Aerosolized Gamma Interferon (IFN-γ) Induces Expression of the Genes Encoding the IFN-γ-Inducible 10-Kilodalton Protein but Not Inducible Nitric Oxide Synthase in the Lung during Tuberculosis

Infection and Immunity

Volumn 72, Issue 3, 2004, Pages 1275-1283

  Raju, Bindu ^a   Hoshino, Yoshihiko ^a   Kuwabara, Kenichi ^a   Belitskaya, Ilana ^a   Prabhakar, Savita ^b   Canova, Antony ^b   Gold, Jeffrey A ^a   Condos, Rany ^a   Pine, Richard I ^b   Brown, Stuart ^a   Rom, William N ^a   Weiden, Michael D ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b PUBLIC HEALTH RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE; GAMMA INTERFERON INDUCIBLE PROTEIN 10; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERFERON INDUCING AGENT; ISONIAZID; MESSENGER RNA; RECOMBINANT GAMMA INTERFERON;

ADULT; AEROSOL; ARTICLE; CLINICAL ARTICLE; CLINICAL TRIAL; CONTROLLED CLINICAL TRIAL; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE ASSOCIATION; DOWNSTREAM PROCESSING; DRUG ADMINISTRATION ROUTE; ENZYME INDUCTION; FEMALE; GENE EXPRESSION REGULATION; GENE IDENTIFICATION; GENETIC ANALYSIS; HUMAN; IMMUNE RESPONSE; IN VITRO STUDY; INFECTION CONTROL; LUNG LAVAGE; LUNG TUBERCULOSIS; MALE; MYCOBACTERIUM TUBERCULOSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUANTITATIVE ASSAY; RANDOMIZED CONTROLLED TRIAL; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION;

ADULT; AEROSOLS; BASE SEQUENCE; BRONCHOALVEOLAR LAVAGE FLUID; CASE-CONTROL STUDIES; CHEMOKINES, CXC; DNA, COMPLEMENTARY; FEMALE; GENE EXPRESSION; HUMANS; INTERFERON-GAMMA, RECOMBINANT; LUNG; MALE; MIDDLE AGED; NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE TYPE II; RNA, MESSENGER; TUBERCULOSIS, PULMONARY;

EID: 10744232820     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.72.3.1275-1283.2004     Document Type: Article

References (59)

