Both basal and enhancer κB elements are required for full induction of the mouse inducible nitric oxide synthase gene

Journal of Endotoxin Research

Volumn 3, Issue 5, 1996, Pages 381-393

  Murphy, W J ^a,c   Muroi, M ^b   Zhang, C X ^a   Suzuki, T ^a   Russell, S W ^a  

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

^b NATIONAL CANCER INSTITUTE   (United States)

^c UNIVERSITY OF KANSAS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; LIPOPOLYSACCHARIDE; NITRIC OXIDE SYNTHASE; TRANSCRIPTION FACTOR;

ANIMAL CELL; ARTICLE; GENE EXPRESSION; MACROPHAGE; MOUSE; NONHUMAN;

ANIMALIA;

EID: 0029773746     PISSN: 09680519     EISSN: None     Source Type: Journal    
DOI: 10.1177/096805199600300502     Document Type: Article

References (51)

1. Hibbs J.B., Taintor R.R., Vavrin Z., Rachlin E.M. Nitric oxide: a cytotoxic activated macrophage effector molecule. Biochem Biophys Res Commun 1988; 157: 87-94.
2. Nathan C. Nitric oxide as a secretory product of mammalian cells. FASEB J 1992; 6: 3051-3064.
3. Yui Y., Hattori R., Kosuga K., Eizawa H., Hiki K., Kawai C. Purification of nitric oxide synthase from rat macrophages. J Biol Chem 1991; 266: 12544-12547.
4. Hevel J.M., White K.A., Marletta M.A. Purification of the inducible murine macrophage nitric oxide synthase. Identification as a flavoprotein. J Biol Chem 1991; 266: 22789-22791.
5. Stuehr D.J., Cho H.J., Kwon N.S., Weise M.F., Nathan C.F. Purification and characterization of the cytokine-induced macrophage nitric oxide synthase: an FAD- and FMN-containing flavoprotein. Proc Natl Acad Sci USA 1991; 88: 7773-7777.
6. Ding A.H., Nathan C.F., Stuehr D.J. Release of reactive nitrogen intermediates and reactive oxygen intermediates from mouse peritoneal macrophages. Comparison of activating cytokines and evidence for independent production. J Immunol 1988; 141: 2407-2412.
7. Stuehr D.J., Marletta M.A. Synthesis of nitrite and nitrate in murine macrophage cell lines. Cancer Res 1987; 47: 5590-5594.
8. Xie Q-W., Cho H.J., Calaycay J. et al. Cloning and characterization of inducible nitric oxide synthase from mouse macrophages. Science 1992; 256: 225-228.
9. Lorsbach R.B., Murphy W.J., Lowenstein C.J., Snyder S.H., Russell S.W. Expression of the nitric oxide synthase gene in mouse macrophages activated for tumor cell killing. Molecular basis for the synergy between interferon-γ and lipopolysaccharide. J Biol Chem 1993; 268: 1908-1913.
10. Liew F.Y., Li Y., Moss D., Parkinson C., Rogers M.V., Moncada S. Resistance to Leishmania major infection correlates with the induction of nitric oxide synthase in murine macrophages. Eur J Immunol 1991; 21: 3009-3014.
11. Xie Q-W., Whisnant R., Nathan C. Promoter of the mouse gene encoding calcium-independent nitric oxide synthase confers inducibility by interferon gamma and bacterial lipopolysaccharide. J Exp Med 1993; 177: 1779-1784.
12. Lowenstein C.J., Alley E.W., Raval P. et al. Macrophage nitric oxide synthase gene: two upstream regions mediate induction by interferon γ and lipopolysaccharide. Proc Natl Acad Sci USA 1993; 90: 9730-9734.
13. Alley E.W., Murphy W.J., Russell S.W. A classical enhancer element responsive to both lipopolysaccharide and interferon-γ augments induction of the iNOS gene in mouse macrophages. Gene 1995; 158: 247-251.
14. Weisz A., Oguchi S., Cicatiello L., Esumi H. Dual mechanism for the control of inducible-type NO synthase gene expression in macrophages during activation by interferon-γ and bacterial lipopolysaccharide. J Biol Chem 1994; 269: 8324-8333.
