Human B lymphoblastoid cells contain distinct patterns of cathepsin activity in endocytic compartments and regulate MHC class II transport in a cathepsin S-independent manner

Journal of Leukocyte Biology

Volumn 75, Issue 5, 2004, Pages 844-855

  Lautwein, Alfred ^a   Kraus, Marianne ^a   Reich, Michael ^a   Burster, Timo ^a   Brandenburg, J ^a   Overkleeft, Herman S ^b   Schwarz, Gerold ^a   Kammer, Winfried ^a   Weber, Ekkehard ^c   Kalbacher, Hubert ^a   Nordheim, Alfred ^a   Driessen, Christoph ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b LEIDEN UNIVERSITY   (Netherlands)

^c MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

Author keywords

Antigen presentation; Endocytic proteases

Indexed keywords

ASPARAGINE SPECIFIC ENDOPROTEASE; CATHEPSIN; CATHEPSIN B; CATHEPSIN D; CATHEPSIN H; CATHEPSIN S; CATHEPSIN Z; DIPEPTIDYL PEPTIDASE I; HLA DM ANTIGEN; LEUCINE HOMOPHENYLALANINE VINYLSULFONE PHENOL; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; PHENOL DERIVATIVE; PROTEINASE; UNCLASSIFIED DRUG; VINYL DERIVATIVE;

AMINO TERMINAL SEQUENCE; ANTIGEN PRESENTATION; ARTICLE; B LYMPHOCYTE; BIOTINYLATION; CARBOXY TERMINAL SEQUENCE; CELL FRACTIONATION; DENDRITIC CELL; ENDOCYTOSIS; ENDOSOME; ENZYME ACTIVITY; HUMAN; HUMAN CELL; INTRACELLULAR TRANSPORT; LYMPHOBLASTOID CELL; LYSOSOME; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN LOCALIZATION;

ANTIGEN PRESENTATION; ANTIGENS, DIFFERENTIATION, B-LYMPHOCYTE; B-LYMPHOCYTES; BIOLOGICAL TRANSPORT; CATHEPSINS; CELL FRACTIONATION; ENDOCYTOSIS; ENDOSOMES; HISTOCOMPATIBILITY ANTIGENS CLASS II; HUMANS; LYSOSOMES;

FELIS CATUS;

EID: 2342464264     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.0803367     Document Type: Article

References (56)

