Critical residues involved in Toll-like receptor 4 activation by cationic lipid nanocarriers are not located at the lipopolysaccharide-binding interface

Cellular and Molecular Life Sciences

Volumn 72, Issue 20, 2015, Pages 3971-3982

  Lonez, Caroline ^a,b   Irvine, Kate L ^a   Pizzuto, Malvina ^b   Schmidt, Boris I ^b   Gay, Nick J ^a   Ruysschaert, Jean Marie ^b   Gangloff, Monique ^a   Bryant, Clare E ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

Author keywords

Activation mechanism; Cationic lipid; Nanoparticle; Species specificity; Toll like receptor

Indexed keywords

CD14 ANTIGEN; DIC14 AMIDINE NANOLIPOSOME; GAMMA INTERFERON INDUCIBLE PROTEIN 10; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERFERON REGULATORY FACTOR 3; INTERLEUKIN 12P40; LIPOPOLYSACCHARIDE; PROTEIN MD 2; SOLID LIPID NANOPARTICLE; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; HYBRID PROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; CYTOKINE RELEASE; DIMERIZATION; HUMAN; HUMAN CELL; HYDROPHILICITY; HYDROPHOBICITY; PROTEIN EXPRESSION; PROTEIN INDUCTION; PROTEIN INTERACTION; PROTEIN LIPID INTERACTION; SIGNAL TRANSDUCTION; AMINO ACID SEQUENCE; ANIMAL; CHEMICAL STRUCTURE; CHEMISTRY; HEK293 CELL LINE; HORSE; LIPID METABOLISM; METABOLISM; MOLECULAR DOCKING; MOUSE; PHYSIOLOGY; SPECIES DIFFERENCE;

AMINO ACID SEQUENCE; ANIMALS; ANTIGENS, CD14; BINDING SITES; HEK293 CELLS; HORSES; HUMANS; LIPID METABOLISM; LIPOPOLYSACCHARIDES; LYMPHOCYTE ANTIGEN 96; MICE; MODELS, MOLECULAR; MOLECULAR DOCKING SIMULATION; RECOMBINANT FUSION PROTEINS; SIGNAL TRANSDUCTION; SPECIES SPECIFICITY; TOLL-LIKE RECEPTOR 4;

EID: 84942371845     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-015-1915-1     Document Type: Article

References (57)

