Mycobacterium tuberculosis Decreases Human Macrophage IFN-γ responsiveness through miR-132 and miR-26a

Journal of Immunology

Volumn 193, Issue 9, 2014, Pages 4537-4547

  Ni, Bin ^a   Rajaram, Murugesan V S ^a   Lafuse, William P ^a   Landes, Michelle B ^a   Schlesinger, Larry S ^a  

^a OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

E1A ASSOCIATED P300 PROTEIN; FC RECEPTOR; FC RECEPTOR I; GAMMA INTERFERON; HLA DR ANTIGEN; MICRORNA 132; MICRORNA 26A; UNCLASSIFIED DRUG; 3' UNTRANSLATED REGION; HISTONE ACETYLTRANSFERASE PCAF; MESSENGER RNA; MICRORNA; MIRN132 MICRORNA, HUMAN; MIRN26A MICRORNA, HUMAN;

3' UNTRANSLATED REGION; ARTICLE; CONTROLLED STUDY; GENE EXPRESSION; HUMAN; HUMAN CELL; MACROPHAGE; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSCRIPTION REGULATION; TRANSLATION REGULATION; UPREGULATION; BINDING SITE; CELL LINE; DRUG EFFECTS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; METABOLISM; REPRODUCIBILITY; RNA INTERFERENCE; TUBERCULOSIS;

3' UNTRANSLATED REGIONS; BINDING SITES; CELL LINE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HLA-DR ANTIGENS; HUMANS; INTERFERON-GAMMA; MACROPHAGES; MICRORNAS; MYCOBACTERIUM TUBERCULOSIS; P300-CBP TRANSCRIPTION FACTORS; RECEPTORS, IGG; REPRODUCIBILITY OF RESULTS; RNA INTERFERENCE; RNA, MESSENGER; TUBERCULOSIS;

EID: 84908120270     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1400124     Document Type: Article

References (37)