1. Wolf, P. R., Ploegh, H. L. (1995) How MHC class H molecules acquire peptide cargo: biosynthesis and trafficking through the endocytic pathway. Annu. Rev. Cell Dev. Biol. 11, 267-306.
2. Villadangos, J. A., Ploegh, H. L. (2000) Proteolysis in MHC class II antigen presentation: who's in charge? Immunity 12, 233-239.
3. Chapman, H. A. (1998) Endosomal proteolysis and MHC class II function. Curr. Opin. Immunol. 10, 93-102.
4. Manoury, B., Hewitt, E. W., Morrice, N., Dando, P. M., Barrett, A. J., Watts, C. (1998) An asparaginyl endopeptidase processes a microbial antigen for class II MHC presentation. Nature 396, 695-699.
5. Chapman, H. A., Riese, R. J., Shi, G. P. (1997) Emerging roles for cysteine proteases in human biology. Annu. Rev. Physiol. 59, 63-88.
6. Beck, H., Schwarz, G., Schroter, C. J., Deeg, M., Baier, D., Stevanovic, S., Weber, E., Driessen, C., Kalbacher, H. (2001) Cathepsin S and an asparagine-specific endoprotease dominate the proteolytic processing of human myelin basic protein in vitro. Eur. J. Immunol. 31, 3726-3736.
7. Riese, R. J., Wolf, P. R., Bromme, D., Natkin, L. R., Villadangos, J. A., Ploegh, H. L., Chapman, H. A. (1996) Essential role for cathepsin S in the MHC class II-associated invariant chain proecessing and peptide loading. Immunity 4, 357-366.
8. Nakagawa, T., Roth, W., Wong, P., Nelson, A., Farr, A., Deussing, J., Villadangos, J. A., Ploegh, H., Peters, C., Rudensky, A. Y. (1998) Cathepsin L: critical role in Ii degradation and CD4 T cell selection in the thymus. Science 280, 450-453.
9. Deussing, J., Roth, W., Saftig, P., Peters, C., Ploegh, H. L., Villadangos, J. A. (1998) Cathepsins B and D are dispensable for major histocompatibility complex class II-mediated antigen presentation. Proc. Natl. Acad. Sci. USA 95, 4516-4521.
10. Driessen, C., Lennon-Dumenil, A. M., Ploegh, H. L. (2001) Individual cathepsins degrade immune complexes internalized by antigen-presenting cells via Fcγ receptors. Eur. J. Immunol. 31, 1592-1601.
11. Pluger, E. B., Boes, M., Alfonso, C., Schroter, C. J., Kalbacher, H., Ploegh, H. L., Driessen, C. (2002) Specific role for cathepsin S in the generation of antigenic peptides in vivo. Eur. J. Immunol. 32, 467-476.
12. Riese, R. J., Chapman, H. A. (2000) Cathepsins and compartmentalization in antigen presentation. Curr. Opin. Immunol. 12, 107-113.
13. Lennon-Dumenil, A. M., Bakker, A. H., Maehr, R., Fiebiger, E., Overkleeft, H. S., Rosemblatt, M., Ploegh, H. L., Lagaudriere-Gesbert, C. (2002) Analysis of protease activity in live antigen-presenting cells shows regulation of the phagosomal proteolytic contents during dendritic cell activation. J. Exp. Med. 196, 529-540.
14. Neefjes, J. J., Stollorz, V., Peters, P. J., Geuze, H. J., Ploegh, H. L. (1990) The biosynthetic pathway of MHC class II but not class I molecules intersects the endocytic route. Cell 61, 171-183.
15. Peters, P. J., Neefjes, J. J., Oorschot, V., Ploegh, H. L., 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.
16. Peters, P. J., Raposo, G., Neefjes, J. J., Oorschot, V., Leijendekker, R. L., Geuze, H. J., Ploegh, H. L. (1995) Major histocompatibility complex class II compartments in human B lymphoblastoid cells are distinct from early endosomes. J. Exp. Med. 182, 325-334.
17. Kleijmeer, M. J., Morkowski, S., Griffith, J. M., Rudensky, A. Y., Geuze, H. J. (1997) Major histocompatibility complex class II compartments in human and mouse B lymphoblasts represent conventional endocytic compartments. J. Cell Biol. 139, 639-649.
18. Maric, M. A., Taylor, M. D., Blum, J. S. (1994) Endosomal aspartic proteinases are required for invariant-chain processing. Proc. Natl. Acad. Sci. USA 91, 2171-2175.
