Cited by 1,442Immune Response and InflammationSepsis Diagnosis and TreatmentInflammation biomarkers and pathways

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Receptor-Dependent Mechanisms of Cell Stimulation by Bacterial Endotoxin

Ulevitch, R J, Tobias, P S·1995·Annual Review of Immunology

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Abstract

In humans and experimental animals the presence of bacterial lipopolysaccharide (endotoxin, LPS) signals the presence of gram-negative bacteria. Recognition of LPS triggers gene induction by myeloid and nonmyeloid lineage cells. These inducible genes encode proteins that include cytokines, adhesive proteins, and enzymes that produce low molecular weight proinflammatory mediators. Together the products of these inducible genes upregulate host defense systems that participate in eliminating the bacterial infection. Unfortunately, these same mediators contribute to a serious human disease known as septic shock. Considerable progress has been made during the past decade in determining the sources, identities, and sequence of release of these mediators. In contrast, until recently, marked gaps in our knowledge existed regarding the identity of the LPS receptor and intracellular signaling pathways responsible for LPS-induced cell activation. The discovery in 1986 of a plasma protein termed LPS binding protein (LBP) led to the discovery of unanticipated mechanisms of LPS-induced cell activation. CD14 was found as a soluble serum protein or as a glycosylphosphatidylinositol (GPI)-anchored protein of myeloid lineage cells; it now occupies a key role in LPS-induced cell activation as we understand it today. Here we discuss how LBP enables LPS binding to CD14 and how complexes of LPS and soluble or GPI-anchored CD14 participate in cell activation. We also review the evidence supporting a model for a functional LPS receptor of myeloid cells, which is multimeric, comprised of GPI-anchored CD14 and a presently unidentified transmembrane protein that together bind LPS and initiate cell activation via kinase cascades.

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Protective effect of resveratrol against LPS-induced extracellular lipoperoxidation in AR42J cells partly via a Myd88-dependent signaling pathway
Sebaï, H., Ristorcelli, E., Sbarra, V., Hovsépian, S., Fayet, G., Aouani, E., & Lombardo, D. (2009) · Archives of Biochemistry and Biophysics · doi:10.1016/j.abb.2009.12.019 · Cited by 26
Roles of Endotoxin-related Signaling Molecules in the Progression of Acute Necrotizing Pancreatitis in Mice
Wang, X., Wu, L.-Y., Wu, K., Zhang, R., & Dong, Y. (2005) · Pancreas · doi:10.1097/01.mpa.0000175179.62916.17 · Cited by 26
“Among them, the roles of LPS binding protein (LBP) and CD14, which are endotoxin-related signaling molecules, have been established.(8) LBP is a 60-kd serum glycoprotein synthesized in the liver and several extrahepatic sites.”
Background
Regulation of the growth hormone and luteinizing hormone response to endotoxin in sheep
Daniel, J. A., Whitlock, B. K., Wagner, C. G., & Sartin, J. L. (2002) · Domestic Animal Endocrinology · doi:10.1016/s0739-7240(02)00171-6 · Cited by 26
Lipopolysaccharide-triggered desensitization of TNF-α mRNA expression involves lack of phosphorylation of IκBα in a murine macrophage-like cell line, P388D1
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“Thus, CD14 and LBP are regarded as one of the components of an LPS receptor complex [16, 33].”
Background
Temporal, regional, and cell-specific changes of iNOS expression after intrastriatal microinjection of interferon gamma and bacterial lipopolysaccharide
Heneka, M. T., Dumitrescu, L., Löschmann, P., Wüllner, U., & Klockgether, T. (2000) · Journal of Chemical Neuroanatomy · doi:10.1016/s0891-0618(00)00041-7 · Cited by 26
Review: Chlamydial lipopolysaccharide
Brade, H., Brabetz, W., Brade, L., Hoist, O., Löbau, S., Lucakova, M., Mamat, U., Różalski, A., Zych, K., & Kosma, P. (1997) · Journal of Endotoxin Research · doi:10.1177/096805199700400108 · Cited by 26
A systematic review of CD14 and toll-like receptors in relation to asthma in Caucasian children
Klaassen, E. M. M., Thönissen, B. E., van Eys, G. J. J. M., Dompeling, E., & Jöbsis, Q. (2013) · Allergy Asthma and Clinical Immunology · doi:10.1186/1710-1492-9-10 · Cited by 25
“It is expressed on the surface of monocytes, macrophages, and neutrophils and occurs as a membrane-bound form and a soluble form [17,18].”
