Lysosomes in programmed cell death pathways: from initiators to amplifiers

Biological Chemistry

Volumn 398, Issue 3, 2017, Pages 289-301

  Kavčič, Nežka ^a   Pegan, Katarina ^a   Turk, Boris ^a,b,c  

^a JO EF STEFAN INSTITUTE   (Slovenia)

^b Center of Excellence CIPKEBIP   (Slovenia)

^c UNIVERSITY OF LJUBLJANA   (Slovenia)

Author keywords

Apoptosis; Cathepsin; Lysosome; Programmed cell death; Programmed necrosis

Indexed keywords

HYDROLASE; PROTEIN; PROTEINASE; REACTIVE OXYGEN METABOLITE; REAGENT;

APOPTOSIS; CELL DEATH; CELL MEMBRANE PERMEABILITY; CORNIFICATION; CYTOLOGY; FERROPTOSIS; HUMAN; LYSOSOME; LYSOSOME MEMBRANE; NECROPTOSIS; NONHUMAN; OXYTOSIS; PRIORITY JOURNAL; PYROPTOSIS; REVIEW;

EID: 85013290735     PISSN: 14316730     EISSN: 14374315     Source Type: Journal    
DOI: 10.1515/hsz-2016-0252     Document Type: Review

References (119)

1. Aits, S. and Jaattela, M. (2013). Lysosomal cell death at a glance. J. Cell Sci. 126, 1905-1912.
2. Appelmans, F., Wattiaux, R., and de Duve, D. (1955). Tissue fractionation studies. 5. The association of acid phosphatase with a special class of cytoplasmic granules in rat liver. Biochem. J. 59, 438-445.
3. Appelqvist, H., Waster, P., Kagedal, K., and Ollinger, K. (2013). The lysosome: from waste bag to potential therapeutic target. J. Mol. Cell Biol. 5, 214-226.
4. Arias, E. and Cuervo, A. M. (2011). Chaperone-mediated autophagy in protein quality control. Curr. Opin. Cell Biol. 23, 184-189.
5. Ashoor, R., Yafawi, R., Jessen, B., and Lu, S. (2013). The contribution of lysosomotropism to autophagy perturbation. PLoS One 8:e82481.
6. Averette, K. M., Pratt, M. R., Yang, Y., Bassilian, S., Whitelegge, J. P., Loo, J. A., Muir, T. W., and Bradley, K. A. (2009). Anthrax lethal toxin induced lysosomal membrane permeabilization and cytosolic cathepsin release is Nlrp1b/Nalp1b-dependent. PLoS One 4:e7913.
7. Blomgran, R., Zheng, L., and Stendahl, O. (2007). Cathepsin-cleaved Bid promotes apoptosis in human neutrophils via oxidative stress-induced lysosomal membrane permeabilization. J. Leukoc. Biol. 81, 1213-1223.
8. Bogdan, A. R., Miyazawa, M., Hashimoto, K., and Tsuji, Y. (2016). Regulators of iron homeostasis: new players in metabolism, cell death, and disease. Trends Biochem. Sci. 41, 274-286.
9. Bojic, L., Petelin, A., Stoka, V., Reinheckel, T., Peters, C., Turk, V., and Turk, B. (2007). Cysteine cathepsins are not involved in Fas/CD95 signalling in primary skin fibroblasts. FEBS Lett. 581, 5185-5190.
10. Brojatsch, J., Lima, H., Jr., Palliser, D., Jacobson, L. S., Muehlbauer, S. M., Furtado, R., Goldman, D. L., Lisanti, M. P., and Chandran, K. (2015). Distinct cathepsins control necrotic cell death mediated by pyroptosis inducers and lysosome-destabilizing agents. Cell Cycle 14, 964-972.
