Phosphorylation of Merkel Cell Polyomavirus Large Tumor Antigen at Serine 816 by ATM Kinase Induces Apoptosis in Host Cells

Journal of Biological Chemistry

Volumn 290, Issue 3, 2015, Pages 1874-1884

  Li, Jing ^a   Diaz, Jason ^b   Wang, Xin ^c   Tsang, Sabrina H ^b   You, Jianxin ^b  

^a WISTAR INSTITUTE   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c LERNER RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; ANTIGENS; CELL DEATH; CELLS; ENZYMES; GENES; PHOSPHORYLATION; TUMORS;

C-TERMINAL DOMAINS; DNA DAMAGE RESPONSE; KINASE ACTIVITY; MERKEL CELL CARCINOMA; PHOSPHORYLATION SITES; POLYOMAVIRUS; TUMOR ANTIGEN; VIRAL REPLICATION;

CYTOLOGY;

ATM PROTEIN; SERINE; VIRUS LARGE T ANTIGEN; ATM PROTEIN, HUMAN; GLUTATHIONE TRANSFERASE; LIPOCORTIN 5; VIRUS T ANTIGEN;

ANIMAL CELL; ANTIGEN FUNCTION; APOPTOSIS; ARTICLE; CANCER INHIBITION; CARBOXY TERMINAL SEQUENCE; CELL STIMULATION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; HUMAN; HUMAN CELL; IN VITRO STUDY; MERKEL CELL POLYOMAVIRUS; NONHUMAN; PROTEIN DOMAIN; PROTEIN PHOSPHORYLATION; VIRUS CELL INTERACTION; CHEMISTRY; HEK293 CELL LINE; HELA CELL LINE; METABOLISM; PHOSPHORYLATION; PLASMID; PROTEIN TERTIARY STRUCTURE; TUMOR CELL LINE;

POLYOMAVIRUS;

ANNEXIN A5; ANTIGENS, POLYOMAVIRUS TRANSFORMING; APOPTOSIS; ATAXIA TELANGIECTASIA MUTATED PROTEINS; CELL LINE, TUMOR; GLUTATHIONE TRANSFERASE; HEK293 CELLS; HELA CELLS; HUMANS; MERKEL CELL POLYOMAVIRUS; PHOSPHORYLATION; PLASMIDS; PROTEIN STRUCTURE, TERTIARY;

EID: 84921825620     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.594895     Document Type: Article

References (54)

