Cysteine proteases: Destruction ability versus immunomodulation capacity in immune cells

Biological Chemistry

Volumn 388, Issue 11, 2007, Pages 1141-1149

  Zavašnik Bergant, Tina ^a   Turk, Boris ^a  

^a JO EF STEFAN INSTITUTE   (Slovenia)

Author keywords

Antigen presentation; Asparagine endopeptidase; Autophagy; Cathepsins; Cystatins; Dipeptidyl peptidase I

Indexed keywords

CATHEPSIN; CYSTATIN; CYSTEINE PROTEINASE; DIPEPTIDYL PEPTIDASE I; GRANZYME A; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; PROTEINASE;

ANTIGEN PRESENTATION; AUTOPHAGY; CELL DESTRUCTION; CELL MATURATION; CONFERENCE PAPER; CYTOSOL; ENDOSOME; ENZYME ACTIVATION; HUMAN; IMMUNE RESPONSE; IMMUNOCOMPETENT CELL; IMMUNOMODULATION; LYSOSOME; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FUNCTION; T LYMPHOCYTE;

ANIMALS; CYSTEINE ENDOPEPTIDASES; ENDOCYTOSIS; HUMANS; HYDROLYSIS; IMMUNE SYSTEM;

EID: 35848948133     PISSN: 14316730     EISSN: 14374315     Source Type: Journal    
DOI: 10.1515/BC.2007.144     Document Type: Conference Paper

References (91)