1. Gay NJ, Gangloff M (2007) Structure and function of Toll receptors and their ligands. Annu Rev Biochem 76:141-165. doi: 10.1146/annurev.biochem.76.060305.151318
2. Bryant CE, Spring DR, Gangloff M, Gay NJ (2010) The molecular basis of the host response to lipopolysaccharide. Nat Rev Microbiol 8:8-14. doi: 10.1038/nrmicro2266
3. Park BS, Song DH, Kim HM, Choi BS, Lee H, Lee JO (2009) The structural basis of lipopolysaccharide recognition by the TLR4-MD-2 complex. Nature 458:1191-1195. doi: 10.1038/nature07830
4. Ohto U, Fukase K, Miyake K, Satow Y (2007) Crystal structures of human MD-2 and its complex with antiendotoxic lipid IVa. Science 316:1632-1634. doi: 10.1126/science.1139111
5. Poltorak A, Ricciardi-Castagnoli P, Citterio S, Beutler B (2000) Physical contact between lipopolysaccharide and toll-like receptor 4 revealed by genetic complementation. Proc Natl Acad Sci USA 97:2163-2167. doi: 10.1073/pnas.040565397
6. DeMarco ML, Woods RJ (2011) From agonist to antagonist: structure and dynamics of innate immune glycoprotein MD-2 upon recognition of variably acylated bacterial endotoxins. Mol Immunol 49:124-133. doi: 10.1016/j.molimm.2011.08.003
7. Chilton PM, Embry CA, Mitchell TC (2012) Effects of differences in lipid a structure on TLR4 pro-inflammatory signaling and inflammasome activation. Front Immunol 3:154. doi: 10.3389/fimmu.2012.00154
8. Oblak A, Jerala R (2014) The molecular mechanism of species-specific recognition of lipopolysaccharides by the MD-2/TLR4 receptor complex. Mol Immunol. doi: 10.1016/j.molimm.2014.06.034
9. Lien E, Means TK, Heine H, Yoshimura A, Kusumoto S, Fukase K, Fenton MJ, Oikawa M, Qureshi N, Monks B, Finberg RW, Ingalls RR, Golenbock DT (2000) Toll-like receptor 4 imparts ligand-specific recognition of bacterial lipopolysaccharide. J Clin. Invest 105:497-504. doi: 10.1172/JCI8541
10. Bryant CE, Monie TP (2012) Mice, men and the relatives: cross-species studies underpin innate immunity. Open Biol 2:120015. doi: 10.1098/rsob.120015
11. Lohmann KL, Vandenplas M, Barton MH, Moore JN (2003) Lipopolysaccharide from Rhodobacter sphaeroides is an agonist in equine cells. J Endotoxin Res 9:33-37. doi: 10.1177/09680519030090010301
12. Lohmann KL, Vandenplas ML, Barton MH, Bryant CE, Moore JN (2007) The equine TLR4/MD-2 complex mediates recognition of lipopolysaccharide from Rhodobacter sphaeroides as an agonist. J Endotoxin Res 13:235-242. doi: 10.1177/0968051907083193
13. Irvine KL, Gangloff M, Walsh CM, Spring DR, Gay NJ, Bryant CE (2014) Identification of key residues that confer Rhodobacter sphaeroides LPS activity at horse TLR4/MD-2. PLoS One 9:e98776. doi: 10.1371/journal.pone.0098776
14. Akashi S, Nagai Y, Ogata H, Oikawa M, Fukase K, Kusumoto S, Kawasaki K, Nishijima M, Hayashi S, Kimoto M, Miyake K (2001) Human MD-2 confers on mouse Toll-like receptor 4 species-specific lipopolysaccharide recognition. Int Immunol 13:1595-1599. doi: 10.1093/intimm/13.12.1595
15. Sauter KS, Brcic M, Franchini M, Jungi TW (2007) Stable transduction of bovine TLR4 and bovine MD-2 into LPS-nonresponsive cells and soluble CD14 promote the ability to respond to LPS. Vet Immunol Immunopathol 118:92-104. doi: 10.1016/j.vetimm.2007.04.017
16. Walsh C, Gangloff M, Monie T, Smyth T, Wei B, McKinley TJ, Maskell D, Gay N, Bryant C (2008) Elucidation of the MD-2/TLR4 interface required for signaling by lipid IVa. J Immunol 181:1245-1254. doi: 10.4049/jimmunol.181.2.1245
17. Ohto U, Fukase K, Miyake K, Shimizu T (2012) Structural basis of species-specific endotoxin sensing by innate immune receptor TLR4/MD-2. Proc Natl Acad Sci USA 109:7421-7426. doi: 10.1073/pnas.1201193109
18. Hajjar AM, Ernst RK, Tsai JH, Wilson CB, Miller SI (2002) Human Toll-like receptor 4 recognizes host-specific LPS modifications. Nat Immunol 3:354-359. doi: 10.1038/ni777
19. Meng J, Drolet JR, Monks BG, Golenbock DT (2010) MD-2 residues tyrosine 42, arginine 69, aspartic acid 122, and leucine 125 provide species specificity for lipid IVA. J Biol Chem 285:27935-27943. doi: 10.1074/jbc.M110.134668
20. Meng J, Lien E, Golenbock DT (2010) MD-2-mediated ionic interactions between lipid A and TLR4 are essential for receptor activation. J Biol Chem 285:8695-8702. doi: 10.1074/jbc.M109.075127
