Apoptin nucleocytoplasmic shuttling is required for cell type-specific localization, apoptosis, and recruitment of the anaphase-promoting complex/cyclosome to PML bodies

Journal of Virology

Volumn 80, Issue 15, 2006, Pages 7535-7545

  Heilman, Destin W ^a   Teodoro, Jose G ^a   Green, Michael R ^a,b  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^b Prog in Gene Funct and Expression   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APOPTIN; PROMYELOCYTIC LEUKEMIA PROTEIN; VIRUS PROTEIN;

ANAPHASE; APOPTOSIS; ARTICLE; CELL TYPE; CIRCOVIRIDAE; FLUORESCENCE MICROSCOPY; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOFLUORESCENCE; IMMUNOPRECIPITATION; NUCLEAR EXPORT SIGNAL; NUCLEAR LOCALIZATION SIGNAL; NUCLEOCYTOPLASMIC TRANSPORT; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION;

ACTIVE TRANSPORT, CELL NUCLEUS; APOPTOSIS; CAPSID PROTEINS; CARCINOMA, NON-SMALL-CELL LUNG; CELL LINE, TRANSFORMED; CELL NUCLEUS; CHICKEN ANEMIA VIRUS; CYTOPLASM; FIBROBLASTS; HUMANS; INTRANUCLEAR INCLUSION BODIES; LUNG NEOPLASMS; MICROSCOPY, FLUORESCENCE; NUCLEAR EXPORT SIGNALS; NUCLEAR LOCALIZATION SIGNALS; SKIN; TUMOR CELLS, CULTURED; UBIQUITIN-PROTEIN LIGASE COMPLEXES;

CHICKEN ANEMIA VIRUS;

EID: 33746215103     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.02741-05     Document Type: Article

References (55)