1. Abdul-Hussein, H., Soekhoe, R.G., Weber, E., von der Thüsen, J.H., Kleemann, R., Mulder, A., van Bockel, J.H., Hanemaaijer, R., and Lindeman, J.H. (2007). Collagen degradation in the abdominal aneurysm: a conspiracy of matrix metalloproteinase and cysteine collagenases. Am. J. Pathol. 170, 809-817.
2. Adkison, A.M., Raptis, S.Z., Kelley D.G., and Pham, C.T. (2002). Dipeptidyl peptidase activates neutrophil-derived serine proteases and regulates the development of acute experimental arthritis. J. Clin. Invest. 109, 363-371.
3. Antoniou, A.N., Blackwood, S.L., Mazzeo, D., and Watts, C. (2000). Control of antigen presentation by a single protease cleavage site. Immunity 12, 391-398.
4. Barrett, A.J., Rawlings, N.D., and Woessner, J.F. Jr. (2004). Handbook of Proteolytic Enzymes (New York, USA: Academic Press).
5. Bevan, M.J. (2006). Cross-priming. Nat. Immunol. 7, 363-365.
6. Bevec, T., Stoka, V., Pungerčič, G., Dolenc, I., and Turk, V. (1996). Major histocompatibility complex class II-associated p41 invariant chain fragment is a strong inhibitor of lysosomal cathepsin L. J. Exp. Med. 183, 1331-1338.
7. Brömme, D., Li, Z., Barnes, M., and Mehler, E. (1999). Human cathepsin V functional expression, tissue distribution, electrostatic surface potential, enzymatic characterization, and chromosomal localization. Biochemistry 38, 2377-2385.
8. Brown, J., Matutes, E., Singleton, A., Price, C., Molgaard, H., Buttle, D., and Enver, T. (1998). Lymphopain, cytotoxic T and natural killer cell-associated cysteine proteinase. Leukemia 12, 1771-1781.
9. Burster, T., Giffon, T., Dahl, M.E., Björck, P., Bogyo, M., Weber, E., Mahmood, K., Lewis, D.B., and Mellins, E.D. (2007). Influenza A virus elevates active cathepsin B in primary murine DC. Int. Immunol. 19, 645-655.
10. Chapman, H.A. (2006). Endosomal proteases in antigen presentation. Curr. Opin. Immunol. 18, 78-84.
11. Chapman, H.A., Riese, R.J., and Shi, G.P. (1997). Emerging roles for cysteine proteases in human biology. Annu. Rev. Physiol. 59, 63-88.
12. Dengjel, J., Schoor, O., Fischer, R., Reich, M., Kraus, M., Müller, M., Kreymborg, K., Altenberend, F., Brandenburg, J., Kalbacher, H., et al. (2005). Autophagy promotes MHC class II presentation of peptides from intracellular source proteins. Proc. Natl. Acad. Sci. USA 102, 7922-7927.
13. Deussing, J., Roth, W., Saftig, P., Peters, C., Ploegh, H.L., and 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.
14. Driessen, C., Bryant, R.A.R., Lennon-Duménil, A.M., Villadangos, J.A., Bryant, P.W., Shi, G.P., Chapman, H.A., and 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.
15. Duffy, M.S., Cevasco, D.K., Zarlenga, D.S., Sukhumavasi, W., and Appleton, J.A. (2006). Cathepsin B homologue at the interface between a parasitic nematode and its intermediate host. Infect. Immun. 74, 1297-1304.
16. Everts, V., Korper, W., Hoeben, K.A., Jansen, I.D., Bromme, D., Cleutjens, K.B., Heeneman, S., Peters, C., Reinheckel, T., Saftig, P., et al. (2006). Osteoclastic bone degradation and the role of different cysteine proteinases and matrix metalloproteinases: differences between calvaria and long bone. J. Bone Miner. Res. 21, 1399-1408.
17. Falk, K. and Rötzschke, O. (2002). The final cut: how ERAP1 trims MHC ligands to size. Nat. Immunol. 3, 1121-1122.
18. Fiebiger, E., Maehr, R., Villadangos, J., Weber, E., Erickson, A., Bikoff, E., Ploegh, H.L., and Lennon-Duménil, A.M. (2002). Invariant chain controls the activity of extracellular cathepsin L. J. Exp. Med. 196, 1263-1269.
19. Friedrichs, B., Tepel, C., Reinheckel, T., Deussing, J., von Figura, K., Herzog, V., Peters, C., Saftig, P., and Brix, K. (2003). Thyroid functions of mouse cathepsins B, K and L. J. Clin. Invest. 111, 1733-1745.
