A role for reactive oxygen species in the antibacterial properties of carbon monoxide-releasing molecules

FEMS Microbiology Letters

Volumn 336, Issue 1, 2012, Pages 1-10

  Tavares, Ana Filipa N ^a   Nobre, Lígia S ^a   Saraiva, Lígia M ^a  

^a INSTITUTO DE TECNOLOGIA QUÍMICA E BIOLÓGICA   (Portugal)

Author keywords

Bactericidal; Carbon monoxide releasing molecules; Escherichia coli; Reactive oxygen species; Staphylococcus aureus

Indexed keywords

BACTERICIDE; CARBON MONOXIDE; CARBON MONOXIDE RELEASING MOLECULE; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG;

AEROBIC BACTERIUM; ANAEROBIC BACTERIUM; ARTICLE; BACTERIAL GENE; BACTERICIDAL ACTIVITY; BINDING AFFINITY; CARDIOVASCULAR DISEASE; CELL DEATH; COMPLEX FORMATION; CONCENTRATION RESPONSE; DOWN REGULATION; DRUG EFFECT; DRUG STRUCTURE; GENE EXPRESSION REGULATION; GENETIC ASSOCIATION; GROWTH INHIBITION; INFLAMMATION; INTRACELLULAR SIGNALING; LUNG INJURY; MALIGNANT NEOPLASTIC DISEASE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN TARGETING; SEPSIS; TRANSCRIPTION REGULATION; UPREGULATION;

ANTI-BACTERIAL AGENTS; BACTERIA; CARBON MONOXIDE; GENE EXPRESSION REGULATION, BACTERIAL; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES;

ANIMALIA; ESCHERICHIA COLI; NEGIBACTERIA; POSIBACTERIA; PSEUDOMONAS AERUGINOSA; STAPHYLOCOCCUS AUREUS;

EID: 84867333665     PISSN: 03781097     EISSN: 15746968     Source Type: Journal    
DOI: 10.1111/j.1574-6968.2012.02633.x     Document Type: Article

References (80)

