Specific functions of lysosomal proteases in endocytic and autophagic pathways

Biochimica et Biophysica Acta - Proteins and Proteomics

Volumn 1824, Issue 1, 2012, Pages 34-43

  Müller, Sabrina ^a   Dennemärker, Julia ^a   Reinheckel, Thomas ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

Author keywords

Autophagy; Endocytosis; Phagocytosis; Protease; Protein turnover

Indexed keywords

AUTOANTIGEN; CARBOXYPEPTIDASE C; CATHEPSIN; CATHEPSIN D; CATHEPSIN L; CYTOKINE; GAMMA INTERFERON; GROWTH FACTOR; INTERLEUKIN 1BETA; LOW DENSITY LIPOPROTEIN; LOW DENSITY LIPOPROTEIN RECEPTOR; LYSOSOME ENZYME; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MYELIN BASIC PROTEIN; PROTEINASE; PROTEINASE INHIBITOR; TOLL LIKE RECEPTOR;

ANTIGEN PRESENTATION; ANTIGEN PRESENTING CELL; ATHEROSCLEROSIS; AUTOPHAGY; CARDIOMYOPATHY; DENDRITIC CELL; EBOLA VIRUS; ENDOCYTOSIS; ENZYME ACTIVITY; ENZYME DEFICIENCY; EPSTEIN BARR VIRUS; EXTRACELLULAR MATRIX; GOODPASTURE SYNDROME; HUMAN; IMMUNE RESPONSE; IMMUNOLOGICAL TOLERANCE; INFECTION; INFLAMMATION; KERATINOCYTE; LYSOSOME; MACROPHAGE; MAJOR HISTOCOMPATIBILITY COMPLEX; NEURONAL CEROID LIPOFUSCINOSIS; NONHUMAN; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; SKIN CANCER; VASCULAR SMOOTH MUSCLE; VESICULAR STOMATITIS VIRUS; VIRUS CELL INTERACTION;

ANIMALS; AUTOPHAGY; ENDOCYTOSIS; HOMEOSTASIS; HUMANS; LYSOSOMES; MODELS, BIOLOGICAL; PEPTIDE HYDROLASES; SIGNAL TRANSDUCTION;

EID: 82755160953     PISSN: 15709639     EISSN: 18781454     Source Type: Journal    
DOI: 10.1016/j.bbapap.2011.07.003     Document Type: Review

References (134)

1. C. De Duve, and R. Wattiaux Functions of lysosomes Annu. Rev. Physiol. 28 1966 435 492
2. R. Willstätter, and E. Bamann Über die Proteasen der Magenschleimhaut. Erste Abhandlung über die Enzyme der Leukozyten., Hoppe-Seyler's Z. Physiol. Chem. 180 1929 127 143
3. N.D. Rawlings, A.J. Barrett, and A. Bateman MEROPS: the peptidase database Nucleic Acids Res. 38 2010 D227 D233
4. B. Goulet, A. Baruch, N.S. Moon, M. Poirier, L.L. Sansregret, A. Erickson, M. Bogyo, and A. Nepveu A cathepsin L isoform that is devoid of a signal peptide localizes to the nucleus in S phase and processes the CDP/Cux transcription factor Mol. Cell 14 2004 207 219 (Pubitemid 38515648)
5. S. Sever, M.M. Altintas, S.R. Nankoe, C.C. Moller, D. Ko, C. Wei, J. Henderson, E.C. del Re, L. Hsing, A. Erickson, C.D. Cohen, M. Kretzler, D. Kerjaschki, A. Rudensky, B. Nikolic, and J. Reiser Proteolytic processing of dynamin by cytoplasmic cathepsin L is a mechanism for proteinuric kidney disease J. Clin. Invest. 117 2007 2095 2104 (Pubitemid 47219554)
6. E.M. Duncan, T.L. Muratore-Schroeder, R.G. Cook, B.A. Garcia, J. Shabanowitz, D.F. Hunt, and C.D. Allis Cathepsin L proteolytically processes histone H3 during mouse embryonic stem cell differentiation Cell 135 2008 284 294
7. J. Reiser, B. Adair, and T. Reinheckel Specialized roles for cysteine cathepsins in health and disease J. Clin. Invest. 120 2010 3421 3431
8. K. Muntener, R. Zwicky, G. Csucs, J. Rohrer, and A. Baici Exon skipping of cathepsin B: mitochondrial targeting of a lysosomal peptidase provokes cell death J. Biol. Chem. 279 2004 41012 41017 (Pubitemid 39287702)
9. M.M. Mohamed, and B.F. Sloane Cysteine cathepsins: multifunctional enzymes in cancer Nat. Rev. Cancer 6 2006 764 775 (Pubitemid 44450465)
10. M. Sameni, J. Dosescu, K. Moin, and B.F. Sloane Functional imaging of proteolysis: stromal and inflammatory cells increase tumor proteolysis Mol. Imaging 2 2003 159 175
11. V. Gocheva, and J.A. Joyce Cysteine cathepsins and the cutting edge of cancer invasion Cell Cycle 6 2007 60 64 (Pubitemid 46173882)
12. V. Gocheva, H.W. Wang, B.B. Gadea, T. Shree, K.E. Hunter, A.L. Garfall, T. Berman, and J.A. Joyce IL-4 induces cathepsin protease activity in tumor-associated macrophages to promote cancer growth and invasion Genes Dev. 24 2010 241 255
