Autophagy induced by cathepsin S inhibition induces early ROS production, oxidative DNA damage, and cell death via xanthine oxidase

Free Radical Biology and Medicine

Volumn 65, Issue , 2013, Pages 1473-1486

  Huang, Chien Chang ^a   Chen, Kuo Li ^a   Cheung, Chun Hei Antonio ^b   Chang, Jang Yang ^a,b,c  

^a NATIONAL HEALTH RESEARCH INSTITUTES   (Taiwan)

^b NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

^c NATIONAL CHENG KUNG UNIVERSITY HOSPITAL   (Taiwan)

Author keywords

Autophagy; Cathepsin S; DNA damage; Early ROS; Xanthine oxidase

Indexed keywords

ATG7 PROTEIN; AUTOPHAGY PROTEIN 5; AUTOPHAGY PROTEIN 7; CATHEPSIN S; CELL DNA; CELL PROTEIN; LC3 PROTEIN; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG; WORTMANNIN; XANTHINE OXIDASE;

APOPTOSIS; ARTICLE; AUTOPHAGY; AUTOSOME; CANCER CELL CULTURE; CELL DEATH; CONTROLLED STUDY; DNA DAMAGE; ENZYME INDUCTION; ENZYME INHIBITION; FEMALE; GENE SILENCING; HUMAN; HUMAN CELL; INTRACELLULAR SIGNALING; LYSOSOME; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN FUNCTION; REGULATORY MECHANISM;

2′,7′-DICHLOROFLUORESCEIN DIACETATE; 3-MA; 3-METHYLADENINE; ACIDIC VESICULAR ORGANELLES; AUTOPHAGY; AVOS; BAF; BAFILOMYCIN A1; CATHEPSIN S; CHLOROQUINE; CQ; DCFH-DA; DHR; DIHYDROETHIDIUM; DIHYDRORHODAMINE; DNA DAMAGE; EARLY ROS; HE; LTR; LYSOTRACKER RED; N-ACETYL-L-CYSTEINE; NAC; REACTIVE OXYGEN SPECIES; ROS; V-ATPASE; VACUOLAR-TYPE H(+)-ATPASE; XANTHINE OXIDASE; XO;

ADENINE; ANDROSTADIENES; ANTIGEN PRESENTATION; APOPTOSIS; AUTOPHAGY; CATHEPSINS; CELL LINE, TUMOR; CELL SURVIVAL; DNA DAMAGE; HUMANS; MICROTUBULE-ASSOCIATED PROTEINS; PHOSPHATIDYLINOSITOL 3-KINASES; PROTEIN KINASE INHIBITORS; REACTIVE OXYGEN SPECIES; RNA INTERFERENCE; RNA, SMALL INTERFERING; UBIQUITIN-ACTIVATING ENZYMES; XANTHINE OXIDASE;

EID: 84890440316     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2013.07.020     Document Type: Article

References (72)

