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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Background
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Background
Potent CD14-mediated signalling of human leukocytes by Escherichia coli can be mediated by interaction of whole bacteria and host cells without extensive prior release of endotoxin
Katz, S. S., Chen, K., Chen, S., Doerfler, M. E., Elsbach, P., & Weiss, J. P. (1996) · Infection and Immunity · doi:10.1128/iai.64.9.3592-3600.1996 · Cited by 34
Induction of IgG3 to LPS via Toll-Like Receptor 4 Co-Stimulation
Quintana, F. J., Solomon, A., Cohen, I. R., & Nussbaum, G. (2008) · PLoS ONE · doi:10.1371/journal.pone.0003509 · Cited by 33
“In vitro, aIgM does not induce isotype switching to IgG3 whereas LPS is a mitogenic signal that does induce switching to IgG3, but at relatively high concentrations (Figure S2 and ([28]).”
Background
Porphyromonas gingivalis lipopolysaccharide rapidly activates trigeminal sensory neurons and may contribute to pulpal pain
Kaewpitak, A., Bauer, C. S., Seward, E. P., Boissonade, F. M., & Douglas, C. W. I. (2020) · International Endodontic Journal · doi:10.1111/iej.13282 · Cited by 33
“With supraphysiological LPS concentrations, LPS signalling could occur via CD14-independent mechanisms (Ulevitch & Tobias 1995) and so the mechanisms revealed in this study may not completely represent the canonical pathway of TLR4–LPS interaction.”
Background
Intravenous administration of LPS activates the kynurenine pathway in healthy male human subjects: a prospective placebo-controlled cross-over trial
Millischer, V., Heinzl, M. W., Faka, A., Resl, M., Trepci, A., Klammer, C., Egger, M., Dieplinger, B., Clodi, M., & Schwieler, L. (2021) · Journal of Neuroinflammation · doi:10.1186/s12974-021-02196-x · Cited by 36
“tokines in a dose-dependent manner [1, 2].”
The roles of TNFR1 in lipopolysaccharide‐induced bone loss: Dual effects of TNFR1 on bone metabolism via osteoclastogenesis and osteoblast survival
Ochi, H., Hara, Y., Tagawa, M., Shinomiya, K., & Asou, Y. (2009) · Journal of Orthopaedic Research · doi:10.1002/jor.21028 · Cited by 33
“Lipopolysaccharide (LPS), a major constituent of Gram-negative bacteria, is one of the molecular factors plays a major role in bone resorption in periodontitis or ostemyelitis 1 by stimulating the the production of proinflammatory cytokines.(3,4) LPS stimulates synthesis of tumor necrosis factor-a (TNF-a), via NF-kB a…”
Background
S-adenosylmethionine prevents the up regulation of Toll-like receptor (TLR) signaling caused by chronic ethanol feeding in rats
Oliva, J., Bardag‐Gorce, F., Li, J., French, B. A., & French, S. W. (2011) · Experimental and Molecular Pathology · doi:10.1016/j.yexmp.2011.01.005 · Cited by 33
“LPS is transferred to CD14 by a lipid transferase LPS-binding protein (Ulevitch and Tobias, 1995).”
