Cellular trafficking of lipoteichoic acid and Toll-like receptor 2 in relation to signaling; role of CD14 and CD36

Journal of Leukocyte Biology

Volumn 84, Issue 1, 2008, Pages 280-291

  Nilsen, Nadra J ^a   Deininger, Susanne ^b   Nonstad, Unni ^a   Skjeldal, Frode ^c   Husebye, Harald ^a   Rodionov, Dmitrii ^c   Von Aulock, Sonja ^b   Hartung, Thomas ^b,d   Lien, Egil ^e   Bakke, Oddmund ^c   Espevik, Terje ^a  

^a NORWEGIAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Norway)

^b UNIVERSITY OF KONSTANZ   (Germany)

^c UNIVERSITY OF OSLO   (Norway)

^d JOINT RESEARCH CENTRE   (Italy)

^e UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

Endocytosis; LTA; TLR

Indexed keywords

ANTIBODY; BACTERIUM LIPOPOLYSACCHARIDE; CD14 ANTIGEN; CD36 ANTIGEN; DYNAMIN I; LIPOTEICHOIC ACID; LYSINE DERIVATIVE; MEMBRANE RECEPTOR; RAB11 PROTEIN; TOLL LIKE RECEPTOR 2; TUMOR NECROSIS FACTOR;

ANIMAL CELL; ANTIGEN EXPRESSION; ARTICLE; CELL MEMBRANE; CHEMICAL BINDING; CHEMICAL LABELING; CONTROLLED STUDY; CYTOKINE RELEASE; EMBRYO; ENDOCYTOSIS; ENDOPLASMIC RETICULUM; ENDOSOME; FLUORESCENCE ANALYSIS; GENETIC TRANSFECTION; GOLGI COMPLEX; HUMAN; HUMAN CELL; INTERNALIZATION; LYSOSOME; MEMBRANE BINDING; MONOCYTE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION;

ANIMALS; ANTIGENS, CD14; ANTIGENS, CD36; BIOLOGICAL TRANSPORT; CELL COMPARTMENTATION; CELL LINE; CELL MEMBRANE; DOGS; DYNAMIN I; ENDOCYTOSIS; ENDOPLASMIC RETICULUM; ENDOSOMES; HUMANS; LIPOPOLYSACCHARIDES; LYSOSOMES; MONOCYTES; NF-KAPPA B; RAB GTP-BINDING PROTEINS; SIGNAL TRANSDUCTION; TEICHOIC ACIDS; TOLL-LIKE RECEPTOR 2; TRANS-GOLGI NETWORK; TUMOR NECROSIS FACTOR-ALPHA; UP-REGULATION;

STAPHYLOCOCCUS AUREUS;

EID: 46949105590     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.0907656     Document Type: Article

References (70)

