Activation of Human Toll-like receptor 4 (TLR4)·myeloid differentiation factor 2 (MD-2) by hypoacylated lipopolysaccharide from a clinical isolate of Burkholderia cenocepacia

Journal of Biological Chemistry

Volumn 290, Issue 35, 2015, Pages 21305-21319

  Di Lorenzo, Flaviana ^a,d   Kubik, Łukasz ^b,c   Oblak, Alja ^d,e   Lorè, Nicola Ivan ^f   Cigana, Cristina ^f   Lanzetta, Rosa ^a   Parrilli, Michelangelo ^a   Hamad, Mohamad A ^g   De Soyza, Anthony ^h   Silipo, Alba ^a   Jerala, Roman ^d,e   Bragonzi, Alessandra ^f   Valvano, Miguel A ^g,i   Martín Santamaría, Sonsoles ^b   Molinaro, Antonio ^a  

^a UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^b UNIVERSIDAD SAN PABLO CEU   (Spain)

^c MEDICAL UNIVERSITY OF GDANSK   (Poland)

^d NATIONAL INSTITUTE OF CHEMISTRY   (Slovenia)

^e Excellent NMR   (Slovenia)

^f SAN RAFFAELE HOSPITAL   (Italy)

^g UNIVERSITY OF WESTERN ONTARIO   (Canada)

^h NEWCASTLE UNIVERSITY   (United Kingdom)

ⁱ QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ACYLATION; BIOLOGICAL ORGANS; CHAINS; MOLECULAR MODELING;

CLINICAL ISOLATES; ENDOTOXIC SHOCK; INTERACTIVE SURFACES; LIPOPOLYSACCHARIDES; MYELOID DIFFERENTIATION; PROINFLAMMATORY RESPONSE; RECEPTOR COMPLEX; TOLL-LIKE RECEPTOR 4;

CHEMICAL ACTIVATION;

BACTERIAL PROTEIN; LIPID A; MYELOID DIFFERENTIATION FACTOR 2; TOLL LIKE RECEPTOR 4; UNCLASSIFIED DRUG; INTERLEUKIN 6; LY96 PROTEIN, HUMAN; PROTEIN MD 2;

ANIMAL EXPERIMENT; ARTICLE; BACTERIAL VIRULENCE; BACTERIUM ISOLATE; BURKHOLDERIA CENOCEPACIA; CELL ACTIVATION; CHEMICAL MODIFICATION; COMPLEX FORMATION; CONTROLLED STUDY; DIMERIZATION; EMBRYO; HUMAN; HUMAN CELL; LONG TERM EXPOSURE; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; SURFACE PROPERTY; ACYLATION; ANIMAL; BURKHOLDERIA INFECTION; C57BL MOUSE; CELL LINE; CHEMISTRY; HEK293 CELL LINE; IMMUNOLOGY; INFLAMMATION; INNATE IMMUNITY; ISOLATION AND PURIFICATION; MICROBIOLOGY; MOLECULAR DOCKING;

ACYLATION; ANIMALS; BURKHOLDERIA CENOCEPACIA; BURKHOLDERIA INFECTIONS; CELL LINE; HEK293 CELLS; HUMANS; IMMUNITY, INNATE; INFLAMMATION; INTERLEUKIN-6; LIPID A; LYMPHOCYTE ANTIGEN 96; MICE, INBRED C57BL; MOLECULAR DOCKING SIMULATION; TOLL-LIKE RECEPTOR 4;

EID: 84940563505     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.649087     Document Type: Article

References (59)