11. Butinar, M., Prebanda, M. T., Rajkovic, J., Jeric, B., Stoka, V., Peters, C., Reinheckel, T., Kruger, A., Turk, V., Turk, B., et al. (2014). Stefin B deficiency reduces tumor growth via sensitization of tumor cells to oxidative stress in a breast cancer model. Oncogene 33, 3392-3400.
12. Chaitanya, G. V., Steven, A. J., and Babu, P. P. (2010). PARP-1 cleavage fragments: signatures of cell-death proteases in neurodegeneration. Cell Commun. Signal 8, 31.
13. Cheng, T., van Vlijmen-Willems, I. M., Hitomi, K., Pasch, M. C., van Erp, P. E., Schalkwijk, J., and Zeeuwen, P. L. (2009). Colocalization of cystatin M/E and its target proteases suggests a role in terminal differentiation of human hair follicle and nail. J. Invest. Dermatol. 129, 1232-1242.
14. Ciechanover, A. (2012). Intracellular protein degradation: from a vague idea thru the lysosome and the ubiquitin-proteasome system and onto human diseases and drug targeting. Biochim. Biophys. Acta. 1824, 3-13.
15. Cirman, T., Oresic, K., Droga-Mazovec, G., Turk, V., Reed, J. C., Myers, R. M., Salvesen, G. S., and Turk, B. (2004). Selective disruption of lysosomes in HeLa cells triggers apoptosis mediated by cleavage of Bid by multiple papain-like lysosomal cathepsins. J. Biol. Chem. 279, 3578-3587.
16. Conus, S., Perozzo, R., Reinheckel, T., Peters, C., Scapozza, L., Yousefi, S., and Simon, H. U. (2008). Caspase-8 is activated by cathepsin D initiating neutrophil apoptosis during the resolution of inflammation. J. Exp. Med. 205, 685-698.
17. Cookson, B. T. and Brennan, M. A. (2001). Pro-inflammatory programmed cell death. Trends Microbiol. 9, 113-114.
18. Costanzo, A., Fausti, F., Spallone, G., Moretti, F., Narcisi, A., and Botti, E. (2015). Programmed cell death in the skin. Int. J. Dev. Biol. 59, 73-78.
19. Cuervo, A. M. and Wong, E. (2014). Chaperone-mediated autophagy: roles in disease and aging. Cell Res. 24, 92-104.
20. Dahl, S. W., Halkier, T., Lauritzen, C., Dolenc, I., Pedersen, J., Turk, V., and Turk, B. (2001). Human recombinant pro-dipeptidyl peptidase I (cathepsin C) can be activated by cathepsins L and S but not by autocatalytic processing. Biochemistry 40, 1671-1678.
21. de Duve, C. (1983). Lysosomes revisited. Eur. J. Biochem. 137, 391-397.
22. Ding, J., Wang, K., Liu, W., She, Y., Sun, Q., Shi, J., Sun, H., Wang, D. C., and Shao, F. (2016). Pore-forming activity and structural autoinhibition of the gasdermin family. Nature 535, 111-116.
23. Dixon, S. J. and Stockwell, B. R. (2014). The role of iron and reactive oxygen species in cell death. Nat. Chem. Biol. 10, 9-17.
24. Dixon, S. J., Lemberg, K. M., Lamprecht, M. R., Skouta, R., Zaitsev, E. M., Gleason, C. E., Patel, D. N., Bauer, A. J., Cantley, A. M., Yang, W. S., et al. (2012). Ferroptosis: an iron-dependent form of nonapoptotic cell death. Cell 149, 1060-1072.
25. Droga-Mazovec, G., Bojic, L., Petelin, A., Ivanova, S., Romih, R., Repnik, U., Salvesen, G. S., Stoka, V., Turk, V., and Turk, B. (2008). Cysteine cathepsins trigger caspase-dependent cell death through cleavage of bid and antiapoptotic Bcl-2 homologues. J. Biol. Chem. 283, 19140-19150.