1. M.M. Mohamed, and B.F. Sloane Cysteine cathepsins: multifunctional enzymes in cancer Nat. Rev. Cancer 6 2006 764 775
2. C. Driessen, R.A. Bryant, A.M. Lennon-Dumenil, J.A. Villadangos, P.W. Bryant, G.P. Shi, H.A. Chapman, and H.L. Ploegh Cathepsin S controls the trafficking and maturation of MHC class II molecules in dendritic cells J. Cell Biol. 147 1999 775 790
3. G.P. Shi, J.A. Villadangos, G. Dranoff, C. Small, L. Gu, K.J. Haley, R. Riese, H.L. Ploegh, and H.A. Chapman Cathepsin S required for normal MHC class II peptide loading and germinal center development Immunity 10 1999 197 206
4. S. Kenig, M.B. Alonso, M.M. Mueller, and T.T. Lah Glioblastoma and endothelial cells cross-talk, mediated by SDF-1, enhances tumour invasion and endothelial proliferation by increasing expression of cathepsins B, S, and MMP-9 Cancer Lett. 289 2010 53 61
5. 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
6. A.K. Clark, R. Wodarski, F. Guida, O. Sasso, and M. Malcangio Cathepsin S release from primary cultured microglia is regulated by the P2X7 receptor Glia 58 2010 1710 1726
7. 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
8. 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
9. J.A. Gormley, S.M. Hegarty, A. O'Grady, M.R. Stevenson, R.E. Burden, H.L. Barrett, C.J. Scott, J.A. Johnston, R.H. Wilson, E.W. Kay, P.G. Johnston, and S.A. Olwill The role of cathepsin S as a marker of prognosis and predictor of chemotherapy benefit in adjuvant CRC: a pilot study Br. J. Cancer 105 2011 1487 1494
10. V. Gocheva, W. Zeng, D. Ke, D. Klimstra, T. Reinheckel, C. Peters, D. Hanahan, and J.A. Joyce Distinct roles for cysteine cathepsin genes in multistage tumorigenesis Genes Dev. 20 2006 543 556
11. P.L. Fernandez, X. Farre, A. Nadal, E. Fernandez, N. Peiro, B.F. Sloane, G.P. Shi, H.A. Chapman, E. Campo, and A. Cardesa Expression of cathepsins B and S in the progression of prostate carcinoma Int. J. Cancer 95 2001 51 55
12. C. Lindahl, M. Simonsson, A. Bergh, E. Thysell, H. Antti, M. Sund, and P. Wikstrom Increased levels of macrophage-secreted cathepsin S during prostate cancer progression in TRAMP mice and patients Cancer Genomics Proteomics 6 2009 149 159
13. J. Xu, D. Li, Z. Ke, R. Liu, G. Maubach, and L. Zhuo Cathepsin S is aberrantly overexpressed in human hepatocellular carcinoma Mol. Med. Rep 2 2009 713 718
14. L. Paraoan, D. Gray, P. Hiscott, M. Garcia-Finana, B. Lane, B. Damato, I. Grierson, and S Cathepsin and its inhibitor cystatin C: imbalance in uveal melanoma Front. Biosci. 14 2009 2504 2513
15. T. Flannery, S. McQuaid, C. McGoohan, R.S. McConnell, G. McGregor, M. Mirakhur, P. Hamilton, J. Diamond, G. Cran, B. Walker, C. Scott, L. Martin, D. Ellison, C. Patel, C. Nicholson, D. Mendelow, D. McCormick, and P.G. Johnston Cathepsin S expression: an independent prognostic factor in glioblastoma tumours - a pilot study Int. J. Cancer 119 2006 854 860
16. T. Flannery, D. Gibson, M. Mirakhur, S. McQuaid, C. Greenan, A. Trimble, B. Walker, D. McCormick, and P.G. Johnston The clinical significance of cathepsin S expression in human astrocytomas Am. J. Pathol. 163 2003 175 182
17. B. Wang, J. Sun, S. Kitamoto, M. Yang, A. Grubb, H.A. Chapman, R. Kalluri, and G.P. Shi Cathepsin S controls angiogenesis and tumor growth via matrix-derived angiogenic factors J. Biol. Chem 281 2006 6020 6029
18. G.P. Shi, G.K. Sukhova, M. Kuzuya, Q. Ye, J. Du, Y. Zhang, J.H. Pan, M.L. Lu, X.W. Cheng, A. Iguchi, S. Perrey, A.M. Lee, H.A. Chapman, and P. Libby Deficiency of the cysteine protease cathepsin S impairs microvessel growth Circ. Res. 92 2003 493 500