15. Kamijo R., Harada H., Matsuyama T. et al. Requirement for transcription factor IRF-1 in NO synthase induction in macrophages. Science 1994; 263: 1612-1615.
16. Martin E., Nathan C., Xie Q-W. Role of interferon regulatory factor 1 in induction of nitric oxide synthase. J Exp Med 1994; 180: 977-984.
17. Baeuerle P.A., Baltimore D. IκB: a specific inhibitor of the NF-κB transcription factor. Science 1988; 242: 540-546.
18. Beg A.A., Baldwin A.S. The IκB proteins: multifunctional regulators of Rel/NF-κB transcription factors. Genes Dev 1993; 7: 2064-2070.
19. Palombella V.J., Rando O.J., Goldberg A.L., Maniatis T. The ubiquitin-proteasome pathway is required for processing the NF-κB1 precursor protein and the activation of NF-κB. Cell 1994; 78: 773-785.
20. Lin Y.C., Brown K., Siebenlist U. Activation of NF-κB requires proteolysis of the inhibitor IκB-α: signal-induced phosphorylation of IκB-α alone does not release active NF-κB. Proc Natl Acad Sci USA 1995; 92: 552-556.
21. DiDonato J.A., Mercurio F., Karin M. Phosphorylation of IκBα precedes but is not sufficient for its dissociation from NF-κB. Mol Cell Biol 1995; 15: 1302-1311.
22. Xie Q-W., Kashiwabara Y., Nathan C. Role of transcription factor NF-κB/Rel in induction of nitric oxide synthase. J Biol Chem 1994; 269: 4705-4708.
23. Morrison D.C., Leive L. Fractions of lipopolysaccharide from Escherichia coli O111:B4 prepared by two extraction procedures. J Biol Chem 1975; 250: 2911-2919.
24. Cassady A.I., Stacey K.J., Nimmo K.A. et al. Constitutive expression of the urokinase plasminogen activator gene in murine RAW264 macrophages involves distal and 5′ noncoding sequences that are conserved between mouse and pig. Nucl Acids Res 1991; 19: 6839-6847.
25. Garrity P.A., Wold B.J. Effects of different DNA polymerases in ligation-mediated PCR: enhanced genomic sequencing and in viro footprinting. Proc Natl Acad Sci USA 1992; 89: 1021-1025.
26. Dignam J.D., Lebovitz R.M., Roeder R.G. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucl Acids Res 1983; 11: 1475-1489.
27. Muroi M, Suzuki T. Role of protein kinase A in LPS-induced activation of NF-κB proteins of a mouse macrophage-like cell line, J774. Cell Signal 1993; 5: 289-298.
28. Sen R., Baltimore D. Multiple nuclear factors interact with the immunoglobulin enhancer sequences. Cell 1986; 46: 705-716.
29. Nabel G., Baltimore D. An inducible transcription factor activates expression of human immunodeficiency virus in T cells. Nature 1987; 326: 711-713.
30. Chen D., Rothenberg E.V. Interleukin 2 transcription factors as molecular targets of cAMP inhibition: delayed inhibition kinetics and combinatorial transcription roles. J Exp Med 1994; 179: 931-942.
31. Fujihara M., Connolly N., Ito N., Suzuki T. Properties of protein kinase C isoforms (β II, ε, and ξ) in a macrophage cell line (J774) and their roles in LPS-induced nitric oxide production. J Immunol 1994; 152: 1898-1906.
32. Muroi M., Muroi Y., Yamamoto K-i., Suzuki T. Influence of 3′ half-site sequence of NF-κB motifs on the binding of lipopolysaccharide-activatable macrophage NF-κB proteins. J Biol Chem 1993; 268: 19534-19539.
33. Ohmori Y., Tebo J., Nedospasov S., Hamilton T.A. κB binding activity in a murine macrophage-like cell line. J Biol Chem 1994; 269: 17684-17690.
34. Brunvand M.W., Krumm A., Groudine M. In vivo footprinting of the human IL-2 gene reveals a nuclear factor bound to the transcription start site in T cells. Nucl Acids Res 1993; 21: 4824-4829.
