LPS-induced clustering of CD14 triggers generation of PI(4,5)P2

Journal of Cell Science

Volumn 128, Issue 22, 2015, Pages 4096-4111

  Płóciennikowska, Agnieszka ^a   Zdioruk, Mykola I ^a   Traczyk, Gabriela ^a   Światkowska, Anna ^a   Kwiatkowska, Katarzyna ^a  

^a NENCKI INSTITUTE OF EXPERIMENTAL BIOLOGY   (Poland)

Author keywords

CD14; Lipopolysaccharide; Phosphatidylinositol 4,5 bisphosphate; TLR4

Indexed keywords

BACTERIUM LIPOPOLYSACCHARIDE; CD14 ANTIGEN; PHOSPHATIDYLINOSITOL 4 PHOSPHATE KINASE; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE; RNA; TOLL LIKE RECEPTOR 4; LIPOPOLYSACCHARIDE;

ANIMAL CELL; ANTIGEN EXPRESSION; ARTICLE; CELL MEMBRANE; CONTROLLED STUDY; DOWNSTREAM PROCESSING; EMBRYO; GENE SILENCING; HEK293 CELL LINE; HUMAN; HUMAN CELL; IMMUNOSTIMULATION; IN VITRO STUDY; INFLAMMATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; ANIMAL; DRUG EFFECTS; MACROPHAGE; METABOLISM; SIGNAL TRANSDUCTION;

ANIMALS; ANTIGENS, CD14; HUMANS; LIPOPOLYSACCHARIDES; MACROPHAGES; MICE; PHOSPHATIDYLINOSITOL 4,5-DIPHOSPHATE; SIGNAL TRANSDUCTION;

EID: 84949844935     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.173104     Document Type: Article

References (69)