1. Janeway, C. A., Jr., and Medzhitov, R. (2002) Innate immune recognition. Annu. Rev. Immunol. 20, 197-216
2. Gay, N. J., and Gangloff, M. (2007) Structure and function of Toll receptors and their ligands. Annu. Rev. Biochem. 76, 141-165
3. Broz, P., and Monack, D. M. (2013) Newly described pattern recognition receptors team up against intracellular pathogens. Nat. Rev. Immunol. 13, 551-565
4. Nagai, Y., Akashi, S., Nagafuku, M., Ogata, M., Iwakura, Y., Akira, S., Kitamura, T., Kosugi, A., Kimoto, M., and Miyake, K. (2002) Essential role of MD-2 in LPS responsiveness and TLR4 distribution. Nat. Immunol. 3, 667-672
5. Angus, D. C., Linde-Zwirble, W. T., Lidicker, J., Clermont, G., Carcillo, J., and Pinsky, M. R. (2001) Epidemiology of severe sepsis in the United States: analysis of incidence, outcome, and associated costs of care. Crit. Care Med. 29, 1303-1310
6. Rangel-Frausto, M. S. (2005) Sepsis: still going strong. Arch. Med. Res. 36, 672-681
7. Raetz, C. R., and Whitfield, C., (2002) Lipopolysaccharide endotoxins. Annu. Rev. Biochem. 71, 635-700
8. Holst, O., and Molinaro, A. (2009) in Microbial Glycobiology: Structures Relevance and Applications (Moran, A. P., Holst, O., Brennan, P. J., von Itzstein, M., eds) pp. 29-56, Elsevier, San Diego, CA
9. Knirel, Y. (2009) in Microbial Glycobiology: Structures Relevance and Applications (Moran, A. P., Holst, O., Brennan, P. J., von Itzstein, M., eds) pp. 57-74, Elsevier, San Diego, CA
10. Silipo, A., Erbs, G., Shinya, T., Dow, J. M., Parrilli, M., Lanzetta, R., Shibuya, N., Newman, M. A., and Molinaro, A. (2010) Glyco-conjugates as elicitors or suppressors of plant innate immunity. Glycobiology 20, 406-419
11. Brandenburg, K., Mayer, H., Koch, M. H., Weckesser, J., Rietschel, E. T., and Seydel, U. (1993) Influence of the supramolecular structure of free lipid A on its biological activity. Eur. J. Biochem. 218, 555-563
12. Rietschel, E. T., Kirikae, T., Schade, F. U., Mamat, U., Schmidt, G., Schmidt, G., Loppnow, H., Ulmer, A. J., Zähringer, U., Seydel, U., Di Padova, F., Schreier, M., and Brade, H. (1994) Bacterial endotoxin: molecular relationships of structure to activity and function. FASEB J. 8, 217-225
13. Brandeburg, K., Seydel, U., Schromm, A. B., Loppnow, H., Koch, M. H., and Rietschel, E. T. (1996) Conformation of lipid A, the endotoxic centre of the bacterial lipopolysaccharide. J. Endotoxin Res. 3, 173-178
14. Seydel, U., Oikawa, M., Fukase, K., Kusumoto, S., and Brandenburg, K. (2000) Intrinsic conformation of lipid A is responsible for agonistic and antagonistic activity. Eur. J. Biochem. 267, 3032-3039
15. Schromm, A. B., Brandenburg, K., Loppnow, H., Moran, A. P., Koch, M.H.,Rietschel,E.T.,andSeydel,U.(2000)Biologicalactivitiesoflipopolysaccharides are determined by the shape of their lipid A portion. Eur. J. Biochem. 267, 2008-2013
16. Fukuoka, S., Brandenburg, K., Müller, M., Lindner, B., Koch, M. H., and Seydel, U. (2001) Physico-chemical analysis of lipid A fractions of lipopolysaccharide from Erwinia carotovora in relation to bioactivity. Biochim. Biophys. Acta 1510, 185-197
17. Oikawa, M., Shintaku, T., Fukuda, N., Sekljic, H., Fukase, Y., Yoshizaki, H., Fukase K., and Kusumoto, S. (2004) NMR conformational analysis of biosynthetic precursor-type lipid A: monomolecular state and supramolecular assembly. Org. Biomol. Chem. 2, 3557-3565
