Differential post-translational modification of CD63 molecules during maturation of human dendritic cells

European Journal of Biochemistry

Volumn 270, Issue 11, 2003, Pages 2412-2420

  Engering, Anneke ^a,c   Kuhn, Lotte ^a,b   Fluitsma, Donna ^c   Hoefsmit, Elisabeth ^c   Pieters, Jean ^a,b  

^a BASEL INSTITUTE FOR IMMUNOLOGY   (Switzerland)

^b UNIVERSITY OF BASEL   (Switzerland)

^c VU UNIVERSITY AMSTERDAM   (Netherlands)

Author keywords

Antigen presentation; Dendritic cells; MHC class II; Poly N acetyl lactosamine addition; Tetraspanins

Indexed keywords

AMINE; CD63 ANTIGEN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; POLY N ACETYLLACTOSAMINE; TETRASPANIN; UNCLASSIFIED DRUG;

ANTIGEN PRESENTATION; ANTIGEN STRUCTURE; ARTICLE; CELL MATURATION; CELL STRUCTURE; DENDRITIC CELL; DOWN REGULATION; HUMAN; HUMAN CELL; MAJOR HISTOCOMPATIBILITY COMPLEX; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROCESSING;

ANTIGEN PRESENTATION; ANTIGENS, CD; CELL ADHESION MOLECULES, NEURONAL; CELL DIVISION; DENDRITIC CELLS; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; GENES, MHC CLASS II; GLYCOSYLATION; HUMANS; IMMUNOHISTOCHEMISTRY; PLATELET MEMBRANE GLYCOPROTEINS; PRECIPITIN TESTS; PROTEIN ISOFORMS; PROTEIN PROCESSING, POST-TRANSLATIONAL; SUBCELLULAR FRACTIONS;

EID: 0038054203     PISSN: 00142956     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1432-1033.2003.03609.x     Document Type: Article

References (56)

