Heme utilization by pathogenic bacteria: Not all pathways lead to biliverdin

Accounts of Chemical Research

Volumn 47, Issue 8, 2014, Pages 2291-2298

  Wilks, Angela ^a   Ikeda Saito, Masao ^b  

^a UNIVERSITY OF MARYLAND SCHOOL OF PHARMACY   (United States)

^b TOHOKU UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BILIVERDIN; CARBON MONOXIDE; ENZYME; HEME; HEME OXYGENASE; IRON;

BACTERIUM; CHEMISTRY; CHINESE MEDICINE; CORYNEBACTERIUM DIPHTHERIAE; ENZYMOLOGY; HYDROXYLATION; METABOLISM; NEISSERIACEAE; OXIDATION REDUCTION REACTION; PROTEIN TERTIARY STRUCTURE; PSEUDOMONAS AERUGINOSA;

BACTERIA; BILIVERDINE; CARBON MONOXIDE; CORYNEBACTERIUM DIPHTHERIAE; ENZYMES; HEME; HEME OXYGENASE (DECYCLIZING); HYDROXYLATION; IRON; NEISSERIACEAE; OXIDATION-REDUCTION; PROTEIN STRUCTURE, TERTIARY; PSEUDOMONAS AERUGINOSA; YIN-YANG;

EID: 84906242486     PISSN: 00014842     EISSN: 15204898     Source Type: Journal    
DOI: 10.1021/ar500028n     Document Type: Article

References (82)