19. Romagnoli, P., Layet, C., Yewdell, J., Bakke, O., Germain, R. N. (1993) Relationship between invariant chain expression and major histocompatibility complex class II transport into early and late endocytic compartments. J. Exp. Med. 177, 583-596.
20. Blum, J. S., Cresswell, P. (1988) Role for intracellular proteases in the processing and transport of class II HLA antigens. Proc. Natl. Acad. Sci. USA 85, 3975-3979.
21. Manoury, B., Mazzeo, D., Li, D. N., Billson, J., Loak, K., Benaroch, P., Watts, C. (2003) Asparagine endopeptidase can initiate the removal of the MHC class II invariant chain chaperone. Immunity 18, 489-498.
22. Roche, P. A., Cresswell, P. (1991) Proteolysis of the class II-associated invariant chain generates a peptide-binding site in intracellular HLA-DR molecules. Proc. Natl. Acad. Sci. USA 88, 3150-3154.
23. Fiebiger, E., Meraner, P., Weber, E., Fang, I. F., Stingl, G., Ploegh, H., Maurer, D. (2001) Cytokines regulate proteolysis in major histocompatibility complex class II-dependent antigen presentation by dendritic: cells. J. Exp. Med. 193, 881-892.
24. Morton, P. A., Zacheis, M. L., Giecoletto, K. S., Manning, J. A., Schwartz, B. D. (1995) Delivery of nascent MHC class II-invariant chain complexes to lysosomal compartments, and proteolysis of invariant chain by cysteine proteases precedes peptide binding in B-lymphoblastoid cells. J. Immunol. 154, 137-150.
25. Nakagawa, T. Y., Rudensky, A. Y. (1999) The role of lysosomal proteinases in MHC class II-mediated antigen processing and presentation. Immunol. Rev. 172, 121-129.
26. Greiner, A., Lautwein, A., Overkleeft, H. S., Weber, E., Driessen, C. (2003) Activity and subcellular distribution of cathepsins in primary human monocytes. J. Leukoc. Biol. 73, 235-242.
27. Guagliardi, L. E., Koppelman, B., Blum, J. S., Marks, M. S., Cresswell, P., Brodsky, F. M. (1990) Co-localization of molecules involved in antigen processing and presentation in an early endocytic compartment. Nature 343, 133-139.
28. Drake, J. R., Lewis, T. A., Condon, K. B., Mitchell, R. N., Webster, P. (1999) Involvement of MIIC-like late endosomes in B cell receptor-mediated antigen processing in murine B cells. J. Immunol. 162, 1150-1155.
29. Neefjes, J. J., Ploegh, H. L. (1992) Inhibition of endosomal proteolytic activity by leupeptin blocks surface expression of MHC class II molecules and their conversion to SDS resistance α β heterodimers in endosomes. EMBO J. 11, 411-416.
30. 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.
31. Loss Jr., G. E., Sant, A. J. (1993) Invariant chain retains MHC class II molecules in the endocytic pathway. J. Immunol. 150, 3187-3197.
32. Shi, G. P., Villadangos, J. A., Dranoff, G., Small, C., Gu, L., Haley, K. J., Riese, R., Ploegh, H. L., Chapman, H. A. (1999) Cathepsin S required for normal MHC class II peptide loading and germinal center development. Immunity 10, 197-206.
33. Wiendl, H., Lautwein, A., Mitsdorffer, M., Krause, S., Erfurth, S., Wienhold, W., Morgalla, M., Weber, E., Overkleeft, H. S., Lochmuller, H., Melms, A., Tolosa, E., Driessen, C. (2003) Antigen processing and presentation in human muscle: cathepsin S is critical for MHC class II expression and upregulated in inflammatory myopathies. J. Neuroimmunol. 138, 132-143.
34. 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.
35. 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.
36. Lautwein, A., Burster, T., Lennon-Dumenil, A. M., Overkleeft, H. S., Weber, E., Kalbacher, H., Driessen, C. (2002) Inflammatory stimuli recruit cathepsin activity to late endosomal compartments in human dendritic cells. Eur. J. Immunol. 32, 3348-3357.
37. Kleijmeer, M., Ramm, G., Schuurhuis, D., Griffith, J., Reseigno, 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.
