Lysosomal cysteine peptidases - Molecules signaling tumor cell death and survival

Seminars in Cancer Biology

Volumn 35, Issue , 2015, Pages 168-179

  Pišlar, Anja ^a   Perišić Nanut, Milica ^b   Kos, Janko ^a,b  

^a UNIVERSITY OF LJUBLJANA   (Slovenia)

^b JO EF STEFAN INSTITUTE   (Slovenia)

Author keywords

Cancer; Cathepsins; Lysosomal peptidases; Signaling

Indexed keywords

CATHEPSIN B; CATHEPSIN H; CATHEPSIN K; CATHEPSIN L; CATHEPSIN S; CATHEPSIN X; DIPEPTIDYL PEPTIDASE I; LYSOSOMAL CYSTEINE PEPTIDASE; MITOGEN ACTIVATED PROTEIN KINASE; PEPTIDASE; PROTEIN KINASE B; STRESS ACTIVATED PROTEIN KINASE; TUMOR PROTEIN; UNCLASSIFIED DRUG; CATHEPSIN; CYSTEINE PROTEINASE;

APOPTOSIS; AUTOPHAGY; CANCER PROGNOSIS; CARCINOGENESIS; CELL ADHESION; CELL DEATH; CELL INVASION; CELL MIGRATION; CELL PROLIFERATION; CELL SURVIVAL; CELLULAR DISTRIBUTION; ENDOCYTOSIS; EPITHELIAL MESENCHYMAL TRANSITION; HUMAN; NONHUMAN; PROTEIN LOCALIZATION; PROTEIN TARGETING; REVIEW; SIGNAL TRANSDUCTION; TUMOR CELL; UPREGULATION; ANIMAL; CELL TRANSFORMATION; DISEASE COURSE; ENDOSOME; GENETICS; LYSOSOME; METABOLISM; NEOPLASMS; PATHOLOGY; PROGNOSIS;

ANIMALS; CATHEPSINS; CELL DEATH; CELL SURVIVAL; CELL TRANSFORMATION, NEOPLASTIC; CYSTEINE ENDOPEPTIDASES; DISEASE PROGRESSION; ENDOSOMES; HUMANS; LYSOSOMES; NEOPLASMS; PROGNOSIS; SIGNAL TRANSDUCTION;

EID: 84948716123     PISSN: 1044579X     EISSN: 10963650     Source Type: Journal    
DOI: 10.1016/j.semcancer.2015.08.001     Document Type: Review

References (175)

1. Rawlings N.D., Barrett A.J., Bateman A. MEROPS: the database of proteolytic enzymes, their substrates and inhibitors. Nucleic Acids Res. 2012, 40(Database issue):D343-D350.
2. Turk B. Targeting proteases: successes, failures and future prospects. Nat. Rev. Drug Discov. 2006, 5(9):785-799.
3. Barry Z.T., Platt M.O. Cathepsin S cannibalism of cathepsin K as a mechanism to reduce type I collagen degradation. J. Biol. Chem. 2012, 287(33):27723-27730.
4. Kwok H.F., et al. Antibody targeting of cathepsin S induces antibody-dependent cellular cytotoxicity. Mol. Cancer 2011, 10:147.
5. Mohamed M.M., Sloane B.F. Cysteine cathepsins: multifunctional enzymes in cancer. Nat. Rev. Cancer 2006, 6(10):764-775.
6. Mirkovic B., et al. Nitroxoline impairs tumor progression in vitro and in vivo by regulating cathepsin B activity. Oncotarget 2015.
7. Gocheva V., Joyce J.A. Cysteine cathepsins and the cutting edge of cancer invasion. Cell Cycle 2007, 6(1):60-64.
8. Kos J., Mitrovic A., Mirkovic B. The current stage of cathepsin B inhibitors as potential anticancer agents. Future Med. Chem. 2014, 6(11):1355-1371.