19. J. Arnlov, and S. Cathepsin as a biomarker: where are we now and what are the future challenges? Biomark. Med 6 2012 9 11
20. A. Lee-Dutra, D.K. Wiener, and S. Sun Cathepsin S inhibitors: 2004-2010 Expert Opin. Ther. Pat. 21 2011 311 337
21. J.C. Chen, B.J. Uang, P.C. Lyu, J.Y. Chang, K.J. Liu, C.C. Kuo, H.P. Hsieh, H.C. Wang, C.S. Cheng, Y.H. Chang, M.D. Chang, W.S. Chang, and C.C. Lin Design and synthesis of alpha-ketoamides as cathepsin S inhibitors with potential applications against tumor invasion and angiogenesis J. Med. Chem. 53 2010 4545 4549
22. B.T. Elie, V. Gocheva, T. Shree, S.A. Dalrymple, L.J. Holsinger, and J.A. Joyce Identification and pre-clinical testing of a reversible cathepsin protease inhibitor reveals anti-tumor efficacy in a pancreatic cancer model Biochimie 92 2010 1618 1624
23. H.F. Kwok, R.J. Buick, D. Kuehn, J.A. Gormley, D. Doherty, T.J. Jaquin, A. McClurg, C. Ward, T. Byrne, J. Jaworski, K.L. Leung, P. Snoddy, C. McAnally, R.E. Burden, B. Gray, J. Lowry, I. Sermadiras, N. Gruszka, N. Courtenay-Luck, A. Kissenpfennig, C.J. Scott, J.A. Johnston, and S.A. Olwill Antibody targeting of cathepsin S induces antibody-dependent cellular cytotoxicity Mol. Cancer 10 2011 147
24. C. Ward, D. Kuehn, R.E. Burden, J.A. Gormley, T.J. Jaquin, M. Gazdoiu, D. Small, R. Bicknell, J.A. Johnston, C.J. Scott, and S.A. Olwill Antibody targeting of cathepsin S inhibits angiogenesis and synergistically enhances anti-VEGF PLoS One 5 2010 e12543
25. R.E. Burden, J.A. Gormley, T.J. Jaquin, D.M. Small, D.J. Quinn, S.M. Hegarty, C. Ward, B. Walker, J.A. Johnston, S.A. Olwill, and C.J. Scott Antibody-mediated inhibition of cathepsin S blocks colorectal tumor invasion and angiogenesis Clin. Cancer Res. 15 2009 6042 6051
26. K.L. Chen, W.S. Chang, C.H. Cheung, C.C. Lin, C.C. Huang, Y.N. Yang, C.P. Kuo, C.C. Kuo, Y.H. Chang, K.J. Liu, C.M. Wu, and J.Y. Chang Targeting cathepsin S induces tumor cell autophagy via the EGFR-ERK signaling pathway Cancer Lett. 317 2011 89 98
27. P. Codogno, and A.J. Meijer Autophagy and signaling: their role in cell survival and cell death Cell Death Differ. 12 Suppl. 2 2005 1509 1518
28. L. Xue, G.C. Fletcher, and A.M. Tolkovsky Autophagy is activated by apoptotic signalling in sympathetic neurons: an alternative mechanism of death execution Mol. Cell. Neurosci. 14 1999 180 198
29. S. Fulda Autophagy and cell death Autophagy 8 2012 1250 1251
30. D. Denton, S. Nicolson, and S. Kumar Cell death by autophagy: facts and apparent artefacts Cell Death Differ. 19 2012 87 95
31. R. Scherz-Shouval, E. Shvets, E. Fass, H. Shorer, L. Gil, and Z. Elazar Reactive oxygen species are essential for autophagy and specifically regulate the activity of Atg4 EMBO J. 26 2007 1749 1760
32. R.A. Kirkland, R.M. Adibhatla, J.F. Hatcher, and J.L. Franklin Loss of cardiolipin and mitochondria during programmed neuronal death: evidence of a role for lipid peroxidation and autophagy Neuroscience 115 2002 587 602
33. I. Kissova, M. Deffieu, and V. Samokhvalov Velours, G.; Bessoule, J. J.; Manon, S.; Camougrand, N. Lipid oxidation and autophagy in yeast Free Radic. Biol. Med. 41 2006 1655 1661
34. M. Djavaheri-Mergny, M. Amelotti, J. Mathieu, F. Besancon, C. Bauvy, S. Souquere, G. Pierron, and P. Codogno NF-kappaB activation represses tumor necrosis factor-alpha-induced autophagy J. Biol. Chem. 281 2006 30373 30382
35. T. Kirisako, Y. Ichimura, H. Okada, Y. Kabeya, N. Mizushima, T. Yoshimori, M. Ohsumi, T. Takao, T. Noda, and Y. Ohsumi The reversible modification regulates the membrane-binding state of Apg8/Aut7 essential for autophagy and the cytoplasm to vacuole targeting pathway J. Cell Biol. 151 2000 263 276