38. Greenbaum, D., Medzihradszky, K. F., Burlingame, A., Bogyo, M. (2000) Epoxide electrophiles as activity-dependent cysteine protease profiling and discovery tools. Chem. Biol. 7, 569-581.
39. Shi, G. P., Bryant, R. A., Riese, R., Verhelst, S., Driessen, C., Li, Z., Bromme, D., Ploegh, H. L., Chapman, H. A. (2000) Role for cathepsin F in invariant chain processing and major histocompatibility complex class II peptide loading by macrophages. J. Exp. Med. 191, 1177-1186.
40. Palmer, J. T., Rasnick, D., Klaus, J. L., Bromme, D. (1995) Vinyl sulfones as mechanism-based cysteine protease inhibitors. J. Med. Chem. 38, 3193-3196.
41. Villadangos, J. A., Driessen, C., Shi, G. P., Chapman, H. A., Ploegh, H. L. (2000) Early endosomal maturation of MHC class II molecules independently of cysteine proteases and H-2DM. EMBO J. 19, 882-891.
42. Schroter, C. J., Braun, M., Englert, J., Beck, H., Schmid, H., Kalbacher, H. (1999) A rapid method to separate endosomes from lysosomal contents using differential centrifugation and hypotonic lysis of lysosomes. J. Immunol. Methods 227, 161-168.
43. Castellino, F., Germain, R. N. (1995) Extensive trafficking of MHC class II-invariant chain complexes in the endocytic pathway and appearance of peptide-loaded class II in multiple compartments. Immunity 2, 73-88.
44. Shevchenko, A., Wilm, M., Vorm, O., Mann, M. (1996) Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal. Chem. 68, 850-858.
45. Perkins, D. N., Pappin, D. J., Creasy, D. M., Cottrell, J. S. (1999) Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis 20, 3551-3567.
46. Villadangos, J. A., Bryant, R. A., Deussing, J., Driessen, C., Lennon-Dumenil, A. M., Riese, R. J., Roth, W., Saftig, P., Shi, G. P., Chapman, H. A., Peters, C., Ploegh, H. L. (1999) Proteases involved in MHC class II antigen presentation. Immunol. Rev. 172, 109-120.
47. Villadangos, J. A., Riese, R. J., Peters, C., Chapman, H. A., Ploegh, H. L. (1997) Degradation of mouse invariant chain: roles of cathepsins S and D and the influence of major histocompatibility complex polymorphism. J. Exp. Med. 186, 549-560.
48. Benaroch, P., Yilla, M., Raposo, G., Ito, K., Miwa, K., Geuze, H. J., Ploegh, H. L. (1995) How MHC class II molecules reach the endocytic pathway. EMBO J. 14, 37-49.
49. Kleijmeer, M. J., Ossevoort, M. A., van Veen, C. J., van Hellemond, J. J., Neefjes, J. J., Kast, W. M., Melief, C. J., Geuze, H. J. (1995) MHC class II compartments and the kinetics of antigen presentation in activated mouse spleen dendritic cells. J. Immunol. 154, 5715-5724.
50. Garin, J., Diez, R., Kieffer, S., Dermine, J. F., Duclos, S., Gagnon, E., Sadoul, R., Rondeau, C., Desjardins, M. (2001) The phagosome proteome: insight into phagosome functions. J. Cell Biol. 152, 165-180.
51. Pierre, P., Mellman, I. (1998) Developmental regulation of invariant chain proteolysis controls MHC class H trafficking in mouse dendritic cells. Cell 93, 1135-1145.
52. 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.
53. Amigorena, S., Webster, P., Drake, J., Newcomb, J., Cresswell, P., Mellman, I. (1995) Invariant chain cleavage and peptide loading in major histocompatibility complex class II vesicles. J. Exp. Med. 181, 1729-1741.
54. Brachet, V., Raposo, G., Amigorena, S., Mellman, I. (1997) Ii chain controls the transport of major histocompatibility complex class II molecules to and from lysosomes. J. Cell Biol. 137, 51-65.
55. Denzin, L. K., Hammond, C., Cresswell, P. (1996) HLA-DM interactions with intermediates in HLA-DR maturation and a role for HLA-DM in stabilizing empty HLA-DR molecules. J. Exp. Med. 184, 2153-2165.
56. Zachgo, S., Dobberstein, B., Griffiths, G. (1992) A block in degradation of MHC class II-associated invariant chain correlates with a reduction in transport from endosome carrier vesicles to the prelysosome compartment. J. Cell Sci. 103, 811-822.