13. J.S. Mort, A.D. Recklies, and A.R. Poole Extracellular presence of the lysosomal proteinase cathepsin B in rheumatoid synovium and its activity at neutral pH Arthritis Rheum. 27 1984 509 515 (Pubitemid 14140024)
14. D. Caglic, A. Globisch, M. Kindermann, N.H. Lim, V. Jeske, H.P. Juretschke, E. Bartnik, K.U. Weithmann, H. Nagase, B. Turk, and K.U. Wendt Functional in vivo imaging of cysteine cathepsin activity in murine model of inflammation Bioorg. Med. Chem. 19 2011 1055 1061
15. U. Pozgan, D. Caglic, B. Rozman, H. Nagase, V. Turk, and B. Turk Expression and activity profiling of selected cysteine cathepsins and matrix metalloproteinases in synovial fluids from patients with rheumatoid arthritis and osteoarthritis Biol. Chem. 391 2010 571 579
16. A.M. Lechner, I. Assfalg-Machleidt, S. Zahler, M. Stoeckelhuber, W. Machleidt, M. Jochum, and D.K. Nagler RGD-dependent binding of procathepsin X to integrin alphavbeta3 mediates cell-adhesive properties J. Biol. Chem. 281 2006 39588 39597 (Pubitemid 46041918)
17. L. Sevenich, F. Werner, M. Gajda, U. Schurigt, C. Sieber, S. Muller, M. Follo, C. Peters, and T. Reinheckel Transgenic expression of human cathepsin B promotes progression and metastasis of polyoma-middle-T-induced breast cancer in mice Oncogene 30 2011 54 64
18. L. Sevenich, U. Schurigt, K. Sachse, M. Gajda, F. Werner, S. Muller, O. Vasiljeva, A. Schwinde, N. Klemm, J. Deussing, C. Peters, and T. Reinheckel Synergistic antitumor effects of combined cathepsin B and cathepsin Z deficiencies on breast cancer progression and metastasis in mice Proc. Natl. Acad. Sci. U. S. A. 107 2010 2497 2502
19. P. Saftig, and J. Klumperman Lysosome biogenesis and lysosomal membrane proteins: trafficking meets function Nat. Rev. Mol. Cell Biol. 10 2009 623 635
20. I. Mellman Endocytosis and molecular sorting Annu. Rev. Cell Dev. Biol. 12 1996 575 625 (Pubitemid 26422725)
21. S. Mukherjee, R.N. Ghosh, and F.R. Maxfield Endocytosis Physiol. Rev. 77 1997 759 803 (Pubitemid 27328740)
22. W. Stoorvogel, G.J. Strous, H.J. Geuze, V. Oorschot, and A.L. Schwartz Late endosomes derive from early endosomes by maturation Cell 65 1991 417 427 (Pubitemid 121002051)
23. M. von Zastrow, and A. Sorkin Signaling on the endocytic pathway Curr. Opin. Cell Biol. 19 2007 436 445 (Pubitemid 47287673)
24. F. Authier, M. Metioui, A.W. Bell, and J.S. Mort Negative regulation of epidermal growth factor signaling by selective proteolytic mechanisms in the endosome mediated by cathepsin B J. Biol. Chem. 274 1999 33723 33731 (Pubitemid 129511688)
25. R. Navab, E. Chevet, F. Authier, G.M. Di Guglielmo, J.J. Bergeron, and P. Brodt Inhibition of endosomal insulin-like growth factor-I processing by cysteine proteinase inhibitors blocks receptor-mediated functions J. Biol. Chem. 276 2001 13644 13649
26. R. Navab, J.S. Mort, and P. Brodt Inhibition of carcinoma cell invasion and liver metastases formation by the cysteine proteinase inhibitor E-64 Clin. Exp. Metastasis 15 1997 121 129 (Pubitemid 27157814)
27. F. Authier, M. Kouach, and G. Briand Endosomal proteolysis of insulin-like growth factor-I at its C-terminal D-domain by cathepsin B FEBS Lett. 579 2005 4309 4316 (Pubitemid 41116357)
28. F. Authier, M. Metioui, S. Fabrega, M. Kouach, and G. Briand Endosomal proteolysis of internalized insulin at the C-terminal region of the B chain by cathepsin D J. Biol. Chem. 277 2002 9437 9446 (Pubitemid 34953030)
29. O. Zwad, B. Kubler, W. Roth, J.G. Scharf, P. Saftig, C. Peters, and T. Braulke Decreased intracellular degradation of insulin-like growth factor binding protein-3 in cathepsin L-deficient fibroblasts FEBS Lett. 510 2002 211 215 (Pubitemid 34093827)
30. T. Reinheckel, S. Hagemann, S. Dollwet-Mack, E. Martinez, T. Lohmuller, G. Zlatkovic, D.J. Tobin, N. Maas-Szabowski, and C. Peters The lysosomal cysteine protease cathepsin L regulates keratinocyte proliferation by control of growth factor recycling J. Cell Sci. 118 2005 3387 3395 (Pubitemid 41246094)
