Interactions of lipopolysaccharide with lipid membranes, raft models - A solid state NMR study

Biochimica et Biophysica Acta - Biomembranes

Volumn 1828, Issue 8, 2013, Pages 1731-1742

  Ciesielski, Filip ^a   Griffin, David C ^a   Rittig, Michael ^a   Moriyón, Ignacio ^b   Bonev, Boyan B ^a  

^a UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^b UNIVERSITY OF NAVARRA   (Spain)

Author keywords

Endotoxin; High resolution solid state NMR; Host pathogen interactions; Lipid domains; Longitudinal relaxation; LPS

Indexed keywords

BACTERIUM LIPOPOLYSACCHARIDE; CARBON 13; CHOLESTEROL; ENDOTOXIN; LIPOPOLYSACCHARIDE BINDING PROTEIN; PHOSPHORUS 31; SPHINGOMYELIN;

ARTICLE; BRUCELLA MELITENSIS; CHEMICAL INTERACTION; ESCHERICHIA COLI; KLEBSIELLA PNEUMONIAE; LIPID BILAYER; LIPID MEMBRANE; LIPID RAFT; MOLECULAR BIOLOGY; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PHOSPHORYLATION; PRIORITY JOURNAL; SOLID STATE;

BRUCELLA MELITENSIS; CELL MEMBRANE; ESCHERICHIA COLI; HOST-PATHOGEN INTERACTIONS; KLEBSIELLA PNEUMONIAE; LIPID BILAYERS; LIPOPOLYSACCHARIDES; MAGNETIC RESONANCE SPECTROSCOPY; MEMBRANE LIPIDS; MEMBRANE MICRODOMAINS; MODELS, MOLECULAR; PHOSPHOLIPIDS;

BACTERIA (MICROORGANISMS); BRUCELLA MELITENSIS; ESCHERICHIA COLI; KLEBSIELLA PNEUMONIAE;

EID: 84877046140     PISSN: 00052736     EISSN: 18792642     Source Type: Journal    
DOI: 10.1016/j.bbamem.2013.03.029     Document Type: Article

References (56)

