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Immune Control of Tuberculosis by IFN-γ-Inducible LRG-47
Open accessAbstract
Interferon-γ (IFN-γ) provides an essential component of immunity to tuberculosis by activating infected host macrophages to directly inhibit the replication of Mycobacterium tuberculosis ( Mtb ). IFN-γ–inducible nitric oxide synthase 2 (NOS2) is considered a principal effector mechanism, although other pathways may also exist. Here, we identify one member of a newly emerging 47-kilodalton (p47) guanosine triphosphatase family, LRG-47, that acts independently of NOS2 to protect against disease. Mice lacking LRG-47 failed to control Mtb replication, unlike those missing the related p47 guanosine triphosphatases IRG-47 or IGTP. Defective bacterial killing in IFN-γ–activated LRG-47 –/– macrophages was associated with impaired maturation of Mtb -containing phagosomes, vesicles that otherwise recruited LRG-47 in wild-type cells. Thus, LRG-47 may serve as a critical vacuolar trafficking component used to dispose of intracellular pathogens like Mtb .
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“Upon stimulation with IFN-γ, macrophages activate GTPases, which are responsible for the recruitment of NOX2 to the mycobacterial phagosome (62, 63).”
From Macrophage defense mechanisms against intracellular bacteria (2015) · cites this paper as [63]
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Kaufmann, S. H. E., Lange, C. G., Rao, M., Balaji, K. N., Lotze, M. T., Schito, M. L., Zumla, A. I., & Maeurer, M. J. (2014) · The Lancet Respiratory Medicine · doi:10.1016/s2213-2600(14)70033-5 · Cited by 219
Interferon-Inducible GTPases in Host Resistance, Inflammation and Disease
Pilla-Moffett, D. M., Barber, M. F., Taylor, G. A., & Coers, J. (2016) · Journal of Molecular Biology · doi:10.1016/j.jmb.2016.04.032 · Cited by 223
Self-citationJayaraman, P., Sada‐Ovalle, I., Nishimura, T., Anderson, A. C., Kuchroo, V. K., Remold, H. G., & Behar, S. M. (2013) · The Journal of Immunology · doi:10.4049/jimmunol.1202688 · Cited by 217
The immunology of tuberculosis: From bench to bedside
Dheda, K. U. J., Schwander, S., Zhu, B., van Zyl-Smit, R. N., & Zhang, Y. (2010) · Respirology · doi:10.1111/j.1440-1843.2010.01739.x · Cited by 212
Autophagy in innate and adaptive immunity
Deretic, V. P. (2005) · Trends in Immunology · doi:10.1016/j.it.2005.08.003 · Cited by 218
Autophagy as an immune defense mechanism
Deretic, V. P. (2006) · Current Opinion in Immunology · doi:10.1016/j.coi.2006.05.019 · Cited by 208
The Trojan horse: survival tactics of pathogenic mycobacteria in macrophages
Nguyen, L., & Pieters, J. (2005) · Trends in Cell Biology · doi:10.1016/j.tcb.2005.03.009 · Cited by 204
Coordinated loading of IRG resistance GTPases on to the Toxoplasma gondii parasitophorous vacuole
Khaminets, A., Hunn, J. P., Könen‐Waisman, S., Zhao, Y. O., Preukschat, D., Coers, J., Boyle, J. P., Ong, Y.-C., Boothroyd, J. C., Reichmann, G., et al. (2010) · Cellular Microbiology · doi:10.1111/j.1462-5822.2010.01443.x · Cited by 204
“Because Irgm1 has been shown to relocate to phagocytic cups and phagosomes during particle uptake (MacMicking et al., 2003; Martens et al., 2004) it has been proposed that this IRG protein can implement a direct cell-autonomous attack on phagocytosed pathogens (MacMicking et al., 2003).”