18. Park, B. S., Song, D. H., Kim, H. M., Choi, B. S., Lee, H., and Lee, J. O. (2009) The structural basis of lipopolysaccharide recognition by the TLR4-MD-2 complex. Nature 458, 1191-1195
19. Maeshima, N., and Fernandez, R.C. (2013) Recognition of lipid A variants by the TLR4-MD-2 receptor complex. Front. Cell. Infect. Microbiol. 3, 3
20. Golenbock, D. T., Hampton, R. Y., Qureshi, N., Takayama, K., and Raetz, C. R. (1991) Lipid A-like molecules that antagonize the effects of endotoxins on human monocytes. J. Biol. Chem. 266, 19490-19498
21. Klett, J., Reeves, J., Oberhauser, N., Pérez-Regidor, L., and Martín-Santamaria, S. (2014) Modulation of toll-like receptor 4. Insights from x-ray crystallography and molecular modeling. Curr. Top. Med. Chem. 14, 2672-2683
22. Resman, N., Vasl, J., Oblak, A., Pristovsek, P., Gioannini, T. L., Weiss, J. P., and Jerala, R. (2009) Essential roles of hydrophobic residues in both MD-2 and toll-like receptor 4 in activation by endotoxin. J. Biol. Chem. 284, 15052-15060
23. A. Science 316, 1632-1634
24. Ernst, R. K., Yi, E. C., Guo, L., Lim, K. B., Burns, J. L., Hackett, M., and Miller, S. I. (1999) Specific lipopolysaccharide found in cystic fibrosis airway Pseudomonas aeruginosa. Science 286, 1561-1565
25. Lohmann, K. L., Vandenplas, M. L., Barton, M. H., Bryant, C. E., and Moore, J. N. (2007) The equine TLR4/MD-2 complex mediates recognition of lipopolysaccharide from Rhodobacter sphaeroides as an agonist. J. Endotoxin Res. 13, 235-242
26. Saitoh, S., Akashi, S., Yamada, T., Tanimura, N., Kobayashi, M., Konno, K., Matsumoto, F., Fukase, K., Kusumoto, S., Nagai, Y., Kusumoto, Y., Kosugi, A., and Miyake, K. (2004) Lipid A antagonist, lipid IVA, is distinct from lipid A in interaction with Toll-like receptor 4 (TLR4)-MD-2 and ligand-induced TLR4 oligomerization. Int. Immunol. 16, 961-969
27. Hajjar, A. M., Ernst, R. K., Tsai, J. H., Wilson, C. B., and Miller, S. I. (2002) Human Toll-like receptor 4 recognizes host-specific LPS modifications. Nat. Immunol. 3, 354-359
28. Herath, T. D., Darveau, R. P., Seneviratne, C. J., Wang, C.Y., Wang, Y., and Jin, L. (2013) Tetra- and Penta-acylated lipid A structures of Porphyromonas gingivalis LPS differentially activate TLR4-mediated NF-κB signal transduction cascade and immuno-inflammatory response in human gingival fibroblasts. PLoS One 8, e58496
29. Speert, D. P. (2002) Advances in Burkholderia cepacia complex. Paediatr. Respir. Rev. 3, 230-235
30. Hamad, M. A., Di Lorenzo, F., Molinaro, A., and Valvano, M. A. (2012) Aminoarabinose is essential for lipopolysaccharide export and intrinsic antimicrobial peptide resistance in Burkholderia cenocepacia. Mol. Microbiol. 85, 962-974
31. Ortega, X. P., Cardona, S. T., Brown, A. R., Loutet, S. A., Flannagan, R. S., Campopiano, D. J., Govan, J. R., and Valvano, M. A. (2007) A putative gene cluster for aminoarabinose biosynthesis is essential for Burkholderia cenocepacia viability. J. Bacteriol. 189, 3639-3644
32. Zughaier, S. M., Ryley, H. C., and Jackson, S. K. (1999) Lipopolysaccharide (LPS) from Burkholderia cepacia is more active than LPS from Pseudomonas aeruginosa and Stenotrophomonas maltophilia in stimulating tumor necrosis factor alpha from human monocytes. Infect. Immun. 67, 1505-1507