1. 2. Metallomics 3: 797-815.
2. Bonam D, Lehman L, Roberts GP & Ludden PW (1989) Regulation of carbon monoxide dehydrogenase and hydrogenase in Rhodospirillum rubrum: effects of CO and oxygen on synthesis and activity. J Bacteriol 171: 3102-3107.
3. Bruggemann H, Bauer R, Raffestin S & Gottschalk G (2004) Characterization of a heme oxygenase of Clostridium tetani and its possible role in oxygen tolerance. Arch Microbiol 182: 259-263.
4. Chang AL, Tuckerman JR, Gonzalez G, Mayer R, Weinhouse H, Volman G, Amikam D, Benziman M & Gilles-Gonzalez MA (2001) Phosphodiesterase A1, a regulator of cellulose synthesis in Acetobacter xylinum, is a heme-based sensor. Biochemistry 40: 3420-3426.
5. Chiang SM & Schellhorn HE (2012) Regulators of oxidative stress response genes in Escherichia coli and their functional conservation in bacteria. Arch Biochem Biophys, in press, doi:10.1016/j.abb.2012.02.007.
6. Davidge KS, Sanguinetti G, Yee CH et al. (2009) Carbon monoxide-releasing antibacterial molecules target respiration and global transcriptional regulators. J Biol Chem 284: 4516-4524.
7. Delgado-Nixon VM, Gonzalez G & Gilles-Gonzalez MA (2000) Dos, a heme-binding PAS protein from Escherichia coli, is a direct oxygen sensor. Biochemistry 39: 2685-2691.
8. Desmard M, Davidge KS, Bouvet O et al. (2009) A carbon monoxide-releasing molecule (CORM-3) exerts bactericidal activity against Pseudomonas aeruginosa and improves survival in an animal model of bacteraemia. FASEB J 23: 1023-1031.
9. Desmard M, Foresti R, Morin D et al. (2011) Differential antibacterial activity against Pseudomonas aeruginosa by carbon monoxide-releasing molecules. Antioxid Redox Signal 16: 153-163.
10. Foresti R, Bani-Hani MG & Motterlini R (2008) Use of carbon monoxide as a therapeutic agent: promises and challenges. Intensive Care Med 34: 649-658.
11. Frankenberg-Dinkel N (2004) Bacterial heme oxygenases. Antioxid Redox Signal 6: 825-834.
12. Gaballa A & Helmann JD (2012) Bacillus subtilis Fur represses one of two paralogous haem-degrading monooxygenases. Microbiology 157: 3221-3231.
13. Gilles-Gonzalez MA, Gonzalez G, Perutz MF, Kiger L, Marden MC & 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.
14. Greenwood NN & Earnshaw A (1997) Chemistry of the Elements. Butterworth Heinemann, Oxford.
15. Gullotta F, di Masi A & Ascenzi P (2012a) Carbon monoxide: an unusual drug. IUBMB Life 64: 378-386.
16. Gullotta F, di Masi A, Coletta M & Ascenzi P (2012b) CO metabolism, sensing, and signaling. BioFactors 38: 1-13.
17. Guo Y, Guo G, Mao X et al. (2008) Functional identification of HugZ, a heme oxygenase from Helicobacter pylori. BMC Microbiol 8: 226.
18. Hassan S, Ohtani K, Wang R, Yuan Y, Wang Y, Yamaguchi Y & Shimizu T (2010) Transcriptional regulation of hemO encoding heme oxygenase in Clostridium perfringens. J Microbiol 48: 96-101.
19. Hondorp ER & Matthews RG (2004) Oxidative stress inactivates cobalamin-independent methionine synthase (MetE) in Escherichia coli. PLoS Biol 2: e336.
20. Hou S, Larsen RW, Boudko D et al. (2000) Myoglobin-like aerotaxis transducers in Archaea and Bacteria. Nature 403: 540-544.
21. Jaouen G & Metzler-Nolte N (2010) Medicinal Organometallic Chemistry. Springer, Berlin.
22. Johnson TR, Mann BE, Clark JE, Foresti R, Green CJ & Motterlini R (2003) Metal carbonyls: a new class of pharmaceuticals? Angew Chem Int Ed Engl 42: 3722-3729.
23. Kerby RL, Youn H & Roberts GP (2008) RcoM: a new single-component transcriptional regulator of CO metabolism in bacteria. J Bacteriol 190: 3336-3343.
24. Kim HP, Ryter SW & Choi AM (2006) CO as a cellular signaling molecule. Annu Rev Pharmacol Toxicol 46: 411-449.
25. Kumar A, Toledo JC, Patel RP, Lancaster JR Jr& Steyn AJ (2007) Mycobacterium tuberculosis DosS is a redox sensor and DosT is a hypoxia sensor. P Natl Acad Sci USA 104: 11568-11573.
26. Kumar A, Deshane JS, Crossman DK et al. (2008) Heme oxygenase-1-derived carbon monoxide induces the Mycobacterium tuberculosis dormancy regulon. J Biol Chem 283: 18032-18039.
27. Li C & Stocker R (2009) Heme oxygenase and iron: from bacteria to humans. Redox Rep 14: 95-101.
28. Migita CT, Zhang X & Yoshida T (2003) Expression and characterization of cyanobacterium heme oxygenase, a key enzyme in the phycobilin synthesis. Properties of the heme complex of recombinant active enzyme. Eur J Biochem 270: 687-698.
29. Motterlini R & Otterbein LE (2010) The therapeutic potential of carbon monoxide. Nat Rev Drug Discov 9: 728-743.