1. Frankenberg-Dinkel, N. Bacterial heme oxygenases Antioxid. Redox Signaling 2004, 6, 825-834
2. Wilks, A. Heme oxygenase: Evolution, structure, and mechanism Antioxid. Redox Signaling 2002, 4, 603-614
3. Wilks, A.; Burkhard, K. A. Heme and virulence: How bacterial pathogens regulate, transport and utilize heme Nat. Prod. Rep. 2007, 24, 511-522
4. Brickman, T. J.; Hanawa, T.; Anderson, M. T.; Suhadolc, R. J.; Armstrong, S. K. Differential expression of Bordetella pertussis iron transport system genes during infection Mol. Microbiol. 2008, 70, 3-14
5. Skaar, E. P.; Gaspar, A. H.; Schneewind, O. IsdG and IsdI, heme-degrading enzymes in the cytoplasm of Staphylococcus aureus J. Biol. Chem. 2004, 279, 436-443
6. Morton, D. J.; Seale, T. W.; Vanwagoner, T. M.; Whitby, P. W.; Stull, T. L. The dppBCDF gene cluster of Haemophilus influenzae: Role in heme utilization BMC Res. Notes 2009, 2, 166
7. Wilks, A.; Schmitt, M. P. Expression and characterization of a heme oxygenase (HmuO) from Corynebacterium diphtheriae. Iron acquisition requires oxidative cleavage of the heme macrocycle J. Biol. Chem. 1998, 273, 837-841
8. Zhu, W.; Wilks, A.; Stojiljkovic, I. Degradation of heme in Gram-negative bacteria: The product of the hemO gene of Neisseriae is a heme oxygenase J. Bacteriol. 2000, 182, 6783-6790
9. Ratliff, M.; Zhu, W.; Deshmukh, R.; Wilks, A.; Stojiljkovic, I. Homologues of Neisserial heme oxygenase in Gram-negative bacteria: Degradation of heme by the product of the pigA gene of Pseudomonas aeruginosa J. Bacteriol. 2001, 183, 6394-6403
10. Skaar, E. P.; Gaspar, A. H.; Schneewind, O. Bacillus anthracis IsdG, a heme-degrading monooxygenase J. Bacteriol. 2006, 188, 1071-1080
11. Chim, N.; Iniguez, A.; Nguyen, T. Q.; Goulding, C. W. Unusual diheme conformation of the heme-degrading protein from Mycobacterium tuberculosis J. Mol. Biol. 2010, 395, 595-608
12. Reniere, M. L.; Ukpabi, G. N.; Harry, S. R.; Stec, D. F.; Krull, R.; Wright, D. W.; Bachmann, B. O.; Murphy, M. E.; Skaar, E. P. The IsdG-family of haem oxygenases degrades haem to a novel chromophore Mol. Microbiol. 2010, 75, 1529-1538
13. Matsui, T.; Nambu, S.; Ono, Y.; Goulding, C. W.; Tsumoto, K.; Ikeda-Saito, M. Heme degradation by Staphylococcus aureus IsdG and IsdI liberates formaldehyde rather than carbon monoxide Biochemistry 2013, 52, 3025-3027
14. Nambu, S.; Matsui, T.; Goulding, C. W.; Takahashi, S.; Ikeda-Saito, M. A New Way to Degrade Heme: The Mycobacterium tuberculosis enzyme MhuD catalyzes heme degradation without generating CO J. Biol. Chem. 2013, 288, 10101-10109
15. Kim, H. P.; Ryter, S. W.; Choi, A. M. CO as a cellular signaling molecule Annu. Rev. Pharmacol. Toxicol. 2006, 46, 411-449
16. Rochette, L.; Cottin, Y.; Zeller, M.; Vergely, C. Carbon monoxide: Mechanisms of action and potential clinical implications Pharmacol. Ther. 2013, 137, 133-152
17. Snyder, S. H.; Baranano, D. E. Heme oxygenase: A font of multiple messengers Neuropsychopharmacology 2001, 25, 294-298
18. Wegiel, B.; Hanto, D. W.; Otterbein, L. E. The social network of carbon monoxide in medicine Trends Mol. Med. 2013, 19, 3-11
19. Antuni, J. D.; Kharitonov, S. A.; Hughes, D.; Hodson, M. E.; Barnes, P. J. Increase in exhaled carbon monoxide during exacerbations of cystic fibrosis Thorax 2000, 55, 138-142
20. Kumar, A.; Deshane, J. S.; Crossman, D. K.; Bolisetty, S.; Yan, B. S.; Kramnik, I.; Agarwal, A.; Steyn, A. J. Heme oxygenase-1-derived carbon monoxide induces the Mycobacterium tuberculosis dormancy regulon J. Biol. Chem. 2008, 283, 18032-18039
21. Tavares, A. F.; Nobre, L. S.; Saraiva, L. M. A role for reactive oxygen species in the antibacterial properties of carbon monoxide-releasing molecules FEMS Microbiol. Lett. 2012, 336, 1-10
