Transcriptional basis for hyporesponsiveness of the human inducible nitric oxide synthase gene to lipopolysaccharide/interferon-γ

Journal of Leukocyte Biology

Volumn 59, Issue 4, 1996, Pages 575-585

  Zhang, Xiaoke ^a,b   Laubach, Victor E ^c   Alley, Evan W ^a,b   Edwards, Kevin A ^c,d   Sherman, Paula A ^c   Russell, Stephen W ^a,b   Murphy, William J ^a,b  

^a UNIVERSITY OF KANSAS MEDICAL CENTER   (United States)

^b UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

^c Burroughs Wellcome Co   (United States)

^d DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Endotoxin; Gene regulation; Macrophage; NF B; U937 monocyte like cell line

Indexed keywords

ENDOTOXIN; LIPOPOLYSACCHARIDE; NITRIC OXIDE SYNTHASE; RECOMBINANT GAMMA INTERFERON;

ARTICLE; CONTROLLED STUDY; GENE EXPRESSION; GENETIC REGULATION; HUMAN; HUMAN CELL; MACROPHAGE; MONOCYTE; PRIORITY JOURNAL;

ANIMALS; BASE SEQUENCE; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HUMANS; INTERFERON-GAMMA, RECOMBINANT; LEUKOCYTES, MONONUCLEAR; LIPOPOLYSACCHARIDES; MICE; MOLECULAR SEQUENCE DATA; NF-KAPPA B; NITRIC OXIDE SYNTHASE; PHAGOCYTES; PROMOTER REGIONS (GENETICS); SEQUENCE HOMOLOGY, NUCLEIC ACID; TRANSCRIPTION, GENETIC;

EID: 0029886747     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1002/jlb.59.4.575     Document Type: Article

References (57)

