Lipopolysaccharide tolerance in murine peritoneal macrophages induces downregulation of the lipopolysaccharide signal transduction pathway through mitogen-activated protein kinase and nuclear factor-κB cascades, but not lipopolysaccharide-incorporation steps

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1450, Issue 2, 1999, Pages 130-144

  Tominaga, Kaoru ^a   Saito, Shinji ^a   Matsuura, Motohiro ^a   Nakano, Masayasu ^a  

^a JICHI MEDICAL UNIVERSITY   (Japan)

Author keywords

Lipopolysaccharide; Macrophage; Mitogen activated protein kinase; Signal transduction

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LIPOPOLYSACCHARIDE; MITOGEN ACTIVATED PROTEIN KINASE;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; MOUSE; NONHUMAN; PERITONEUM MACROPHAGE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

ANIMALS; CA(2+)-CALMODULIN DEPENDENT PROTEIN KINASE; DOWN-REGULATION; DRUG TOLERANCE; INTERLEUKIN-6; LIPOPOLYSACCHARIDES; MACROPHAGES, PERITONEAL; MICE; MICE, INBRED C3H; MITOGEN-ACTIVATED PROTEIN KINASE 1; NF-KAPPA B; PACLITAXEL; PHOSPHORYLATION; SIGNAL TRANSDUCTION; TETRADECANOYLPHORBOL ACETATE; TUMOR NECROSIS FACTOR-ALPHA; TYROSINE;

MURINAE;

EID: 0033021299     PISSN: 01674889     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0167-4889(99)00037-3     Document Type: Article

References (45)

