Table of Contents Author Guidelines Submit a Manuscript
Mediators of Inflammation
Volume 2013 (2013), Article ID 824919, 12 pages
http://dx.doi.org/10.1155/2013/824919
Research Article

CD14 Mediates Binding of High Doses of LPS but Is Dispensable for TNF-α Production

1Department of Cell Biology, Nencki Institute of Experimental Biology, 3 Pasteur Street, 02-093 Warsaw, Poland
2Ridgeview Instruments AB, Skillsta 4, 740 20 Vänge, Sweden
3Biomedical Radiation Sciences, Department of Radiology, Oncology and Radiation Sciences, Uppsala University, Dag Hammarskjölds väg 20, 751 85 Uppsala, Sweden

Received 30 June 2013; Revised 29 August 2013; Accepted 11 October 2013

Academic Editor: Linda Burkly

Copyright © 2013 Kinga Borzęcka et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. H. Kumar, T. Kawai, and S. Akira, “Pathogen recognition by the innate immune system,” International Reviews of Immunology, vol. 30, no. 1, pp. 16–34, 2011. View at Publisher · View at Google Scholar · View at Scopus
  2. A. Poltorak, X. He, I. Smirnova et al., “Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene,” Science, vol. 282, no. 5396, pp. 2085–2088, 1998. View at Publisher · View at Google Scholar · View at Scopus
  3. H. Björkbacka, K. A. Fitzgerald, F. Huet et al., “The induction of macrophage gene expression by LPS predominantly utilizes Myd88-independent signaling cascades,” Physiological Genomics, vol. 19, no. 3, pp. 319–330, 2004. View at Publisher · View at Google Scholar · View at Scopus
  4. S. M. Opal, P. J. Scannon, J.-L. Vincent et al., “Relationship between plasma levels of lipopolysaccharide (LPS) and LPS-binding protein in patients with severe sepsis and septic shock,” The Journal of Infectious Diseases, vol. 180, no. 5, pp. 1584–1589, 1999. View at Publisher · View at Google Scholar · View at Scopus
  5. R. Salomao, M. K. Brunialti, M. M. Rapozo, G. L. Baggio-Zappia, C. Galanos, and M. Freudenberg, “Bacterial sensing, cell signaling, and modulation of the immune response during sepsis,” Shock, vol. 38, no. 3, pp. 227–242, 2012. View at Publisher · View at Google Scholar
  6. C. Erridge, E. Bennett-Guerrero, and I. R. Poxton, “Structure and function of lipopolysaccharides,” Microbes and Infection, vol. 4, no. 8, pp. 837–851, 2002. View at Publisher · View at Google Scholar · View at Scopus
  7. C. R. Raetz and C. Whitfield, “Lipopolysaccharide endotoxins,” Annual Review of Biochemistry, vol. 71, pp. 635–700, 2002. View at Publisher · View at Google Scholar · View at Scopus
  8. M. G. Rittig, A. Kaufmann, A. Robins et al., “Smooth and rough lipopolysaccharide phenotypes of Brucella induce different intracellular trafficking and cytokine/chemokine release in human monocytes,” Journal of Leukocyte Biology, vol. 74, no. 6, pp. 1045–1055, 2003. View at Publisher · View at Google Scholar · View at Scopus
  9. Z. Jiang, P. Georgel, X. Du et al., “CD14 is required for MyD88-independent LPS signaling,” Nature Immunology, vol. 6, no. 6, pp. 565–570, 2005. View at Publisher · View at Google Scholar · View at Scopus
  10. M. Huber, C. Kalis, S. Keck et al., “R-form LPS, the master key to the activation of TLR4/MD-2-positive cells,” European Journal of Immunology, vol. 36, no. 3, pp. 701–711, 2006. View at Publisher · View at Google Scholar · View at Scopus
