Through its nonstructural protein NS1, parvovirus H-1 induces apoptosis via accumulation of reactive oxygen species

Journal of Virology

Volumn 84, Issue 12, 2010, Pages 5909-5922

  Hristov, Georgi ^a   Krämer, Melanie ^a   Li, Junwei ^a   El Andaloussi, Nazim ^a   Mora, Rodrigo ^a   Daeffler, Laurent ^a   Zentgraf, Hanswalter ^a   Rommelaere, Jean ^a   Marchini, Antonio ^a  

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; CASPASE 9; DOUBLE STRANDED DNA; NONSTRUCTURAL PROTEIN 1; REACTIVE OXYGEN METABOLITE;

APOPTOSIS; ARTICLE; CELL CYCLE ARREST; CELL CYCLE G2 PHASE; CELL PROLIFERATION; CELL STRAIN HEK293; CELL VIABILITY; CONTROLLED STUDY; CYTOLYSIS; CYTOTOXICITY; DNA DAMAGE; DOUBLE STRANDED DNA BREAK; ENZYME ACTIVATION; FEMALE; HELA CELL; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; NONHUMAN; PARVOVIRUS; PRIORITY JOURNAL; PROTEIN EXPRESSION; WILD TYPE;

APOPTOSIS; CELL CYCLE; CELL LINE; DNA DAMAGE; H-1 PARVOVIRUS; HUMANS; PARVOVIRIDAE INFECTIONS; REACTIVE OXYGEN SPECIES; VIRAL NONSTRUCTURAL PROTEINS;

H-1 PARVOVIRUS; RATTUS;

EID: 77952737333     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.01797-09     Document Type: Article

References (49)

