochem. 100, 542-550.
8. Park, K. W., Kim, K. J., Howard, A. J., Stark, B. C., and Webster, D. A. (2002) Vitreoscilla hemoglobin binds to subunit I of cytochrome bo ubiquinol oxidases, J. Biol. Chem. 277, 33334-33337.
9. Elvers, K. T., Wu, G., Gilberthorpe, N. J., Poole, R. K., and Park, S. F. (2004) Role of an inducible single-domain hemoglobin in mediating resistance to nitric oxide and nitrosative stress in Campylobacter jejuni and Campylobacter coli, J. Bacteriol. 186, 5332-5341.
10. Elvers, K. T., Turner, S. M., Wainwright, L. M., Marsden, G., Hinds, J., Cole, J. A., Poole, R. K., Penn, C. W., and Park, S. F. (2005) NssR, a member of the Crp-Fnr superfamily from Campylobacter jejuni, regulates a nitrosative stress-responsive regulon that includes both a single-domain and a truncated haemoglobin, Mol. Microbiol. 57, 735-750.
11. Pesce, A., Couture, M., Dewilde, S., Guertin, M., Yamauchi, K., Ascenzi, P., Moens, L., and Bolognesi, M. (2000) A novel two-over-two alpha-helical sandwich fold is characteristic of the truncated hemoglobin family, EMBO J. 19, 2424-2434.
12. 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.
13. Egawa, T., and Yeh, S.-R. (2005) Structural and functional properties of hemoglobins from unicellular organisms as revealed by resonance Raman spectroscopy, J. Inorg. Biochem. 99, 72-96.
14. 2 diffusion to the heme, EMBO J. 20, 3902-3909.
15. 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.
16. Hoy, J. A., Kundu, S., Trent, J. T., Ramaswamy, S., and Hargrove, M. S. (2004) The crystal structure of Synechocystis hemoglobin with a covalent heme linkage, J. Biol. Chem. 279, 16535-16542.
17. Milani, M., Pesce, A., Bolognesi, M., and Ascenzi, P. (2001) Truncated hemoglobins: trimming the classical 'three-over-three' globin fold to a minimal size, Biochem. Mol. Biol. Edu. 29, 123-125.
18. Pathania, R., Navani, N. K., Rajomohan, G., and Dikshit, K. L. (2002) Mycobacterium tuberculosis hemoglobin HbO associates with membranes and stimulates cellular respiration of recombinant Escherichia coli, J. Biol. Chem. 277, 15293-15302.
19. Wainwright, L. M., Elvers, K. T., Park, S. F., and Poole, R. K. (2005) A truncated haemoglobin implicated in oxygen metabolism by the microaerophilic food-borne pathogen Campylobacter jejuni, Microbiology (Reading, U.K.) 151, 4079-4091.
20. Friedman, C. R., Neimann, J., Wegener, H. C., and Tauxe, R. V. (2000) in Campylobacter (Nachamkin, I., and Blaser, M. J., Eds.) 2nd ed., pp 121-138, ASM Press, Washington, DC.
21. Pitcher, D. G., Saunders, N. A., and Owen, R. J. (1989) Rapid extraction of bacterial genomic DNA with guanidium thiocyanate, Lett. Appl. Microbiol. 8, 151-156.
22. Inoue, H., Nojima, N., and Okayama, H. (1990) High efficiency transformation of Escherichia coli with plasmids, Gene 96, 23-28.
23. Kalnenieks, U., Galinina, N., Bringer-Meyer, S., and Poole, R. K. (1998) Membrane D-lactate oxidase in Zymomonas mobilis: evidence for a branched respiratory chain, FEMS Microbiol. Lett. 168, 91-97.
24. Dutton, P. L. (1978) Redox potentiometry: determination of midpoint potentials of oxidation-reduction components of biological electron-transfer systems, Methods Enzymol. 54, 411-435.
25. 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.
26. Yeh, S. R., Couture, M., Ouellet, Y., Guertin, M., and Rousseau, D. L. (2000) A cooperative oxygen finding hemoglobin from Mycobacterium tuberculosis - Stabilization of heme ligands by a distal tyrosine residue, J. Biol. Chem. 275, 1679-1684.
27. Lemberg, R., and Barrett, J. (1973) Cytochromes, Academic Press, London.
28. Li, X.-Y., and Spiro, T. G. (1988) Is bound CO linear or bent in heme proteins? Evidence from resonance Raman and infrared spectroscopic data, J. Am. Chem. Soc. 110, 6024-6033.
29. Ray, G. B., Li, X.-Y., Ibers, J. A., Sessler, J. L., and Spiro, T. G. (1994) How far can proteins bend the FeCO unit? Distal polar and steric effects in heme proteins and models, J. Am. Chem. Soc. 116, 162-176.