  11. P. S. Tobias, K. Soldau, L. Kline et al., “Cross-linking of lipopolysaccharide (LPS) to CD14 on THP-1 cells mediated by LPS-binding protein,” The Journal of Immunology, vol. 150, no. 7, pp. 3011–3021, 1993. View at Google Scholar · View at Scopus
  12. J.-I. Kim, J. L. Chang, S. J. Mi et al., “Crystal structure of CD14 and its implications for lipopolysaccharide signaling,” The Journal of Biological Chemistry, vol. 280, no. 12, pp. 11347–11351, 2005. View at Publisher · View at Google Scholar · View at Scopus
  13. J. Meng, P. Parroche, D. T. Golenbock, and C. J. McKnight, “The differential impact of disulfide bonds and N-linked glycosylation on the stability and function of CD14,” The Journal of Biological Chemistry, vol. 283, no. 6, pp. 3376–3384, 2007. View at Publisher · View at Google Scholar · View at Scopus
  14. T. Horng, G. M. Barton, R. A. Flavell, and R. Medzhitov, “The adaptor molecule TIRAP provides signalling specificity for Toll-like receptors,” Nature, vol. 420, no. 6913, pp. 329–333, 2002. View at Publisher · View at Google Scholar · View at Scopus
  15. M. Yamamoto, S. Sato, H. Hemmi et al., “TRAM is specifically involved in the Toll-like receptor 4-mediated MyD88-independent signaling pathway,” Nature Immunology, vol. 4, no. 11, pp. 1144–1150, 2003. View at Publisher · View at Google Scholar · View at Scopus
  16. B. S. Park, D. H. Song, H. M. Kim, B.-S. Choi, H. Lee, and J.-O. Lee, “The structural basis of lipopolysaccharide recognition by the TLR4-MD-2 complex,” Nature, vol. 458, no. 7242, pp. 1191–1195, 2009. View at Publisher · View at Google Scholar · View at Scopus
  17. G. Panter and R. Jerala, “The ectodomain of the Toll-Like receptor 4 prevents constitutive receptor activation,” The Journal of Biological Chemistry, vol. 286, no. 26, pp. 23334–23344, 2011. View at Publisher · View at Google Scholar · View at Scopus
  18. I. Zanoni, R. Ostuni, L. R. Marek et al., “CD14 controls the LPS-induced endocytosis of Toll-Like receptor 4,” Cell, vol. 147, no. 4, pp. 868–880, 2011. View at Publisher · View at Google Scholar · View at Scopus
  19. R. Y. Hampton, D. T. Golenbock, M. Penman, M. Krieger, and C. R. Raetz, “Recognition and plasma clearance of endotoxin by scavenger receptors,” Nature, vol. 352, no. 6333, pp. 342–344, 1991. View at Publisher · View at Google Scholar · View at Scopus
  20. R. Haworth, N. Platt, S. Keshav et al., “The macrophage scavenger receptor type A is expressed by activated macrophages and protects the host against lethal endotoxic shock,” The Journal of Experimental Medicine, vol. 186, no. 9, pp. 1431–1439, 1997. View at Publisher · View at Google Scholar · View at Scopus
  21. S. Dunzendorfer, R.-K. Lee, K. Soldau, and P. S. Tobias, “TLR4 is the signaling but not the lipopolysaccharide uptake receptor,” The Journal of Immunology, vol. 173, no. 2, pp. 1166–1170, 2004. View at Google Scholar · View at Scopus
  22. M. Czerkies, K. Borzęcka, M. I. Zdioruk, A. Płóciennikowska, A. Sobota, and K. Kwiatkowska, “An interplay between scavenger receptor A and CD14 during activation of J774 cells by high concentrations of LPS,” Immunobiology, vol. 218, no. 10, pp. 1217–1226, 2013. View at Publisher · View at Google Scholar
  23. A. Pfeiffer, A. Böttcher, E. Orsó et al., “Lipopolysaccharide and ceramide docking to CD14 provokes ligand-specific receptor clustering in rafts,” European Journal of Immunology, vol. 31, no. 11, pp. 3153–3164, 2001. View at Publisher · View at Google Scholar