Background
The gut reaction to couples’ relationship troubles: A route to gut dysbiosis through changes in depressive symptoms
Kiecolt‐Glaser, J. K., Wilson, S. J., Shrout, M. R., Madison, A. A., Andridge, R., Peng, J., Malarkey, W. B., & Bailey, M. T. (2021) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2021.105132 · Cited by 25
“LBP binds LPS and presents LPS to CD14, the receptor for LPS-LBP complexes (Stehle et al., 2012; Ulevitch and Tobias, 1995; Wright et al., 1990).”
Background
Single-dose versus short-course prophylactic antibiotics for peroral endoscopic myotomy: a randomized controlled trial
Maselli, R., Oliva, A., Badalamenti, M., Galtieri, P. A., Belletrutti, P. J., Spadaccini, M., Nicoletti, R., Finati, E., Vetrano, S., Fosso, F., et al. (2021) · Gastrointestinal Endoscopy · doi:10.1016/j.gie.2021.05.045 · Cited by 25
Erlotinib protests against LPS-induced parthanatos through inhibiting macrophage surface TLR4 expression
Xue, Q., Liu, X., Chen, C., Zhang, X., Xie, P., Liu, Y., Zhou, S.-N., & Tang, J. Y. (2021) · Cell Death Discovery · doi:10.1038/s41420-021-00571-4 · Cited by 26
“Recent studies have revealed that TLR4 alone is not sufficient for an overall innate immune response and requires coordination through CD14 and MD2 [16, 17].”
Background
Association between CD14 Gene Polymorphisms and Cancer Risk: A Meta-Analysis
Wang, J., Guo, X., Yu, S., Song, J., Zhang, J., Cao, Z., Wang, J., Liu, M., & Dong, W. (2014) · PLoS ONE · doi:10.1371/journal.pone.0100122 · Cited by 25
“CD14 is expressed on the surface of monocytes, macrophages, and neutrophils as membrane CD14 (mCD14) and in the serum as soluble CD14 (sCD14) and its expression may be partially regulated at the genetic level [7,8].”
Background
Local Expression of Interleukin‐10 and mCD14 in Relation to the −1087 IL‐10 and −159 CD14 Gene Polymorphisms in Chronic Periodontitis
Donati, M., Liljenberg, B., Padyukov, L., & Berglundh, T. (2008) · Journal of Periodontology · doi:10.1902/jop.2008.070299 · Cited by 25
Apoptosis signal-regulating kinase 1 in peptidoglycan-induced COX-2 expression in macrophages
Hsu, M., Chang, C.-K., Chen, M.-C., Chen, B.-C., Ma, H., Hong, C.-Y., & Lin, C. (2010) · Journal of Leukocyte Biology · doi:10.1189/jlb.1009668 · Cited by 25
“PGN, the main cell-wall component of gram-positive bacteria, is composed of alternating N-acetyl glycosamine and N-acetyl muramic acid long sugar chains that are interlinked by peptide bridges, resulting in a large, complex macromolecular structure [2, 3].”
Background
Association of CD14 G(-1145)A and C(-159)T polymorphisms with reduced risk for tuberculosis in a Chinese Han population
Zhao, M. Y., Xue, Y., Zhao, Z., Li, F. J., Fan, D. P., Wei, L., Sun, X. J., Zhang, X., Wang, X. C., Zhang, Y. X., et al. (2012) · Genetics and Molecular Research · doi:10.4238/2012.september.25.11 · Cited by 25
“CD14 is constitutively expressed primarily on the surface of monocytes, macrophages, and neutrophils as membrane CD14 (mCD14) (Ulevitch and Tobias, 1995).”
