Microparticles released from Mycobacterium tuberculosis-infected human macrophages contain increased levels of the type I interferon inducible proteins including ISG15

Proteomics

Volumn 15, Issue 17, 2015, Pages 3020-3029

  Hare, Nathan J ^a   Chan, Brian ^a   Chan, Edwina ^a   Kaufman, Kimberley L ^b   Britton, Warwick J ^a   Saunders, Bernadette M ^a,c  

^a UNIVERSITY OF SYDNEY   (Australia)

^b UNIVERSITY OF SYDNEY   (Australia)

^c UNIVERSITY OF TECHNOLOGY SYDNEY   (Australia)

Author keywords

Macrophage; Microbiology; Microparticle; Mycobacterium tuberculosis

Indexed keywords

PROTEIN IFIT1; PROTEIN IFIT2; PROTEIN IFIT3; PROTEIN ISG15; PROTEOME; REGULATOR PROTEIN; UNCLASSIFIED DRUG; CARRIER PROTEIN; CYTOKINE; IFIT1 PROTEIN, HUMAN; IFIT2 PROTEIN, HUMAN; IFIT3 PROTEIN, HUMAN; INTERFERON; ISG15 PROTEIN, HUMAN; PROTEIN; SIGNAL PEPTIDE; UBIQUITIN;

ANTIGEN PRESENTATION; ARTICLE; CELL MATURATION; ENDOSOME; GENE EXPRESSION; HUMAN; HUMAN CELL; LYSOSOME; MACROPHAGE; MEMBRANE MICROPARTICLE; MYCOBACTERIUM TUBERCULOSIS; NUCLEOSOME; PRIORITY JOURNAL; TUBERCULOSIS; CELL LINE; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; HOST PATHOGEN INTERACTION; METABOLISM; MICROBIOLOGY; MONOCYTE; PATHOGENICITY; TANDEM MASS SPECTROMETRY;

CARRIER PROTEINS; CELL LINE; CELL-DERIVED MICROPARTICLES; CYTOKINES; GENE EXPRESSION REGULATION; HOST-PATHOGEN INTERACTIONS; HUMANS; INTERFERON TYPE I; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MACROPHAGES; MONOCYTES; MYCOBACTERIUM TUBERCULOSIS; PROTEINS; TANDEM MASS SPECTROMETRY; TUBERCULOSIS; UBIQUITINS;

EID: 84940608300     PISSN: 16159853     EISSN: 16159861     Source Type: Journal    
DOI: 10.1002/pmic.201400610     Document Type: Article

References (42)