20. Grabowska, U., Chambers, T.J., and Shiroo, M. (2005). Recent developments in cathepsin K inhibitor design. Curr. Opin. Drug Discov. Dev. 8, 619-630.
21. Gunc? ar, G., Pungerčič, G., Klemenčič, I., Turk, V., and Turk, D. (1999). Crystal structure of MHC class II-associated p41 fragment bound to cathepsin L reveals the structural basis for differentiation between cathepsins L and S. EMBO J. 18, 793-803.
22. Hagemann, S., Günther, T., Dennemärker, J., Lohmüller, T., Brömme, D., Schüle, R., Peters, C., and Reinheckel, T. (2004). The human cysteine protease cathepsin V can compensate for murine cathepsin L in mouse epidermis and hair follicles. Eur. J. Cell Biol. 83, 775-780.
23. Honey, K. and Rudensky, A.Y. (2003). Lysosomal cysteine proteases regulate antigen presentation. Nat. Rev. Immunol. 3, 472-482.
24. + T cell selection independently of its effect on invariant chain: a role in the generation of positively selecting peptide ligands. J. Exp. Med. 195, 1349-1358.
25. Hu, Y. and Pham, C.T. (2005). Dipeptidyl peptidase I regulates the development of collagen-induced arthritis. Arthritis Rheum. 52, 2553-2558.
26. Ishidoh, K., Takeda-Ezaki, M., Watanabe, S., Sato, N., Aihara, M., Imagawa, K., Kikuchi, M., and Kominami, E. (1999). Analysis of where and which types of proteinases participate in lysosomal proteinase processing using bafilomycin A1 and Helicobacter pylori Vac A toxin. J. Biochem. 125, 770-779.
27. Kitamoto, S., Sukhova, G.K., Sun, J., Yang, M., Libby, P., Love, V., Duramad, P., Sun, C., Zhang, Y., Yang, X., et al. (2007). Cathepsin L deficiency reduces diet-induced atherosclerosis in low-density lipoprotein receptor-knockout mice. Circulation 115, 2065-2075.
28. Koike, M., Nakanishi, H., Saftig, P., Ezaki, J., Isahara, K., Ohsawa, Y., Schulz-Schaeffer, W., Watanabe, T., Waguri, S., Kametaka, S., et al. (2000). Cathepsin D deficiency induces lysosomal storage with ceroid lipofuscin in mouse CNS neurons. J. Neurosci. 20, 6898-6906.
29. Kos, J., Sekirnik, A., Premzl, A., Zavašnik Bergant, V., Langerholc, T., Turk, B., Werle, B., Golouh, R., Repnik, U., Jeras, M., et al. (2005). Carboxypeptidases cathepsins X and B display distinct protein profile in human cells and tissues. Exp. Cell Res. 306, 103-113.
30. 3 mediates cell-adhesive properties. J. Biol. Chem. 281, 39588-39597.
31. Lennon-Duménil, A.M., Roberts, R.A., Valentijn, K., Driessen, C., Overkleeft, H.S., Erickson, A., Peters, P.J., Bikoff, E., Ploegh, H.L., and Wolf Bryant, P. (2001). The p41 isoform of invariant chain is a chaperone for cathepsin L. EMBO J. 20, 4055-4064.
32. Lennon-Duménil, A.M., Bakker, A.H., Maehr, R., Fiebiger, E., Overkleeft, H.S., Rosemblatt, M., Ploegh, H.L., and Lagaudrière-Gesbert, C. (2002). Analysis of protease activity in live antigen-presenting cells shows regulation of phagosomal proteolytic content during dendritic cell activation. J. Exp. Med. 196, 529-540.
33. Li, Z., Hou, W.S., and Brömme, D. (2000). Collagenolytic activity of cathepsin K is specifically modulated by cartilage-resident chondroitin sulfates. Biochemistry 39, 529-536.
34. Li, Z., Yasuda, Y., Li, W., Bogyo, M., Katz, N., Gordon, R.E., Fields, G.B., and Brömme, D. (2004). Regulation of collagenase activities of human cathepsins by glycosaminoglycans. J. Biol. Chem. 279, 5470-5479.
35. Liu, J., Sukhova, G.K., Yang, J.T., Sun, J., Ma, L., Ren, A., Xu, W.H., Fu, H., Dolganov, G.M., Hu, C., et al. (2006). Cathepsin L expression and regulation in human abdominal aortic aneurysm, atherosclerosis, and vascular cells. Atherosclerosis 184, 302-311.
36. Maehr, R., Hang, H.C., Mintern, J.D., Kim, Y.M., Cuvillier, A., Nishimura, M., Yamada, K., Shirahama-Noda, K., Hara-Nishimura, I., and Ploegh, H.L. (2005). Asparagine endopeptidase is not essential for class II MHC antigen presentation but is required for processing of cathepsin L in mice. J. Immunol. 174, 7066-7074.