1. Plüddemann, A., S. Mukhopadhyay, and S. Gordon. 2011. Innate immunity to intracellular pathogens: macrophage receptors and responses to microbial entry. Immunol. Rev. 240: 11-24.
2. Fenton, M. J. 1998. Macrophages and tuberculosis. Curr. Opin. Hematol. 5: 72-78.
3. Schroder, K., P. J. Hertzog, T. Ravasi, and D. A. Hume. 2004. Interferon-gamma: an overview of signals, mechanisms and functions. J. Leukoc. Biol. 75: 163-189.
4. Platanias, L. C. 2005. Mechanisms of type-I- and type-II-interferon-mediated signalling. Nat. Rev. Immunol. 5: 375-386.
5. Lagos, D., G. Pollara, S. Henderson, F. Gratrix, M. Fabani, R. S. Milne, F. Gotch, and C. Boshoff. 2010. miR-132 regulates antiviral innate immunity through suppression of the p300 transcriptional co-activator. Nat. Cell Biol. 12: 513-519.
6. Bouhet, S., V. Lafont, E. Billard, A. Gross, and J. Dornand. 2009. The IFNgamma-induced STAT1-CBP/P300 association, required for a normal response to the cytokine, is disrupted in Brucella-infected macrophages. Microb. Pathog. 46: 88-97.
7. Darieva, Z., E. B. Lasunskaia, M. N. Campos, T. L. Kipnis, and W. D. Da Silva. 2004. Activation of phosphatidylinositol 3-kinase and c-Jun-N-terminal kinase cascades enhances NF-kappaB-dependent gene transcription in BCG-stimulated macrophages through promotion of p65/p300 binding. J. Leukoc. Biol. 75: 689-697.
8. Sen, N., M. R. Hara, M. D. Kornberg, M. B. Cascio, B. I. Bae, N. Shahani, B. Thomas, T. M. Dawson, V. L. Dawson, S. H. Snyder, and A. Sawa. 2008. Nitric oxide-induced nuclear GAPDH activates p300/CBP and mediates apoptosis. Nat. Cell Biol. 10: 866-873.
9. Ting, L.-M., A. C. Kim, A. Cattamanchi, and J. D. Ernst. 1999. Mycobacterium tuberculosis inhibits IFN-γ transcriptional responses without inhibiting activation of STAT1. J. Immunol. 163: 3898-3906.
10. Flynn, J. L., J. Chan, K. J. Triebold, D. K. Dalton, T. A. Stewart, and B. R. Bloom. 1993. An essential role for interferon gamma in resistance to Mycobacterium tuberculosis infection. J. Exp. Med. 178: 2249-2254.
11. Jouanguy, E., F. Altare, S. Lamhamedi-Cherradi, and J. L. Casanova. 1997. Infections in IFNGR-1-deficient children. J. Interferon Cytokine Res. 17: 583-587.
12. Newport, M. J., C. M. Huxley, S. Huston, C. M. Hawrylowicz, B. A. Oostra, R. Williamson, and M. Levin. 1996. A mutation in the interferon-gamma-receptor gene and susceptibility to mycobacterial infection. N. Engl. J. Med. 335: 1941-1949.
13. Dorman, S. E., and S. M. Holland. 1998. Mutation in the signal-transducing chain of the interferon-gamma receptor and susceptibility to mycobacterial infection. J. Clin. Invest. 101: 2364-2369.
14. Ribera, E., I. Ocaña, J. M. Martinez-Vazquez, M. Rossell, T. Español, and A. Ruibal. 1988. High level of interferon gamma in tuberculous pleural effusion. Chest 93: 308-311.
15. Rook, G. A., J. Steele, M. Ainsworth, and B. R. Champion. 1986. Activation of macrophages to inhibit proliferation of Mycobacterium tuberculosis: comparison of the effects of recombinant gamma-interferon on human monocytes and mu-rine peritoneal macrophages. Immunology 59: 333-338.
16. Bartel, D. P. 2004. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116: 281-297.
17. Rajaram, M. V., B. Ni, J. D. Morris, M. N. Brooks, T. K. Carlson, B. Bakthavachalu, D. R. Schoenberg, J. B. Torrelles, and L. S. Schlesinger. 2011. Mycobacterium tuberculosis lipomannan blocks TNF biosynthesis by regulating macrophage MAPK-activated protein kinase 2 (MK2) and microRNA miR-125b. Proc. Natl. Acad. Sci. USA 108: 17408-17413.
18. Schlesinger, L. S., C. G. Bellinger-Kawahara, N. R. Payne, and M. A. Horwitz. 1990. Phagocytosis of Mycobacterium tuberculosis is mediated by human monocyte complement receptors and complement component C3. J. Immunol. 144: 2771-2780.
19. Horwitz, M. A., and S. C. Silverstein. 1980. Influence of the Escherichia coli capsule on complement fixation and on phagocytosis and killing by human phagocytes. J. Clin. Invest. 65: 82-94.
