Recognition of LPS by TLR4: Potential for anti-inflammatory therapies

Marine Drugs

Volumn 12, Issue 7, 2014, Pages 4260-4273

  Nijland, Reindert ^a   Hofland, Tom ^a   Van Strijp, Jos A G ^a  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

Lipid A; LPS; Sepsis therapy; TLR4

Indexed keywords

ARSENIC TRIOXIDE; ARYLIDENE MALONATE DERIVATIVE; BACTERIUM LIPOPOLYSACCHARIDE; ERITORAN; LIPID A; MALONIC ACID DERIVATIVE; PROTEIN MD 2; RESATORVID; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 4 INHIBITOR; TOLL LIKE RECEPTOR AGONIST; UNCLASSIFIED DRUG; TLR4 PROTEIN, HUMAN;

ACINETOBACTER BAUMANNII; ACYLATION; ALTEROMONAS ADDITA; ALTEROMONAS MACLEODII; BORDETELLA PERTUSSIS; CHEMICAL STRUCTURE; CHRYSEOBACTERIUM SCOPHTALMUM; COMPLEX FORMATION; ESCHERICHIA COLI; IMMNUNE RECOGNITION; IMMUNE RESPONSE; IMMUNOGENICITY; IMMUNOSTIMULATION; LEGIONELLA PNEUMOPHILA; LEPTOSPIRA INTERROGANS; LOW TEMPERATURE; MARINE BACTERIUM; MARINOMONAS COMMUNIS; MARINOMONAS MEDITERRANEA; MARINOMONAS VAGA; NONHUMAN; PRESSURE; PROTEIN PROTEIN INTERACTION; PSEUDOALTEROMONAS HALOPLANKTIS; PSEUDOALTEROMONAS ISSACHENKONII; REVIEW; SEPSIS; SHEWANELLA PACIFICA; SIGNAL TRANSDUCTION; SYNECHOCOCCUS; TOXICITY; ANTAGONISTS AND INHIBITORS; CHEMISTRY; DRUG EFFECTS; HUMAN; IMMUNOLOGY; MICROBIOLOGY; PHYSIOLOGY; PROTEIN MULTIMERIZATION;

ACYLATION; HUMANS; LIPID A; PROTEIN MULTIMERIZATION; SEPSIS; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 4; WATER MICROBIOLOGY;

EID: 84905864797     PISSN: None     EISSN: 16603397     Source Type: Journal    
DOI: 10.3390/md12074260     Document Type: Review

References (56)