37. Manoury, B., Hewitt, E.W., Morrice, N., Dando, P.M., Barrett, A.J., and Watts, C. (1998). An asparaginyl endopeptidase processes a microbial antigen for class II MHC presentation. Nature 396, 695-699.
38. Manoury, B., Mazzeo, D., Fugger, L., Viner, N., Ponsford, M., Streeter, H., Mazza, G., Wraith, D.C., and Watts, C. (2002). Destructive processing by asparagine endopeptidase limits presentation of a dominant T cell epitope in MBP. Nat. Immunol. 3, 169-174.
39. Manoury, B., Mazzeo, D., Li, D.N., Billson, J., Loak, K., Benaroch, P., and Watts, C. (2003). Asparagine endopeptidase can initiate the removal of the MHC class II invariant chain chaperone. Immunity 18, 489-498.
40. Menéndez-Benito, V. and Neefjes, J. (2007). Autophagy in MHC class II presentation: sampling from within. Immunity 26, 1-3.
41. Mohamed, M.M. and Sloane, B.F. (2006). Cysteine cathepsins: multifunctional enzymes in cancer. Nat. Rev. Cancer 6, 764-775. Monu, N. and Trombetta, E.S. (2007). Cross-talk between the endocytic pathway and the endoplasmic reticulum in cross-presentation by MHC class I molecules. Curr. Opin. Immunol. 19, 66-72.
42. Nakagawa, T.Y., Brissette, W.H., Lira, P.D., Griffiths, R.J., Petrushova, N., Stock, J., McNeish, J.D., Eastman. S.E., Howard, E.D., Clarke, S.R., et al. (1999). Impaired invariant chain degradation and antigen presentation and diminished collagen-induced arthritis in cathepsin S null mice. Immunity 10, 207-217.
43. Nakagawa, T.Y. and Rudensky, A.Y. (1999). The role of lysosomal proteinases in MHC class II-mediated antigen processing and presentation. Immunol. Rev. 172, 121-129.
44. Nakagawa, T., Roth, W., Wong, P., Nelson, A., Farr, A., Deussing, J., Villadangos, J.A., Ploegh, H., Peters, C., and Rudensky, A.Y. (1998). Cathepsin L: critical role in Ii degradation and CD4 T cell selection in the thymus. Science 280, 450-453.
45. Nimmerjahn, F., Milosevic, S., Behrends, U., Jaffee, E.M., Pardoll, D.M., Bornkamm, G.W., and Mautner, J. (2003). Major histocompatibility complex class II-restricted presentation of a cytosolic antigen by autophagy. Eur. J. Immunol. 33, 1250-1259.
46. Obermajer, N., Premzl, A., Zavašnik-Bergant, T., Turk, B., and Kos, J. (2006). Carboxypeptidase cathepsin X mediates β2-integrin-dependent adhesion of differentiated U-937 cells. Exp. Cell Res. 312, 2515-2527.
47. Ondr, J.K. and Pham, C.T. (2004). Characterization of murine cathepsin W and its role in cell-mediated cytotoxicity. J. Biol. Chem. 279, 27525-27533.
48. Pagano, M.B., Bartoli, M.A., Ennis, T.L., Mao, D., Simmons, P.M., Thompson, R.W., and Pham, C.T. (2007). Critical role of dipeptidyl peptidase I in neutrophil recruitment during the development of experimental abdominal aortic aneurysms. Proc. Natl. Acad. Sci. USA 104, 2855-2860.
49. Paludan, C., Schmid, D., Landthaler, M., Vockerodt, M., Kube, D., Tuschl, T., and Münz, C. (2005). Endogenous MHC class II processing of a viral nuclear antigen after autophagy. Science 307, 593-596.
50. Petanceska, S., Canoll, P., and Devi, L.A. (1996). Expression of rat cathepsin S in phagocytic cells. J. Biol. Chem. 271, 4403-4409.
51. Pham, C.T. and Ley, T.J. (1999). Dipeptidyl peptidase I is required for the processing and activation of granzymes A and B in vivo. Proc. Natl. Acad. Sci. USA 96, 8627-8632.
52. Pham, C.T., Ivanovich, J.L., Raptis, S.Z., Zehnbauer, B., and Ley, T.J. (2004). Papillon-Lefèvre syndrome: correlating the molecular, cellular, and clinical consequences of cathepsin C/dipeptidyl peptidase I deficiency in humans. J. Immunol. 173, 7277-7281.
53. Pierre, P. and Mellman, I. (1998). Developmental regulation of invariant chain proteolysis controls MHC class II trafficking in mouse dendritic cells. Cell 93, 1135-1145.
