Dynamics within tetraspanin pairs affect MHC class II expression

Journal of Cell Science

Volumn 125, Issue 2, 2012, Pages 328-339

  van den Hoorn, Tineke ^a   Paul, Petra ^a   Janssen, Lennert ^a   Janssen, Hans ^a   Neefjes, Jacques ^a  

^a NETHERLANDS CANCER INSTITUTE   (Netherlands)

Author keywords

CD63; CD82; FRET; HLA DM; MHC class II; MVB; Tetraspanin

Indexed keywords

CD63 ANTIGEN; CD81 ANTIGEN; CD82 ANTIGEN; CD9 ANTIGEN; HLA DM ANTIGEN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2;

ARTICLE; CONTROLLED STUDY; FLUORESCENCE RESONANCE ENERGY TRANSFER; GENE SILENCING; HUMAN; HUMAN CELL; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION;

ANTIGENS, CD63; ANTIGENS, CD82; CELL LINE; CELL MEMBRANE; CHLOROQUINE; DIFFUSION; FLUORESCENCE RESONANCE ENERGY TRANSFER; HEK293 CELLS; HLA-D ANTIGENS; HLA-DR ANTIGENS; HUMANS; MULTIVESICULAR BODIES; TETRASPANINS;

EID: 84858148393     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.088047     Document Type: Article

References (37)