31. J. Dennemarker, T. Lohmuller, J. Mayerle, M. Tacke, M.M. Lerch, L.M. Coussens, C. Peters, and T. Reinheckel Deficiency for the cysteine protease cathepsin L promotes tumor progression in mouse epidermis Oncogene 29 2010 1611 1621
32. S. Schubbert, K. Shannon, and G. Bollag Hyperactive Ras in developmental disorders and cancer Nat. Rev. Cancer 7 2007 295 308 (Pubitemid 46480970)
33. W. Roth, J. Deussing, V.A. Botchkarev, M. Pauly-Evers, P. Saftig, A. Hafner, P. Schmidt, W. Schmahl, J. Scherer, I. Anton-Lamprecht, K. Von Figura, R. Paus, and C. Peters Cathepsin L deficiency as molecular defect of furless: hyperproliferation of keratinocytes and pertubation of hair follicle cycling FASEB J. 14 2000 2075 2086
34. D.J. Tobin, K. Foitzik, T. Reinheckel, L. Mecklenburg, V.A. Botchkarev, C. Peters, and R. Paus The lysosomal protease cathepsin L is an important regulator of keratinocyte and melanocyte differentiation during hair follicle morphogenesis and cycling Am. J. Pathol. 160 2002 1807 1821 (Pubitemid 34525660)
35. J.L. Goldstein, M.S. Brown, R.G. Anderson, D.W. Russell, and W.J. Schneider Receptor-mediated endocytosis: concepts emerging from the LDL receptor system Annu. Rev. Cell Biol. 1 1985 1 39
36. H.H. Hobbs, M.S. Brown, and J.L. Goldstein Molecular genetics of the LDL receptor gene in familial hypercholesterolemia Hum. Mutat. 1 1992 445 466
37. A. Tybjaerg-Hansen, and S.E. Humphries Familial defective apolipoprotein B-100: a single mutation that causes hypercholesterolemia and premature coronary artery disease Atherosclerosis 96 1992 91 107
38. S.M. Rankin, M.E. Knowles, and D.S. Leake Macrophages possess both neutral and acidic protease activities toward low density lipoproteins Atherosclerosis 79 1989 71 78 (Pubitemid 19219631)
39. B.J. Van Lenten, and A.M. Fogelman Processing of lipoproteins in human monocyte-macrophages J. Lipid Res. 31 1990 1455 1466 (Pubitemid 20261909)
40. D.I. Simon, H. Xu, and D.E. Vaughan Cathepsin D-like aspartyl protease activity mediates the degradation of tissue-type plasminogen activator/plasminogen activator inhibitor-1 complexes in human monocytes Biochim. Biophys. Acta 1268 1995 143 151
41. G.K. Sukhova, G.P. Shi, D.I. Simon, H.A. Chapman, and P. Libby Expression of the elastolytic cathepsins S and K in human atheroma and regulation of their production in smooth muscle cells J. Clin. Invest. 102 1998 576 583 (Pubitemid 28376160)
42. G.K. Sukhova, Y. Zhang, J.H. Pan, Y. Wada, T. Yamamoto, M. Naito, T. Kodama, S. Tsimikas, J.L. Witztum, M.L. Lu, Y. Sakara, M.T. Chin, P. Libby, and G.P. Shi Deficiency of cathepsin S reduces atherosclerosis in LDL receptor-deficient mice J. Clin. Invest. 111 2003 897 906 (Pubitemid 37074965)
43. P. Duewell, H. Kono, K.J. Rayner, C.M. Sirois, G. Vladimer, F.G. Bauernfeind, G.S. Abela, L. Franchi, G. Nunez, M. Schnurr, T. Espevik, E. Lien, K.A. Fitzgerald, K.L. Rock, K.J. Moore, S.D. Wright, V. Hornung, and E. Latz NLRP3 inflammasomes are required for atherogenesis and activated by cholesterol crystals Nature 464 2010 1357 1361
44. J. Banchereau, and R.M. Steinman Dendritic cells and the control of immunity Nature 392 1998 245 252 (Pubitemid 28155090)
45. A. Savina, C. Jancic, S. Hugues, P. Guermonprez, P. Vargas, I.C. Moura, A.M. Lennon-Dumenil, M.C. Seabra, G. Raposo, and S. Amigorena NOX2 controls phagosomal pH to regulate antigen processing during crosspresentation by dendritic cells Cell 126 2006 205 218 (Pubitemid 44026552)
46. L. Delamarre, R. Couture, I. Mellman, and E.S. Trombetta Enhancing immunogenicity by limiting susceptibility to lysosomal proteolysis J. Exp. Med. 203 2006 2049 2055 (Pubitemid 44352226)
47. B. Manoury, D. Mazzeo, L. Fugger, N. Viner, M. Ponsford, H. Streeter, G. Mazza, D.C. Wraith, and C. Watts Destructive processing by asparagine endopeptidase limits presentation of a dominant T cell epitope in MBP Nat. Immunol. 3 2002 169 174 (Pubitemid 34141447)
48. C.M. Costantino, H.C. Hang, S.C. Kent, D.A. Hafler, and H.L. Ploegh Lysosomal cysteine and aspartic proteases are heterogeneously expressed and act redundantly to initiate human invariant chain degradation J. Immunol. 180 2008 2876 2885
