Expression of the vault RNA protects cells from undergoing apoptosis

Nature Communications

Volumn 6, Issue , 2015, Pages

  Amort, Melanie ^a   Nachbauer, Birgit ^a,b   Tuzlak, Selma ^a   Kieser, Arnd ^c,d   Schepers, Aloys ^c,d   Villunger, Andreas ^a   Polacek, Norbert ^a,b  

^a INNSBRUCK MEDICAL UNIVERSITY   (Austria)

^b UNIVERSITY OF BERN   (Switzerland)

^c INSTITUTE OF EPIDEMIOLOGY   (Germany)

^d German Center for Infection Research DZIF Partner Site Munich   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LATENT MEMBRANE PROTEIN 1; LUNG RESISTANCE PROTEIN; RNA; UNCLASSIFIED DRUG; UNTRANSLATED RNA; VAULT COMPLEX ASSOCIATED RNA; VIRUS PROTEIN; EBV-ASSOCIATED MEMBRANE ANTIGEN, EPSTEIN-BARR VIRUS; MATRIX PROTEIN; RIBONUCLEOPROTEIN;

APOPTOSIS; GENE EXPRESSION; INFECTIVITY; MEMBRANE; PHENOTYPE; PROTEIN; RNA; VIRUS;

APOPTOSIS; ARTICLE; B LYMPHOCYTE; CELL DEATH; CELL PROTECTION; CONTROLLED STUDY; EPSTEIN BARR VIRUS; FEMALE; GENE EXPRESSION; HUMAN; HUMAN CELL; PHENOTYPE; PROTEIN EXPRESSION; STIMULATION; UPREGULATION; CHEMISTRY; CONFORMATION; GENETICS; HEK293 CELL LINE; METABOLISM; MOLECULAR GENETICS; MUTATION; NUCLEOTIDE SEQUENCE; SIGNAL TRANSDUCTION; TUMOR CELL LINE; VIRUS LATENCY;

HUMAN HERPESVIRUS 4;

APOPTOSIS; BASE SEQUENCE; CELL LINE, TUMOR; CYTOPROTECTION; HEK293 CELLS; HUMANS; MOLECULAR SEQUENCE DATA; MUTATION; NUCLEIC ACID CONFORMATION; RIBONUCLEOPROTEINS; RNA; SIGNAL TRANSDUCTION; VIRAL MATRIX PROTEINS; VIRUS LATENCY;

EID: 84929192997     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms8030     Document Type: Article

References (56)