26. Duewell, P., Kono, H., Rayner, K. J., Sirois, C. M., Vladimer, G., Bauernfeind, F. G., Abela, G. S., Franchi, L., Nunez, G., Schnurr, M., et al. (2010). NLRP3 inflammasomes are required for atherogenesis and activated by cholesterol crystals. Nature 464, 1357-1361.
27. Duncan, J. A., Gao, X., Huang, M. T., O'Connor, B. P., Thomas, C. E., Willingham, S. B., Bergstralh, D. T., Jarvis, G. A., Sparling, P. F., and Ting, J. P. (2009). Neisseria gonorrhoeae activates the proteinase cathepsin B to mediate the signaling activities of the NLRP3 and ASC-containing inflammasome. J. Immunol. 182, 6460-6469.
28. Eckhart, L., Lippens, S., Tschachler, E., and Declercq, W. (2013). Cell death by cornification. Biochim. Biophys. Acta. 1833, 3471-3480.
29. Eskelinen, E. L. and Saftig, P. (2009). Autophagy: a lysosomal degradation pathway with a central role in health and disease. Biochim. Biophys. Acta. 1793, 664-673.
30. Filicko-O'Hara, J., Grosso, D., Flomenberg, P. R., Friedman, T. M., Brunner, J., Drobyski, W., Ferber, A., Kakhniashvili, I., Keever-Taylor, C., Mookerjee, B., et al. (2009). Antiviral responses following L-leucyl-L-leucine methyl esther (LLME) -treated lymphocyte infusions: graft-versus-infection without graft-versushost disease. Biol. Blood Marrow. Transplant. 15, 1609-1619.
31. Fuchs, R. and Blaas, D. (2010). Uncoating of human rhinoviruses. Rev. Med. Virol. 20, 281-297.
32. Galluzzi, L., Bravo-San Pedro, J. M., and Kroemer, G. (2014). Organellespecific initiation of cell death. Nat. Cell Biol. 16, 728-736.
33. Ghosh, M., Carlsson, F., Laskar, A., Yuan, X. M., and Li, W. (2011). Lysosomal membrane permeabilization causes oxidative stress and ferritin induction in macrophages. FEBS Lett. 585, 623-629.
34. Gomez-Sintes, R., Ledesma, M. D., and Boya, P. (2016). Lysosomal cell death mechanisms in aging. Ageing Res. Rev. doi:10.1016/j.arr.2016.02.009.
35. Guicciardi, M. E., Leist, M., and Gores, G. J. (2004). Lysosomes in cell death. Oncogene 23, 2881-2890.
36. Guo, H., Callaway, J. B., and Ting, J. P. (2015). Inflammasomes: mechanism of action, role in disease, and therapeutics. Nat. Med. 21, 677-687.
37. Hafner Česen, M., Pegan, K., Špes, A., and Turk, B. (2012). Lysosomal pathways to cell death and their therapeutic applications. Exp. Cell Res. 318, 1245-1251.
38. Hafner Česen, M., Repnik, U., Turk, V., and Turk, B. (2013). Siramesine triggers cell death through destabilisation of mitochondria, but not lysosomes. Cell Death Dis. 4:e818.
39. Hafner Česen, M., Stoka, V., and Turk, B. (2016). Role of lysosomes in intracellular degradation. In: Encyclopedia of Cell Biology, Molecular Cell Biology, Vol. 1. R. A. Bradshaw and P. D. Stahl, eds. (San Diego: Elsevier), pp. 612-620.
40. Heid, M. E., Keyel, P. A., Kamga, C., Shiva, S., Watkins, S. C., and Salter, R. D. (2013). Mitochondrial reactive oxygen species induces NLRP3-dependent lysosomal damage and inflammasome activation. J. Immunol. 191, 5230-5238.