49. T. Burster, A. Beck, E. Tolosa, V. Marin-Esteban, O. Rotzschke, K. Falk, A. Lautwein, M. Reich, J. Brandenburg, G. Schwarz, H. Wiendl, A. Melms, R. Lehmann, S. Stevanovic, H. Kalbacher, and C. Driessen Cathepsin G, and not the asparagine-specific endoprotease, controls the processing of myelin basic protein in lysosomes from human B lymphocytes J. Immunol. 172 2004 5495 5503 (Pubitemid 38542050)
50. B. Manoury, E.W. Hewitt, N. Morrice, P.M. Dando, A.J. Barrett, and C. Watts An asparaginyl endopeptidase processes a microbial antigen for class II MHC presentation Nature 396 1998 695 699 (Pubitemid 29003950)
51. A.N. Antoniou, S.L. Blackwood, D. Mazzeo, and C. Watts Control of antigen presentation by a single protease cleavage site Immunity 12 2000 391 398
52. S.P. Matthews, I. Werber, J. Deussing, C. Peters, T. Reinheckel, and C. Watts Distinct protease requirements for antigen presentation in vitro and in vivo J. Immunol. 184 2010 2423 2431
53. M. Reich, P.F. van Swieten, V. Sommandas, M. Kraus, R. Fischer, E. Weber, H. Kalbacher, H.S. Overkleeft, and C. Driessen 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 2007 990 1001 (Pubitemid 46495648)
54. A.M. Lennon-Dumenil, A.H. Bakker, R. Maehr, E. Fiebiger, H.S. Overkleeft, M. Rosemblatt, H.L. Ploegh, and C. Lagaudriere-Gesbert Analysis of protease activity in live antigen-presenting cells shows regulation of the phagosomal proteolytic contents during dendritic cell activation J. Exp. Med. 196 2002 529 540
55. E.B.E. Pluger, M. Boes, C. Alfonso, C.J. Schroter, H. Kalbacher, H.L. Ploegh, and C. Driessen Specific role for cathepsin S in the generation of antigenic peptides in vivo Eur. J. Immunol. 32 2002 467 476 (Pubitemid 34173338)
56. C.M. Costantino, H.C. Hang, S.C. Kent, D.A. Hafler, and H.L. Ploegh Lysosomal cysteine and aspartic proteases are heterogeneously expressed and act redundantly to initiate human invariant chain degradation J. Immunol. 180 2008 2876 2885
57. M. Reich, P.F. van Swieten, V. Sommandas, M. Kraus, R. Fischer, E. Weber, H. Kalbacher, H.S. Overkleeft, and C. Driessen 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 2007 990 1001 (Pubitemid 46495648)
58. J. Deussing, W. Roth, P. Saftig, C. Peters, H.L. Ploegh, and J.A. Villadangos Cathepsins B and D are dispensable for major histocompatibility complex class II-mediated antigen presentation Proc. Natl. Acad. Sci. U. S. A. 95 1998 4516 4521 (Pubitemid 28207944)
59. C. Tulone, Y. Uchiyama, M. Novelli, N. Grosvenor, P. Saftig, and B.M. Chain Haematopoietic development and immunological function in the absence of cathepsin D BMC Immunol. 8 2007 22 10.1186/1471-2172-8-22 (Pubitemid 350048272)
60. C.X. Moss, J.A. Villadangos, and C. Watts Destructive potential of the aspartyl protease cathepsin D in MHC class II-restricted antigen processing Eur. J. Immunol. 35 2005 3442 3451 (Pubitemid 43025525)
61. J. Zou, L. Henderson, V. Thomas, P. Swan, A.N. Turner, and R.G. Phelps Presentation of the Goodpasture autoantigen requires proteolytic unlocking steps that destroy prominent T cell epitopes J. Am. Soc. Nephrol. 18 2007 771 779 (Pubitemid 46434494)
62. A. Rodriguez, A. Regnault, M. Kleijmeer, P. Ricciardi-Castagnoli, and S. Amigorena Selective transport of internalized antigens to the cytosol for MHC class I presentation in dendritic cells Nat. Cell Biol. 1 1999 362 368 (Pubitemid 129493579)
63. H.A. Chapman Endosomal proteases in antigen presentation Curr. Opin. Immunol. 18 2006 78 84 (Pubitemid 43049652)
64. N. Tiwari, N. Garbi, T. Reinheckel, G. Moldenhauer, G.J. Hammerling, and F. Momburg A transporter associated with antigen-processing independent vacuolar pathway for the MHC class I-mediated presentation of endogenous transmembrane proteins J. Immunol. 178 2007 7932 7942 (Pubitemid 46898065)
65. L. Shen, L.J. Sigal, M. Boes, and K.L. Rock Important role of cathepsin S in generating peptides for TAP-independent MHC class I crosspresentation in vivo Immunity 21 2004 155 165 (Pubitemid 39094046)