1. Aston, C., W. N. Rom, A. T. Talbot, and J. Reibman. 1998. Early inhibition of mycobacterial growth by human alveolar macrophages is not due to nitric oxide. Am. J. Respir. Crit. Care Med. 157:1943-1950.
2. Benyamini, Y., and Y. Hochberg. 1995. Controlling the false discovery rate: a powerful and practical approach to multiple testing. J. R. Stat. Soc. Ser. B 57:289-300.
3. Bertholet, S., E. Tzeng, E. Felley-Bosco, and J. Manel. 1999. Expression of the inducible NO synthase in human monocytic U937 cells allows high output nitric oxide production. J. Leukoc. Biol. 65:50-58.
4. Bonecini-Almeida, M. G., S. Chitale, I. Bontsikakis, J. Geng, H. Doo, S. He, and J. L. Ho. 1998. Induction of in vitro human macrophage anti-Mycobacterium tuberculosis activity: requirement for IFN-gamma and primed lymphocytes. J. Immunol. 160:4490-4499.
5. Chan, J., K. Tanaka, D. Carroll, J. Flynn, and B. R. Bloom. 1995. Effects of nitric oxide synthase inhibitors on murine infection with Mycobacterium tuberculosis. Infect. Immun. 63:736-740.
6. Chan, J., Y. Xing, R. S. Magliozzo, and B. R. Bloom. 1992. Killing of virulent Mycobacterium tuberculosis by reactive nitrogen intermediates produced by activated murine macrophages. J. Exp. Med. 175:1111-1122.
7. Chen, F., D. C. Kuhn, L. J. Gaydos, and L. M. Demers. 1996. Induction of nitric oxide and nitric oxide synthase mRNA by silica and lipopolysaccharide in PMA-primed THP-1 cells. APMIS 104:176-182.
8. Choi, H. S., P. R. Rai, H. W. Chu, C. Cool, and E. D. Chan. 2002. Analysis of nitric oxide synthase and nitrotyrosine expression in human pulmonary tuberculosis. Am. J. Respir. Crit. Care Med. 166:178-186.
9. Condos, R., B. Raju, A. Canova, B. Y. Zhao, M. Weiden, W. N. Rom, and R. Pine. 2003. Recombinant gamma interferon stimulates signal transduction and gene expression in alveolar macrophages in vitro and in tuberculosis patients. Infect. Immun. 71:2058-2064.
10. Condos, R., W. N. Rom, Y. M. Liu, and N. W. Schluger. 1998. Local immune responses correlate with presentation and outcome in tuberculosis. Am. J. Respir. Crit. Care Med. 157:729-735.
11. Condos, R., W. N. Rom, and N. W. Schluger. 1997. Treatment of multidrug-resistant pulmonary tuberculosis with interferon-gamma via aerosol. Lancet 349:1513-1515.
12. Cooper, A. M., D. K. Dalton, T. A. Stewart, J. P. Griffin, D. G. Russell, and I. M. Orme. 1993. Disseminated tuberculosis in interferon gamma gene-disrupted mice. J. Exp. Med. 178:2243-2247.
13. Dalton, D. K., S. Pitts-Meek, S. Keshav, I. S. Figari, A. Bradley, and T. A. Stewart. 1993. Multiple defects of immune cell function in mice with disrupted interferon-gamma genes. Science 259:1739-1742.
14. Denis, M. 1994. Human monocytes/macrophages: NO or no NO? J. Leukoc. Biol. 55:682-684.
15. Denis, M. 1991. Interferon-gamma-treated murine macrophages inhibit growth of tubercle bacilli via the generation of reactive nitrogen intermediates. Cell Immunol. 132:150-157.
16. Denis, M. 1991. Tumor necrosis factor and granulocyte macrophage-colony stimulating factor stimulate human macrophages to restrict growth of virulent Mycobacterium avium and to kill avirulent M. avium: killing effector mechanism depends on the generation of reactive nitrogen intermediates. J. Leukoc. Biol. 49:380-387.
17. 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. Investig. 101:2364-2369.
18. Dufour, J. H., M. Dziejman, M. T. Liu, J. H. Leung, T. E. Lane, and A. D. Luster. 2002. IFN-gamma-inducible protein 10 (IP-10; CXCL10)-deficient mice reveal a role for IP-10 in effector T cell generation and trafficking. J. Immunol. 168:3195-3204.
19. Dumarey, C. H., V. Labrousse, N. Rastogi, B. B. Vargaftig, and M. Bachelet. 1994. Selective Mycobacterium avium-induced production of nitric oxide by human monocyte-derived macrophages. J. Leukoc. Biol. 56:36-40.
20. Ehrt, S., D. Schnappinger, S. Bekiranov, J. Drenkow, S. Shi, T. R. Gingeras, T. Gaasterland, G. Schoolnik, and C. Nathan. 2001. Reprogramming of the macrophage transcriptome in response to interferon-gamma and Mycobacterium tuberculosis: signaling roles of nitric oxide synthase-2 and phagocyte oxidase. J. Exp. Med. 194:1123-1140.
21. Facchetti, F., W. Vermi, S. Fiorentini, M. Chilosi, A. Caruso, M. Duse, L. D. Notarangelo, and R. Badolato. 1999. Expression of inducible nitric oxide synthase in human granulomas and histiocytic reactions. Am. J. Pathol. 154:145-152.