1. Agathanggelou, A., W. N. Cooper, and F. Latif. 2005. Role of the Ras-association domain family 1 tumor suppressor gene in human cancers. Cancer Res. 65:3497-3508.
2. Anton, L. C., U. Schubert, I. Bacik, M. F. Princiotta, P. A. Wearsch, J. Gibbs, P. M. Day, C. Realini, M. C. Rechsteiner, J. R. Bennink, and J. W. Yewdell. 1999. Intracellular localization of proteasomal degradation of a viral antigen. J. Cell Biol. 146:113-124.
3. Bacchetti, S., and F. L. Graham. 1993. Inhibition of cell proliferation by an adenovirus vector expressing the human wild-type p53 protein. Int. J. Oncol. 3:781-788.
4. Berger, J., C. Aepinus, M. Dobrovnik, B. Fleckenstein, J. Hauber, and E. Bohnlein. 1991. Mutational analysis of functional domains in the HIV-1 Rev trans-regulatory protein. Virology 183:630-635.
5. Bernardi, R., and P. P. Pandolfi. 2003. Role of PML and the PML-nuclear body in the control of programmed cell death. Oncogene 22:9048-9057.
6. Counter, C. M., A. A. Avilion, C. E. LeFeuvre, N. G. Stewart, C. W. Greider, C. B. Harley, and S. Bacchetti. 1992. Telomere shortening associated with chromosome instability is arrested in immortal cells which express telomerase activity. EMBO J. 11:1921-1929.
7. Danen-Van Oorschot, A. A., D. F. Fischer, J. M. Grimbergen, B. Klein, S. Zhuang, J. H. Falkenburg, C. Backendorf, P. H. Quax, A. J. Van der Eb, and M. H. Noteborn. 1997. Apoptin induces apoptosis in human transformed and malignant cells but not in normal cells. Proc. Natl. Acad. Sci. USA 94:5843-5847.
8. Danen-Van Oorschot, A. A., A. J. van der Eb, and M. H. Noteborn. 1999. BCL-2 stimulates Apoptin-induced apoptosis. Adv. Exp. Med. Biol. 457:245-249.
9. Danen-Van Oorschot, A. A., Y. H. Zhang, S. R. Leliveld, J. L. Rohn, M. C. Seelen, M. W. Bolk, A. Van Zon, S. J. Erkeland, J. P. Abrahams, D. Mumberg, and M. H. Noteborn. 2003. Importance of nuclear localization of apoptin for tumor-specific induction of apoptosis. J. Biol. Chem. 278:27729-27736.
10. Dellaire, G., and D. P. Bazett-Jones. 2004. PML nuclear bodies: dynamic sensors of DNA damage and cellular stress. Bioessays 26:963-977.
11. de Stanchina, E., E. Querido, M. Narita, R. V. Davuluri, P. P. Pandolfi, G. Ferbeyre, and S. W. Lowe. 2004. PML is a direct p53 target that modulates p53 effector functions. Mol. Cell 13:523-535.
12. Dieckhoff, P., M. Bolte, Y. Sancak, G. H. Braus, and S. Irniger. 2004. Smt3/SUMO and Ubc9 are required for efficient APC/C-mediated proteolysis in budding yeast. Mol. Microbiol. 51:1375-1387.
13. Gorlich, D., N. Pante, U. Kutay, U. Aebi, and F. R. Bischoff. 1996. Identification of different roles for RanGDP and RanGTP in nuclear protein import. EMBO J. 15:5584-5594.
14. Heilman, D. W., M. R. Green, and J. G. Teodoro. 2005. The anaphase promoting complex: a critical target for viral proteins and anti-cancer drugs. Cell Cycle 4:560-563.
15. Henderson, B. R., and A. Eleftheriou. 2000. A comparison of the activity, sequence specificity, and CRM1-dependence of different nuclear export signals. Exp. Cell Res. 256:213-224.
16. Huang, J., and J. W. Raff. 1999. The disappearance of cyclin B at the end of mitosis is regulated spatially in Drosophila cells. EMBO J. 18:2184-2195.
17. Huang, J. Y., and J. W. Raff. 2002. The dynamic localization of the Drosophila APC/C: evidence for the existence of multiple complexes that perform distinct functions and are differentially localized. J. Cell Sci. 115:2847-2856.
18. Jeurissen, S. H., F. Wagenaar, J. M. Pol, A. J. van der Eb, and M. H. Noteborn. 1992. Chicken anemia virus causes apoptosis of thymocytes after in vivo infection and of cell lines after in vitro infection. J. Virol. 66:7383-7388.
