Nitrate reduction pathways in mycobacteria and their implications during latency

Microbiology

Volumn 158, Issue 2, 2012, Pages 301-307

  Khan, Arshad ^a   Sarkar, Dhiman ^b  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^b NATIONAL CHEMICAL LABORATORY   (India)

Author keywords

[No Author keywords available]

Indexed keywords

INDUCIBLE NITRIC OXIDE SYNTHASE; NITRATE REDUCTASE; NITRITE; NITROGEN; OXYGEN;

ADAPTATION; BACTERIAL GENOME; BACTERIAL STRAIN; BACTERIAL SURVIVAL; ENVIRONMENT; ENZYME ACTIVITY; GENE CLUSTER; GENE EXPRESSION; HOST CELL; MYCOBACTERIUM; MYCOBACTERIUM BOVIS; MYCOBACTERIUM SMEGMATIS; MYCOBACTERIUM TUBERCULOSIS; NITRATE METABOLISM; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; SINGLE NUCLEOTIDE POLYMORPHISM; TUBERCULOSIS;

ANIMALS; ANTITUBERCULAR AGENTS; DRUG DESIGN; HUMANS; MYCOBACTERIUM; MYCOBACTERIUM INFECTIONS; NITRATES; OXIDATION-REDUCTION;

CORYNEBACTERINEAE; MYCOBACTERIUM TUBERCULOSIS;

EID: 84856695691     PISSN: 13500872     EISSN: None     Source Type: Journal    
DOI: 10.1099/mic.0.054759-0     Document Type: Review

References (68)