9. Huotari J., Helenius A. Endosome maturation. EMBO J. 2011, 30(17):3481-3500.
10. Conner S.D., Schmid S.L. Regulated portals of entry into the cell. Nature 2003, 422(6927):37-44.
11. Doherty G.J., McMahon H.T. Mechanisms of endocytosis. Annu. Rev. Biochem 2009, 78:857-902.
12. Luzio J.P., Pryor P.R., Bright N.A. Lysosomes: fusion and function. Nat. Rev. Mol. Cell Biol. 2007, 8(8):622-632.
13. Kiss A.L. Caveolae and the regulation of endocytosis. Adv. Exp. Med. Biol. 2012, 729:14-28.
14. Swanson J.A. Shaping cups into phagosomes and macropinosomes. Nat. Rev. Mol. Cell Biol. 2008, 9(8):639-649.
15. Donaldson J.G., Porat-Shliom N., Cohen L.A. Clathrin-independent endocytosis: a unique platform for cell signaling and PM remodeling. Cell. Signal. 2009, 21(1):1-6.
16. Engqvist-Goldstein A.E., Drubin D.G. Actin assembly and endocytosis: from yeast to mammals. Annu. Rev. Cell Dev. Biol. 2003, 19:287-332.
17. Grant B.D., Donaldson J.G. Pathways and mechanisms of endocytic recycling. Nat. Rev. Mol. Cell Biol. 2009, 10(9):597-608.
18. Gruenberg J. The endocytic pathway: a mosaic of domains. Nat. Rev. Mol. Cell Biol. 2001, 2(10):721-730.
19. Rink J., et al. Rab conversion as a mechanism of progression from early to late endosomes. Cell 2005, 122(5):735-749.
20. Geuze H.J., et al. Sorting of mannose 6-phosphate receptors and lysosomal membrane proteins in endocytic vesicles. J. Cell Biol. 1988, 107(6 Pt. 2):2491-2501.
21. Futter C.E., et al. Multivesicular endosomes containing internalized EGF-EGF receptor complexes mature and then fuse directly with lysosomes. J. Cell Biol. 1996, 132(6):1011-1023.
22. Murphy R.F. Maturation models for endosome and lysosome biogenesis. Trends Cell Biol. 1991, 1(4):77-82.
23. Repnik U., Cesen M.H., Turk B. The endolysosomal system in cell death and survival. Cold Spring Harb. Perspect. Biol. 2013, 5(1):a008755.
24. Ciechanover A. Intracellular protein degradation: from a vague idea through the lysosome and the ubiquitin-proteasome system and onto human diseases and drug targeting. Rambam Maimonides Med. J. 2012, 3(1):e0001.
25. Repnik U., et al. Lysosomes and lysosomal cathepsins in cell death. Biochim. Biophys. Acta 2012, 1824(1):22-33.
26. Roberts R. Lysosomal cysteine proteases: structure, function and inhibition of cathepsins. Drug News Perspect. 2005, 18(10):605-614.
27. Stoka V., Turk B., Turk V. Lysosomal cysteine proteases: structural features and their role in apoptosis. IUBMB Life 2005, 57(4-5):347-353.
28. Chwieralski C.E., Welte T., Buhling F. Cathepsin-regulated apoptosis. Apoptosis 2006, 11(2):143-149.
29. Turk V., et al. Cysteine cathepsins: from structure, function and regulation to new frontiers. Biochim. Biophys. Acta 2012, 1824(1):68-88.
30. Turk V., Turk B., Turk D. Lysosomal cysteine proteases: facts and opportunities. EMBO J. 2001, 20(17):4629-4633.
31. Roshy S., Sloane B.F., Moin K. Pericellular cathepsin B and malignant progression. Cancer Metastasis Rev. 2003, 22(2-3):271-286.
32. Brix K., et al. Cysteine cathepsins: cellular roadmap to different functions. Biochimie 2008, 90(2):194-207.
33. Blott E.J., Griffiths G.M. Secretory lysosomes. Nat. Rev. Mol. Cell Biol. 2002, 3(2):122-131.
34. Braulke T., Bonifacino J.S. Sorting of lysosomal proteins. Biochim. Biophys. Acta 2009, 1793(4):605-614.
35. Dell'Angelica E.C., Payne G.S. Intracellular cycling of lysosomal enzyme receptors: cytoplasmic tails' tales. Cell 2001, 106(4):395-398.
36. Ghosh P., Dahms N.M., Kornfeld S. Mannose 6-phosphate receptors: new twists in the tale. Nat. Rev. Mol. Cell Biol. 2003, 4(3):202-212.