22. Nobre, L. S.; Seixas, J. D.; Romao, C. C.; Saraiva, L. M. Antimicrobial action of carbon monoxide-releasing compounds Antimicrob. Agents Chemother. 2007, 51, 4303-4307
23. Naito, Y.; Uchiyama, K.; Takagi, T.; Yoshikawa, T. Therapeutic potential of carbon monoxide (CO) for intestinal inflammation Curr. Med. Chem. 2012, 19, 70-76
24. Onyiah, J. C.; Sheikh, S. Z.; Maharshak, N.; Steinbach, E. C.; Russo, S. M.; Kobayashi, T.; Mackey, L. C.; Hansen, J. J.; Moeser, A. J.; Rawls, J. F.; Borst, L. B.; Otterbein, L. E.; Plevy, S. E. Carbon monoxide and heme oxygenase-1 prevent intestinal inflammation in mice by promoting bacterial clearance Gastroenterology 2013, 144, 789-798
25. Falk, J. E. Porphyrins and Metalloporphyrins; Elsevier: Amsterdam, 1964.
26. Warburg, O.; Negelein, E. Grunes Haemin aus Blast-haemin Chem. Ber. 1930, 63, 1816-1819
27. Lemberg, R. Transformation of hemins into bile pigments Biochem. J. 1935, 29, 1322-1336
28. OCarra, P.; Colleran, E. Coupled oxidation of myoglobin with ascorbate as a model of haem breakdown in vivo Biochem. J. 1969, 115, 13P-14P
29. OCarra, P.; Colleran, E. Methine-bridge specificity of the coupled oxidation of myoglobin and haemoglobin with ascorbate Biochem. J. 1970, 119, 42P-43P
30. Lemberg, R. Chemical mechanism of bile pigment formation Rev. Pure Appl. Chem. 1956, 6, 1-23
31. Sano, S.; Sugiura, Y. Penta-co-ordinate iron (II) oxyporphyrin-2- methylimidazole complex; Model of the heme oxygenase reaction J. Chem. Soc., Chem. Commun. 1982, 750-752
32. Kondo, T.; Nicholson, D. C.; Jackson, A. H.; Kenner, G. W. Isotopic studies of the conversion of oxophlorins and their ferrihaems into bile pigments in the rat Biochem. J. 1971, 121, 601-607
33. Jackson, A. H. Iron in Biochemistry and Medicine; Academic Press: New York, 1974.
34. Docherty, J. C.; Firneisz, G. D.; Schacter, B. A. Methene bridge carbon atom elimination in oxidative heme degradation catalyzed by heme oxygenase and NADPH-cytochrome P-450 reductase Arch. Biochem. Biophys. 1984, 235, 657-664
35. 18O labeling J. Biol. Chem. 1984, 259, 13066-13069
36. 18O labelling and metal substitution Biochem. J. 1978, 174, 103-109
37. Saito, S.; Itano, H. A. Verdohemochrome IX alpha: Preparation and oxidoreductive cleavage to biliverdin IX alpha Proc. Natl. Acad. Sci. U.S.A. 1982, 79, 1393-1397
38. Sano, S.; Sano, T.; Morishima, I.; Shiro, Y.; Maeda, Y. On the mechanism of the chemical and enzymic oxygenations of alpha-oxyprotohemin IX to Fe.biliverdin IX alpha Proc. Natl. Acad. Sci. U.S.A. 1986, 83, 531-535
39. 5 J. Am. Chem. Soc. 2003, 125, 4103-4110
40. Sigman, J. A.; Wang, X.; Lu, Y. Coupled oxidation of heme by myoglobin is mediated by exogenous peroxide J. Am. Chem. Soc. 2001, 123, 6945-6946
41. Wilks, A.; Ortiz de Montellano, P. R. Rat liver heme oxygenase. High level expression of a truncated soluble form and nature of the meso-hydroxylating species J. Biol. Chem. 1993, 268, 22357-22362
42. Suits, M. D.; Pal, G. P.; Nakatsu, K.; Matte, A.; Cygler, M.; Jia, Z. Identification of an Escherichia coli O157:H7 heme oxygenase with tandem functional repeats Proc. Natl. Acad. Sci. U.S.A. 2005, 102, 16955-16960
43. Guo, Y.; Guo, G.; Mao, X.; Zhang, W.; Xiao, J.; Tong, W.; Liu, T.; Xiao, B.; Liu, X.; Feng, Y.; Zou, Q. Functional identification of HugZ, a heme oxygenase from Helicobacter pylori BMC Microbiol. 2008, 8 226
44. Stojiljkovic, I.; Hantke, K. Transport of haemin across the cytoplasmic membrane through a haemin-specific periplasmic binding-protein-dependent transport system in Yersinia enterocolitica Mol. Microbiol. 1994, 13, 719-732
45. Suits, M. D.; Lang, J.; Pal, G. P.; Couture, M.; Jia, Z. Structure and heme binding properties of Escherichia coli O157:H7 ChuX Protein Sci. 2009, 18, 825-838
46. Suits, M. D.; Jaffer, N.; Jia, Z. Structure of the Escherichia coli O157:H7 heme oxygenase ChuS in complex with heme and enzymatic inactivation by mutation of the heme coordinating residue His-193 J. Biol. Chem. 2006, 281, 36776-36782
