Cited by 519Immune Response and InflammationNF-κB Signaling PathwaysInflammasome and immune disorders

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Lipopolysaccharide-mediated Reactive Oxygen Species and Signal Transduction in the Regulation of Interleukin-1 Gene Expression

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Hsu, Hsien-Yeh, Wen, Meng-Hsuan·2002·Journal of Biological Chemistry

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Abstract

Lipopolysaccharide (LPS) stimulates macrophages to release inflammatory cytokines, interleukin-1 beta (IL-1), and tumor necrosis factor (TNF). LPS-induced TNF suppresses scavenger receptor functions in macrophages (van Lenten, B. J., and Fogelman, A. M. (1992) J. Immunol. 148, 112-116), which is regulated by TNF-mediated protein kinases (Hsu, H. Y., and Twu, Y. C. (2000) J. Biol. Chem. 275, 41035-41048). To examine the molecular mechanism for LPS induction of IL-1 in macrophages, we demonstrated that LPS quickly stimulated reactive oxygen species (ROS), and 3 h later induced prointerleukin-1 beta (pro-IL-1, precursor of IL-1) production and IL-1 secretion. LPS stimulated pro-IL-1 message/protein between 3 and 10 h; however, there was a 40% reduction of pro-IL-1 in preincubation of the antioxidant, N-acetylcysteine (NAC). Moreover, NAC moderated LPS-induced IL-1 secretion partially via interleukin 1-converting enzyme. The maximal activity of LPS-induced ERK, JNK, and p38 was 12- (30 min), 5- (30 min), and 16-fold (15 min), respectively. In contrast, NAC reduced ERK activity to 60% and decreased p38 activity to the basal level, but JNK activity was induced 2-fold. Furthermore, the pharmacological antagonists LY294002, SB203580, curcumin, calphostin C, and PD98059 revealed the diverse roles of LPS-mediated protein kinases in pro-IL-1. On the other hand, NAC and diphenyleneiodonium chloride partially inhibited LPS-induced Rac activity and protein-tyrosine kinase (PTK), indicating that LPS-mediated ROS and NADPH oxidase correspond to Rac activation and IL-1 expression. Our findings establish for the first time that LPS-mediated PTK/phosphatidylinositol 3-kinase/Rac/p38 pathways play a more important role than pathways of PTK/PKC/MEK/ERK and of PTK/phosphatidylinositol 3-kinase/Rac/JNK in the regulation of pro-IL-1/IL-1. The findings also further elucidate the critical role of LPS-mediated ROS in signal transduction pathways. Our results suggest that understanding LPS-transduced signals in IL-1 induction upon the antibacterial action of macrophages should provide a therapeutic strategy for aberrant inflammatory responses leading to severe cellular injury or concurrent multiorgan septic damage.