33. De Soyza, A., Ellis, C. D., Khan, C. M., Corris, P. A., and Demarco de Hormaeche, R. (2004) Burkholderia cenocepacia lipopolysaccharide, lipid A, and proinflammatory activity. Am. J. Respir. Crit. Care Med. 170, 70-77
34. Bamford, S., Ryley, H., and Jackson, S. K.(2007) Highly purified lipopolysaccharides from Burkholderia cepacia complex clinical isolates induce inflammatory cytokine responses via TLR4-mediated MAPK signalling pathways and activation of NFκB. Cell. Microbiol. 9, 532-543
35. Silipo, A., Molinaro, A., Ieranò, T., De Soyza, A., Sturiale, L., Garozzo, D., Aldridge, C., Corris, P. A., Khan, C. M., Lanzetta, R., and Parrilli, M. (2007) The complete structure and pro-inflammatory activity of the lipooligosaccharide of the highly epidemic and virulent gram-negative bacterium Burkholderia cenocepacia ET-12 (strain J2315). Chem. Eur. J. 13, 3501-3511
36. Hollaus, R., Ittig, S., Hofinger, A., Haegman, M., Beyaert, R., Kosma, P., and Zamyatina, A. (2015) Chemical synthesis of Burkholderia lipid A modified with glycosyl phosphodiester-linked 4-amino-4-deoxy-β-L-arabinose and its immunomodulatory potential. Chem. Eur. J. 21, 4102-4114
37. Di Lorenzo, F., Silipo, A., Bianconi, I., Lore', N. I., Scamporrino, A., Sturiale, L., Garozzo, D., Lanzetta, R., Parrilli, M., Bragonzi, A., and Molinaro, A. (2015) Persistent cystic fibrosis isolate Pseudomonas aeruginosa strain RP73 exhibits an under-acylated LPS structure responsible of its low inflammatory activity. Mol. Immunol. 63, 166-175
38. Jeukens, J., Boyle, B., Bianconi, I., Kukavica-Ibrulj, I., Tümmler, B., Bragonzi, A., and Levesque, R. C. (2013) Complete genome sequence of persistent cystic fibrosis isolate Pseudomonas aeruginosa strain RP73. Genome Announc. 1, e00568-13
39. Westphal, O. J., and Jann, K. (1965) Bacterial lipopolysaccharides: extraction with phenol-water and further applications of the procedure. Methods Carbohydr. Chem. 5, 83-91
40. Kittelberger, R., and Hilbink, F. (1993) Sensitive silver-staining detection of bacterial lipopolysaccharides in polyacrylamide gels. J. Biochem. Biophys. Methods 26, 81-86
41. Ortega, X., Silipo, A., Saldías, M. S., Bates, C. C., Molinaro, A., and Valvano, M. A. (2009) Biosynthesis and structure of the Burkholderia cenocepacia K56-2 lipopolysaccharide core oligosaccharide: truncation of the core oligosaccharide leads to increased binding and sensitivity to polymyxin B. J. Biol. Chem. 284, 21738-21751
42. Schrödinger (2012) Suite 2012: Maestro, version 9.3, Schrödinger, LLC, New York
43. Frisch, M. J., Trucks, G. W., Schlegel, H. B., Scuseria, G. E., Robb, M. A., Cheeseman, J. R., Montgomery, J. A., Jr., Vreven, T., Kudin, K. N., Burant, J. C., Millam, J. M., Iyengar, S. S., Tomasi, J., Barone, V., Mennucci, B., Cossi, M., Scalmani, G., Rega, N., Petersson, G. A., Nakatsuji, H., Hada, M., Ehara, M., Toyota, K., Fukuda, R., Hasegawa, J., Ishida, M., Nakajima, T., Honda, Y., Kitao, O., Nakai, H., Klene, M., Li, X., Knox, J. E., Hratchian, H. P., Cross, J. B., Bakken, V., Adamo, C., Jaramillo, J., Gomperts, R., Stratmann, R. E., Yazyev, O., Austin, A. J., Cammi, R., Pomelli, C., Ochterski, J. W., Ayala, P. Y., Morokuma, K., Voth, G. A., Salvador, P., Dannenberg, J. J., Zakrzewski, V. G., Dapprich, S., Daniels, A. D., Strain, M. C., Farkas, O., Malick, D. K., Rabuck, A. D., Raghavachari, K., Foresman, J. B., Ortiz, J. V., Cui, Q., Baboul, A. G., Clifford, S., Cioslowski, J., Stefanov, B. B., Liu, G., Liashenko, A., Piskorz, P., Komaromi, I., Martin, R. L., Fox, D. J., Keith, T., Al-Laham, M. A., Peng, C. Y., Nanayakkara, A., Challacombe, M., Gill, P. M. W., Johnson, B., Chen, W., Wong, M. W., Gonzalez, C., and Pople, J. A. (2004) Gaussian 03, Revision E.01, Gaussian, Inc., Wallingford, CT