1. Lanzavecchia, A. & Sallusto, F. (2001) Regulation of T cell immunity by dendritic cells. Cell 106, 263-266.
2. Cella, M., Sallusto, F. & Lanzavecchia, A. (1997) Origin, maturation and antigen presenting function of dendritic cells. Curr. Opin. Immunol. 9, 10-16.
3. Pieters, J. (2000) MHC Class II restricted antigen processing and presentation. Adv. Immunol. 75, 159-200.
4. Engering, A.J., Cella, M., Fluitsma, D.M., Hoefsmit, E.C.M., Lanzavecchia, A. & Pieters, J. (1997) The mannose receptor functions as a high capacity and broad specificity antigen receptor in human dendritic cells. Eur. J. Immunol. 27, 2417-2425.
5. Watts, C. (1997) Capture and processing of exogenous antigens for presentation on MHC molecules. Annu. Rev. Immunol. 15, 821-850.
6. Amigorena, S., Drake, J.R., Webster, P. & Mellman, I. (1994) Transient accumulation of new MHC molecules in a novel endocytic compartment in B lymphocytes. Nature 369, 113-120.
7. Tulp, A., Verwoerd, D., Dobberstein, B., Ploegh, H.L. & Pieters, J. (1994) Isolation and characterization of the intracellular MHC class II compartment. Nature 369, 120-126.
8. West, M.A., Lucocq, J.M. & Watts, C. (1994) Antigen processing and class II MHC peptide-loading compartments in human B-lymphoblastoid cells. Nature. 369, 147-151.
9. Ferrari, G., Knight, A.M., Watts, C. & Pieters, J. (1997) Distinct intracellular compartments involved in invariant chain degradation and antigenic peptide loading of major histocompatibility complex (MHC) class II molecules. J Cell Biol. 139, 1433-1446.
10. Cella, M., Engering, A., Pinet, V., Pieters, J. & Lanzavecchia, A. (1997) Inflammatory stimuli induce accumulation of MHC class II complexes on dendritic cells. Nature 388, 782-787.
11. Pierre, P., Turley, S.J., Gatti, E., Hull, M., Meltzer, J., Mirza, A., Inaba, K., Steinman, R.M. & Mellman, I. (1997) Developmental regulation of MHC class II transport in mouse dendritic cells. Nature 388, 787-792.
12. Driessen, C., Bryant, R.A., Lennon-Dumenil, A.M., Villadangos, J.A., Bryant, P.W., Shi, G.P., Chapman, H.A. & Ploegh, H.L. (1999) Cathepsin S controls the trafficking and maturation of MHC class II molecules in dendritic cells. J Cell Biol. 147, 775-790.
13. Pierre, P. & Mellman, I. (1998) Developmental regulation of invariant chain proteolysis controls MHC class II trafficking in mouse dendritic cells. Cell 93, 1135-1145.
14. Bakke, O. & Dobberstein, B. (1990) MHC class II-associated invariant chain contains a sorting signal for endosomal compartments. Cell 63, 707-716.
15. Lotteau, V., Teyton, L., Peleraux, A., Nilsson, T., Karlsson, L., Schmid, S.L., Quaranta, V. & Peterson, P.A. (1990) Intracellular transport of class II MHC molecules directed by invariant chain. Nature 348, 600-605.
16. Pieters, J., Bakke, O. & Dobberstein, B. (1993) The MHC class II-associated Invariant chain contains two endosomal sorting signals within its cytoplasmic tail. J. Cell Sci. 106, 831-846.
17. Villadangos, J.A., Cardoso, M., Steptoe, R.J., van Berkel, D., Pooley, J., Carbone, F.R. & Shortman, K. (2001) MHC class II expression is regulated in dendritic cells independently of invariant chain degradation. Immunity 14, 739-749.
18. Banchereau, J. & Steinman, R.M. (1998) Dendritic cells and the control of immunity. Nature 392, 245-252.
19. Hiltbold, E.M. & Roche, P.A. (2002) Trafficking of MHC class II molecules in the late secretory pathway. Curr. Opin. Immunol. 14, 30-35.
20. Yewdell, J.W. & Tscharke, D.C. (2002) Inside the professionals. Nature 418, 923-924.
21. Zitvogel, L., Regnault, A., Lozier, A., Wolfers, J., Flament, C., Tenza, D., Ricciardi-Castagnoli, P., Raposo, G. & Amigorena, S. (1998) Eradication of established murine tumors using a novel cell-free vaccine: dendritic cell-derived exosomes. Nat. Med. 4, 594-600.
22. Raposo, G., Nijman, H.W., Stoorvogel, W., Leijendekker, R., Harding, C.V., Melief, C.J.M. & Geuze, H.J. (1996) B lymphocytes secrete antigen-presentnig vesicles. J. Exp. Med. 183, 1161-1172.
23. Thery, C., Regnault, A., Garin, J., Wolfers, J., Zitvogel, L., Ricciardi-Castagnoli, P., Raposo, G. & Amigorena, S. (1999) Molecular characterization of dendritic cell-derived exosomes. Selective accumulation of the heat shock protein hsc73. J. Cell Biol. 147, 599-610.
24. Boes, M., Cerny, J., Massol, R., Op den Brouw, M., Kirchhausen, T., Chen, J. & Ploegh, H.L. (2002) T-cell engagement of dendritic cells rapidly rearranges MHC class II transport. Nature 418, 983-988.
25. Chow, A., Toomre, D., Garrett, W. & Mellman, I. (2002) Dendritic cell maturation triggers retrograde MHC class II transport from lysosomes to the plasma membrane. Nature 418, 988-994.
26. Barois, N., De Saint-Vis, B., Lebecque, S., Geuze, H.J. & Kleijmeer, M.J. (2002) MHC class II compartments in human dendritic cells undergo profound structural changes upon activation. Traffic 3, 894-905.
27. Kleijmeer, M., Ramm, G., Schuurhuis, D., Griffith, J., Rescigno, M., Ricciardi-Castagnoli, P., Rudensky, A.Y., Ossendorp, F., Melief, C.J., Stoorvogel, W. & Geuze, H.J. (2001) Reorganization of multivesicular bodies regulates MHC class II antigen presentation by dendritic cells. J. Cell Biol. 155, 53-63.
28. Engering, A. & 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.
29. Hammond, C., Denzin, L.K., Pan, M., Griffith, J.M., Geuze, H.J. & 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.
