The Warburg effect in mycobacterial granulomas is dependent on the recruitment and activation of macrophages by interferon-γ

Immunology

Volumn 145, Issue 4, 2015, Pages 498-507

  Appelberg, Rui ^a   Moreira, Diana ^a,b   Barreira Silva, Palmira ^c,d   Borges, Margarida ^a,b   Silva, Letícia ^a   Dinis Oliveira, Ricardo Jorge ^b,e,f   Resende, Mariana ^c,d   Correia Neves, Margarida ^c,d   Jordan, Michael B ^g   Ferreira, Nuno C ^h   Abrunhosa, Antero J ^h   Silvestre, Ricardo ^a,c,d  

^a UNIVERSITY OF PORTO   (Portugal)

^b UNIVERSITY OF PORTO   (Portugal)

^c UNIVERSITY OF MINHO   (Portugal)

^d UNIVERSITY OF MINHO   (Portugal)

^e University of Porto   (Portugal)

^f INSTITUTO DE INVESTIGAÇÃO E FORMAÇÃO AVANÇADA EM CIÊNCIAS E TECNOLOGIAS DA SAÚDE   (Portugal)

^g UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^h UNIVERSITY OF COIMBRA   (Portugal)

Author keywords

Glycolysis; Infection; Interferon ; Macrophages; Mycobacteria

Indexed keywords

GLYCOLYTIC ENZYME; LACTIC ACID; RECOMBINANT INTERFERON; FLUORODEOXYGLUCOSE F 18; GAMMA INTERFERON; RADIOPHARMACEUTICAL AGENT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ATYPICAL MYCOBACTERIOSIS; CELL ACTIVITY; CONTROLLED STUDY; EX VIVO STUDY; GLUCOSE METABOLISM; GLUCOSE TRANSPORT; GLYCOLYSIS; GRANULOMA; GRANULOMATOSIS; IN VITRO STUDY; MACROPHAGE; MACROPHAGE ACTIVATION; MOUSE; MYCOBACTERIUM AVIUM; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; WARBURG EFFECT; ANIMAL; DRUG EFFECTS; GENETICS; IMMUNOLOGY; KNOCKOUT MOUSE; MICROBIOLOGY; PATHOLOGY; TUBERCULOSIS; VETERINARY;

ANIMALS; FLUORODEOXYGLUCOSE F18; GLYCOLYSIS; GRANULOMA; INTERFERON-GAMMA; LACTIC ACID; MACROPHAGE ACTIVATION; MACROPHAGES; MICE; MICE, KNOCKOUT; MYCOBACTERIUM AVIUM; RADIOPHARMACEUTICALS; TUBERCULOSIS;

EID: 84936175105     PISSN: 00192805     EISSN: 13652567     Source Type: Journal    
DOI: 10.1111/imm.12464     Document Type: Article

References (35)