22. Farber, J. M. 1997. Mig and IP-10: CXC chemokines that target lymphocytes. J. Leukoc. Biol. 61:246-257.
23. Farrar, J. D., J. D. Smith, T. L. Murphy, S. Leung, G. R. Stark, and K. M. Murphy. 2000. Selective loss of type 1 interferon-induced STAT4 activation caused by a minisatellite insertion in mouse Stat2. Nat. Immunol. 1:65-69.
24. Flesch, I. E., and S. H. Kaufmann. 1991. Mechanisms involved in mycobacterial growth inhibition by gamma interferon-activated bone marrow macrophages: role of reactive nitrogen intermediates. Infect. Immun. 59:3213-3218.
25. Flynn, J. L., and J. Chan. 2001. Immunology of tuberculosis. Annu. Rev. Immunol. 19:93-129.
26. 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.
27. Gangur, V., F. E. Simons, and K. T. Hayglass. 1998. Human IP-10 selectively promotes dominance of polyclonally activated and environmental antigen-driven IFN-gamma over IL-4 responses. FASEB J. 12:705-713.
28. Honda, Y., L. Rogers, K. Nakata, B. Y. Zhao, R. Pine, Y. Nakai, K. Kurosu, W. N. Rom, and M. Weiden. 1998. Type 1 interferon induces inhibitory 16-kD CCAAT/enhancer binding protein (C/EBP)beta, repressing the HIV-1 long terminal repeat in macrophages: pulmonary tuberculosis alters C/EBP expression, enhancing HIV-1 replication. J. Exp. Med. 188:1255-1265.
29. Hoshino, Y., K. Nakata, S. Hoshino, Y. Honda, D. B. Tse, T. Shioda, W. N. Rom, and M. Weiden. 2002. Maximal HIV-1 replication in alveolar macrophages during tuberculosis requires both lymphocyte contact and cytokines. J. Exp. Med. 195:495-505.
30. Jaffe, H. A., R. Buhl, A. Mastrangeli, K. J. Holroyd, C. Saltini, D. Czerski, H. S. Jaffe, S. Kramer, S. Sherwin, and R. G. Crystal. 1991. Organ specific cytokine therapy. Local activation of mononuclear phagocytes by delivery of an aerosol of recombinant interferon-gamma to the human lung. J. Clin. Investig. 88:297-302.
31. Jagannath, C., J. K. Actor, and R. L. Hunter, Jr. 1998. Induction of nitric oxide in human monocytes and monocyte cell lines by Mycobacterium tuberculosis. Nitric Oxide 2:174-186.
32. Kamijo, R., H. Harada, T. Matsuyama, M. Bosland, J. Gerecitano, D. Shapiro, J. Le, S. I. Koh, T. Kimura, S. J. Green, et al. 1994. Requirement for transcription factor IRF-1 in NO synthase induction in macrophages. Science 263:1612-1615.
33. Kamijo, R., J. Le, D. Shapiro, E. A. Havell, S. Huang, M. Aguet, M. Bosland, and J. Vilcek. 1993. Mice that lack the interferon-gamma receptor have profoundly altered responses to infection with Bacillus Calmette-Guerin and subsequent challenge with lipopolysaccharide. J. Exp. Med. 178:1435-1440.
34. Khan, I. A., J. A. MacLean, F. S. Lee, L. Casciotti, E. DeHaan, J. D. Schwartzman, and A. D. Luster. 2000. IP-10 is critical for effector T cell trafficking and host survival in Toxoplasma gondii infection. Immunity 12:483-494.
35. Law, K. F., J. Jagirdar, M. D. Weiden, M. Bodkin, and W. N. Rom. 1996. Tuberculosis in HIV-positive patients: cellular response and immune activation in the lung. Am. J. Respir. Crit. Care Med. 153:1377-1384.
36. MacMicking, J. D., R. J. North, R. LaCourse, J. S. Mudgett, S. K. Shah, and C. F. Nathan. 1997. Identification of nitric oxide synthase as a protective locus against tuberculosis. Proc. Natl. Acad. Sci. USA 94:5243-5248.
37. Majumder, S., L. Z. Zhou, P. Chaturvedi, G. Babcock, S. Aras, and R. M. Ransohoff. 1998. p48/STAT-1alpha-containing complexes play a predominant role in induction of IFN-gamma-inducible protein, 10 kDa (IP-10) by IFN-gamma alone or in synergy with TNF-alpha. J. Immunol. 161:4736-4744.
38. Moreira, A. L., L. Tsenova, P. J. Murray, S. Freeman, A. Bergtold, L. Chiriboga, and G. Kaplan. 2000. Aerosol infection of mice with recombinant BCG secreting murine IFN-gamma partially reconstitutes local protective immunity. Microb. Pathog. 29:175-185.
39. Murray, H. W., and R. F. Teitelbaum. 1992. L-arginine-dependent reactive nitrogen intermediates and the antimicrobial effect of activated human mononuclear phagocytes. J. Infect. Dis. 165:513-517.
40. Neville, L. F., G. Mathiak, and O. Bagasra. 1997. The immunobiology of interferon-gamma inducible protein 10 kD (IP-10): a novel, pleiotropic member of the C-X-C chemokine superfamily. Cytokine Growth Factor Rev. 8:207-219.