1. Aksoy, E., Taboubi, S., Torres, D., Delbauve, S., Hachani, A., Whitehead, M. A., Pearce, W. P., Berenjeno, I. M., Nock, G., Filloux, A. et al. (2012). The p110d isoform of the kinase PI(3)K controls the subcellular compartmentalization of TLR4 signaling and protects from endotoxic shock. Nat. Immunol. 13, 1045-1054.
2. Antal-Szalmas, P., Poppelier, M. J. J. G., Broekhuizen, R., Verhoef, J., van Strijp, J. A. G. and van Kessel, K. P. M. (2000). Diverging pathways for lipopolysaccharide and CD14 in human monocytes. Cytometry 41, 279-288.
3. Balla, A., Kim, Y. J., Varnai, P., Szentpetery, Z., Knight, Z., Shokat, K. M. and Balla, T. (2008). Maintenance of hormone-sensitive phosphoinositide pools in the plasma membrane requires phosphatidylinositol 4-kinase IIIa. Mol. Biol. Cell 19, 711-721.
4. Barylko, B., Mao, Y. S., Wlodarski, P., Jung, G., Binns, D. D., Sun, H.-Q., Yin, H. L. and Albanesi, J. P. (2009). Palmitoylation controls the catalytic activity and subcellular distribution of phosphatidylinositol 4-kinase IIa. J. Biol. Chem. 284, 9994-10003.
5. Bjorkbacka, H., Fitzgerald, K. A., Huet, F., Li, X., Gregory, J. A., Lee, M. A., Ordija, C. M., Dowley, N. E., Golenbock, D. T. and Freeman, M.W. (2004). The induction of macrophage gene expression by LPS predominantly utilizes Myd88-independent signaling cascades. Physiol. Genomics 19, 319-330.
6. Borzecka, K., Plociennikowska, A., Bjorkelund, H., Sobota, A. and Kwiatkowska, K. (2013). CD14 mediates binding of high doses of LPS but is dispensable for TNF-α production. Mediators Inflamm. 2013, 824919.
7. Brown, D. A. (2002). Isolation and use of rafts. Curr. Protoc. Immunol. Chapter 11: Unit 11.10, 11.10.1-11.10-23.
8. Chaudhuri, A., Bhattacharya, B., Gowrishankar, K., Mayor, S. and Rao, M. (2011). Spatiotemporal regulation of chemical reactions by active cytoskeletal remodeling. Proc. Natl. Acad. Sci. USA 108, 14825-14830.
9. Chiang, C.-Y., Veckman, V., Limmer, K. and David, M. (2012). Phospholipase Cγ-2 and intracellular calcium are required for lipopolysaccharide-induced Toll-like receptor 4 (TLR4) endocytosis and interferon regulatory factor 3 (IRF3) activation. J. Biol. Chem. 287, 3704-3709.
10. Czerkies, M., Borzecka, K., Zdioruk, M. I., Plociennikowska, A., Sobota, A. and Kwiatkowska, K. (2013). An interplay between scavenger receptor A and CD14 during activation of J774 cells by high concentrations of LPS. Immunobiology 218, 1217-1226.
11. Da Silva Correia, J., Soldau, K., Christen, U., Tobias, P. S. and Ulevitch, R. J. (2001). 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, 21129-21135.
12. Davda, D., El Azzouny, M. A., Tom, C. T. M. B., Hernandez, J. L., Majmudar, J. D., Kennedy, R. T. and Martin, B. R. (2013). Profiling targets of the irreversible palmitoylation inhibitor 2-bromopalmitate. ACS Chem. Biol. 8, 1912-1917.
13. Dhungana, S., Merrick, B. A., Tomer, K. B. and Fessler, M. B. (2009). Quantitative proteomics analysis of macrophage rafts reveals compartmentalized activation of the proteasome and of proteasome-mediated ERK activation in response to lipopolysaccharide. Mol. Cell. Proteomics 8, 201-213.
14. Furt, F., König, S., Bessoule, J. J., Sargueil, F., Zallot, R., Stanislas, T., Noirot, E., Lherminier, J., Simon-Plas, F., Heilmann, I. et al. (2010). Polyphosphoinositides are enriched in plant membrane rafts and form microdomains in the plasma membrane. Plant Physiol. 152, 2173-2187.
15. Gao, J., Takeuchi, H., Zhang, Z., Fuji, M., Kanematsu, T. and Hirata, M. (2009). Binding of phospholipase C-related but catalytically inactive protein to phosphatidylinositol 4,5-bisphosphate via the PH domain. Cell. Signal. 21, 1180-1186.
16. Gioannini, T. L., Teghanemt, A., Zhang, D., Levis, E. N. and Weiss, J. P. (2005). Monomeric endotoxin: protein complexes are essential for TLR4-dependent cell activation. J. Endotoxin Res. 11, 117-123.
