Type I IFN signaling triggers immunopathology in tuberculosis-susceptible mice by modulating lung phagocyte dynamics

European Journal of Immunology

Volumn 44, Issue 8, 2014, Pages 2380-2393

  Dorhoi, Anca ^a   Yeremeev, Vladimir ^a,b   Nouailles, Geraldine ^a,c   Weiner, January ^a   Jörg, Sabine ^a   Heinemann, Ellen ^a   Oberbeck Müller, Dagmar ^a   Knaul, Julia K ^a   Vogelzang, Alexis ^a   Reece, Stephen T ^a   Hahnke, Karin ^a   Mollenkopf, Hans Joachim ^a   Brinkmann, Volker ^a   Kaufmann, Stefan H E ^a  

^a MAX PLANCK INSTITUTE FOR INFECTION BIOLOGY   (Germany)

^b CENTRAL TUBERCULOSIS RESEARCH INSTITUTE   (Russian Federation)

^c CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

Alveolar macrophages; Inflammation; Interferon type I; Mycobacterium tuberculosis; Neutrophils

Indexed keywords

CXCL1 CHEMOKINE; EPITHELIAL DERIVED NEUTROPHIL ACTIVATING FACTOR 78; INTERFERON;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL MIGRATION; CHRONIC INFLAMMATION; CONTROLLED STUDY; DYNAMICS; IMMUNOMODULATION; IMMUNOPATHOLOGY; LUNG TUBERCULOSIS; MONOCYTE; MOUSE; NEUTROPHIL; NONHUMAN; NUCLEOTIDE SEQUENCE; PHAGOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; T LYMPHOCYTE;

ALVEOLAR MACROPHAGES; INFLAMMATION; INTERFERON TYPE I; MYCOBACTERIUM TUBERCULOSIS; NEUTROPHILS;

ANIMALS; CELLS, CULTURED; CHEMOKINE CXCL1; CHEMOKINE CXCL5; INFLAMMATION; INTERFERON TYPE I; LUNG; MICE; MICE, INBRED C57BL; MONOCYTES; MYCOBACTERIUM TUBERCULOSIS; NEUTROPHILS; PHAGOCYTES; PULMONARY ALVEOLI; RECEPTOR, INTERFERON ALPHA-BETA; SIGNAL TRANSDUCTION; T-LYMPHOCYTES; TUBERCULOSIS, PULMONARY;

EID: 84906088413     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201344219     Document Type: Article

References (49)

