Cutting edge: Mycobacterium tuberculosis induces aerobic glycolysis in human alveolar macrophages that is required for control of intracellular bacillary replication

Journal of Immunology

Volumn 196, Issue 6, 2016, Pages 2444-2449

  Gleeson, Laura E ^a   Sheedy, Frederick J ^a   Palsson McDermott, Eva M ^b   Triglia, Denise ^a   O'Leary, Seonadh M ^a   O'Sullivan, Mary P ^a   O'Neill, Luke A J ^b   Keane, Joseph ^a  

^a ST JAMES S HOSPITAL   (Ireland)

^b TRINITY COLLEGE DUBLIN   (Ireland)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 1 RECEPTOR; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; LACTATE DEHYDROGENASE; TUMOR NECROSIS FACTOR ALPHA;

AEROBIC METABOLISM; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BACTERIAL STRAIN; BACTERIAL SURVIVAL; BACTERICIDAL ACTIVITY; BACTERIUM ISOLATION; CELL GROWTH; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENZYME KINETICS; ENZYME RELEASE; ENZYME SYNTHESIS; GLUCOSE METABOLISM; GLYCOLYSIS; HUMAN; HUMAN CELL; MACROPHAGE; MONOCYTE; MOUSE; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; OXIDATIVE PHOSPHORYLATION; PRIORITY JOURNAL; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; CELL CULTURE; ENZYME LINKED IMMUNOSORBENT ASSAY; IMMUNOLOGY; INNATE IMMUNITY; LUNG ALVEOLUS MACROPHAGE; LUNG TUBERCULOSIS; METABOLISM; MICROBIOLOGY; REAL TIME POLYMERASE CHAIN REACTION;

ANIMALS; CELLS, CULTURED; ENZYME-LINKED IMMUNOSORBENT ASSAY; GLYCOLYSIS; HUMANS; IMMUNITY, INNATE; INTERLEUKIN-1BETA; MACROPHAGES, ALVEOLAR; MICE; MICE, INBRED C57BL; MYCOBACTERIUM TUBERCULOSIS; REAL-TIME POLYMERASE CHAIN REACTION; TUBERCULOSIS, PULMONARY;

EID: 84962617442     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1501612     Document Type: Article

References (23)