1. Leone, S.; Silipo, A.; Nazarenko, E.L.; Lanzetta, R.; Parrilli, M.; Molinaro, A. Molecular structure of endotoxins from Gram-negative marine bacteria: An update. Mar. Drugs 2007, 5, 85-112. (Pubitemid 47511035)
2. Rietschel, E.T.; Kirikae, T.; Schade, F.U.; Mamat, U.; Schmidt, G.; Loppnow, H.; Ulmer, A.J.; Zähringer, U.; Seydel, U.; di Padova, F. Bacterial endotoxin: Molecular relationships of structure to activity and function. FASEB J. 1994, 8, 217-225. (Pubitemid 24067145)
3. Cohen, J. The immunopathogenesis of sepsis. Nature 2002, 420, 885-891. (Pubitemid 36019643)
4. Van Amersfoort, E.S.; van Berkel, T.J.; Kuiper, J. Receptors, mediators, and mechanisms involved in bacterial sepsis and septic shock. Clin. Microbiol. Rev. 2003, 16, 379-414. (Pubitemid 36871313)
5. Solov'eva, T.; Davydova, V.; Krasikova, I.; Yermak, I. Marine compounds with therapeutic potential in Gram-negative sepsis. Mar. Drugs 2013, 11, 2216-2229.
6. Fitzgerald, K.A.; Rowe, D.C.; Golenbock, D.T. Endotoxin recognition and signal transduction by the TLR4/MD2-complex. Microbes Infect./Inst. Pasteur 2004, 6, 1361-1367. (Pubitemid 41110578)
7. Poltorak, A.; He, X.; Smirnova, I.; Liu, M.-Y.; Huffel, C.V.; Du, X.; Birdwell, D.; Alejos, E.; Silva, M.; Galanos, C.; et al. Defective lps signaling in C3H/HeJ and C57BL/10ScCr mice: Mutations in TLR4 gene. Science 1998, 282, 2085-2088.
8. Gioannini, T.L.; Teghanemt, A.; Zhang, D.; Coussens, N.P.; Dockstader, W.; Ramaswamy, S.; Weiss, J.P. Isolation of an endotoxin-MD-2 complex that produces Toll-like receptor 4-dependent cell activation at picomolar concentrations. Proc. Natl. Acad. Sci. USA 2004, 101, 4186-4191. (Pubitemid 38405904)
9. Da Silva Correia, J.; Soldau, K.; Christen, U.; Tobias, P.S.; Ulevitch, R.J. Lipopolysaccharide is in close proximity to each of the proteins in its membrane receptor complex: Transfer from CD14 to TLR4 and MD-2. J. Biol. Chem. 2001, 276, 21129-21135.
10. DeMarco, M.L.; Woods, R.J. From agonist to antagonist: Structure and dynamics of innate immune glycoprotein MD-2 upon recognition of variably acylated bacterial endotoxins. Mol. Immunol. 2011, 49, 124-133.
11. Huber, M.; Kalis, C.; Keck, S.; Jiang, Z.; Georgel, P.; Du, X.; Shamel, L.; Sovath, S.; Mudd, S.; Beutler, B.; et al. R-form LPS, the master key to the activation ofTLR4/MD-2-positive cells. Eur. J. Immunol. 2006, 36, 701-711.
12. Kagan, J.C.; Su, T.; Horng, T.; Chow, A.; Akira, S.; Medzhitov, R. Tram couples endocytosis of Toll-like receptor 4 to the induction of interferon-β. Nat. Immunol. 2008, 9, 361-368. (Pubitemid 351405105)
13. Tanimura, N.; Saitoh, S.; Matsumoto, F.; Akashi-Takamura, S.; Miyake, K. Roles for LPS-dependent interaction and relocation of TLR4 and tram in TRIF-signaling. Biochem. Biophys. Res. Commun. 2008, 368, 94-99.
14. Raetz, C.R.; Reynolds, C.M.; Trent, M.S.; Bishop, R.E. Lipid a modification systems in Gram-negative bacteria. Annu. Rev. Biochem. 2007, 76, 295-329.
15. Vorobeva, E.V.; Krasikova, I.N.; Solov'eva, T.F. Influence of lipopolysaccharides and lipids a from some marine bacteria on spontaneous and Escherichia coli LPS-induced TNF-alpha release from peripheral human blood cells. Biochem. Biokhimiia 2006, 71, 759-766. (Pubitemid 44092039)