1. Feng, H., Shuda, M., Chang, Y., and Moore, P. S. (2008) Clonal integration of a polyomavirus in human Merkel cell carcinoma. Science 319, 1096-1100
2. Gjoerup, O., and Chang, Y. (2010) Update on human polyomaviruses and cancer. Adv. Cancer Res. 106, 1-51
3. Shuda, M., Feng, H., Kwun, H. J., Rosen, S. T., Gjoerup, O., Moore, P. S., and Chang, Y. (2008) T antigen mutations are a human tumor-specific signature for Merkel cell polyomavirus. Proc. Natl. Acad. Sci. U.S.A. 105, 16272-16277
4. Kassem, A., Schöpflin, A., Diaz, C., Weyers, W., Stickeler, E., Werner, M., and Zur Hausen, A. (2008) Frequent detection of Merkel cell polyomavirus in human Merkel cell carcinomas and identification of a unique deletion in the VP1 gene. Cancer Res. 68, 5009-5013
5. Lemos, B., and Nghiem, P. (2007) Merkel cell carcinoma: more deaths but still no pathway to blame. J. Invest. Dermatol. 127, 2100-2103
6. Agelli, M., and Clegg, L. X. (2003) Epidemiology of primary Merkel cell carcinoma in the United States. J. Am. Acad. Dermatol. 49, 832-841
7. Bichakjian, C. K., Lowe, L., Lao, C. D., Sandler, H. M., Bradford, C. R., Johnson, T. M., and Wong, S. L. (2007) Merkel cell carcinoma: critical review with guidelines for multidisciplinary management. Cancer 110, 1-12
8. Schrama, D., Ugurel, S., and Becker, J. C. (2012) Merkel cell carcinoma: recent insights and new treatment options. Curr. Opin. Oncol. 24, 141-149
9. Tolstov, Y. L., Pastrana, D. V., Feng, H., Becker, J. C., Jenkins, F. J., Moschos, S., Chang, Y., Buck, C. B., and Moore, P. S. (2009) Human Merkel cell polyomavirus infection II. MCV is a common human infection that can be detected by conformational capsid epitope immunoassays. Int. J. Cancer 125, 1250-1256
10. Schowalter, R. M., Pastrana, D. V., Pumphrey, K. A., Moyer, A. L., and Buck, C. B. (2010) Merkel cell polyomavirus and two previously unknown polyomaviruses are chronically shed from human skin. Cell Host Microbe 7, 509-515
11. Foulongne, V., Sauvage, V., Hebert, C., Dereure, O., Cheval, J., Gouilh, M. A., Pariente, K., Segondy, M., Burguière, A., Manuguerra, J. C., Caro, V., and Eloit, M. (2012) Human skin microbiota: high diversity of DNA viruses identified on the human skin by high throughput sequencing. PLoS ONE 7, e38499
12. Feng, H., Kwun, H. J., Liu, X., Gjoerup, O., Stolz, D. B., Chang, Y., and Moore, P. S. (2011) Cellular and viral factors regulating Merkel cell polyomavirus replication. PLoS ONE 6, e22468
13. Carter, J. J., Daugherty, M. D., Qi, X., Bheda-Malge, A., Wipf, G. C., Robinson, K., Roman, A., Malik, H. S., and Galloway, D. A. (2013) Identification of an overprinting gene in Merkel cell polyomavirus provides evolutionary insight into the birth of viral genes. Proc. Natl. Acad. Sci. U.S.A. 110, 12744-12749
14. Wang, X., Li, J., Schowalter, R. M., Jiao, J., Buck, C. B., and You, J. (2012) Bromodomain protein Brd4 plays a key role in Merkel cell polyomavirus DNA replication. PLoS Pathog. 8, e1003021
15. Demetriou, S. K., Ona-Vu, K., Sullivan, E. M., Dong, T. K., Hsu, S. W., and Oh, D. H. (2012) Defective DNA repair and cell cycle arrest in cells expressing Merkel cell polyomavirus T antigen. Int. J. Cancer 131, 1818-1827
16. Li, J., Wang, X., Diaz, J., Tsang, S. H., Buck, C. B., and You, J. (2013) Merkel cell polyomavirus large T antigen disrupts host genomic integrity and inhibits cellular proliferation. J. Virol. 87, 9173-9188
17. Hahn, W. C., Counter, C. M., Lundberg, A. S., Beijersbergen, R. L., Brooks, M. W., and Weinberg, R. A. (1999) Creation of human tumour cells with defined genetic elements. Nature 400, 464-468