1. S. Akira Mammalian Toll-like receptors Curr. Opin. Immunol. 15 2003 5 11 (Pubitemid 35454185)
2. A. Martirosyan, E. Moreno, and J.P. Gorvel An evolutionary strategy for a stealthy intracellular Brucella pathogen Immunol. Rev. 240 2011 211 234
3. E. Barquero-Calvo, R. Conde-Alvarez, C. Chacon-Diaz, L. Quesada-Lobo, A. Martirosyan, C. Guzman-Verri, M. Iriarte, M. Mancek-Keber, R. Jerala, J.P. Gorvel, I. Moriyon, E. Moreno, and E. Chaves-Olarte The differential interaction of Brucella and Ochrobactrum with innate immunity reveals traits related to the evolution of stealthy pathogens PLoS One 4 2009
4. C.R.H. Raetz, and C. Whitfield Lipopolysaccharide endotoxins Annu. Rev. Biochem. 71 2002 635 700 (Pubitemid 34800232)
5. L.J. Pike Lipid rafts: bringing order to chaos J. Lipid Res. 44 2003 655 667 (Pubitemid 37279667)
6. K. Simons, and E. Ikonen Functional rafts in cell membranes Nature 387 1997 569 572 (Pubitemid 27248754)
7. J.D. Correia, K. Soldau, U. Christen, P.S. Tobias, and R.J. Ulevitch 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. 276 2001 21129 21135
8. D.A. Brown, and J.K. Rose Sorting of GPI-anchored proteins to glycolipid-enriched membrane subdomains during transport to the apical cell-surface Cell 68 1992 533 544
9. G. Schmitz, and E. Orso CD14 signalling in lipid rafts: new ligands and co-receptors Curr. Opin. Lipidol. 13 2002 513 521 (Pubitemid 35231931)
10. J. Cuschieri, J. Billgren, and R.V. Maier Phosphatidylcholine-specific phospholipase C (PC-PLC) is required for LPS-mediated macrophage activation through CD14 J. Leukoc. Biol. 80 2006 407 414 (Pubitemid 44835514)
11. M.B. Fessler, and J.S. Parks Intracellular lipid flux and membrane microdomains as organizing principles in inflammatory cell signaling J. Immunol. 187 2011 1529 1535
12. F.S. Vieira, G. Correa, M. Einicker-Lamas, and R. Coutinho-Silva Host-cell lipid rafts: a safe door for micro-organisms? Biol. Cell 102 2010 391 407
13. A. Hartlova, L. Cerveny, M. Hubalek, Z. Krocova, and J. Stulik Membrane rafts: a potential gateway for bacterial entry into host cells Microbiol. Immunol. 54 2010 237 245
14. S. Olsson, and R. Sundler The role of lipid rafts in LPS-induced signaling in a macrophage cell line Mol. Immunol. 43 2006 607 612 (Pubitemid 41785388)
15. A. Naroeni, and F. Porte Role of cholesterol and the ganglioside GM(1) in entry and short-term survival of Brucella suis in murine macrophages Infect. Immun. 70 2002 1640 1644 (Pubitemid 34163449)
16. S. Kim, M. Watarai, H. Suzuki, S. Makino, T. Kodama, and T. Shirahata Lipid raft microdomains mediate class A scavenger receptor-dependent infection of Brucella abortus Microb. Pathog. 37 2004 11 19 (Pubitemid 38759614)
17. F. Ciesielski, B. Davis, M. Rittig, B.B. Bonev, and P. O'Shea Receptor-independent interaction of bacterial lipopolysaccharide with lipid and lymphocyte membranes; the role of cholesterol PLoS One 7 2012 e38677
18. J. Kubiak, J. Brewer, S. Hansen, and L.A. Bagatolli Lipid lateral organization on giant unilamellar vesicles containing lipopolysaccharides Biophys. J. 100 2011 978 986
19. C. Forestier, E. Moreno, S. Meresse, A. Phalipon, D. Olive, P. Sansonetti, and J.P. Gorvel Interaction of Brucella abortus lipopolysaccharide with major histocompatibility complex class II molecules in B lymphocytes Infect. Immun. 67 1999 4048 4054 (Pubitemid 29357027)
20. C. Forestier, F. Deleuil, N. Lapaque, E. Moreno, and J.P. Gorvel Brucella abortus lipopolysaccharide in murine peritoneal macrophages acts as a down-regulator of T cell activation J. Immunol. 165 2000 5202 5210
21. R.F.M. de Almeida, A. Fedorov, and M. Prieto Sphingomyelin/ phosphatidylcholine/cholesterol phase diagram: boundaries and composition of lipid rafts Biophys. J. 85 2003 2406 2416 (Pubitemid 37210789)
22. J. Velasco, J.A. Bengoechea, K. Brandenburg, B. Lindner, U. Seydel, D. Gonzalez, U. Zahringer, E. Moreno, and I. Moriyon Brucella abortus and its closest phylogenetic relative, Ochrobactrum spp., differ in outer membrane permeability and cationic peptide resistance Infect. Immun. 68 2000 3210 3218 (Pubitemid 30340411)