1. Chackerian, A. A., J. M. Alt, T. V. Perera, C. C. Dascher, and S. M. Behar. 2002. Dissemination of Mycobacterium tuberculosis is influenced by host factors and precedes the initiation of T-cell immunity. Infect. Immun. 70:4501-4509.
2. Mayer-Barber, K. D., D. L. Barber, K. Shenderov, S. D. White, M. S. Wilson, A. Cheever, D. Kugler, S. Hieny, P. Caspar, G. Núñez, et al. 2010. Caspase-1 independent IL-1beta production is critical for host resistance to Mycobacterium tuberculosis and does not require TLR signaling in vivo. J. Immunol. 184:3326-3330.
3. Fremond, C. M., D. Togbe, E. Doz, S. Rose, V. Vasseur, I. Maillet, M. Jacobs, B. Ryffel, and V. F. Quesniaux. 2007. IL-1 receptor-mediated signal is an essential component of MyD88-dependent innate response to Mycobacterium tuberculosis infection. J. Immunol. 179:1178-1189.
4. Schenk, M., M. Fabri, S. R. Krutzik, D. J. Lee, D. M. Vu, P. A. Sieling, D. Montoya, P. T. Liu, and R. L. Modlin. 2014. Interleukin-1β triggers the differentiation of macrophages with enhanced capacity to present mycobacterial antigen to T cells. Immunology 141:174-180.
5. Krawczyk, C. M., T. Holowka, J. Sun, J. Blagih, E. Amiel, R. J. De Berardinis, J. R. Cross, E. Jung, C. B. Thompson, R. G. Jones, and E. J. Pearce. 2010. Toll-like receptor-induced changes in glycolytic metabolism regulate dendritic cell activation. Blood 115:4742-4749.
6. Tannahill, G. M., A. M. Curtis, J. Adamik, E. M. Palsson-McDermott, A. F. McGettrick, G. Goel, C. Frezza, N. J. Bernard, B. Kelly, N. H. Foley, et al. 2013. Succinate is an inflammatory signal that induces IL-1β through HIF-1α. Nature 496:238-242.
7. Palsson-McDermott, E. M., A. M. Curtis, G. Goel, M. A. Lauterbach, F. J. Sheedy, L. E. Gleeson, M. W. Van Den Bosch, S. R. Quinn, R. Domingo-Fernandez, D. G. Johnston, et al. 2015. Pyruvate kinase M2 regulates Hif-1α activity and IL-1β induction and is a critical determinant of the warburg effect in LPS-activated macrophages. Cell Metab. 21:65-80.
8. O'Leary, S., M. P. O'Sullivan, and J. Keane. 2011. IL-10 blocks phagosome maturation in Mycobacterium tuberculosis-infected human macrophages. Am. J. Respir. Cell Mol. Biol. 45:172-180.
9. O'Leary, S. M., M. M. Coleman, W. M. Chew, C. Morrow, A. M. McLaughlin, L. E. Gleeson, M. P. O'Sullivan, and J. Keane. 2014. Cigarette smoking impairs human pulmonary immunity to Mycobacterium tuberculosis. Am. J. Respir. Crit. Care Med. 190:1430-1436.
10. Doherty, J. R., and J. L. Cleveland. 2013. Targeting lactate metabolism for cancer therapeutics. J. Clin. Invest. 123:3685-3692.
11. Marroquin, L. D., J. Hynes, J. A. Dykens, J. D. Jamieson, and Y. Will. 2007. Circumventing the Crabtree effect: replacing media glucose with galactose increases susceptibility of HepG2 cells to mitochondrial toxicants. Toxicol. Sci. 97:539-547.
12. Rossignol, R., R. Gilkerson, R. Aggeler, K. Yamagata, S. J. Remington, and R. A. Capaldi. 2004. Energy substrate modulates mitochondrial structure and oxidative capacity in cancer cells. Cancer Res. 64:985-993.
13. Mayer-Barber, K. D., B. B. Andrade, S. D. Oland, E. P. Amaral, D. L. Barber, J. Gonzales, S. C. Derrick, R. Shi, N. P. Kumar, W. Wei, et al. 2014. Host-directed therapy of tuberculosis based on interleukin-1 and type I interferon crosstalk. Nature 511:99-103.
14. Mathis, D., and S. E. Shoelson. 2011. Immunometabolism: an emerging frontier. Nat. Rev. Immunol. 11:81.
15. Martinez, J., K. Verbist, R. Wang, and D. R. Green. 2013. The relationship between metabolism and the autophagy machinery during the innate immune response. Cell Metab. 17:895-900.
16. Cheng, S. C., J. Quintin, R. A. Cramer, K. M. Shepardson, S. Saeed, V. Kumar, E. J. Giamarellos-Bourboulis, J. H. Martens, N. A. Rao, A. Aghajanirefah, et al. 2014. mTOR- and HIF-1α-mediated aerobic glycolysis as metabolic basis for trained immunity. Science 345:1250684.
17. Lachmandas, E., F. Vrieling, L. G. Wilson, S. A. Joosten, M. G. Netea, T. H. Ottenhoff, and R. Van Crevel. 2015. The effect of hyperglycaemia on in vitro cytokine production and macrophage infection with Mycobacterium tuberculosis. PLoS One 10:e0117941.
18. Jayaraman, P., I. Sada-Ovalle, T. Nishimura, A. C. Anderson, V. K. Kuchroo, H. G. Remold, and S. M. Behar. 2013. IL-1β promotes antimicrobial immunity in macrophages by regulating TNFR signaling and caspase-3 activation. J. Immunol. 190:4196-4204.
19. Mehrotra, P., S. V. Jamwal, N. Saquib, N. Sinha, Z. Siddiqui, V. Manivel, S. Chatterjee, and K. V. Rao. 2014. Pathogenicity of Mycobacterium tuberculosis is expressed by regulating metabolic thresholds of the host macrophage. PLoS Pathog. 10:e1004265.
20. Chen, M., M. Divangahi, H. Gan, D. S. Shin, S. Hong, D. M. Lee, C. N. Serhan, S. M. Behar, and H. G. Remold. 2008. Lipid mediators in innate immunity against tuberculosis: opposing roles of PGE2 and LXA4 in the induction of macrophage death. J. Exp. Med. 205:2791-2801.
21. Rosa, L. F., Y. Cury, and R. Curi. 1992. Effects of insulin, glucocorticoids and thyroid hormones on the activities of key enzymes of glycolysis, glutaminolysis, the pentose-phosphate pathway and the Krebs cycle in rat macrophages. J. Endocrinol. 135:213-219.
22. Yamasawa, H., M. Nakayama, M. Bando, and Y. Sugiyama. 2012. Impaired inflammatory responses to multiple toll-like receptor ligands in alveolar macrophages of streptozotocin-induced diabetic mice. Inflamm. Res. 61:417-426.
23. Gohil, V. M., S. A. Sheth, R. Nilsson, A. P. Wojtovich, J. H. Lee, F. Perocchi, W. Chen, C. B. Clish, C. Ayata, P. S. Brookes, and V. K. Mootha. 2010. Nutrientsensitized screening for drugs that shift energy metabolism from mitochondrial respiration to glycolysis. Nat. Biotechnol. 28:249-255.