Suppression of IFNγ + mycobacterial lipoarabinomannan-induced NO by IL-4 is due to decreased IRF-1 expression

Tuberculosis

Volumn 89, Issue 4, 2009, Pages 294-303

  Morris, Kristin R ^b   Lutz, Ryan D ^b   Bai, Xiyuan ^b   McGibney, Mischa T ^b   Cook, Danielle ^b   Ordway, Diane ^d   Chan, Edward D ^a,b,c  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b UNIVERSITY OF COLORADO   (United States)

^c DEPARTMENT OF MEDICINE   (United States)

^d Department of Environmental and Radiological Health Sciences   (United States)

Author keywords

Inducible nitric oxide synthase; Interferon gamma; Interleukin 4; Lipoarabinomannan; Nitric oxide; Transcriptional regulation

Indexed keywords

ARGINASE; ARGININE; GAMMA INTERFERON; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERFERON REGULATORY FACTOR 1; INTERLEUKIN 4; LIPOARABINOMANNAN; NITRIC OXIDE; INTERLEUKIN 18; LIPOPOLYSACCHARIDE; MESSENGER RNA; STAT6 PROTEIN; STAT6 PROTEIN, MOUSE;

ANIMAL CELL; ARTICLE; ENZYME ACTIVITY; GENE EXPRESSION; MACROPHAGE; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; TRANSCRIPTION REGULATION; ANIMAL; BAGG ALBINO MOUSE; BIOSYNTHESIS; CELL CULTURE; DRUG EFFECT; ENZYME LINKED IMMUNOSORBENT ASSAY; GENETICS; HUMAN; IMMUNOLOGY; METABOLISM; MOUSE; PHYSIOLOGY; PROMOTER REGION; WESTERN BLOTTING;

ANIMALS; ARGINASE; ARGININE; BLOTTING, WESTERN; CELLS, CULTURED; ENZYME-LINKED IMMUNOSORBENT ASSAY; GENE EXPRESSION; HUMANS; INTERFERON REGULATORY FACTOR-1; INTERFERON-GAMMA; INTERLEUKIN-18; INTERLEUKIN-4; LIPOPOLYSACCHARIDES; MACROPHAGES; MICE; MICE, INBRED BALB C; MYCOBACTERIUM TUBERCULOSIS; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE II; PROMOTER REGIONS, GENETIC; RNA, MESSENGER; STAT6 TRANSCRIPTION FACTOR;

EID: 67650621565     PISSN: 14729792     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.tube.2009.03.004     Document Type: Article

References (47)