21. Ruysschaert JM, El OA, Willeaume V, Huez G, Fuks R, Vandenbranden M, Di SP (1994) A novel cationic amphiphile for transfection of mammalian cells. Biochem Biophys Res Commun 203:1622-1628. doi: 10.1006/bbrc.1994.2372
22. Elouahabi A, Flamand V, Ozkan S, Paulart F, Vandenbranden M, Goldman M, Ruysschaert JM (2003) Free cationic liposomes inhibit the inflammatory response to cationic lipid-DNA complex injected intravenously and enhance its transfection efficiency. Mol Ther 7:81-88. doi: 10.1016/S1525-0016(02)00032-1
23. Tanaka T, Legat A, Adam E, Steuve J, Gatot JS, Vandenbranden M, Ulianov L, Lonez C, Ruysschaert JM, Muraille E, Tuynder M, Goldman M, Jacquet A (2008) DiC14-amidine cationic liposomes stimulate myeloid dendritic cells through Toll-like receptor 4. Eur J Immunol 38:1351-1357. doi: 10.1002/eji.200737998
24. Lonez C, Vandenbranden M, Ruysschaert JM (2008) Cationic liposomal lipids: from gene carriers to cell signaling. Prog Lipid Res 47:340-347. doi: 10.1016/j.plipres.2008.03.002
25. Lonez C, Lensink MF, Vandenbranden M, Ruysschaert JM (2009) Cationic lipids activate cellular cascades. Which receptors are involved? Biochim Biophys Acta 1790:425-430. doi: 10.1016/j.bbagen.2009.02.015
26. Lonez C, Vandenbranden M, Ruysschaert JM (2012) Cationic lipids activate intracellular signaling pathways. Adv Drug Deliv Rev 64:1749-1758. doi: 10.1016/j.addr.2012.05.009
27. Trott O, Olson AJ (2010) AutoDock Vina: improving the speed and accuracy of docking with a new scoring function, efficient optimization, and multithreading. J Comput Chem 31:455-461. doi: 10.1002/jcc.21334
28. Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, Ferrin TE (2004) UCSF Chimera-a visualization system for exploratory research and analysis. J Comput Chem 25:1605-1612. doi: 10.1002/jcc.20084
29. Wallace AC, Laskowski RA, Thornton JM (1995) LIGPLOT: a program to generate schematic diagrams of protein-ligand interactions. Protein Eng 8:127-134. doi: 10.1093/protein/8.2.127
30. Schmidt M, Raghavan B, Muller V, Vogl T, Fejer G, Tchaptchet S, Keck S, Kalis C, Nielsen PJ, Galanos C, Roth J, Skerra A, Martin SF, Freudenberg MA, Goebeler M (2010) Crucial role for human Toll-like receptor 4 in the development of contact allergy to nickel. Nat Immunol 11:814-819. doi: 10.1038/ni.1919
31. Oblak A, Pohar J, Jerala R (2015) MD-2 determinants of nickel and cobalt-mediated activation of human TLR4. PLoS One 10:e0120583. doi: 10.1371/journal.pone.0120583
32. Inohara N, Nunez G (2002) ML - a conserved domain involved in innate immunity and lipid metabolism. Trends Biochem Sci 27:219-221. doi: 10.1016/S0968-0004(02)02084-4
33. Dundas J, Ouyang Z, Tseng J, Binkowski A, Turpaz Y, Liang J (2006) CASTp: computed atlas of surface topography of proteins with structural and topographical mapping of functionally annotated residues. Nucleic Acids Res 34:W116-W118. doi: 10.1093/nar/gkl282
34. Jin MS, Kim SE, Heo JY, Lee ME, Kim HM, Paik SG, Lee H, Lee JO (2007) Crystal structure of the TLR1-TLR2 heterodimer induced by binding of a tri-acylated lipopeptide. Cell 130:1071-1082. doi: 10.1016/j.cell.2007.09.008
35. Kang JY, Nan X, Jin MS, Youn SJ, Ryu YH, Mah S, Han SH, Lee H, Paik SG, Lee JO (2009) Recognition of lipopeptide patterns by Toll-like receptor 2-Toll-like receptor 6 heterodimer. Immunity 31:873-884. doi: 10.1016/j.immuni.2009.09.018
36. Nattermann J, Du X, Wei Y, Shevchenko D, Beutler B (2000) Endotoxin-mimetic effect of antibodies against Toll-like receptor 4. J Endotoxin Res 6:257-264. doi: 10.1177/09680519000060030701
37. Latz E, Visintin A, Lien E, Fitzgerald KA, Monks BG, Kurt-Jones EA, Golenbock DT, Espevik T (2002) Lipopolysaccharide rapidly traffics to and from the Golgi apparatus with the toll-like receptor 4-MD-2-CD14 complex in a process that is distinct from the initiation of signal transduction. J Biol Chem 277:47834-47843. doi: 10.1074/jbc.M207873200
38. Kawai Y, Takasuka N, Inoue K, Akagawa K, Nishijima M (2000) Ornithine-containing lipids stimulate CD14-dependent TNF-alpha production from murine macrophage-like J774.1 and RAW 264.7 cells. FEMS Immunol Med Microbiol 28:197-203. doi: 10.1111/j.1574-695X.2000.tb01477.x
