A new way to degrade heme: The mycobacterium tuberculosis enzyme MhuD catalyzes heme degradation without generating CO

Journal of Biological Chemistry

Volumn 288, Issue 14, 2013, Pages 10101-10109

  Nambu, Shusuke ^a   Matsui, Toshitaka ^a   Goulding, Celia W ^b   Takahashi, Satoshi ^a   Ikeda Saito, Masao ^a  

^a TOHOKU UNIVERSITY   (Japan)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVE SITE STRUCTURE; CARBONYL GROUPS; HEME DEGRADATION; HEME-DEGRADING ENZYMES; MYCOBACTERIUM TUBERCULOSIS; PRODUCT ANALYSIS; SEQUENCE SIMILARITY; STAPHYLOCOCCUS AUREUS;

BACTERIA; CATALYSIS; DEGRADATION; ELECTROSPRAY IONIZATION; ENZYMES; TUBES (COMPONENTS);

PORPHYRINS;

ALANINE; BACTERIAL ENZYME; HEME OXYGENASE; HISTIDINE; PROTEIN MHUD; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; ARTICLE; CATALYSIS; CHROMATOPHORE; CONTROLLED STUDY; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME DEGRADATION; ENZYME METABOLISM; ENZYME STRUCTURE; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN FUNCTION;

BACTERIAL PROTEINS; CARBON MONOXIDE; CATALYTIC DOMAIN; GENE EXPRESSION REGULATION, BACTERIAL; HEME; HEME OXYGENASE (DECYCLIZING); MAGNETIC RESONANCE SPECTROSCOPY; MODELS, CHEMICAL; MYCOBACTERIUM TUBERCULOSIS; NADPH-FERRIHEMOPROTEIN REDUCTASE; OXYGENASES; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION; SPECTRUM ANALYSIS, RAMAN;

MYCOBACTERIUM TUBERCULOSIS; STAPHYLOCOCCUS AUREUS;

EID: 84875981467     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.448399     Document Type: Article

References (41)

