Mycobacterium tuberculosis Senses Host-Derived Carbon Monoxide during Macrophage Infection

Cell Host and Microbe

Volumn 3, Issue 5, 2008, Pages 323-330

  Shiloh, Michael U ^a,b   Manzanillo, Paolo ^a,b   Cox, Jeffery S ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

CELLBIO; MICROBIO; SIGNALING

Indexed keywords

BACTERIAL PROTEIN; CARBON MONOXIDE; DOSR PROTEIN; DOSS PROTEIN; DOST PROTEIN; HEME OXYGENASE 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL SURVIVAL; CONTROLLED STUDY; GENE DELETION; GENE EXPRESSION; GENE INDUCTION; HOST PATHOGEN INTERACTION; LUNG ALVEOLUS MACROPHAGE; MACROPHAGE; MACROPHAGE ACTIVATION; MOUSE; MYCOBACTERIOSIS; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUORUM SENSING; REGULON; SENSORY SYSTEM;

ANIMALS; CARBON MONOXIDE; CELLS, CULTURED; GENE EXPRESSION REGULATION, BACTERIAL; HEME OXYGENASE-1; MACROPHAGES; MICE; MICE, INBRED BALB C; MYCOBACTERIUM TUBERCULOSIS; REGULON; TUBERCULOSIS;

MYCOBACTERIUM TUBERCULOSIS;

EID: 43049170080     PISSN: 19313128     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.chom.2008.03.007     Document Type: Article

References (65)

