Tubulation of endosomal structures in human dendritic cells by toll-like receptor ligation and lymphocyte contact accompanies antigen cross-presentation

Journal of Biological Chemistry

Volumn 289, Issue 1, 2014, Pages 520-528

  Compeer, Ewoud B ^a   Flinsenberg, Thijs W H ^a   Boon, Louis ^b   Hoekstra, Mirjam E ^a   Boes, Marianne ^a  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^b BIOCEROS   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGENS; CELL MEMBRANES; CYTOLOGY; RECYCLING;

CELL INTERACTION; DENDRITIC CELLS (DCS); ENDOSOMAL COMPARTMENTS; ENDOSOMAL RECYCLING; HUMAN DENDRITIC CELLS; T CELL ACTIVATION; TOLL-LIKE RECEPTORS; TUBULAR STRUCTURES;

T-CELLS;

HLA A2 ANTIGEN; LYMPHOCYTE FUNCTION ASSOCIATED ANTIGEN 1; T LYMPHOCYTE RECEPTOR; TOLL LIKE RECEPTOR; INTERCELLULAR ADHESION MOLECULE 1;

ANTIGEN SPECIFICITY; ARTICLE; CD8+ T LYMPHOCYTE; CELL ACTIVITY; CELL COMPARTMENTALIZATION; CELL INTERACTION; CELL SHAPE; CELL STRUCTURE; CONTROLLED STUDY; CROSS PRESENTATION; DENDRITIC CELL; ENDOSOME; HUMAN; HUMAN CELL; IMMUNE RESPONSE; LYMPHOCYTE ACTIVATION; LYMPHOCYTE FUNCTION; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; ANIMAL; ANTIGEN PRESENTATION; CELL CULTURE; CELLULAR IMMUNITY; CLINICAL TRIAL; COCULTURE; CYTOLOGY; FEMALE; IMMUNOLOGY; INNATE IMMUNITY; MALE; MONOCYTE; MOUSE; PHYSIOLOGY;

ANIMALS; ANTIGEN PRESENTATION; CD8-POSITIVE T-LYMPHOCYTES; CELLS, CULTURED; COCULTURE TECHNIQUES; DENDRITIC CELLS; ENDOSOMES; FEMALE; HLA-A2 ANTIGEN; HUMANS; IMMUNITY, CELLULAR; IMMUNITY, INNATE; INTERCELLULAR ADHESION MOLECULE-1; LYMPHOCYTE FUNCTION-ASSOCIATED ANTIGEN-1; MALE; MICE; MONOCYTES; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTORS;

EID: 84891716962     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.511147     Document Type: Article

References (32)