20. Schlesinger, L. S. 1993. Macrophage phagocytosis of virulent but not attenuated strains of Mycobacterium tuberculosis is mediated by mannose receptors in addition to complement receptors. J. Immunol. 150: 2920-2930.
21. Rajaram, M. V., M. N. Brooks, J. D. Morris, J. B. Torrelles, A. K. Azad, and L. S. Schlesinger. 2010. Mycobacterium tuberculosis activates human macrophage peroxisome proliferator-activated receptor gamma linking mannose receptor recognition to regulation of immune responses. J. Immunol. 185: 929-942.
22. Brooks, M. N., M. V. Rajaram, A. K. Azad, A. O. Amer, M. A. Valdivia-Arenas, J. H. Park, G. Núñez, and L. S. Schlesinger. 2011. NOD2 controls the nature of the inflammatory response and subsequent fate of Mycobacterium tuberculosis and M. bovis BCG in human macrophages. Cell. Microbiol. 13: 402-418.
23. Henning, L. N., A. K. Azad, K. V. Parsa, J. E. Crowther, S. Tridandapani, and L. S. Schlesinger. 2008. Pulmonary surfactant protein A regulates TLR expression and activity in human macrophages. J. Immunol. 180: 7847-7858.
24. Ganesan, L. P., G. Wei, R. A. Pengal, L. Moldovan, N. Moldovan, M. C. Ostrowski, and S. Tridandapani. 2004. The serine/threonine kinase Akt Promotes Fc gamma receptor-mediated phagocytosis in murine macrophages through the activation of p70S6 kinase. J. Biol. Chem. 279: 54416-54425.
25. Kang, P. B., A. K. Azad, J. B. Torrelles, T. M. Kaufman, A. Beharka, E. Tibesar, L. E. DesJardin, and L. S. Schlesinger. 2005. The human macrophage mannose receptor directs Mycobacterium tuberculosis lipoarabinomannan-mediated phagosome biogenesis. J. Exp. Med. 202: 987-999.
26. Ramana, C. V., M. P. Gil, R. D. Schreiber, and G. R. Stark. 2002. Stat1-dependent and -independent pathways in IFN-gamma-dependent signaling. Trends Immunol. 23: 96-101.
27. Hu, J., S. K. Roy, P. S. Shapiro, S. R. Rodig, S. P. Reddy, L. C. Platanias, R. D. Schreiber, and D. V. Kalvakolanu. 2001. ERK1 and ERK2 activate CCAAAT/enhancer-binding protein-beta-dependent gene transcription in response to interferon-gamma. J. Biol. Chem. 276: 287-297.
28. Eulalio, A., L. Schulte, and J. Vogel. 2012. The mammalian microRNA response to bacterial infections. RNA Biol. 9: 742-750.
29. Singh, P. K., A. V. Singh, and D. S. Chauhan. 2013. Current understanding on micro RNAs and its regulation in response to Mycobacterial infections. J. Biomed. Sci. 20: 14.
30. Dorhoi, A., M. Iannaccone, M. Farinacci, K. C. Faé, J. Schreiber, P. Moura-Alves, G. Nouailles, H. J. Mollenkopf, D. Oberbeck-Müller, S. Jörg, et al. 2013. MicroRNA-223 controls susceptibility to tuberculosis by regulating lung neu-trophil recruitment. J. Clin. Invest. 123: 4836-4848.
31. Ma, F., S. Xu, X. Liu, Q. Zhang, X. Xu, M. Liu, M. Hua, N. Li, H. Yao, and X. Cao. 2011. The microRNA miR-29 controls innate and adaptive immune responses to intracellular bacterial infection by targeting interferon-γ. Nat. Immunol. 12: 861-869.
32. ∗ with elevated expression in patients with pulmonary tuberculosis. Mol. Immunol. 48: 1084-1090.
33. Liu, Y., J. Jiang, X. Wang, F. Zhai, and X. Cheng. 2013. miR-582-5p is up-regulated in patients with active tuberculosis and inhibits apoptosis of monocytes by targeting FOXO1. PLoS ONE 8: e78381.
34. Kumar, R., P. Halder, S. K. Sahu, M. Kumar, M. Kumari, K. Jana, Z. Ghosh, P. Sharma, M. Kundu, and J. Basu. 2012. Identification of a novel role of ESAT-6-dependent miR-155 induction during infection of macrophages with Mycobacterium tuberculosis. Cell. Microbiol. 14: 1620-1631.
35. Wang, J., K. Yang, L. Zhou, Y. Minhaowu, Y. Wu, M. Zhu, X. Lai, T. Chen, L. Feng, M. Li, et al. 2013. MicroRNA-155 promotes autophagy to eliminate intracellular mycobacteria by targeting Rheb. PLoS Pathog. 9: e1003697.
36. Gagneux, S. 2012. Host-pathogen coevolution in human tuberculosis. Philos. Trans. R. Soc. Lond. B Biol. Sci. 367: 850-859.
37. Das, K., S. Saikolappan, and S. Dhandayuthapani. 2013. Differential expression of miRNAs by macrophages infected with virulent and avirulent Mycobacterium tuberculosis. Tuberculosis (Edinb.) 93(Suppl.): S47-S50.