18. Cheng, J., DeCaprio, J. A., Fluck, M. M., and Schaffhausen, B. S. (2009) Cellular transformation by simian virus 40 and murine polyoma virus T antigens. Semin. Cancer Biol. 19, 218-228
19. Harris, K. F., Christensen, J. B., and Imperiale, M. J. (1996) BK virus large T antigen: interactions with the retinoblastoma family of tumor suppressor proteins and effects on cellular growth control. J. Virol. 70, 2378-2386
20. Shivakumar, C. V., and Das, G. C. (1996) Interaction of human polyomavirus BK with the tumor-suppressor protein p53. Oncogene 13, 323-332
21. Bollag, B., Prins, C., Snyder, E. L., and Frisque, R. J. (2000) Purified JC virus T and T′ proteins differentially interact with the retinoblastoma family of tumor suppressor proteins. Virology 274, 165-178
22. Poulin, D. L., Kung, A. L., and DeCaprio, J. A. (2004) p53 targets simian virus 40 large T antigen for acetylation by CBP. J. Virol. 78, 8245-8253
23. Houben, R., Adam, C., Baeurle, A., Hesbacher, S., Grimm, J., Angermeyer, S., Henzel, K., Hauser, S., Elling, R., Bröcker, E. B., Gaubatz, S., Becker, J. C., and Schrama, D. (2012) An intact retinoblastoma protein-binding site in Merkel cell polyomavirus large T antigen is required for promoting growth of Merkel cell carcinoma cells. Int. J. Cancer 130, 847-856
24. Cheng, J., Rozenblatt-Rosen, O., Paulson, K. G., Nghiem, P., and De-Caprio, J. A. (2013) Merkel cell polyomavirus large T antigen has growth-promoting and inhibitory activities. J. Virol. 87, 6118-6126
25. Borchert, S., Czech-Sioli, M., Neumann, F., Schmidt, C., Wimmer, P., Dobner, T., Grundhoff, A., and Fischer, N. (2014) High-affinity Rb binding, p53 inhibition, subcellular localization, and transformation by wild-type or tumor-derived shortened Merkel cell polyomavirus large T antigens. J. Virol. 88, 3144-3160
26. Kwun, H. J., Guastafierro, A., Shuda, M., Meinke, G., Bohm, A., Moore, P. S., and Chang, Y. (2009) The minimum replication origin of Merkel cell polyomavirus has a unique large T-antigen loading architecture and requires small T-antigen expression for optimal replication. J. Virol. 83, 12118-12128
27. Tsang, S. H., Wang, X., Li, J., Buck, C. B., and You, J. (2014) Host DNA damage response factors localize to Merkel cell polyomavirus DNA replication sites to support efficient viral DNA replication. J. Virol. 88, 3285-3297
28. McVey, D., Brizuela, L., Mohr, I., Marshak, D. R., Gluzman, Y., and Beach, D. (1989) Phosphorylation of large tumour antigen by Cdc2 stimulates SV40 DNA replication. Nature 341, 503-507
29. Grässer, F. A., Scheidtmann, K. H., Tuazon, P. T., Traugh, J. A., and Walter, G. (1988) In vitro phosphorylation of SV40 large T antigen. Virology 165, 13-22
30. Prives, C. (1990) The replication functions of SV40 T antigen are regulated by phosphorylation. Cell 61, 735-738
31. McVey, D., Woelker, B., and Tegtmeyer, P. (1996) Mechanisms of simian virus 40 T-antigen activation by phosphorylation of threonine 124. J. Virol. 70, 3887-3893
32. Shi, Y., Dodson, G. E., Shaikh, S., Rundell, K., and Tibbetts, R. S. (2005) Ataxia-telangiectasia-mutated (ATM) is a T-antigen kinase that controls SV40 viral replication in vivo. J. Biol. Chem. 280, 40195-40200
33. Shimazu, T., Komatsu, Y., Nakayama, K. I., Fukazawa, H., Horinouchi, S., and Yoshida, M. (2006) Regulation of SV40 large T-antigen stability by reversible acetylation. Oncogene 25, 7391-7400
34. Diaz, J., Wang, X., Tsang, S. H., Jiao, J., and You, J. (2014) Phosphorylation of large T antigen regulates Merkel cell polyomavirus replication. Cancers 6, 1464-1486