16. Park, B.S.; Song, D.H.; Kim, H.M.; Choi, B.S.; Lee, H.; Lee, J.O. The structural basis of lipopolysaccharide recognition by the TLR4-MD-2 complex. Nature 2009, 458, 1191-1195.
17. Schromm, A.B.; Brandenburg, K.; Loppnow, H.; Moran, A.P.; Koch, M.H.; Rietschel, E.T.; Seydel, U. Biological activities of lipopolysaccharides are determined by the shape of their lipid a portion. Eur. J. Biochem. 2000, 267, 2008-2013. (Pubitemid 30185287)
18. Erridge, C.; Moncayo-Nieto, O.L.; Morgan, R.; Young, M.; Poxton, I.R. Acinetobacter baumannii lipopolysaccharides are potent stimulators of human monocyte activation via Toll-like receptor 4 signalling. J. Med. Microbiol. 2007, 56, 165-171.
19. Leone, S.; Sturiale, L.; Pessione, E.; Mazzoli, R.; Giunta, C.; Lanzetta, R.; Garozzo, D.; Molinaro, A.; Parrilli, M. Detailed characterization of the lipid a fraction from the nonpathogen Acinetobacter radioresistens strain s13. J. Lipid Res. 2007, 48, 1045-1051. (Pubitemid 46708671)
20. Pelletier, M.R.; Casella, L.G.; Jones, J.W.; Adams, M.D.; Zurawski, D.V.; Hazlett, K.R.; Doi, Y.; Ernst, R.K. Unique structural modifications are present in the lipopolysaccharide from colistin-resistant strains of Acinetobacter baumannii. Antimicrob. Agents Chemother. 2013, 57, 4831-4840.
21. Zahringer, U.; Lindner, B.; Inamura, S.; Heine, H.; Alexander, C. Tlr2-Promiscuous or specific? A critical re-evaluation of a receptor expressing apparent broad specificity. Immunobiology 2008, 213, 205-224.
22. Girard, R.; Pedron, T.; Uematsu, S.; Balloy, V.; Chignard, M.; Akira, S.; Chaby, R. Lipopolysaccharides from legionella and rhizobium stimulate mouse bone marrow granulocytes via Toll-like receptor 2. J. Cell Sci. 2003, 116, 293-302. (Pubitemid 36163870)
23. Werts, C.; Tapping, R.I.; Mathison, J.C.; Chuang, T.H.; Kravchenko, V.; Saint Girons, I.; Haake, D.A.; Godowski, P.J.; Hayashi, F.; Ozinsky, A.; et al. Leptospiral lipopolysaccharide activates cells through a TLR2-dependent mechanism. Nat. Immunol. 2001, 2, 346-352.
24. Hirschfeld, M.; Ma, Y.; Weis, J.H.; Vogel, S.N.; Weis, J.J. Cutting edge: Repurification of lipopolysaccharide eliminates signaling through both human and murine Toll-like receptor 2. J. Immunol. 2000, 165, 618-622. (Pubitemid 30484724)
25. Hellman, J.; Tehan, M.M.; Shaw Warren, H. Murein lipoprotein, peptidoglycan-associated lipoprotein, and outer membrane protein a are present in purified rough and smooth lipopolysaccharides. J. Infect. Dis. 2003, 188, 286-289.
26. Lee, H.-K.; Lee, J.; Tobias, P.S. Two lipoproteins extracted from Escherichia coli K-12 LCD25 lipopolysaccharide are the major components responsible for Toll-like receptor 2-mediated signaling. J. Immunol. 2002, 168, 4012-4017. (Pubitemid 34298406)
27. Kawahara, K.; Tsukano, H.; Watanabe, H.; Lindner, B.; Matsuura, M. Modification of the structure and activity of lipid a in Yersinia pestis lipopolysaccharide by growth temperature. Infect. Immun. 2002, 70, 4092-4098. (Pubitemid 34790917)
28. Hajjar, A.M.; Ernst, R.K.; Tsai, J.H.; Wilson, C.B.; Miller, S.I. Human Toll-like receptor 4 recognizes host-specific LPS modifications. Nat. Immunol. 2002, 3, 354-359. (Pubitemid 34308623)
29. Stover, A.G.; da Silva Correia, J.; Evans, J.T.; Cluff, C.W.; Elliott, M.W.; Jeffery, E.W.; Johnson, D.A.; Lacy, M.J.; Baldridge, J.R.; Probst, P.; et al. Structure-activity relationship of synthetic Toll-like receptor 4 agonists. J. Biol. Chem. 2004, 279, 4440-4449.