41. Heinrich, M., Neumeyer, J., Jakob, M., Hallas, C., Tchikov, V., Winoto-Morbach, S., Wickel, M., Schneider-Brachert, W., Trauzold, A., Hethke, A., et al. (2004). Cathepsin D links TNF- induced acid sphingomyelinase to Bid-mediated caspase-9 and -3 activation. Cell Death Differ. 11, 550-563.
42. Henke, N., Albrecht, P., Bouchachia, I., Ryazantseva, M., Knoll, K., Lewerenz, J., Kaznacheyeva, E., Maher, P., and Methner, A. (2013). The plasma membrane channel ORAI1 mediates detrimental calcium influx caused by endogenous oxidative stress. Cell Death Dis. 4:e470.
43. Hernandez, L., KIM, M. K., Noonan, A. M., Sagher, E., Kohlhammer, H., Wright, G., Lyle, L. T., Steeg, P. S., Anver, M., Bowtell, D. D., et al. (2015). A dual role for Caspase8 and NF-κB interactions in regulating apoptosis and necroptosis of ovarian cancer, with correlation to patient survival. Cell Death Discovery 1, 15053. doi:10.1038/cddiscovery.2015.53.
44. Hohn, A. and Grune, T. (2013). Lipofuscin: formation, effects and role of macroautophagy. Redox Biol 1, 140-144.
45. Hornung, V., Bauernfeind, F., Halle, A., Samstad, E. O., Kono, H., Rock, K. L., Fitzgerald, K. A., and Latz, E. (2008). Silica crystals and aluminum salts activate the NALP3 inflammasome through phagosomal destabilization. Nat. Immunol. 9, 847-856.
46. Houseweart, M. K., Vilaythong, A., Yin, X. M., Turk, B., Noebels, J. L., and Myers, R. M. (2003). Apoptosis caused by cathepsins does not require Bid signaling in an in vivo model of progressive myoclonus epilepsy (EPM1). Cell Death Differ. 10, 1329-1335.
47. Hu, Y. B., Dammer, E. B., Ren, R. J., and Wang, G. (2015). The endosomal-lysosomal system: from acidification and cargo sorting to neurodegeneration. Transl. Neurodegener. 4, 18.
48. Hung, Y. H., Chen, L. M., Yang, J. Y., and Yang, W. Y. (2013). Spatiotemporally controlled induction of autophagy-mediated lysosome turnover. Nat. Commun. 4, 2111.
49. Jansen, P. A., van den Bogaard, E. H., Kersten, F. F., Oostendorp, C., van Vlijmen-Willems, I. M., Oji, V., Traupe, H., Hennies, H. C., Schalkwijk, J., and Zeeuwen, P. L. (2012). Cystatin M/E knockdown by lentiviral delivery of shRNA impairs epidermal morphogenesis of human skin equivalents. Exp. Dermatol. 21, 889-891.
50. Jiang, P. and Mizushima, N. (2014). Autophagy and human diseases. Cell Res. 24, 69-79.
51. Johansson, A. C., Appelqvist, H., Nilsson, C., Kagedal, K., Roberg, K., and Ollinger, K. (2010). Regulation of apoptosis-associated lysosomal membrane permeabilization. Apoptosis 15, 527-540.
52. Ju, X., Yan, Y., Liu, Q., Li, N., Sheng, M., Zhang, L., Li, X., Liang, Z., Huang, F., Liu, K., et al. (2015). Neuraminidase of influenza A virus binds lysosome-associated membrane proteins directly and induces lysosome rupture. J. Virol. 89, 10347-10358.
53. Kaminskyy, V. and Zhivotovsky, B. (2012). Proteases in autophagy. Biochim. Biophys. Acta. 1824, 44-50.
54. Karlsson, M., Frennesson, C., Gustafsson, T., Brunk, U. T., Nilsson, S. E., and Kurz, T. (2013). Autophagy of iron-binding proteins may contribute to the oxidative stress resistance of ARPE-19 cells. Exp. Eye Res. 116, 359-365.