1. Aly, S., Wagner, K., Keller, C., Malm, S., Malzan, A., Brandau, S., Bange, F. C. & Ehlers, S. (2006). Oxygen status of lung granulomas in Mycobacterium tuberculosis-infected mice. J Pathol 210, 298-305
2. Berks, B. C., Ferguson, S. J., Moir, J. W. & Richardson, D. J. (1995). Enzymes and associated electron transport systems that catalyse the respiratory reduction of nitrogen oxides and oxyanions. Biochim Biophys Acta 1232, 97-173
3. Betts, J. C., Lukey, P. T., Robb, L. C., McAdam, R. A. & Duncan, K. (2002). Evaluation of a nutrient starvation model of Mycobacterium tuberculosis persistence by gene and protein expression profiling. Mol Microbiol 43, 717-731
4. Bogdan, C., Röllinghoff, M. & Diefenbach, A. (2000). Reactive oxygen and reactive nitrogen intermediates in innate and specific immunity. Curr Opin Immunol 12, 64-76
5. Borgdorff, M. W., Floyd, K. & Broekmans, J. F. (2002). Interventions to reduce tuberculosis mortality and transmission in low-and middle-income countries. Bull World Health Organ 80, 217-227
6. Brown, G. C. (1999). Nitric oxide and mitochondrial respiration. Biochim Biophys Acta 1411, 351-369
7. Camus, J. C., Pryor, M. J., Médigue, C. & Cole, S. T. (2002). Reannotation of the genome sequence of Mycobacterium tuberculosis H37Rv. Microbiology 148, 2967-2973
8. Cegielski, J. P., Chin, D. P., Espinal, M. A., Frieden, T. R., Rodriquez Cruz, R., Talbot, E. A., Weil, D. E. C., Zaleskis, R. & Raviglione, M. C. (2002). The global tuberculosis situation. Progress and problems in the 20th century, prospects for the 21st century. Infect Dis Clin North Am 16, 1-58
9. Cole, S. T., Brosch, R., Parkhill, J., Garnier, T., Churcher, C., Harris, D., Gordon, S. V., Eiglmeier, K., Gas, S. & other authors (1998). Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 393, 537-544
10. Cosma, C. L., Sherman, D. R. & Ramakrishnan, L. (2003). The secret lives of the pathogenic mycobacteria. Annu Rev Microbiol 57, 641-676
11. Dick, T. (2001). Dormant tubercle bacilli: the key to more effective TB chemotherapy? J Antimicrob Chemother 47, 117-118
12. Dick, T., Lee, B. H. & Murugasu-Oei, B. (1998). Oxygen depletion induced dormancy in Mycobacterium smegmatis. FEMS Microbiol Lett 163, 159-164
13. Dye, C., Scheele, S., Dolin, P., Pathania, V. & Raviglione, M. C. (1999). Consensus statement. Global burden of tuberculosis: estimated incidence, prevalence, and mortality by country. WHO Global Surveillance and Monitoring Project. JAMA 282, 677-686
14. Ehrt, S. D. & Schnappinger, D. (2007). Mycobacterium tuberculosis virulence: lipids inside and out. Nat Med 13, 284-285
15. Flesch, I. E. & Kaufmann, S. H. (1991). Mechanisms involved in mycobacterial growth inhibition by gamma interferon-activated bone marrow macrophages: role of reactive nitrogen intermediates. Infect Immun 59, 3213-3218
16. Fritz, C., Maass, S., Kreft, A. & Bange, F. C. (2002). Dependence of Mycobacterium bovis BCG on anaerobic nitrate reductase for persistence is tissue specific. Infect Immun 70, 286-291
17. Gandhi, N. R., Moll, A., Sturm, A. W., Pawinski, R., Govender, T., Lalloo, U., Zeller, K., Andrews, J. & Friedland, G. (2006). Extensively drug-resistant tuberculosis as a cause of death in patients co-infected with tuberculosis and HIV in a rural area of South Africa. Lancet 368, 1575-1580
18. Gbayisomore, A., Lardizabal, A. A. & Reichman, L. B. (2000). Update: prevention and treatment of tuberculosis. Curr Opin Infect Dis 13, 155-159
19. Glaziou, P., Floyd, K. & Raviglione, M. (2009). Global burden and epidemiology of tuberculosis. Clin Chest Med 30, 621-636
20. Goh, K. S., Rastogi, N., Berchel, M., Huard, R. C. & Sola, C. (2005). Molecular evolutionary history of tubercle bacilli assessed by study of the polymorphic nucleotide within the nitrate reductase (narGHJI) operon promoter. J Clin Microbiol 43, 4010-4014
21. Gomez, J. E. & McKinney, J. D. (2004). M. tuberculosis persistence, latency, and drug tolerance. Tuberculosis (Edinb) 84, 29-44
22. Hedgecock, L. W. & Costello, R. L. (1962). Utilization of nitrate by pathogenic and saprophytic mycobacteria. J Bacteriol 84, 195-205
23. Hochstein, L. I. & Tomlinson, G. A. (1988). The enzymes associated with denitrification. Annu Rev Microbiol 42, 231-261
24. Höner zu Bentrup, K. & Russell, D. G. (2001). Mycobacterial persistence: adaptation to a changing environment. Trends Microbiol 9, 597-605