37. Castonguay A.C., Olson L.J., Dahms N.M. Mannose 6-phosphate receptor homology (MRH) domain-containing lectins in the secretory pathway. Biochim. Biophys. Acta 2011, 1810(9):815-826.
38. Doray B., et al. Cooperation of GGAs and AP-1 in packaging MPRs at the trans-Golgi network. Science 2002, 297(5587):1700-1703.
39. Rodriguez-Gabin A.G., et al. Transport of mannose-6-phosphate receptors from the trans-Golgi network to endosomes requires Rab31. Exp. Cell Res. 2009, 315(13):2215-2230.
40. Canuel M., Libin Y., Morales C.R. The interactomics of sortilin: an ancient lysosomal receptor evolving new functions. Histol. Histopathol. 2009, 24(4):481-492.
41. Arighi C.N., et al. Role of the mammalian retromer in sorting of the cation-independent mannose 6-phosphate receptor. J. Cell Biol. 2004, 165(1):123-133.
42. Seaman M.N. Cargo-selective endosomal sorting for retrieval to the Golgi requires retromer. J. Cell Biol. 2004, 165(1):111-122.
43. Barbero P., Bittova L., Pfeffer S.R. Visualization of Rab9-mediated vesicle transport from endosomes to the trans-Golgi in living cells. J. Cell Biol. 2002, 156(3):511-518.
44. Jadot M., et al. Characterization of the signal for rapid internalization of the bovine mannose 6-phosphate/insulin-like growth factor-II receptor. J. Biol. Chem. 1992, 267(16):11069-11077.
45. Storch S., Braulke T. Multiple C-terminal motifs of the 46-kDa mannose 6-phosphate receptor tail contribute to efficient binding of medium chains of AP-2 and AP-3. J. Biol. Chem. 2001, 276(6):4298-4303.
46. Brady R.O. Enzyme replacement for lysosomal diseases. Annu. Rev. Med. 2006, 57:283-296.
47. Saftig P., Klumperman J. Lysosome biogenesis and lysosomal membrane proteins: trafficking meets function. Nat. Rev. Mol. Cell Biol. 2009, 10(9):623-635.
48. Reczek D., et al. LIMP-2 is a receptor for lysosomal mannose-6-phosphate-independent targeting of beta-glucocerebrosidase. Cell 2007, 131(4):770-783.
49. Turk V., Kos J., Turk B. Cysteine cathepsins (proteases) - on the main stage of cancer?. Cancer Cell 2004, 5(5):409-410.
50. Turk B., Turk D., Turk V. Protease signalling: the cutting edge. EMBO J. 2012, 31(7):1630-1643.
51. Repnik U., et al. Cysteine cathepsins activate ELR chemokines and inactivate non-ELR chemokines. J. Biol. Chem. 2015, 290(22):13800-13811.
52. Perisic Nanut M., et al. Cysteine cathepsins as regulators of the cytotoxicity of NK and T cells. Front. Immunol. 2014, 5:616.
53. Goulet B., et al. 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 2004, 14(2):207-219.
54. Duncan E.M., et al. Cathepsin L proteolytically processes histone H3 during mouse embryonic stem cell differentiation. Cell 2008, 135(2):284-294.
55. Fonovic M., Turk B. Cysteine cathepsins and their potential in clinical therapy and biomarker discovery. Proteom. Clin. Appl. 2014, 8(5-6):416-426.
56. Aits S., Jaattela M. Lysosomal cell death at a glance. J. Cell Sci. 2013, 126(Pt. 9):1905-1912.
57. Boya P., Kroemer G. Lysosomal membrane permeabilization in cell death. Oncogene 2008, 27(50):6434-6451.
58. Cavallo-Medved D., et al. Mutant K-ras regulates cathepsin B localization on the surface of human colorectal carcinoma cells. Neoplasia 2003, 5(6):507-519.
59. Cheng X.W., et al. Localization of cysteine protease, cathepsin S, to the surface of vascular smooth muscle cells by association with integrin alphanubeta3. Am. J. Pathol. 2006, 168(2):685-694.
60. Kos J., et al. Intracellular signaling by cathepsin X: molecular mechanisms and diagnostic and therapeutic opportunities in cancer. Semin. Cancer Biol. 2015, 31:76-83.