30. Vogel, K. M., Kozlowski, P. M., Zgierski, M. Z., and Spiro, T. G. (2000) Role of the axial ligand in heme-CO backbonding; DFT analysis of vibrational data, Inorg. Chim. Acta 297, 11-17.
31. Mukai, M., Mills, C. E., Poole, R. K., and Yeh, S. R. (2001) Flavohemoglobin, a globin with a peroxidase-like catalytic site, J. Biol. Chem. 276, 7272-7277.
32. Antonini, E., and Brunori, M. (1971) Hemoglobin and Myoglobin in Their Reactions with Ligands, North-Holland Publishing, Amsterdam, The Netherlands.
33. Poole, R. K., Ioannidis, N., and Orii, Y. (1994) Reactions of the Escherichia coli flavohaemoglobin (Hmp) with oxygen and reduced nicotinamide adenine dinucleotide: evidence for oxygen switching of flavin oxidoreduction and a mechanism for oxygen sensing, Proc. R. Soc. London, Ser. B 255, 251-258.
34. 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.
35. 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.
36. Samuni, A., Ouellet, Y., Guertin, M., Friedman, J. M., and Yeh, S.-R. (2004) The absence of proximal strain in the truncated hemoglobins from Mycobacterium tuberculosis, J. Am. Chem. Soc. 126, 2682-2683.
37. Das, T. K., Weber, R. E., Dewilde, S., Wittenberg, J. B., Wittenberg, B. A., Yamauchi, K., VanHauwaert, M. L., Moens, L., and Rousseau, D. L. (2000) Ligand binding in the ferric and ferrous states of Paramecium hemoglobin, Biochemistry 39, 14330-14340.
38. Friedman, J. M., Scott, T. W., Stepnoski, R. A., Ikeda-Saito, M., and Yonetani, T. (1983) The iron-proximal histidine linkage and protein control of oxygen binding in hemoglobin. A transient Raman study, J. Biol. Chem. 258, 10564-10572.
39. 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.
40. Ouellett, H., Ouellett, 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.
41. Mukai, M., Ouellet, Y., Ouellet, H., Guertin, M., and Yeh, S. R. (2004) No binding induced conformational changes in a truncated hemoglobin from Mycobacterium tuberculosis, Biochemistry 43, 2764-2770.
42. Crespo, A., Marti, M. A., Kalko, S. G., Morreale, A., Orozco, M., Gelpi, J. L., Luque, F. J., and Estrin, D. A. (2005) Theoretical study of the truncated hemoglobin HbN: Exploring the molecular basis of the NO detoxification mechanism, J. Am. Chem. Soc. 127, 4433-4444.
43. 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.
44. 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.
45. Liu, C., He, Y., and Chang, Z. Y. (2004) Truncated hemoglobin o of Mycobacterium tuberculosis: the oligomeric state change and the interaction with membrane components, Biochem. Biophys. Res. Commun. 316, 1163-1172.
46. Ascenzi, P., Bocedi, A., Bolognesi, M., Fabozzi, G., Milani, M., and Visca, P. (2006) Nitric oxide scavenging by Mycobacterium leprae GlbO involves the formation of the ferric heme-bound peroxynitrite intermediate, Biochem. Biophys. Res. Commun. 339, 450-456.
47. m values for oxygen are in the submicromolar range. J. Bacteriol. 177, 867-870.
48. D'mello, R., Hill, S., and Poole, R. K. (1996) The cytochrome bd quinol oxidase in Escherichia coli has an extremely high oxygen affinity and two oxygen-binding haems: implications for regulation of activity in vivo by oxygen inhibition, Microbiology 142, 755-763.
49. Pesci, E. C., Cottle, D. L. and Pickett, C. L. (1994) Genetic, enzymatic and pathogenic studies of the iron superoxide dismutase of Campylobacter jejuni, Infect. Immun. 62, 2687-2694.
50. Frey, A. D., Farres, J., Bollinger, C. J. T., and Kallio, P. T. (2002) Bacterial hemoglobins and flavohemoglobins for alleviation of nitrosative stress in Escherichia coli, Appl. Environ. Microbiol. 68, 4835-4840.
51. Brunori, M., Saggese, U., Rotilio, G. C., Antonini, E., and Wyman, J. (1971) Redox equilibrium of sperm-whale myoglobin, Aplysia myoglobin and Chironomus thummi hemoglobin, Biochemistry 10, 1604-1609.
52. Dorman, S. C., Harrington, J. P., Martin, M. S., and Johnson, T. V. (2004) Determination of the formal reduction potential of Lumbricus terrestris hemoglobin using thin layer spectroelectrochemistry, J. Inorg. Biochem. 98, 185-188.
53. Tyree, B., and Webster, D. A. (1978) Electron-accepting properties of cytochrome o purified from Vitreoscilla, J. Biol. Chem. 253, 7635-7637.