25. Hutter, B. & Dick, T. (1999). Up-regulation of narX, encoding a putative 'fused nitrate reductase' in anaerobic dormant Mycobacterium bovis BCG. FEMS Microbiol Lett 178, 63-69
26. Hutter, B. & Dick, T. (2000). Analysis of the dormancy-inducible narK2 promoter in Mycobacterium bovis BCG. FEMS Microbiol Lett 188, 141-146
27. Kelm, M. (1999). Nitric oxide metabolism and breakdown. Biochim Biophys Acta 1411, 273-289
28. Khan, A. & Sarkar, D. (2006). Identification of a respiratory-type nitrate reductase and its role for survival of Mycobacterium smegmatis in Wayne model. Microb Pathog 41, 90-95
29. Khan, A., Akhtar, S., Ahmad, J. N. & Sarkar, D. (2008). Presence of a functional nitrate assimilation pathway in Mycobacterium smegmatis. Microb Pathog 44, 71-77
30. Lim, A., Eleuterio, M., Hutter, B., Murugasu-Oei, B. & Dick, T. (1999). Oxygen depletion-induced dormancy in Mycobacterium bovis BCG. J Bacteriol 181, 2252-2256
31. Liu, K., Yu, J. & Russell, D. G. (2003). pckA-deficient Mycobacterium bovis BCG shows attenuated virulence in mice and in macrophages. Microbiology 149, 1829-1835
32. Malm, S., Tiffert, Y., Micklinghoff, J., Schultze, S., Joost, I., Weber, I., Horst, S., Ackermann, B., Schmidt, M. & other authors (2009). The roles of the nitrate reductase NarGHJI, the nitrite reductase NirBD and the response regulator GlnR in nitrate assimilation of Mycobacterium tuberculosis. Microbiology 155, 1332-1339
33. McKinney, J. D., Höner zu Bentrup, K., Muñoz-Elías, E. J., Miczak, A., Chen, B., Chan, W. T., Swenson, D., Sacchettini, J. C., Jacobs, W. R., Jr & Russell, D. G. (2000). Persistence of Mycobacterium tuberculosis in macrophages and mice requires the glyoxylate shunt enzyme isocitrate lyase. Nature 406, 735-738
34. Moreno-Vivián, C., Cabello, P., Martínez-Luque, M., Blasco, R. & Castillo, F. (1999). Prokaryotic nitrate reduction: molecular properties and functional distinction among bacterial nitrate reductases. J Bacteriol 181, 6573-6584
35. Muñoz-Elías, E. J. & McKinney, J. D. (2005). Mycobacterium tuberculosis isocitrate lyases 1 and 2 are jointly required for in vivo growth and virulence. Nat Med 11, 638-644
36. Muñoz-Elías, E. J., Upton, A. M., Cherian, J. & McKinney, J. D. (2006). Role of the methylcitrate cycle in Mycobacterium tuberculosis metabolism, intracellular growth, and virulence. Mol Microbiol 60, 1109-1122
37. Pandey, A. K. & Sassetti, C. M. (2008). Mycobacterial persistence requires the utilization of host cholesterol. Proc Natl Acad Sci U S A 105, 4376-4380
38. Parrish, N. M., Dick, J. D. & Bishai, W. R. (1998). Mechanisms of latency in Mycobacterium tuberculosis. Trends Microbiol 6, 107-112
39. Rhee, K. Y., de Carvalho, L. P., Bryk, R., Ehrt, S., Marrero, J., Park, S. W., Schnappinger, D., Venugopal, A. & Nathan, C. (2011). Central carbon metabolism in Mycobacterium tuberculosis: an unexpected frontier. Trends Microbiol 19, 307-314
40. Russell, D. G., VanderVen, B. C., Lee, W., Abramovitch, R. B., Kim, M. J., Homolka, S., Niemann, S. & Rohde, K. H. (2010). Mycobacterium tuberculosis wears what it eats. Cell Host Microbe 8, 68-76
41. Rustad, T. R., Harrell, M. I., Liao, R. & Sherman, D. R. (2008). The enduring hypoxic response of Mycobacterium tuberculosis. PLoS ONE 3, e1502.
42. Rustad, T. R., Sherrid, A. M., Minch, K. J. & Sherman, D. R. (2009). Hypoxia: a window into Mycobacterium tuberculosis latency. Cell Microbiol 11, 1151-1159
43. Savvi, S., Warner, D. F., Kana, B. D., McKinney, J. D., Mizrahi, V. & Dawes, S. S. (2008). Functional characterization of a vitamin B12-dependent methylmalonyl pathway in Mycobacterium tuberculosis: implications for propionate metabolism during growth on fatty acids. J Bacteriol 190, 3886-3895
44. Schnappinger, D., Ehrt, S., Voskuil, M. I., Liu, Y., Mangan, J. A., Monahan, I. M., Dolganov, G., Efron, B., Butcher, P. D. & other authors (2003). Transcriptional adaptation of Mycobacterium tuberculosis within macrophages: insights into the phagosomal environment. J Exp Med 198, 693-704
45. Shi, S. & Ehrt, S. (2006). Dihydrolipoamide acyltransferase is critical for Mycobacterium tuberculosis pathogenesis. Infect Immun 74, 56-63