54. Que, X., Engel, J.C., Ferguson, D., Wunderlich, A., Tomavo, S., and Reed, S.L. (2007). Cathepsin Cs are key for the intracellular survival of the protozoan parasite, Toxoplasma gondii. J. Biol. Chem. 282, 4994-5003.
55. Rawlings, N.D., Morton, F.R., and Barrett, A.J. (2006). MEROPS: the peptidase database. Nucleic Acids Res. 34, D270-D272.
56. Reddy, V.Y., Zhang, Q.Y., and Weiss, S.J. (1995). Pericellular mobilization of the tissue-destructive cysteine proteinases, cathepsins B, L and S, by human monocyte-derived macrophages. Proc. Natl. Acad. Sci. USA 92, 3849-3853.
57. Reich, M., van Swieten, P.F., Sommandas, V., Kraus, M., Fischer, R., Weber, E., Kalbacher, H., Overkleeft, H.S., and Driessen, C. (2007). Endocytosis targets exogenous material selectively to cathepsin S in live human dendritic cells, while cell-penetrating peptides mediate nonselective transport to cysteine cathepsins. J. Leukoc. Biol. 81, 990-1001.
58. Reits, E., Neijssen, J., Herberts, C., Benckhuijsen, W., Janssen, L., Drijfhout, J.W., and Neefjes, J. (2004). A major role for TPPII in trimming proteasomal degradation products for MHC I antigen presentation. Immunity 20, 495-506.
59. Rock, K.L., York, I.A., and Goldberg, A.L. (2004). Post-proteasomal antigen processing for major histocompatibility complex class I presentation. Nat. Immunol. 5, 670-677.
60. Rossi, A., Deveraux, Q., Turk, B., and Šali, A. (2004). Comprehensive search for cysteine cathepsins in the human genome. Biol. Chem. 385, 363-372.
61. Roth, W., Deussing, J., Botchkarev, V.A., Pauly-Evers, M., Saftig, P., Hafner, A., Schmidt, P., Schmahl, W., Scherer, J., Anton-Lamprecht, I., et al. (2000). Cathepsin L deficiency as molecular defect of furless: hyperproliferation of keratinocytes and perturbation of hair follicle cycling. FASEB J. 14, 2075-2086.
62. Sevenich, L., Pennacchio, L.A., Peters, C., and Reinheckel, T. (2006). Human cathepsin L rescues the neurodegeneration and lethality in cathepsin B/L double-deficient mice. Biol. Chem. 387, 885-891.
63. Shi, G.P., Villadangos, J.A., Dranoff, G., Small, C., Gu, L., Haley, K.J., Riese, R., Ploegh, H.L., and Chapman, H.A. (1999). Cathepsin S is required for normal MHC class II peptide loading and germinal center development. Immunity 10, 197-206.
64. Shi, G.P., Bryant, R.A., Riese, R., Verhelst, S., Driessen, C., Li, Z., Brömme, D., Ploegh, H.L., and 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.
65. Sojka, D., Hajdušek, O., Dvorák, J., Sajid, M., Franta, Z., Schneider, E.L., Craik, C.S., Vancová, M., Burešová, V., Bogyo, M., et al. (2007). IrAE - an asparaginyl endopeptidase (legumain) in the gut of the hard tick Ixodes ricinus. Int. J. Parasitol. 37, 713-724.
66. Strawbridge, A.B. and Blum, J.S. (2007). Autophagy in MHC class II antigen processing. Curr. Opin. Immunol. 19, 87-92.
67. Stypmann, J., Gläser, K., Roth, W., Tobin, D.J., Petermann, I., Matthias, R., Monnig, G., Haverkamp, W., Breithardt, G., Schmahl, W., et al. (2002). Dilated cardiomyopathy in mice deficient for the lysosomal cysteine peptidase cathepsin L. Proc. Natl. Acad. Sci. USA 99, 6234-6239.
68. Sutton, V.R., Waterhouse, N.J., Browne, K.A., Sedelies, K., Ciccone A., Anthony, D., Koskinen, A., Mullbacher, A., and Trapani, J.A. (2007). Residual active granzyme B in cathepsin C-null lymphocytes is sufficient for perforin-dependent target cell apoptosis. J. Cell Biol. 176, 425-433.
69. Tang, C.H., Lee, J.W., Galvez, M.G., Robillard, L., Mole, S.E., and Chapman, H.A. (2006). Murine cathepsin F deficiency causes neuronal lipofuscinosis and late-onset neurological disease. Mol. Cell. Biol. 26, 2309-2316.
70. Teitelbaum, S.L. (2007). Osteoclasts: what do they do and how do they do it? Am. J. Pathol. 170, 427-435.
71. Thurmond, R.L., Sun, S., Karlsson, L., and Edwards, J.P. (2005). Cathepsin S inhibitors as novel immunomodulators. Curr. Opin. Invest. Drugs 6, 473-482.
