Cytosolic activation of cathepsins mediates parvovirus H-1-induced killing of cisplatin and TRAIL-resistant glioma cells

Journal of Virology

Volumn 81, Issue 8, 2007, Pages 4186-4198

  Di Piazza, Matteo ^a   Mader, Carmen ^a   Geletneky, Karsten ^b   Herrero Y Calle, Marta ^c   Weber, Ekkehard ^d   Schlehofer, Jörg ^a   Deleu, Laurent ^a   Rommelaere, Jean ^a  

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^b UNIVERSITY OF HEIDELBERG   (Germany)

^c UNIVERSITY OF FREIBURG   (Germany)

^d MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CATHEPSIN; CATHEPSIN B; CATHEPSIN L; CISPLATIN; CYSTATIN B; CYSTATIN C; PROTEIN BCL 2; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; ASTROCYTE; CONTROLLED STUDY; CYTOSOL; GLIOMA CELL; HUMAN; HUMAN CELL; MALIGNANT TRANSFORMATION; NONHUMAN; PARVOVIRUS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT;

ANIMALS; ANTINEOPLASTIC AGENTS; ASTROCYTES; BRAIN NEOPLASMS; CATHEPSIN B; CATHEPSINS; CELL DEATH; CISPLATIN; CYSTATINS; CYSTEINE ENDOPEPTIDASES; CYTOSOL; DISEASE MODELS, ANIMAL; DRUG RESISTANCE, NEOPLASM; ENZYME ACTIVATION; GLIOMA; H-1 PARVOVIRUS; HUMANS; LYSOSOMES; ONCOLYTIC VIROTHERAPY; RATS; RATS, INBRED WKY; RECOMBINANT PROTEINS; TNF-RELATED APOPTOSIS-INDUCING LIGAND; TUMOR CELLS, CULTURED;

ANIMALIA; H-1 PARVOVIRUS; RATTUS;

EID: 34247170947     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.02601-06     Document Type: Article

References (49)