66. R. Song, and C.V. Harding Roles of proteasomes, transporter for antigen presentation (TAP), and beta(2)-microglobulin in the processing of bacterial or particulate antigens via an alternate class I MHC processing pathway J. Immunol. 156 1996 4182 4190
67. R. Belizaire, and E.R. Unanue Targeting proteins to distinct subcellular compartments reveals unique requirements for MHC class I and II presentation Proc. Natl. Acad. Sci. U. S. A. 106 2009 17463 17468
68. H.A. Chapman, R.J. Riese, and G.P. Shi Emerging roles for cysteine proteases in human biology Annu. Rev. Physiol. 59 1997 63 88 (Pubitemid 27142435)
69. P.E. Jensen Recent advances in antigen processing and presentation Nat. Immunol. 8 2007 1041 1048 (Pubitemid 47423752)
70. K. Honey, and A.Y. Rudensky Lysosomal cysteine proteases regulate antigen presentation Nat. Rev. Immunol. 3 2003 472 482 (Pubitemid 37339187)
71. B. Manoury, D. Mazzeo, D.N. Li, J. Billson, K. Loak, P. Benaroch, and C. Watts Asparagine endopeptidase can initiate the removal of the MHC class II invariant chain chaperone Immunity 18 2003 489 498 (Pubitemid 36513631)
72. M.A. Maric, M.D. Taylor, and J.S. Blum Endosomal aspartic proteinases are required for invariant-chain processing Proc. Natl. Acad. Sci. U. S. A. 91 1994 2171 2175 (Pubitemid 24092065)
73. T.Q. Zhang, Y. Maekawa, K. Yasutomo, H. Ishikawa, B.F. Nashed, T. Dainichi, H. Hisaeda, T. Sakai, M. Kasai, T. Mizuochi, T. Asao, N. Katunuma, and K. Himeno Pepstatin A-sensitive aspartic proteases in lysosome are involved in degradation of the invariant chain and antigen-processing in antigen presenting cells of mice infected with Leishmania major Biochem. Biophys. Res. Commun. 276 2000 693 701
74. J.C. Kwan, E.A. Eksioglu, C. Liu, V.J. Paul, and H. Luesch Grassystatins A-C from marine cyanobacteria, potent cathepsin E inhibitors that reduce antigen presentation J. Med. Chem. 52 2009 5732 5747
75. R.J. Riese, P.R. Wolf, D. Bromme, L.R. Natkin, J.A. Villadangos, H.L. Ploegh, and H.A. Chapman Essential role for cathepsin S in MHC class II - associated invariant chain processing and peptide loading Immunity 4 1996 357 366 (Pubitemid 26174051)
76. G.P. Shi, A.C. Webb, K.E. Foster, J.H.M. Knoll, C.A. Lemere, J.S. Munger, and H.A. Chapman Human cathepsin-S - chromosomal localization, gene structure, and tissue distribution J. Biol. Chem. 269 1994 11530 11536 (Pubitemid 24200373)
77. T.Y. Nakagawa, W.H. Brissette, P.D. Lira, R.J. Griffiths, N. Petrushova, J. Stock, J.D. McNeish, S.E. Eastman, E.D. Howard, S.R. Clarke, E.F. Rosloniec, E.A. Elliott, and A.Y. Rudensky Impaired invariant chain degradation and antigen presentation and diminished collagen-induced arthritis in cathepsin S null mice Immunity 10 1999 207 217 (Pubitemid 29115626)
78. T. Nakagawa, W. Roth, P. Wong, A. Nelson, A. Farr, J. Deussing, J.A. Villadangos, H. Ploegh, C. Peters, and A.Y. Rudensky Cathepsin L: critical role in Ii degradation and CD4 T cell selection in the thymus Science 280 1998 450 453 (Pubitemid 28208170)
79. J.D. Colbert, S.P. Matthews, G. Miller, and C. Watts Diverse regulatory roles for lysosomal proteases in the immune response Eur. J. Immunol. 39 2009 2955 2965
80. L.C. Hsing, and A.Y. Rudensky The lysosomal cysteine proteases in MHC class II antigen presentation Immunol. Rev. 207 2005 229 241 (Pubitemid 41415021)
81. L. Sevenich, S. Hagemann, C. Stoeckle, E. Tolosa, C. Peters, and T. Reinheckel Expression of human cathepsin L or human cathepsin V in mouse thymus mediates positive selection of T helper cells in cathepsin L knock-out mice Biochimie 92 2010 1674 1680
82. E. Tolosa, W. Li, Y. Yasuda, W. Wienhold, L.K. Denzin, A. Lautwein, C. Driessen, P. Schnorrer, E. Weber, S. Stevanovic, R. Kurek, A. Melms, and D. Bromme Cathepsin V is involved in the degradation of invariant chain in human thymus and is overexpressed in myasthenia gravis J. Clin. Invest. 112 2003 517 526 (Pubitemid 38056336)
