Lysosomal pathways to cell death and their therapeutic applications

Experimental Cell Research

Volumn 318, Issue 11, 2012, Pages 1245-1251

  Hafner Česen, Maruša ^a   Pegan, Katarina ^a   Špes, Aleš ^a   Turk, Boris ^a,b,c,d  

^a JO EF STEFAN INSTITUTE   (Slovenia)

^b Center of Excellence CIPKEBIP   (Slovenia)

^c Center of Excellence NIN   (Slovenia)

^d UNIVERSITY OF LJUBLJANA   (Slovenia)

Author keywords

Apoptosis; Autophagy; Cancer; Cathepsin; Lysosome; Neurodegeneration

Indexed keywords

CATHEPSIN; HYDROLASE; PROTEIN BCL 2; PROTEIN BID;

APOPTOSIS; CELL DEATH; CYTOSOL; DEGENERATIVE DISEASE; DRUG TARGETING; HUMAN; LYSOSOME; LYSOSOME MEMBRANE; MEMBRANE PERMEABILITY; NEOPLASM; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; REVIEW;

EID: 84861671713     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2012.03.005     Document Type: Review

References (52)

1. Luzio J.P., Pryor P.R., Bright N.A. Lysosomes: fusion and function. Nat. Rev. Mol. Cell Biol. 2007, 8:622-632.
2. Huotari J., Helenius A. Endosome maturation. EMBO J. 2011, 30:3481-3500.
3. Saftig P., Klumperman J. Lysosome biogenesis and lysosomal membrane proteins: trafficking meets function. Nat. Rev. Mol. Cell Biol. 2009, 10:623-635.
4. Repnik U., Stoka V., Turk V., Turk B. Lysosomes and lysosomal cathepsins in cell death. Biochim. Biophys. Acta 2012, 1824:22-33.
5. Rossi A., Deveraux Q., Turk B., Sali A. Comprehensive search for cysteine cathepsins in the human genome. Biol. Chem. 2004, 385:363-372.
6. Turk V., Stoka V., Vasiljeva O., Renko M., Sun T., Turk B., Turk D. Cysteine cathepsins: from structure, function and regulation to new frontiers. Biochim. Biophys. Acta 2012, 1824:68-88.
7. Turk V., Turk B., Turk D. Lysosomal cysteine proteases: facts and opportunities. EMBO J. 2001, 20:4629-4633.
8. Turk B., Turk V. Lysosomes as "suicide bags" in cell death: myth or reality?. J. Biol. Chem. 2009, 284:21783-21787.
9. Boya P., Kroemer G. Lysosomal membrane permeabilization in cell death. Oncogene 2008, 27:6434-6451.
10. Golstein P., Kroemer G. Cell death by necrosis: towards a molecular definition. Trends Biochem. Sci. 2007, 32:37-43.
11. Kirkegaard T., Jaattela M. Lysosomal involvement in cell death and cancer. Biochim. Biophys. Acta 2009, 1793:746-754.
12. Hengartner M.O. The biochemistry of apoptosis. Nature 2000, 407:770-776.
13. Chipuk J.E., Bouchier-Hayes L., Green D.R. Mitochondrial outer membrane permeabilization during apoptosis: the innocent bystander scenario. Cell Death Differ. 2006, 13:1396-1402.
14. Youle R.J., Strasser A. The BCL-2 protein family: opposing activities that mediate cell death. Nat. Rev. Mol. Cell Biol. 2008, 9:47-59.
15. Pop C., Salvesen G.S. Human caspases: activation, specificity, and regulation. J. Biol. Chem. 2009, 284:21777-21781.
16. Oberst A., Pop C., Tremblay A.G., Blais V., Denault J.B., Salvesen G.S., Green D.R. Inducible dimerization and inducible cleavage reveal a requirement for both processes in caspase-8 activation. J. Biol. Chem. 2010, 285:16632-16642.
17. Turk B., Turk D., Turk V. Protease signalling: the cutting edge. EMBO J. 2012, 31:1630-1643.
18. Stoka V., Turk V., Turk B. Lysosomal cysteine cathepsins: signaling pathways in apoptosis. Biol. Chem. 2007, 388:555-560.
19. Kurz T., Terman A., Gustafsson B., Brunk U.T. Lysosomes and oxidative stress in aging and apoptosis. Biochim. Biophys. Acta 2008, 1780:1291-1303.