30. Sallusto, F. & Lanzavecchia, A. (1994) Efficient presentation of soluble antigen by cultured human dendritic cells is maintained by granulocyte/macrophage colony-stimulating factor plus interleukin 4 and downregulated by tumor necrosis factor alpha. J. Exp. Med. 179, 1109-1118.
31. Johnson, J.P., Demmer-Dieckmann, M., Meo, T., Hadam, M.R. & Riethmuller, G. (1981) Surface antigens of human melanoma cells defined by monoclonal antibodies. I. Biochemical characterization of two antigens found on cell lines and fresh tumors of diverse tissue origin. Eur. J. Immunol. 11, 825-831.
32. Pieters, J., Horstmann, H., Bakke, O., Griffiths, G. & Lipp, J. (1991) Intracellular transport and localization of major histocompatibility complex class II molecules and associated invariant chain. J. Cell Biol. 115, 1213-1223.
33. Engering, A.J., Richters, C.D., Fluitsma, D.M., van Pelt, A.M., Kamperdijk, E.W., Hoefsmit, E.C. & Pieters, J. (1998) MHC class II and invariant chain biosynthesis and transport during maturation of human precursor dendritic cells. Int. Immunol. 10, 1713-1723.
34. Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
35. O'Farrell, P.H. (1975) High resolution two-dimensional electrophoresis of proteins. J. Biol. Chem. 250, 4007-4021.
36. Lefkovits, I., Young, P., Kuhn, L., Kettman, J., Gemmell, A., Tollaksen, S., Anderson, L. & Anderson, N. (1985) Use of Large-Scale Two-Dimensional ISODALT Gel Electrophoresis Systems in Immunology. Academic Press, Orlando, FL.
37. Tulp, A., Verwoerd, D. & Pieters, J. (1993) Application of an improved density gradient electrophoresis apparatus to the separation of proteins, cells and subcellular organelles. Electrophoresis 14, 1295-1301.
38. Bradford, M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254.
39. Koldovsky, O. & Palmieri, M. (1971) Cortisone-evoked decrease of acid β-galactosidase, β-glucuronidase, N-acetyl-β-glucosaminidase and acrylsulphatase in the ileum of sucling rats. Biochem. J. 125, 697-701.
40. Escola, J.M., Kleijmeer, M.J., Stoorvogel, W., Griffith, J.M., Yoshie, O. & 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.
41. Metzelaar, M.J., Wijngaard, P.L., Peters, P.J., Sixma, J.J., Nieuwenhuis, H.K. & Clevers, H.C. (1991) CD63 antigen. A novel lysosomal membrane glycoprotein, cloned by a screening procedure for intracellular antigens in eukaryotic cells. J. Biol. Chem. 266, 3239-3245.
42. Carlsson, S.R. & Fukuda, M. (1990) The polylactosaminoglycans of human lysosomal membrane glycoproteins lamp-1 and lamp-2. Localization on the peptide backbones. J. Biol. Chem. 265, 20488-20495.
43. Lee, N., Wang, W.C. & Fukuda, M. (1990) Granulocytic differentiation of HL-60 cells is associated with increase of poly-N-acetyllactosamine in Asn-linked oligosaccharides attached to human lysosomal membrane glycoproteins. J. Biol. Chem. 265, 20476-20487.
44. Sallusto, F., Cella, M., Danieli, C. & Lanzavecchia, A. (1995) Dendritic cells use macropinocytosis and the mannose receptor to concentrate macromolecules in the major histocompatibility complex class II compartment: downregulation by cytokines and bacterial products. J. Exp Med. 182, 389-400.
45. Hunziker, W. & Geuze, H.J. (1996) Intracellular trafficking of lysosomal membrane proteins. Bioessays 18, 379-389.
46. Kleijmeer, M.J., Raposo, G. & Geuze, H.J. (1996) Characterization of MHC Class II Compartments by Immunoelectron Microscopy. Methods. 10, 191-207.
47. Maecker, H.T., Todd, S.C. & Levy, S. (1997) The tetraspanin superfamily: molecular facilitators. FASEB J. 11, 428-442.
48. Kropshofer, H., Spindeldreher, S., Rohn, T.A., Platania, N., Grygar, C., Daniel, N., Wolpl, A., Langen, H., Horejsi, V. & Vogt, A.B. (2002) Tetraspan microdomains distinct from lipid rafts enrich select peptide-MHC class II complexes. Nat. Immunol. 3, 61-68.
49. Vogt, A.B., Spindeldreher, S. & Kropshofer, H. (2002) Clustering of MHC-peptide complexes prior to their engagement in the immunological synapse: lipid raft and tetraspan microdomains. Immunol. Rev. 189, 136-151.
50. Peters, P.J., Borst, J., Oorschot, V., Fukuda, M., Krahenbuhl, O., Tschopp, J., Slot, J.W. & Geuze, H.J. (1991) Cytotoxic T lymphocyte granules are secretory lysosomes, containing both perforin and granzymes. J. Exp. Med. 173, 1099-1109.
51. Griffiths, G.M. (1995) The cell biology of CTL killing, Curr. Opin. Immunol. 7, 343-348.
52. Vischer, U.M. & Wagner, D.D. (1993) CD63 is a component of Weibel-Palade bodies of human endothelial cells. Blood 82, 1184-1191.
53. Tapper, H. & Grinstein, S. (1997) Fc receptor-triggered insertion of secretory granules into the plasma membrane of human neutrophils: selective retrieval during phagocytosis. J. Immunol. 159, 409-418.
54. Calafat, J., Janssen, H., Knol, E.F., Weller, P.F. & Egesten, A. (1997) Ultrastructural localization of Charcot-Leyden crystal protein in human eosinophils and basophils. Eur. J. Haematol. 58, 56-66.
55. Heijnen, H.F., Debili, N., Vainchencker, W., Breton-Gorius, J., Geuze, H.J. & Sixma, J.J. (1998) Multivesicular bodies are an intermediate stage in the formation of platelet alpha-granules. Blood 91, 2313-2325.
56. Stossel, H., Koch, F., Kampgen, E., Stoger, P., Lenz, A., Heufler, C., Romani, N. & Schuler, G. (1990) Disappearance of certain acidic organelles (endosomes and Langerhans cell granules) accompanies loss of antigen processing capacity upon culture of epidermal Langerhans cells. J. Exp. Med. 172, 1471-1482.