72. Tolosa, E., Li, W., Yasuda, Y., Wienhold, W., Denzin, L.K., Lautwein, A., Driessen, C., Schnorrer, P., Weber, E., Stevanovic, S., et al. (2003). Cathepsin V is involved in the degradation of invariant chain in human thymus and is overexpressed in myasthenia gravis. J. Clin. Invest. 112, 517-526.
73. Trombetta, E.S., Ebersold, M., Garrett, W., Pypaert, M., and Mellman, I. (2003). Activation of lysosomal function during dendritic cell maturation. Science 299, 1400-1403.
74. Turk, B. (2006). Targeting proteases: successes, failures and future prospects. Nat. Rev. 5, 785-799.
75. Turk, B., Turk, D., and Turk, V. (2000). Lysosomal cysteine proteases: more than scavengers. Biochim. Biophys. Acta 1477, 98-111.
76. Turk, B., Stoka, V., Rozman-Pungerčar, J., Cirman, T., Droga-Mazovec, G., Orešić, K., and Turk, V. (2002a). Apoptotic pathways: involvement of lysosomal proteases. Biol. Chem. 383, 1035-1044.
77. Turk, B., Turk, D., and Salvesen, G. (2002b). Regulating cysteine protease activity: essential role of protease inhibitors as guardians and regulators. Curr. Pharm. Des. 8, 1623-1637.
78. Turk, D., Janjić, V., Štern, I., Podobnik, M., Lamba, D., Dahl., S.W., Lauritzen, C., Pedersen, J., Turk, V., and Turk, B. (2001a). Structure of human dipeptidyl peptidase I (cathepsin C): exclusion domain added to an endopeptidase framework creates the machine for activation of granular serine proteases. EMBO J. 20, 6570-6582.
79. Turk, V., Turk, B., and Turk, D. (2001b). Lysosomal cysteine proteases: facts and opportunities. EMBO J. 20, 4629-4633.
80. Twining, S.S. (1994). Regulation of proteolytic activity in tissues. Crit. Rev. Biochem. Mol. Biol. 29, 315-383.
81. Vasiljeva, O., Reinheckel, T., Peters, C., Turk, D., Turk, V., and Turk, B. (2007). Emerging roles of cysteine cathepsins in disease and their potential as drug targets. Curr. Pharm. Des. 13, 387-403.
82. Villadangos, J.A., Schnorrer, P., and Wilson, N.S. (2005). Control of MHC class II antigen presentation in dendritic cells: a balance between creative and destructive forces. Immunol. Rev. 207, 191-205.
83. Watari, M., Watari, H., DiSanto, M.E., Chacko, S., Shi, G.P., and Strauss, J.F. (1999). Pro-inflammatory cytokines induce expression of matrix-metabolizing enzymes in human cervical smooth muscle cells. Am. J. Pathol. 154, 1755-1762.
84. Watts, C. (2001). Antigen processing in the endocytic compartment. Curr. Opin. Immunol. 13, 26-31.
85. Wex, T., Bühling, F., Wex, H., Günther, D., Malfertheiner, P., Weber, E., and Brömme, D. (2001). Human cathepsin W, a cysteine protease predominantly expressed in NK cells, is mainly localized in the endoplasmic reticulum. J. Immunol. 167, 2172-2178.
86. Wex, T., Wex., H., Hartig, R., Wilhelmsen, S., and Malfertheiner, P. (2003). Functional involvement of cathepsin W in the cytotoxic activity of NK-92 cells. FEBS Lett. 552, 115-119.
87. Wolf, P.R. and Ploegh, H.L. (1995). How MHC class II molecules acquire peptide cargo: biosynthesis and trafficking through the endocytic pathway. Annu. Rev. Cell Dev. Biol. 11, 267-306.
88. Xing, R., Addington, A.K., and Mason, R.W. (1998). Quantification of cathepsins B and L in cells. Biochem. J. 332, 499-505.
89. Yasuda, Y., Kaleta, J., and Brömme, D. (2005). The role of cathepsins in osteoporosis and arthritis: rationale for the design of new therapeutics. Adv. Drug Deliv. Rev. 57, 973-993.
90. Zavašnik-Bergant, T. and Turk, B. (2006). Cysteine cathepsins in immune response. Tissue Antigens 67, 349-355.
91. Zavašnik-Bergant, T., Repnik, U., Schweiger, A., Romih, R., Jeras, M., Turk, V., and Kos, J. (2005). Differentiation- and maturation-dependent content, localization, and secretion of cystatin C in human dendritic cells. J. Leukoc. Biol. 78, 122-134.