1. Raetz C.R.H., Ulevitch R.J., Wright S.D., Sibley C.H., Ding A., Nathan C.F. Gram-negative endotoxin: an extraordinary lipid with profound effects on eukaryotic signal transduction. FASEB J. 5:1991;2652-2660.
2. Ulevitch R.J., Tobias P.S. Receptor-dependent mechanisms of cell stimulation by bacterial endotoxin. Annu. Rev. Immunol. 13:1995;437-457.
3. Sweet M.J., Hume D.A. Endotoxin signal transduction in macrophages. J. Leukocyte Biol. 60:1996;8-26.
4. Weinstein S.L., Gold M.R., DeFranco A.L. Bacterial lipopolysaccharide stimulates protein tyrosine phosphorylation in macrophages. Proc. Natl. Acad. Sci. USA. 88:1991;4148-4152.
5. Weinstein S.L., Sanghera J.S., Lemke K., DeFranco A.L., L Pelech S. Bacterial lipopolysaccharide induces tyrosine phosphorylation and activation of mitogen-activated protein kinases in macrophages. J. Biol. Chem. 267:1992;14955-14962.
6. Dong Z., Qi X., Fidler I.J. Tyrosine phosphorylation of mitogen-activated protein kinases is necessary for activation of murine macrophages by natural and synthetic bacterial products. J. Exp. Med. 177:1993;1071-1077.
7. Weinstein S.L., June C.H., DeFranco A.L. Lipopolysaccharide-induced protein tyrosine phosphorylation in human macrophages is mediated by CD14. J. Immunol. 151:1993;3829-3838.
8. Beaty C.D., Franklin T.L., Uehara Y., Wilson C.B. Lipopolysaccharide-induced cytokine production in human monocytes: role of tyrosine phosphorylation in transmembrane signal transduction. Eur. J. Immunol. 24:1994;1278-1284.
9. Novogrodsky A., Vanichkin A., Patya M., Gazit A., Osherov N., Levitzki A. Prevention of lipopolysaccharide-induced lethal toxicity by tyrosine kinase inhibitors. Science. 264:1994;1319-1322.
10. Chanmugam P., Feng L., Liou S., Jang B.C., Boudreau M., Yu G., Lee J.H., Kwon H.J., Beppu T., Yoshida M., Xia Y., Wilson C.B., Hwang D. Radicicol, a protein tyrosine kinase inhibitor, suppresses the expression of mitogen-inducible cyclooxygenase in macrophages stimulated with lipopolysaccharide and in experimental glomerulonephritis. J. Biol. Chem. 270:1995;5418-5426.
11. Yoza B.K., Hu J.Y.Q., McCall C.E. Protein-tyrosine kinase activation is required for lipopolysaccharide induction of interleukin 1β and NFκB activation, but not NFκB nuclear translocation. J. Biol. Chem. 271:1996;18306-18309.
12. Han J., Lee J.-D., Bibbs L., Ulevitch R.J. A MAP kinase targeted by endotoxin and hyperosmolarity in mammalian cells. Science. 265:1994;808-811.
13. Lee J.C., Laydon J.T., McDonnell P.C., Gallagher T.F., Kumar S., Green D., McNulty D., Blumenthal M.J., Heys J.R., Landvatter S.W., Strickler J.E., McLaughlin M.M., Siemens I.R., Fisher S.M., Livi G.P., White J.R., Adams J.L., Young P.R. A protein kinase involved in the regulation of inflammatory cytokine biosynthesis. Nature. 372:1994;739-746.
14. Reimann T., Büscher D., Hipskind R.A., Krautwald S., Lohmann-Matthes M.-L., Baccarini M. Lipopolysaccharide induces activation of the Raf-1/MAP kinase pathway. J. Immunol. 153:1994;5740-5749.
15. Hambleton J., Weinstein S.L., Lem L., DeFranco A.L. Activation of c-Jun N-terminal kinase in bacterial lipopolysaccharide-stimulated macrophages. Proc. Natl. Acad. Sci. USA. 93:1996;2774-2778.
16. Sanghera J.S., Weinstein S.L., Aluwalia M., Girn J., Pelech S.L. Activation of multiple proline-directed kinases by bacterial lipopolysaccharide in murine macrophages. J. Immunol. 156:1996;4457-4465.
17. Muller J.M., Loms Ziegler-Heitbrock H.W., Baeuerle P.A. Nuclear factor kappa B, a mediator of lipopolysaccharide effects. Immunobiology. 187:1993;233-256.
18. Verma I.M., Stevenson J.K., Schwarz E.M., Van Antwerp D., Miyamoto S. Rel/NF-κB/IκB family: intimate tales of association and dissociation. Genes Dev. 9:1995;2723-2735.
19. Virca G.D., Kim S.Y., Glaser K.B., Ulevitch R.J. Lipopolysaccharide induced hyporesponsiveness to its own action in RAW264.7 cells. J. Biol. Chem. 264:1989;21951-21956.
20. Takasuka N., Tokunaga T., Akagawa K.S. Preexposure of macrophages to low doses of lipopolysaccharide inhibits the expression of tumor necrosis factor-α mRNA but not of IL-1β mRNA. J. Immunol. 146:1991;3824-3830.
21. Matsuura M., Kiso M., Hasegawa A., Nakano M. Multistep regulation mechanisms for tolerance induction to lipopolysaccharide lethality in the tumor-necrosis-factor-α-mediated pathway: application of non-toxic monosaccharide lipid A analogues for elucidation of mechanisms. Eur. J. Biochem. 221:1994;335-341.
22. West M.A., Bennet T., Seatter S.C., Clair L., Bellingham J. LPS pretreatment reprograms macrophage LPS-stimulated TNF and IL-1 release without protein tyrosine kinase activation. J. Leukocyte Biol. 61:1997;88-95.