Background
A novel toll-like receptor from the pearl oyster Pinctada fucata martensii is induced in response to stress
Wu, Y., Liang, H., Wang, Z., Lei, Q., & Xia, L. (2017) · Comparative Biochemistry and Physiology Part B Biochemistry and Molecular Biology · doi:10.1016/j.cbpb.2017.08.006 · Cited by 25
Terminalia bellirica (Gaertn.) Roxb fruit exerts anti-inflammatory effect via regulating arachidonic acid pathway and pro-inflammatory cytokines in lipopolysaccharide-induced RAW 264.7 macrophages
Jayesh, K., Karishma, R., Vysakh, A., Gopika, P., & Latha, M. S. (2018) · Inflammopharmacology · doi:10.1007/s10787-018-0513-x · Cited by 25
Robustaflavone Isolated from Nandina domestica Using Bioactivity-Guided Fractionation Downregulates Inflammatory Mediators
Jo, A., Yoo, H. J., & Lee, M. (2019) · Molecules · doi:10.3390/molecules24091789 · Cited by 25
“The data showed that R is involved in the inhibition of pERK1/2 in RAW 264.7 cells (Figure 7B).”
BackgroundInfluential
Peptidoglycan recognition protein 3 (PglyRP3) has an anti-inflammatory role in intestinal epithelial cells
Zenhom, M., Hyder, A., de Vrese, M., Heller, K. J., Roeder, T., & Schrezenmeir, J. (2011) · Immunobiology · doi:10.1016/j.imbio.2011.10.013 · Cited by 25
“the various signs and symptoms that occur during bacterial infections, including fever, inflammation, and acute phase responses (Dziarski et al. 2000; Ulevitch and Tobias 1995).”
Background
A synthetic cyclic peptide derived from Limulus anti-lipopolysaccharide factor neutralizes endotoxin in vitro and in vivo
Ren, J., Gu, J., Gao, H.-F., Xia, P., & Xiao, G. (2008) · International Immunopharmacology · doi:10.1016/j.intimp.2008.01.015 · Cited by 25
Rapid induction of apoptosis in B‐cell lymphoma by functionally isolated human antibodies
Fransson, J., Tornberg, U., Borrebaeck, C. A. K., Carlsson, R. N. K., & Frendéus, B. (2006) · International Journal of Cancer · doi:10.1002/ijc.21829 · Cited by 25
Geldanamycin Interferes with the 90-kDa Heat Shock Protein, Affecting Lipopolysaccharide-Mediated Interleukin-1 Expression and Apoptosis within Macrophages
Hsu, H.-Y., Wu, H.-L., Tan, S.-K., Li, V. P.-H., Wang, W.-T., Hsu, J., & Cheng, C.-H. (2006) · Molecular Pharmacology · doi:10.1124/mol.106.024240 · Cited by 25
N-formyl-methionyl-leucyl-phenylalanine (fMLP) inhibits tumour necrosis factor-alpha (TNF-α) production on lipopolysaccharide (LPS)-stimulated human neutrophils
Vulcano, M., Rosa, M., Minnucci, F. S., Cherñavsky, A. C., & Isturiz, M. A. (1998) · Clinical & Experimental Immunology · doi:10.1046/j.1365-2249.1998.00631.x · Cited by 25
Endotoxin Stimulates Liver Macrophages To Release Mediators That Inhibit an Early Step in Hepadnavirus Replication
Klöcker, U., Schultz, U., Schaller, H., & Protzer, U. (2000) · Journal of Virology · doi:10.1128/jvi.74.12.5525-5533.2000 · Cited by 28
Presepsin: solving a soluble (CD14) problem in sepsis?
Ackland, G. L., & Prowle, J. R. (2015) · Intensive Care Medicine · doi:10.1007/s00134-014-3642-8 · Cited by 25
“(TLR) 2 and TLR-4 trans-membrane signalling, both at the cell surface and within the endosomal compartment [8].”
Background
Application of Acute Phase Proteins for Monitoring Inflammatory States in Cattle
Burim, N., Hosseini, A., John, F., Iqbal, S., Sharma, S., Deng, Q., Tran, H., Farooq, U., Zebeli, Q., & Suzanna, M. (2011) · InTech eBooks · doi:10.5772/19492 · Cited by 25
Effect of Cannabis sativa on oxidative stress and organ damage after systemic endotoxin administration in mice
Abdel‐Salam, O. M. E., Nada, S. A., Salem, N. A., El-Shamarka, M. E.-S., & Omara, E. A. A. (2013) · Comparative Clinical Pathology · doi:10.1007/s00580-013-1745-1 · Cited by 24
“Lipopolysaccharide (LPS), a product of the Gramnegative bacterial cell wall, potently stimulates the innate immune system, eliciting both pro- and anti-inflammatory responses (Ulevitch and Tobias 1995; Heine et al. 2001).”