20. Terman A., Kurz T., Gustafsson B., Brunk U.T. Lysosomal labilization. IUBMB Life 2006, 58:531-539.
21. Zhao M., Antunes F., Eaton J.W., Brunk U.T. Lysosomal enzymes promote mitochondrial oxidant production, cytochrome c release and apoptosis. Eur. J. Biochem. 2003, 270:3778-3786.
22. Chwieralski C.E., Welte T., Buhling F. Cathepsin-regulated apoptosis. Apoptosis 2006, 11:143-149.
23. Liu L., Zhang Z., Xing D. Cell death via mitochondrial apoptotic pathway due to activation of Bax by lysosomal photodamage. Free Radic. Biol. Med. 2011, 51:53-68.
24. Ostenfeld M.S., Fehrenbacher N., Hoyer-Hansen M., Thomsen C., Farkas T., Jaattela M. Effective tumor cell death by sigma-2 receptor ligand siramesine involves lysosomal leakage and oxidative stress. Cancer Res. 2005, 65:8975-8983.
25. de Duve C., de Barsy T., Poole B., Trouet A., Tulkens P., Van Hoof F. Commentary. Lysosomotropic agents. Biochem. Pharmacol. 1974, 23:2495-2531.
26. Miller D.K., Griffiths E., Lenard J., Firestone R.A. Cell killing by lysosomotropic detergents. J. Cell Biol. 1983, 97:1841-1851.
27. Mohamed M.M., Sloane B.F. Cysteine cathepsins: multifunctional enzymes in cancer. Nat. Rev. Cancer 2006, 6:764-775.
28. Werneburg N.W., Guicciardi M.E., Bronk S.F., Gores G.J. Tumor necrosis factor-alpha-associated lysosomal permeabilization is cathepsin B dependent. Am. J. Physiol. Gastrointest. Liver Physiol. 2002, 283:G947-G956.
29. Johansson A.C., Appelqvist H., Nilsson C., Kagedal K., Roberg K., Ollinger K. Regulation of apoptosis-associated lysosomal membrane permeabilization. Apoptosis 2010, 15:527-540.
30. Werneburg N.W., Guicciardi M.E., Bronk S.F., Kaufmann S.H., Gores G.J. Tumor necrosis factor-related apoptosis-inducing ligand activates a lysosomal pathway of apoptosis that is regulated by Bcl-2 proteins. J. Biol. Chem. 2007, 282:28960-28970.
31. Oberle C., Huai J., Reinheckel T., Tacke M., Rassner M., Ekert P.G., Buellesbach J., Borner C. Lysosomal membrane permeabilization and cathepsin release is a Bax/Bak-dependent, amplifying event of apoptosis in fibroblasts and monocytes. Cell Death Differ. 2010, 17:1167-1178.
32. Droga-Mazovec G., Bojič L., Petelin A., Ivanova S., Romih R., Repnik U., Salvesen G.S., Stoka V., Turk V., Turk B. Cysteine cathepsins trigger caspase-dependent cell death through cleavage of bid and antiapoptotic Bcl-2 homologues. J. Biol. Chem. 2008, 283:19140-19150.
33. Cirman T., Orešić K., Droga-Mazovec G., Turk V., Reed J.C., Myers R.M., Salvesen G.S., Turk B. Selective disruption of lysosomes in HeLa cells triggers apoptosis mediated by cleavage of Bid by multiple papain-like lysosomal cathepsins. J. Biol. Chem. 2004, 279:3578-3587.
34. Gyrd-Hansen M., Farkas T., Fehrenbacher N., Bastholm L., Hoyer-Hansen M., Elling F., Wallach D., Flavell R., Kroemer G., Nylandsted J., Jaattela M. Apoptosome-independent activation of the lysosomal cell death pathway by caspase-9. Mol. Cell. Biol. 2006, 26:7880-7891.
35. Werneburg N., Guicciardi M.E., Yin X.M., Gores G.J. TNF-alpha-mediated lysosomal permeabilization is FAN and caspase 8/Bid dependent. Am. J. Physiol. Gastrointest. Liver Physiol. 2004, 287:G436-G443.
36. Schrader K., Huai J., Jockel L., Oberle C., Borner C. Non-caspase proteases: triggers or amplifiers of apoptosis?. Cell. Mol. Life Sci. 2010, 67:1607-1618.