1. Huttenhofer, A., Schattner, P. & Polacek, N. Non-coding RNAs: hope or hype? Trends Genet. 21, 289-297 (2005).
2. Amaral, P. P., Dinger, M. E., Mercer, T. R. & Mattick, J. S. The eukaryotic genome as an RNA machine. Science 319, 1787-1789 (2008).
3. Gebetsberger, J. & Polacek, N. Slicing tRNAs to boost functional ncRNA diversity. RNA Biol. 10, 1798-1806 (2013).
4. Sabin, L. R., Delas, M. J. & Hannon, G. J. Dogma derailed: the many influences of RNA on the genome. Mol. Cell 49, 783-794 (2013).
5. Tuck, A. C. & Tollervey, D. RNA in pieces. Trends Genet. 27, 422-432 (2011).
6. Mattick, J. S. RNA regUlation: a new genetics? Nat. Rev. 5, 316-323 (2004).
7. Kedersha, N. L. & Rome, L. H. Isolation and characterization of a novel ribonucleoprotein particle: large structures contain a single species of small RNA. J. Cell Biol. 103, 699-709 (1986).
8. Stadler, P. F. et al. Evolution of vault RNAs. Mol. Biol. Evol. 26, 1975-1991 (2009).
9. van Zon, A. et al. Vault mobility depends in part on microtubules and vaults can be recruited to the nuclear envelope. Exp. Cell Res. 312, 245-255 (2006).
10. Kickhoefer, V. A. et al. Vaults are up-regulated in multidrug-resistant cancer cell lines. J. Biol. Chem. 273, 8971-8974 (1998).
11. Kitazono, M. et al. Multidrug resistance and the lung resistance-related protein in human colon carcinoma SW-620 cells. J. Nat. Cancer Inst. 91, 1647-1653 (1999).
12. Chung, J. H., Ginn-Pease, M. E. & Eng, C. Phosphatase and tensin homologue deleted on chromosome 10 (PTEN) has nuclear localization signal-like sequences for nuclear import mediated by major vault protein. Cancer Res. 65, 4108-4116 (2005).
13. Kim, E. et al. Crosstalk between Src and major vault protein in epidermal growth factor-dependent cell signalling. FEBS J. 273, 793-804 (2006).
14. Ryu, S. J. et al. On the role of major vault protein in the resistance of senescent human diploid fibroblasts to apoptosis. Cell Death Differ. 15, 1673-1680 (2008).
15. Kowalski, M. P. et al. Host resistance to lung infection mediated by major vault protein in epithelial cells. Science 317, 130-132 (2007).
16. Shimamoto, Y. et al Direct activation of the human major vault protein gene by DNA-damaging agents. Oncol. Rep. 15, 645-652 (2006).
17. Vollmar, F. et al. Assembly of nuclear pore complexes mediated by major vault protein. J. Cell Sci. 122, 780-786 (2009).
18. Stephen, A. G. et al. Assembly of vault-like particles in insect cells expressing only the major vault protein. J. Biol. Chem. 276, 23217-23220 (2001).
19. Nandy, C. et al. Epstein-barr virus-induced expression of a novel human vault RNA. J. Mol. Biol. 388, 776-784 (2009).
20. Kong, L. B., Siva, A. C., Kickhoefer, V. A., Rome, L. H. & Stewart, P. L. RNA location and modeling of a WD40 repeat domain within the vault. RNA 6, 890-900 (2000).
21. Abbondanza, C. et al. Interaction of vault particles with estrogen receptor in the MCF-7 breast cancer cell. J. Cell Biol. 141, 1301-1310 (1998).
22. Mrazek, J., Kreutmayer, S. B., Grasser, F. A., Polacek, N. & Huttenhofer, A. Subtractive hybridization identifies novel differentially expressed ncRNA species in EBV-infected human B cells. Nucleic Acids Res. 35, e73 (2007).
23. Shah, K. M. & Young, L. S. Epstein-Barr virus and carcinogenesis: beyond Burkitt's lymphoma. Clin. Microbiol. Infect. 15, 982-988 (2009).
24. Thorley-Lawson, D. A. Epstein-Barr virus: exploiting the immune system. Nat. Rev. Immunol. 1, 75-82 (2001).
25. Abdulkarim, B. et al. Antiviral agent cidofovir decreases Epstein-Barr virus (EBV) oncoproteins and enhances the radiosensitivity in EBV-related malignancies. Oncogene 22, 2260-2271 (2003).
26. Murray, R. J. et al. Epstein-Barr virus-specific cytotoxic T-cell recognition of transfectants expressing the virus-coded latent membrane protein LMP. J. Virol. 62, 3747-3755 (1988).
27. Bain, M., Watson, R. J., Farrell, P. J. & Allday, M. J. Epstein-Barr virus nuclear antigen 3C is a powerful repressor of transcription when tethered to DNA. J. Virol. 70, 2481-2489 (1996).
28. Cludts, I. & Farrell, P. J. Multiple functions within the Epstein-Barr virus EBNA-3A protein. J. Virol. 72, 1862-1869 (1998).
29. Kieser, A. Signal transduction by the Epstein-Barr virus oncogene latent membrane protein 1 (LMP1). Signal Transduct. 7, 20-33 (2007).
30. Wong, D. et al. Extensive characterization of NF-kappaB binding uncovers non-canonical motifs and advances the interpretation of genetic functional traits. Genome Biol. 12, R70 (2011).
31. The ENCODE project consortium. A user's guide to the encyclopedia of DNA elements (ENCODE). PLoS Biol. 9, e1001046 (2011).