Background
Pro-inflammatory genetic background and zinc status in old atherosclerotic subjects
Giacconi, R., Caruso, C., Malavolta, M., Lio, D., Balistreri, C. R., Scola, L., Candore, G., Muti, E., & Mocchegiani, E. (2008) · Ageing Research Reviews · doi:10.1016/j.arr.2008.06.001 · Cited by 24
“CD14 (mCD14) is a 55 kDa glycoprotein localised on the surface of monocytes/macrophages and neutrophils (Ulevitch and Tobias, 1995), which exerts a central role in pro-inflammatory signalling in response to a variety of ligands, like LPS and bacterial products (Heumann et al., 1998).”
Association of Endotoxemia and Production of Antibodies against Endotoxins after Multiple Injuries
Buttenschoen, K., Berger, D., Strecker, W., Buttenschoen, D. C., Stenzel, K., Pieper, T., & Beger, H. G. (2000) · The Journal of Trauma: Injury, Infection, and Critical Care · doi:10.1097/00005373-200005000-00017 · Cited by 24
Involvement of Kupffer cells in lipopolysaccharide-induced rapid accumulation of platelets in the liver and the ensuing anaphylaxis-like shock in mice
Yamaguchi, K., Yu, Z., Kumamoto, H., Sugawara, Y., Kawamura, H., Takada, H., Yokochi, T., Sugawara, S., & Endo, Y. (2006) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2005.11.010 · Cited by 24
“Lipopolysaccharide (LPS) is a constituent of the cell wall of gram-negative bacteria with the potential to induce various nonspecific immune responses [5,6].”
Background
Essential role of MD-2 in B-cell responses to lipopolysaccharide and Toll-like receptor 4 distribution
Miyake, K., Nagai, Y., Akashi, S., Nagafuku, M., Ogata, M., & Kosugi, A. (2002) · Journal of Endotoxin Research · doi:10.1179/096805102125001055 · Cited by 24
Induction of nitric oxide synthase in raw 264.7 macrophages by lipoteichoic acid fromStaphylococcus aureus: Involvement of protein kinase C- and nuclear factor-kB-dependent mechanisms
Kuo, C., Chiang, L.-L., Lee, C.-N., Yu, M.-C., Bai, K., Lee, H.-M., Lee, W., Sheu, J., & Lin, C. (2003) · Journal of Biomedical Science · doi:10.1007/bf02256005 · Cited by 24
“Moreover, a transmembrane co-receptor (signaltransducing receptor) for CD 14 has been postulated [ 31 ]. Recently, toll-like receptor 2 (TLR2) and TLR4 have been identified as the signal-transducing receptors for LTA and LPS, respectively [27, 28].”
Background
Inhibition of LPS-induced activation of alveolar macrophages by high concentrations of LPS-binding protein
Hamann, L., Stamme, C., Ulmer, A. J., & Schumann, R. R. (2002) · Biochemical and Biophysical Research Communications · doi:10.1016/s0006-291x(02)00710-6 · Cited by 24
“Lipopolysaccaride (LPS), the major cell wall component of Gram-negative bacteria, is a strong activator of the innate immune system triggering the release of various proinflammatory mediators, among them cytokines such as TNF-a, IL-1b, and IL-6 [1–3].”
Background
N-Linked Glycosylation at Asn3and the Positively Charged Residues within the Amino-Terminal Domain of the C1 Inhibitor Are Required for Interaction of the C1 Inhibitor withSalmonella entericaSerovar Typhimurium Lipopolysaccharide and Lipid A
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“the hydrophilic repeating polysaccharide of the core and Oantigen structures and the hydrophobic LPA domain (56).”