1. Maines, M. D. (1997) The heme oxygenase system: A regulator of second messenger gases. Annu. Rev. Pharmacol. Toxicol. 37, 517-554
2. Poss, K. D., and Tonegawa, S. (1997) Reduced stress defense in heme oxygenase 1-deficient cells. Proc. Natl. Acad. Sci. U.S.A. 94, 10925-10930
3. Yoshida, T., and Kikuchi, G. (1978) Features of the reaction of heme degradation catalyzed by the reconstituted microsomal heme oxygenase system. J. Biol. Chem. 253, 4230-4236
4. Tenhunen, R., Marver, H. S., and Schmid, R. (1969) Microsomal heme oxygenase: characterization of the enzyme. J. Biol. Chem. 244, 6388-6394
5. Ortiz de Montellano, P. R. (1998) Heme oxygenase mechanism: Evidence for an electrophilic, ferric peroxide species. Acc. Chem. Res. 31, 543-549
6. Matsui, T., Unno, M., and Ikeda-Saito, M. (2010) Heme oxygenase reveals its strategy for catalyzing three successive oxygenation reactions. Acc. Chem. Res. 43, 240-247
7. Schmitt, M. P. (1997) Utilization of host iron sources by Corynebacterium diphtheriae: identification of a gene whose product is homologous to eukaryotic heme oxygenases and is required for acquisition of iron from heme and hemoglobin. J. Bacteriol. 179, 838-845
8. Wandersman, C., and Stojiljkovic, I. (2000) Bacterial heme sources: the role of heme, hemoprotein receptors and hemophores. Curr. Opin. Microbiol. 3, 215-220
9. Genco, C. A., and Dixon, D. W. (2001) Emerging strategies in microbial haem capture. Mol. Microbiol. 39, 1-11
10. Skaar, E. P., Gaspar, A. H., and Schneewind, O. (2004) IsdG and IsdI, heme-degrading enzymes in the cytoplasm of Staphylococcus aureus. J. Biol. Chem. 279, 436-443
11. Mazmanian, S. K., Skaar, E. P., Gaspar, A. H., Humayun, M., Gornicki, P., Jelenska, J., Joachmiak, A., Missiakas, D. M., and Schneewind, O. (2003) Passage of heme-iron across the envelope of Staphylococcus aureus. Science 299, 906-909
12. Lee, W. C., Reniere, M. L., Skaar, E. P., and Murphy, M. E. (2008) Ruffling of metalloporphyrins bound to IsdG and IsdI, two heme-degrading enzymes in Staphylococcus aureus. J. Biol. Chem. 283, 30957-30963
13. Reniere, M. L., Ukpabi, G. N., Harry, S. R., Stec, D. F., Krull, R., Wright, D. W., Bachmann, B. O., Murphy, M. E., and Skaar, E. P. (2010) The IsdG-family of haem oxygenases degrades haem to a novel chromophore. Mol. Microbiol. 75, 1529-1538
14. Ukpabi, G., Takayama, S. J., Mauk, A. G., and Murphy, M. E. (2012) Inactivation of the heme degrading enzyme IsdI by an active site substitution that diminishes heme ruffling. J. Biol. Chem. 287, 34179-34188
15. Haley, K. P., Janson, E. M., Heilbronner, S., Foster, T. J., and Skaar, E. P. (2011) Staphylococcus lugdunensis IsdG liberates iron from host heme. J. Bacteriol. 193, 4749-4757
16. Chim, N., Iniguez, A., Nguyen, T. Q., and Goulding, C. W. (2010) Unusual diheme conformation of the heme-degrading protein from Mycobacterium tuberculosis. J. Mol. Biol. 395, 595-608
17. Skaar, E. P., Gaspar, A. H., and Schneewind, O. (2006) Bacillus anthracis IsdG, a heme-degrading monooxygenase. J. Bacteriol. 188, 1071-1080
18. Puri, S., and O'Brian, M. R. (2006) The hmuQ and hmuD genes from Bradyrhizobium japonicum encode heme-degrading enzymes. J. Bacteriol. 188, 6476-6482
19. 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
20. Migita, C. T., Togashi, S., Minakawa, M., Zhang, X., and Yoshida, T. (2005) Evidence for the hydrophobic cavity of heme oxygenase-1 to be a CO trapping site. Biochem. Biophys. Res. Commun. 338, 584-589
21. Matera, K. M., Zhou, H., Migita, C. T., Hobert, S. E., Ishikawa, K., Katakura, K., Maeshima, H., Yoshida, T., and Ikeda-Saito, M. (1997) Histidine-132 does not stabilize a distal water ligand and is not an important residue for the enzyme activity in heme oxygenase-1. Biochemistry 36, 4909-4915
22. Takahashi, S., Wang, J., Rousseau, D. L., Ishikawa, K., Yoshida, T., Takeuchi, N., and Ikeda-Saito, M. (1994) Heme-heme oxygenase complex: Structure and properties of the catalytic site from resonance Raman scattering. Biochemistry 33, 5531-5538