Therapeutic approach to regulate innate immune response by Toll‐like receptor 4 antagonist E5564 in rats with D‐galactosamine‐induced acute severe liver injury
Kitazawa, T., Tsujimoto, T., Kawaratani, H., & Fukui, H. (2009) · Journal of Gastroenterology and Hepatology · doi:10.1111/j.1440-1746.2008.05770.x · Cited by 33
Anti-inflammatory activity of brown alga Dictyota dichotoma in murine macrophage RAW 264.7 cells
Yoon, W., Ham, Y., Kim, K., Park, S.-Y., Lee, N. H., Hyun, C., & Lee, W. J. (2009) · Journal of Medicinal Plants Research · doi:10.5897/jmpr.9000099 · Cited by 33
The Polysaccharide Portion of Lipopolysaccharide Regulates Antigen-Specific T-Cell Activation via Effects on Macrophage-Mediated Antigen Processing
Zirk, N. M., Hashmi, S., & Ziegler, H. (1999) · Infection and Immunity · doi:10.1128/iai.67.1.319-326.1999 · Cited by 33
Blood Interleukin-6 and Tumor Necrosis Factor-α Elevation after Intracerebroventricular Injection of Escherichia coli Endotoxin in the Rat Is Determined by Two Opposing Factors: Peripheral Induction by LPS Transferred from Brain to Blood and Inhibition of Peripheral Response by a Brain-Mediated Mechanism
Chen, G.-J., McCuskey, R. S., & Reichlin, S. (2000) · NeuroImmunoModulation · doi:10.1159/000026454 · Cited by 33
Dissecting the contribution of innate and antigen-specific pathways to the breach of self-tolerance observed in a murine model of arthritis
Nickdel, M. B., Conigliaro, P., Valesini, G., Hutchison, S., Benson, R., Bundick, R., Leishman, A., McInnes, I., Brewer, J. M., & Garside, P. (2008) · Annals of the Rheumatic Diseases · doi:10.1136/ard.2008.089300 · Cited by 35
LPS-induced cytokine production and expression of β2-integrins and CD14 by peripheral blood mononuclear cells of patients with homozygous familial hypercholesterolemia
Bleeker‐Rovers, C. P., Netea, M. G., de Bont, N., Demacker, P. N. M., Jacobs, C. W. M., Kullberg, B. J., van der Meer, J. W. M., & Stalenhoef, A. F. H. (1998) · Atherosclerosis · doi:10.1016/s0021-9150(98)00152-x · Cited by 33
TLR2 and AP-1/NF-kappaB are involved in the regulation of MMP-9 elicited by heat killed Listeria monocytogenes in human monocytic THP-1 cells
Kochumon, S., Al-Roub, A., Al-Ghanim, M., Al‐Mass, A., Behbehani, K., & Ahmad, R. (2015) · Journal of Inflammation · doi:10.1186/s12950-015-0077-0 · Cited by 33
“MAPKs are activated largely by bacterial products through TLRs and participated in the inflammatory response induced by TLR2 activation in monocytes/macrophages [53,55].”
Background
Simple and Label‐Free Liquid Crystal‐based Optical Sensor for Highly Sensitive and Selective Endotoxin Detection by Aptamer Binding and Separation
An, Z., & Jang, C. (2019) · ChemistrySelect · doi:10.1002/slct.201803774 · Cited by 32
Killing three birds with one BPI: Bactericidal, opsonic, and anti-inflammatory functions
Theprungsirikul, J., Skopelja‐Gardner, S., & Rigby, W. F. C. (2021) · Journal of Translational Autoimmunity · doi:10.1016/j.jtauto.2021.100105 · Cited by 31
Concentration-dependent roles for heparin in modifying liopolysaccharide-induced activation of mononuclear cells in whole blood
Hochart, H., Jenkins, P. V., Preston, R. J. S., Smith, O. P., White, B., & O’Donnell, J. S. (2008) · Thrombosis and Haemostasis · doi:10.1160/th07-06-0424 · Cited by 32
OUTER MEMBRANE VESICLES FROM NEISSERIA MENINGITIDIS: EFFECTS ON CYTOKINE PRODUCTION IN HUMAN WHOLE BLOOD
Mirlashari, M. R., Høiby, E. A., Holst, J., & Lyberg, T. (2001) · Cytokine · doi:10.1006/cyto.2000.0803 · Cited by 32
Antimicrobial peptide of an anti-lipopolysaccharide factor modulates of the inflammatory response in RAW264.7 cells
Lin, M., Lin, S., Lee, S.-C., Lin, C.-C., Hui, C., & Chen, J. (2010) · Peptides · doi:10.1016/j.peptides.2010.04.004 · Cited by 32
Absence of Common Polymorphisms of Toll Like Receptor 4 (TLR4): Asp299Gly, Thr399Ile in Patients with Gastroduodenal Diseases in Japan
Tahara, T., Arisawa, T., Shibata, T., Hirata, I., & Nakano, H. (2007) · Journal of Clinical Biochemistry and Nutrition · doi:10.3164/jcbn.40.62 · Cited by 32
“These signals in turn activate transcription factors, mainly nuclear factor-κB (NFκB) and cytokines [10, 14].”