Background
Acylation of lysophosphatidylcholine plays a key role in the response of monocytes to lipopolysaccharide
Schmid, B., Finnen, M. J., Harwood, J. L., & Jackson, S. K. (2003) · European Journal of Biochemistry · doi:10.1046/j.1432-1033.2003.03649.x · Cited by 24
Lipopolysaccharide-Mimetic Activities of a Toll-Like Receptor 2-Stimulatory Substance(s) in Enterobacterial Lipopolysaccharide Preparations
Muroi, M., Ohnishi, T., Azumi, S., & Tanamoto, K. (2003) · Infection and Immunity · doi:10.1128/iai.71.6.3221-3226.2003 · Cited by 24
“Bacterial lipopolysaccharide (LPS) is a constituent of the outer membrane of the cell wall in gram-negative bacteria and plays a major role in septic shock in humans (32, 41).”
Background
Effects of acetylcholine on an animal model of inflammation
Silva-Herdade, A. S., & Saldanha, C. (2013) · Clinical Hemorheology and Microcirculation · doi:10.3233/ch-121646 · Cited by 23
“agent and plays a primary role in bacterial-induced leukocyte recruitment [8, 9, 11, 30].”
Polymorphisms in the promoter of the CD14 gene and their associations with susceptibility to pulmonary tuberculosis
Xue, Y., Zhao, Z., Chen, F., Zhang, L., Li, G. D., W., K., Bai, X. F., & Zuo, Y. J. (2012) · Tissue Antigens · doi:10.1111/j.1399-0039.2012.01958.x · Cited by 23
MAPK phosphatase-1 contributes to trichostatin A inhibition of cyclooxygenase-2 expression in human umbilical vascular endothelial cells exposed to lipopolysaccharide
Hsu, Y.-F., Sheu, J., Lin, C., Chen, W.-C., Hsiao, G., Ou, G., Chiu, P.-T., & Hsu, M. (2011) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/j.bbagen.2011.08.015 · Cited by 22
α-Dihydroxychalcone-glycoside (α-DHC) isolated from the heartwood of Pterocarpus marsupium inhibits LPS induced MAPK activation and up regulates HO-1 expression in murine RAW 264.7 macrophage
Chakraborty, P., Saraswat, G., & Kabir, S. N. (2014) · Toxicology and Applied Pharmacology · doi:10.1016/j.taap.2014.03.011 · Cited by 23

Authors: Ulevitch, R. J., & Tobias, P. S.
Affiliations: Scripps Research Institute (US)
ORCID: Ulevitch, R J
Venue: Annual Review of Immunology
Publisher: Annual Reviews
Published: 1995-04
Volume: 13
Issue: 1
Pages: 437-457
ISSN: 0732-0582 (ISSN-L)
1545-3278
DOI: 10.1146/annurev.iy.13.040195.002253
OpenAlex: W2113828544
Cited by: 1,442
References: 36
Citations by year: 2026: 4 · 2025: 11 · 2024: 8 · 2023: 11 · 2022: 13 · 2021: 25 · 2020: 23 · 2019: 21 · 2018: 22 · 2017: 24 · 2016: 37 · 2015: 29 · 2014: 39 · 2013: 43 · 2012: 38
FWCI: 20.96
Type: journal article
Language: en
Open access: closed
Locations: Annual Review of Immunology (publishedVersion)
PubMed (publishedVersion)
Funders: National Institute of General Medical Sciences (GM28485, GM3769)
National Institute of Allergy and Infectious Diseases (AI 15136, R01AI015136)
Topics: Life Sciences › Immunology and Microbiology › Immunology › Immune Response and Inflammation
Health Sciences › Medicine › Critical Care and Intensive Care Medicine › Sepsis Diagnosis and Treatment
Life Sciences › Immunology and Microbiology › Immunology › Inflammation biomarkers and pathways
Keywords: lipopolysaccharide, endotoxin, LPS receptor, CD14, LPS-binding protein, septic shock, myeloid cells, intracellular signaling, transmembrane proteins, pro-inflammatory mediators
MeSH terms: Lipopolysaccharide-Binding Protein, Acute-Phase Proteins, Amino Acid Sequence, Animals, Carbohydrate Sequence, Carrier Proteins, Humans, Lipopolysaccharides, Membrane Glycoproteins, Models, Biological, Molecular Sequence Data, Receptors, Immunologic, Shock, Septic, Antigens, Differentiation, Myelomonocytic, Molecular Structure, Signal Transduction, Antigens, CD, Calcium-Calmodulin-Dependent Protein Kinases, Lipopolysaccharide Receptors

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Receptor-Dependent Mechanisms of Cell Stimulation by Bacterial Endotoxin

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