Abstract
Preculture of thioglycollate-elicited C3HeB/FeJ mouse peritoneal macrophages in vitro with subthreshold stimulatory concentrations of lipopolysaccharide (LPS) can induce hyporesponsiveness (desensitization) to both tumor necrosis factor alpha (TNF-alpha) and nitric oxide (NO) production when these cells are subsequently stimulated with 100 ng/ml of LPS. We have established, however, that the primary dose of LPS required for inducing downregulation of NO production is significantly lower than that required for inducing downregulation of TNF-alpha production. Further, when LPS-pretreated macrophages become refractory to subsequent LPS stimulation for NO production, the secondary LPS-stimulated TNF-alpha production is markedly enhanced, and vice versa. These results indicate that LPS-induced TNF-alpha and NO production by macrophages are differentially regulated, and that the observed desensitization process may not reflect a state in which macrophages are totally refractory to subsequent LPS stimulation. Rather, our data suggest that LPS-pretreated macrophages become selectively primed for differential responses to LPS. The LPS-induced selective priming effects are not restricted to LPS stimulation, but extend as well to stimuli such as zymosan, Staphylococcus aureus, and heat-killed Listeria monocytogenes.
MeSH Terms
Animals
Escherichia coli
Female
In Vitro Techniques
Lipopolysaccharides/administration & dosage
Macrophage Activation
Macrophages/physiology
Mice
Mice, Inbred C3H
Nitric Oxide/metabolism
Peritoneal Cavity/cytology
Tumor Necrosis Factor-alpha/biosynthesis
Chemicals
Lipopolysaccharides
Tumor Necrosis Factor-alpha
Nitric Oxide
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Zhang X
Department of Microbiology, Molecular Genetics, and Immunology, University of Kansas Medical Center, Kansas City 66160.
Morrison D C
References (18)
18 references, click to expand
-
Fractions of lipopolysaccharide from Escherichia coli O111:B4 prepared by two extraction procedures.
J Biol Chem. 1975 Apr 25;250(8):2911-19
PMID: 804483
-
Purification and physico-chemical characterization of rabbit tumor necrosis factor.
J Immunol. 1980 Oct;125(4):1671-7
PMID: 6997383
-
Rapid colorimetric assay for cell growth and survival. Modifications to the tetrazolium dye procedure giving improved sensitivity and reliability.
J Immunol Methods. 1986 May 22;89(2):271-7
PMID: 3486233
-
Homologous and heterologous desensitization of proto-oncogene cfos expression in murine peritoneal macrophages.
J Cell Physiol. 1987 Apr;131(1):36-42
PMID: 3571335
-
Human pro-IL-1 beta gene expression in monocytic cells is regulated by two distinct pathways.
J Immunol. 1988 Apr 1;140(7):2267-73
PMID: 3258333
-
Induction of tolerance to lipopolysaccharide (LPS)-D-galactosamine lethality by pretreatment with LPS is mediated by macrophages.
Infect Immun. 1988 May;56(5):1352-7
PMID: 3356468
-
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 Oct 1;141(7):2407-12
PMID: 3139757
-
Interferon-gamma and tumor necrosis factor induce the L-arginine-dependent cytotoxic effector mechanism in murine macrophages.
Eur J Immunol. 1988 Oct;18(10):1587-92
PMID: 3142779
-
Nitric oxide. A macrophage product responsible for cytostasis and respiratory inhibition in tumor target cells.
J Exp Med. 1989 May 1;169(5):1543-55
PMID: 2497225
-
Lipopolysaccharide induces hyporesponsiveness to its own action in RAW 264.7 cells.
J Biol Chem. 1989 Dec 25;264(36):21951-6
PMID: 2480960
-
Adaptation to bacterial lipopolysaccharide controls lipopolysaccharide-induced tumor necrosis factor production in rabbit macrophages.
J Clin Invest. 1990 Apr;85(4):1108-18
PMID: 2318968
-
Regulation of tumor necrosis factor alpha transcription in macrophages: involvement of four kappa B-like motifs and of constitutive and inducible forms of NF-kappa B.
Mol Cell Biol. 1990 Apr;10(4):1498-506
PMID: 2181276
-
Molecular mechanisms in down-regulation of tumor necrosis factor expression.
Proc Natl Acad Sci U S A. 1990 Dec;87(24):9563-7
PMID: 2263611
-
Preexposure of macrophages to low doses of lipopolysaccharide inhibits the expression of tumor necrosis factor-alpha mRNA but not of IL-1 beta mRNA.
J Immunol. 1991 Jun 1;146(11):3824-30
PMID: 1903414
-
Nitric oxide: physiology, pathophysiology, and pharmacology.
Pharmacol Rev. 1991 Jun;43(2):109-42
PMID: 1852778
-
Activation by bacterial lipopolysaccharide causes changes in the cytosolic free calcium concentration in single peritoneal macrophages.
J Immunol. 1991 Aug 1;147(3):980-3
PMID: 1907309
-
Functional consequences of engagement of the T cell receptor by low affinity ligands.
J Immunol. 1993 Jan 1;150(1):1-7
PMID: 8417115
-
Tumor necrosis factor.
Sci Am. 1988 May;258(5):59-60, 69-75
PMID: 3051354