41. Nicholson, S., G. Bonecini-Almeida Mda, J. R. Lapa e Silva, C. Nathan, Q. W. Xie, R. Mumford, J. R. Weidner, J. Calaycay, J. Geng, N. Boechat, et al. 1996. Inducible nitric oxide synthase in pulmonary alveolar macrophages from patients with tuberculosis. J. Exp. Med. 183:2293-2302.
42. Nozaki, Y., Y. Hasegawa, S. Ichiyama, I. Nakashima, and K. Shimokata. 1997. Mechanism of nitric oxide-dependent killing of Mycobacterium bovis BCG in human alveolar macrophages. Infect. Immun. 65:3644-3647.
43. Ohmori, Y., and T. A. Hamilton. 1995. The interferon-stimulated response element and a kappa B site mediate synergistic induction of murine IP-10 gene transcription by IFN-gamma and TNF-alpha. J. Immunol. 154:5235-5244.
44. O'Shea, J. J., and R. Visconti. 2000. Type 1 IFNs and regulation of TH1 responses: enigmas both resolved and emerge. Nat. Immunol. 1:17-19.
45. Piali, L., C. Weber, G. LaRosa, C. R. Mackay, T. A. Springer, I. Clark-Lewis, and B. Moser. 1998. The chemokine receptor CXCR3 mediates rapid and shear-resistant adhesion-induction of effector T lymphocytes by the chemokines IP10 and Mig. Eur. J. Immunol. 28:961-972.
46. Pine, R., T. Decker, D. S. Kessler, D. E. Levy, and J. E. Darnell, Jr. 1990. Purification and cloning of interferon-stimulated gene factor 2 (ISGF2): ISGF2 (IRF-1) can bind to the promoters of both beta interferon- and interferon-stimulated genes but is not a primary transcriptional activator of either. Mol. Cell. Biol. 10:2448-2457.
47. Qiao, Y., S. Prabhakar, E. M. Coccia, M. Weiden, A. Canova, E. Giacomini, and R. Pine. 2002. Host defense responses to infection by Mycobacterium tuberculosis. Induction of IRF-1 and a serine protease inhibitor. J. Biol. Chem. 277:22377-22385.
48. Raju, B., C. F. Tung, D. Cheng, N. Yousefzadeh, R. Condos, W. N. Rom, and D. B. Tse. 2001. In situ activation of helper T cells in the lung. Infect. Immun. 69:4799-4798.
49. Rhoadès, E. R., A. M. Cooper, and I. M. Orme. 1995. Chemokine response in mice infected with Mycobacterium tuberculosis. Infect. Immun. 63:3871-3877.
50. Rich, E. A., M. Torres, E. Sada, C. K. Finegan, B. D. Hamilton, and Z. Toossi. 1997. Mycobacterium tuberculosis (MTB)-stimulated production of nitric oxide by human alveolar macrophages and relationship of nitric oxide production to growth inhibition of MTB. Tuber. Lung Dis. 78:247-255.
51. Rossouw, M., H. J. Nel, G. S. Cooke, P. D. van Helden, and E. G. Hoal. 2003. Association between tuberculosis and a polymorphic NFkappaB binding site in the interferon gamma gene. Lancet 361:1871-1872.
52. Sauty, A., M. Dziejman, R. A. Taha, A. S. Iarossi, K. Neote, E. A. Garcia-Zepeda, Q. Hamid, and A. D. Luster. 1999. The T cell-specific CXC chemokines IP-10, Mig, and I-TAC are expressed by activated human bronchial epithelial cells. J. Immunol. 162:3549-3558.
53. Schluger, N. W., and W. N. Rom. 1998. The host immune response to tuberculosis. Am. J. Respir. Crit. Care Med. 157:679-691.
54. Schneemann, M., G. Schoedon, S. Hofer, N. Blau, L. Guerrero, and A. Schaffner. 1993. Nitric oxide synthase is not a constituent of the antimicrobial armature of human mononuclear phagocytes. J. Infect. Dis. 167:1358-1363.
55. Storey, J. 2002. A direct approach to false discovery rates. J. R. Stat. Soc. Ser. B 64:479-498.
56. Tusher, V. G., R. Tibshirani, and G. Chu. 2001. Significance analysis of microarrays applied to the ionizing radiation response. Proc. Natl. Acad. Sci. USA 98:5116-5121.
57. Tyagi, S., D. P. Bratu, and F. R. Kramer. 1998. Multicolor molecular beacons for allele discrimination. Nat. Biotechnol. 16:49-53.
58. Weiden, M., N. Tanaka, Y. Qiao, B. Y. Zhao, Y. Honda, K. Nakata, A. Canova, D. E. Levy, W. N. Rom, and R. Pine. 2000. Differentiation of monocytes to macrophages switches the Mycobacterium tuberculosis effect on HIV-1 replication from stimulation to inhibition: modulation of interferon response and CCAAT/enhancer binding protein beta expression. J. Immunol. 165:2028-2039.
59. Weinberg, J. B., M. A. Misukonis, P. J. Shami, S. N. Mason, D. L. Sauls, W. A. Dittman, E. R. Wood, G. K. Smith, B. McDonald, K. E. Bachus, et al. 1995. Human mononuclear phagocyte inducible nitric oxide synthase (iNOS): analysis of iNOS mRNA, iNOS protein, biopterin, and nitric oxide production by blood monocytes and peritoneal macrophages. Blood 86:1184-1195.