  24. M. Triantafilou, K. Brandenburg, S. Kusumoto et al., “Combinational clustering of receptors following stimulation by bacterial products determines lipopolysaccharide responses,” Biochemical Journal, vol. 381, no. 2, pp. 527–536, 2004. View at Publisher · View at Google Scholar · View at Scopus
  25. K. Triantafilou, M. Triantafilou, and R. L. Dedrick, “A CD14-independent LPS receptor cluster,” Nature Immunology, vol. 2, no. 4, pp. 338–345, 2001. View at Publisher · View at Google Scholar · View at Scopus
  26. M. Triantafilou, P. M. Lepper, C. D. Briault et al., “Chemokine receptor 4 (CXCR4) is part of the lipopolysaccharide ‘sensing apparatus’,” European Journal of Immunology, vol. 38, no. 1, pp. 192–203, 2008. View at Publisher · View at Google Scholar · View at Scopus
  27. K. Triantafilou, M. Triantafilou, and N. Fernandez, “Lipopolysaccharide (LPS) labeled with Alexa 488 hydrazide as a novel probe for LPS binding studies,” Cytometry, vol. 41, no. 4, pp. 316–320, 2000. View at Publisher · View at Google Scholar
  28. H. Björke and K. Andersson, “Automated, high-resolution cellular retention and uptake studies in vitro,” Applied Radiation and Isotopes, vol. 64, no. 8, pp. 901–905, 2006. View at Publisher · View at Google Scholar · View at Scopus
  29. Y. Adachi, C. Satokawa, M. Saeki et al., “Inhibition by a CD14 monoclonal antibody of lipopolysaccharide binding to murine macrophages,” Journal of Endotoxin Research, vol. 5, no. 3, pp. 139–146, 1999. View at Publisher · View at Google Scholar · View at Scopus
  30. N. W. Schröder, H. Heine, C. Alexander et al., “Lipopolysaccharide binding protein binds to triacylated and diacylated lipopeptides and mediates innate immune responses,” Journal of Immunology, vol. 173, no. 4, pp. 2683–2691, 2004. View at Google Scholar · View at Scopus
  31. N. J. Nilsen, S. Deininger, U. Nonstad et al., “Cellular trafficking of lipoteichoic acid and Toll-like receptor 2 in relation to signaling; role of CD14 and CD36,” Journal of Leukocyte Biology, vol. 84, no. 1, pp. 280–291, 2008. View at Publisher · View at Google Scholar · View at Scopus
  32. D. R. Ranoa, S. L. Kelley, and R. I. Tapping, “Human lipopolysaccharide-binding protein (LBP) and CD14 independently deliver triacylated lipoproteins to Toll-like receptor 1 (TLR1) and TLR2 and enhance formation of the ternary signaling complex,” The Journal of Biological Chemistry, vol. 288, no. 14, pp. 9729–9741, 2013. View at Publisher · View at Google Scholar
  33. G. V. Limmon, M. Arredouani, K. L. McCann, R. A. C. Minor, L. Kobzik, and F. Imani, “Scavenger receptor class-A is a novel cell surface receptor for double-stranded RNA,” The FASEB Journal, vol. 22, no. 1, pp. 159–167, 2008. View at Publisher · View at Google Scholar · View at Scopus
  34. L. Peiser and S. Gordon, “The function of scavenger receptors expressed by macrophages and their rolein the regulation of inflammation,” Microbes and Infection, vol. 3, no. 2, pp. 149–159, 2001. View at Publisher · View at Google Scholar · View at Scopus
  35. W.-J. Lin and W.-C. Yeh, “Implication of Toll-Like receptor and tumor necrosis factor α signaling in septic shock,” Shock, vol. 24, no. 3, pp. 206–209, 2005. View at Publisher · View at Google Scholar · View at Scopus
  36. D.-E. Zhang, C. J. Hetherington, D. A. Gonzalez, H.-M. Chen, and D. G. Tenen, “Regulation of CD14 expression during monocytic differentiation induced with 1 α,25-dihydroxyvitamin D3,” Journal of Immunology, vol. 153, no. 7, pp. 3276–3285, 1994. View at Google Scholar · View at Scopus