61. Hanahan D., Weinberg R.A. The hallmarks of cancer. Cell 2000, 100(1):57-70.
62. Tan G.J., et al. Cathepsins mediate tumor metastasis. World J. Biol. Chem. 2013, 4(4):91-101.
63. Nomura T., Katunuma N. Involvement of cathepsins in the invasion, metastasis and proliferation of cancer cells. J. Med. Invest. 2005, 52(1-2):1-9.
64. Aggarwal N., Sloane B.F. Cathepsin B: multiple roles in cancer. Proteom. Clin. Appl. 2014, 8(5-6):427-437.
65. Berdowska I. Cysteine proteases as disease markers. Clin. Chim. Acta 2004, 342(1-2):41-69.
66. Jedeszko C., Sloane B.F. Cysteine cathepsins in human cancer. Biol. Chem. 2004, 385(11):1017-1027.
67. Bian B., et al. Cathepsin B promotes colorectal tumorigenesis, cell invasion, and metastasis. Mol. Carcinog. 2015.
68. Sloane B.F., Dunn J.R., Honn K.V. Lysosomal cathepsin B: correlation with metastatic potential. Science 1981, 212(4499):1151-1153.
69. Chen Q., et al. Detection of cathepsin B, cathepsin L, cystatin C, urokinase plasminogen activator and urokinase plasminogen activator receptor in the sera of lung cancer patients. Oncol. Lett. 2011, 2(4):693-699.
70. Premzl A., et al. Intracellular and extracellular cathepsin B facilitate invasion of MCF-10A neoT cells through reconstituted extracellular matrix in vitro. Exp. Cell Res. 2003, 283(2):206-214.
71. Bao W., et al. Silencing of cathepsin B suppresses the proliferation and invasion of endometrial cancer. Oncol. Rep. 2013, 30(2):723-730.
72. Rousselet N., et al. Inhibition of tumorigenicity and metastasis of human melanoma cells by anti-cathepsin L single chain variable fragment. Cancer Res. 2004, 64(1):146-151.
73. Levicar N., et al. Selective suppression of cathepsin L by antisense cDNA impairs human brain tumor cell invasion in vitro and promotes apoptosis. Cancer Gene Ther. 2003, 10(2):141-151.
74. Zhang W., et al. Overexpression of cysteine cathepsin L is a marker of invasion and metastasis in ovarian cancer. Oncol. Rep. 2014, 31(3):1334-1342.
75. Brindle N.R., et al. Deficiency for the cysteine protease cathepsin L impairs Myc-induced tumorigenesis in a mouse model of pancreatic neuroendocrine cancer. PLOS ONE 2015, 10(4):e0120348.
76. Fernandez P.L., et al. Expression of cathepsins B and S in the progression of prostate carcinoma. Int. J. Cancer 2001, 95(1):51-55.
77. Ogbomo S.M., et al. 177Lu-labeled HPMA copolymers utilizing cathepsin B and S cleavable linkers: synthesis, characterization and preliminary in vivo investigation in a pancreatic cancer model. Nucl. Med. Biol. 2013, 40(5):606-617.
78. Yang Y., et al. Cathepsin S mediates gastric cancer cell migration and invasion via a putative network of metastasis-associated proteins. J. Proteome Res. 2010, 9(9):4767-4778.
79. Gormley J.A., et al. The role of cathepsin S as a marker of prognosis and predictor of chemotherapy benefit in adjuvant CRC: a pilot study. Br. J. Cancer 2011, 105(10):1487-1494.
80. Xu J., et al. Cathepsin S is aberrantly overexpressed in human hepatocellular carcinoma. Mol. Med. Rep. 2009, 2(5):713-718.
81. Paraoan L., et al. Cathepsin S and its inhibitor cystatin C: imbalance in uveal melanoma. Front. Biosci. (Landmark Ed.) 2009, 14:2504-2513.
82. Flannery T., et al. Cathepsin S expression: an independent prognostic factor in glioblastoma tumours - a pilot study. Int. J. Cancer 2006, 119(4):854-860.
83. Flannery T., et al. The clinical significance of cathepsin S expression in human astrocytomas. Am. J. Pathol. 2003, 163(1):175-182.