1. Grant, B. D., and Donaldson, J. G. (2009) Pathways and mechanisms of endocytic recycling. Nat Rev. Mol. Cell Biol. 10, 597-608
2. Sönnichsen, B., De Renzis, S., Nielsen, E., Rietdorf, J., and Zerial, M. (2000) Distinct membrane domains on endosomes in the recycling pathway visualized by multicolor imaging of Rab4, Rab5, and Rab11. J. Cell Biol. 149, 901-914
3. Compeer, E. B., Flinsenberg, T. W., Van Der Grein, S. G., and Boes, M. (2012) Antigen processing and remodeling of the endosomal pathway: requirements for antigen cross-presentation. Front. Immunol. 3, 37
4. Villadangos, J. A., and Schnorrer, P. (2007) Intrinsic and cooperative antigen-presenting functions of dendritic cell subsets in vivo. Nat. Rev. Immunol. 7, 543-555 (Pubitemid 46987783)
5. Burgdorf, S., Schölz, C., Kautz, A., Tampé, R., and Kurts, C. (2008) Spatial and mechanistic separation of cross-presentation and endogenous antigen presentation. Nat. Immunol. 9, 558-566 (Pubitemid 351560525)
6. Ackerman, A. L., Kyritsis, C., Tampé, R., and Cresswell, P. (2005) Access of soluble antigens to the endoplasmic reticulum can explain cross-presentation by dendritic cells. Nat Immunol. 6, 107-113 (Pubitemid 40136702)
7. Boes, M., Cerny, J., Massol, R., Op Den Brouw, M., Kirchhausen, T., Chen, J., and Ploegh, H. L. (2002) T-cell engagement of dendritic cells rapidly rearranges MHC class II transport. Nature 418, 983-988 (Pubitemid 34976034)
8. Boes, M., Bertho, N., Cerny, J., Op Den Brouw, M., Kirchhausen, T., and Ploegh, H. (2003) T cells induce extended class II MHC compartments in dendritic cells in a Toll-like receptor-dependent manner. J. Immunol. 171, 4081-4088 (Pubitemid 37238683)
9. Kleijmeer, M., Ramm, G., Schuurhuis, D., Griffith, J., Rescigno, M., Ricciardi-Castagnoli, P., Rudensky, A. Y., Ossendorp, F., Melief, C. J., Stoorvogel, W., and Geuze, H. J. (2001) Reorganization of multivesicular bodies regulates MHC class II antigen presentation by dendritic cells. J. Cell Biol. 155, 53-63 (Pubitemid 34286207)
10. Chow, A., Toomre, D., Garrett, W., and Mellman, I. (2002) Dendritic cell maturation triggers retrograde MHC class II transport from lysosomes to the plasma membrane. Nature 418, 988-994 (Pubitemid 34976035)
11. Vyas, J. M., Kim, Y. M., Artavanis-Tsakonas, K., Love, J. C., Van Der Veen, A. G., and Ploegh, H. L. (2007) Tubulation of class II MHC compartments is microtubule-dependent and involves multiple endolysosomal membrane proteins in primary dendritic cells. J. Immunol. 178, 7199-7210 (Pubitemid 46847446)
12. Barois, N., De Saint-Vis, B., Lebecque, S., Geuze, H. J., and Kleijmeer, M. J. (2002) MHC class II compartments in human dendritic cells undergo profound structural changes upon activation. Traffic 3, 894-905 (Pubitemid 35460594)
13. Kaniuk, N. A., Canadien, V., Bagshaw, R. D., Bakowski, M., Braun, V., Landekic, M., Mitra, S., Huang, J., Heo, W. D., Meyer, T., Pelletier, L., Andrews-Polymenis, H., McClelland, M., Pawson, T., Grinstein, S., and Brumell, J. H. (2011) Salmonella exploits Arl8B-directed kinesin activity to promote endosome tubulation and cell-to-cell transfer. Cell. Microbiol. 13, 1812-1823
14. Caplan, S., Naslavsky, N., Hartnell, L. M., Lodge, R., Polishchuk, R. S., Donaldson, J. G., and Bonifacino, J. S. (2002) A tubular EHD1-containing compartment involved in the recycling of major histocompatibility complex class I molecules to the plasma membrane. EMBOJ. 21, 2557-2567 (Pubitemid 34619372)
15. Flinsenberg, T. W., Compeer, E. B., Koning, D., Klein, M., Amelung, F. J., Van Baarle, D., Boelens, J. J., and Boes, M. (2012) Fcγ receptor antigen targeting potentiates cross-presentation by human blood and lymphoid tissue BDCA-3+ dendritic cells. Blood 120, 5163-5172