17. Gray, A., Olsson, H., Batty, I. H., Priganica, L. and Peter Downes, C. (2003). Nonradioactive methods for the assay of phosphoinositide 3-kinases and phosphoinositide phosphatases and selective detection of signaling lipids in cell and tissue extracts. Anal. Biochem. 313, 234-245.
18. Husebye, H., Halaas, O., Stenmark, H., Tunheim, G., Sandanger, O., Bogen, B., Brech, A., Latz, E. and Espevik, T. (2006). Endocytic pathways regulate Toll-like receptor 4 signaling and link innate and adaptive immunity. EMBO J. 25, 683-692.
19. Jiang, Z., Georgel, P., Du, X., Shamel, L., Sovath, S., Mudd, S., Huber, M., Kalis, C., Keck, S., Galanos, C. et al. (2005). CD14 is required for MyD88-independent LPS signaling. Nat. Immunol. 6, 565-570.
20. Jung, G., Wang, J., Wlodarski, P., Barylko, B., Binns, D. D., Shu, H., Yin, H. L. and Albanesi, J. P. (2008). Molecular determinants of activation and membrane targeting of phosphoinositol 4-kinase IIß. Biochem. J. 409, 501-509.
21. Kagan, J. C. and Medzhitov, R. (2006). Phosphoinositide-mediated adaptor recruitment controls Toll-like receptor signaling. Cell 125, 943-955.
22. Kagan, J. C., Su, T., Horng, T., Chow, A., Akira, S. and Medzhitov, R. (2008). TRAM couples endocytosis of Toll-like receptor 4 to the induction of interferon-ß. Nat. Immunol. 9, 361-368.
23. Kang, J. Y., Nan, X., Jin, M. S., Youn, S.-J., Ryu, Y. H., Mah, S., Han, S. H., Lee, H., Paik, S.-G. and Lee, J.-O. (2009). Recognition of lipopeptide patterns by Toll-like receptor 2-Toll-like receptor 6 heterodimer. Immunity 31, 873-884.
24. Kawai, T. and Akira, S. (2011). Toll-like receptors and their crosstalk with other innate receptors in infection and immunity. Immunity 34, 637-650.
25. Kawai, T., Adachi, O., Ogawa, T., Takeda, K. and Akira, S. (1999). Unresponsiveness of MyD88-deficient mice to endotoxin. Immunity 11, 115-122.
26. Kelley, S. L., Lukk, T., Nair, S. K. and Tapping, R. I. (2013). The crystal structure of human soluble CD14 reveals a bent solenoid with a hydrophobic amino-terminal pocket. J. Immunol. 190, 1304-1311.
27. Kitchens, R. L., Wang, P. and Munford, R. S. (1998). Bacterial lipopolysaccharide can enter monocytes via two CD14-dependent pathways. J. Immunol. 161, 5534-5545.
28. Kunz, J., Wilson, M. P., Kisseleva, M., Hurley, J. H., Majerus, P. W. and Anderson, R. A. (2000). The activation loop of phosphatidylinositol phosphate kinases determines signaling specificity. Mol. Cell 5, 1-11.
29. Kusumi, A., Fujiwara, T. K., Morone, N., Yoshida, K. J., Chadda, R., Xie, M., Kasai, R. S. and Suzuki, K. G. N. (2012). Membrane mechanisms for signal transduction: the coupling of the meso-scale raft domains to membrane-skeleton-induced compartments and dynamic protein complexes. Semin. Cell Dev. Biol. 23, 126-144.
30. Kwiatkowska, K. (2010). One lipid, multiple functions: how various pools of PI (4,5)P2 are created in the plasma membrane. Cell. Mol. Life Sci. 67, 3927-3946.
31. Kwiatkowska, K., Frey, J. and Sobota, A. (2003). Phosphorylation of FcγRIIA is required for the receptor-induced actin rearrangement and capping: the role of membrane rafts. J. Cell Sci. 116, 537-550.
32. Kwiatkowska, K., Marszalek-Sadowska, E., Traczyk, G., Koprowski, P., Musielak, M., Lugowska, A., Kulma, M., Grzelczyk, A. and Sobota, A. (2014). Visualization of cholesterol deposits in lysosomes of Niemann-Pick type C fibroblasts using recombinant perfringolysin O. Orphanet J. Rare Dis. 9, 64.
33. 2 at plasmalemmal rafts, and regulate cell cortex actin dynamics through a common mechanism. J. Cell Biol. 149, 1455-1472.
34. Lingwood, D. and Simons, K. (2010). Lipid rafts as a membrane-organizing principle. Science 327, 46-50.