84. Zhang L., Wang H., Xu J. Cathepsin S as a cancer target. Neoplasma 2015, 62(1):16-26.
85. Ryschich E., et al. Molecular fingerprinting and autocrine growth regulation of endothelial cells in a murine model of hepatocellular carcinoma. Cancer Res. 2006, 66(1):198-211.
86. Wang B., et al. Cathepsin S controls angiogenesis and tumor growth via matrix-derived angiogenic factors. J. Biol. Chem. 2006, 281(9):6020-6029.
87. Small D.M., et al. Cathepsin S from both tumor and tumor-associated cells promote cancer growth and neovascularization. Int. J. Cancer 2013, 133(9):2102-2112.
88. Gocheva V., et al. Deletion of cathepsin H perturbs angiogenic switching, vascularization and growth of tumors in a mouse model of pancreatic islet cell cancer. Biol. Chem. 2010, 391(8):937-945.
89. Jevnikar Z., et al. Cathepsin H mediates the processing of talin and regulates migration of prostate cancer cells. J. Biol. Chem. 2013, 288(4):2201-2209.
90. Nagler D.K., et al. Up-regulation of cathepsin X in prostate cancer and prostatic intraepithelial neoplasia. Prostate 2004, 60(2):109-119.
91. Krueger S., et al. Up-regulation of cathepsin X in Helicobacter pylori gastritis and gastric cancer. J. Pathol. 2005, 207(1):32-42.
92. Jechorek D., et al. Characterization of cathepsin X in colorectal cancer development and progression. Pathol. Res. Pract. 2014, 210(12):822-829.
93. Kraus S., et al. Cellular senescence induced by cathepsin X downregulation. Eur. J. Cell Biol. 2011, 90(8):678-686.
94. Wang J., et al. Overexpression of cathepsin Z contributes to tumor metastasis by inducing epithelial-mesenchymal transition in hepatocellular carcinoma. PLoS ONE 2011, 6(9):e24967.
95. Levicar N., Nuttall R.K., Lah T.T. Proteases in brain tumour progression. Acta Neurochir. (Wien) 2003, 145(9):825-838.
96. Kos J., Lah T.T. Cysteine proteinases and their endogenous inhibitors: target proteins for prognosis, diagnosis and therapy in cancer (review). Oncol. Rep. 1998, 5(6):1349-1361.
97. Mai J., et al. Human procathepsin B interacts with the annexin II tetramer on the surface of tumor cells. J. Biol. Chem. 2000, 275(17):12806-12812.
98. Kobayashi H., et al. Effects of membrane-associated cathepsin B on the activation of receptor-bound prourokinase and subsequent invasion of reconstituted basement membranes. Biochim. Biophys. Acta 1993, 1178(1):55-62.
99. Cavallo-Medved D., et al. Caveolin-1 mediates the expression and localization of cathepsin B, pro-urokinase plasminogen activator and their cell-surface receptors in human colorectal carcinoma cells. J. Cell Sci. 2005, 118(Pt. 7):1493-1503.
100. Rozhin J., et al. Membrane-associated cathepsin L: a role in metastasis of melanomas. Biochem. Biophys. Res. Commun. 1989, 164(1):556-561.
101. Nascimento F.D., et al. Cathepsin X binds to cell surface heparan sulfate proteoglycans. Arch. Biochem. Biophys. 2005, 436(2):323-332.
102. Mort J.S., Recklies A.D., Poole A.R. Release of cathepsin B precursors from human and murine tumours. Prog. Clin. Biol. Res. 1985, 180:243-245.
103. Fonovic M., Turk B. Cysteine cathepsins and extracellular matrix degradation. Biochim. Biophys. Acta 2014, 1840(8):2560-2570.
104. Gocheva V., et al. Distinct roles for cysteine cathepsin genes in multistage tumorigenesis. Genes Dev. 2006, 20(5):543-556.
105. Ward C., et al. Antibody targeting of cathepsin S inhibits angiogenesis and synergistically enhances anti-VEGF. PLoS ONE 2010, 5(9).
106. Seftor R.E., et al. Cooperative interactions of laminin 5 gamma2 chain, matrix metalloproteinase-2, and membrane type-1-matrix/metalloproteinase are required for mimicry of embryonic vasculogenesis by aggressive melanoma. Cancer Res. 2001, 61(17):6322-6327.
