Isocitrate lyase mediates broad antibiotic tolerance in Mycobacterium tuberculosis

Nature Communications

Volumn 5, Issue , 2014, Pages

  Nandakumar, Madhumitha ^a   Nathan, Carl ^a   Rhee, Kyu Y ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ISOCITRATE LYASE; ISONIAZID; RIFAMPICIN; STREPTOMYCIN; BACTERIAL PROTEIN; TUBERCULOSTATIC AGENT;

ANTIBIOTICS; ANTIOXIDANT; BACTERIUM; CELL ORGANELLE; ENZYME ACTIVITY; HOST-PATHOGEN INTERACTION; METABOLISM;

ANTIBIOTIC SENSITIVITY; ANTIBIOTIC THERAPY; ARTICLE; BACTERIAL STRAIN; CITRIC ACID CYCLE; DRUG METABOLISM; DRUG TOLERANCE; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; WILD TYPE; ANTIBIOTIC RESISTANCE; DRUG EFFECTS; ENZYMOLOGY; GENETICS; METABOLISM; MICROBIAL VIABILITY;

ANTITUBERCULAR AGENTS; BACTERIAL PROTEINS; CITRIC ACID CYCLE; DRUG RESISTANCE, BACTERIAL; ISOCITRATE LYASE; MICROBIAL VIABILITY; MYCOBACTERIUM TUBERCULOSIS;

EID: 84903593464     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms5306     Document Type: Article

References (37)