1. Raposo, G., Stoorvogel, W., Extracellular vesicles: exosomes, microvesicles, and friends. J. Cell. Biol. 2013, 200, 373-383.
2. Wolf, P., The nature and significance of platelet products in human plasma. Br. J. Haematol. 1967, 13, 269-288.
3. Ismail, N., Wang, Y., Dakhlallah, D., Moldovan, L. et al., Macrophage microvesicles induce macrophage differentiation and miR-223 transfer. Blood 2013, 121, 984-995.
4. Skog, J., Wurdinger, T., vanRijn, S., Meijer, D. H. et al., Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat. Cell Biol. 2008, 10, 1470-1476.
5. Al-Nedawi, K., Meehan, B., Micallef, J., Lhotak, V. et al., Intercellular transfer of the oncogenic receptor EGFRvIII by microvesicles derived from tumour cells. Nat. Cell Biol. 2008, 10, 619-624.
6. Pilzer, D., Gasser, O., Moskovich, O., Schifferli, J. A., Fishelson, Z., Emission of membrane vesicles: roles in complement resistance, immunity and cancer. Springer Semin. Immunopathol. 2005, 27, 375-387.
7. Walters, S. B., Kieckbusch, J., Nagalingam, G., Swain, A. et al., Microparticles from mycobacteria-infected macrophages promote inflammation and cellular migration. J. Immunol. 2013, 190, 669-677.
8. Global Tuberculosis Report 2013, World Health Organisation, Switzerland 2013.
9. Gobom, J., Nordhoff, E., Mirgorodskaya, E., Ekman, R., Roepstorff, P., Sample purification and preparation technique based on nano-scale reversed-phase columns for the sensitive analysis of complex peptide mixtures by matrix-assisted laser desorption/ionization mass spectrometry. J. Mass Spectrom. 1999, 34, 105-116.
10. Deshpande, N. P., Kaakoush, N. O., Mitchell, H., Janitz, K. et al., Sequencing and validation of the genome of a Campylobacter concisus reveals intra-species diversity. PLoS One 2011, 6, e22170.
11. Ashburner, M., Ball, C. A., Blake, J. A., Botstein, D. et al., Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat. Genet. 2000, 25, 25-29.
12. Pham, T. V., Jimenez, C. R., An accurate paired sample test for count data. Bioinformatics 2012, 28, i596-i602.
13. Ogata, H., Goto, S., Sato, K., Fujibuchi, W. et al., KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Res. 1999, 27, 29-34.
14. Franceschini, A., Szklarczyk, D., Frankild, S., Kuhn, M. et al., STRING v9.1: protein-protein interaction networks, with increased coverage and integration. Nucleic Acids Res. 2013, 41, D808-D815.
15. Kalra, H., Simpson, R. J., Ji, H., Aikawa, E. et al., Vesiclepedia: a compendium for extracellular vesicles with continuous community annotation. PLoS Biol. 2012, 10, e1001450.
16. Mathivanan, S., Fahner, C. J., Reid, G. E., Simpson, R. J. et al., ExoCarta 2012: database of exosomal proteins, RNA and lipids. Nucleic Acids Res. 2012, 40, D1241-D1244.
17. Via, L. E., Deretic, D., Ulmer, R. J., Hibler, N. S. et al., Arrest of mycobacterial phagosome maturation is caused by a block in vesicle fusion between stages controlled by rab5 and rab7. J. Biol. Chem. 1997, 272, 13326-13331.
18. Kyei, G. B., Vergne, I., Chua, J., Roberts, E. et al., Rab14 is critical for maintenance of Mycobacterium tuberculosis phagosome maturation arrest. EMBO J. 2006, 25, 5250-5259.
19. Berry, M. P., Graham, C. M., McNab, F. W., Xu, Z. et al., An interferon-inducible neutrophil-driven blood transcriptional signature in human tuberculosis. Nature 2010, 466, 973-977.
20. Bloom, C. I., Graham, C. M., Berry, M. P., Rozakeas, F. et al., Transcriptional blood signatures distinguish pulmonary tuberculosis, pulmonary sarcoidosis, pneumonias and lung cancers. PLoS One 2013, 8, e70630.
21. Ottenhoff, T. H., Dass, R. H., Yang, N., Zhang, M. M. et al., Genome-wide expression profiling identifies type 1 interferon response pathways in active tuberculosis. PLoS One 2012, 7, e45839.
22. Bogunovic, D., Byun, M., Durfee, L. A., Abhyankar, A. et al., Mycobacterial disease and impaired IFN-gamma immunity in humans with inherited ISG15 deficiency. Science 2012, 337, 1684-1688.