  37. T. L. Gioannini, A. Teghanemt, D. Zhang, E. N. Levis, and J. P. Weiss, “Monomeric endotoxin: protein complexes are essential for TLR4-dependent cell activation,” Journal of Endotoxin Research, vol. 11, no. 2, pp. 117–123, 2005. View at Publisher · View at Google Scholar · View at Scopus
  38. G. A. Esparza, A. Teghanemt, T. L. Gioannini, and J. P. Weiss, “Endotoxin·albumin complexes transfer endotoxin monomers to MD-2 resulting in activation of TLR4,” Innate Immunology, vol. 18, no. 3, pp. 478–491, 2012. View at Publisher · View at Google Scholar
  39. I. Zanoni, C. Bodio, A. Broggi et al., “Similarities and differences of innate immune responses elicited by smooth and rough LPS,” Immunology Letters, vol. 142, no. 1-2, pp. 41–47, 2012. View at Publisher · View at Google Scholar · View at Scopus
  40. E. Pupo, B. Lindner, H. Brade, and A. B. Schromm, “Intact rough- and smooth-form lipopolysaccharides from Escherichia coli separated by preparative gel electrophoresis exhibit differential biologic activity in human macrophages,” The FEBS Journal, vol. 280, no. 4, pp. 1095–1111, 2013. View at Publisher · View at Google Scholar
  41. M. Mueller, B. Lindner, S. Kusumoto, K. Fukase, A. B. Schromm, and U. Seydel, “Aggregates are the biologically active units of endotoxin,” The Journal of Biological Chemistry, vol. 279, no. 25, pp. 26307–26313, 2004. View at Publisher · View at Google Scholar · View at Scopus
  42. S. Watanabe, Y. Kumazawa, and J. Inoue, “Liposomal lipopolysaccharide initiates TRIF dependent signaling pathway independent of CD14,” PLoS One, vol. 8, no. 3, Article ID e60078, 2013. View at Publisher · View at Google Scholar
  43. C. Poussin, M. Foti, J.-L. Carpentier, and J. Pugin, “CD14-dependent endotoxin internalization via a macropinocytic pathway,” The Journal of Biological Chemistry, vol. 273, no. 32, pp. 20285–20291, 1998. View at Publisher · View at Google Scholar · View at Scopus
  44. S. Mukhopadhyay, A. Varin, Y. Chen, B. Liu, K. Tryggvason, and S. Gordon, “SR-A/MARCO-mediated ligand delivery enhances intracellular TLR and NLR function, but ligand scavenging from cell surface limits TLR4 response to pathogens,” Blood, vol. 117, no. 4, pp. 1319–1328, 2011. View at Publisher · View at Google Scholar · View at Scopus
  45. H. Yu, T. Ha, I. Liu et al., “Scavenger receptor A (SR-A) is required for LPS-induced TLR4 mediated NF-κB activation in macrophages,” Biochimica and Biophysica Acta, vol. 1823, no. 7, pp. 1192–1198, 2012. View at Publisher · View at Google Scholar
  46. 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,” Journal of Cell Science, vol. 115, no. 12, pp. 2603–2611, 2002. View at Google Scholar · View at Scopus
  47. T. Kiyanagi, K. Iwabuchi, K. Shimada et al., “Involvement of cholesterol-enriched microdomains in class A scavenger receptor-mediated responses in human macrophages,” Atherosclerosis, vol. 215, no. 1, pp. 60–69, 2011. View at Publisher · View at Google Scholar · View at Scopus
  48. J. Ben, Y. Zhang, R. Zhou et al., “Major vault protein regulates class A scavenger receptor-mediated tumor necrosis factor-α synthesis and apoptosis in macrophages,” The Journal of Biological Chemistry, vol. 288, no. 27, pp. 20076–20084, 2013. View at Publisher · View at Google Scholar