1. Schmidt, H. H. H. W., Walter, U. (1994) NO at work. Cell 78, 919-925.
2. Nathan, C. Z. (1992) Nitric oxide as a secretory product of mammalian cells. FASEB J. 6, 3051-3064.
3. Dawson, D. A. (1994) Nitric oxide and focal cerebral ischemia: multiplicity of actions and diverse outcome. Cerebrovasc. Brain Metab. Rev. 6, 299-324.
4. Billiar, T. R. (1995) Nitric oxide. Novel biology with clinical relevance. Ann. Surg. 221, 339-349.
5. Lowenstein, C. J., Dinerman, J. L., Snyder, S. H. (1994) Nitric oxide: a physiologic messenger. Ann Intern. Med. 120, 227-237.
6. Wolfe, T. A., Dasta, J. F. (1995) Use of nitric oxide synthase inhibitors as a novel treatment for septic shock. Ann. Pharmacother. 29, 36-46.
7. McCartney-Francis, N., Allen, J. B., Mizel, D. E., Albina, J. E., Xie, Q. -W., Nathan, C. F., Wahl, S. M. (1993) Suppression of arthritis by an inhibitor of nitric oxide synthase. J. Exp. Med. 178, 749-754.
8. Marletta, M. A. (1993) Nitric oxide synthase structure and mechanism. J Biol. Chem. 268, 12231-12234.
9. Nathan, C., Xie, Q. -W. (1994) Nitric oxide synthases: roles, tolls, and controls. Cell 78, 915-918.
10. Stuehr, D. J., Griffith, O. W. (1992) Mammalian nitric oxide synthases. Adv. Enzymol. Relat. Areas Mol. Biol. 65, 287-346.
11. Xie, Q. -W., Cho, H. J., Calaycay, J., Mumford, R. A., Swiderek, K. M., Lee, T. D., Ding, A., Troso, T., Nathan, C. (1992) Cloning and characterization of inducible nitric oxide synthase from mouse macrophages. Science 256, 225-258.
12. Geller, D. A., Lowenstein, C. J., Shapiro, R. A., Nussler, A. K., Di-Silvio, M., Wang, S. C., Nakayama, D. K., Simmons, R. L., Snyder, S. H., Billiar, T. R. (1993) Molecular cloning and expression of inducible nitric oxide synthase from human hepatocytes. Proc. Natl. Acad. Sci. USA 90, 3491-3495.
13. Nunokawa, Y., Ishida, N., Tanaka, S. (1993) Cloning of inducible nitric oxide synthase in rat vascular smooth muscle cells. Biochem. Biophys. Res. Commun. 191, 89-94.
14. Adler, H., Frech, B., Thony, M., Pfister, H., Peterhans, E., Jungi, T.W. (1995) Inducible nitric oxide synthase in cattle. Differential cytokine regulation of nitric oxide synthase in bovine and murine macrophages. J. Immunol. 154, 4710-4718.
15. Xie, Q. -W., Whisnant, R., Nathan, C. (1993) Promoter of the mouse gene encoding calcium-independent nitric oxide synthase confers inducibility by interferon gamma and bacterial lipopolysaccharide. J. Exp. Med. 177, 1779-1784.
16. Lowenstein, C. J, Alley, E. W., Raval, P., Snowman, A. M., Snyder, S. H., Russell, S. W., Murphy, W. J. (1993) Macrophage nitric oxide synthase gene: Two upstream regions mediate induction by interferon-gamma and lipopolysaccharide. Proc. Natl. Acad. Sci. USA 90, 9730-9734.
17. Xie, Q. -W., Kashiwabara, Y., Nathan, C. (1993) Role of transcription factor NF-kappa B/Rel in induction of nitric oxide synthase. J. Biol. Chem. 269, 4705-4708.
18. Alley, E. W., Murphy, W. J., Russell, S. W. (1995) A classical enhancer element responsive to both lipopolysaccharide and interferon-gamma, but not interferon-beta, augments induction of the iNOS gene in mouse macrophages. Gene 158, 247-251.
19. Martin, E., Nathan, C., Xie, Q. -W. (1994) Role of interferon regulatory factor 1 in induction of nitric oxide synthase. J. Exp. Med. 180, 977-984.
20. Denis, M. (1994) Human monocytes/macrophages: NO or NO? J. Leukoc. Biol. 55, 682-684.
21. Cameron, M. L., Granger, D. L., Weinberg, B. J., Kozumbo, W. J., Koren, H. S. (1990) Human Alveolar and peritoneal macrophages mediate fungistasis independently of L-arginine oxidation to nitrite or nitrate. Am. Rev. Respir. Dis. 142, 1313-1319.
22. Schneemann, M., Schoedon, G., Hofer, S., Blau, N., Guerrero, L., Schaffner, A. (1993) Nitric oxide synthase is not a constituent of the antimicrobial armature of human mononuclear phagocytes. J. Infect. Dis. 167, 1358-1363.