1. Janeway Jr., C. A. (1992) The immune system evolved to discriminate infectious nonself from noninfectious self. Immunol. Today 13, 11-16.
2. Medzhitov, R., Janeway Jr., C. A. (1997) Innate immunity: impact on the adaptive immune response. Curr. Opin. Immunol. 9, 4-9.
3. Marshall, C., Kossmann, T., Wesselingh, S., Spelman, D. (2004) Methicillin-resistant Staphylococcus aureus and beyond: what's new in the world of the golden staph? ANZ J. Surg. 74, 465-469.
4. Raetz, C. R., Brozek, K. A., Clementz, T., Coleman, J. D., Galloway, S. M., Golenbock, D. T., Hampton, R. Y. (1988) Gram-negative endotoxin: a biologically active lipid. Cold Spring Harb. Symp. Quant. Biol. 53, 973-982.
5. Raetz, C. R., Ulevitch, R. J., Wright, S. D., Sibley, C. H., Ding, A., Nathan, C. F. (1991) Gram-negative endotoxin: an extraordinary lipid with profound effects on eukaryotic signal transduction. FASEB J. 5, 2652-2660.
6. Ginsburg, I. (2002) Role of lipoteichoic acid in infection and inflammation. Lancet Infect. Dis. 2, 171-179.
7. Lien, E., Ingalls, R. R. (2002) Toll-like receptors. Crit. Care Med. 30, S1-S11.
8. Rock, F. L., Hardiman, G., Timans, J. C., Kastelein, R. A., Bazan, J. F. (1998) A family of human receptors structurally related to Drosophila Toll. Proc. Natl. Acad. Sci. USA 95, 588-593.
9. Akira, S., Hemmi, H. (2003) Recognition of pathogen-associated molecular patterns by TLR family. Immunol. Lett. 85, 85-95.
10. Barton, G. M., Medzhitov, R. (2003) Toll-like receptor signaling pathways. Science 300, 1524-1525.
11. Poltorak, A., He, X., Smirnova, I., Liu, M. Y., Van Huffel, C., Du, X., Birdwell, D., Alejos, E., Silva, M., Galanos, C., Freudenberg, M., Ricciardi-Castagnoli, P., Layton, B., Beutler, B. (1998) Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science 282, 2085-2088.
12. Qureshi, S. T., Medzhitov, R. (2003) Toll-like receptors and their role in experimental models of microbial infection. Genes Immun. 4, 87-94.
13. Yoshimura, A., Lien, E., Ingalls, R. R., Tuomanen, E., Dziarski, R., Golenbock, D. (1999) Cutting edge: recognition of Gram-positive bacterial cell wall components by the innate immune system occurs via Toll-like receptor 2. J. Immunol. 163, 1-5.
14. Flo, T. H., Ryan, L., Latz, E., Takeuchi, O., Monks, B. G., Lien, E., Halaas, O., Akira, S., Skjak-Braek, G., Golenbock, D. T., Espevik, T. (2002) Involvement of Toll-like receptor (TLR) 2 and TLR4 in cell activation by mannuronic acid polymers. J. Biol. Chem. 277, 35489-35495.
15. Schwandner, R., Dziarski, R., Wesche, H., Rothe, M., Kirschning, C. J. (1999) Peptidoglycan- and lipoteichoic acid-induced cell activation is mediated by Toll-like receptor 2. J. Biol. Chem. 274, 17406-17409.
16. Morath, S., Geyer, A., Hartung, T. (2001) Structure-function relationship of cytokine induction by lipoteichoic acid from Staphylococcus aureus. J. Exp. Med. 193, 393-397.
17. Brightbill, H. D., Libraty, D. H., Krutzik, S. R., Yang, R. B., Belisle, J. T., Bleharski, J. R., Maitland, M., Norgard, M. V., Plevy, S. E., Smale, S. T., Brennan, P. J., Bloom, B. R., Godowski, P. J., Modlin, R. L. (1999) Host defense mechanisms triggered by microbial lipoproteins through Toll-like receptors. Science 285, 732-736.
18. Flo, T. H., Halaas, O., Lien, E., Ryan, L., Teti, G., Golenbock, D. T., Sundan, A., Espevik, T. (2000) Human Toll-like receptor 2 mediates monocyte activation by Listeria monocytogenes, but not by group B streptococci or lipopolysaccharide. J. Immunol. 164, 2064-2069.
19. Takeda, K., Akira, S. (2001) Roles of Toll-like receptors in innate immune responses. Genes Cells 6, 733-742.
20. Takeuchi, O., Sato, S., Horiuchi, T., Hoshino, K., Takeda, K., Dong, Z., Modlin, R. L., Akira, S. (2002) Cutting edge: role of Toll-like receptor 1 in mediating immune response to microbial lipoproteins. J. Immunol. 169, 10-14.