16. Traer, C. J., Rutherford, A. C., Palmer, K. J., Wassmer, T., Oakley, J., Attar, N., Carlton, J. G., Kremerskothen, J., Stephens, D. J., and Cullen, P. J. (2007) SNX4 coordinates endosomal sorting of TfnR with dynein-mediated transport into the endocytic recycling compartment. Nat. Cell Biol. 9, 1370-1380 (Pubitemid 350201750)
17. Scholer, A., Hugues, S., Boissonnas, A., Fetler, L., and Amigorena, S. (2008) Intercellular adhesion molecule-1-dependent stable interactions between T cells and dendritic cells determine CD8+ T cell memory. Immunity 28, 258-270 (Pubitemid 351222655)
18. Dustin, M. L., and Springer, T. A. (1989) T-cell receptor cross-linking transiently stimulates adhesiveness through LFA-1. Nature 341, 619-624 (Pubitemid 19257309)
19. Lebedeva, T., Anikeeva, N., Kalams, S. A., Walker, B. D., Gaidarov, I., Keen, J. H., and Sykulev, Y. (2004) T-cell receptor cross-linking transiently stimulates adhesiveness through LFA-1. Immunology 113, 460-471
20. Bertho, N., Cerny, J., Kim, Y. M., Fiebiger, E., Ploegh, H., and Boes, M. (2003) Requirements for T cell-polarized tubulation of class II+ compartments in dendritic cells. J. Immunol. 171, 5689-5696 (Pubitemid 37467183)
21. Van Weert, A. W., Geuze, H. J., Groothuis, B., and Stoorvogel, W. (2000) Primaquine interferes with membrane recycling from endosomes to the plasma membrane through a direct interaction with endosomes which does not involve neutralisation of endosomal pH nor osmotic swelling of endosomes. Eur. J. Cell Biol. 79, 394-399 (Pubitemid 30433641)
22. Hasegawa, S., Hirashima, N., and Nakanishi, M. (2001) Microtubule involvement in the intracellular dynamics for gene transfection mediated by cationic liposomes. Gene Ther. 8, 1669-1673 (Pubitemid 33085589)
23. Blander, J. M., and Medzhitov, R. (2004) Regulation of phagosome maturation by signals from toll-like receptors. Science 304, 1014-1018 (Pubitemid 38638100)
24. Dustin, M. L., Tseng, S. Y., Varma, R., and Campi, G. (2006) T cell-dendritic cell immunological synapses. Curr. Opin. Immunol. 18, 512-516 (Pubitemid 43947585)
25. Grommé, M., Uytde Haag, F. G., Janssen, H., Calafat, J., Van Binnendijk, R. S., Kenter, M. J., Tulp, A., Verwoerd, D., and Neefjes, J. (1999) Recycling MHC class I molecules and endosomal peptide loading. Proc. Natl. Acad. Sci. U. S. A. 96, 10326-10331 (Pubitemid 29422557)
26. Di Pucchio T., Chatterjee, B., Smed-Sörensen, A., Clayton, S., Palazzo, A., Montes, M., Xue, Y., Mellman, I., Banchereau, J., and Connolly, J. E. (2008) Direct proteasome-independent cross-presentation of viral antigen by plasmacytoid dendritic cells on major histocompatibility complex class I. Nat. Immunol. 9, 551-557 (Pubitemid 351560524)
27. Reid, P. A., and Watts, C. (1990) Cycling of cell surface MHC glycoproteins through primaquine-sensitive intracellular compartments. Nature 346, 655-657
28. Lizée, G., Basha, G., Tiong, J., Julien, J. P., Tian, M., Biron, K. E., and Jefferies, W. A. (2003) Control of dendritic cell cross-presentation by the major histocompatibility complex class I cytoplasmic domain. Nat. Immunol. 4, 1065-1073 (Pubitemid 37428034)
29. Christinck, E. R., Luscher, M. A., Barber, B. H., and Williams, D. B. (1991) Peptide binding to class I MHC on living cells and quantitation of complexes required for CTL lysis. Nature 352, 67-70 (Pubitemid 21896699)
30. Cella, M., Engering, A., Pinet, V., Pieters, J., and Lanzavecchia, A. (1997) Inflammatory stimuli induce accumulation of MHC class II complexes on dendritic cells. Nature 388, 782-787 (Pubitemid 27375158)
31. Ackerman, A. L., and Cresswell, P. (2003) Regulation of MHC class I transport in human dendritic cells and the dendritic-like cell line KG-1. J. Immunol. 170, 4178-4188 (Pubitemid 36428183)
32. Delamarre, L., Holcombe, H., and Mellman, I. (2003) Presentation of exogenous antigens on major histocompatibility complex (MHC) class I and MHC class II molecules is differentially regulated during dendritic cell maturation. J. Exp. Med. 198, 111-122 (Pubitemid 36870191)