47. Schneider, S.; Sharp, K. H.; Barker, P. D.; Paoli, M. An induced fit conformational change underlies the binding mechanism of the heme transport proteobacteria-protein HemS J. Biol. Chem. 2006, 281, 32606-32610
48. Barker, K. D.; Barkovits, K.; Wilks, A. Metabolic flux of extracellular heme uptake in Pseudomonas aeruginosa is driven by the iron-regulated heme oxygenase (HemO) J. Biol. Chem. 2012, 287, 18342-18350
49. ONeill, M. J.; Wilks, A. The P. aeruginosa heme binding protein PhuS is a heme oxygenase titratable regulator of heme uptake ACS Chem. Biol. 2013, 8, 1794-1802
50. Lee, M. J.; Schep, D.; McLaughlin, B.; Kaufmann, M.; Jia, Z. Structural Analysis and Identification of PhuS as a Heme-Degrading Enzyme from Pseudomonas aeruginosa J. Mol. Biol. 2014, 426, 1936-1946
51. Oldham, A. L.; Wood, T. A.; Henderson, D. P. Plesiomonas shigelloides hugZ encodes an iron-regulated heme binding protein required for heme iron utilization Can. J. Microbiol. 2008, 54, 97-102
52. Zhang, R.; Zhang, J.; Guo, G.; Mao, X.; Tong, W.; Zhang, Y.; Wang, D. C.; Hu, Y.; Zou, Q. Crystal structure of Campylobacter jejuni ChuZ: A split-barrel family heme oxygenase with a novel heme-binding mode Biochem. Biophys. Res. Commun. 2011, 415, 82-87
53. Friedman, J.; Lad, L.; Li, H.; Wilks, A.; Poulos, T. L. Structural basis for novel regioselective heme oxygenation in the opportunistic pathogen Pseudomonas aeruginosa Biochemistry 2004, 43, 5239-5245
54. Hirotsu, S.; Chu, G. C.; Unno, M.; Lee, D. S.; Yoshida, T.; Park, S. Y.; Shiro, Y.; Ikeda-Saito, M. The crystal structures of the ferric and ferrous forms of the heme complex of HmuO, a heme oxygenase of Corynebacterium diphtheriae J. Biol. Chem. 2004, 279, 11937-11947
55. Schuller, D. J.; Zhu, W.; Stojiljkovic, I.; Wilks, A.; Poulos, T. L. Crystal structure of heme oxygenase from the Gram-negative pathogen Neisseria meningitidis and a comparison with mammalian heme oxygenase-1 Biochemistry 2001, 40, 11552-11558
56. Lee, W. C.; Reniere, M. L.; Skaar, E. P.; Murphy, M. E. Ruffling of metalloporphyrins bound to IsdG and IsdI, two heme-degrading enzymes in Staphylococcus aureus J. Biol. Chem. 2008, 283, 30957-30963
57. Ukpabi, G.; Takayama, S. J.; Mauk, A. G.; Murphy, M. E. Inactivation of the heme degrading enzyme IsdI by an active site substitution that diminishes heme ruffling J. Biol. Chem. 2012, 287, 34179-34188
58. Matsui, T.; Unno, M.; Ikeda-Saito, M. Heme oxygenase reveals its strategy for catalyzing three successive oxygenation reactions Acc. Chem. Res. 2010, 43, 240-247
59. Ortiz de Montellano, P. R. The mechanism of heme oxygenase Curr. Opin. Chem. Biol. 2000, 4, 221-227
60. Ortiz de Montellano, P. R.; Wilks, A. Heme Oxygenase Structure and Mechanism Adv. Inorg. Chem. 2000, 51, 359-402
61. Yoshida, T.; Noguchi, M.; Kikuchi, G. Oxygenated form of heme. Heme oxygenase complex and requirement for second electron to initiate heme degradation from the oxygenated complex J. Biol. Chem. 1980, 255, 4418-4420
62. Takahashi, S.; Ishikawa, K.; Takeuchi, E.; Ikeda-Saito, M.; Yoshida, T.; Rousseau, D. L. Oxygen-bound heme-heme oxygenase complex: Evidence for a highly bent structure of the coordinated oxygen J. Am. Chem. Soc. 1995, 117, 6002-6006
63. Unno, M.; Matsui, T.; Chu, G. C.; Couture, M.; Yoshida, T.; Rousseau, D. L.; Olson, J. S.; Ikeda-Saito, M. Crystal structure of the dioxygen-bound heme oxygenase from Corynebacterium diphtheriae: Implications for heme oxygenase function J. Biol. Chem. 2004, 279, 21055-21061
64. Davydov, R. M.; Yoshida, T.; Ikeda-Saito, M.; Hoffman, B. M. Hydroperoxy-Heme Oxygenase generated by cryoreduction catalyzes the formation of α- meso -hydroxyheme as detected by EPR and ENDOR J. Am. Chem. Soc. 1999, 121, 10656-10657