35. Ciccia, A., and Elledge, S. J. (2010) The DNA damage response: making it safe to play with knives. Mol. Cell 40, 179-204
36. Schreiber, E., Matthias, P., Müller, M. M., and Schaffner, W. (1989) Rapid detection of octamer binding proteins with 'mini-extracts', prepared from a small number of cells. Nucleic Acids Res. 17, 6419
37. Yang, J., Yu, Y., Hamrick, H. E., and Duerksen-Hughes, P. J. (2003) ATM, ATR and DNA-PK: initiators of the cellular genotoxic stress responses. Carcinogenesis 24, 1571-1580
38. Brown, E. J., and Baltimore, D. (2003) Essential and dispensable roles of ATR in cell cycle arrest and genome maintenance. Genes Dev. 17, 615-628
39. Cimprich, K. A., and Cortez, D. (2008) ATR: an essential regulator of genome integrity. Nat. Rev. Mol. Cell Biol. 9, 616-627
40. Cuadrado, M., Martinez-Pastor, B., Murga, M., Toledo, L. I., Gutierrez-Martinez, P., Lopez, E., and Fernandez-Capetillo, O. (2006) ATM regulates ATR chromatin loading in response to DNA double-strand breaks. J. Exp. Med. 203, 297-303
41. Koopman, G., Reutelingsperger, C. P., Kuijten, G. A., Keehnen, R. M., Pals, S. T., and van Oers, M. H. (1994) Annexin V for flow cytometric detection of phosphatidylserine expression on B cells undergoing apoptosis. Blood 84, 1415-1420
42. Salvesen, G. S. (2002) Caspases: opening the boxes and interpreting the arrows. Cell Death Differ. 9, 3-5
43. Ghavami, S., Hashemi, M., Ande, S. R., Yeganeh, B., Xiao, W., Eshraghi, M., Bus, C. J., Kadkhoda, K., Wiechec, E., Halayko, A. J., and Los, M. (2009) Apoptosis and cancer: mutations within caspase genes. J. Med. Genet. 46, 497-510
44. Porter, A. G., and Jänicke, R. U. (1999) Emerging roles of caspase-3 in apoptosis. Cell Death Differ. 6, 99-104
45. Katunuma, N., Matsui, A., Le, Q. T., Utsumi, K., Salvesen, G., and Ohashi, A. (2001) Novel procaspase-3 activating cascade mediated by lysoapoptases and its biological significances in apoptosis. Adv. Enzyme Regul. 41, 237-250
46. Li, P., Nijhawan, D., and Wang, X. (2004) Mitochondrial activation of apoptosis. Cell 116, S57-S59
47. Chaitanya, G. V., Steven, A. J., and Babu, P. P. (2010) PARP-1 cleavage fragments: signatures of cell-death proteases in neurodegeneration. Cell Commun. Signal. 8, 31
48. D'Amours, D., Sallmann, F. R., Dixit, V. M., and Poirier, G. G. (2001) Gain-of-function of poly(ADP-ribose) polymerase-1 upon cleavage by apoptotic proteases: implications for apoptosis. J. Cell Sci. 114, 3771-3778
49. Kaufmann, S. H., Desnoyers, S., Ottaviano, Y., Davidson, N. E., and Poirier, G. G. (1993) Specific proteolytic cleavage of poly(ADP-ribose) polymerase: an early marker of chemotherapy-induced apoptosis. Cancer Res. 53, 3976-3985
50. Tewari, M., Quan, L. T., O'Rourke, K., Desnoyers, S., Zeng, Z., Beidler, D. R., Poirier, G. G., Salvesen, G. S., and Dixit, V. M. (1995) Yama/CPP32β, a mammalian homolog of CED-3, is a CrmA-inhibitable protease that cleaves the death substrate poly(ADP-ribose) polymerase. Cell 81, 801-809
51. Fradet-Turcotte, A., Vincent, C., Joubert, S., Bullock, P. A., and Archambault, J. (2007) Quantitative analysis of the binding of simian virus 40 large T antigen to DNA. J. Virol. 81, 9162-9174
52. Barlow, C., Brown, K. D., Deng, C. X., Tagle, D. A., and Wynshaw-Boris, A. (1997) Atm selectively regulates distinct p53-dependent cell-cycle checkpoint and apoptotic pathways. Nat. Genet. 17, 453-456
53. Abraham, R. T. (2001) Cell cycle checkpoint signaling through the ATM and ATR kinases. Genes Dev. 15, 2177-2196
54. Zhou, B. B., and Elledge, S. J. (2000) The DNA damage response: putting checkpoints in perspective. Nature 408, 433-439