Modification of small hepatitis delta virus antigen by SUMO protein

Journal of Virology

Volumn 84, Issue 2, 2010, Pages 918-927

  Tseng, Chung Hsin ^a,b   Cheng, Tai Shan ^b   Shu, Chiung Yueh ^c   Jeng, King Song ^a   Lai, Michael M C ^a,b,d,e  

^a INSTITUTE OF MOLECULAR BIOLOGY   (Taiwan)

^b NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^c CNRS   (France)

^d UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^e NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

GENOMIC RNA; LYSINE; MESSENGER RNA; SUMO 1 PROTEIN; SUMO PROTEIN; VIRUS ANTIGEN;

ACETYLATION; ARTICLE; BACTERIUM CONJUGATION; CONTROLLED STUDY; GENE FUSION; GENE MAPPING; HEPATITIS DELTA VIRUS; METHYLATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN MODIFICATION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; RNA REPLICATION; RNA SYNTHESIS; SUMOYLATION;

AMINO ACID SEQUENCE; CELL LINE, TUMOR; GENOME, VIRAL; HEPATITIS DELTA ANTIGENS; HEPATITIS DELTA VIRUS; HUMANS; MOLECULAR SEQUENCE DATA; PROTEIN PROCESSING, POST-TRANSLATIONAL; RNA, MESSENGER; RNA, VIRAL; SUMO-1 PROTEIN; TRANSFECTION; TWO-HYBRID SYSTEM TECHNIQUES;

HEPATITIS DELTA VIRUS;

EID: 73849140875     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.01034-09     Document Type: Article

References (56)