44. Schrödinger (2012) Suite 2012: MacroModel, version 9.9, Schrödinger, LLC, New York
45. Schrödinger (2012) Suite 2012: Impact, version 5.8, Schrödinger, LLC, New York, NY
46. Schrödinger (2012) Suite 2012: Protein Preparation Wizard: Epik, version 2.3; Impact, version 5.8; Prime, version 3.1, Schrödinger, LLC, New York
47. Goodsell, D. S., Morris, G. M., and Olson, A. J. (1996) Automated docking of flexible ligands: applications of AutoDock. J. Mol. Recognit. 9, 1-5
48. Trott, O., and Olson, A. J. (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
49. Morris, G. M., Huey, R., Lindstrom, W., Sanner, M. F., Belew, R. K., Goodsell, D. S., and Olson, A. J. (2009) AutoDock4 and AutoDockTools4: automated docking with selective receptor flexibility. J. Comput. Chem. 30, 2785-2791
50. Klett, J., Núñez-Salgado, A., Dos Santos, H. G., Corteôs-Cabrera, A., Perona, A., Gil-Redondo, R., Abia, D., Gago, F., and Morreale, A. (2012) MM-ISMSA: an ultrafast and accurate scoring function for protein-protein docking. J. Chem. Theory Comput. 9, 3395-3408
51. A. J. Biol. Chem. 285, 27935-27943
52. Ohto, U., Fukase, K., Miyake, K., and Shimizu, T., (2012) Structural basis of species-specific endotoxin sensing by innate immune receptor TLR4/MD-2. Proc. Natl. Acad. Sci. U.S.A. 109, 7421-7426
53. Kobayashi, M., Saitoh, S., Tanimura, N., Takahashi, K., Kawasaki, K., Nishijima, M., Fujimoto, Y., Fukase, K., Akashi-Takamura, S., and Miyake, K. (2006) Regulatory roles for MD-2 and TLR4 in ligand-induced receptor clustering. J. Immunol. 176, 6211-6518
54. Molinaro, A., Holst, O., Di Lorenzo, F., Callaghan, M., Nurisso, A., D'Errico, G., Zamyatina, A., Peri, F., Berisio, R., Jerala, R., Jiménez-Barbero, J., Silipo, A., and Martín-Santamaría, S. (2015) Chemistry of lipid A: at the heart of innate immunity. Chem. Eur. J. 21, 500-519
55. Bainbridge, B. W., Coats, S. R., Pham, T. T., Reife, R. A., and Darveau, R. P. (2006) Expression of a Porphyromonas gingivalis lipid A palmitylacyltransferase in Escherichia coli yields a chimeric lipid A with altered ability to stimulate interleukin-8 secretion. Cell. Microbiol. 8, 120-129
56. Maeshima, N., Evans-Atkinson, T., Hajjar, A. M., and Fernandez, R. C. (2015) Bordetella pertussis lipid A recognition by Toll-like receptor 4 and MD-2 is dependent on distinct charged and uncharged interfaces. J. Biol. Chem. 290, 13440-13453
57. Gruber, A., Mancek, M., Wagner, H., Kirschning, C. J., and Jerala, R. (2004) Structural model of MD-2 and functional role of its basic amino acid clusters involved in cellular lipopolysaccharide recognition. J. Biol. Chem. 279, 28475-28482
58. Re, F., and Strominger, J. L. (2003) Separate functional domains of human MD-2 mediate Toll-like receptor 4-binding and lipopolysaccharide responsiveness. J. Immunol. 171, 5272-5276
59. Visintin, A., Latz, E., Monks, B. G., Espevik, T., and Golenbock, D. T. (2003) Lysines 128 and 132 enable lipopolysaccharide binding to MD-2, leading to Toll-like receptor-4 aggregation and signal transduction. J. Biol. Chem. 278, 48313-48320