Background
Freund adjuvant induces TLR2 but not TLR4 expression in the liver of mice
Lim, S. K. (2003) · International Immunopharmacology · doi:10.1016/s1567-5769(02)00256-4 · Cited by 32
γ‐Interferon enhances expression of CD14/MyD88 and subsequent responsiveness to lipopolysaccharide from Actinobacillus actinomycetemcomitans in human gingival fibroblasts
Mochizuki, S., Kobayashi, M., Suzuki, T., Oikawa, A., Koseki, T., Nishihara, T., & Hasegawa, K. (2004) · Journal of Periodontal Research · doi:10.1111/j.1600-0765.2004.00749.x · Cited by 32
Interactions of bacterial lipopolysaccharide and peptidoglycan with a 70 kDa and an 80 kDa protein on the cell surface of CD14+ and CD14− cells
Triantafilou, K., Triantafilou, M., & Dedrick, R. L. (2001) · Human Immunology · doi:10.1016/s0198-8859(00)00222-6 · Cited by 32
Endotoxin potency in the A549 lung epithelial cell bioassay and the limulus amebocyte lysate assay
Hansen, L. A., Poulsen, O. M., & Würtz, H. (1999) · Journal of Immunological Methods · doi:10.1016/s0022-1759(99)00047-2 · Cited by 32
Heparin Binding Protein (CAP37) is an Opsonin for Staphylococcus aureus and Increases Phagocytosis in Monocytes
Heinzelmann, M., Platz, A., Flodgaard, H., & Miller, F. (1998) · Inflammation · doi:10.1023/a:1022398027143 · Cited by 29
Pasteurella haemolyticaA1-Derived Leukotoxin and Endotoxin Induce Intracellular Calcium Elevation in Bovine Alveolar Macrophages by Different Signaling Pathways
Hsuan, S., Kannan, M., Jeyaseelan, S., Prakash, Y. S., Sieck, G. C., & Maheswaran, S. K. (1998) · Infection and Immunity · doi:10.1128/iai.66.6.2836-2844.1998 · Cited by 31
Human- and Mouse-Inducible Nitric Oxide Synthase Promoters Require Activation of Phosphatidylcholine-Specific Phospholipase C and NF-κB
Spitsin, S. V., Farber, J. L., Bertovich, M. J., Moehren, G., Koprowski, H., & Michaels, F. H. (1997) · Molecular Medicine · doi:10.1007/bf03401810 · Cited by 32
HIV-1 exposed dendritic cells show increased pro-inflammatory cytokine production but reduced IL-1ra following lipopolysaccharide stimulation
Loré, K., Sönnerborg, A. B., Olsson, J., Patterson, B. K., Fehniger, T. E., Perbeck, L. G., & Andersson, J. (1999) · AIDS · doi:10.1097/00002030-199910220-00003 · Cited by 32
Lipopolysaccharide increases arginine-vasopressin release from rat suprachiasmatic nucleus slice cultures
Nava, F. A., Carta, G., & Haynes, L. W. (2000) · Neuroscience Letters · doi:10.1016/s0304-3940(00)01199-x · Cited by 31
Stabilization of tumor necrosis factor-alpha mRNA in macrophages in response to chronic ethanol exposure
Nagy, L. E. (2004) · Alcohol · doi:10.1016/j.alcohol.2004.09.002 · Cited by 30
Degraded λ-carrageenan activates NF-κB and AP-1 pathways in macrophages and enhances LPS-induced TNF-α secretion through AP-1
Chen, H., Wang, F., Mao, H., & Yan, X. (2014) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/j.bbagen.2014.03.011 · Cited by 31
“We proposed that the inflammatory response induced by dCGN might be enhanced by some factors such as bacterial lipopolysaccharide (LPS), a major constituent of the outer membrane of the cell wall of all Gram-negative bacteria and one of the most potent inducers of inflammation [13].”
Background
A novel lipid A from Halomonas magadiensis inhibits enteric LPS‐induced human monocyte activation
Ialenti, A., Meglio, P. D., Grassia, G., Maffia, P., Rosa, M. D., Lanzetta, R., Molinaro, A., Silipo, A., Grant, W., & Ianaro, A. (2005) · European Journal of Immunology · doi:10.1002/eji.200535305 · Cited by 31
Soluble CD14 Discriminates Slight Structural Differences between Lipid As That Lead to Distinct Host Cell Activation
Asai, Y., Makimura, Y., Kawabata, A., & Ogawa, T. (2007) · The Journal of Immunology · doi:10.4049/jimmunol.179.11.7674 · Cited by 31
“the cell surface or soluble CD14 (sCD14) (12, 13).”