36. I. Tanida, T. Ueno, and E. Kominami LC3 conjugation system in mammalian autophagy Int. J. Biochem. Cell Biol. 36 2004 2503 2518
37. Y. Kabeya, N. Mizushima, T. Ueno, A. Yamamoto, T. Kirisako, T. Noda, E. Kominami, Y. Ohsumi, and T. Yoshimori LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing EMBO J. 19 2000 5720 5728
38. J. Huang, V. Canadien, G.Y. Lam, B.E. Steinberg, M.C. Dinauer, M.A. Magalhaes, M. Glogauer, S. Grinstein, and J.H. Brumell Activation of antibacterial autophagy by NADPH oxidases Proc. Natl. Acad. Sci. USA 106 2009 6226 6231
39. R. Scherz-Shouval, and Z. Elazar ROS, mitochondria and the regulation of autophagy Trends Cell Biol. 17 2007 422 427
40. M.B. Azad, Y. Chen, and S.B. Gibson Regulation of autophagy by reactive oxygen species (ROS): implications for cancer progression and treatment Antioxid. Redox Signal. 11 2009 777 790
41. C.H. Wong, K.B. Iskandar, S.K. Yadav, J.L. Hirpara, T. Loh, and S. Pervaiz Simultaneous induction of non-canonical autophagy and apoptosis in cancer cells by ROS-dependent ERK and JNK activation PLoS One 5 2010 e9996
42. B. Kalyanaraman, V. Darley-Usmar, K.J. Davies, P.A. Dennery, H.J. Forman, M.B. Grisham, G.E. Mann, K. Moore, and L.J. Roberts 2nd; Ischiropoulos, H. Measuring reactive oxygen and nitrogen species with fluorescent probes: challenges and limitations Free Radic. Biol. Med. 52 2012 1 6
43. H.H. Chen, Y.T. Chen, Y.W. Huang, H.J. Tsai, and C.C. Kuo 4-Ketopinoresinol, a novel naturally occurring ARE activator, induces the Nrf2/HO-1 axis and protects against oxidative stress-induced cell injury via activation of PI3K/AKT signaling Free Radic. Biol. Med. 52 2012 1054 1066
44. M.H. Shin, Y.J. Moon, J.E. Seo, Y. Lee, K.H. Kim, and J.H. Chung Reactive oxygen species produced by NADPH oxidase, xanthine oxidase, and mitochondrial electron transport system mediate heat shock-induced MMP-1 and MMP-9 expression Free Radic. Biol. Med. 44 2008 635 645
45. H. Zhao, S. Kalivendi, H. Zhang, J. Joseph, K. Nithipatikom, J. Vasquez-Vivar, and B. Kalyanaraman Superoxide reacts with hydroethidine but forms a fluorescent product that is distinctly different from ethidium: potential implications in intracellular fluorescence detection of superoxide Free Radic. Biol. Med. 34 2003 1359 1368
46. J. Lee, J.S. Hwang, I.S. Hwang, J. Cho, E. Lee, Y. Kim, and D.G. Lee Coprisin-induced antifungal effects in Candida albicans correlate with apoptotic mechanisms Free Radic. Biol. Med. 52 2012 2302 2311
47. N. Mizushima, Y. Ohsumi, and T. Yoshimori Autophagosome formation in mammalian cells Cell Struct. Funct. 27 2002 421 429
48. V.N. Pivtoraiko, S.L. Stone, K.A. Roth, and J.J. Shacka Oxidative stress and autophagy in the regulation of lysosome-dependent neuron death Antioxid. Redox Signal. 11 2009 481 496
49. T. Kurz, A. Terman, and U.T. Brunk Autophagy, ageing and apoptosis: the role of oxidative stress and lysosomal iron Arch. Biochem. Biophys. 462 2007 220 230
50. D. Shao, S. Oka, C.D. Brady, J. Haendeler, P. Eaton, and J. Sadoshima Redox modification of cell signaling in the cardiovascular system J. Mol. Cell. Cardiol. 52 2012 550 558
51. L.B. Becker, T.L. vanden Hoek, Z.H. Shao, C.Q. Li, and P.T. Schumacker Generation of superoxide in cardiomyocytes during ischemia before reperfusion Am. J. Physiol. 277 1999 H2240 H2246
52. S.G. Carriedo, S.L. Sensi, H.Z. Yin, and J.H. Weiss AMPA exposures induce mitochondrial Ca(2+) overload and ROS generation in spinal motor neurons in vitro J. Neurosci. 20 2000 240 250