35. Liu, Y., Casey, L. and Pike, L. J. (1998). Compartmentalization of phosphatidylinositol 4,5-bisphosphate in low-density membrane domains in the absence of caveolin. Biochem. Biophys. Res. Commun. 245, 684-690.
36. Morgan, B. P., van den Berg, C. W., Davies, E. V., Hallett, M. B. and Horejsi, V. (1993). Cross-linking of CD59 and of other glycosyl phosphatidylinositol-anchored molecules on neutrophils triggers cell activation via tyrosine kinase. Eur. J. Immunol. 23, 2841-2850.
37. Nakatsu, F., Baskin, J. M., Chung, J., Tanner, L. B., Shui, G., Lee, S. Y., Pirruccello, M., Hao, M., Ingolia, N. T., Wenk, M. R. et al. (2012). PtdIns4P synthesis by PI4KIIIa at the plasma membrane and its impact on plasma membrane identity. J. Cell Biol. 199, 1003-1016.
38. Nguyen, T. T. N., Kim, Y. M., Kim, T. D., Le, O. T. T., Kim, J. J., Kang, H. C., Hasegawa, H., Kanaho, Y., Jou, I. and Lee, S. Y. (2013). Phosphatidylinositol 4-phosphate 5-kinase α facilitates Toll-like receptor 4-mediated microglial inflammation through regulation of the Toll/interleukin-1 receptor domain-containing adaptor protein (TIRAP) location. J. Biol. Chem. 288, 5645-5659.
39. Ohnishi, T., Ohba, H., Seo, K.-C., Im, J., Sato, Y. and Iwayama, Y. (2007). Spatial expression patterns and biochemical properties distinguish a second myo-inositol monophosphatase IMPA2 from IMPA1. J. Biol. Chem. 282, 637-646.
40. 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.
41. Parmryd, I., Adler, J., Patel, R. and Magee, A. I. (2003). Imaging metabolism of phosphatidylinositol 4,5-bisphosphate in T-cell GM1-enriched domains containing Ras proteins. Exp. Cell Res. 285, 27-38.
42. Perera, P. Y., Vogel, S. N., Detore, G. R., Haziot, A. and Goyert, S. M. (1997). CD14-dependent and CD14-independent signaling pathways in murine macrophages from normal and CD14 knockout mice stimulated with lipopolysaccharide or taxol. J. Immunol. 158, 4422-4429.
43. Pfeiffer, A., Böttcher, A., Orso, E., Kapinsky, M., Nagy, P., Bodnar, A., Spreitzer, I., Liebisch, G., Drobnik, W., Gempel, K. et al. (2001). Lipopolysaccharide and ceramide docking to CD14 provokes ligand-specific receptor clustering in rafts. Eur. J. Immunol. 31, 3153-3164.
44. Plociennikowska, A., Hromada-Judycka, A., Borzecka, K. and Kwiatkowska, K. (2015). Co-operation of TLR4 and raft proteins in LPS-induced pro-inflammatory signaling. Cell. Mol. Life Sci. 72, 557-581.
45. Poltorak, A., He, X., Smirnova, I., Liu, M.-Y., Van Huffel, C., Du, X., Birdwell, D., Alejos, E., Silva, M., Galanos, C. et al. (1998). Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science 282, 2085-2088.
46. Pugin, J., Kravchenko, V. V., Lee, J. D., Kline, L., Ulevitch, R. J. and Tobias, P. S. (1998). Cell activation mediated by glycosylphosphatidylinositol-anchored or transmembrane forms of CD14. Infect. Immun. 66, 1174-1180.
47. 2 synthesis: importance for calciumsignaling and PI3K activity. Immunity 19, 669-677.
48. Salomao, R., Brunialti, M. K. C., Rapozo, M. M., Baggio-Zappia, G. L., Galanos, C. and Freudenberg, M. (2012). Bacterial sensing, cell signaling, and modulation of the immune response during sepsis. Shock 38, 227-242.
49. Sanan, D. A. and Anderson, R. G. (1991). Simultaneous visualization of LDL receptor distribution and clathrin lattices on membranes torn from the upper surface of cultured cells. J. Histochem. Cytochem. 39, 1017-1024.
50. Schroder, N.W. J., Heine, H., Alexander, C., Manukyan, M., Eckert, J., Hamann, L., Göbel, U. B. and Schumann, R. R. (2004). Lipopolysaccharide binding protein binds to triacylated and diacylated lipopeptides and mediates innate immune responses. J. Immunol. 173, 2683-2691.
51. Shenoy-Scaria, A. M., Kwong, J., Fujita, T., Olszowy, M. W., Shaw, A. S. and Lublin, D. M. (1992). Signal transduction through decay-accelerating factor. Interaction of glycosyl-phosphatidylinositol anchor and protein tyrosine kinases p56lck and p59fyn 1. J. Immunol. 149, 3535-3541.