21. Sandor, F., Latz, E., Re, F., Mandell, L., Repik, G., Golenbock, D. T., Espevik, T., Kurt-Jones, E. A., Finberg, R. W. (2003) Importance of extraand intracellular domains of TLR1 and TLR2 in NFκ B signaling. J. Cell Biol. 162, 1099-1110.
22. Takeuchi, O., Kawai, T., Muhlradt, P. F., Morr, M., Radolf, J. D., Zychlinsky, A., Takeda, K., Akira, S. (2001) Discrimination of bacterial lipoproteins by Toll-like receptor 6. Int. Immunol. 13, 933-940.
23. Ozinsky, A., Underhill, D. M., Fontenot, J. D., Hajjar, A. M., Smith, K. D., Wilson, C. B., Schroeder, L., Aderem, A. (2000) The repertoire for pattern recognition of pathogens by the innate immune system is defined by cooperation between Toll-like receptors. Proc. Natl. Acad. Sci. USA 97, 13766-13771.
24. Henneke, P., Morath, S., Uematsu, S., Weichert, S., Pfitzenmaier, M., Takeuchi, O., Muller, A., Poyart, C., Akira, S., Berner, R., Teti, G., Geyer, A., Hartung, T., Trieu-Cuot, P., Kasper, D. L., Golenbock, D. T. (2005) Role of lipoteichoic acid in the phagocyte response to group B streptococcus. J. Immunol. 174, 6449-6455.
25. Goyert, S. M., Ferrero, E., Rettig, W. J., Yenamandra, A. K., Obata, F., Le Beau, M. M. (1988) The CD14 monocyte differentiation antigen maps to a region encoding growth factors and receptors. Science 239, 497-500.
26. Haziot, A., Chen, S., Ferrero, E., Low, M. G., Silber, R., Goyert, S. M. (1988) The monocyte differentiation antigen, CD14, is anchored to the cell membrane by a phosphatidylinositol linkage. J. Immunol. 141, 547-552.
27. Pfeiffer, A., Bottcher, A., Orso, E., Kapinsky, M., Nagy, P., Bodnar, A., Spreitzer, I., Liebisch, G., Drobnik, W., Gempel, K., Horn, M., Holmer, S., Hartung, T., Multhoff, G., Schutz, G., Schindler, H., Ulmer, A. J., Heine, H., Stelter, F., Schutt, C., Rothe, G., Szolosi, J., Damjanovich, S., Schmitz, G. (2001) Lipopolysaccharide and ceramide docking to CD14 provokes ligand-specific receptor clustering in rafts. Eur. J. Immunol. 31, 3153-3164.
28. Schumann, R. R., Leong, S. R., Flaggs, G. W., Gray, P. W., Wright, S. D., Mathison, J. C., Tobias, P. S., Ulevitch, R. J. (1990) Structure and function of lipopolysaccharide binding protein. Science 249, 1429-1431.
29. Schromm, A. B., Brandenburg, K., Rietschel, E. T., Flad, H. D., Carroll, S. F., Seydel, U. (1996) Lipopolysaccharide-binding protein mediates CD14-independent intercalation of lipopolysaccharide into phospholipid membranes. FEBS Lett. 399, 267-271.
30. Blondin, C., Le Dur, A., Cholley, B., Caroff, M., Haeffner-Cavaillon, N. (1997) Lipopolysaccharide complexed with soluble CD14 binds to normal human monocytes. Eur. J. Immunol. 27, 3303-3309.
31. Wright, S. D., Ramos, R. A., Tobias, P. S., Ulevitch, R. J., Mathison, J. C. (1990) CD14, a receptor for complexes of lipopolysaccharide (LPS) and LPS binding protein. Science 249, 1431-1433.
32. Thieblemont, N., Wright, S. D. (1999) Transport of bacterial lipopolysaccharide to the Golgi apparatus. J. Exp. Med. 190, 523-534.
33. Latz, E., Visintin, A., Lien, E., Fitzgerald, K. A., Espevik, T., Golenbock, D. T. (2003) The LPS receptor generates inflammatory signals from the cell surface. J. Endotoxin Res. 9, 375-380.
34. Schroder, N. W., Morath, S., Alexander, C., Hamann, L., Hartung, T., Zahringer, U., Gobel, U. B., Weber, J. R., Schumann, R. R. (2003) Lipoteichoic acid (LTA) of Streptococcus pneumoniae and Staphylococcus aureus activates immune cells via Toll-like receptor (TLR)-2, lipopolysaccharide- binding protein (LBP), and CD14, whereas TLR-4 and MD-2 are not involved. J. Biol. Chem. 278, 15587-15594.
35. Manukyan, M., Triantafilou, K., Triantafilou, M., Mackie, A., Nilsen, N., Espevik, T., Wiesmuller, K. H., Ulmer, A. J., Heine, H. (2005) Binding of lipopeptide to CD14 induces physical proximity of CD14, TLR2 and TLR1. Eur. J. Immunol. 35, 911-921.