55. Kaur, J. and Debnath, J. (2015). Autophagy at the crossroads of catabolism and anabolism. Nat. Rev. Mol. Cell Biol. 16, 461-472.
56. Kayagaki, N., Stowe, I. B., Lee, B. L., O'Rourke, K., Anderson, K., Warming, S., Cuellar, T., Haley, B., Roose-Girma, M., Phung, Q. T., et al. (2015). Caspase-11 cleaves gasdermin D for noncanonical inflammasome signalling. Nature 526, 666-671.
57. Kirkegaard, T. and Jaattela, M. (2009). Lysosomal involvement in cell death and cancer. Biochim. Biophys. Acta. 1793, 746-754.
58. Kubota, C., Torii, S., Hou, N., Saito, N., Yoshimoto, Y., Imai, H., and Takeuchi, T. (2010). Constitutive reactive oxygen species generation from autophagosome/lysosome in neuronal oxidative toxicity. J. Biol. Chem. 285, 667-674.
59. Kurz, T., Terman, A., and Brunk, U. T. (2007). Autophagy, ageing and apoptosis: the role of oxidative stress and lysosomal iron. Arch. Biochem. Biophys. 462, 220-230.
60. Kurz, T., Eaton, J. W., and Brunk, U. T. (2011). The role of lysosomes in iron metabolism and recycling. Int. J. Biochem. Cell Biol. 43, 1686-1697.
61. Lamkanfi, M. and Dixit, V. M. (2014). Mechanisms and functions of inflammasomes. Cell 157, 1013-1022.
62. Li, W., Yuan, X., Nordgren, G., Dalen, H., Dubowchik, G. M., Firestone, R. A., and Brunk, U. T. (2000). Induction of cell death by the lysosomotropic detergent MSDH. FEBS Lett. 470, 35-39.
63. Li, W. W., Li, J., and Bao, J. K. (2012). Microautophagy: lesser-known self-eating. Cell Mol. Life Sci. 69, 1125-1136.
64. Lima, H., Jr., Jacobson, L. S., Goldberg, M. F., Chandran, K., Diaz-Griffero, F., Lisanti, M. P., and Brojatsch, J. (2013). Role of lysosome rupture in controlling Nlrp3 signaling and necrotic cell death. Cell Cycle 12, 1868-1878.
65. Lippens, S., Hoste, E., Vandenabeele, P., Agostinis, P., and Declercq, W. (2009). Cell death in the skin. Apoptosis 14, 549-569.
66. Luzio, J. P., Rous, B. A., Bright, N. A., Pryor, P. R., Mullock, B. M., and Piper, R. C. (2000). Lysosome-endosome fusion and lysosome biogenesis. J. Cell Sci. 113, 1515-1524.
67. Maejima, I., Takahashi, A., Omori, H., Kimura, T., Takabatake, Y., Saitoh, T., Yamamoto, A., Hamasaki, M., Noda, T., Isaka, Y., et al. (2013). Autophagy sequesters damaged lysosomes to control lysosomal biogenesis and kidney injury. EMBO J. 32, 2336-2347.
68. Maier, O., Galan, D. L., Wodrich, H., and Wiethoff, C. M. (2010). An N-terminal domain of adenovirus protein VI fragments membranes by inducing positive membrane curvature. Virology 402, 11-19.
69. Marino, J., Garcia Vior, M. C., Furmento, V. A., Blank, V. C., Awruch, J., and Roguin, L. P. (2013). Lysosomal and mitochondrial permeabilization mediates zinc (II) cationic phthalocyanine phototoxicity. Int. J. Biochem. Cell Biol. 45, 2553-2562.
70. McComb, S., Shutinoski, B., Thurston, S., Cessford, E., Kumar, K., and Sad, S. (2014). Cathepsins limit macrophage necroptosis through cleavage of Rip1 kinase. J. Immunol. 192, 5671-5678.