65. Wilks, A.; Torpey, J.; Ortiz de Montellano, P. R. Heme oxygenase (HO-1). Evidence for electrophilic oxygen addition to the porphyrin ring in the formation of α- meso -hydroxyheme J. Biol. Chem. 1994, 269, 29553-29556
66. Garcia-Serres, R.; Davydov, R. M.; Matsui, T.; Ikeda-Saito, M.; Hoffman, B. M.; Huynh, B. H. Distinct reaction pathways followed upon reduction of oxy-heme oxygenase and oxy-myoglobin as characterized by Mössbauer spectroscopy J. Am. Chem. Soc. 2007, 129, 1402-1412
67. Schuller, D. J.; Wilks, A.; Ortiz de Montellano, P. R.; Poulos, T. L. Crystal structure of human heme oxygenase-1 Nat. Struct. Biol. 1999, 6, 860-867
68. 15N NMR spectroscopic characterization of substrate-bound, cyanide-inhibited human heme oxygenase: Water occupation of the distal cavity J. Am. Chem. Soc. 2003, 125, 13392-13403
69. 1H NMR detection of immobilized water molecules within a strong distal hydrogen-bonding network of substrate-bound human heme oxygenase-1 J. Am. Chem. Soc. 2002, 124, 14296-14297
70. Fujii, H.; Zhang, X.; Tomita, T.; Ikeda-Saito, M.; Yoshida, T. A role for highly conserved carboxylate, aspartate-140, in oxygen activation and heme degradation by heme oxygenase-1 J. Am. Chem. Soc. 2001, 123, 6475-6484
71. Lightning, L. K.; Huang, H.; Moënne-Loccoz, P.; Loehr, T. M.; Schuller, D. J.; Poulos, T. L.; Ortiz de Montellano, P. R. Disruption of an active site hydrogen bond converts human heme oxygenase-1 into a peroxidase J. Biol. Chem. 2001, 276, 10612-10619
72. Davydov, R.; Kofman, V.; Fujii, H.; Yoshida, T.; Ikeda-Saito, M.; Hoffman, B. M. Catalytic mechanism of heme oxygenase through EPR and ENDOR of cryoreduced oxy-heme oxygenase and its Asp 140 mutants J. Am. Chem. Soc. 2002, 124, 1798-1808
73. Lad, L.; Wang, J.; Li, H.; Friedman, J.; Bhaskar, B.; Ortiz de Montellano, P. R.; Poulos, T. L. Crystal structures of the ferric, ferrous, and ferrous-NO forms of the Asp140Ala mutant of human heme oxygenase-1: Catalytic implications J. Mol. Biol. 2003, 330, 527-538
74. Matsui, T.; Furukawa, M.; Unno, M.; Tomita, T.; Ikeda-Saito, M. Roles of distal Asp in heme oxygenase from Corynebacterium diphteriae, HmuO: A water-driven oxygen activation mechanism J. Biol. Chem. 2004, 280, 2981-2989
75. 13C NMR spectroscopic studies suggest the active participation of the heme in macrocycle hydroxylation J. Am. Chem. Soc. 2003, 125, 11842-11852
76. xy electronic state at ambient temperatures J. Am. Chem. Soc. 2002, 124, 6077-6089
77. Walker, F. Magnetic spectroscopic (EPR, ESEEM, Mössbauer, MCD, NMR) studies of low-spin ferriheme centers and their corresponding heme proteins Coord. Chem. Rev. 1999, 185-186, 471-534
78. Chen, H.; Moreau, Y.; Derat, E.; Shaik, S. Quantum mechanical/molecular mechanical study of mechanisms of heme degradation by the enzyme heme oxygenase: The strategic function of the water cluster J. Am. Chem. Soc. 2008, 130, 1953-1965
79. Takayama, S. J.; Ukpabi, G.; Murphy, M. E.; Mauk, A. G. Electronic properties of the highly ruffled heme bound to the heme degrading enzyme IsdI Proc. Natl. Acad. Sci. U.S.A. 2011, 108, 13071-13076
80. Liu, Y.; Moënne-Loccoz, P.; Loehr, T. M.; Ortiz de Montellano, P. R. Heme oxygenase-1, intermediates in verdoheme formation and the requirement for reduction equivalents J. Biol. Chem. 1997, 272, 6909-6917
81. Liu, Y.; Ortiz de Montellano, P. R. Reaction intermediates and single turnover rate constants for the oxidation of heme by human heme oxygenase-1 J. Biol. Chem. 2000, 275, 5297-5307
82. Matera, K. M.; Takahashi, S.; Fujii, H.; Zhou, H.; Ishikawa, K.; Yoshimura, T.; Rousseau, D. L.; Yoshida, T.; Ikeda-Saito, M. Oxygen and one reducing equivalent are both required for the conversion of α-hydroxyhemin to verdoheme in heme oxygenase J. Biol. Chem. 1996, 271, 6618-6624