23. Knight, E., Jr., Cordova, B., IFN-induced 15-kDa protein is released from human lymphocytes and monocytes. J. Immunol. 1991, 146, 2280-2284.
24. D'Cunha, J., Knight, E., Jr., Haas, A. L., Truitt, R. L., Borden, E. C., Immunoregulatory properties of ISG15, an interferon-induced cytokine. Proc. Natl. Acad. Sci. USA 1996, 93, 211-215.
25. Zhang, X., Bogunovic, D., Payelle-Brogard, B., Francois-Newton, V. et al., Human intracellular ISG15 prevents interferon-alpha/beta over-amplification and auto-inflammation. Nature 2015, 517, 89-93.
26. Jeon, Y. J., Yoo, H. M., Chung, C. H., ISG15 and immune diseases. Biochim. Biophys. Acta 2010, 1802, 485-496.
27. Zhao, C., Denison, C., Huibregtse, J. M., Gygi, S., Krug, R. M., Human ISG15 conjugation targets both IFN-induced and constitutively expressed proteins functioning in diverse cellular pathways. Proc. Natl. Acad. Sci. USA 2005, 102, 10200-10205.
28. Giannakopoulos, N. V., Luo, J. K., Papov, V., Zou, W. et al., Proteomic identification of proteins conjugated to ISG15 in mouse and human cells. Biochem. Biophys. Res. Commun. 2005, 336, 496-506.
29. Malakhov, M. P., Kim, K. I., Malakhova, O. A., Jacobs, B. S. et al., High-throughput immunoblotting. Ubiquitin-like protein ISG15 modifies key regulators of signal transduction. J. Biol. Chem. 2003, 278, 16608-16613.
30. Lenschow, D. J., Lai, C., Frias-Staheli, N., Giannakopoulos, N. V. et al., IFN-stimulated gene 15 functions as a critical antiviral molecule against influenza, herpes, and Sindbis viruses. Proc. Natl. Acad. Sci. USA 2007, 104, 1371-1376.
31. Yuan, W., Krug, R. M., Influenza B virus NS1 protein inhibits conjugation of the interferon (IFN)-induced ubiquitin-like ISG15 protein. EMBO J. 2001, 20, 362-371.
32. Dauphinee, S. M., Richer, E., Eva, M. M., McIntosh, F. et al., Contribution of increased ISG15, ISGylation and deregulated type I IFN signaling in Usp18 mutant mice during the course of bacterial infections. Genes Immun. 2014, 15, 282-292.
33. Diamond, M. S., Farzan, M., The broad-spectrum antiviral functions of IFIT and IFITM proteins. Nat. Rev. Immunol. 2013, 13, 46-57.
34. Terenzi, F., White, C., Pal, S., Williams, B. R., Sen, G. C., Tissue-specific and inducer-specific differential induction of ISG56 and ISG54 in mice. J. Virol. 2007, 81, 8656-8665.
35. Flynn, J. L., Chan, J., Triebold, K. J., Dalton, D. K. et al., An essential role for interferon gamma in resistance to Mycobacterium tuberculosis infection. J. Exp. Med. 1993, 178, 2249-2254.
36. Jouanguy, E., Lamhamedi-Cherradi, S., Lammas, D., Dorman, S. E. et al., A human IFNGR1 small deletion hotspot associated with dominant susceptibility to mycobacterial infection. Nat. Genet. 1999, 21, 370-378.
37. Taki, S., Type I interferons and autoimmunity: lessons from the clinic and from IRF-2-deficient mice. Cytokine Growth Factor Rev. 2002, 13, 379-391.
38. Rayamajhi, M., Humann, J., Kearney, S., Hill, K. K., Lenz, L. L., Antagonistic crosstalk between type I and II interferons and increased host susceptibility to bacterial infections. Virulence 2010, 1, 418-422.
39. Stanley, S. A., Johndrow, J. E., Manzanillo, P., Cox, J. S., The Type I IFN response to infection with Mycobacterium tuberculosis requires ESX-1-mediated secretion and contributes to pathogenesis. J. Immunol. 2007, 178, 3143-3152.
40. Zerial, M., McBride, H., Rab proteins as membrane organizers. Nat. Rev. Mol. Cell Biol. 2001, 2, 107-117.
41. Marquet, J., Lasoudris, F., Cousin, C., Puiffe, M. L. et al., Dichotomy between factors inducing the immunosuppressive enzyme IL-4-induced gene 1 (IL4I1) in B lymphocytes and mononuclear phagocytes. Eur. J. Immunol. 2010, 40, 2557-2568.
42. Puiffe, M. L., Lachaise, I., Molinier-Frenkel, V., Castellano, F., et al., Antibacterial properties of the mammalian L-amino acid oxidase IL4I1. PLoS One 2013, 8, e54589.