30. Motterlini R, Mann BE & Foresti R (2005) Therapeutic applications of carbon monoxide-releasing molecules. Expert Opin Investig Drugs 14: 1305-1318.
31. Murray TS, Okegbe C, Gao Y, Kazmierczak BI, Motterlini R, Dietrich LE & Bruscia EM (2012) The carbon monoxide releasing molecule CORM-2 attenuates Pseudomonas aeruginosa biofilm formation. PLoS One 7: e35499.
32. Nobre LS, Seixas JD, Romao CC & Saraiva LM (2007) Antimicrobial action of carbon monoxide-releasing compounds. Antimicrob Agents Chemother 51: 4303-4307.
33. Nobre LS, Al-Shahrour F, Dopazo J & Saraiva LM (2009) Exploring the antimicrobial action of a carbon monoxide-releasing compound through whole-genome transcription profiling of Escherichia coli. Microbiology 155: 813-824.
34. Oelgeschlager E & Rother M (2008) Carbon monoxide-dependent energy metabolism in anaerobic bacteria and archaea. Arch Microbiol 190: 257-269.
35. Ogata H, Mizoguchi Y, Mizuno N et al. (2002) Structural studies of the carbon monoxide complex of [NiFe]hydrogenase from Desulfovibrio vulgaris Miyazaki F: suggestion for the initial activation site for dihydrogen. J Am Chem Soc 124: 11628-11635.
36. Ojeda JF, Martinson D, Menscher E & Roop RM 2nd (2012) The bhuQ gene encodes a heme oxygenase that contributes to the ability of Brucella abortus 2308 to use heme as an iron source and is regulated by Irr. J Bacteriol, in press. doi: 10.1128/JB.00367-12.
37. Otterbein LE, May A & Chin BY (2005) Carbon monoxide increases macrophage bacterial clearance through Toll-like receptor (TLR)4 expression. Cell Mol Biol (Noisy-le-grand) 51: 433-440.
38. Pena AC, Penacho N, Mancio-Silva L et al. (2012) A novel carbon monoxide-releasing molecule fully protects mice from severe malaria. Antimicrob Agents Chemother 56: 1281-1290.
39. Perez JM, Arenas FA, Pradenas GA, Sandoval JM & Vasquez CC (2008) Escherichia coli YqhD exhibits aldehyde reductase activity and protects from the harmful effect of lipid peroxidation-derived aldehydes. J Biol Chem 283: 7346-7353.
40. Puranik M, Weeks CL, Lahaye D et al. (2006) Dynamics of carbon monoxide binding to cystathionine beta-synthase. J Biol Chem 281: 13433-13438.
41. Puri S & O'Brian MR (2006) The hmuQ and hmuD genes from Bradyrhizobium japonicum encode heme-degrading enzymes. J Bacteriol 188: 6476-6482.
42. Ragsdale SW (2004) Life with carbon monoxide. Crit Rev Biochem Mol Biol 39: 165-195.
43. Ratliff M, Zhu W, Deshmukh R, Wilks A & Stojiljkovic I (2001) Homologues of neisserial heme oxygenase in Gram-negative bacteria: degradation of heme by the product of the pigA gene of Pseudomonas aeruginosa. J Bacteriol 183: 6394-6403.
44. Ren D, Bedzyk LA, Thomas SM, Ye RW & Wood TK (2004) Gene expression in Escherichia coli biofilms. Appl Microbiol Biotechnol 64: 515-524.
45. Reniere ML, Torres VJ & Skaar EP (2007) Intracellular metalloporphyrin metabolism in Staphylococcus aureus. Biometals 20: 333-345.
46. Ridley KA, Rock JD, Li Y & Ketley JM (2006) Heme utilization in Campylobacter jejuni. J Bacteriol 188: 7862-7875.
47. Roberts GP, Thorsteinsson MV, Kerby RL, Lanzilotta WN & Poulos T (2001) CooA: a heme-containing regulatory protein that serves as a specific sensor of both carbon monoxide and redox state. Prog Nucleic Acid Res Mol Biol 67: 35-63.
48. 2 sensing from structure-function relationships in the FixL proteins. J Inorg Biochem 99: 963-977.
49. Romao CC, Blattler WA, Seixas JD & Bernardes GJ (2012) Developing drug molecules for therapy with carbon monoxide. Chem Soc Rev 41: 3571-3583.
50. Ryter SW, Alam J & Choi AM (2006) Heme oxygenase-1/carbon monoxide: from basic science to therapeutic applications. Physiol Rev 86: 583-650.
51. Santos-Silva T, Mukhopadhyay A, Seixas JD, Bernardes GJ, Romao CC & Romao MJ (2011) Towards improved therapeutic CORMs: understanding the reactivity of CORM-3 with proteins. Curr Med Chem 18: 3361-3366.
52. Schmitt MP (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.
53. Seixas JD (2010) Development of CO-Releasing Molecules for the Treatment of Inflammatory Diseases. Thesis, Instituto de Tecnologia Química e Biológica - Universidade Nova de Lisboa.
54. Sjostrand T (1951) Formation of carbon monoxide in connexion with haemoglobin catabolism. Nature 168: 1118-1119.
55. Skaar EP, Gaspar AH & Schneewind O (2004) IsdG and IsdI, heme-degrading enzymes in the cytoplasm of Staphylococcus aureus. J Biol Chem 279: 436-443.