1. Ahschuetz, A., T. Kehl, R. Geibig, B. Leuchs, J. Rommelaere, and A. Régnier-Vigoureux. 2006. Oncolytic murine autonomous parvovirus, a candidate vector for glioma gene therapy, is innocuous to normal and immunocompetent mouse glial cells. Cell Tissue Res. 325:423-436.
2. Antunes, F., E. Cadenas, and U. T. Brunk. 2001. Apoptosis induced by exposure to a low steady-state concentration of H2O2 is a consequence of lysosomal rupture. Biochem. J. 356:549-555.
3. Danial, N. N., and S. J. Korsmeyer. 2004. Cell death: critical control points. Cell 116:205-219.
4. Deiss, L. P., H. Galinka, H. Berissi, O. Cohen, and A, Kimchi. 1996. Cathepsin D protease mediates programmed cell death induced by interferon-gamma, Fas/APO-1 and TNF-alpha. EMBO J. 15:3861-3870.
5. Erdal, H., M. Berndtsson, J. Castro, U. Brunk, M. C. Shoshan, and S. Linder. 2005. Induction of lysosomal membrane permeabilization by compounds that activate p53-independent apoptosis. Proc. Natl. Acad. Sci. USA 102:192-197.
6. Farr, G. A., L. Zhang, and P. Tattersall. 2005. Parvoviral virions deploy a capsid-tethered lipolytic enzyme to breach the endosomal membrane during cell entry. Proc. Natl. Acad. Sci. USA 102:17148-17153.
7. Foghsgaard, L., D. Wissing, D. Mauch, U. Lademann, L. Bastholm, M. Boes, F. Elling, M. Leist, and M. Jaattela. 2001. Cathepsin B acts as a dominant execution protease in tumor cell apoptosis induced by tumor necrosis factor. J. Cell Biol. 153:999-1010.
8. Fulda, S., E. Meyer, C. Friesen, S. A. Susin, G. Kroemer, and K. M. Debatin. 2001. Cell type specific involvement of death receptor and mitochondrial pathways in drug-induced apoptosis. Oncogene 20:1063-1075.
9. Gille, L., and H. Nohl. 2000. The existence of a lysosomal redox chain and the role of ubiquinone. Arch. Biochem. Biophys. 375:347-354.
10. Guicciardi, M. E., J. Deussing, H. Miyoshi, S. F. Bronk, P. A. Svingen, C. Peters, S. H. Kaufmann, and G. J. Gores. 2000. Cathepsin B contributes to TNF-alpha-mediated hepatocyte apoptosis by promoting mitochondrial release of cytochrome c. J. Clin. Investig. 106:1127-1137.
11. Guicciardi, M. E., M. Leist, and G. J. Gores. 2004. Lysosomes in cell death. Oncogene 23:2881-2890.
12. Hanahan, D., and R. A. Weinberg. 2000. The hallmarks of cancer. Cell 100:57-70.
13. Hao, C., F. Beguinot, G. Condorelli, A. Trencia, E. G. Van Meir, V. W. Yong, I. F. Parney, W. H. Roa, and K. C. Petruk. 2001. Induction and intracellular regulation of tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) mediated apoptosis in human malignant glioma cells. Cancer Res. 61:1162-1170.
14. Herold-Mende, C, H. H. Steiner, T. Andl, D. Riede, A. Buttler, C. Reisser, N. E. Fusenig, and M. M. Mueller. 1999. Expression and functional significance of vascular endothelial growth factor receptors in human tumor cells. Lab. Investig. 79:1573-1582.
15. Herrero y Calle, M., J. J. Cornells, C. Herold-Mende, J. Rommelaere, J. R. Schlehofer, and K. Geletneky. 2004. Parvovirus H-1 infection of human glioma cells leads to complete viral replication and efficient cell killing. Int. J. Cancer 109:76-84.
16. Hirt, B. 1967. Selective extraction of polyoma DNA from infected mouse cell cultures. J. Mol. Biol. 26:365-369.
17. Hishita, T., S. Tada-Oikawa, K. Tohyama, Y. Miura, T. Nishihara, Y. Tohyama, Y. Yoshida, T. Uchiyama, and S. Kawanishi. 2001. Caspase-3 activation by lysosomal enzymes in cytochrome c-independent apoptosis in myelodysplastic syndrome-derived cell line P39. Cancer Res. 61:2878-2884.
18. Hsu, T. C., W. J. Wu, M. C. Chen, and G. J. Tsay. 2004. Human parvovirus B19 non-structural protein (NS1) induces apoptosis through mitochondria cell death pathway in COS-7 cells. Scand. J. Infect. Dis. 36:570-577.
19. Jiang, X., and X. Wang. 2004. Cytochrome C-mediated apoptosis. Annu. Rev. Biochem. 73:87-106.
20. Johansson, A. C., H. Steen, K. Ollinger, and K. Roberg. 2003. Cathepsin D mediates cytochrome c release and caspase activation in human fibroblast apoptosis induced by staurosporine. Cell Death Differ. 10:1253-1259.
21. Kartalou, M., and J. M. Essigmann. 2001. Mechanisms of resistance to cisplatin. Mutat. Res. 478:23-43.
22. Kwant, M. M., and P. C. van der Vliet. 1980. Differential effect of aphidicolin on adenovirus DNA synthesis and cellular DNA synthesis. Nucleic Acids Res. 8:3993-4008.
23. Lavrik, I., A. Golks, and P. H. Krammer. 2005. Death receptor signaling. J. Cell Sci. 118:265-267.
24. Liu, N., S. M. Raja, F. Zazzeroni, S. S. Metkar, R. Shah, M. Zhang, Y. Wang, D. Bromine, W. A. Russin, J. C. Lee, M. E. Peter, C. J. Froelich, G. Franzoso, and P. G. Ashton-Rickardt. 2003. NF-κB protects from the lysosomal pathway of cell death. EMBO J. 22:5313-5322.