1. Raviglione, M. et al. Scaling up interventions to achieve global tuberculosis control: progress and new developments. Lancet 379, 1902-1913 (2012).
2. Russell, D. G., Barry, 3rd C. E. & Flynn, J. L. Tuberculosis: what we don't know can, and does, hurt us. Science 328, 852-856 (2010).
3. Nguyen, L. & Thompson, C. J. Foundations of antibiotic resistance in bacterial physiology: the mycobacterial paradigm. Trends Microbiol. 14, 304-312 (2006). (Pubitemid 43963364)
4. Silver, L. L. Challenges of antibacterial discovery. Clin. Microbiol. Rev. 24, 71-109 (2011).
5. Jarlier, V. & Nikaido, H. Mycobacterial cell wall: structure and role in natural resistance to antibiotics. FEMS Microbiol. Lett. 123, 11-18 (1994). (Pubitemid 24312557)
6. Nikaido, H. Prevention of drug access to bacterial targets: permeability barriers and active efflux. Science 264, 382-388 (1994). (Pubitemid 24178901)
7. Baek, S. H., Li, A. H. & Sassetti, C. M. Metabolic regulation of mycobacterial growth and antibiotic sensitivity. PLoS Biol. 9, e1001065 (2011).
8. Morris, R. P. et al. Ancestral antibiotic resistance in Mycobacterium tuberculosis. Proc. Natl Acad. Sci. USA 102, 12200-12205 (2005). (Pubitemid 41291152)
9. Nguyen, D. et al. Active starvation responses mediate antibiotic tolerance in biofilms and nutrient-limited bacteria. Science 334, 982-986 (2011).
10. Smith, P. A. & Romesberg, F. E. Combating bacteria and drug resistance by inhibiting mechanisms of persistence and adaptation. Nat. Chem. Biol. 3, 549-556 (2007). (Pubitemid 47294401)
11. Theodore, A., Lewis, K. & Vulic, M. Tolerance of Escherichia coli to fluoroquinolone antibiotics depends on specific components of the SOS response pathway. Genetics 195, 1265-1276 (2013).
12. Amato, S. M., Orman, M. A. & Brynildsen, M. P. Metabolic control of persister formation in Escherichia coli. Mol. Cell 50, 475-487 (2013).
13. Saghatelian, A. & Cravatt, B. F. Global strategies to integrate the proteome and metabolome. Curr. Opin. Chem. Biol. 9, 62-68 (2005). (Pubitemid 40208626)
14. Chakraborty, S., Gruber, T., Barry, 3rd C. E., Boshoff, H. I. & Rhee, K. Y. Paraaminosalicylic acid acts as an alternative substrate of folate metabolism in Mycobacterium tuberculosis. Science 339, 88-91 (2013).
15. Brook, I. Inoculum effect. Rev. Infect. Dis. 11, 361-368 (1989).
16. Kohanski, M. A., Dwyer, D. J., Hayete, B., Lawrence, C. A. & Collins, J. J. A common mechanism of cellular death induced by bactericidal antibiotics. Cell 130, 797-810 (2007). (Pubitemid 47332566)
17. Gould, T. A., van de Langemheen, H., Munoz-Elias, E. J., McKinney, J. D. & Sacchettini, J. C. Dual role of isocitrate lyase 1 in the glyoxylate and methylcitrate cycles in Mycobacterium tuberculosis. Mol. Microbiol. 61, 940-947 (2006). (Pubitemid 44134171)
18. McKinney, J. D. et al. Persistence of Mycobacterium tuberculosis in macrophages and mice requires the glyoxylate shunt enzyme isocitrate lyase. Nature 406, 735-738 (2000).
19. Munoz-Elias, E. J. & McKinney, J. D. Mycobacterium tuberculosis isocitrate lyases 1 and 2 are jointly required for in vivo growth and virulence. Nat. Med. 11, 638-644 (2005). (Pubitemid 40868304)
20. Trivedi, A., Singh, N., Bhat, S. A., Gupta, P. & Kumar, A. Redox biology of tuberculosis pathogenesis. Adv. Microb. Physiol. 60, 263-324 (2012).
21. Cole, S. T. et al. Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 393, 537-544 (1998). (Pubitemid 28319235)
22. Boshoff, H. I. et al. The transcriptional responses of Mycobacterium tuberculosis to inhibitors of metabolism: novel insights into drug mechanisms of action. J. Biol. Chem. 279, 40174-40184 (2004). (Pubitemid 39258293)
23. Timm, J. 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, 14321-14326 (2003). (Pubitemid 37499235)
24. Voskuil, M. I. et al. Inhibition of respiration by nitric oxide induces a Mycobacterium tuberculosis dormancy program. J. Exp. Med. 198, 705-713 (2003). (Pubitemid 37087770)
25. Imlay, J. A. The molecular mechanisms and physiological consequences of oxidative stress: lessons from a model bacterium. Nat. Rev. Microbiol. 11, 443-454 (2013).
26. Wilcox, C. S. & Pearlman, A. Chemistry and antihypertensive effects of tempol and other nitroxides. Pharmacol. Rev. 60, 418-469 (2008).
27. Allison, K. R., Brynildsen, M. P. & Collins, J. J. Metabolite-enabled eradication of bacterial persisters by aminoglycosides. Nature 473, 216-220 (2011).
28. Tuomanen, E., Cozens, R., Tosch, W., Zak, O. & Tomasz, A. The rate of killing of Escherichia coli by beta-lactam antibiotics is strictly proportional to the rate of bacterial growth. J. Gen. Microbiol. 132, 1297-1304 (1986). (Pubitemid 16115638)
29. Keren, I., Wu, Y., Inocencio, J., Mulcahy, L. R. & Lewis, K. Killing by bactericidal antibiotics does not depend on reactive oxygen species. Science 339, 1213-1216 (2013).
30. Liu, Y. & Imlay, J. A. Cell death from antibiotics without the involvement of reactive oxygen species. Science 339, 1210-1213 (2013).
31. Garrett, R. & Grisham, C. M. Biochemistry 5th edn (Cengage Learning, 2013).
32. Kohanski, M. A., Dwyer, D. J., Wierzbowski, J., Cottarel, G. & Collins, J. J. Mistranslation of membrane proteins and two-component system activation trigger antibiotic-mediated cell death. Cell 135, 679-690 (2008).
33. Shen, E. Z. et al. Mitoflash frequency in early adulthood predicts lifespan in Caenorhabditis elegans. Nature 508, 128-132 (2014).
34. du Preez, I. & Loots, D. T. New sputum metabolite markers implicating adaptations of the host to Mycobacterium tuberculosis, and vice versa. Tuberculosis (Edinb) 93, 330-337 (2013).
35. Eoh, H. & Rhee, K. Y. Multifunctional essentiality of succinate metabolism in adaptation to hypoxia in Mycobacterium tuberculosis. Proc. Natl Acad. Sci. USA 110, 6554-6559 (2013).
36. Gengenbacher, M., Xu, T., Niyomrattanakit, P., Spraggon, G. & Dick, T. Biochemical and structural characterization of the putative dihydropteroate synthase ortholog Rv1207 of Mycobacterium tuberculosis. FEMS Microbiol. Lett. 287, 128-135 (2008).
37. de Carvalho, L. P. et al. Metabolomics of Mycobacterium tuberculosis reveals compartmentalized co-catabolism of carbon substrates. Chem. Biol. 17, 1122-1131 (2010).