71. Miller, D. K., Griffiths, E., Lenard, J., and Firestone, R. A. (1983). Cell killing by lysosomotropic detergents. J. Cell Biol. 97, 1841-1851.
72. Mizushima, N., Levine, B., Cuervo, A. M., and Klionsky, D. J. (2008). Autophagy fights disease through cellular self-digestion. Nature 451, 1069-1075.
73. Mrschtik, M. and Ryan, K. M. (2015). Lysosomal proteins in cell death and autophagy. FEBS J. 282, 1858-1870.
74. Newman, Z. L., Leppla, S. H., and Moayeri, M. (2009). CA-074Me protection against anthrax lethal toxin. Infect. Immun. 77, 4327-4336.
75. Oberle, C., Huai, J., Reinheckel, T., Tacke, M., Rassner, M., Ekert, P. G., Buellesbach, J., and Borner, C. (2010). Lysosomal membrane permeabilization and cathepsin release is a Bax/Bak-dependent, amplifying event of apoptosis in fibroblasts and monocytes. Cell Death Differ. 17, 1167-1178.
76. Ofengeim, D. and Yuan, J. (2013). Regulation of RIP1 kinase signalling at the crossroads of inflammation and cell death. Nat. Rev. Mol. Cell Biol. 14, 727-736.
77. Ostenfeld, M. S., Fehrenbacher, N., Hoyer-Hansen, M., Thomsen, C., Farkas, T., and Jaattela, M. (2005). Effective tumor cell death by sigma-2 receptor ligand siramesine involves lysosomal leakage and oxidative stress. Cancer Res. 65, 8975-8983.
78. Ostenfeld, M. S., Hoyer-Hansen, M., Bastholm, L., Fehrenbacher, N., Olsen, O. D., Groth-Pedersen, L., Puustinen, P., Kirkegaard-Sorensen, T., Nylandsted, J., Farkas, T., et al. (2008). Anti-cancer agent siramesine is a lysosomotropic detergent that induces cytoprotective autophagosome accumulation. Autophagy 4, 487-499.
79. Parenti, G., Andria, G., and Ballabio, A. (2015). Lysosomal storage diseases: from pathophysiology to therapy. Annu. Rev. Med. 66, 471-486.
80. Pasparakis, M. and Vandenabeele, P. (2015). Necroptosis and its role in inflammation. Nature 517, 311-320.
81. Repnik, U., Stoka, V., Turk, V., and Turk, B. (2012). Lysosomes and lysosomal cathepsins in cell death. Biochim. Biophys. Acta. 1824, 22-33.
82. Repnik, U., Hafner Cesen, M., and Turk, B. (2014). Lysosomal membrane permeabilization in cell death: concepts and challenges. Mitochondrion 19 (Pt A), 49-57.
83. Saftig, P., Schroder, B., and Blanz, J. (2010). Lysosomal membrane proteins: life between acid and neutral conditions. Biochem. Soc. Trans. 38, 1420-1423.
84. Sborgi, L., Ruhl, S., Mulvihill, E., Pipercevic, J., Heilig, R., Stahlberg, H., Farady, C. J., Muller, D. J., Broz, P., and Hiller, S. (2016). GSDMD membrane pore formation constitutes the mechanism of pyroptotic cell death. EMBO J. 35, 1766-1778.
85. Serrano-Puebla, A. and Boya, P. (2016). Lysosomal membrane permeabilization in cell death: new evidence and implications for health and disease. Ann. N Y Acad. Sci. 1371, 30-44.
86. Settembre, C., Fraldi, A., Medina, D. L., and Ballabio, A. (2013). Signals from the lysosome: a control centre for cellular clearance and energy metabolism. Nat. Rev. Mol. Cell Biol. 14, 283-296.
87. Sigismund, S., Confalonieri, S., Ciliberto, A., Polo, S., Scita, G., and Di Fiore, P. P. (2012). Endocytosis and signaling: cell logistics shape the eukaryotic cell plan. Physiol. Rev. 92, 273-366.