1. Alcaraz M.J., Habib A., Creminon C., Vicente A.M., Lebret M., Levy-Toledano S., and Maclouf J. Heme oxygenase-1 induction by nitric oxide in RAW 264.7 macrophages is upregulated by a cyclo-oxygenase-2 inhibitor. Biochim. Biophys. Acta 1526 (2001) 13-16
2. Aono S., Honma Y., Ohkubo K., Tawara T., Kamiya T., and Nakajima H. CO sensing and regulation of gene expression by the transcriptional activator CooA. J. Inorg. Biochem. 82 (2000) 51-56
3. Archakov A.I., Karuzina I.I., Petushkova N.A., Lisitsa A.V., and Zgoda V.G. Production of carbon monoxide by cytochrome P450 during iron-dependent lipid peroxidation. Toxicol. In Vitro 16 (2002) 1-10
4. Ascenzi P., Bocedi A., Leoni L., Visca P., Zennaro E., Milani M., and Bolognesi M. CO sniffing through heme-based sensor proteins. IUBMB Life 56 (2004) 309-315
5. Boon C., and Dick T. Mycobacterium bovis BCG response regulator essential for hypoxic dormancy. J. Bacteriol. 184 (2002) 6760-6767
6. Chauveau C., Remy S., Royer P.J., Hill M., Tanguy-Royer S., Hubert F.X., Tesson L., Brion R., Beriou G., Gregoire M., et al. Heme oxygenase-1 expression inhibits dendritic cell maturation and proinflammatory function but conserves IL-10 expression. Blood 106 (2005) 1694-1702
7. Desjardin L.E., Hayes L.G., Sohaskey C.D., Wayne L.G., and Eisenach K.D. Microaerophilic induction of the alpha-crystallin chaperone protein homologue (hspX) mRNA of Mycobacterium tuberculosis. J. Bacteriol. 183 (2001) 5311-5316
8. Dioum E.M., Rutter J., Tuckerman J.R., Gonzalez G., Gilles-Gonzalez M.A., and McKnight S.L. NPAS2: A gas-responsive transcription factor. Science 298 (2002) 2385-2387
9. Fenhalls G., Stevens L., Moses L., Bezuidenhout J., Betts J.C., Helden Pv P., Lukey P.T., and Duncan K. In situ detection of Mycobacterium tuberculosis transcripts in human lung granulomas reveals differential gene expression in necrotic lesions. Infect. Immun. 70 (2002) 6330-6338
10. Fenhalls G., Stevens-Muller L., Warren R., Carroll N., Bezuidenhout J., Van Helden P., and Bardin P. Localisation of mycobacterial DNA and mRNA in human tuberculous granulomas. J. Microbiol. Methods 51 (2002) 197-208
11. Florczyk M.A., McCue L.A., Stack R.F., Hauer C.R., and McDonough K.A. Identification and characterization of mycobacterial proteins differentially expressed under standing and shaking culture conditions, including Rv2623 from a novel class of putative ATP-binding proteins. Infect. Immun. 69 (2001) 5777-5785
12. Gilles-Gonzalez M.A., and Gonzalez G. Heme-based sensors: Defining characteristics, recent developments, and regulatory hypotheses. J. Inorg. Biochem. 99 (2005) 1-22
13. Gomez J.E., and McKinney J.D. M. tuberculosis persistence, latency, and drug tolerance. Tuberculosis (Edinb.) 84 (2004) 29-44
14. Hu Y., Movahedzadeh F., Stoker N.G., and Coates A.R. Deletion of the Mycobacterium tuberculosis alpha-crystallin-like hspX gene causes increased bacterial growth in vivo. Infect. Immun. 74 (2006) 861-868
15. Ingi T., Chiang G., and Ronnett G.V. The regulation of heme turnover and carbon monoxide biosynthesis in cultured primary rat olfactory receptor neurons. J. Neurosci. 16 (1996) 5621-5628
16. Ioanoviciu A., Yukl E.T., Moenne-Loccoz P., and de Montellano P.R. DevS, a heme-containing two-component oxygen sensor of Mycobacterium tuberculosis. Biochemistry 46 (2007) 4250-4260
17. Kampfer H., Kolb N., Manderscheid M., Wetzler C., Pfeilschifter J., and Frank S. Macrophage-derived heme-oxygenase-1: Expression, regulation, and possible functions in skin repair. Mol. Med. 7 (2001) 488-498
18. Kendall S.L., Movahedzadeh F., Rison S.C., Wernisch L., Parish T., Duncan K., Betts J.C., and Stoker N.G. The Mycobacterium tuberculosis dosRS two-component system is induced by multiple stresses. Tuberculosis (Edinb.) 84 (2004) 247-255
19. Kendall S.L., Rison S.C., Movahedzadeh F., Frita R., and Stoker N.G. What do microarrays really tell us about M. tuberculosis?. Trends Microbiol. 12 (2004) 537-544
20. Kim H.P., Wang X., Galbiati F., Ryter S.W., and Choi A.M. Caveolae compartmentalization of heme oxygenase-1 in endothelial cells. FASEB J. 18 (2004) 1080-1089
21. Kumar A., Toledo J.C., Patel R.P., Lancaster Jr. J.R., and Steyn A.J. Mycobacterium tuberculosis DosS is a redox sensor and DosT is a hypoxia sensor. Proc. Natl. Acad. Sci. USA 104 (2007) 11568-11573
22. Laubach V.E., Shesely E.G., Smithies O., and Sherman P.A. Mice lacking inducible nitric oxide synthase are not resistant to lipopolysaccharide-induced death. Proc. Natl. Acad. Sci. USA 92 (1995) 10688-10692