1. WHO. Global Tuberculosis Report 2013. WHO Press, Geneva, 2013.
2. Berry, M. P., Graham, C. M., McNab, F. W., Xu, Z., Bloch, S. A., Oni, T., Wilkinson, K. A. et al., An interferon-inducible neutrophil-driven blood transcriptional signature in human tuberculosis. Nature 2010. 466: 973-977.
3. Maertzdorf, J., Repsilber, D., Parida, S. K., Stanley, K., Roberts, T., Black, G., Walzl, G. et al., Human gene expression profiles of susceptibility and resistance in tuberculosis. Genes Immun. 2011. 12: 15-22.
4. Ottenhoff, T. H., Dass, R. H., Yang, N., Zhang, M. M., Wong, H. E., Sahiratmadja, E., Khor, C. C. et al., Genome-wide expression profiling identifies type 1 interferon response pathways in active tuberculosis. PLoS One 2012. 7: e45839.
5. Stetson, D. B. and Medzhitov, R., Type I interferons in host defense. Immunity 2006. 25: 373-381.
6. Platanias, L. C., Mechanisms of type-I- and type-II-interferon-mediated signalling. Nat. Rev. Immunol. 2005. 5: 375-386.
7. Trinchieri, G., Type I interferon: friend or foe? J. Exp. Med. 2010. 207: 2053-2063.
8. Manca, C., Tsenova, L., Bergtold, A., Freeman, S., Tovey, M., Musser, J. M., Barry, C. E., III et al., Virulence of a Mycobacterium tuberculosis clinical isolate in mice is determined by failure to induce Th1 type immunity and is associated with induction of IFN-alpha /beta. Proc. Natl. Acad. Sci. USA 2001. 98: 5752-5757.
9. Manca, C., Tsenova, L., Freeman, S., Barczak, A. K., Tovey, M., Murray, P. J., Barry, C. et al., Hypervirulent M. tuberculosis W/Beijing strains upregulate type I IFNs and increase expression of negative regulators of the Jak-Stat pathway. J. Interferon. Cytokine Res. 2005. 25: 694-701.
10. Antonelli, L. R., Gigliotti, R. A., Goncalves, R., Roffe, E., Cheever, A. W., Bafica, A., Salazar, A. M. et al., Intranasal Poly-IC treatment exacerbates tuberculosis in mice through the pulmonary recruitment of a pathogen-permissive monocyte/macrophage population. J. Clin. Invest. 2010. 120: 1674-1682.
11. Cooper, A. M., Pearl, J. E., Brooks, J. V., Ehlers, S. and Orme, I. M., Expression of the nitric oxide synthase 2 gene is not essential for early control of Mycobacterium tuberculosis in the murine lung. Infect. Immun. 2000. 68: 6879-6882.
12. Stanley, S. A., Johndrow, J. E., Manzanillo, P. and 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.
13. Turner, J. and Orme, I. M., The expression of early resistance to an infection with Mycobacterium tuberculosis by old mice is dependent on IFN type II (IFN-gamma) but not IFN type I. Mech. Ageing Dev. 2004. 125: 1-9.
14. Teles, R. M., Graeber, T. G., Krutzik, S. R., Montoya, D., Schenk, M., Lee, D. J., Komisopoulou, E. et al., Type I interferon suppresses type II interferon-triggered human anti-mycobacterial responses. Science 2013. 339: 1448-1453.
15. Mayer-Barber, K. D., Andrade, B. B., Barber, D. L., Hieny, S., Feng, C. G., Caspar, P., Oland, S. et al., Innate and adaptive interferons suppress IL-1alpha and IL-1beta production by distinct pulmonary myeloid subsets during Mycobacterium tuberculosis infection. Immunity 2011. 35: 1023-1034.
16. Desvignes, L., Wolf, A. J. and Ernst, J. D., Dynamic roles of type I and type II IFNs in early infection with Mycobacterium tuberculosis. J. Immunol. 2012. 188: 6205-6215.
17. Flynn, J. L. and Chan, J., Immunology of tuberculosis. Annu. Rev. Immunol. 2001. 19: 93-129.
18. Eden, E., Navon, R., Steinfeld, I., Lipson, D. and Yakhini, Z., GOrilla: a tool for discovery and visualization of enriched GO terms in ranked gene lists. BMC Bioinformatics 2009. 10: 48.