23. R.W. Martin, and K.W. Zilm Variable temperature system using vortex tube cooling and fiber optic temperature measurement for low temperature magic angle spinning NMR J. Magn. Reson. 168 2004 202 209
24. F. Ciesielski, D.C. Griffin, M. Rittig, and B.B. Bonev High-resolution J-coupled C-13 MAS NMR spectroscopy of lipid membranes Chem. Phys. Lipids 161 2009 77 85
25. S.R. Hartmann, and E.L. Hahn Nuclear double resonance in rotating frame Phys. Rev. 128 1962 2042 2053
26. G. Metz, X.L. Wu, and S.O. Smith Ramped-amplitude cross-polarization in magic-angle-spinning NMR J. Magn. Reson., Ser. A 110 1994 219 227
27. B.M. Fung, A.K. Khitrin, and K. Ermolaev An improved broadband decoupling sequence for liquid crystals and solids J. Magn. Reson. 142 2000 97 101
28. V. Zorin, F. Ciesielski, D.C. Griffin, M. Rittig, and B.B. Bonev Heteronuclear chemical shift correlation and J-resolved MAS NMR spectroscopy of lipid membranes Magn. Reson. Chem. 48 2010 925 934
29. J. Forbes, C. Husted, and E. Oldfield High-field, high-resolution proton magic-angle sample-spinning nuclear magnetic-resonance spectroscopic studies of gel and liquid-crystalline lipid bilayers and the effects of cholesterol J. Am. Chem. Soc. 110 1988 1059 1065 (Pubitemid 18058814)
30. O.A. Valueva, D. Rakhuba, A.S. Shashkov, E.L. Zdorovenko, E. Kiseleva, G. Novik, and Y.A. Knirel Structure of the major O-specific polysaccharide from the lipopolysaccharide of Pseudomonas fluorescens BIM B-582: identification of 4-Deoxy-d-xylo-hexose as a component of bacterial polysaccharides J. Nat. Prod. 74 2011 2161 2167
31. K. Nomura, M. Maeda, K. Sugase, and S. Kusumoto Lipopolysaccharide induces raft domain expansion in membrane composed of a phospholipid- cholesterol-sphingomyelin ternary system Innate Immun. 17 2011 256 268
32. R. Conde-Alvarez, V. Arce-Gorvel, M. Iriarte, M. Mancek-Keber, E. Barquero-Calvo, L. Palacios-Chaves, C. Chacon-Diaz, E. Chaves-Olarte, A. Martirosyan, K. von Bargen, M.J. Grillo, R. Jerala, K. Brandenburg, E. Llobet, J.A. Bengoechea, E. Moreno, I. Moriyon, and J.P. Gorvel The lipopolysaccharide core of Brucella abortus acts as a shield against innate immunity recognition PLoS Pathog. 8 2012
33. N. Sanghera, B.E.F.S. Correia, J.R.S. Correia, C. Ludwig, S. Agarwal, H.K. Nakamura, K. Kuwata, E. Samain, A.C. Gill, B.B. Bonev, and T.J.T. Pinheiro Deciphering the molecular details for the binding of the prion protein to main ganglioside GM1 of neuronal membranes Chem. Biol. 18 2011 1422 1431
34. J. Forbes, J. Bowers, X. Shan, L. Moran, E. Oldfield, and M.A. Moscarello Some new developments in solid-state nuclear magnetic-resonance spectroscopic studies of lipids and biological-membranes, including the effects of cholesterol in model and natural systems J. Chem. Soc., Faraday Trans. 1 84 1988 3821 3849
35. G.P. Holland, and T.M. Alam Multi-dimensional H-1-C-13 HETCOR and FSLG-HETCOR NMR study of sphingomyelin bilayers containing cholesterol in the gel and liquid crystalline states J. Magn. Reson. 181 2006 316 326 (Pubitemid 44107749)
36. J. Velasco, C. Romero, I. Lopez-Goni, J. Leiva, R. Diaz, and I. Moriyon Evaluation of the relatedness of Brucella spp. and Ochrobactrum anthropi and description of Ochrobactrum intermedium sp. nov., a new species with a closer relationship to Brucella spp Int. J. Syst. Bacteriol. 48 1998 759 768 (Pubitemid 28394655)
37. B. Bonev, A. Watts, M. Bokvist, and G. Grobner Electrostatic peptide-lipid interactions of amyloid-beta peptide and pentalysine with membrane surfaces monitored by P-31 MAS NMR Phys. Chem. Chem. Phys. 3 2001 2904 2910 (Pubitemid 32686117)
38. B.B. Bonev, Y.H. Lam, G. Anderluh, A. Watts, R.S. Norton, and F. Separovic Effects of the eukaryotic pore-forming cytolysin equinatoxin II on lipid membranes and the role of sphingomyelin Biophys. J. 84 2003 2382 2392 (Pubitemid 36373561)
39. X.Y. Wang, A.A. Ribeiro, Z.Q. Guan, and C.R.H. Raetz Identification of undecaprenyl phosphate-beta-D-galactosalmine in Francisella novicida and its function in lipid A modification Biochemistry 48 2009 1162 1172