23. Weinberg, J. B., Misukonis, M. A., Shami, P. J., Mason, S. N., Sauls, D. L., Dillman, W. A, Wood, E. R., Smith, G. K., McDonald, B., Bachaus, K. E., Haney, A. F., Granger, D. L. (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.
24. Hunt, N. C., Goldin, R. D. (1992) Nitric oxide production by monocytes in alcoholic liver disease. J. Hepatol. 14, 146-150.
25. Leibovich, J. S., Polverini, P. J., Fong, T. W., Harlow, L. A., Koch, A. E. (1994) Production of angiogenic activity by human monocytes requires an L-arginine/nitric oxide-synthase-dependent effector mechanism. Proc. Natl. Acad. Sci. USA 91, 4190-4194.
26. Morrison, D. C., Leive, L. (1975) Fractions of lipopolysaccharide from Escherichia coli 0111:B4 prepared by two extraction procedures. J Biol. Chem. 250, 2911-2919.
27. Eilers, A., Seegeri, D., Schindler, C., Baccarini, M., Decker, T. (1993) The response of gamma interferon activation factor is under developmental control in cells of the macrophage lineage. Mol. Cell. Biol. 13, 3245-3254.
28. Lorsbach, R. B., Murphy, W. J., Lowenstein, C. J., Snyder, S. H., Russell, S. W. (1993) Expression of the nitric oxide synthase gene in mouse macrophages activated for tumor cell killing. J. Biol Chem. 268, 1908-1913.
29. Sherman, P. A., Laubach, V. E., Reep, B. R., Wood, E. R. (1993) Purification and cDNA sequence of an inducible nitric oxide synthase from a human tumor cell line. Biochemistry 32, 11600-11605.
30. Cowley, B. C., Chadwick, Jr., L. J., Gramham, J. J., Calvet J. P. (1989) Sequential protooncogene expression in regenerating kidney following acute renal injury. J. Biol. Chem. 264, 8389-8393.
31. Chartrain, N. A., Geller, D. A., Koty, P. P., Sitrin, N. F., Nussler, A. K., Hoffman, E. P., Billiar, T. R., Hutchinson, N. I., Mudgett, J. S. (1994) Molecular cloning, structure, and chromosomal localization of the human inducible nitric oxide synthase gene. J. Biol. Chem. 269, 6765-6772.
32. Sambrook, J., Fritsch, E. F., Maniatis, T. (1989) Sequencing by the Sanger dideoxy-mediated chain-termination method. In Molecular Cloning, vol. 2 (C. Nolan, ed.), Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, 13.42-13.74.
33. Cassady, A. I., Stacey, K. J., Nimmo, K. A., Murphy, K. M., Von der Ahe, D., Pearson, D., Botteri, F. M., Nagamine, Y., Hume, D. A. (1991) Constitutive expression of the urokinase plasminogen activator gene in murine RAW264 macrophages involves distal and 5 non-coding sequences that are conserved between mouse and pig. Nucleic Acids Res. 19, 6839-6847.
34. Muroi, M., Muroi, Y., Yamamoto, K. I., Suzuki, T. (1993) Influence of 3′ half-site sequence of NF-kappa B motifs on the binding of lipopolysaccharide-activalable macrophage NF-kappa B proteins. J. Biol. Chem. 268, 19534-19539.
35. 15N]nitrate in biological fluids. Anal. Biochem. 126, 131-138.
36. Grilli, M., Chiu, J. J.-S., Lenardo, M. J. (1993) NF-kappaB and Rel: Participants in a multiform transcriptional regulatory system. Int. Rev. Cytol. 143, 1-62.
37. Akira, S., Kishimoto, T. (1992) IL-6 and NF-IL-6 in acute-phase response and viral infection. Immunol. Rev. 127, 25-50.
38. Tanaka, N., Kawakami, T., Taniguchi, T. (1993) Recognition DNA sequences of interferon regulatory factor (IRF-1) and IRF-2, regulators of cell growth and the interferon system. Mol. Cell. Biol. 13, 4531-4538.
39. Seidel, H. M., Milocco, L. H., Lamb, P., Darnell, J. E., Stein, Jr., R. B., Rosen, J. (1995) Spacing of palindromic half sites as a determinant of selective STAT (signal transducers and activators of transcription) DNA binding and transcriptional activity. Proc. Natl. Acad. Sci. USA 92, 3041-3045.
40. Libermann, T. A., Baltimore, D. (1990) Activation of interleukin-6 gene expression through the NF-κB transcription factor. Mol. Cell. Biol. 10, 2327-2334.