1. Armstrong, J. S., and M. Whiteman. 2007. Measurement of reactive oxygen species in cells and mitochondria. Methods Cell Biol. 80:355-377.
2. Atkuri, K. R., J. J. Mantovani, and L. A. Herzenberg. 2007. N-acetylcysteine - a safe antidote for cysteine/glutathione deficiency. Curr. Opin. Pharmacol. 7:355-359.
3. Bashir, T., R. Horlein, J. Rommelaere, and K. Willwand. 2000. Cyclin A activates the DNA polymerase delta-dependent elongation machinery in vitro: a parvovirus DNA replication model. Proc. Natl. Acad. Sci. U. S. A. 97:5522-5527.
4. Bashir, T., J. Rommelaere, and C. Cziepluch. 2001. In vivo accumulation of cyclin A and cellular replication factors in autonomous parvovirus minute virus of mice-associated replication bodies. J. Virol. 75:4394-4398.
5. Bodendorf, U., C. Cziepluch, J. C. Jauniaux, J. Rommelaere, and N. Salome. 1999. Nuclear export factor CRM1 interacts with nonstructural proteins NS2 from parvovirus minute virus of mice. J. Virol. 73:7769-7779.
6. Caillet-Fauquet, P., M. Perros, A. Brandenburger, P. Spegelaere, and J. Rommelaere. 1990. Programmed killing of human cells by means of an inducible clone of parvoviral genes encoding non-structural proteins. EMBO J. 9:2989-2995.
7. Cornelis, J. J., L. Deleu, U. Kock, and J. Rommelaere. 2006. Parvovirus oncosuppression, p. 365-378. In J. R. Kerr, M. E. Bloom, R. M. Linden, and C. R. Parrish (ed.), Parvoviruses. Hodder Arnold E. Ltd., London, United Kingdom.
8. Cotmore, S. F., and P. Tattersall. 1986. Organization of nonstructural genes of the autonomous parvovirus minute virus of mice. J. Virol. 58:724-732.
9. Cotmore, S. F., and P. Tattersall. 2007. Parvoviral host range and cell entry mechanisms. Adv. Virus Res. 70:183-232.
10. Cziepluch, C., E. Kordes, R. Poirey, A. Grewenig, J. Rommelaere, and J. C. Jauniaux. 1998. Identification of a novel cellular TPR-containing protein, SGT, that interacts with the nonstructural protein NS1 of parvovirus H-1. J. Virol. 72:4149-4156.
11. Cziepluch, C., S. Lampel, A. Grewenig, C. Grund, P. Lichter, and J. Rommelaere. 2000. H-1 parvovirus-associated replication bodies: a distinct virus-induced nuclear structure. J. Virol. 74:4807-4815.
12. Daeffler, L., R. Horlein, J. Rommelaere, and J. P. Nuesch. 2003. Modulation of minute virus of mice cytotoxic activities through site-directed mutagenesis within the NS coding region. J. Virol. 77:12466-12478.
13. Davy, C., and J. Doorbar. 2007. G2/M cell cycle arrest in the life cycle of viruses. Virology 368:219-226.
14. Deleu, L., F. Fuks, D. Spitkovsky, R. Horlein, S. Faisst, and J. Rommelaere. 1998. Opposite transcriptional effects of cyclic AMP-responsive elements in confluent or p27KIP-overexpressing cells versus serum-starved or growing cells. Mol. Cell. Biol. 18:409-419.
15. Deshmane, S. L., R. Mukerjee, S. Fan, L. Del Valle, C. Michiels, T. Sweet, I. Rom, K. Khalili, J. Rappaport, S. Amini, and B. E. Sawaya. 2009. Activation of the oxidative stress pathway by HIV-1 Vpr leads to induction of hypoxiainducible factor 1alpha expression. J. Biol. Chem. 284:11364-11373.
16. Di Piazza, M., C. Mader, K. Geletneky, Y. C. M. Herrero, E. Weber, J. Schlehofer, L. Deleu, and J. Rommelaere. 2007. Cytosolic activation of cathepsins mediates parvovirus H-1-induced killing of cisplatin and TRAIL-resistant glioma cells. J. Virol. 81:4186-4198.
17. Faisst, S., D. Guittard, A. Benner, J. Y. Cesbron, J. R. Schlehofer, J. Rommelaere, and T. Dupressoir. 1998. Dose-dependent regression of HeLa cellderived tumours in SCID mice after parvovirus H-1 infection. Int. J. Cancer 75:584-589.
18. Genovese, C., D. Trani, M. Caputi, and P. P. Claudio. 2006. Cell cycle control and beyond: emerging roles for the retinoblastoma gene family. Oncogene 25:5201-5209.
19. Gruhne, B., R. Sompallae, D. Marescotti, S. A. Kamranvar, S. Gastaldello, and M. G. Masucci. 2009. The Epstein-Barr virus nuclear antigen-1 promotes genomic instability via induction of reactive oxygen species. Proc. Natl. Acad. Sci. U. S. A. 106:2313-2318.
20. Kang, S. M., S. J. Kim, J. H. Kim, W. Lee, G. W. Kim, K. H. Lee, K. Y. Choi, and J. W. Oh. 2009. Interaction of hepatitis C virus core protein with Hsp60 triggers the production of reactive oxygen species and enhances TNF-alpha-mediated apoptosis. Cancer Lett. 279:230-237.
21. Kavouras, J. H., E. Prandovszky, K. Valyi-Nagy, S. K. Kovacs, V. Tiwari, M. Kovacs, D. Shukla, and T. Valyi-Nagy. 2007. Herpes simplex virus type 1 infection induces oxidative stress and the release of bioactive lipid peroxidation by-products in mouse P19N neural cell cultures. J. Neurovirol. 13: 416-425.
22. Kinner, A., W. Wu, C. Staudt, and G. Iliakis. 2008. Gamma-H2AX in recognition and signaling of DNA double-strand breaks in the context of chromatin. Nucleic Acids Res. 36:5678-5694.