23. Takahashi, S., Wang, J., Rousseau, D. L., Ishikawa, K., Yoshida, T., Host, J. R., and Ikeda-Saito, M. (1994) Heme-heme oxygenase complex: structure of the catalytic site and its implication for oxygen activation. J. Biol. Chem. 269, 1010-1014
24. Kerr, E. A., Mackin, H. C., and Yu, N. T. (1983) Resonance Raman studies of carbon monoxide binding to iron "picket fence" porphyrin with unhindered and hindered axial bases. An inverse relationship between binding affinity and the strength of iron-carbon bond. Biochemistry 22, 4373-4379
25. Kitagawa, T. (1988). in Biological Applications of Raman Spectroscopy (Spiro, T. G., ed) pp. 97-131, John Wiley & Sons, Inc., New York
26. Yonetani, T., Yamamoto, H., Erman, J. E., Leigh, J. S., Jr., and Reed, G. H. (1972) Electromagnetic properties of hemoproteins. V. Optical and electron paramagnetic resonance characteristics of nitric oxide derivatives of metalloporphyrin-apohemoprotein complexes. J. Biol. Chem. 247, 2447-2455
27. Shelnutt, J. A., Song, X. Z., Ma, J. G., Jia, S. L., Jentzen, W., and Medforth, C. J. (1998) Nonplanar porphyrins and their significance in proteins. Chem. Soc. Rev. 27, 31-41
28. Hawkins, B. K., Wilks, A., Powers, L. S., Ortiz de Montellano, P. R., and Dawson, J. H. (1996) Ligation of the iron in the heme-heme oxygenase complex: X-ray absorption, electronic absorption, and magnetic circular dichroism studies. Biochim. Biophys. Acta 1295, 165-173
29. Takayama, S. J., Ukpabi, G., Murphy, M. E., and Mauk, A. G. (2011) Electronic properties of the highly ruffled heme bound to the heme degrading enzyme IsdI. Proc. Natl. Acad. Sci. U.S.A. 108, 13071-13076
30. Antonini, E., and Brunori, M. (1971) Hemoglobin and Myoglobin in Their Reactions with Ligands, pp. 40-54, North-Holland Publishing Co., Amsterdam
31. Wu, R., Skaar, E. P., Zhang, R., Joachimiak, G., Gornicki, P., Schneewind, O., and Joachimiak, A. (2005) Staphylococcus aureus IsdG and IsdI, hemedegrading enzymes with structural similarity to monooxygenases. J. Biol. Chem. 280, 2840-2846
32. Pruzinská, A., Tanner, G., Anders, I., Roca, M., and Hörtensteiner, S. (2003) Chlorophyll breakdown: pheophorbide a oxygenase is a Riesketype iron-sulfur protein, encoded by the accelerated cell death 1 gene. Proc. Natl. Acad. Sci. U.S.A. 100, 15259-15264
33. 2-dependent verdoheme degradation by heme oxygenase: reaction mechanisms and potential physiological roles of the dual pathway degradation. J. Biol. Chem. 280, 36833-36840
34. Matsui, T., Omori, K., Jin, H., and Ikeda-Saito, M. (2008) Alkyl peroxides reveal the ring opening mechanism of verdoheme catalyzed by heme oxygenase. J. Am. Chem. Soc. 130, 4220-4221
35. Lai, W., Chen, H., Matsui, T., Omori, K., Unno, M., Ikeda-Saito, M., and Shaik, S. (2010) Enzymatic ring-opening mechanism of verdoheme by the heme oxygenase: A combined X-ray crystallography and QM/MM study. J. Am. Chem. Soc. 132, 12960-12970
36. Morishima, I., Fujii, H., Shiro, Y., and Sano, S. (1995) Studies on the iron(II) meso-oxyporphyrin π-neutral radical as a reaction intermediate in heme catabolism. Inorg. Chem. 34, 1528-1535
37. Suematsu, M., and Ishimura, Y. (2000) The heme oxygenase-carbon monoxide system: A regulator of hepatobiliary function. Hepatology 31, 3-6
38. Voskuil, M. I., Schnappinger, D., Visconti, K. C., Harrell, M. I., Dolganov, G. M., Sherman, D. R., and Schoolnik, G. K. (2003) Inhibition of respiration by nitric oxide induces a Mycobacterium tuberculosis dormancy program. J. Exp. Med. 198, 705-713
39. Roberts, D. M., Liao, R. P., Wisedchaisri, G., Hol, W. G., and Sherman, D. R. (2004) Two sensor kinases contribute to the hypoxic response of Mycobacterium tuberculosis. J. Biol. Chem. 279, 23082-23087
40. Shiloh, M. U., Manzanillo, P., and Cox, J. S. (2008) Mycobacterium tuberculosis senses host-derived carbon monoxide during macrophage infection. Cell Host Microbe 3, 323-330
41. Kumar, A., Deshane, J. S., Crossman, D. K., Bolisetty, S., Yan, B. S., Kramnik, I., Agarwal, A., and Steyn, A. J. (2008) Heme oxygenase-1-derived carbon monoxide induces the Mycobacterium tuberculosis dormancy regulon. J. Biol. Chem. 283, 18032-18039