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Background
Janus kinase 2 is involved in lipopolysaccharide-induced activation of macrophages
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Protective Role of Ternatin Anthocyanins and Quercetin Glycosides from Butterfly Pea (Clitoria ternatea Leguminosae) Blue Flower Petals against Lipopolysaccharide (LPS)-Induced Inflammation in Macrophage Cells
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“This was stimulated by LPS treatment in RAW 264.7 cells as previously described (Hsu and Wen, 2002) and free radical production was analyzed using DCF-DA.”
MethodInfluential
Positive Role of CCAAT/Enhancer-Binding Protein Homologous Protein, a Transcription Factor Involved in the Endoplasmic Reticulum Stress Response in the Development of Colitis
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“Treatment of WT macrophages with LPS stimulated ROS production (Figure 8C), as has been described previously.(46) However, this stimulation was not clearly observed in CHOPnull macrophages, indicating that CHOP is responsible for LPS-stimulated ROS production (Figure 8C).”
Method
Multifunctional hydrogels based on chitosan, hyaluronic acid and other biological macromolecules for the treatment of inflammatory bowel disease: A review
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Early Growth Response-1 Transcription Factor Is Essential for Ethanol-Induced Fatty Liver Injury in Mice
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“The signaling pathways by which this occurs are not completely known, but may include extracellular signal-related kinase and p38 (45) or NF- B, activator protein–1, and cyclic adenosine monophosphate response element binding protein (47).”
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5-Aminoimidazole-4-carboxamide riboside suppresses lipopolysaccharide-induced TNF-α production through inhibition of phosphatidylinositol 3-kinase/Akt activation in RAW 264.7 murine macrophages
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“These classical MAPKs, extracellular signal regulated kinase (ERKs), p38 MAPK, and c-Jun NH2-terminal kinase (JNKs) have been implicated in the transcriptional regulation of inflammatory genes (Herlaar and Brown, 1999).”
Influential
Lipopolysaccharide/adenosine triphosphate induces IL-1β and IL-18 secretion through the NLRP3 inflammasome in RAW264.7 murine macrophage cells
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“The NLRP3 inflammasome is activated in response to a variety of signals that include pathogen-associated molecular patterns (PAMPs) or danger-associated molecular patterns (DAMPs) (6).”
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PI3K and ERK-Induced Rac1 Activation Mediates Hypoxia-Induced HIF-1α Expression in MCF-7 Breast Cancer Cells
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“Their ability to suppress pro-inflammatory mediators, such as IL-1b, TNF-a and IL-6, has also been well documented in the cells of the monocyte–macrophage lineage (15,16,36).”
Anti-Inflammatory Bioactivities of Honokiol through Inhibition of Protein Kinase C, Mitogen-Activated Protein Kinase, and the NF-κB Pathway To Reduce LPS-Induced TNFα and NO Expression
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QTL for white spot syndrome virus resistance and the sex-determining locus in the Indian black tiger shrimp (Penaeus monodon)
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Poly-quercetin-based nanoVelcro as a multifunctional wound dressing for effective treatment of chronic wound infections
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Endotoxin Induces Toll-Like Receptor 4 Expression in Vascular Smooth Muscle Cells via NADPH Oxidase Activation and Mitogen-Activated Protein Kinase Signaling Pathways
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Germling fusion via conidial anastomosis tubes in the grey mould Botrytis cinerea requires NADPH oxidase activity
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Authors: Hsu, H.-Y., & Wen, M.-H.
Affiliations: National Yang Ming University (TW)
Corresponding author: Hsu, Hsien-Yeh
ORCID: Wen, Meng-Hsuan
Venue: Journal of Biological Chemistry
Publisher: Elsevier BV
Published: 2002-06
Volume: 277
Issue: 25
Pages: 22131-22139
ISSN: 0021-9258 (ISSN-L)
DOI: 10.1074/jbc.m111883200
OpenAlex: W2016146035
Cited by: 519
References: 72
Citations by year: 2026: 13 · 2025: 17 · 2024: 20 · 2023: 21 · 2022: 21 · 2021: 27 · 2020: 22 · 2019: 23 · 2018: 25 · 2017: 33 · 2016: 27 · 2015: 21 · 2014: 18 · 2013: 19 · 2012: 14
FWCI: 7.22
Type: journal article
Language: en
Open access: hybrid
doi.org
Licence: cc-by
www.elsevier.com/tdm/userlicense/1.0/ (tdm)
creativecommons.org/licenses/by/4.0/ (vor, 6719 d)
Locations: Journal of Biological Chemistry (publishedVersion, cc-by)
PubMed (publishedVersion)
Topics: Life Sciences › Immunology and Microbiology › Immunology › Immune Response and Inflammation
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › NF-κB Signaling Pathways
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Inflammasome and immune disorders
Keywords: lipopolysaccharide, IL-1β, reactive oxygen species, N-acetylcysteine, macrophages, Rac, p38 MAPK, JNK, ERK, phosphatidylinositol 3-kinase, tyrosine kinase, NADPH oxidase, signal transduction, inflammatory cytokines, TNF-α
MeSH terms: Animals, Carrier Proteins, Cell Line, Chromones, Curcumin, Enzyme Activation, Enzyme Inhibitors, Enzyme-Linked Immunosorbent Assay, Flavonoids, Gene Expression Regulation, Genes, Dominant, Imidazoles, Interleukin-1, Lipopolysaccharides, Macrophages, Models, Biological, Morpholines, Naphthalenes, Oxygen, Protein Binding, Pyridines, Time Factors, Transfection, Signal Transduction, Reactive Oxygen Species, rac1 GTP-Binding Protein, Mitogen-Activated Protein Kinases, Mitogen-Activated Protein Kinase Kinases, Intracellular Signaling Peptides and Proteins, JNK Mitogen-Activated Protein Kinases, p38 Mitogen-Activated Protein Kinases, MAP Kinase Kinase 4, Mice

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Lipopolysaccharide-mediated Reactive Oxygen Species and Signal Transduction in the Regulation of Interleukin-1 Gene Expression

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