19. Jeyaseelan, S., Manzer, R., Young, S. K., Yamamoto, M., Akira, S., Mason, R. J. and Worthen, G. S., Induction of CXCL5 during inflammation in the rodent lung involves activation of alveolar epithelium. Am. J. Respir. Cell Mol. Biol. 2005. 32: 531-539.
20. Balamayooran, G., Batra, S., Fessler, M. B., Happel, K. I. and Jeyaseelan, S., Mechanisms of neutrophil accumulation in the lungs against bacteria. Am. J. Respir. Cell Mol. Biol. 2010. 43: 5-16.
21. Yang, D., Wei, F., Tewary, P., Howard, O. M. and Oppenheim, J. J., Alarmin-induced cell migration. Eur. J. Immunol. 2013. 43: 1412-1418.
22. Simpson, E. M., Linder, C. C., Sargent, E. E., Davisson, M. T., Mobraaten, L. E. and Sharp, J. J., Genetic variation among 129 substrains and its importance for targeted mutagenesis in mice. Nat. Genet. 1997. 16: 19-27.
23. Medina, E. and North, R. J., Resistance ranking of some common inbred mouse strains to Mycobacterium tuberculosis and relationship to major histocompatibility complex haplotype and Nramp1 genotype. Immunology 1998. 93: 270-274.
24. Muller, U., Steinhoff, U., Reis, L. F., Hemmi, S., Pavlovic, J., Zinkernagel, R. M. and Aguet, M., Functional role of type I and type II interferons in antiviral defense. Science 1994. 264: 1918-1921.
25. Dunn, G. P., Bruce, A. T., Sheehan, K. C., Shankaran, V., Uppaluri, R., Bui, J. D., Diamond, M. S. et al., A critical function for type I interferons in cancer immunoediting. Nat. Immunol. 2005. 6: 722-729.
26. Shahangian, A., Chow, E. K., Tian, X., Kang, J. R., Ghaffari, A., Liu, S. Y., Belperio, J. A. et al., Type I IFNs mediate development of postinfluenza bacterial pneumonia in mice. J. Clin. Invest. 2009. 119: 1910-1920.
27. Weighardt, H., Kaiser-Moore, S., Schlautkotter, S., Rossmann-Bloeck, T., Schleicher, U., Bogdan, C. and Holzmann, B., Type I IFN modulates host defense and late hyperinflammation in septic peritonitis. J. Immunol. 2006. 177: 5623-5630.
28. Qiu, H., Fan, Y., Joyee, A. G., Wang, S., Han, X., Bai, H., Jiao, L. et al., Type I IFNs enhance susceptibility to Chlamydia muridarum lung infection by enhancing apoptosis of local macrophages. J. Immunol. 2008. 181: 2092-2102.
29. Majer, O., Bourgeois, C., Zwolanek, F., Lassnig, C., Kerjaschki, D., Mack, M., Muller, M. et al., Type I interferons promote fatal immunopathology by regulating inflammatory monocytes and neutrophils during Candida infections. PLoS Pathog. 2012. 8: e1002811.
30. Lee, P. Y., Li, Y., Kumagai, Y., Xu, Y., Weinstein, J. S., Kellner, E. S., Nacionales, D. C. et al., Type I interferon modulates monocyte recruitment and maturation in chronic inflammation. Am. J. Pathol. 2009. 175: 2023-2033.
31. Nouailles, G., Dorhoi, A., Koch, M., Zerrahn, J., Weiner, J., III, Fae, K. C., Arrey, F. et al., CXCL5/LIX-secreting pulmonary epithelial cells drive destructive neutrophilic inflammation in tuberculosis. J. Clin. Invest. 2014. 124: 1268-1282.
32. Robinson, N., McComb, S., Mulligan, R., Dudani, R., Krishnan, L. and Sad, S., Type I interferon induces necroptosis in macrophages during infection with Salmonella enterica serovar Typhimurium. Nat. Immunol. 2012. 13: 954-962.
33. Roca, F. J. and Ramakrishnan, L., TNF dually mediates resistance and susceptibility to mycobacteria via mitochondrial reactive oxygen species. Cell 2013. 153: 521-534.
34. Dorhoi, A., Desel, C., Yeremeev, V., Pradl, L., Brinkmann, V., Mollenkopf, H. J., Hanke, K. et al., The adaptor molecule CARD9 is essential for tuberculosis control. J. Exp. Med. 2010. 207: 777-792.