107. Obermajer N., et al. Carboxypeptidase cathepsin X mediates beta2-integrin-dependent adhesion of differentiated U-937 cells. Exp. Cell Res. 2006, 312(13):2515-2527.
108. Colin C., et al. High expression of cathepsin B and plasminogen activator inhibitor type-1 are strong predictors of survival in glioblastomas. Acta Neuropathol. 2009, 118(6):745-754.
109. Singh N., et al. Plasma cathepsin L: a prognostic marker for pancreatic cancer. World J. Gastroenterol. 2014, 20(46):17532-17540.
110. Kos J., et al. Cathepsin S in tumours, regional lymph nodes and sera of patients with lung cancer: relation to prognosis. Br. J. Cancer 2001, 85(8):1193-1200.
111. Kageshita T., et al. Biochemical and immunohistochemical analysis of cathepsins B, H, L and D in human melanocytic tumours. Arch. Dermatol. Res. 1995, 287(3-4):266-272.
112. Frohlich E., et al. Activity, expression, and transcription rate of the cathepsins B, D, H, and L in cutaneous malignant melanoma. Cancer 2001, 91(5):972-982.
113. Zhang X., et al. Clinical significance of detection of cathepsin X and cystatin C in the sera of patients with lung cancer. Zhongguo Fei Ai Za Zhi 2013, 16(8):411-416.
114. Vizin T., et al. Cathepsin X in serum from patients with colorectal cancer: relation to prognosis. Radiol. Oncol. 2012, 46(3):207-212.
115. Vizin T., et al. Prognostic and predictive value of cathepsin X in serum from colorectal cancer patients. BMC Cancer 2014, 14:259.
116. Bianco R., et al. Key cancer cell signal transduction pathways as therapeutic targets. Eur. J. Cancer 2006, 42(3):290-294.
117. Kaplan D.R., Miller F.D. Signal transduction by the neurotrophin receptors. Curr. Opin. Cell Biol. 1997, 9(2):213-221.
118. Yarden Y., Sliwkowski M.X. Untangling the ErbB signalling network. Nat. Rev. Mol. Cell Biol. 2001, 2(2):127-137.
119. Authier F., et al. Negative regulation of epidermal growth factor signaling by selective proteolytic mechanisms in the endosome mediated by cathepsin B. J. Biol. Chem. 1999, 274(47):33723-33731.
120. Glogowska A., et al. Epidermal growth factor cytoplasmic domain affects ErbB protein degradation by the lysosomal and ubiquitin-proteasome pathway in human cancer cells. Neoplasia 2012, 14(5):396-409.
121. Navab R., et al. Inhibition of endosomal insulin-like growth factor-I processing by cysteine proteinase inhibitors blocks receptor-mediated functions. J. Biol. Chem. 2001, 276(17):13644-13649.
122. Authier F., Kouach M., Briand G. Endosomal proteolysis of insulin-like growth factor-I at its C-terminal D-domain by cathepsin B. FEBS Lett. 2005, 579(20):4309-4316.
123. Massague J. TGFbeta in cancer. Cell 2008, 134(2):215-230.
124. Yin M., et al. TGF-beta signaling, activated stromal fibroblasts, and cysteine cathepsins B and L drive the invasive growth of human melanoma cells. Am. J. Pathol. 2012, 181(6):2202-2216.
125. Kraus S., et al. IGF-I receptor phosphorylation is impaired in cathepsin X-deficient prostate cancer cells. Biol. Chem. 2012, 393(12):1457-1462.
126. Hiwasa T., et al. Inhibition of cathepsin L-induced degradation of epidermal growth factor receptors by c-Ha-ras gene products. Biochem. Biophys. Res. Commun. 1988, 151(1):78-85.
127. Reinheckel T., et al. The lysosomal cysteine protease cathepsin L regulates keratinocyte proliferation by control of growth factor recycling. J. Cell Sci. 2005, 118(Pt. 15):3387-3395.
128. Dennemarker J., et al. Deficiency for the cysteine protease cathepsin L promotes tumor progression in mouse epidermis. Oncogene 2010, 29(11):1611-1621.
129. Hafner A., Obermajer N., Kos J. gamma-Enolase C-terminal peptide promotes cell survival and neurite outgrowth by activation of the PI3K/Akt and MAPK/ERK signalling pathways. Biochem. J. 2012, 443(2):439-450.