36. Triantafilou, M., Manukyan, M., Mackie, A., Morath, S., Hartung, T., Heine, H., Triantafilou, K. (2004) Lipoteichoic acid and Toll-like receptor 2 internalization and targeting to the Golgi are lipid raft-dependent. J. Biol. Chem. 279, 40882-40889.
37. Hoebe, K., Georgel, P., Rutschmann, S., Du, X., Mudd, S., Crozat, K., Sovath, S., Shamel, L., Hartung, T., Zahringer, U., Beutler, B. (2005) CD36 is a sensor of diacylglycerides. Nature 433, 523-527.
38. Triantafilou, M., Gamper, F. G., Haston, R. M., Mouratis, M. A., Morath, S., Hartung, T., Triantafilou, K. (2006) Membrane sorting of Toll-like receptor (TLR)-2/6 and TLR2/1 heterodimers at the cell surface determines heterotypic associations with CD36 and intracellular targeting. J. Biol. Chem. 281, 31002-31011.
39. Stuart, L. M., Deng, J., Silver, J. M., Takahashi, K., Tseng, A. A., Hennessy, E. J., Ezekowitz, R. A., Moore, K. J. (2005) Response to Staphylococcus aureus requires CD36-mediated phagocytosis triggered by the COOH-terminal cytoplasmic domain. J. Cell Biol. 170, 477-485.
40. Shimazu, R., Akashi, S., Ogata, H., Nagai, Y., Fukudome, K., Miyake, K., Kimoto, M. (1999) MD-2, a molecule that confers lipopolysaccharide responsiveness on Toll-like receptor 4. J. Exp. Med. 189, 1777-1782.
41. Van Voorhis, W. C., Steinman, R. M., Hair, L. S., Luban, J., Witmer, M. D., Koide, S., Cohn, Z. A. (1983) Specific antimononuclear phagocyte monoclonal antibodies. Application to the purification of dendritic cells and the tissue localization of macrophages. J. Exp. Med. 158, 126-145.
42. Lien, E., Sellati, T. J., Yoshimura, A., Flo, T. H., Rawadi, G., Finberg, R. W., Carroll, J. D., Espevik, T., Ingalls, R. R., Radolf, J. D., Golenbock, D. T. (1999) Toll-like receptor 2 functions as a pattern recognition receptor for diverse bacterial products. J. Biol. Chem. 274, 33419-33425.
43. Latz, E., Visintin, A., Lien, E., Fitzgerald, K. A., Monks, B. G., Kurt-Jones, E. A., Golenbock, D. T., 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.
44. McBride, H. M., Rybin, V., Murphy, C., Giner, A., Teasdale, R., Zerial, M. (1999) Oligomeric complexes link Rab5 effectors with NSF and drive membrane fusion via interactions between EEA1 and syntaxin 13. Cell 98, 377-386.
45. Yang, H., Young, D. W., Gusovsky, F., Chow, J. C. (2000) Cellular events mediated by lipopolysaccharide-stimulated Toll-like receptor 4. MD-2 is required for activation of mitogen-activated protein kinases and Elk-1. J. Biol. Chem. 275, 20861-20866.
46. Flo, T. H., Halaas, O., Torp, S., Ryan, L., Lien, E., Dybdahl, B., Sundan, A., Espevik, T. (2001) Differential expression of Toll-like receptor 2 in human cells. J. Leukoc. Biol. 69, 474-481.
47. Griffith, K. J., Chan, E. K., Lung, C. C., Hamel, J. C., Guo, X., Miyachi, K., Fritzler, M. J. (1997) Molecular cloning of a novel 97-kd Golgi complex autoantigen associated with Sjogren's syndrome. Arthritis Rheum. 40, 1693-1702.
48. Nakamura, N., Rabouille, C., Watson, R., Nilsson, T., Hui, N., Slusarewicz, P., Kreis, T. E., Warren, G. (1995) Characterization of a cis-Golgi matrix protein, GM130. J. Cell Biol. 131, 1715-1726.
49. Chen, W., Feng, Y., Chen, D., Wandinger-Ness, A. (1998) Rab11 is required for trans-Golgi network-to-plasma membrane transport and a preferential target for GDP dissociation inhibitor. Mol. Biol. Cell 9, 3241-3257.
50. Deretic, D. (1997) Rab proteins and post-Golgi trafficking of rhodopsin in photoreceptor cells. Electrophoresis 18, 2537-2541.
51. Ullrich, O., Reinsch, S., Urbe, S., Zerial, M., Parton, R. G. (1996) Rab11 regulates recycling through the pericentriolar recycling endosome. J. Cell Biol. 135, 913-924.
52. Satoh, A. K., O'Tousa, J. E., Ozaki, K., Ready, D. F. (2005) Rab11 mediates post-Golgi trafficking of rhodopsin to the photosensitive apical membrane of Drosophila photoreceptors. Development 132, 1487-1497.