46. Shi, L. B., Sohaskey, C. D., Kana, B. D., Dawes, S., North, R. J., Mizrahi, V. & Gennaro, M. L. (2005). Changes in energy metabolism of Mycobacterium tuberculosis in mouse lung and under in vitro conditions affecting aerobic respiration. Proc Natl Acad Sci U S A 102, 15629-15634
47. Shi, L., Sohaskey, C. D., Pfeiffer, C., Datta, P., Parks, M., McFadden, J., North, R. J. & Gennaro, M. L. (2010). Carbon flux rerouting during Mycobacterium tuberculosis growth arrest. Mol Microbiol 78, 1199-1215
48. Sohaskey, C. D. (2005). Regulation of nitrate reductase activity in Mycobacterium tuberculosis by oxygen and nitric oxide. Microbiology 151, 3803-3810
49. Sohaskey, C. D. (2008). Nitrate enhances the survival of Mycobacterium tuberculosis during inhibition of respiration. J Bacteriol 190, 2981-2986
50. Sohaskey, C. D. & Modesti, L. (2009). Differences in nitrate reduction between Mycobacterium tuberculosis and Mycobacterium bovis are due to differential expression of both narGHJI and narK2. FEMS Microbiol Lett 290, 129-134
51. Sohaskey, C. D. & Wayne, L. G. (2003). Role of narK2X and narGHJI in hypoxic upregulation of nitrate reduction by Mycobacterium tuberculosis. J Bacteriol 185, 7247-7256
52. Stermann, M., Bohrssen, A., Diephaus, C., Maass, S. & Bange, F. C. (2003). Polymorphic nucleotide within the promoter of nitrate reductase (NarGHJI) is specific for Mycobacterium tuberculosis. J Clin Microbiol 41, 3252-3259
53. Stermann, M., Sedlacek, L., Maass, S. & Bange, F. C. (2004). A promoter mutation causes differential nitrate reductase activity of Mycobacterium tuberculosis and Mycobacterium bovis. J Bacteriol 186, 2856-2861
54. Stewart, G. R., Robertson, B. D. & Young, D. B. (2003). Tuberculosis: a problem with persistence. Nat Rev Microbiol 1, 97-105
55. Stuehr, D. J. (1999). Mammalian nitric oxide synthases. Biochim Biophys Acta 1411, 217-230
56. Tan, M. P., Sequeira, P., Lin, W. W., Phong, W. Y., Cliff, P., Ng, S. H., Lee, B. H., Camacho, L., Schnappinger, D. & other authors (2010). Nitrate respiration protects hypoxic Mycobacterium tuberculosis against acid-and reactive nitrogen species stresses. PLoS ONE 5, e13356.
57. Tsai, M. C., Chakravarty, S., Zhu, G. F., Xu, J. Y., Tanaka, K., Koch, C., Tufariello, J., Flynn, J. & Chan, J. (2006). Characterization of the tuberculous granuloma in murine and human lungs: cellular composition and relative tissue oxygen tension. Cell Microbiol 8, 218-232
58. Via, L. E., Lin, P. L., Ray, S. M., Carrillo, J., Allen, S. S., Eum, S. Y., Taylor, K., Klein, E., Manjunatha, U. & other authors (2008). Tuberculous granulomas are hypoxic in guinea pigs, rabbits, and nonhuman primates. Infect Immun 76, 2333-2340
59. Virtanen, S. (1960). A study of nitrate reduction by mycobacteria. The use of the nitrate reduction test in the identification of mycobacteria. Acta Tuberc Scand, Suppl 48, 1-119
60. Wayne, L. G. (2001). In vitro model of hypoxically induced nonreplicating persistence of Mycobacterium tuberculosis. Methods Mol Med 54, 247-269
61. Wayne, L. G. & Doubek, J. R. (1965). Classification and identification of mycobacteria. II. Tests employing nitrate and nitrite as substrate. Am Rev Respir Dis 91, 738-745
62. Wayne, L. G. & Hayes, L. G. (1996). An in vitro model for sequential study of shiftdown of Mycobacterium tuberculosis through two stages of nonreplicating persistence. Infect Immun 64, 2062-2069
63. Wayne, L. G. & Hayes, L. G. (1998). Nitrate reduction as a marker for hypoxic shiftdown of Mycobacterium tuberculosis. Tuber Lung Dis 79, 127-132
64. Wayne, L. G. & Lin, K. Y. (1982). Glyoxylate metabolism and adaptation of Mycobacterium tuberculosis to survival under anaerobic conditions. Infect Immun 37, 1042-1049
65. Wayne, L. G. & Sohaskey, C. D. (2001). Nonreplicating persistence of Mycobacterium tuberculosis. Annu Rev Microbiol 55, 139-163
66. Weber, I., Fritz, C., Ruttkowski, S., Kreft, A. & Bange, F. C. (2000). Anaerobic nitrate reductase (narGHJI) activity of Mycobacterium bovis BCG in vitro and its contribution to virulence in immunodeficient mice. Mol Microbiol 35, 1017-1025
67. World Health Organization (2007). Tuberculosis fact sheet number 104, revised March 2007. World Health Organization, Geneva, Switzerland. http://www.who.int/mediacentre/factsheets/fs104/en/.
68. World Health Organization (2008). WHO Report: Global Tuberculosis Control: Surveillance, Planning, Financing. (WHO/HTM/TB/2008.376). Geneva: World Health Organization.