Background
Lipopolysaccharide from Rhodobacter sphaeroides is an agonist in equine cells
Lohmann, K. L., Vandenplas, M. L., Barton, M. H., & Moore, J. N. (2003) · Journal of Endotoxin Research · doi:10.1177/09680519030090010301 · Cited by 31
Lipopolysaccharide Induces Epithelium- and Prostaglandin E2-Dependent Relaxation of Mouse Isolated Trachea through Activation of Cyclooxygenase (COX)-1 and COX-2
Balzary, R. W., & Cocks, T. M. (2006) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.105.097634 · Cited by 31
“Lipopolysaccharide (LPS), a product of the Gram negative bacterial cell wall, potently stimulates the innate immune system, eliciting both pro- and anti-inflammatory responses (Ulevitch and Tobias, 1995).”
Background
Relation between complement and the febrile response of guinea pigs to systemic endotoxin
Li, S., SEHIC, E., Wang, Y., Ungar, A. L., & Blatteis, C. M. (1999) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1999.277.6.r1635 · Cited by 31
Soluble CD14 and lipopolysaccharide-binding protein from bovine serum enable bacterial lipopolysaccharide-mediated cytotoxicity and activation of bovine vascular endothelial cells in vitro
Yang, Z., Breider, M. A., Carroll, R. C., Miller, M. S., & Bochsler, P. N. (1996) · Journal of Leukocyte Biology · doi:10.1002/jlb.59.2.241 · Cited by 31
Differential activation of murine macrophages by angelan and LPS
Jeon, Y. J., Han, S. B., Ahn, K. S., & Kim, H. M. (2000) · Immunopharmacology · doi:10.1016/s0162-3109(00)00243-5 · Cited by 31
Cytosine-phosphate-guanine (CpG) motifs are sensitizing agents for lipopolysaccharide in toxic shock model
Cornélie, S., Wiel, É., Lund, N., Lebuffe, G., Vendeville, C., Riveau, G. J., Vallet, B., & Ban, E. (2002) · Intensive Care Medicine · doi:10.1007/s00134-002-1418-z · Cited by 31
“The signal transduction pathways activated by LPS are well characterized [36, 37] and differ from those triggered after bacterial DNA exposure.”
Modulation of an Interleukin-12 and Gamma Interferon Synergistic Feedback Regulatory Cycle of T-Cell and Monocyte Cocultures byPorphyromonas gingivalisLipopolysaccharide in the Absence or Presence of Cysteine Proteinases
Yun, P. L. W., DeCarlo, A. A., Collyer, C. A., & Hunter, N. (2002) · Infection and Immunity · doi:10.1128/iai.70.10.5695-5705.2002 · Cited by 31
“High concentrations of LPS are known to activate cells in a CD14independent mechanism (44).”
Background
Seasonal variations in haemocyte response in the mussel Mytilus galloprovincialis Lmk
Cao, A., Novas, A. J., Ramos-Martı́nez, J. I., & Barcia, R. (2006) · Aquaculture · doi:10.1016/j.aquaculture.2006.11.004 · Cited by 31
“Bacterial lipopolysaccharides (LPS) stimulate the innate immunity in diverse eukaryotic species, from insects to human beings (Ulevitch and Tobias, 1995), activating several pathways of signal transduction in macrophage-like cells.”
Background
Identification from a Positional Scanning Peptoid Library of in Vivo Active Compounds That Neutralize Bacterial Endotoxins
Mora, P., Masip, I., Cortés, N., Marquina, R., Merino, R., Merino, J., Carbonell, T., Mingarro, I., Messeguer, Á., & Pérez‐Payá, E. (2005) · Journal of Medicinal Chemistry · doi:10.1021/jm040834i · Cited by 31
Heparin coating reduces cell activation and mediator release in an in vitro venovenous bypass model for liver transplantation
Solberg, R., Scholz, T., Videm, V., Okkenhaug, C., & Aasen, A. O. (1998) · Transplant International · doi:10.1111/j.1432-2277.1998.tb00966.x · Cited by 31

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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