BackgroundThe Innate Immune Response to Mycobacterium tuberculosis Infection
Ravesloot-Chávez, M. M., Dis, E. S. V., & Stanley, S. A. (2021) · Annual Review of Immunology · doi:10.1146/annurev-immunol-093019-010426 · Cited by 213
Salgame, P. (2005) · Current Opinion in Immunology · doi:10.1016/j.coi.2005.06.006 · Cited by 209
Tim3 binding to galectin-9 stimulates antimicrobial immunity
Jayaraman, P., Sada‐Ovalle, I., Beladi, S., Anderson, A. C., Dardalhon, V., Hotta, C., Kuchroo, V. K., & Behar, S. M. (2010) · The Journal of Experimental Medicine · doi:10.1084/jem.20100687 · Cited by 201
“To definitively rule out the involvement of IFN- and iNOS in Tim3–Gal9–mediated Mtb killing, IFN-R/ and iNOS/ macrophages were infected with Mtb and treated with Tim3-Ig.”
BackgroundInfluentialMycobacterium tuberculosis Wears What It Eats
Russell, D. G., VanderVen, B. C., Lee, W., Abramovitch, R. B., Kim, M., Homolka, S., Niemann, S., & Rohde, K. H. (2010) · Cell Host & Microbe · doi:10.1016/j.chom.2010.06.002 · Cited by 198
“Activation of the host macrophage by either TLR agonists or IFN-γ leads to alterations in the Mtb-containing phagosome that impact negatively on the bacterium’s capacity to replicate and/or survive (MacMicking et al., 2003; Schaible et al., 1998; Via et al., 1998).”
BackgroundMcNab, F. W., Ewbank, J., Howes, A., Moreira-Teixeira, L., Մարտիրոսյան, Ա., Ghilardi, N., Saraiva, M., & O’Garra, A. (2014) · The Journal of Immunology · doi:10.4049/jimmunol.1401088 · Cited by 198
“cellular bacterial growth through induction of antimicrobial effectors such as iNOS (5, 6, 12, 14).”
BackgroundBaldwin, C. L., & Goenka, R. (2006) · Critical Reviews in Immunology · doi:10.1615/critrevimmunol.v26.i5.30 · Cited by 191
The macrophage marches on its phagosome: dynamic assays of phagosome function
Russell, D. G., VanderVen, B. C., Glennie, S. J., Mwandumba, H. C., & Heyderman, R. S. (2009) · Nature reviews. Immunology · doi:10.1038/nri2591 · Cited by 187
Kahnert, A., Seiler, P. J., Stein, M., Bandermann, S., Hahnke, K., Mollenkopf, H., & Kaufmann, S. H. E. (2006) · European Journal of Immunology · doi:10.1002/eji.200535496 · Cited by 190
NLRP4 Negatively Regulates Autophagic Processes through an Association with Beclin1
Jounai, N., Kobiyama, K., Shiina, M., Ogata, K., Ishii, K. J., & Takeshita, F. (2011) · The Journal of Immunology · doi:10.4049/jimmunol.1001654 · Cited by 190
Selective Killing of Nonreplicating Mycobacteria
Bryk, R., Gold, B., Venugopal, A., Singh, J., Samy, R. D., Pupek, K., Cao, H., Popescu, C., Gurney, M., Hotha, S., et al. (2008) · Cell Host & Microbe · doi:10.1016/j.chom.2008.02.003 · Cited by 183
“The following conditions are thought to exist in the Mtb-containing phagosome in immunocompetent hosts: a pH of 4.5 (MacMicking et al., 2003); NO diffusing from the cytosol and/or locally generated after acidification of its auto-oxidation product, nitrite (Nathan and Ehrt, 2004); lack of leucine…”
BackgroundMethodInfluentialTuberculosis and the art of macrophage manipulation
Upadhyay, S., Mittal, E., & Philips, J. A. (2018) · Pathogens and Disease · doi:10.1093/femspd/fty037 · Cited by 186
Bougnères, L., Helft, J., Tiwari, S., Vargas, P., Chang, B. H.-J., Chan, L., Campisi, L., Lauvau, G. S., Hugues, S., Kumar, P., et al. (2009) · Immunity · doi:10.1016/j.immuni.2009.06.022 · Cited by 179
“Previous studies have shown that the expression of Igtp is uniformly low in various cell types and further increased by IFN exposure (MacMicking et al., 2003; Taylor et al., 2000, 1996).”