37. Vince J.E., Chau D., Callus B., Wong W.W., Hawkins C.J., Schneider P., McKinlay M., Benetatos C.A., Condon S.M., Chunduru S.K., Yeoh G., Brink R., Vaux D.L., Silke J. TWEAK-FN14 signaling induces lysosomal degradation of a cIAP1-TRAF2 complex to sensitize tumor cells to TNFalpha. J. Cell Biol. 2008, 182:171-184.
38. Stoka V., Turk B., Schendel S.L., Kim T.H., Cirman T., Snipas S.J., Ellerby L.M., Bredesen D., Freeze H., Abrahamson M., Bromme D., Krajewski S., Reed J.C., Yin X.M., Turk V., Salvesen G.S. Lysosomal protease pathways to apoptosis. Cleavage of bid, not pro-caspases, is the most likely route. J. Biol. Chem. 2001, 276:3149-3157.
39. Conus S., Perozzo R., Reinheckel T., Peters C., Scapozza L., Yousefi S., Simon H.U. Caspase-8 is activated by cathepsin D initiating neutrophil apoptosis during the resolution of inflammation. J. Exp. Med. 2008, 205:685-698.
40. Houseweart M.K., Vilaythong A., Yin X.M., Turk B., Noebels J.L., Myers R.M. Apoptosis caused by cathepsins does not require Bid signaling in an in vivo model of progressive myoclonus epilepsy (EPM1). Cell Death Differ. 2003, 10:1329-1335.
41. Reiser J., Adair B., Reinheckel T. Specialized roles for cysteine cathepsins in health and disease. J. Clin. Invest. 2010, 120:3421-3431.
42. Vasiljeva O., Reinheckel T., Peters C., Turk D., Turk V., Turk B. Emerging roles of cysteine cathepsins in disease and their potential as drug targets. Curr. Pharm. Des. 2007, 13:387-403.
43. Palermo C., Joyce J.A. Cysteine cathepsin proteases as pharmacological targets in cancer. Trends Pharmacol. Sci. 2008, 29:22-28.
44. Shree T., Olson O.C., Elie B.T., Kester J.C., Garfall A.L., Simpson K., Bell-McGuinn K.M., Zabor E.C., Brogi E., Joyce J.A. Macrophages and cathepsin proteases blunt chemotherapeutic response in breast cancer. Genes Dev. 2011, 25:2465-2479.
45. Mikhaylov G., Mikac U., Magaeva A.A., Itin V.I., Naiden E.P., Psakhye I., Babes L., Reinheckel T., Peters C., Zeiser R., Bogyo M., Turk V., Psakhye S.G., Turk B., Vasiljeva O. Ferri-liposomes as an MRI-visible drug-delivery system for targeting tumours and their microenvironment. Nat. Nanotechnol. 2011, 6:594-602.
46. Gocheva V., Wang H.W., Gadea B.B., Shree T., Hunter K.E., Garfall A.L., Berman T., Joyce J.A. IL-4 induces cathepsin protease activity in tumor-associated macrophages to promote cancer growth and invasion. Genes Dev. 2010, 24:241-255.
47. Mathew R., Karantza-Wadsworth V., White E. Role of autophagy in cancer. Nat. Rev. Cancer 2007, 7:961-967.
48. Repnik U., Turk B. Lysosomal-mitochondrial cross-talk during cell death. Mitochondrion 2010, 10:662-669.
49. Rubinsztein D.C. The roles of intracellular protein-degradation pathways in neurodegeneration. Nature 2006, 443:780-786.
50. Schultz M.L., Tecedor L., Chang M., Davidson B.L. Clarifying lysosomal storage diseases. Trends Neurosci. 2011, 34:401-410.
51. Zhang L., Sheng R., Qin Z. The lysosome and neurodegenerative diseases. Acta Biochim. Biophys. Sin. (Shanghai) 2009, 41:437-445.
52. Kirkegaard T., Roth A.G., Petersen N.H., Mahalka A.K., Olsen O.D., Moilanen I., Zylicz A., Knudsen J., Sandhoff K., Arenz C., Kinnunen P.K., Nylandsted J., Jaattela M. Hsp70 stabilizes lysosomes and reverts Niemann-Pick disease-associated lysosomal pathology. Nature 2010, 463:549-553.