83. T. Bevec, V. Stoka, G. Pungercic, I. Dolenc, and V. Turk Major histocompatibility complex class II-associated p41 invariant chain fragment is a strong inhibitor of lysosomal cathepsin L J. Exp. Med. 183 1996 1331 1338 (Pubitemid 26134276)
84. A.M. Lennon-Dumenil, R.A. Roberts, K. Valentijn, C. Driessen, H.S. Overkleeft, A. Erickson, P.J. Peters, E. Bikoff, H.L. Ploegh, and P. Wolf Bryant The p41 isoform of invariant chain is a chaperone for cathepsin L EMBO J. 20 2001 4055 4064 (Pubitemid 32751822)
85. E. Fiebiger, R. Maehr, J. Villadangos, E. Weber, A. Erickson, E. Bikoff, H.L. Ploegh, and A.M. Lennon-Dumenil Invariant chain controls the activity of extracellular cathepsin L J. Exp. Med. 196 2002 1263 1269 (Pubitemid 35304191)
86. M. Mihelic, A. Dobersek, G. Guncar, and D. Turk Inhibitory fragment from the p41 form of invariant chain can regulate activity of cysteine cathepsins in antigen presentation J. Biol. Chem. 283 2008 14453 14460
87. L. Alexopoulou, A.C. Holt, R. Medzhitov, and R.A. Flavell Recognition of double-stranded RNA and activation of NF-kappa B by Toll-like receptor 3 Nature 413 2001 732 738 (Pubitemid 33009951)
88. F. Heil, H. Hemmi, H. Hochrein, F. Ampenberger, C. Kirschning, S. Akira, G. Lipford, H. Wagner, and S. Bauer Species-specific recognition of single-stranded RNA via toll-like receptor 7 and 8 Science 303 2004 1526 1529 (Pubitemid 38314424)
89. H. Hemmi, O. Takeuchi, T. Kawai, T. Kaisho, S. Sato, H. Sanjo, M. Matsumoto, K. Hoshino, H. Wagner, K. Takeda, and S. Akira A Toll-like receptor recognizes bacterial DNA Nature 408 2000 740 745 (Pubitemid 32015992)
90. A.L. Blasius, and B. Beutler Intracellular Toll-like receptors Immunity 32 2010 305 315
91. K. Yasuda, M. Rutz, B. Schlatter, J. Metzger, P.B. Luppa, F. Schmitz, T. Haas, A. Heit, S. Bauer, and H. Wagner CpG motif-independent activation of TLR9 upon endosomal translocation of "natural" phosphodiester DNA Eur. J. Immunol. 36 2006 431 436 (Pubitemid 43257466)
92. H. Hacker, H. Mischak, T. Miethke, S. Liptay, R. Schmid, T. Sparwasser, K. Heeg, G.B. Lipford, and H. Wagner CpG-DNA-specific activation of antigen-presenting cells requires stress kinase activity and is preceded by non-specific endocytosis and endosomal maturation EMBO J. 17 1998 6230 6240 (Pubitemid 28497796)
93. S.E. Ewald, B.L. Lee, L. Lau, K.E. Wickliffe, G.P. Shi, H.A. Chapman, and G.M. Barton The ectodomain of Toll-like receptor 9 is cleaved to generate a functional receptor Nature 456 2008 658 662
94. B. Park, M.M. Brinkmann, E. Spooner, C.C. Lee, Y.M. Kim, and H.L. Ploegh Proteolytic cleavage in an endolysosomal compartment is required for activation of Toll-like receptor 9 Nat. Immunol. 9 2008 1407 1414
95. M. Asagiri, T. Hirai, T. Kunigami, S. Kamano, H.J. Gober, K. Okamoto, K. Nishikawa, E. Latz, D.T. Golenbock, K. Aoki, K. Ohya, Y. Imai, Y. Morishita, K. Miyazono, S. Kato, P. Saftig, and H. Takayanagi Cathepsin K-dependent Toll-like receptor 9 signaling revealed in experimental arthritis Science 319 2008 624 627 (Pubitemid 351197065)
96. F.E. Sepulveda, S. Maschalidi, R. Colisson, L. Heslop, C. Ghirelli, E. Sakka, A.M. Lennon-Dumenil, S. Amigorena, L. Cabanie, and B. Manoury Critical role for asparagine endopeptidase in endocytic Toll-like receptor signaling in dendritic cells Immunity 31 2009 737 748
97. K. Chandran, N.J. Sullivan, U. Felbor, S.P. Whelan, and J.M. Cunningham Endosomal proteolysis of the Ebola virus glycoprotein is necessary for infection Science 308 2005 1643 1645 (Pubitemid 40807517)
98. K. Schornberg, S. Matsuyama, K. Kabsch, S. Delos, A. Bouton, and J. White Role of endosomal cathepsins in entry mediated by the Ebola virus glycoprotein J. Virol. 80 2006 4174 4178
99. D.H. Ebert, J. Deussing, C. Peters, and T.S. Dermody Cathepsin L and cathepsin B mediate reovirus disassembly in murine fibroblast cells J. Biol. Chem. 277 2002 24609 24617 (Pubitemid 34951989)