32. Delecluse, H. J., Hilsendegen, T., Pich, D., Zeidler, R. & Hammerschmidt, W. Propagation and recovery of intact, infectious Epstein-Barr virus from prokaryotic to human cells. Proc. Natl Acad. Sci. USA 95, 8245-8250 (1998).
33. Ideue, T., Hino, K., Kitao, S., Yokoi, T. & Hirose, T. Efficient oligonucleotide-mediated degradation of nuclear noncoding RNAs in mammalian cultured cells. RNA 15, 1578-1587 (2009).
34. Koseki, T., Inohara, N., Chen, S. & Nunez, G. ARC, an inhibitor of apoptosis expressed in skelet al muscle and heart that interacts selectively with caspases. Proc. Natl Acad. Sci. USA 95, 5156-5160 (1998).
35. Wang, M., Qanungo, S., Crow, M. T., Watanabe, M. & Nieminen, A. L. Apoptosis repressor with caspase recruitment domain (ARC) is expressed in cancer cells and localizes to nuclei. FEBS Lett. 579, 2411-2415 (2005).
36. Ludwig-Galezowska, A. H., Flanagan, L. & Rehm, M. Apoptosis repressor with caspase recruitment domain, a multifunctional modulator of cell death. J. Cell. Mol. Med. 15, 1044-1053 (2011).
37. Czabotar, P. E., Lessene, G., Strasser, A. & Adams, J. M. Control of apoptosis by the BCL-2 protein family: implications for physiology and therapy. Nat. Rev. Mol. Cell Biol. 15, 49-63 (2014).
38. Silke, J. & Hartland, E. L. Masters, marionettes and modulators: intersection of pathogen virulence factors and mammalian death receptor signaling. Curr. Opin. Immunol. 25, 436-440 (2013).
39. Berger, W., Elbling, L. & Micksche, M. Expression of the major vault protein LRP in human non-small-cell lung cancer cells: activation by short-term exposure to antineoplastic drugs. Int. J. Cancer 88, 293-300 (2000).
40. Lara, P. C., Pruschy, M., Zimmermann, M. & Henriquez-Hernandez, L. A. MVP and vaults: a role in the radiation response. Radiat. Oncol. 6, 148 (2011).
41. Persson, H. et al. The non-coding RNA ofthe multidrug resistance-linked vault particle encodes multiple regulatory small RNAs. Nat. Cell Biol. 11, 1268-1271 (2009).
42. Lee, K. S. et al. nc886, a non-coding RNA of anti-proliferative role, is suppressed by CpG DNA methylation in human gastric cancer. Oncotarget 5, 3944-3955 (2014).
43. Novoa, R. R. et al. Virus factories: associations of cell organelles for viral replication and morphogenesis. Biol. Cell 97, 147-172 (2005).
44. Huang, Y. et al. Molecular functions of small regulatory noncoding RNA. Biochemistry (Mosc) 78, 221-230 (2013).
45. Winterling, C. et al. Evidence for a crucial role of a host non-coding RNA in influenza A virus replication. RNA Biol. 11, 66-75 (2014).
46. Felton-Edkins, Z. A. et al. Epstein-Barr virus induces cellular transcription factors to allow active expression of EBER genes by RNA polymerase III. J. Biol. Chem. 281, 33871-33880 (2006).
47. Yang, G. D. et al. Epstein-Barr Virus-Encoded LMP1 upregulates microRNA-21 to promote the resistance of nasopharyngeal carcinoma cells to cisplatin-induced Apoptosis by suppressing PDCD4 and Fas-L. PLoS ONE 8, e78355 (2013).
48. Erlacher, M. et al. Puma cooperates with Bim, the rate-limiting BH3-only protein in cell death during lymphocyte development, in apoptosis induction. J. Exp. Med. 203, 2939-2951 (2006).
49. Danial, N. N. & Korsmeyer, S. J. Cell death: critical control points. Cell 116, 205-219 (2004).
50. Gopinath, S. C., Wadhwa, R. & Kumar, P. K. Expression of noncoding vault RNA in human malignant cells and its importance in mitoxantrone resistance. Mol. Cancer Res. 8, 1536-1546 (2010).
51. Cohen, J. H. et al. B-cell maturation stages of Burkitt's lymphoma cell lines according to Epstein-Barr virus status and type ofchromosome translocation. J. Nat. Cancer Inst. 78, 235-242 (1987).
52. Lenoir, G. M. et al. The use of lymphomatous and lymphoblastoid cell lines in the study of Burkitt's lymphoma. IARC Sci. Publ. 60, 309-318 (1985).
53. Shkoda, A. et al. The germinal center kinase TNIK is required for canonical NF-kappaB and JNK signaling in B-cells by the EBV oncoprotein LMP1 and the CD40 receptor. PLoS Biol. 10, e1001376 (2012).
54. Gebetsberger, J., Zywicki, M., Kunzi, A. & Polacek, N. tRNA-derived fragments target the ribosome and function as regulatory non-coding RNA in Haloferax volcanii. Archaea 2012, 260909 (2012).
55. Grasser, F. A. et al. Monoclonal antibodies directed against the Epstein-Barr virus-encoded nuclear antigen 1 (EBNA1): immunohistologic detection of EBNA1 in the malignant cells of Hodgkin's disease. Blood 84, 3792-3798 (1994).
56. Zimber-Strobl, U. et al. The Epstein-Barr virus nuclear antigen 2 interacts with an EBNA2 responsive cis-element of the terminal protein 1 gene promoter. EMBO J. 12, 167-175 (1993).