35. Dorhoi, A., Iannaccone, M., Farinacci, M., Fae, K. C., Schreiber, J., Moura-Alves, P., Nouailles, G. et al., MicroRNA-223 controls susceptibility to tuberculosis by regulating lung neutrophil recruitment. J. Clin. Invest. 2013. 123: 4836-4848.
36. Abadie, V., Badell, E., Douillard, P., Ensergueix, D., Leenen, P. J., Tanguy, M., Fiette, L. et al., Neutrophils rapidly migrate via lymphatics after Mycobacterium bovis BCG intradermal vaccination and shuttle live bacilli to the draining lymph nodes. Blood 2005. 106: 1843-1850.
37. Telesca, C., Angelico, M., Piccolo, P., Nosotti, L., Morrone, A., Longhi, C., Carbone, M. et al., Interferon-alpha treatment of hepatitis D induces tuberculosis exacerbation in an immigrant. J. Infect. 2007. 54: e223-e226.
38. Babudieri, S., Soddu, A., Murino, M., Molicotti, P., Muredda, A. A., Madeddu, G., Fois, A. G. et al., Tuberculosis screening before anti-hepatitis C virus therapy in prisons. Emerg. Infect. Dis. 2012. 18: 689-691.
39. Belkahla, N., Kchir, H., Maamouri, N., Ouerghi, H., Hariz, F. B., Chouaib, S., Chaabouni, H. et al., Reactivation of tuberculosis during dual therapy with pegylated interferon and ribavirin for chronic hepatitis C. Rev. Med. Interne 2010. 31: e1-e3.
40. Giosue, S., Casarini, M., Alemanno, L., Galluccio, G., Mattia, P., Pedicelli, G., Rebek, L. et al., Effects of aerosolized interferon-alpha in patients with pulmonary tuberculosis. Am. J. Respir. Crit. Care Med. 1998. 158: 1156-1162.
41. Palmero, D., Eiguchi, K., Rendo, P., Castro, Z. L., Abbate, E. and Gonzalez Montaner, L. J., Phase II trial of recombinant interferon-alpha2b in patients with advanced intractable multidrug-resistant pulmonary tuberculosis: long-term follow-up. Int. J. Tuberc. Lung Dis. 1999. 3: 214-218.
42. Zhukova, E. M., Krasnov, V. A., Petrenko, T. I. and Romanov, V. V., Interferon alpha-2b in the complex therapy of patients with pulmonary tuberculosis concurrent with bronchoobstructive syndrome. Probl. Tuberk. Bolezn. Legk. 2009. 12: 58-61.
43. Tsai, M. C., Lin, M. C. and Hung, C. H., Successful antiviral and antituberculosis treatment with pegylated interferon-alfa and ribavirin in a chronic hepatitis C patient with pulmonary tuberculosis. J. Formos. Med. Assoc. 2009. 108: 746-750.
44. Fejer, G., Drechsel, L., Liese, J., Schleicher, U., Ruzsics, Z., Imelli, N., Greber, U. F. et al., Key role of splenic myeloid DCs in the IFN-alphabeta response to adenoviruses in vivo. PLoS Pathog. 2008. 4: e1000208.
45. Kremer, L., Baulard, A., Estaquier, J., Poulain-Godefroy, O. and Locht, C., Green fluorescent protein as a new expression marker in mycobacteria. Mol. Microbiol. 1995. 17: 913-922.
46. Dorhoi, A., Nouailles, G., Jorg, S., Hagens, K., Heinemann, E., Pradl, L., Oberbeck-Muller, D. et al., Activation of the NLRP3 inflammasome by Mycobacterium tuberculosis is uncoupled from susceptibility to active tuberculosis. Eur. J. Immunol. 2012. 42: 374-384.
47. Smyth, G. K., Limma: linear models for microarray data. In Gentleman, R., Carey, V., Dudoit, S., Irizarry, R. and Huber, W. (Eds.), Bioinformatics and computational biology solutions using R and bioconductor. Springer, New York 2005, pp. 397-420.
48. Benjamini, Y. and Hochberg, Y., Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. Roy. Stat. Soc. 1995. 57: 289-300.
49. Tarca, A. L., Draghici, S., Khatri, P., Hassan, S. S., Mittal, P., Kim, J. S., Kim, C. J. et al., A novel signaling pathway impact analysis. Bioinformatics 2009. 25: 75-82.