56. Skaar EP, Gaspar AH & Schneewind O (2006) Bacillus anthracis IsdG, a heme-degrading monooxygenase. J Bacteriol 188: 1071-1080.
57. Smith H, Mann BE, Motterlini R & Poole RK (2011) The carbon monoxide-releasing molecule, CORM-3 (RU(CO)(3) CL(glycinate)), targets respiration and oxidases in Campylobacter jejuni, generating hydrogen peroxide. IUBMB Life 63: 363-371.
58. Storz G & Imlay JA (1999) Oxidative stress. Curr Opin Microbiol 2: 188-194.
59. Suits MD, Pal GP, Nakatsu K, Matte A, Cygler M & Jia Z (2005) Identification of an Escherichia coli O157:H7 heme oxygenase with tandem functional repeats. P Natl Acad Sci USA 102: 16955-16960.
60. Taille C, El-Benna J, Lanone S, Boczkowski J & Motterlini R (2005) Mitochondrial respiratory chain and NAD(P)H oxidase are targets for the antiproliferative effect of carbon monoxide in human airway smooth muscle. J Biol Chem 280: 25350-25360.
61. Tavares AF, Teixeira M, Romao CC, Seixas JD, Nobre LS & Saraiva LM (2011) Reactive oxygen species mediate bactericidal killing elicited by carbon monoxide-releasing molecules. J Biol Chem 286: 26708-26717.
62. Tenhunen R, Marver HS & Schmid R (1970) The enzymatic catabolism of hemoglobin: stimulation of microsomal heme oxygenase by hemin. J Lab Clin Med 75: 410-421.
63. Tsai AL, Berka V, Martin E & Olson JS (2012) A 'sliding scale rule' for selectivity among NO, CO, and O(2) by heme protein sensors. Biochemistry 51: 172-186.
64. Wagener FA, Volk HD, Willis D, Abraham NG, Soares MP, Adema GJ & Figdor CG (2003) Different faces of the heme-heme oxygenase system in inflammation. Pharmacol Rev 55: 551-571.
65. Wang S, Deng K, Zaremba S et al. (2009) Transcriptomic response of Escherichia coli O157:H7 to oxidative stress. Appl Environ Microbiol 75: 6110-6123.
66. Weber MM, French CL, Barnes MB, Siegele DA & McLean RJ (2010) A previously uncharacterized gene, yjfO (bsmA), influences Escherichia coli biofilm formation and stress response. Microbiology 156: 139-147.
67. Wegele R, Tasler R, Zeng Y, Rivera M & Frankenberg-Dinkel N (2004) The heme oxygenase(s)-phytochrome system of Pseudomonas aeruginosa. J Biol Chem 279: 45791-45802.
68. Wikström M, Krab K & Saraste M (1981) Cytochrome Oxidase - A Synthesis. Academic Press, London.
69. Wu L & Wang R (2005) Carbon monoxide: endogenous production, physiological functions, and pharmacological applications. Pharmacol Rev 57: 585-630.
70. Wyckoff EE, Schmitt M, Wilks A & Payne SM (2004) HutZ is required for efficient heme utilization in Vibrio cholerae. J Bacteriol 186: 4142-4151.
71. Wyckoff EE, Lopreato GF, Tipton KA & Payne SM (2005) Shigella dysenteriae ShuS promotes utilization of heme as an iron source and protects against heme toxicity. J Bacteriol 187: 5658-5664.
72. Yamamoto T, Takano N, Ishiwata K & Suematsu M (2011) Carbon monoxide stimulates global protein methylation via its inhibitory action on cystathionine beta-synthase. J Clin Biochem Nutr 48: 96-100.
73. Youn H, Kerby RL, Conrad M & Roberts GP (2004) Functionally critical elements of CooA-related CO sensors. J Bacteriol 186: 1320-1329.
74. Zegdi R, Perrin D, Burdin M, Boiteau R & Tenaillon A (2002) Increased endogenous carbon monoxide production in severe sepsis. Intensive Care Med 28: 793-796.
75. Zhang X, Migita CT, Sato M, Sasahara M & Yoshida T (2005) Protein expressed by the ho2 gene of the cyanobacterium Synechocystis sp. PCC 6803 is a true heme oxygenase. Properties of the heme and enzyme complex. FEBS J 272: 1012-1022.
76. Zhang XS, Garcia-Contreras R & Wood TK (2007) YcfR (BhsA) influences Escherichia coli biofilm formation through stress response and surface hydrophobicity. J Bacteriol 189: 3051-3062.
77. Zheng M, Wang X, Templeton LJ, Smulski DR, LaRossa RA & Storz G (2001) DNA microarray-mediated transcriptional profiling of the Escherichia coli response to hydrogen peroxide. J Bacteriol 183: 4562-4570.
78. Zhu W, Wilks A & Stojiljkovic I (2000a) Degradation of heme in Gram-negative bacteria: the product of the hemO gene of Neisseriae is a heme oxygenase. J Bacteriol 182: 6783-6790.
79. Zhu W, Hunt DJ, Richardson AR & Stojiljkovic I (2000b) Use of heme compounds as iron sources by pathogenic Neisseriae requires the product of the hemO gene. J Bacteriol 182: 439-447.
80. Zuckerbraun BS, Chin BY, Bilban M, d'Avila JC, Rao J, Billiar TR & Otterbein LE (2007) Carbon monoxide signals via inhibition of cytochrome c oxidase and generation of mitochondrial reactive oxygen species. FASEB J 21: 1099-1106.