40. B.B. Bonev, E. Breukink, E. Swiezewska, B. De Kruijff, and A. Watts Targeting extracellular pyrophosphates underpins the high selectivity of nisin FASEB J. 18 2004 1862 1869 (Pubitemid 39602271)
41. J. Vestergren, A.G. Vincent, M. Jansson, P. Persson, U. Ilstedt, G. Grobner, R. Giesler, and J. Schleucher High-resolution characterization of organic phosphorus in soil extracts using 2D (1)H-(31)P NMR correlation spectroscopy Environ. Sci. Technol. 46 2012 3950 3956
42. M.I. Torres-Sanchez, C. Zaccaria, B. Buzzi, G. Miglio, G. Lombardi, L. Polito, G. Russo, and L. Lay Synthesis and biological evaluation of phosphono analogues of capsular polysaccharide fragments from Neisseria meningitidis A Chem. Eur. J. 13 2007 6623 6635 (Pubitemid 47240958)
43. J.H. Davis The description of membrane lipid conformation, order and dynamics by H-2-NMR Biochim. Biophys. Acta 737 1983 117 171 (Pubitemid 13129060)
44. P. Garidel, J. Howe, and K. Brandenburg Thermodynamic analysis of the interaction of lipopolysaccharides with cationic compounds Eng. Life Sci. 8 2008 523 529
45. M.W. Hornef, M.J. Wick, M. Rhen, and S. Normark Bacterial strategies for overcoming host innate and adaptive immune responses Nat. Immunol. 3 2002 1033 1040 (Pubitemid 35363654)
46. S. Manes, G. del Real, and C. Martinez-A Pathogens: raft hijackers Nat. Rev. Immunol. 3 2003 557 568 (Pubitemid 37328675)
47. M. Triantafilou, K. Miyake, D.T. Golenbock, and K. Triantafilou Mediators of innate immune recognition of bacteria concentrate in lipid rafts and facilitate lipopolysaccharide-induced cell activation J. Cell Sci. 115 2002 2603 2611 (Pubitemid 34778077)
48. M.J. Duncan, G.J. Li, J.S. Shin, J.L. Carson, and S.N. Abraham Bacterial penetration of bladder epithelium through lipid rafts J. Biol. Chem. 279 2004 18944 18951 (Pubitemid 38623323)
49. C.F. Fortin, O. Lesur, and T. Fulop Effects of TREM-1 activation in human neutrophils: activation of signaling pathways, recruitment into lipid rafts and association with TLR4 Int. Immunol. 19 2007 41 50 (Pubitemid 46017886)
50. M. Triantafilou, S. Morath, A. Mackie, T. Hartung, and K. Triantafilou Lateral diffusion of Toll-like receptors reveals that they are transiently confined within lipid rafts on the plasma membrane J. Cell Sci. 117 2004 4007 4014 (Pubitemid 39207336)
51. X.W. Zhu, J.S. Owen, M.D. Wilson, H.T. Li, G.L. Griffiths, M.J. Thomas, E.M. Hiltbold, M.B. Fessler, and J.S. Parks Macrophage ABCA1 reduces MyD88-dependent Toll-like receptor trafficking to lipid rafts by reduction of lipid raft cholesterol J. Lipid Res. 51 2010 3196 3206
52. N. Sanghera, Bruno E.F.S. Correia, Joana R.S. Correia, C. Ludwig, S. Agarwal, Hironori K. Nakamura, K. Kuwata, E. Samain, Andrew C. Gill, Boyan B. Bonev, and Teresa J.T. Pinheiro Deciphering the molecular details for the binding of the prion protein to main ganglioside GM1 of neuronal membranes Chem. Biol. 18 2011 1422 1431
53. Z.M. Zhou, A.A. Ribeiro, and C.R.H. Raetz High-resolution NMR spectroscopy of lipid A molecules containing 4-amino-4-deoxy-l-arabinose and phosphoethanolamine substituents - different attachment sites on lipid A molecules from NH4VO3-treated Escherichia coli versus kdsA mutants of Salmonella typhimurium J. Biol. Chem. 275 2000 13542 13551 (Pubitemid 30257420)
54. Z.M. Zhou, A.A. Ribeiro, S.H. Lin, R.J. Cotter, S.I. Miller, and C.R.H. Raetz Lipid A modifications in polymyxin-resistant Salmonella typhimurium - PMRA-dependent 4-amino-4-deoxy-l-arabinose, and phosphoethanolamine incorporation J. Biol. Chem. 276 2001 43111 43121
55. N. Lapaque, F. Forquet, C. de Chastellier, Z. Mishal, G. Jolly, E. Moreno, I. Moriyon, J.E. Heuser, H.T. He, and J.P. Gorvel Characterization of Brucella abortus lipopolysaccharide macrodomains as mega rafts Cell. Microbiol. 8 2006 197 206 (Pubitemid 43356043)
56. J. Kubler-Kielb, and E. Vinogradov The study of the core part and non-repeating elements of the O-antigen of Brucella lipopolysaccharide Carbohydr. Res. 366 2013 33 37