100. I.C. Huang, B.J. Bosch, F. Li, W.H. Li, K.H. Lee, S. Ghiran, N. Vasilieva, T.S. Dermody, S.C. Harrison, P.R. Dormitzer, M. Farzan, P.J.M. Rottier, and H. Choe SARS coronavirus, but not human coronavirus NL63, utilizes cathepsin L to infect ACE2-expressing cells J. Biol. Chem. 281 2006 3198 3203 (Pubitemid 43845930)
101. G. Simmons, D.N. Gosalia, A.J. Rennekamp, J.D. Reeves, S.L. Diamond, and P. Bates Inhibitors of cathepsin L prevent severe acute respiratory syndrome coronavirus entry Proc. Natl. Acad. Sci. U. S. A. 102 2005 11876 11881 (Pubitemid 41170818)
102. E.J. Parkinson-Lawrence, T. Shandala, M. Prodoehl, R. Plew, G.N. Borlace, and D.A. Brooks Lysosomal storage disease: revealing lysosomal function and physiology Physiology 25 2010 102 115
103. B. Levine, and D.J. Klionsky Development by self-digestion: molecular mechanisms and biological functions of autophagy Dev. Cell 6 2004 463 477 (Pubitemid 38456176)
104. D.J. Klionsky, A.M. Cuervo, W.A. Dunn Jr., B. Levine, I. van der Klei, and P.O. Seglen How shall I eat thee? Autophagy 3 2007 413 416 (Pubitemid 47293721)
105. B. Turk, and V. Turk Lysosomes as "suicide bags" in cell death: myth or reality? J. Biol. Chem. 284 2009 21783 21787
106. A.M. Cuervo, L. Mann, E.J. Bonten, A. d'Azzo, and J.F. Dice Cathepsin A regulates chaperone-mediated autophagy through cleavage of the lysosomal receptor EMBO J. 22 2003 47 59 (Pubitemid 36091268)
107. A.M. Cuervo, and J.F. Dice A receptor for the selective uptake and degradation of proteins by lysosomes Science 273 1996 501 503 (Pubitemid 26286451)
108. D.S. Konecki, K. Foetisch, K.P. Zimmer, M. Schlotter, and U. Lichter-Konecki An alternatively spliced form of the human lysosome-associated membrane protein-2 gene is expressed in a tissue-specific manner Biochem. Biophys. Res. Commun. 215 1995 757 767
109. U. Bandyopadhyay, S. Kaushik, L. Varticovski, and A.M. Cuervo The chaperone-mediated autophagy receptor organizes in dynamic protein complexes at the lysosomal membrane Mol. Cell. Biol. 28 2008 5747 5763
110. A.M. Cuervo, and J.F. Dice Regulation of lamp2a levels in the lysosomal membrane Traffic 1 2000 570 583
111. S.J. Orenstein, and A.M. Cuervo Chaperone-mediated autophagy: molecular mechanisms and physiological relevance Semin. Cell Dev. Biol. 21 2010 719 726
112. J. Tyynela, I. Sohar, D.E. Sleat, R.M. Gin, R.J. Donnelly, M. Baumann, M. Haltia, and P. Lobel A mutation in the ovine cathepsin D gene causes a congenital lysosomal storage disease with profound neurodegeneration EMBO J. 19 2000 2786 2792 (Pubitemid 30386751)
113. E. Siintola, S. Partanen, P. Stromme, A. Haapanen, M. Haltia, J. Maehlen, A.E. Lehesjoki, and J. Tyynela Cathepsin D deficiency underlies congenital human neuronal ceroid-lipofuscinosis Brain 129 2006 1438 1445 (Pubitemid 43999376)
114. R. Steinfeld, K. Reinhardt, K. Schreiber, M. Hillebrand, R. Kraetzner, W. Bruck, P. Saftig, and J. Gartner Cathepsin D deficiency is associated with a human neurodegenerative disorder Am. J. Hum. Genet. 78 2006 988 998 (Pubitemid 43787690)
115. M. Koike, H. Nakanishi, P. Saftig, J. Ezaki, K. Isahara, Y. Ohsawa, W. Schulz-Schaeffer, T. Watanabe, S. Waguri, S. Kametaka, M. Shibata, K. Yamamoto, E. Kominami, C. Peters, K. von Figura, and Y. Uchiyama Cathepsin D deficiency induces lysosomal storage with ceroid lipofuscin in mouse CNS neurons J. Neurosci. 20 2000 6898 6906
116. M. Koike, M. Shibata, Y. Ohsawa, H. Nakanishi, T. Koga, S. Kametaka, S. Waguri, T. Momoi, E. Kominami, C. Peters, K. Figura, P. Saftig, and Y. Uchiyama Involvement of two different cell death pathways in retinal atrophy of cathepsin D-deficient mice Mol. Cell. Neurosci. 22 2003 146 161 (Pubitemid 36379180)
117. M. Koike, M. Shibata, S. Waguri, K. Yoshimura, I. Tanida, E. Kominami, T. Gotow, C. Peters, K. von Figura, N. Mizushima, P. Saftig, and Y. Uchiyama Participation of autophagy in storage of lysosomes in neurons from mouse models of neuronal ceroid-lipofuscinoses (Batten disease) Am. J. Pathol. 167 2005 1713 1728 (Pubitemid 41713322)