53. Johnsen, I. B., Nguyen, T. T., Ringdal, M., Tryggestad, A. M., Bakke, O., Lien, E., Espevik, T., Anthonsen, M. W. (2006) Toll-like receptor 3 associates with c-Src tyrosine kinase on endosomes to initiate antiviral signaling. EMBO J. 25, 3335-3346.
54. Latz, E., Schoenemeyer, A., Visintin, A., Fitzgerald, K. A., Monks, B. G., Knetter, C. F., Lien, E., Nilsen, N. J., Espevik, T., Golenbock, D. T. (2004) TLR9 signals after translocating from the ER to CpG DNA in the lysosome. Nat. Immunol. 5, 190-198.
55. Talle, M. A., Rao, P. E., Westberg, E., Allegar, N., Makowski, M., Mittler, R. S., Goldstein, G. (1983) Patterns of antigenic expression on human monocytes as defined by monoclonal antibodies. Cell. Immunol. 78, 83-99.
56. Bazil, V., Baudys, M., Hilgert, I., Stefanova, I., Low, M. G., Zbrozek, J., Horejsi, V. (1989) Structural relationship between the soluble and membrane-bound forms of human monocyte surface glycoprotein CD14. Mol. Immunol. 26, 657-662.
57. Nilsen, N., Nonstad, U., Khan, N., Knetter, C. F., Akira, S., Sundan, A., Espevik, T., Lien, E. (2004) Lipopolysaccharide and double-stranded RNA up-regulate Toll-like receptor 2 independently of myeloid differentiation factor 88. J. Biol. Chem. 279, 39727-39735.
58. Damke, H., Baba, T., Warnock, D. E., Schmid, S. L. (1994) Induction of mutant dynamin specifically blocks endocytic coated vesicle formation. J. Cell Biol. 127, 915-934.
59. Chuang, T. H., Ulevitch, R. J. (2004) Triad3A, an E3 ubiquitin-protein ligase regulating Toll-like receptors. Nat. Immunol. 5, 495-502.
60. Schjetne, K. W., Thompson, K. M., Nilsen, N., Flo, T. H., Fleckenstein, B., Iversen, J. G., Espevik, T., Bogen, B. (2003) Cutting edge: link between innate and adaptive immunity: Toll-like receptor 2 internalizes antigen for presentation to CD4- T cells and could be an efficient vaccine target. J. Immunol. 171, 32-36.
61. Husebye, H., Halaas, O., Stenmark, H., Tunheim, G., Sandanger, O., Bogen, B., Brech, A., Latz, E., Espevik, T. (2006) Endocytic pathways regulate Toll-like receptor 4 signaling and link innate and adaptive immunity. EMBO J. 25, 683-692.
62. Sandvig, K., Grimmer, S., Lauvrak, S. U., Torgersen, M. L., Skretting, G., van Deurs, B., Iversen, T. G. (2002) Pathways followed by ricin and Shiga toxin into cells. Histochem. Cell Biol. 117, 131-141.
63. Munro, S., Pelham, H. R. (1987) A C-terminal signal prevents secretion of luminal ER proteins. Cell 48, 899-907.
64. Griffiths, G., Ericsson, M., Krijnse-Locker, J., Nilsson, T., Goud, B., Soling, H. D., Tang, B. L., Wong, S. H., Hong, W. (1994) Localization of the Lys, Asp, Glu, Leu tetrapeptide receptor to the Golgi complex and the intermediate compartment in mammalian cells. J. Cell Biol. 127, 1557-1574.
65. Miesenbock, G., Rothman, J. E. (1995) The capacity to retrieve escaped ER proteins extends to the trans-most cisterna of the Golgi stack. J. Cell Biol. 129, 309-319.
66. Sandvig, K., van Deurs, B. (2000) Entry of ricin and shiga toxin into cells: molecular mechanisms and medical perspectives. EMBO J. 19, 5943-5950.
67. Torgersen, M. L., Skretting, G., van Deurs, B., Sandvig, K. (2001) Internalization of cholera toxin by different endocytic mechanisms. J. Cell Sci. 114, 3737-3747.
68. Kirkham, M., Fujita, A., Chadda, R., Nixon, S. J., Kurzchalia, T. V., Sharma, D. K., Pagano, R. E., Hancock, J. F., Mayor, S., Parton, R. G. (2005) Ultrastructural identification of uncoated caveolin-independent early endocytic vehicles. J. Cell Biol. 168, 465-476.
69. Kirkham, M., Parton, R. G. (2005) Clathrin-independent endocytosis: new insights into caveolae and non-caveolar lipid raft carriers. Biochim. Biophys. Acta 1745, 273-286.
70. Kitchens, R. L., Wang, P., Munford, R. S. (1998) Bacterial lipopolysaccharide can enter monocytes via two CD14-dependent pathways. J. Immunol. 161, 5534-5545.