41. Veals, S. A., Santa Maria, T., Levy, D. E. (1993) Two domains of ISGF3γ that mediate protein-DNA and protein-protein interactions during transcription factor assembly contribute to DNA-binding specificity. Mol. Cell. Biol. 13, 196-206.
42. Levy, D. E., Kessler, D. S., Pine, R., Reich, N., Darnell, Jr., J. E. (1988) Interferon-induced nuclear factors that bind a shared promoter element correlate with positive and negative transcriptional control. Genes Dev. 2, 383-393.
43. Pearse, R. N., Feinman, R., Shuai, K., Darnell, Jr., J. E., Ravetch, J. V. (1993). Interferon γ-induced transcription of the high-affinity Fc receptor for IgG requires assembly of a complex that includes the 91-kDa subunit of transcription factor ISGF3. Proc. Natl. Acad. Sci. USA 90, 4314-4318.
44. Kamijo, R., Harada, H., Matsuyama, T., Bosland, M., Gerecitano, J., Shapiro, D., Le, J., Koh, S. I., Kimura, T., Green, S. J., Mak, T. W., Taniguchi, T., Vilcek, J. (1994) Requirement for transcription factor IRF-1 in NO synthase induction in macrophages. Science 263, 1612-1615.
45. Griffin, G. E., Leung, K., Folks, T. M., Kunkel, S., Nabel, G. J. (1989) Activation of HIV gene expression during monocyte differentiation by induction of NF-κB. Nature 339, 70-73.
46. Haas, J. G., Baeuerle, P. A., Riethmüller, G., Ziegler-Heitbrock, H. W. L. (1990) Molecular mechanisms in down-regulation of tumor necrosis factor expression. Proc. Natl. Acad. Sci. USA 87, 9563-9567.
47. Kaufman, P. A., Weinberg, J. B., Greene, W. C. (1992) Nuclear expression of the 50- and 65-kD Rel-related subunits of nuclear factor-κB is differentially regulated in human monocytic cells. J. Clin. Invest. 90, 121-129.
48. Frankenberger, M., Pforte, A., Sternsdorf, T., Passlick, B., Baeuerle, P. A., Ziegler-Heitbrock, H. W. L. (1994) Constitutive nuclear NF-κB in cells of the monocyte lineage. Biochem. J. 304, 87-94.
49. Perkins, N. D., Schmid, R. M., Duckett, C. S., Leung, K., Rice, N. R., Nabel, G. J. (1992) Distinct combinations of NF-κB subunits determine the specificity of transcriptional activation. Proc. Natl. Acad. Sci. USA 89, 1529-1533.
50. 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.
51. Munoz-Fernandez, M. A., Fernandez, M. A., Fresno, M. (1992) Activation of human macrophages for the killing of intracellular Trypanosoma cruzi by TNF-alpha and IFN-gamma through a nitric oxide-dependent mechanism. Immunol Lett. 33, 35-40.
52. Gyan, B., Troye-Blomberg, M., Perlmann, P., Bjorkman, A. (1994) Human monocytes cultured with and without interferon-gamma inhibit Plasmodium falciparum parasite growth in vitro via secretion of reactive nitrogen intermediates. Parasite Immunol. 16, 371-375.
53. Tufano, M. A., Rossano, F., Catalanotti, P., Liguoti, G., Marinelli, A., Baroni, A., Marinelli, P. (1994) Properties of Yersinia enterocolitica porins: interference with biological functions of phagocytes, nitric oxide production and selective cytokine release. Res. Microbiol. 145, 297-307.
54. Zembala, M, Siedlar, M., Marcinkiewicz, J., Pryjma, J. (1994) Human monocytes are stimulated for nitric oxide release in vitro by some tumor cells but not by cytokines and lipopolysaccharide. Eur. J. Immunol. 24, 435-439.
55. Maria, R. D., Cifone, M. G., Trotta, R., Rippo, M. R., Festuccia, C., Samoni, A., Testi, R. (1994) Triggering of human monocyte activation through CD69, a member of the natural killer cell gene complex family of signal transducing receptors. J. Exp. Med. 180, 1999-2004.
56. Nussler, A. K., Di, S. M., Billiar, T. R., Hoffman, R. A., Geller, D. A., Selby, R., Madariaga, J., Simmons, R. L., (1992) Stimulation of the nitric oxide synthase pathway in human hepatocytes by cytokines and endotoxin. J. Exp. Med. 176, 261-264.
57. Weisz, A., Oguchi, S., Cicatiello, L., Esumi, H. (1994) Dual mechanism for the control of inducible-type NO synthase gene expression in macrophages during activation by interferon-gamma and bacterial lipopolysaccharide. J. Biol. Chem. 269, 8324-8333.