19. Jorgensen, P. M., E. Brundell, M. Starborg, and C. Hoog. 1998. A subunit of the anaphase-promoting complex is a centromere-associated protein in mammalian cells. Mol. Cell. Biol. 18:468-476.
20. Kalland, K. H., A. M. Szilvay, K. A. Brokstad, W. Saetrevik, and G. Haukenes. 1994. The human immunodeficiency virus type 1 Rev. protein shuttles between the cytoplasm and nuclear compartments. Mol. Cell. Biol. 14:7436-7444.
21. Klebe, C., F. R. Bischoff, H. Ponstingl, and A. Wittinghofer. 1995. Interaction of the nuclear GTP-binding protein Ran with its regulatory proteins RCC1 and RanGAP1. Biochemistry 34:639-647.
22. Klein, G. 2002. Perspectives in studies of human tumor viruses. Front. Biosci. 7:d268-d274.
23. Koken, M. H., G. Linares-Cruz, F. Quignon, A. Viron, M. K. Chelbi-Alix, J. Sobczak-Thepot, L. Juhlin, L. Degos, F. Calvo, and H. de The. 1995. The PML growth-suppressor has an altered expression in human oncogenesis. Oncogene 10:1315-1324.
24. Kornitzer, D., R. Sharf, and T. Kleinberger. 2001. Adenovirus E4orf4 protein induces PP2A-dependent growth arrest in Saccharomyces cerevisiae and interacts with the anaphase-promoting complex/cyclosome. J. Cell Biol. 154: 331-344.
25. Kudo, N., B. Wolff, T. Sekimoto, E. P. Schreiner, Y. Yoneda, M. Yanagida, S. Horinouchi, and M. Yoshida. 1998. Leptomycin B inhibition of signal-mediated nuclear export by direct binding to CRM1. Exp. Cell Res. 242:540-547.
26. Lafarga, M., M. T. Berciano, E. Pena, I. Mayo, J. G. Castano, D. Bohmann, J. P. Rodrigues, J. P. Tavanez, and M. Carmo-Fonseca. 2002. Clastosome: a subtype of nuclear body enriched in 19S and 20S proteasomes, ubiquitin, and protein substrates of proteasome. Mol. Biol. Cell 13:2771-2782.
27. Lallemand-Breitenbach, V., J. Zhu, F. Puvion, M. Koken, N. Honore, A. Doubeikovsky, E. Duprez, P. P. Pandolfi, E. Puvion, P. Freemont, and H. de The. 2001. Role of promyelocytic leukemia (PML) sumolation in nuclear body formation, 11S proteasome recruitment, and As2O3-induced PML or PML/retinoic acid receptor alpha degradation. J. Exp. Med. 193:1361-1371.
28. Leliveld, S. R., Y. H. Zhang, J. L. Rohn, M. H. Noteborn, and J. P. Abrahams. 2003. Apoptin induces tumor-specific apoptosis as a globular multimer. J. Biol. Chem. 278:9042-9051.
29. Liu, B., S. Hong, Z. Tang, H. Yu, and C. Z. Giam. 2005. HTLV-1 Tax directly binds the Cdc20-associated anaphase-promoting complex and activates it ahead of schedule. Proc. Natl. Acad. Sci. USA 102:63-68.
30. Meyer, B. E., and M. H. Malim. 1994. The HIV-1 Rev. transactivator shuttles between the nucleus and the cytoplasm. Genes Dev. 8:1538-1547.
31. Meyer, B. E., J. L. Meinkoth, and M. H. Malim. 1996. Nuclear transport of human immunodeficiency virus type 1, visna virus, and equine infectious anemia virus Rev. proteins: identification of a family of transferable nuclear export signals. J. Virol. 70:2350-2359.
32. Noteborn, M. H., D. Todd, C. A. Verschueren, H. W. de Gauw, W. L. Curran, S. Veldkamp, A. J. Douglas, M. S. McNulty, E. A. van der, and G. Koch. 1994. A single chicken anemia virus protein induces apoptosis. J. Virol. 68:346-351.
33. Peters, J. M. 2002. The anaphase-promoting complex: proteolysis in mitosis and beyond. Mol. Cell 9:931-943.
34. Poon, I. K., C. Oro, M. M. Dias, J. Zhang, and D. A. Jans. 2005. Apoptin nuclear accumulation is modulated by a CRM1-recognized nuclear export signal that is active in normal but not in tumor cells. Cancer Res. 65:7059-7064.
35. Rape, M., and M. W. Kirschner. 2004. Autonomous regulation of the anaphase-promoting complex couples mitosis to S-phase entry. Nature 432:588-595.