1. Warburg O, Wind F, Negelein E. The metabolism of tumors in the body. J Gen Physiol 1927; 8: 519-30.
2. Palsson-McDermott EM, O'Neill LAJ. The Warburg effect then and now: from cancer to inflammatory diseases. BioEssays 2013; 35:965-73.
3. Schmidt KC, Lucignami G, Sokoloff L. Fluorine-18-Fluorodeoxyglucose PET to determine regional cerebral glucose utilization: a re-examination. J Nucl Med 1996; 37:394-9.
4. Gotthardt M, Bleeker-Rovers CP, Boerman OC, Oyen WJG. Imaging of inflammation by PET, conventional scintigraphy, and other imaging techniques. J Nucl Med 2010; 51:1937-49.
5. 18F]-2-fluoro-2-deoxyglucose transport kinetics as a function of extracellular glucose concentration in malignant glioma, fibroblast and macrophage cells in vitro. Nucl Med Biol 2004; 31:1-9.
6. Hofmeyr A, Eddie Lau WF, Slavin MA. Mycobacterium tuberculosis infection in patients with cancer, the role of 18-fluorodeoxyglucose positron emission tomography for diagnosis and monitoring treatment response. Tuberculosis 2007; 87:459-63.
7. 18F-FDG Pet-CT for determination of pulmonary tuberculoma activity. Eur J Nucl Med Mol Imaging 2008; 35:808-14.
8. 18F]-2-Fluoro-deoxy-d-glucose positron emission tomography correlates with bactericidal activity of tuberculosis drug treatment. Antimicrob Agents Chemother 2009; 53:4879-84.
9. 18F]2-fluoro-deoxy-d-glucose positron emission tomography and computed tomography. Antimicrob Agents Chemother 2012; 56:4391-402.
10. Somashekar BS, Amin AG, Rithner CD, Troudt J, Basaraba R, Izzo A, Crick DC, Chatterjee D. Metabolic profiling of lung granuloma in Mycobacterium tuberculosis infected guinea pigs: ex vivo 1H magic angle spinnng NMR studies. J Proteome Res 2011; 10:4186-95.
11. Mehrotra P, Jamwal SV, Saquib N, Sinha N, Siddiqui Z, Manivel V, Chatterjee S, Rao KV. Pathogenicity of Mycobacterium tuberculosis is expressed by regulating metabolic thresholds of the host macrophage. PLoS Pathog 2014; 10:e1004265.
12. Newsholme P, Curi R, Gordon S, Newsholme EA. Metabolism of glucose, glutamine, long-chain fatty acids and ketone bodies by murine macrophages. Biochem J 1986; 239:121-5.
13. McGettrick AF, O'Neill LAJ. How metabolism generates signals during innate immunity and inflammation. J Biol Chem 2013; 288:22893-7.
14. Rodriguez-Prados J-C, Través PG, Cuenca J, Rico D, Aragonés J, Martin-Sanz P, Cascante M, Boscá L. Substrate fate in activated macrophages: a comparison between innate, classic, and alternative activation. J Immunol 2010; 185:605-14.
15. Krawczyk CM, Holowka T, Sun J et al. Toll-like receptor-induced changes in glycolytic metabolism regulate dendritic cell activation. Blood 2010; 115:4742-9.
16. Wang R, Green DR. Metabolic checkpoints in activated T cells. Nat Immunol 2012; 13:907-15.
17. Pearce EL, Pearce EJ. Metabolic pathways in immune cell activation and quiescence. Immunity 2013; 38:633-43.
18. Shaler CR, Horvath CN, Jeyanathan M, Xing Z. Within the Enemy's Camp: contribution of the granuloma to the dissemination, persistence and transmission of Mycobacterium tuberculosis. Front Immunol 2013; 4:30.
19. Gonzalez-Juarrero M, Turner OC, Turner J, Marietta P, Brooks JV, Orme IM. Temporal and spatial arrangement of lymphocytes within lung granulomas induced by aerosol infection with Mycobacterium tuberculosis. Infect Immun 2001; 69:1722-8.
20. Tsai MC, Chakravarty S, Zhu G et al. Characterization of the tuberculous granuloma in murine and human lungs: cellular composition and relative tissue oxygen tension. Cell Microbiol 2006; 8:218-32.
21. Egen JG, Rothfuchs AG, Feng CG, Winter N, Sher A, Germain RN. Macrophage and T cell dynamics during the development and disintegration of mycobacterial granulomas. Immunity 2008; 28: 271-84.
22. Appelberg R, Castro AG, Pedrosa J, Silva RA, Orme IM, Minóprio P. The role of gamma interferon and tumor necrosis factor-alpha during the T cell independent and dependent phases of Mycobacterium avium infection. Infect Immun 1994; 62:3962-71.
23. Flórido M, Gonçalves AS, Silva RA, Ehlers S, Cooper AM, Appelberg R. Resistance of virulent Mycobacterium avium to interferon-γ-mediated antimicrobial activity suggests additional signals for induction of mycobacteriostasis. Infect Immun 1999; 67:3610-8.
24. Flórido M, Pearl JE, Solache A, Borges M, Haynes L, Cooper AM, Appelberg R. Gamma interferon-induced T cell loss in virulent Mycobacterium avium infection. Infect Immun 2005; 73:3577-86.
25. Flórido M, Cooper AM, Appelberg R. Immunological basis of the development of necrotic lesions following Mycobacterium avium infection. Immunology 2002; 106:590-601.
26. Aly S, Wagner K, Keller C, Malm S, Malzan A, Brandau S, Bange FC, Ehlers S. Oxygen status of lung granulomas in Mycobacterium tuberculosis-infected mice. J Pathol 2006; 210:298-305.
27. Lykens JE, Terrell CE, Zoller EE et al. Mice with a selective impairment of IFN-γ signaling in macrophage lineage cells demonstrate the critical role of IFN-γ-activated macrophages for the control of protozoan parasitic infections in vivo. J Immunol 2010; 184:877-85.
28. Hamacher K, Coennen HH, Stoecklin G. Efficient stereospecific synthesis of no-carrier-added 2-[F-18]-fluoro-2-deoxy-d-glucose using aminopolyether supported nucleophilic substitution. J Nucl Med 1986; 27:235-8.
29. 18F]-FDG production with terminal sterilization by autoclave. J Nucl Med 2012; 53:524.
30. Abreu MC, Aguiar JD, Almeida FG et al. Design and evaluation of the Clear-PEM scanner for positron emission mammography. IEEE Trans Nucl Sci 2006; 53:71-7.
31. Garedew A, Moncada S. Mitochondrial dysfunction and HIF1α stabilization in inflammation. J Cell Sci 2008; 121:3468-75.
32. Gomes MS, Flórido M, Pais TF, Appelberg R. Improved clearance of Mycobacterium avium upon disruption of the iNOS gene. J Immunol 1999; 162:6734-9.
33. Fischer K, Hoffmann P, Voekl S et al. Inhibitory effect of tumor cell-derived lactic acid on human T cells. Blood 2007; 109: 3812-9.
34. Egen JG, Rothfuchs AG, Feng CG, Horwitz MA, Sher A, Germain RN. Intravital imaging reveals limited antigen presentation and T cell effector function in mycobacterial granulomas. Immunity 2011; 34:807-19.
35. Pearce EL, Poffenberger MC, Chang CH, Jones RG Fueling immunity: insights into metabolism and lymphocyte function. Science 2013; 342: 1242454. doi: 10.1126/science.1242454.