1. Boddy, M. N., K. Howe, L. D. Etkin, E. Solomon, and P. S. Freemont.1996. PIC 1, a novel ubiquitin-like protein which interacts with the PML component of a multiprotein complex that is disrupted in acute promyelocytic leukaemia. Oncogene 13:971-982.
2. Boggio, R., and S. Chiocca.2006. Viruses and sumoylation: recent highlights. Curr. Opin. Microbiol. 9:430-436.
3. Bossis, G., C. E. Malnou, R. Farras, E. Andermarcher, R. Hipskind, M. Rodriguez, D. Schmidt, S. Muller, I. Jariel-Encontre, and M. Piechaczyk. 2005. Down-regulation of c-Fos/c-Jun AP-1 dimer activity by sumoylation. Mol. Cell. Biol. 25:6964-6979.
4. Carter, S., and K. H. Vousden.2008. p53-Ubl fusions as models of ubiquitination, sumoylation and neddylation of p53. Cell Cycle 7:2519-2528.
5. Chang, F. L., P. J. Chen, S. J. Tu, C. J. Wang, and D. S. Chen.1991. The large form of hepatitis delta antigen is crucial for assembly of hepatitis delta virus. Proc. Natl. Acad. Sci. USA 88:8490-8494.
6. Chang, M. F., S. C. Baker, L. H. Soe, T. Kamahora, J. G. Keck, S. Makino, S. Govindarajan, and M. M. Lai.1988. Human hepatitis delta antigen is a nuclear phosphoprotein with RNA-binding activity. J. Virol. 62:2403-2410.
7. Chao, M., S. Y. Hsieh, and J. Taylor.1990. Role of two forms of hepatitis delta virus antigen: evidence for a mechanism of self-limiting genome replication. J. Virol. 64:5066-5069.
8. Chien, C. T., P. L. Bartel, R. Sternglanz, and S. Fields.1991. The two-hybrid system: a method to identify and clone genes for proteins that interact with a protein of interest. Proc. Natl. Acad. Sci. USA 88:9578-9582.
9. Choi, S. H., K. J. Park, and S. B. Hwang.2002. Large hepatitis delta antigen is phosphorylated at multiple sites and phosphorylation is associated with protein conformational change. Intervirology 45:142-149.
10. Desterro, J. M., M. S. Rodriguez, and R. T. Hay.1998. SUMO-1 modification of IkappaBalpha inhibits NF-kappaB activation. Mol. Cell 2:233-239.
11. Everett, R. D.2001. DNA viruses and viral proteins that interact with PML nuclear bodies. Oncogene 20:7266-7273.
12. Fields, S., and O. Song.1989. A novel genetic system to detect proteinprotein interactions. Nature 340:245-246.
13. Geiss-Friedlander, R., and F. Melchior.2007. Concepts in sumoylation: a decade on. Nat. Rev. Mol. Cell. Biol. 8:947-956.
14. Glenn, J. S., J. A. Watson, C. M. Havel, and J. M. White.1992. Identification of a prenylation site in delta virus large antigen. Science 256:1331-1333.
15. Gostissa, M., A. Hengstermann, V. Fogal, P. Sandy, S. E. Schwarz, M. Scheffner, and G. Del Sal.1999. Activation of p53 by conjugation to the ubiquitin-like protein SUMO-1. EMBO J. 18:6462-6471.
16. Govindarajan, S., K. P. Chin, A. G. Redeker, and R. L. Peters.1984. Fulminant B viral hepatitis: role of delta agent. Gastroenterology 86:1417-1420.
17. Guo, D., M. Li, Y. Zhang, P. Yang, S. Eckenrode, D. Hopkins, W. Zheng, S. Purohit, R. H. Podolsky, A. Muir, J. Wang, Z. Dong, T. Brusko, M. Atkinson, P. Pozzilli, A. Zeidler, L. J. Raffel, C. O. Jacob, Y. Park, M. Serrano-Rios, M. T. Larrad, Z. Zhang, H. J. Garchon, J. F. Bach, J. I. Rotter, J. X. She, and C. Y. Wang.2004. A functional variant of SUMO4, a new I kappa B alpha modifier, is associated with type 1 diabetes. Nat. Genet. 36:837-841.
18. Hay, R. T.2007. SUMO-specific proteases: a twist in the tail. Trends Cell Biol. 17:370-376.
19. Heun, P.2007. SUMOrganization of the nucleus. Curr. Opin. Cell Biol. 19:350-355.
20. Hoege, C., B. Pfander, G. L. Moldovan, G. Pyrowolakis, and S. Jentsch.2002. RAD6-dependent DNA repair is linked to modification of PCNA by ubiquitin and SUMO. Nature 419:135-141.
21. Huang, W. H., C. W. Chen, H. L. Wu, and P. J. Chen.2006. Post-translational modification of delta antigen of hepatitis D virus. Curr. Top. Microbiol. Immunol. 307:91-112.
22. Huang, Z. S., and H. N. Wu.1998. Identification and characterization of the RNA chaperone activity of hepatitis delta antigen peptides. J. Biol. Chem. 273:26455-26461.
23. Jeng, K. S., A. Daniel, and M. M. Lai.1996. A pseudoknot ribozyme structure is active in vivo and required for hepatitis delta virus RNA replication. J. Virol. 70:2403-2410.
24. Johnson, E. S.2004. Protein modification by SUMO. Annu. Rev. Biochem. 73:355-382.
25. Kuo, M. Y., M. Chao, and J. Taylor.1989. Initiation of replication of the human hepatitis delta virus genome from cloned DNA: role of delta antigen. J. Virol. 63:1945-1950.