23. Lighthart B. Survival of airborne bacteria in a high urban concentration of carbon monoxide. Appl. Microbiol. 25 (1973) 86-91
24. Maines M.D. The heme oxygenase system: Past, present, and future. Antioxid. Redox Signal. 6 (2004) 797-801
25. Malhotra V., Sharma D., Ramanathan V.D., Shakila H., Saini D.K., Chakravorty S., Das T.K., Li Q., Silver R.F., Narayanan P.R., and Tyagi J.S. Disruption of response regulator gene, devR, leads to attenuation in virulence of Mycobacterium tuberculosis. FEMS Microbiol. Lett. 231 (2004) 237-245
26. Nathan C. Role of iNOS in human host defense. Science 312 (2006) 1874-1875
27. Nobre L.S., Seixas J.D., Romao C.C., and Saraiva L.M. The antimicrobial action of carbon monoxide releasing compounds. Antimicrob. Agents Chemother. 51 (2007) 4303-4307
28. Oh G.S., Pae H.O., Lee B.S., Kim B.N., Kim J.M., Kim H.R., Jeon S.B., Jeon W.K., Chae H.J., and Chung H.T. Hydrogen sulfide inhibits nitric oxide production and nuclear factor-kappaB via heme oxygenase-1 expression in RAW264.7 macrophages stimulated with lipopolysaccharide. Free Radic. Biol. Med. 41 (2006) 106-119
29. Ohno H., Zhu G., Mohan V.P., Chu D., Kohno S., Jacobs Jr. W.R., and Chan J. The effects of reactive nitrogen intermediates on gene expression in Mycobacterium tuberculosis. Cell. Microbiol. 5 (2003) 637-648
30. Pae H.O., Oh G.S., Choi B.M., Chae S.C., and Chung H.T. Differential expressions of heme oxygenase-1 gene in CD25- and CD25+ subsets of human CD4+ T cells. Biochem. Biophys. Res. Commun. 306 (2003) 701-705
31. Parish T., Smith D.A., Kendall S., Casali N., Bancroft G.J., and Stoker N.G. Deletion of two-component regulatory systems increases the virulence of Mycobacterium tuberculosis. Infect. Immun. 71 (2003) 1134-1140
32. Purkayastha A., McCue L.A., and McDonough K.A. Identification of a Mycobacterium tuberculosis putative classical nitroreductase gene whose expression is coregulated with that of the acr aene within macrophages, in standing versus shaking cultures, and under low oxygen conditions. Infect. Immun. 70 (2002) 1518-1529
33. Ricagno S., de Rosa M., Aliverti A., Zanetti G., and Bolognesi M. The crystal structure of FdxA, a 7Fe ferredoxin from Mycobacterium smegmatis. Biochem. Biophys. Res. Commun. 360 (2007) 97-102
34. Roberts D.M., Liao R.P., Wisedchaisri G., Hol W.G., and Sherman D.R. Two sensor kinases contribute to the hypoxic response of Mycobacterium tuberculosis. J. Biol. Chem. 279 (2004) 23082-23087
35. Roberts G.P., Thorsteinsson M.V., Kerby R.L., Lanzilotta W.N., and Poulos T. 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 (2001) 35-63
36. Roberts G.P., Youn H., and Kerby R.L. CO-Sensing mechanisms. Microbiol. Mol. Biol. Rev. 68 (2004) 453-473
37. Rohde K.H., Abramovitch R.B., and Russell D.G. Mycobacterium tuberculosis invasion of macrophages: Linking bacterial gene expression to environmental cues. Cell Host Microbe 2 (2007) 352-364
38. Rustad T.R., Harrell M.I., Liao R., and Sherman D.R. The enduring hypoxic response of Mycobacterium tuberculosis. PLoS ONE 3 (2008) e1502 10.1371/journal.pone.0001502
39. Ryter S.W., Morse D., and Choi A.M. Carbon monoxide: To boldly go where NO has gone before. Sci. STKE 2004 (2004) RE6
40. Saini D.K., Malhotra V., Dey D., Pant N., Das T.K., and Tyagi J.S. DevR-DevS is a bona fide two-component system of Mycobacterium tuberculosis that is hypoxia-responsive in the absence of the DNA-binding domain of DevR. Microbiology 150 (2004) 865-875
41. Sardiwal S., Kendall S.L., Movahedzadeh F., Rison S.C., Stoker N.G., and Djordjevic S. A GAF domain in the hypoxia/NO-inducible Mycobacterium tuberculosis DosS protein binds haem. J. Mol. Biol. 353 (2005) 929-936
42. Schnappinger D., Ehrt S., Voskuil M.I., Liu Y., Mangan J.A., Monahan I.M., Dolganov G., Efron B., Butcher P.D., Nathan C., and Schoolnik G.K. Transcriptional Adaptation of Mycobacterium tuberculosis within Macrophages: Insights into the Phagosomal Environment. J. Exp. Med. 198 (2003) 693-704
43. Sharma D., Bose A., Shakila H., Das T.K., Tyagi J.S., and Ramanathan V.D. Expression of mycobacterial cell division protein, FtsZ, and dormancy proteins, DevR and Acr, within lung granulomas throughout guinea pig infection. FEMS Immunol. Med. Microbiol. 48 (2006) 329-336
44. Sherman D.R., Voskuil M., Schnappinger D., Liao R., Harrell M.I., and Schoolnik G.K. Regulation of the Mycobacterium tuberculosis hypoxic response gene encoding alpha -crystallin. Proc. Natl. Acad. Sci. USA 98 (2001) 7534-7539