88. Spes, A., Sobotic, B., Turk, V., and Turk, B. (2012). Cysteine cathepsins are not critical for TRAIL- and CD95-induced apoptosis in several human cancer cell lines. Biol. Chem. 393, 1417-1431.
89. Stoka, V., Turk, B., Schendel, S. L., Kim, T. H., Cirman, T., Snipas, S. J., Ellerby, L. M., Bredesen, D., Freeze, H., Abrahamson, M., et al. (2001). Lysosomal protease pathways to apoptosis. Cleavage of bid, not pro-caspases, is the most likely route. J. Biol. Chem. 276, 3149-3157.
90. Stoka, V., Turk, V., and Turk, B. (2016). Lysosomal cathepsins and their regulation in aging and neurodegeneration. Ageing Res. Rev.
91. Tan, S., Schubert, D., and Maher, P. (2001). Oxytosis: a novel form of programmed cell death. Curr. Top Med. Chem. 1, 497-506.
92. Terman, A. and Brunk, U. T. (2004). Lipofuscin. Int. J. Biochem. Cell Biol. 36, 1400-1404.
93. Thiele, D. L. and Lipsky, P. E. (1990). Mechanism of L-leucyl-L-leucine methyl ester-mediated killing of cytotoxic lymphocytes: dependence on a lysosomal thiol protease, dipeptidyl peptidase I, that is enriched in these cells. Proc. Natl. Acad. Sci. USA 87, 83-87.
94. Tosteson, M. T. and Chow, M. (1997). Characterization of the ion channels formed by poliovirus in planar lipid membranes. J. Virol. 71, 507-511.
95. Tseng, W. A., Thein, T., Kinnunen, K., Lashkari, K., Gregory, M. S., D'Amore, P. A., and Ksander, B. R. (2013). NLRP3 inflammasome activation in retinal pigment epithelial cells by lysosomal destabilization: implications for age-related macular degeneration. Invest. Ophthalmol. Vis. Sci. 54, 110-120.
96. Turk, B. (2006). Targeting proteases: successes, failures and future prospects. Nat. Rev. Drug Discov. 5, 785-799.
97. Turk, B. and Turk, V. (2009). Lysosomes as "suicide bags" in cell death: myth or reality? J. Biol. Chem. 284, 21783-21787.
98. Turk, V., Turk, B., and Turk, D. (2001). Lysosomal cysteine proteases: facts and opportunities. EMBO J. 20, 4629-4633.
99. Turk, V., Stoka, V., Vasiljeva, O., Renko, M., Sun, T., Turk, B., and Turk, D. (2012). Cysteine cathepsins: from structure, function and regulation to new frontiers. Biochim. Biophys. Acta. 1824, 68-88.
100. Uchimoto, T., Nohara, H., Kamehara, R., Iwamura, M., Watanabe, N., and Kobayashi, Y. (1999). Mechanism of apoptosis induced by a lysosomotropic agent, L-Leucyl-L-Leucine methyl ester. Apoptosis 4, 357-362.
101. Vanden Berghe, T., Vanlangenakker, N., Parthoens, E., Deckers, W., Devos, M., Festjens, N., Guerin, C. J., Brunk, U. T., Declercq, W., and Vandenabeele, P. (2010). Necroptosis, necrosis and secondary necrosis converge on similar cellular disintegration features. Cell Death Differ. 17, 922-930.
102. Vanden Berghe, T., Linkermann, A., Jouan-Lanhouet, S., Walczak, H., and Vandenabeele, P. (2014). Regulated necrosis: the expanding network of non-apoptotic cell death pathways. Nat. Rev. Mol. Cell Biol. 15, 135-147.
103. Vasiljeva, O. and Turk, B. (2008). Dual contrasting roles of cysteine cathepsins in cancer progression: apoptosis versus tumour invasion. Biochimie 90, 380-386.