53. 2+-dependent generation of mitochondrial reactive oxygen species serves as a signal for poly(ADP-ribose) polymerase-1 activation during glutamate excitotoxicity J. Physiol 585 2007 741 758
54. J. Pan, M. She, Z.X. Xu, L. Sun, and S.C. Yeung Farnesyltransferase inhibitors induce DNA damage via reactive oxygen species in human cancer cells Cancer Res. 65 2005 3671 3681
55. G.Y. Lam, J. Huang, and J.H. Brumell The many roles of NOX2 NADPH oxidase-derived ROS in immunity Semin. Immunopathol. 32 2010 415 430
56. Z. Liu, and M.J. Lenardo Reactive oxygen species regulate autophagy through redox-sensitive proteases Dev. Cell 12 2007 484 485
57. I. Mitroulis, I. Kourtzelis, K. Kambas, S. Rafail, A. Chrysanthopoulou, M. Speletas, and K. Ritis Regulation of the autophagic machinery in human neutrophils Eur. J. Immunol. 40 2010 1461 1472
58. A. Bidani, B.S. Reisner, A.K. Haque, J. Wen, R.E. Helmer, D.M. Tuazon, and T.A. Heming Bactericidal activity of alveolar macrophages is suppressed by V-ATPase inhibition Lung 178 2000 91 104
59. J.K. Murphy, and H.J. Forman Effects of sodium and proton pump activity on respiratory burst and pH regulation of rat alveolar macrophages Am. J. Physiol 264 1993 L523 L532
60. C.J. Swallow, S. Grinstein, R.A. Sudsbury, and O.D. Rotstein Relative roles of Na+/H+ exchange and vacuolar-type H+ ATPases in regulating cytoplasmic pH and function in murine peritoneal macrophages J. Cell. Physiol. 157 1993 453 460
61. A. Yamamoto, Y. Tagawa, T. Yoshimori, Y. Moriyama, R. Masaki, and Y. Tashiro Bafilomycin A1 prevents maturation of autophagic vacuoles by inhibiting fusion between autophagosomes and lysosomes in rat hepatoma cell line, H-4-II-E cells Cell Struct. Funct. 23 1998 33 42
62. T. Yoshimori, A. Yamamoto, Y. Moriyama, M. Futai, and Y. Tashiro Bafilomycin A1, a specific inhibitor of vacuolar-type H(+)-ATPase, inhibits acidification and protein degradation in lysosomes of cultured cells J. Biol. Chem. 266 1991 17707 17712
63. M.P. Murphy How mitochondria produce reactive oxygen species Biochem. J. 417 2009 1 13
64. W.M. Nauseef Biological roles for the NOX family NADPH oxidases J. Biol. Chem. 283 2008 16961 16965
65. A. Orient, A. Donko, A. Szabo, T.L. Leto, and M. Geiszt Novel sources of reactive oxygen species in the human body Nephrol. Dial. Transplant. 22 2007 1281 1288
66. W.K. Alderton, C.E. Cooper, and R.G. Knowles Nitric oxide synthases: structure, function and inhibition Biochem. J. 357 2001 593 615
67. S. Pou, W.S. Pou, D.S. Bredt, S.H. Snyder, and G.M. Rosen Generation of superoxide by purified brain nitric oxide synthase J. Biol. Chem. 267 1992 24173 24176
68. E.C. Viel, K. Benkirane, D. Javeshghani, R.M. Touyz, and E.L. Schiffrin Xanthine oxidase and mitochondria contribute to vascular superoxide anion generation in DOCA-salt hypertensive rats Am. J. Physiol. Heart Circ. Physiol 295 2008 H281 H288
69. C.E. Griguer, C.R. Oliva, E.E. Kelley, G.I. Giles, J.R. Lancaster Jr, and G.Y. Gillespie Xanthine oxidase-dependent regulation of hypoxia-inducible factor in cancer cells Cancer Res. 66 2006 2257 2263
70. A.I. Bernstein, S.P. Garrison, G.P. Zambetti, and K.L. O'Malley 6-OHDA generated ROS induces DNA damage and p53- and PUMA-dependent cell death Mol. Neurodegener 6 2011 2
71. M.D. Evans, M. Dizdaroglu, and M.S. Cooke Oxidative DNA damage and disease: induction, repair and significance Mutat. Res. 567 2004 1 61
72. C.C. Huang, and W.S. Chang Cooperation between NRF-2 and YY-1 transcription factors is essential for triggering the expression of the PREPL-C2ORF34 bidirectional gene pair BMC Mol. Biol 10 2009 67