25. Longley, D. B., and P. G. Johnston. 2005. Molecular mechanisms of drug resistance. J. Pathol. 205:275-292.
26. Maher, E. A., F. B. Furnari, R. M. Bachoo, D. H. Rowitch, D. N. Louis, W. K. Cavenee, and R. A. DePinho. 2001. Malignant glioma: genetics and biology of a grave matter. Genes Dev. 15:1311-1333.
27. Moehler, M, B. Blechacz, N. Weiskopt M. Zeidler, W. Stremmel, J. Rommelaere, P. R. Galle, and J. J. Cornelis. 2001. Effective infection, apoptotic cell killing and gene transfer of human hepatoma cells but not primary hepatocytes by parvovirus H1 and derived vectors. Cancer Gene Ther. 8:158-167.
28. Mohanam, S., S. L. Jasti, S. R. Kondraganti, N. Chandrasekar, S. S. Lakka, Y. Kin, G. N. Fuller, A. W. Yung, A. P. Kyritsis, D. H. Dinh, W. C. Olivero, M. Gujrati, F. Ali-Osman, and J. S. Rao. 2001. Down-regulation of cathepsin B expression impairs the invasive and tumorigenic potential of human glioblastoma cells. Oncogene 20:3665-3673.
29. Nagaraj, N. S., N. Vigneswaran, and W. Zacharias. 2006. Cathepsin B mediates TRAIL-induced apoptosis in oral cancer cells. J. Cancer Res. Clin. Oncol. 132:171-183.
30. Nakabayashi, H., M. Kara, and K. Shimuzu. 2005. Clinicopathologic significance of cystatin C expression in gliomas. Hum. Pathol. 36:1008-1015.
31. Pan, G., J. Ni, Y. F. Wei, G. Yu, R. Gentz, and V. M. Dixit. 1997. An antagonist decoy receptor and a death domain-containing receptor for TRAIL. Science 277:815-818.
32. Peter, M, E., and P. H. Krammer. 1998. Mechanisms of CD95 (APO-1/Fas)-mediated apoptosis. Curr. Opin. Immunol. 10:545-551.
33. Ran, Z., B. Rayet, J. Rommelaere, and S. Faisst. 1999. Parvovirus H-1-induced cell death: influence of intracellular NAD consumption on the regulation of necrosis and apoptosis. Virus Res. 65:161-174.
34. Rawlings, N. D., D. P. Tolle, and A. J. Barrett. 2004. Evolutionary families of peptidase inhibitors. Biochem. J. 378:705-716.
35. Rayet, B., J. A. Lopez-Guerrero, J. Rommelaere, and C. Dinsart. 1998. Induction of programmed cell death by parvovirus H-1 in U937 cells: connection with the tumor necrosis factor alpha signalling pathway. J. Virol. 72:8893-8903.
36. Rempel, S. A., M. L. Rosenblum, T. Mikkelsen, P. S. Yan, K. D. Ellis, W. A. Golembieski, M. Sameni, J. Rozhin, G. Ziegler, and B. F. Sloane. 1994. Cathepsin B expression and localization in glioma progression and invasion. Cancer Res. 54:6027-6031.
37. Rhode, S. L. 1974. Replication process of the Parvovirus H-1. III. Factors affecting H-1 RF DNA synthesis. J. Virol. 14:791-801.
38. Rommelaere, J., and J. J. Cornelis. 1991. Antineoplastic activity of parvoviruses. J. Virol. Methods 33:233-251.
39. Sambrook, J., and D. W. Russell. 2001. Molecular cloning: a laboratory manual, 3rd ed., vol. 1. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
40. Scaffidi, C., S. Fulda, A. Srinivasan, C. Friesen, F. Li, K. J. Tomaselli, K. M. Debatin, P. H. Krammer, and M. E. Peter. 1998. Two CD95 (APO-1/Fas) signaling pathways. EMBO J. 17:1675-1687.
41. Suikkanen, S., M. Antila, A. Jaatinen, M. Vihinen-Ranta, and M. Vuento. 2003. Release of canine parvovirus from endocytic vesicles. Virology 316:267-280.
42. Vanacker, J. M., and J. Rommelaere. 1995. Non-structural proteins of autonomous parvoviruses: from cellular effects to molecular mechanisms. Semin. Virol. 6:291-297.
43. Wrzesinski, C., L. Tesfay, N. Salome, J. C. Jauniaux, J. Rommelaere, J. Cornells, and C, Dinsart. 2003. Chimeric and pseudotyped parvoviruses minimize the contamination of recombinant stocks with replication-competent viruses and identify a DNA sequence that restricts parvovirus H-1 in mouse cells. J. Virol. 77:3851-3858.
44. Xiao, C., B. F. Yang, N, Asadi, F. Beguinot, and C. Hao. 2002. Tumor necrosis factor-related apoptosis-inducing ligand-induced death-inducing signaling complex and its modulation by c-FLIP and PED/PEA-15 in glioma cells. J. Biol. Chem. 277:25020-25025.
45. Yuan, X. M., W. Li, H. Dalen, J. Lotem, R. Kama, L. Sachs, and U. T. Brunk. 2002. Lysosomal destabilization in p53-induced apoptosis. Proc. Natl. Acad. Sci. USA 99:6286-6291.
46. Zádori, Z., J. Szelei, M. C. Lacoste, Y. Li, S. Gariepy, P. Raymond, M. Allaire, I. R. Nabi, and P. Tijssen. 2001. A viral phospholipase A2 is required for parvovirus infectivity. Dev. Cell 1:291-302.
47. Zhang, R., T. L. Tremblay, A. McDermid, P. Thibault, and D. Stanimirovic. 2003. Identification of differentially expressed proteins in human glioblastoma cell lines and tumors. Glia 42:194-208.
48. Zhao, M., U. T. Brunk, and J. W. Eaton. 2001. Delayed oxidant-induced cell death involves activation of phospholipase A2. FEBS Lett. 509:399-404.
49. Zhu, Y., and L. F. Parada. 2002. The molecular and genetic basis of neurological tumours. Nat. Rev. Cancer 2:616-626.