130. Alapati K., et al. uPAR and cathepsin B-mediated compartmentalization of JNK regulates the migration of glioma-initiating cells. Stem Cell Res. 2014, 12(3):716-729.
131. Chen H., et al. Extracellular signal-regulated kinase signaling pathway regulates breast cancer cell migration by maintaining slug expression. Cancer Res. 2009, 69(24):9228-9235.
132. Tardy C., et al. Lysosomes and lysosomal proteins in cancer cell death (new players of an old struggle). Biochim. Biophys. Acta 2006, 1765(2):101-125.
133. Taylor R.C., Cullen S.P., Martin S.J. Apoptosis: controlled demolition at the cellular level. Nat. Rev. Mol. Cell Biol. 2008, 9(3):231-241.
134. Pop C., Salvesen G.S. Human caspases: activation, specificity, and regulation. J. Biol. Chem. 2009, 284(33):21777-21781.
135. Hengartner M.O. The biochemistry of apoptosis. Nature 2000, 407(6805):770-776.
136. Li H., et al. Cleavage of BID by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis. Cell 1998, 94(4):491-501.
137. Youle R.J., Strasser A. The BCL-2 protein family: opposing activities that mediate cell death. Nat. Rev. Mol. Cell Biol. 2008, 9(1):47-59.
138. Schotte P., et al. Cathepsin B-mediated activation of the proinflammatory caspase-11. Biochem. Biophys. Res. Commun. 1998, 251(1):379-387.
139. Vancompernolle K., et al. Atractyloside-induced release of cathepsin B, a protease with caspase-processing activity. FEBS Lett. 1998, 438(3):150-158.
140. Stoka V., et al. Lysosomal protease pathways to apoptosis. Cleavage of bid, not pro-caspases, is the most likely route. J. Biol. Chem. 2001, 276(5):3149-3157.
141. Vasiljeva O., Turk B. Dual contrasting roles of cysteine cathepsins in cancer progression: apoptosis versus tumour invasion. Biochimie 2008, 90(2):380-386.
142. Droga-Mazovec G., et al. Cysteine cathepsins trigger caspase-dependent cell death through cleavage of bid and antiapoptotic Bcl-2 homologues. J. Biol. Chem. 2008, 283(27):19140-19150.
143. Malla R., et al. Downregulation of uPAR and cathepsin B induces apoptosis via regulation of Bcl-2 and Bax and inhibition of the PI3K/Akt pathway in gliomas. PLoS ONE 2010, 5(10):e13731.
144. Teller A., et al. Dysregulation of apoptotic signaling pathways by interaction of RPLP0 and cathepsin X/Z in gastric cancer. Pathol. Res. Pract. 2015, 211(1):62-70.
145. Elmore S. Apoptosis: a review of programmed cell death. Toxicol. Pathol. 2007, 35(4):495-516.
146. Brunner T., et al. Fas (CD95/Apo-1) ligand regulation in T cell homeostasis, cell-mediated cytotoxicity and immune pathology. Semin. Immunol. 2003, 15(3):167-176.
147. Trapani J.A., Smyth M.J. Functional significance of the perforin/granzyme cell death pathway. Nat. Rev. Immunol. 2002, 2(10):735-747.
148. Adrain C., Murphy B.M., Martin S.J. Molecular ordering of the caspase activation cascade initiated by the cytotoxic T lymphocyte/natural killer (CTL/NK) protease granzyme B. J. Biol. Chem. 2005, 280(6):4663-4673.
149. Waterhouse N.J., et al. A central role for Bid in granzyme B-induced apoptosis. J. Biol. Chem. 2005, 280(6):4476-4482.
150. Lieberman J., Fan Z. Nuclear war: the granzyme A-bomb. Curr. Opin. Immunol. 2003, 15(5):553-559.
151. Kummer J.A., et al. Expression of human recombinant granzyme A zymogen and its activation by the cysteine proteinase cathepsin C. J. Biol. Chem. 1996, 271(16):9281-9286.
152. Pham C.T., Ley T.J. Dipeptidyl peptidase I is required for the processing and activation of granzymes A and B in vivo. Proc. Natl. Acad. Sci. U. S. A. 1999, 96(15):8627-8632.