23. Wright S.D., Ramos R.A., Tobias P.S., Ulevitch R.J., Mathison J.C. CD14, a receptor for complexes of lipopolysaccharide (LPS) and LPS-binding protein. Science. 249:1990;1431-1433.
24. Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162:1987;156-159.
25. J. Sambrook, E.F. Fritsch, T. Maniatis, Molecular Cloning: A Laboratory Manual, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, 1989.
26. Han J., Lee J.-D., Tobias P.S., Ulevitch R.J. Endotoxin induces rapid protein tyrosine phosphorylation in 70Z/3 cells expressing CD14. J. Biol. Chem. 268:1993;25009-25014.
27. Delude R.L., Fenton M.J., Savedra J.R., Perera P.-Y., Vogel S.N., Thieringer R., Golenbock D.T. CD14-mediated translocation of nuclear factor-κB induced by lipopolysaccharide does not require tyrosine kinase activity. J. Biol. Chem. 269:1994;22253-22260.
28. Libermann T.A., Baltimore D. Activation of interleukin-6 gene expression through the NF-κB transcription factor. Mol. Cell. Biol. 10:1990;2327-2334.
29. Ruff M.R., Gifford G.E. Tumor necrosis factor. Lymphokines. 2:1981;235-272.
30. Ulevitch R.J. The preparation and characterization of a radioiodinated bacterial lipopolysaccharide. Immunochemistry. 15:1978;157-164.
31. Ding A., Porteu F., Sanchez E., Nathan C.F. Shared actions of endotoxin and Taxol on TNF receptors and TNF release. Science. 248:1990;370-372.
32. Manthey C.L., Brandes M.E., Perera P.-Y., Vogel S.N. Taxol increases steady-state levels of lipopolysaccharide-inducible genes and protein-tyrosine phosphorylation in murine macrophages. J. Immunol. 149:1992;2459-2465.
33. Ding A., Sanchez E., Nathan C.F. Taxol shares the ability of bacterial lipopolysaccharide to induce tyrosine phosphorylation of microtubule-associated protein kinase. J. Immunol. 151:1993;5596-5602.
34. Dérijard B., Raingeaud J., Barrett T., Wu I.-H., Han J., Ulevitch R.J., Davis R.J. Independent human MAP kinase signal transduction pathways defined by MEK and MKK isoforms. Science. 267:1995;682-685.
35. Akira S., Isshiki H., Sugita T., Tanabe O., Kinoshita S., Nishio Y., Nakajima T., Hirana T., Kishimoto T. A nuclear factor for IL-6 expression (NF-IL6) is a member of a C/EBP family. EMBO J. 9:1990;1897-1906.
36. Nakajima T., Kinoshita S., Sasagawa T., Sasaki K., Naruto M., Kishimoto T., Akira S. Phosphorylation at threonine-235 by a ras-dependent mitogen-activated protein kinase cascade is essential for transcription factor NF-IL6. Proc. Natl. Acad. Sci. USA. 90:1993;2207-2211.
37. Zhang Y., Broser M., Rom W.N. Activation of the interleukin 6 gene by Mycobacterium tuberculosis or lipopolysaccharide is mediated by nuclear factors NF-IL6 and NF-κB. Proc. Natl. Acad. Sci. USA. 91:1994;2225-2229.
38. Han J., Jiang Y., Li Z., Kravchenko V.V., Ulevicth R.J. Activation of the transcription factor MEF2C by the MAP kinase p38 in inflammation. Nature. 386:1997;296-299.
39. Manthey C.L., Qureshi N., Stütz P.L., Vogel S.N. Lipopolysaccharide antagonists block taxol-induced signaling in murine macrophages. J. Exp. Med. 178:1993;695-702.
40. Perera P.-Y., Qureshi N., Vogel S.N. Paclitaxel (taxol)-induced NF-κB translocation in murine macrophages. Infect. Immun. 64:1996;878-884.
41. Ziegler-Heitbrock H.W.L., Wedel A., Schraut W., Ströbel M., Wendelgass P., Sternsdorf T., Bäuerle P.A., Haas J.G.R. Tolerance to lipopolysaccharide involves mobilization of nuclear factor κB with predominance of p50 homodimers. J. Biol. Chem. 269:1994;17001-17004.
42. Takasuka N., Matsuura K., Yamamoto S., Akagawa K.S. Suppression of TNF-α mRNA expression in LPS-primed macrophages occurs at the level of nuclear factor-kB activation, but not at the level of protein kinase C or CD14 expression. J. Immunol. 154:1995;4803-4812.
43. Qureshi N., Takayama K., Kurtz R. Diphosphoryl lipid A obtained from the nontoxic lipopolysaccharide of Rhodopseudomonas sphaeroides is an endotoxin antagonist in mice. Infect. Immun. 59:1991;441-444.
44. Henricson B.E., Perera P.-Y., Qureshi N., Takayama K., Vogel S.N. Rhodopseudomonas sphaeroides lipid A derivatives block in vitro induction of tumor necrosis factor and endotoxin tolerance by smooth lipopolysaccharide and monophosphoryl lipid A. Infect. Immun. 60:1992;4285-4290.
45. Kirikae F., Kirikae T., Qureshi N., Takayama K., Morrison D.C., Nakano M. CD14 is not involved in Rhodobactor spheroides diphosphoryl lipid A inhibition of tumor necrosis factor alpha and nitric oxide induction by taxol in murine macrophages. Infect. Immun. 63:1995;486-497.