30. Corsaro, M.M.; Piaz, F.D.; Lanzetta, R.; Parrilli, M. Lipid a structure of Pseudoalteromonas haloplanktis TAC 125: Use of electrospray ionization tandem mass spectrometry for the determination of fatty acid distribution. J. Mass Spectrom. 2002, 37, 481-488. (Pubitemid 34578390)
31. Leone, S.; Molinaro, A.; Sturiale, L.; Garozzo, D.; Nazarenko, E.L.; Gorshkova, R.P.; Ivanova, E.P.; Shevchenko, L.S.; Lanzetta, R.; Parrilli, M. The outer membrane of the marine Gram-negative bacterium Alteromonas addita is composed of a very short-chain lipopolysaccharide with a high negative charge density. Eur. J. Org. Chem. 2007, 2007, 1113-1122.
32. Krasikova, I.N.; Kapustina, N.V.; Isakov, V.V.; Dmitrenok, A.S.; Dmitrenok, P.S.; Gorshkova, N.M.; Solov'eva, T.F. Detailed structure of lipid a isolated from lipopolysaccharide from the marine Proteobacterium marinomonas vaga ATCC 27119. Eur. J. Biochem. 2004, 271, 2895-2904. (Pubitemid 38986926)
33. Silipo, A.; Leone, S.; Lanzetta, R.; Parrilli, M.; Sturiale, L.; Garozzo, D.; Nazarenko, E.L.; Gorshkova, R.P.; Ivanova, E.P.; Gorshkova, N.M.; et al. The complete structure of the lipooligosaccharide from the halophilic bacterium Pseudoalteromonas issachenkonii KMM 3549 T. Carbohydr. Res. 2004, 339, 1985-1993.
34. Liparoti, V.; Molinaro, A.; Sturiale, L.; Garozzo, D.; Nazarenko, E.L.; Gorshkova, R.P.; Ivanova, E.P.; Shevcenko, L.S.; Lanzetta, R.; Parrilli, M. Structural analysis of the deep rough lipopolysaccharide from gram negative bacterium alteromonas macleodii atcc 27126t: The first finding of?-kdo in the inner core of lipopolysaccharides. Eur. J. Org. Chem. 2006, 2006, 4710-4716.
35. Snyder, D.S.; Brahamsha, B.; Azadi, P.; Palenik, B. Structure of compositionally simple lipopolysaccharide from marine Synechococcus. J. Bacteriol. 2009, 191, 5499-5509.
36. Silipo, A.; Leone, S.; Molinaro, A.; Sturiale, L.; Garozzo, D.; Nazarenko, E.L.; Gorshkova, R.P.; Ivanova, E.P.; Lanzetta, R.; Parrilli, M. Complete structural elucidation of a novel lipooligosaccharide from the outer membrane of the marine bacterium Shewanella pacifica. Eur. J. Org. Chem. 2005, 2005, 2281-2291.
37. Maaetoft-Udsen, K.; Vynne, N.; Heegaard, P.M.; Gram, L.; Frøkiær, H. Pseudoalteromonas strains are potent immunomodulators owing to low-stimulatory LPS. Innate Immun. 2013, 19, 160-173.
38. Sinensky, M. Homeoviscous adaptation-A homeostatic process that regulates the viscosity of membrane lipids in Escherichia coli. Proc. Natl. Acad. Sci. USA 1974, 71, 522-525.
39. Carty, S.M.; Sreekumar, K.R.; Raetz, C.R.H. Effect of cold shock on lipid a biosynthesis Inescherichia coli: Induction at 12 degrees C of an acyltransferase specific for palmitoleoyl-acyl carrier protein. J. Biol. Chem. 1999, 274, 9677-9685.
40. Ramos, J.L.; Gallegos, M.T.; Marqués, S.; Ramos-González, M.I.; Espinosa-Urgel, M.; Segura, A. Responses of Gram-negative bacteria to certain environmental stressors. Curr. Opin. Microbiol. 2001, 4, 166-171. (Pubitemid 32294418)
41. Peri, F.; Piazza, M. Therapeutic targeting of innate immunity with Toll-like receptor 4 (TLR4) antagonists. Biotechnol. Adv. 2011, 30, 251-260.