153. Sutton V.R., et al. Residual active granzyme B in cathepsin C-null lymphocytes is sufficient for perforin-dependent target cell apoptosis. J. Cell Biol. 2007, 176(4):425-433.
154. D'Angelo M.E., et al. Cathepsin H is an additional convertase of pro-granzyme B. J. Biol. Chem. 2010, 285(27):20514-20519.
155. Magister S., et al. Regulation of split anergy in natural killer cells by inhibition of cathepsins C and H and cystatin F. Oncotarget 2015, (advance publications).
156. Lu S.Z., Harrison-Findik D.D. Autophagy and cancer. World J. Biol. Chem. 2013, 4(3):64-70.
157. Klionsky D.J., Emr S.D. Autophagy as a regulated pathway of cellular degradation. Science 2000, 290(5497):1717-1721.
158. Kondo Y., et al. The role of autophagy in cancer development and response to therapy. Nat. Rev. Cancer 2005, 5(9):726-734.
159. Vivanco I., Sawyers C.L. The phosphatidylinositol 3-Kinase AKT pathway in human cancer. Nat. Rev. Cancer 2002, 2(7):489-501.
160. Ogier-Denis E., et al. Erk1/2-dependent phosphorylation of Galpha-interacting protein stimulates its GTPase accelerating activity and autophagy in human colon cancer cells. J. Biol. Chem. 2000, 275(50):39090-39095.
161. Shimizu S., et al. Autophagic cell death and cancer. Int. J. Mol. Sci. 2014, 15(2):3145-3153.
162. Huang C.C., et al. Autophagy induced by cathepsin S inhibition induces early ROS production, oxidative DNA damage, and cell death via xanthine oxidase. Free Radic. Biol. Med. 2013, 65:1473-1486.
163. Zhang L., et al. Inhibition of cathepsin S induces autophagy and apoptosis in human glioblastoma cell lines through ROS-mediated PI3K/AKT/mTOR/p70S6K and JNK signaling pathways. Toxicol. Lett. 2014, 228(3):248-259.
164. Chen K.L., et al. Targeting cathepsin S induces tumor cell autophagy via the EGFR-ERK signaling pathway. Cancer Lett. 2012, 317(1):89-98.
165. Bhoopathi P., et al. Cathepsin B facilitates autophagy-mediated apoptosis in SPARC overexpressed primitive neuroectodermal tumor cells. Cell Death Differ. 2010, 17(10):1529-1539.
166. Hsu K.F., et al. Cathepsin L mediates resveratrol-induced autophagy and apoptotic cell death in cervical cancer cells. Autophagy 2009, 5(4):451-460.
167. Garg M. Epithelial-mesenchymal transition - activating transcription factors - multifunctional regulators in cancer. World J. Stem Cells 2013, 5(4):188-195.
168. Kalluri R., Weinberg R.A. The basics of epithelial-mesenchymal transition. J. Clin. Invest. 2009, 119(6):1420-1428.
169. Kern U., et al. Lysosomal protein turnover contributes to the acquisition of TGFbeta-1 induced invasive properties of mammary cancer cells. Mol. Cancer 2015, 14:39.
170. Zhang Q., et al. Downregulation of cathepsin L suppresses cancer invasion and migration by inhibiting transforming growth factorbetamediated epithelialmesenchymal transition. Oncol. Rep. 2015, 33(4):1851-1859.
171. Bengsch F., et al. Cell type-dependent pathogenic functions of overexpressed human cathepsin B in murine breast cancer progression. Oncogene 2014, 33(36):4474-4484.
172. Ochieng J., Chaudhuri G. Cystatin superfamily. J. Health Care Poor Underserved 2010, 21(1 Suppl.):51-70.
173. Sadaghiani A.M., et al. Design, synthesis, and evaluation of in vivo potency and selectivity of epoxysuccinyl-based inhibitors of papain-family cysteine proteases. Chem. Biol. 2007, 14(5):499-511.
174. Loser R., Pietzsch J. Cysteine cathepsins: their role in tumor progression and recent trends in the development of imaging probes. Front. Chem. 2015, 3:37.
175. Langerholc T., et al. Inhibitory properties of cystatin F and its localization in U937 promonocyte cells. FEBS J. 2005, 272(6):1535-1545.