BackgroundSelf-citationBagshaw, R. D., Mahuran, D. J., & Callahan, J. W. (2004) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m400128-mcp200 · Cited by 175
Mycobacterium tuberculosis-Specific CD8+ T Cells and Their Role in Immunity
Woodworth, J. S., & Behar, S. M. (2006) · Critical Reviews in Immunology · doi:10.1615/critrevimmunol.v26.i4.30 · Cited by 180
Autophagy and pattern recognition receptors in innate immunity
Delgado, M. A., Singh, S., Haro, S. A. D., Master, S. S., Ponpuak, M., Dinkins, C., Ornatowski, W., Vergne, I., & Deretic, V. P. (2008) · Immunological Reviews · doi:10.1111/j.1600-065x.2008.00725.x · Cited by 175
Interferon- γ and infectious diseases: Lessons and prospects
Casanova, J., MacMicking, J. D., & Nathan, C. (2024) · Science · doi:10.1126/science.adl2016 · Cited by 184
Self-citationIFN-γ Elicits Macrophage Autophagy via the p38 MAPK Signaling Pathway
Matsuzawa, T., Kim, B.-H., Shenoy, A. R., Kamitani, S., Miyake, M., & MacMicking, J. D. (2012) · The Journal of Immunology · doi:10.4049/jimmunol.1102041 · Cited by 181
Self-citation
Metadata
- Authors
- MacMicking, J. D., Taylor, G. A., & McKinney, J. D.
- Affiliations
- Duke University (US)
- Corresponding author
- MacMicking, John D.
- Venue
- Science
- Published
- 2003-10-24
- Volume
- 302
- Issue
- 5645
- Pages
- 654-659
- ISSN
- 0036-8075 (ISSN-L)
- 1095-9203
- OpenAlex
- W1989883893
- Cited by
- 685
- References
- 31
- Citations by year
- 2026: 11 · 2025: 15 · 2024: 16 · 2023: 21 · 2022: 15 · 2021: 27 · 2020: 23 · 2019: 26 · 2018: 27 · 2017: 21 · 2016: 21 · 2015: 34 · 2014: 31 · 2013: 44 · 2012: 44
- FWCI
- 19.81
- Type
- journal article
- Language
- en
- Open access
- green
- infoscience.epfl.ch
- Locations
- Science (publishedVersion)
- PubMed (publishedVersion)
- Infoscience (Ecole Polytechnique Fédérale de Lausanne) (submittedVersion)
- Infoscience (Ecole Polytechnique Fédérale de Lausanne) (submittedVersion, cc-by-nc-nd)
- Funders
- U.S. Public Health Service (R01 A1051702)
- Topics
- Health Sciences › Medicine › Infectious Diseases › Tuberculosis Research and Epidemiology
- Life Sciences › Immunology and Microbiology › Immunology › Immune responses and vaccinations
- Life Sciences › Immunology and Microbiology › Immunology › Immune Response and Inflammation
- Keywords
- tuberculosis, interferon-gamma, Mycobacterium tuberculosis, nitric oxide synthase 2, intracellular pathogen clearance, vacuolar trafficking, host immunity
- MeSH terms
- Animals, Cells, Cultured, Disease Susceptibility, Female, Hydrogen-Ion Concentration, Immunity, Innate, Interferon-gamma, Macrophage Activation, Macrophages, Male, Mice, Inbred C57BL, Mutation, Mycobacterium tuberculosis, Phagosomes, Tuberculosis, Signal Transduction, Macrophages, Alveolar, Nitric Oxide Synthase, GTP-Binding Proteins, Computational Biology, Reverse Transcriptase Polymerase Chain Reaction, Oligonucleotide Array Sequence Analysis, GTP Phosphohydrolases, Mice, Nitric Oxide Synthase Type II
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