42. Kim, H.M.; Park, B.S.; Kim, J.I.; Kim, S.E.; Lee, J.; Oh, S.C.; Enkhbayar, P.; Matsushima, N.; Lee, H.; Yoo, O.J.; et al. Crystal structure of the TLR4-MD-2 complex with bound endotoxin antagonist eritoran. Cell 2007, 130, 906-917.
43. Czeslick, E.; Struppert, A.; Simm, A.; Sablotzki, A. E5564 (eritoran) inhibits lipopolysaccharide-induced cytokine production in human blood monocytes. Inflamm. Res. 2006, 55, 511-515. (Pubitemid 44826742)
44. Opal, S.M.; Laterre, P.F.; Francois, B.; LaRosa, S.P.; Angus, D.C.; Mira, J.P.; Wittebole, X.; Dugernier, T.; Perrotin, D.; Tidswell, M.; et al. Effect of eritoran, an antagonist of MD2-TLR4, on mortality in patients with severe sepsis: The access randomized trial. JAMA 2013, 309, 1154-1162.
45. Takashima, K.; Matsunaga, N.; Yoshimatsu, M.; Hazeki, K.; Kaisho, T.; Uekata, M.; Hazeki, O.; Akira, S.; Iizawa, Y.; Ii, M. Analysis of binding site for the novel small-molecule TLR4 signal transduction inhibitor TAK-242 and its therapeutic effect on mouse sepsis model. Br. J. Pharmacol. 2009, 157, 1250-1262.
46. Rooijakkers, S.H.; van Strijp, J.A. Bacterial complement evasion. Mol. Immunol. 2007, 44, 23-32. (Pubitemid 44647108)
47. Rooijakkers, S.H.; van Kessel, K.P.; van Strijp, J.A. Staphylococcal innate immune evasion. Trends Microbiol. 2005, 13, 596-601.
48. Bardoel, B.W.; van der Ent, S.; Pel, M.J.; Tommassen, J.; Pieterse, C.M.; van Kessel, K.P.; van Strijp, J.A. Pseudomonas evades immune recognition of flagellin in both mammals and plants. PLoS Pathog. 2011, 7, e1002206.
49. Laarman, A.J.; Bardoel, B.W.; Ruyken, M.; Fernie, J.; Milder, F.J.; van Strijp, J.A.; Rooijakkers, S.H. Pseudomonas aeruginosa alkaline protease blocks complement activation via the classical and lectin pathways. J. Immunol. (Baltim.) 2012, 188, 386-393.
50. Bardoel, B.W.; Vos, R.; Bouman, T.; Aerts, P.C.; Bestebroer, J.; Huizinga, E.G.; Brondijk, T.H.; van Strijp, J.A.; de Haas, C.J. Evasion of Toll-like receptor 2 activation by staphylococcal superantigen-like protein 3. J. Mol. Med. (Berl.) 2012, 90, 1109-1120.
51. Gomery, K.; Muller-Loennies, S.; Brooks, C.L.; Brade, L.; Kosma, P.; Di Padova, F.; Brade, H.; Evans, S.V. Antibody WN1 222-5 mimics Toll-like receptor 4 binding in the recognition of LPS. Proc. Natl. Acad. Sci. USA 2012, 109, 20877-20882.
52. Zhang, S.; Cheng, K.; Wang, X.; Yin, H. Selection, synthesis, and anti-inflammatory evaluation of the arylidene malonate derivatives as tlr4 signaling inhibitors. Bioorg. Med. Chem. 2012, 20, 6073-6079.
53. Zhang, D.; Li, Y.; Liu, Y.; Xiang, X.; Dong, Z. Paclitaxel ameliorates lipopolysaccharide-induced kidney injury by binding myeloid differentiation protein-2 to block Toll-like receptor 4-mediated nuclear factor-kappab activation and cytokine production. J. Pharmacol. Exp. Ther. 2013, 345, 69-75.
54. Piao, W.; Vogel, S.N.; Toshchakov, V.Y. Inhibition of TLR4 signaling by tram-derived decoy peptides in vitro and in vivo. J. Immunol. (Baltim.) 2013, 190, 2263-2272.
55. Takahashi, M.; Ota, A.; Karnan, S.; Hossain, E.; Konishi, Y.; Damdindorj, L.; Konishi, H.; Yokochi, T.; Nitta, M.; Hosokawa, Y. Arsenic trioxide prevents nitric oxide production in lipopolysaccharide-stimulated raw 264.7 by inhibiting a TRIF-dependent pathway. Cancer Sci. 2012, 104, 165-170.
56. Coburn, B.; Sekirov, I.; Finlay, B.B. Type III secretion systems and disease. Clin. Microbiol. Rev. 2007, 20, 535-549. (Pubitemid 47623767)