1. Avva, R. R. and Cresswell, P. (1994). In vivo and in vitro formation and dissociation of HLA-DR complexes with invariant chain-derived peptides. Immunity 1, 763-774.
2. Bakke, O. and Dobberstein, B. (1990). MHC class II-associated invariant chain contains a sorting signal for endosomal compartments. Cell 63, 707-716.
3. Blott, E. J., Bossi, G., Clark, R., Zvelebil, M. and Griffiths, G. M. (2001). Fas ligand is targeted to secretory lysosomes via a proline-rich domain in its cytoplasmic tail. J. Cell Sci. 114, 2405-2416.
4. Denzin, L. K. and Cresswell, P. (1995). HLA-DM induces CLIP dissociation from MHC class II alpha beta dimers and facilitates peptide loading. Cell 82, 155-165.
5. Denzin, L. K., Robbins, N. F., Carboy-Newcomb, C. and Cresswell, P. (1994). Assembly and intracellular transport of HLA-DM and correction of the class II antigen-processing defect in T2 cells. Immunity 1, 595-606.
6. Engering, A. and Pieters, J. (2001). Association of distinct tetraspanins with MHC class II molecules at different subcellular locations in human immature dendritic cells. Int. Immunol. 13, 127-134.
7. Escola, J. M., Kleijmeer, M. J., Stoorvogel, W., Griffith, J. M., Yoshie, O. and Geuze, H. J. (1998). Selective enrichment of tetraspan proteins on the internal vesicles of multivesicular endosomes and on exosomes secreted by human B- lymphocytes. J. Biol. Chem. 273, 20121-20127.
8. Fukudome, K., Furuse, M., Imai, T., Nishimura, M., Takagi, S., Hinuma, Y. and Yoshie, O. (1992). Identification of membrane antigen C33 recognized by monoclonal antibodies inhibitory to human T-cell leukemia virus type 1 (HTLV-1)- induced syncytium formation: altered glycosylation of C33 antigen in HTLV-1- positive T cells. J. Virol. 66, 1394-1401.
9. Griffiths, G., Hoflack, B., Simons, K., Mellman, I. and Kornfeld, S. (1988). The mannose 6-phosphate receptor and the biogenesis of lysosomes. Cell 52, 329-341.
10. Gromme, M., Uytdehaag, 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. USA 96, 10326-10331.
11. Hammond, C., Denzin, L. K., Pan, M., Griffith, J. M., Geuze, H. J. and Cresswell, P. (1998). The tetraspan protein CD82 is a resident of MHC class II compartments where it associates with HLA-DR, -DM, and -DO molecules. J. Immunol. 161, 3282-3291.
12. Imai, T., Fukudome, K., Takagi, S., Nagira, M., Furuse, M., Fukuhara, N., Nishimura, M., Hinuma, Y. and Yoshie, O. (1992). C33 antigen recognized by monoclonal antibodies inhibitory to human T cell leukemia virus type 1-induced syncytium formation is a member of a new family of transmembrane proteins including CD9, CD37, CD53, and CD63. J. Immunol. 149, 2879-2886.
13. Kobayashi, T., Stang, E., Fang, K. S., de Moerloose, P., Parton, R. G. and Gruenberg, J. (1998). A lipid associated with the antiphospholipid syndrome regulates endosome structure and function. Nature 392, 193-197.
14. Kropshofer, H., Arndt, S. O., Moldenhauer, G., Hammerling, G. J. and Vogt, A. B. (1997). HLA-DM acts as a molecular chaperone and rescues empty HLA-DR molecules at lysosomal pH. Immunity 6, 293-302.
15. Lampson, L. A. and Levy, R. (1980). Two populations of Ia-like molecules on a human B cell line. J. Immunol. 125, 293-299.
16. Matsuo, H., Chevallier, J., Mayran, N., Le Blanc, I., Ferguson, C., Faure, J., Blanc, N. S., Matile, S., Dubochet, J., Sadoul, R. et al. (2004). Role of LBPA and Alix in multivesicular liposome formation and endosome organization. Science 303, 531-534.
17. Min, G., Wang, H., Sun, T. T. and Kong, X. P. (2006). Structural basis for tetraspanin functions as revealed by the cryo-EM structure of uroplakin complexes at 6-A resolution. J. Cell Biol. 173, 975-983.
18. Miyawaki, A., Llopis, J., Heim, R., McCaffery, J. M., Adams, J. A., Ikura, M. and Tsien, R. Y. (1997). Fluorescent indicators for Ca2+ based on green fluorescent proteins and calmodulin. Nature 388, 882-887.
19. Mukherjee, S. and Maxfield, F. R. (2000). Role of membrane organization and membrane domains in endocytic lipid trafficking. Traffic 1, 203-211.
20. Neefjes, J. (1999). CIIV, MIIC and other compartments for MHC class II loading. Eur. J. Immunol. 29, 1421-1425.
21. Neefjes, J. J., Stollorz, V., Peters, P. J., Geuze, H. J. and Ploegh, H. L. (1990). The biosynthetic pathway of MHC class II but not class I molecules intersects the endocytic route. Cell 61, 171-183.
22. Paul, P., van den Hoorn, T., Jongsma, M. L., Bakker, M. J., Hengeveld, R., Janssen, L., Cresswell, P., Egan, D. A., van Ham, M., Ten Brinke, A. et al. (2011). A genome-wide multidimensional RNAi screen reveals pathways controlling MHC class II antigen presentation. Cell 145, 268-283.
23. Peters, P. J., Neefjes, J. J., Oorschot, V., Ploegh, H. L. and Geuze, H. J. (1991). Segregation of MHC class II molecules from MHC class I molecules in the Golgi complex for transport to lysosomal compartments. Nature 349, 669-676.
24. Reits, E. A. and Neefjes, J. J. (2001). From fixed to FRAP: measuring protein mobility and activity in living cells. Nat. Cell Biol. 3, E145-E147.
25. Rocha, N., Kuijl, C., van der Kant, R., Janssen, L., Houben, D., Janssen, H., Zwart, W. and Neefjes, J. (2009). Cholesterol sensor ORP1L contacts the ER protein VAP to control Rab7-RILP-p150 Glued and late endosome positioning. J. Cell Biol. 185, 1209-1225.
26. Roche, P. A. and Cresswell, P. (1990). Invariant chain association with HLA-DR molecules inhibits immunogenic peptide binding. Nature 345, 615-618.
27. Rubinstein, E., Le Naour, F., Lagaudriere-Gesbert, C., Billard, M., Conjeaud, H. and Boucheix, C. (1996). CD9, CD63, CD81, and CD82 are components of a surface tetraspan network connected to HLA-DR and VLA integrins. Eur. J. Immunol. 26, 2657-2665.
28. Saffman, P. G. and Delbruck, M. (1975). Brownian motion in biological membranes. Proc. Natl. Acad. Sci. USA 72, 3111-3113.
29. Sanderson, F., Thomas, C., Neefjes, J. and Trowsdale, J. (1996). Association between HLA-DM and HLA-DR in vivo. Immunity 4, 87-96.
30. Tarrant, J. M., Robb, L., van Spriel, A. B. and Wright, M. D. (2003). Tetraspanins: molecular organisers of the leukocyte surface. Trends Immunol. 24, 610-617.
31. Teis, D., Saksena, S. and Emr, S. D. (2009). SnapShot: the ESCRT machinery. Cell 137, 182-182.e181.
32. Unternaehrer, J. J., Chow, A., Pypaert, M., Inaba, K. and Mellman, I. (2007). The tetraspanin CD9 mediates lateral association of MHC class II molecules on the dendritic cell surface. Proc. Natl. Acad. Sci. USA 104, 234-239.
33. van Rheenen, J., Langeslag, M. and Jalink, K. (2004). Correcting confocal acquisition to optimize imaging of fluorescence resonance energy transfer by sensitized emission. Biophys. J. 86, 2517-2529.
34. Vennegoor, C. and Rumke, P. (1986). Circulating melanoma-associated antigen detected by monoclonal antibody NKI/C-3. Cancer Immunol. Immunother. 23, 93-100.
35. Wang, H. X., Kolesnikova, T. V., Denison, C., Gygi, S. P. and Hemler, M. E. (2011). The C-terminal tail of tetraspanin protein CD9 contributes to its function and molecular organization. J. Cell Sci. 124, 2702-2710.
36. Wubbolts, R., Leckie, R. S., Veenhuizen, P. T., Schwarzmann, G., Mobius, W., Hoernschemeyer, J., Slot, J. W., Geuze, H. J. and Stoorvogel, W. (2003). Proteomic and biochemical analyses of human B cell-derived exosomes. Potential implications for their function and multivesicular body formation. J. Biol. Chem. 278, 10963-10972.
37. Zwart, W., Griekspoor, A., Kuijl, C., Marsman, M., van Rheenen, J., Janssen, H., Calafat, J., van Ham, M., Janssen, L., van Lith, M. et al. (2005). Spatial separation of HLA-DM/HLA-DR interactions within MIIC and phagosome-induced immune escape. Immunity 22, 221-233.