118. P. Saftig, M. Hetman, W. Schmahl, K. Weber, L. Heine, H. Mossmann, A. Koster, B. Hess, M. Evers, and K. von Figura Mice deficient for the lysosomal proteinase cathepsin D exhibit progressive atrophy of the intestinal mucosa and profound destruction of lymphoid cells EMBO J. 14 1995 3599 3608
119. J.J. Shacka, B.J. Klocke, C. Young, M. Shibata, J.W. Olney, Y. Uchiyama, P. Saftig, and K.A. Roth Cathepsin D deficiency induces persistent neurodegeneration in the absence of Bax-dependent apoptosis J. Neurosci. 27 2007 2081 2090
120. U. Felbor, B. Kessler, W. Mothes, H.H. Goebel, H.L. Ploegh, R.T. Bronson, and B.R. Olsen Neuronal loss and brain atrophy in mice lacking cathepsins B and L Proc. Natl. Acad. Sci. U. S. A. 99 2002 7883 7888 (Pubitemid 34650974)
121. L. Sevenich, L.A. Pennacchio, C. Peters, and T. Reinheckel Human cathepsin L rescues the neurodegeneration and lethality in cathepsin B/L double-deficient mice Biol. Chem. 387 2006 885 891 (Pubitemid 44100235)
122. T. Reinheckel, J. Deussing, W. Roth, and C. Peters Towards specific functions of lysosomal cysteine peptidases: phenotypes of mice deficient for cathepsin B or cathepsin L Biol. Chem. 382 2001 735 741 (Pubitemid 32631710)
123. O. Vasiljeva, T. Reinheckel, C. Peters, D. Turk, V. Turk, and B. Turk Emerging roles of cysteine cathepsins in disease and their potential as drug targets Curr. Pharm. Des. 13 2007 387 403 (Pubitemid 46477760)
124. B. Friedrichs, C. Tepel, T. Reinheckel, J. Deussing, K. von Figura, V. Herzog, C. Peters, P. Saftig, and K. Brix Thyroid functions of mouse cathepsins B, K, and L J. Clin. Invest. 111 2003 1733 1745 (Pubitemid 38057754)
125. J. Stypmann, K. Glaser, W. Roth, D.J. Tobin, I. Petermann, R. Matthias, G. Monnig, W. Haverkamp, G. Breithardt, W. Schmahl, C. Peters, and T. Reinheckel Dilated cardiomyopathy in mice deficient for the lysosomal cysteine peptidase cathepsin L Proc. Natl. Acad. Sci. U. S. A. 99 2002 6234 6239 (Pubitemid 34493295)
126. D. Spira, J. Stypmann, D.J. Tobin, I. Petermann, C. Mayer, S. Hagemann, O. Vasiljeva, T. Gunther, R. Schule, C. Peters, and T. Reinheckel Cell type-specific functions of the lysosomal protease cathepsin L in the heart J. Biol. Chem. 282 2007 37045 37052
127. I. Petermann, C. Mayer, J. Stypmann, M.L. Biniossek, D.J. Tobin, M.A. Engelen, T. Dandekar, T. Grune, L. Schild, C. Peters, and T. Reinheckel Lysosomal, cytoskeletal, and metabolic alterations in cardiomyopathy of cathepsin L knockout mice FASEB J. 20 2006 1266 1268
128. J. Dennemarker, T. Lohmuller, S. Muller, S.V. Aguilar, D.J. Tobin, C. Peters, and T. Reinheckel Impaired turnover of autophagolysosomes in cathepsin L deficiency Biol. Chem. 391 2010 913 922
129. A. Wille, A. Gerber, A. Heimburg, A. Reisenauer, C. Peters, P. Saftig, T. Reinheckel, T. Welte, and F. Buhling Cathepsin L is involved in cathepsin D processing and regulation of apoptosis in A549 human lung epithelial cells Biol. Chem. 385 2004 665 670 (Pubitemid 39144949)
130. G. Blum, G. von Degenfeld, M.J. Merchant, H.M. Blau, and M. Bogyo Noninvasive optical imaging of cysteine protease activity using fluorescently quenched activity-based probes Nat. Chem. Biol. 3 2007 668 677 (Pubitemid 47417706)
131. G. Blum, R.M. Weimer, L.E. Edgington, W. Adams, and M. Bogyo Comparative assessment of substrates and activity based probes as tools for non-invasive optical imaging of cysteine protease activity PLoS ONE 4 2009 e6374
132. O. Kleifeld, A. Doucet, U. auf dem Keller, A. Prudova, O. Schilling, R.K. Kainthan, A.E. Starr, L.J. Foster, J.N. Kizhakkedathu, and C.M. Overall Isotopic labeling of terminal amines in complex samples identifies protein N-termini and protease cleavage products Nat. Biotechnol. 28 2010 281 288
133. O. Schilling, O. Barre, P.F. Huesgen, and C.M. Overall Proteome-wide analysis of protein carboxy termini: C terminomics Nat. Methods 7 2010 508 511
134. P. Van Damme, J. Van Damme, H. Demol, A. Staes, J. Vandekerckhove, and K. Gevaert A review of COFRADIC techniques targeting protein N-terminal acetylation BMC Proc. 3 Suppl 6 2009 S6