52. Simmons, D. L., Tan, S., Tenen, D. G., Nicholson-Weller, A. and Seed, B. (1989). Monocyte antigen CD14 is a phospholipid anchored membrane protein. Blood 73, 284-289.
53. Strzelecka-Kiliszek, A., Korzeniowski, M., Kwiatkowska, K., Mrozinóska, K. and Sobota, A. (2004). Activated FcγRII and signalling molecules revealed in rafts by ultra-structural observations of plasma-membrane sheets. Mol. Membr. Biol. 21, 101-108.
54. 2+ signaling: single-molecule tracking study 2. J. Cell Biol. 177, 731-742.
55. Suzuki, K. G. N., Kasai, R. S., Hirosawa, K. M., Nemoto, Y. L., Ishibashi, M., Miwa, Y., Fujiwara, T. K. and Kusumi, A. (2012). Transient GPI-anchored protein homodimers are units for raft organization and function. Nat. Chem. Biol. 8, 774-783.
56. 2 level and inhibits FcγRIIA-mediated cell spreading and phagocytosis. Eur. J. Immunol. 38, 260-272.
57. Szymanska, E., Korzeniowski, M., Raynal, P., Sobota, A. and Kwiatkowska, K. (2009). Contribution of PIP-5 kinase Ia to raft-based FcγRIIA signaling. Exp. Cell Res. 315, 981-995.
58. Tanimura, N., Saitoh, S., Matsumoto, F., Akashi-Takamura, S. and Miyake, K. (2008). Roles for LPS-dependent interaction and relocation of TLR4 and TRAM in TRIF-signaling. Biochem. Biophys. Res. Commun. 368, 94-99.
59. Triantafilou, M., Brandenburg, K., Kusumoto, S., Fukase, K., Mackie, A., Seydel, U. and Triantafilou, K. (2004a). Combinational clustering of receptors following stimulation by bacterial products determines lipopolysaccharide responses. Biochem. J. 381, 527-536.
60. Triantafilou, M., Morath, S., Mackie, A., Hartung, T. and Triantafilou, K. (2004b). Lateral diffusion of Toll-like receptors reveals that they are transiently confined within lipid rafts on the plasma membrane. J. Cell Sci. 117, 4007-4014.
61. 3H]inositol-labeled phosphoinositide pools. J. Cell Biol. 143, 501-510.
62. Vasselon, T., Hailman, E., Thieringer, R. and Detmers, P. A. (1999). Internalization of monomeric lipopolysaccharide occurs after transfer out of cell surface CD14. J. Exp. Med. 190, 509-522.
63. Wang, Y., Yang, Y., Liu, X., Wang, N., Cao, H., Lu, Y., Zhou, H. and Zhneg, J. (2012). Inhibition of clathrin/dynamin-dependent internalization interferes with LPS-mediated TRAM-TRIF-dependent signaling pathway. Cell. Immunol. 274, 121-129.
64. Yamamoto, M., Sato, S., Hemmi, H., Sanjo, H., Uematsu, S., Kaisho, T., Hoshino, K., Takeuchi, O., Kobayashi, M., Fujita, T. et al. (2002). Essential role for TIRAP in activation of the signalling cascade shared by TLR2 and TLR4. Nature 420, 324-329.
65. Yamamoto, M., Sato, S., Hemmi, H., Hoshino, K., Kaisho, T., Sanjo, H., Takeuchi, O., Sugiyama, M., Okabe, M., Takeda, K. et al. (2003). Role of adaptor TRIF in the MyD88-independent toll-like receptor signaling pathway. Science 301, 640-643.
66. Zanoni, I., Ostuni, R., Capuano, G., Collini, M., Caccia, M., Ronchi, A. E., Rocchetti, M., Mingozzi, F., Foti, M., Chirico, G. et al. (2009). CD14 regulates the dendritic cell life cycle after LPS exposure through NFAT activation. Nature 460, 264-268.
67. Zanoni, I., Ostuni, R., Marek, L. R., Barresi, S., Barbalat, R., Barton, G. M., Granucci, F. and Kagan, J. C. (2011). CD14 controls the LPS-induced endocytosis of Toll-like receptor 4. Cell 147, 868-880.
68. Zhang, L., Mao, Y. S., Janmey, P. A. and Yin, H. L. (2012). Phosphatidylinositol 4,5-bisphosphate and the actin cytoskeleton. Subcell. Biochem. 59, 177-215.
69. Zhu, X., Owen, J. S., Wilson, M. D., Li, H., Griffiths, G. L., Thomas, M. J., Hiltbold, E. M., Fessler, M. B. and Parks, J. S. (2010). Macrophage ABCA1 reduces MyD88-dependent Toll-like receptor trafficking to lipid rafts by reduction of lipid raft cholesterol. J. Lipid Res. 51, 3196-3206.