39. Gomi K, Kawasaki K, Kawai Y, Shiozaki M, Nishijima M (2002) Toll-like receptor 4-MD-2 complex mediates the signal transduction induced by flavolipin, an amino acid-containing lipid unique to Flavobacterium meningosepticum. J Immunol 168:2939-2943. doi: 10.4049/jimmunol.168.6.2939
40. Jou I, Lee JH, Park SY, Yoon HJ, Joe EH, Park EJ (2006) Gangliosides trigger inflammatory responses via TLR4 in brain glia. Am J Pathol 168:1619-1630. doi: 10.2353/ajpath.2006.050924
41. Fischer H, Ellstrom P, Ekstrom K, Gustafsson L, Gustafsson M, Svanborg C (2007) Ceramide as a TLR4 agonist; a putative signalling intermediate between sphingolipid receptors for microbial ligands and TLR4. Cell Microbiol 9:1239-1251. doi: 10.1111/j.1462-5822.2006.00867.x
42. Hung LC, Lin CC, Hung SK, Wu BC, Jan MD, Liou SH, Fu SL (2007) A synthetic analog of alpha-galactosylceramide induces macrophage activation via the TLR4-signaling pathways. Biochem Pharmacol 73:1957-1970. doi: 10.1016/j.bcp.2007.03.006
43. Kedmi R, Ben-Arie N, Peer D (2010) The systemic toxicity of positively charged lipid nanoparticles and the role of Toll-like receptor 4 in immune activation. Biomaterials 31:6867-6875. doi: 10.1016/j.biomaterials.2010.05.027
44. Uto T, Akagi T, Yoshinaga K, Toyama M, Akashi M, Baba M (2011) The induction of innate and adaptive immunity by biodegradable poly(gamma-glutamic acid) nanoparticles via a TLR4 and MyD88 signaling pathway. Biomaterials 32:5206-5212. doi: 10.1016/j.biomaterials.2011.03.052
45. Mano SS, Kanehira K, Taniguchi A (2013) Comparison of cellular uptake and inflammatory response via toll-like receptor 4 to lipopolysaccharide and titanium dioxide nanoparticles. Int J Mol Sci 14:13154-13170. doi: 10.3390/ijms140713154
46. Qu G, Liu S, Zhang S, Wang L, Wang X, Sun B, Yin N, Gao X, Xia T, Chen JJ, Jiang GB (2013) Graphene oxide induces toll-like receptor 4 (TLR4)-dependent necrosis in macrophages. ACS Nano 7:5732-5745. doi: 10.1021/nn402330b
47. Jiang Z, Georgel P, Du X, Shamel L, Sovath S, Mudd S, Huber M, Kalis C, Keck S, Galanos C, Freudenberg M, Beutler B (2005) CD14 is required for MyD88-independent LPS signaling. Nat Immunol 6:565-570. doi: 10.1038/ni1207
48. Huber M, Kalis C, Keck S, Jiang Z, Georgel P, Du X, Shamel L, Sovath S, Mudd S, Beutler B, Galanos C, Freudenberg MA (2006) R-form LPS, the master key to the activation of TLR4/MD-2-positive cells. Eur J Immunol 36:701-711. doi: 10.1002/eji.200535593
49. Legat A, Thomas S, Hermand P, Van Mechelen M, Goldman M, De Wit D (2010) CD14-independent responses induced by a synthetic lipid A mimetic. Eur J Immunol 40:797-802. doi: 10.1002/eji.200939992
50. Tanimura N, Saitoh SI, Ohto U, Akashi-Takamura S, Fujimoto Y, Fukase K, Shimizu T, Miyake K (2014) The attenuated inflammation of MPL is due to the lack of CD14-dependent tight dimerization of the TLR4/MD2 complex at the plasma membrane. Int Immunol. doi: 10.1093/intimm/dxt071
51. Ostuni R, Zanoni I, Granucci F (2010) Deciphering the complexity of Toll-like receptor signaling. Cell Mol Life Sci 67:4109-4134. doi: 10.1007/s00018-010-0464-x
52. Oliveira TR, Duarte EL, Lamy MT, Vandenbranden M, Ruysschaert JM, Lonez C (2012) Temperature-dependence of cationic lipid bilayer intermixing: possible role of interdigitation. Langmuir 28:4640-4647. doi: 10.1021/la3001569
53. Lonez C, Lensink MF, Kleiren E, Vanderwinden JM, Ruysschaert JM, Vandenbranden M (2010) Fusogenic activity of cationic lipids and lipid shape distribution. Cell Mol Life Sci 67:483-494. doi: 10.1007/s00018-009-0197-x
54. Zanoni I, Ostuni R, Marek LR, Barresi S, Barbalat R, Barton GM, Granucci F, Kagan JC (2011) CD14 controls the LPS-induced endocytosis of Toll-like receptor 4. Cell 147:868-880
55. Kagan JC, Su T, Horng T, Chow A, Akira S, Medzhitov R (2008) TRAM couples endocytosis of Toll-like receptor 4 to the induction of interferon-beta. Nat Immunol 9:361-368. doi: 10.1038/ni1569
56. Watanabe S, Kumazawa Y, Inoue J (2013) Liposomal lipopolysaccharide initiates TRIF-dependent signaling pathway independent of CD14. PLoS One 8:e60078. doi: 10.1371/journal.pone.0060078
57. El Ouahabi A, Thiry M, Pector V, Fuks R, Ruysschaert JM, Vandenbranden M (1997) The role of endosome destabilizing activity in the gene transfer process mediated by cationic lipids. FEBS Lett 414:187-192. doi: 10.1016/S0014-5793(97)00973-3