45. Sjostrand T. Endogenous formation of carbon monoxide; the CO concentration in the inspired and expired air of hospital patients. Acta Physiol. Scand. 22 (1951) 137-141
46. Slebos D.J., Ryter S.W., and Choi A.M. Heme oxygenase-1 and carbon monoxide in pulmonary medicine. Respir. Res. 4 (2003) 7
47. Sohaskey C.D., and Wayne L.G. Role of narK2X and narGHJI in hypoxic upregulation of nitrate reduction by Mycobacterium tuberculosis. J. Bacteriol. 185 (2003) 7247-7256
48. Sousa E.H., Tuckerman J.R., Gonzalez G., and Gilles-Gonzalez M.A. DosT and DevS are oxygen-switched kinases in Mycobacterium tuberculosis. Protein Sci. 16 (2007) 1708-1719
49. Stanley S.A., Johndrow J.E., Manzanillo P., and Cox J.S. The Type I IFN response to infection with Mycobacterium tuberculosis requires ESX-1-mediated secretion and contributes to pathogenesis. J. Immunol. 178 (2007) 3143-3152
50. Tailleux L., Waddell S.J., Pelizzola M., Mortellaro A., Withers M., Tanne A., Castagnoli P.R., Gicquel B., Stoker N.G., Butcher P.D., et al. Probing host pathogen cross-talk by transcriptional profiling of both mycobacterium tuberculosis and infected human dendritic cells and macrophages. PLoS ONE 3 (2008) e1403 10.1371/journal.pone.0001403
51. Talaat A.M., Lyons R., Howard S.T., and Johnston S.A. The temporal expression profile of Mycobacterium tuberculosis infection in mice. Proc. Natl. Acad. Sci. USA 101 (2004) 4602-4607
52. Timm J., Post F.A., Bekker L.G., Walther G.B., Wainwright H.C., Manganelli R., Chan W.T., Tsenova L., Gold B., Smith I., et al. Differential expression of iron-, carbon-, and oxygen-responsive mycobacterial genes in the lungs of chronically infected mice and tuberculosis patients. Proc. Natl. Acad. Sci. USA 100 (2003) 14321-14326
53. Tsai M.C., Chakravarty S., Zhu G., Xu J., Tanaka K., Koch C., Tufariello J., Flynn J., and Chan J. Characterization of the tuberculous granuloma in murine and human lungs: Cellular composition and relative tissue oxygen tension. Cell. Microbiol. 8 (2006) 218-232
54. Vicente A.M., Guillen M.I., and Alcaraz M.J. Modulation of haem oxygenase-1 expression by nitric oxide and leukotrienes in zymosan-activated macrophages. Br. J. Pharmacol. 133 (2001) 920-926
55. Voskuil M.I., Schnappinger D., Visconti K.C., Harrell M.I., Dolganov G.M., Sherman D.R., and Schoolnik G.K. Inhibition of respiration by nitric oxide induces a Mycobacterium tuberculosis dormancy program. J. Exp. Med. 198 (2003) 705-713
56. Voskuil M.I., Visconti K.C., and Schoolnik G.K. Mycobacterium tuberculosis gene expression during adaptation to stationary phase and low-oxygen dormancy. Tuberculosis (Edinb.) 84 (2004) 218-227
57. Wald N.J., Idle M., Boreham J., and Bailey A. Carbon monoxide in breath in relation to smoking and carboxyhaemoglobin levels. Thorax 36 (1981) 366-369
58. Wang C.H., Liu C.Y., Lin H.C., Yu C.T., Chung K.F., and Kuo H.P. Increased exhaled nitric oxide in active pulmonary tuberculosis due to inducible NO synthase upregulation in alveolar macrophages. Eur. Respir. J. 11 (1998) 809-815
59. Wayne L.G., and Sohaskey C.D. Nonreplicating persistence of mycobacterium tuberculosis. Annu. Rev. Microbiol. 55 (2001) 139-163
60. Weigel P.H., and Englund P.T. Inhibition of DNA replication in Escherichia coli by cyanide and carbon monoxide. J. Biol. Chem. 250 (1975) 8536-8542
61. Wu L., and Wang R. Carbon monoxide: Endogenous production, physiological functions, and pharmacological applications. Pharmacol. Rev. 57 (2005) 585-630
62. Yet S.F., Perrella M.A., Layne M.D., Hsieh C.M., Maemura K., Kobzik L., Wiesel P., Christou H., Kourembanas S., and Lee M.E. Hypoxia induces severe right ventricular dilatation and infarction in heme oxygenase-1 null mice. J. Clin. Invest. 103 (1999) R23-R29
63. Youn H., Kerby R.L., Conrad M., and Roberts G.P. Functionally critical elements of CooA-related CO sensors. J. Bacteriol. 186 (2004) 1320-1329
64. Yukl E.T., Ioanoviciu A., de Montellano P.R., and Moenne-Loccoz P. Interdomain interactions within the two-component heme-based sensor DevS from Mycobacterium tuberculosis. Biochemistry 46 (2007) 9728-9736
65. Zhou H., Lu F., Latham C., Zander D.S., and Visner G.A. Heme oxygenase-1 expression in human lungs with cystic fibrosis and cytoprotective effects against Pseudomonas aeruginosa in vitro. Am. J. Respir. Crit. Care Med. 170 (2004) 633-640