35. Goldring C.E.P., Reveneau S., Algarte M., Jeannin J-F. In vivo footprinting of the mouse inducible nitric oxide synthase gene: inducible protein occupation of numerous sites including Oct and NF-IL6. Nucl Acids Res 1996; 24: 1682-1687.
36. Kunsch C., Ruben S.M., Rosen C.A. Selection of optimal κB/Rel DNA-binding motifs: interaction of both subunits of NF-κB with DNA is required for transcriptional activation. Mol Cell Biol 1992; 12: 4412-4421.
37. Parkins N.D., Schmid R.M., Duckett C.S., Leung K., Rice N.R., Nabel G.J. Distinct combinations of NF-κB subunits determine the specificity of transcriptional activation. Proc Natl Acad Sci USA 1992; 89: 1529-1533.
38. Lin R., Gewert D., Hiscott J. Differential transcriptional activation in vitro by NF-κB/Rel proteins. J Biol Chem 1995; 270: 3123-3131.
39. Shimizu H., Mitomo K., Watanabe T., Okamoto S., Yamamoto K. Involvement of a NF-κB-like transcription factor in the activation of the interleukin-6 gene by inflammatory lymphokines. Mol Cell Biol 1990; 10: 561-568.
40. Nakayama K., Shimizu H., Mitomo K., Watanabe T., Okamoto S., Yamamoto K. A lymphoid cell-specific nuclear factor containing c-Rel-like proteins preferentially interacts with interleukin-6 κB-related motifs whose activities are repressed in lymphoid cells. Mol Cell Biol 1992; 12: 1736-1746.
41. Matsusaka T., Fujikawa K., Nishio Y. et al. Transcription factors NF-IL6 and NF-κB synergistically activate transcription of the inflammatory cytokines, interleukin 6 and interleukin 8. Proc Natl Acad Sci USA 1993; 90: 10193-10197.
42. Sanceau J., Kaisho T., Hirano T., Wietzerbin J. Triggering of the human interleukin-6 gene by interferon-γ and tumor necrosis factor-α in monocytic cells involves cooperation between interferon regulatory factor-1, NFκB, and Sp1 transcription factors. J Biol Chem 1995; 270: 27920-27931.
43. Hansen S.K., Guerrini L., Blasi F. Differential DNA sequence specificity and regulation of HW-1 enhancer activity by cRel-RelA transcription factor. J Biol Chem 1994; 269: 22230-22237.
44. Urban M.B., Baeuerle P.A. The role of the p50 and p65 subunits of NF-κB in the recognition of cognate sequences. New Biol 1991; 3: 279-288.
45. Franzoso G., Bours V., Azarenko V. et al. The oncoprotein Bcl-3 can facilitate NF-κB-mediated transactivation by removing inhibiting p50 homodimers from select κB sites. EMBO J 1993; 12: 3893-3901.
46. Muller-Immergluck M.M., Schaffner W., Matthias P. Transcription factor Oct-2A contains functionally redundant activating domains and works selectively from a promoter but not from a remote enhancer position in non-lymphoid (HeLa) cells. EMBO J 1990; 9: 1625-1634.
47. Thanos D., Maniatis T. Virus induction of human IFNβ gene expression requires the assembly of an enhanceosome. Cell 1995; 83: 1091-1100.
48. Alley E.W., Zhang X., Russell S.W. Contribution of clonally distinct subpopulations to heterogeneous production of inducible nitric oxide synthase by LPS-stimulated mouse macrophages. J Endotoxin Res 1994; 1: 235-242.
49. Pace J.L., Lowenstein C.J., Phillips T.A. et al. Population dynamics of inducible nitric oxide synthase production by LPS- and LPS/IFN-γ-stimulated mouse macrophages. J Endotoxin Res 1994; 1: 227-233.
50. Gordon S. The macrophage. Bioessays 1995; 17: 977-986.
51. Rutherford M.S., Witsell A., Schook L.B. Mechanisms generating functionally heterogeneous macrophages: chaos revisited. J Leukoc Biol 1993; 53: 602-618.