23. Lobrich, M., and P. A. Jeggo. 2007. The impact of a negligent G2/M checkpoint on genomic instability and cancer induction. Nat. Rev. Cancer 7:861-869.
24. Machida, K., K. T. Cheng, C. K. Lai, K. S. Jeng, V. M. Sung, and M. M. Lai. 2006. Hepatitis C virus triggers mitochondrial permeability transition with production of reactive oxygen species, leading to DNA damage and STAT3 activation. J. Virol. 80:7199-7207.
25. Mathew, R., C. M. Karp, B. Beaudoin, N. Vuong, G. Chen, H. Y. Chen, K. Bray, A. Reddy, G. Bhanot, C. Gelinas, R. S. Dipaola, V. Karantza-Wadsworth, and E. White. 2009. Autophagy suppresses tumorigenesis through elimination of p62. Cell 137:1062-1075.
26. Meister, G., M. Landthaler, L. Peters, P. Y. Chen, H. Urlaub, R. Luhrmann, and T. Tuschl. 2005. Identification of novel argonaute-associated proteins. Curr. Biol. 15:2149-2155.
27. Moffatt, S., N. Yaegashi, K. Tada, N. Tanaka, and K. Sugamura. 1998. Human parvovirus B19 nonstructural (NS1) protein induces apoptosis in erythroid lineage cells. J. Virol. 72:3018-3028.
28. 1 phase. J. Virol. 77:2915-2921.
29. Morita, E., and K. Sugamura. 2002. Human parvovirus B19-induced cell cycle arrest and apoptosis. Springer Semin. Immunopathol. 24:187-199.
30. Morita, E., K. Tada, H. Chisaka, H. Asao, H. Sato, N. Yaegashi, and K. Sugamura. 2001. Human parvovirus B19 induces cell cycle arrest at G(2) phase with accumulation of mitotic cyclins. J. Virol. 75:7555-7563.
31. Nakamura, H., H. Masutani, and J. Yodoi. 2002. Redox imbalance and its control in HIV infection. Antioxid. Redox Signal. 4:455-464.
32. Nakashima, A., E. Morita, S. Saito, and K. Sugamura. 2004. Human Parvovirus B19 nonstructural protein transactivates the p21/WAF1 through Sp1. Virology 329:493-504.
33. Nuesch, J. P., S. Lachmann, and J. Rommelaere. 2005. Selective alterations of the host cell architecture upon infection with parvovirus minute virus of mice. Virology 331:159-174.
34. Nuesch, J. P., and J. Rommelaere. 2007. A viral adaptor protein modulating casein kinase II activity induces cytopathic effects in permissive cells. Proc. Natl. Acad. Sci. U. S. A. 104:12482-12487.
35. Ohshima, T., M. Iwama, Y. Ueno, F. Sugiyama, T. Nakajima, A. Fukamizu, and K. Yagami. 1998. Induction of apoptosis in vitro and in vivo by H-1 parvovirus infection. J. Gen. Virol. 79(Pt. 12):3067-3071.
36. Op De Beeck, A., F. Anouja, S. Mousset, J. Rommelaere, and P. Caillet- Fauquet. 1995. The nonstructural proteins of the autonomous parvovirus minute virus of mice interfere with the cell cycle, inducing accumulation in G2. Cell Growth Differ. 6:781-787.
37. Op De Beeck, A., and P. Caillet-Fauquet. 1997. The NS1 protein of the autonomous parvovirus minute virus of mice blocks cellular DNA replication: a consequence of lesions to the chromatin? J. Virol. 71:5323-5329.
38. Op De Beeck, A., J. Sobczak-Thepot, H. Sirma, F. Bourgain, C. Brechot, and P. Caillet-Fauquet. 2001. NS1- and minute virus of mice-induced cell cycle arrest: involvement of p53 and p21(cip1). J. Virol. 75:11071-11078.
39. Plesca, D., M. E. Crosby, D. Gupta, and A. Almasan. 2007. E2F4 function in G2: maintaining G2-arrest to prevent mitotic entry with damaged DNA. Cell Cycle 6:1147-1152.
40. Raj, K., P. Ogston, and P. Beard. 2001. Virus-mediated killing of cells that lack p53 activity. Nature 412:914-917.
41. 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.
42. 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 signaling pathway. J. Virol. 72:8893-8903.
43. Saudan, P., J. Vlach, and P. Beard. 2000. Inhibition of S-phase progression by adeno-associated virus Rep78 protein is mediated by hypophosphorylated pRb. EMBO J. 19:4351-4361. (Pubitemid 30623746)
44. Scherz-Shouval, R., and Z. Elazar. 2007. ROS, mitochondria and the regulation of autophagy. Trends Cell Biol. 17:422-427.
45. Schmidt, M., S. Afione, and R. M. Kotin. 2000. Adeno-associated virus type 2 Rep78 induces apoptosis through caspase activation independently of p53. J. Virol. 74:9441-9450.
46. Ueno, Y., T. Harada, H. Iseki, T. Ohshima, F. Sugiyama, and K. Yagami. 2001. Propagation of rat parvovirus in thymic lymphoma cell line C58(NT)d and subsequent appearance of a resistant cell clone after lytic infection. J. Virol. 75:3965-3970. (Pubitemid 32246405)
47. Wang, Y. 2008. Bulky DNA lesions induced by reactive oxygen species. Chem. Res. Toxicol. 21:276-281.
48. Winocour, E., M. F. Callaham, and E. Huberman. 1988. Perturbation of the cell cycle by adeno-associated virus. Virology 167:393-399. (Pubitemid 19037133)
49. Wrzesinski, C., L. Tesfay, N. Salome, J. C. Jauniaux, J. Rommelaere, J. Cornelis, 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. (Pubitemid 36297305)