36. Rohn, J. L., Y.-H. Zhang, S. R. Leliveld, A. A. A. M. Danen-Van Oorschot, N. V. Henriquez, J. P. Abrahams, and M. H. M. Noteborn. 2005. Relevance of Apoptin's integrity for its functional behavior. J. Virol. 79:1337-1338.
37. Rohn, J. L., Y. H. Zhang, R. I. Aalbers, N. Otto, J. Den Hertog, N. V. Henriquez, C. J. Van De Velde, P. J. Kuppen, D. Mumberg, P. Donner, and M. H. Noteborn. 2002. A tumor-specific kinase activity regulates the viral death protein Apoptin. J. Biol. Chem. 277:50820-50827.
38. Roulston, A., R. C. Marcellus, and P. E. Branton. 1999. Viruses and apoptosis. Annu. Rev. Microbiol. 53:577-628.
39. Seeler, J. S., and A. Dejean. 2003. Nuclear and unclear functions of SUMO. Nat. Rev. Mol. Cell. Biol. 4:690-699.
40. Sherr, C. J. 2004. Principles of tumor suppression. Cell 116:235-246.
41. Soussi, T., and G. Lozano. 2005. p53 mutation heterogeneity in cancer. Biochem. Biophys. Res. Commun. 331:834-842.
42. 2/M arrest and apoptosis in the absence of p53. Genes Dev. 18: 1952-1957.
43. Terris, B., V. Baldin, S. Dubois, C. Degott, J. F. Flejou, D. Henin, and A. Dejean. 1995. PML nuclear bodies are general targets for inflammation and cell proliferation. Cancer Res. 55:1590-1597.
44. van Roessel, P., D. A. Elliott, I. M. Robinson, A. Prokop, and A. H. Brand. 2004. Independent regulation of synaptic size and activity by the anaphase-promoting complex. Cell 119:707-718.
45. Venkatesh, L. K., and G. Chinnadurai. 1990. Mutants in a conserved region near the carboxy terminus of HIV-1 Rev. identify functionally important residues and exhibit a dominant negative phenotype. Virology 178:327-330.
46. Venkatesh, L. K., T. Gettemeier, and G. Chinnadurai. 2003. A nuclear kinesin-like protein interacts with and stimulates the activity of the leucine-rich nuclear export signal of the human immunodeficiency virus type 1 rev protein. J. Virol. 77:7236-7243.
47. Wadia, J. S., M. V. Wagner, S. A. Ezhevsky, and S. F. Dowdy. 2004. Apoptin/ VP3 contains a concentration-dependent nuclear localization signal (NLS), not a tumorigenic selective NLS. J. Virol. 78:6077-6078.
48. Wang, Z. G., L. Delva, M. Gaboli, R. Rivi, M. Giorgio, C. Cordon-Cardo, F. Grosveld, and P. P. Pandolfi. 1998. Role of PML in cell growth and the retinoic acid pathway. Science 279:1547-1551.
49. Wang, Z. G., D. Ruggero, S. Ronchetti, S. Zhong, M. Gaboli, R. Rivi, and P. P. Pandolfi. 1998. PML is essential for multiple apoptotic pathways. Nat. Genet. 20:266-272.
50. Wen, W., J. L. Meinkoth, R. Y. Tsien, and S. S. Taylor. 1995. Identification of a signal for rapid export of proteins from the nucleus. Cell 82:463-473.
51. Wiebusch, L., M. Bach, R. Uecker, and C. Hagemeier. 2005. Human cytomegalovirus inactivates the G(0)/G(1)-APC/C ubiquitin ligase by cdh1 dissociation. Cell Cycle 4:1435-1439.
52. Wolff, B., J. J. Sanglier, and Y. Wang. 1997. Leptomycin B is an inhibitor of nuclear export: inhibition of nucleo-cytoplasmic translocation of the human immunodeficiency virus type 1 (HIV-1) Rev protein and Rev-dependent mRNA. Chem. Biol. 4:139-147.
53. Xu, Z. X., R. X. Zhao, T. Ding, T. T. Tran, W. Zhang, P. P. Pandolfi, and K. S. Chang. 2004. Promyelocytic leukemia protein 4 induces apoptosis by inhibition of survivin expression. J. Biol. Chem. 279:1838-1844.
54. Zhong, S., P. Salomoni, S. Ronchetti, A. Guo, D. Ruggero, and P. P. Pandolfi. 2000. Promyelocytic leukemia protein (PML) and Daxx participate in a novel nuclear pathway for apoptosis. J. Exp. Med. 191:631-640.
55. zur Hausen, H. 2001. Oncogenic DNA viruses. Oncogene 20:7820-7823.