1. MacMicking J.D., Nathan C., Hom G., Chartrain N., Fletcher D.S., Trumbauer M., et al. Altered responses to bacterial infection and endotoxic shock in mice lacking inducible nitric oxide synthase. Cell 81 (1995) 641-650
2. Chan J., Xing Y., Magliozzo R.S., and Bloom B.R. Killing of virulent Mycobacterium tuberculosis by reactive nitrogen intermediates produced by activated murine macrophages. J Exp Med 175 (1992) 1111-1122
3. MacMicking J.D., North R.J., LaCourse R., Mudgett J.S., Shah S.K., and Nathan C.F. Identification of nitric oxide synthase as a protective locus against tuberculosis. Proc Natl Acad Sci U S A 94 (1997) 5243-5248
4. Chan E.D., Chan J., and Schluger N.W. What is the role of nitric oxide in murine and human host defense against tuberculosis? Current knowledge. Am J Respir Cell Mol Biol 25 (2001) 606-612
5. Axelrod S., Oschkinat H., Enders J., Schlegel B., Brinkmann V., Kaufmann S.H., et al. Delay of phagosome maturation by a mycobacterial lipid is reversed by nitric oxide. Cell Microbiol 10 (2008) 1530-1545
6. Voskuil M.I., Schnappinger D., Visconti K.C., Harrell M.I., Dolganov G.M., Sherman D.R., et al. Inhibition of respiration by nitric oxide induces a Mycobacterium tuberculosis dormancy program. J Exp Med 198 (2003) 705-713
7. Brennan P.J. Structure, function, and biogenesis of the cell wall of Mycobacterium tuberculosis. Tuberculosis 83 (2003) 91-97
8. Barnes P.F., Chatterjee D., Abrams J.S., Lu S., Wang E., Yamamura M., et al. Cytokine production induced by Mycobacterium tuberculosis lipoarabinomannan: relationship to chemical structure. J Immunol 149 2 (1992) 541-547
9. Chatterjee D., and Khoo K.H. Mycobacterial lipoarabinomannan: an extraordinary lipoheteroglycan with profound physiological effects. Glycobiology 8 (1998) 113-120
10. Chatterjee D., Roberts A.D., Lowell K., Brennan P.J., and Orme I.M. Structural basis of capacity of lipoarabinomannan to induce secretion of tumor necrosis factor. Infect Immun 60 (1992) 1249-1253
11. Dahl K.E., Shiratsuchi H., Hamilton B.D., Ellner J.J., and Toossi Z. Selective induction of transforming growth factor beta in human monocytes by lipoarabinomannan of Mycobacterium tuberculosis. Infect Immun 64 (1996) 399-405
12. Zhang Y., Doerfler M., Lee T.C., Guillemin B., and Rom W.N. Mechanisms of stimulation of interleukin-1 beta and tumor necrosis factor-alpha by Mycobacterium tuberculosis components. J Clin Invest 91 (1993) 2076-2083
13. Schlesinger L.S. Macrophage phagocytosis of virulent but not attenuated strains of Mycobacterium tuberculosis is mediated by mannose receptors in addition to complement receptors. J Immunol 150 (1993) 2920-2930
14. Rojas M., Garcia L.F., Nigou J., Puzo G., and Olivier M. Mannosylated lipoarabinomannan antagonizes Mycobacterium tuberculosis - induced macrophage apoptosis by altering Ca + 2-dependent cell signaling. J Infect Dis 182 (2000) 240-251
15. Chan E.D., Morris K.R., Belisle J.T., Hill P.J., Remigio L.K., Brennan P.J., et al. Induction of inducible nitric oxide synthase-NO by lipoarabinomannan of Mycobacterium tuberculosis is mediated by MEK1-ERK, MKK7-JNK and NF-kB signaling pathways. Infect Immun 69 (2001) 2001-2010
16. Morris K.R., Lutz R.D., Choi H.-S., Kamitani T., Chmura K., and Chan E.D. Role of the NF-kB signaling pathway and kB cis-regulatory elements on the IRF-1 and iNOS promoter regions in mycobacterial lipoarabinomannan induction of nitric oxide. Infect Immun 71 (2003) 1442-1452
17. Rutschman R., Lang R., Hesse M., Ihle J.N., Wynn T.A., and Murray P.J. Cutting edge: Stat6-dependent substrate depletion regulates nitric oxide production. J Immunol 166 (2001) 2173-2177
18. Hesse M., Modolell M., La Flamme A.C., Schito M., Fuentes J.M., Cheever A.W., et al. Differential regulation of nitric oxide synthase-2 and arginase-1 by type 1/type 2 cytokines in vivo: granulomatous pathology is shaped by the pattern of arginine metabolism. J Immunol 167 (2001) 6533-6544
19. Bogdan C. Nitric oxide and the immune response. Nat Immunol 2 (2001) 907-916
20. Modolell M., Corraliza I.M., Link F., Soler G., and Eichmann K. Reciprocal regulation of the nitric oxide synthase/arginase balance in mouse bone marrow-derived macrophages by TH1 and TH2 cytokines. Eur J Immunol 25 (1995) 1101-1104
21. Murphy W.J., Muroi M., Zhang X., Suzuki T., and Russell S.W. Both a basal and an enhancer IB element is (sic) required for full induction of the mouse inducible nitric oxide synthase gene. J Endotoxin Res 3 (1996) 381-393
22. Riches D.W., and Underwood G.A. Expression of interferon-beta during the triggering phase of macrophage cytocidal activation. Evidence for an autocrine/paracrine role in the regulation of this state. J Biol Chem 266 (1991) 24785-24792
23. Corraliza I.M., Campo M.L., Soler G., and Modolell M. Determination of arginase activity in macrophages: a micromethod. J Immunol Methods 174 (1994) 231-235
24. Chang C.-I., Liao J.C., and Kuo L. Arginase modulates nitric oxide production in activated macrophages. Am J Physiol Heart Circ Physiol 274 (1998) H342-H348