104. 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. Design 13, 387-403.
105. Vasiljeva, O., Korovin, M., Gajda, M., Brodoefel, H., Bojic, L., Kruger, A., Schurigt, U., Sevenich, L., Turk, B., Peters, C., et al. (2008). Reduced tumour cell proliferation and delayed development of high-grade mammary carcinomas in cathepsin B-deficient mice. Oncogene 27, 4191-4199.
106. Villamil Giraldo, A. M., Appelqvist, H., Ederth, T., and Ollinger, K. (2014). Lysosomotropic agents: impact on lysosomal membrane permeabilization and cell death. Biochem. Soc. Trans. 42, 1460-1464.
107. Wallach, D., Kang, T. B., Dillon, C. P., and Green, D. R. (2016). Programmed necrosis in inflammation: toward identification of the effector molecules. Science 352, aaf2154.
108. Wattiaux, R., Wattiaux-de Coninck, S., Thirion, J., Gasingirwa, M. C., and Jadot, M. (2007). Lysosomes and Fas-mediated liver cell death. Biochem J 403, 89-95.
109. Willingham, S. B., Bergstralh, D. T., O'Connor, W., Morrison, A. C., Taxman, D. J., Duncan, J. A., Barnoy, S., Venkatesan, M. M., Flavell, R. A., Deshmukh, M., et al. (2007). Microbial pathogeninduced necrotic cell death mediated by the inflammasome components CIAS1/cryopyrin/NLRP3 and ASC. Cell Host. Microbe. 2, 147-159.
110. Xu, H., and Ren, D. (2015). Lysosomal physiology. Annu. Rev. Physiol. 77, 57-80.
111. 2+ -dependent proteases in ischemic neuronal death: a conserved'calpain-cathepsin cascade' from nematodes to primates. Cell Calcium 36, 285-293.
112. Young, M. M., Kester, M., and Wang, H. G. (2013). Sphingolipids: regulators of crosstalk between apoptosis and autophagy. J. Lipid. Res. 54, 5-19.
113. Yu, F., Chen, Z., Wang, B., Jin, Z., Hou, Y., Ma, S., and Liu, X. (2016). The role of lysosome in cell death regulation. Tumour Biol. 37, 1427-1436.
114. Zeeuwen, P. L. (2004). Epidermal differentiation: the role of proteases and their inhibitors. Eur. J. Cell Biol. 83, 761-773.
115. Zeeuwen, P. L., van Vlijmen-Willems, I. M., Hendriks, W., Merkx, G. F., and Schalkwijk, J. (2002). A null mutation in the cystatin M/E gene of ichq mice causes juvenile lethality and defects in epidermal cornification. Hum. Mol. Genet. 11, 2867-2875.
116. Zeeuwen, P. L., Cheng, T., and Schalkwijk, J. (2009). The biology of cystatin M/E and its cognate target proteases. J. Invest. Dermatol. 129, 1327-1338.
117. Zeeuwen, P. L., van Vlijmen-Willems, I. M., Cheng, T., Rodijk-Olthuis, D., Hitomi, K., Hara-Nishimura, I., John, S., Smyth, N., Reinheckel, T., Hendriks, W. J., et al. (2010). The cystatin M/E-cathepsin L balance is essential for tissue homeostasis in epidermis, hair follicles, and cornea. FASEB J. 24, 3744-3755.
118. Zhou, Q., and Salvesen, G. S. (1997). Activation of pro-caspase-7 by serine proteases includes a non-canonical specificity. Biochem. J. 324, 361-364.
119. Zou, J., Kawai, T., Tsuchida, T., Kozaki, T., Tanaka, H., Shin, K. S., Kumar, H., and Akira, S. (2013). Poly IC triggers a cathepsin D- and IPS-1-dependent pathway to enhance cytokine production and mediate dendritic cell necroptosis. Immunity 38, 717-728.