25. Brown M.C., and Taffet S.M. Lipoarabinomannans derived from different strains of Mycobacterium tuberculosis differentially stimulate the activation of NF-kappa B and KBF1 in murine macrophages. Infect Immun 63 (1995) 1960-1968
26. Donnelly R.P., Crofford L.J., Freeman S.L., Buras J., Remmers E., Wilder R.L., et al. Tissue-specific regulation of IL-6 production by IL-4. Differential effects of IL-4 on nuclear factor-kappa B activity in monocytes and fibroblasts. J Immunol 151 (1993) 5603-5612
27. Schindler C., Kashleva H., Pernis A., Pine R., and Rothman P. STF-IL-4: a novel IL-4-induced signal transducing factor. Embo J 13 (1994) 1350-1356
28. Coccia E.M., Stellacci E., Marziali G., Weiss G., and Battistini A. IFN-g and Il-4 differently regulate inducible NO synthase gene expression through IRF-1 modulation. Int Immunol 12 (2000) 977-985
29. Kahnert A., Seiler P., Stein M., Bandermann S., Hahnke K., Mollenkopf H., et al. Alternative activation deprives macrophages of a coordinated defense program to Mycobacterium tuberculosis. Eur J Immunol 36 (2006) 631-647
30. Yamamura M., Uyemura K., Deans R.J., Weinberg K., Rea T.H., Bloom B.R., et al. Defining protective responses to pathogens: cytokine profiles in leprosy lesions. Science 254 (1991) 277-279
31. Gordon S. Alternative activation of macrophages. Nat Rev Immunol 3 (2003) 23-35
32. Buccheri S., Reljic R., Caccamo N., Ivanyi J., Singh M., Salerno A., et al. IL-4 depletion enhances host resistance and passive IgA protection against tuberculosis infection in BALB/c mice. Eur J Immunol 37 (2007) 729-737
33. North R.J. Mice incapable of making IL-4 or IL-10 display normal resistance to infection with Mycobacterium tuberculosis. Clin Exp Immunol 113 (1998) 55-58
34. Jung Y.-J., LaCourse R., Ryan L., and North R.J. Evidence inconsistent with a negative influence of T helper 2 cells on protection afforded by a dominant T helper 1 response against Mycobacterium tuberculosis lung infection in mice. Infect Immun 70 (2002) 6436-6443
35. Dlugovitzky D., Bay M.L., Rateni L., Urizar L., Rondelli C.F., Largacha C., et al. In vitro synthesis of interferon-gamma, interleukin-4, transforming growth factor-beta and interleukin-1 beta by peripheral blood mononuclear cells from tuberculosis patients: relationship with the severity of pulmonary involvement. Scand J Immunol 49 (1999) 210-217
36. van Crevel R., Karyadi E., Preyers F., Leenders M., Kullberg B.-J., Nelwan R.H.H., et al. Increased production of interleukin 4 by CD4+ and CD8+ T cells from patients with tuberculosis is related to the presence of pulmonary cavities. J Infect Dis 181 (2000) 1194-1197
37. Ordway D.J., Costa L., Martins M., Silveira H., Amaral L., Arroz M.J., et al. Increased interleukin-4 production by CD8 and gamma-delta T cells in health-care workers is associated with the subsequent development of active tuberculosis. J Infect Dis 190 (2004) 756-766
38. Rook G.A.W., Hernandez-Pando R., Dheda K., and Seah G.T. IL-4 in tuberculosis: implications for vaccine design. Trends Immunol 25 (2004) 483-488
39. Aung H., Toossi Z., McKenna S.M., Gogate P., Sierra J., Sada E., et al. Expression of transforming growth factor-beta but not tumor necrosis factor-alpha, interferon-gamma, and interleukin-4 in granulomatous lung lesions in tuberculosis. Tuber Lung Dis 80 2 (2000) 61-67
40. Bai X., Wilson S.E., Chmura K., Feldman N.E., and Chan E.D. Morphometric analysis of Th1 and Th2 cytokine expression in human pulmonary tuberculosis. Tuberculosis 84 (2004) 375-385
41. Choi H.-S., Rai P.R., Chu H.-W., Cool C., and Chan E.D. Analysis of nitric oxide synthase and nitrotyrosine expression in human pulmonary tuberculosis. Am J Respir Crit Care Med 166 (2002) 178-186
42. Vidyarani M., Selvaraj P., Prabhu Anand S., Jawahar M.S., Adhilakshmi A.R., and Narayanan P.R. Interferon gamma (IFNgamma) and interleukin-4 (IL-4) gene variants and cytokine levels in pulmonary tuberculosis. Indian J Med Res 124 (2006) 403-410
43. Reczkowski R.S., and Ash D.E. Rat liver arginase: kinetic mechanism, alternative substrates, and inhibitors. Arch Biochem Biophys 312 (1994) 31-37
44. G-hydroxy-l-arginine: Implications for the regulation of nitric oxide biosynthesis by arginase. Biochem Biophys Res Commun 202 (1994) 174-180
45. Bennett B.L., Cruz R., Lacson R.G., and Manning A.M. Interleukin-4 suppression of tumor necrosis factor alpha-stimulated E-selectin gene transcription is mediated by STAT6 antagonism of NF-kappaB. J Biol Chem 272 15 (1997) 10212-10219
46. Paludan S.R., Ellermann-Eriksen S., Lovmand J., and Mogensen S.C. Interleukin-4-mediated inhibition of nitric oxide production in interferon-g-treated and virus-infected macrophages. Scand J Immunol 49 (1999) 169-176
47. Ohmori Y., and Hamilton T.A. IL-4-induced STAT6 suppresses IFN-g-stimulated STAT1-dependent transcription in mouse macrophages. J Immunol 159 (1997) 5474-5482