26. Lai, M. M.2005. RNA replication without RNA-dependent RNA polymerase: surprises from hepatitis delta virus. J. Virol. 79:7951-7958.
27. Lamsoul, I., J. Lodewick, S. Lebrun, R. Brasseur, A. Burny, R. B. Gaynor, and F. Bex.2005. Exclusive ubiquitination and sumoylation on overlapping lysine residues mediate NF-kappaB activation by the human T-cell leukemia virus Tax oncoprotein. Mol. Cell. Biol. 25:10391-10406.
28. Lee, C. Z., P. J. Chen, and D. S. Chen.1995. Large hepatitis delta antigen in packaging and replication inhibition: role of the carboxyl-terminal 19 amino acids and amino-terminal sequences. J. Virol. 69:5332-5336.
29. Li, Y. J., M. R. Stallcup, and M. M. Lai.2004. Hepatitis delta virus antigen is methylated at arginine residues, and methylation regulates subcellular localization and RNA replication. J. Virol. 78:13325-13334.
30. Lin, D. Y., Y. S. Huang, J. C. Jeng, H. Y. Kuo, C. C. Chang, T. T. Chao, C. C. Ho, Y. C. Chen, T. P. Lin, H. I. Fang, C. C. Hung, C. S. Suen, M. J. Hwang, K. S. Chang, G. G. Maul, and H. M. Shih.2006. Role of SUMO-interacting motif in Daxx SUMO modification, subnuclear localization, and repression of sumoylated transcription factors. Mol. Cell 24:341-354.
31. Macnaughton, T. B., and M. M. Lai.2006. HDV RNA replication: ancient relic or primer? Curr. Top. Microbiol. Immunol. 307:25-45.
32. Macnaughton, T. B., and M. M. Lai.2002. Large hepatitis delta antigen is not a suppressor of hepatitis delta virus RNA synthesis once RNA replication is established. J. Virol. 76:9910-9919.
33. Macnaughton, T. B., S. T. Shi, L. E. Modahl, and M. M. Lai.2002. Rolling circle replication of hepatitis delta virus RNA is carried out by two different cellular RNA polymerases. J. Virol. 76:3920-3927.
34. Mahajan, R., C. Delphin, T. Guan, L. Gerace, and F. Melchior.1997. A small ubiquitin-related polypeptide involved in targeting RanGAP1 to nuclear pore complex protein RanBP2. Cell 88:97-107.
35. Matunis, M. J., E. Coutavas, and G. Blobel.1996. A novel ubiquitin-like modification modulates the partitioning of the Ran-GTPase-activating protein RanGAP1 between the cytosol and the nuclear pore complex. J. Cell Biol. 135:1457-1470.
36. Melchior, F.2000. SUMO - nonclassical ubiquitin. Annu. Rev. Cell Dev. Biol. 16:591-626.
37. Meulmeester, E., M. Kunze, H. H. Hsiao, H. Urlaub, and F. Melchior.2008. Mechanism and consequences for paralog-specific sumoylation of ubiquitinspecific protease 25. Mol. Cell 30:610-619.
38. Meulmeester, E., and F. Melchior.2008. Cell biology: SUMO. Nature 452:709-711.
39. Modahl, L. E., and M. M. Lai.1998. Transcription of hepatitis delta antigen mRNA continues throughout hepatitis delta virus (HDV) replication: a new model of HDV RNA transcription and replication. J. Virol. 72:5449-5456.
40. Mu, J. J., D. S. Chen, and P. J. Chen.2001. The conserved serine 177 in the delta antigen of hepatitis delta virus is one putative phosphorylation site and is required for efficient viral RNA replication. J. Virol. 75:9087-9095.
41. Mu, J. J., Y. G. Tsay, L. J. Juan, T. F. Fu, W. H. Huang, D. S. Chen, and P. J. Chen.2004. The small delta antigen of hepatitis delta virus is an acetylated protein and acetylation of lysine 72 may influence its cellular localization and viral RNA synthesis. Virology 319:60-70.
42. Mu, J. J., H. L. Wu, B. L. Chiang, R. P. Chang, D. S. Chen, and P. J. Chen. 1999. Characterization of the phosphorylated forms and the phosphorylated residues of hepatitis delta virus delta antigens. J. Virol. 73:10540-10545.
43. Mukhopadhyay, D., and M. Dasso.2007. Modification in reverse: the SUMO proteases. Trends Biochem. Sci. 32:286-295.
44. Muller, S., A. Ledl, and D. Schmidt.2004. SUMO: a regulator of gene expression and genome integrity. Oncogene 23:1998-2008.
45. Pichler, A., P. Knipscheer, E. Oberhofer, W. J. van Dijk, R. Korner, J. V. Olsen, S. Jentsch, F. Melchior, and T. K. Sixma.2005. SUMO modification of the ubiquitin-conjugating enzyme E2-25K. Nat. Struct. Mol. Biol. 12:264-269.
46. Rizzetto, M., B. Hoyer, M. G. Canese, J. W. Shih, R. H. Purcell, and J. L. Gerin.1980. Delta agent: association of delta antigen with hepatitis B surface antigen and RNA in serum of delta-infected chimpanzees. Proc. Natl. Acad. Sci. USA 77:6124-6128.
47. Sheu, G. T., and M. M. Lai.2000. Recombinant hepatitis delta antigen from E. coli promotes hepatitis delta virus RNA replication only from the genomic strand but not the antigenomic strand. Virology 278:578-586.
48. Tseng, C. H., K. S. Jeng, and M. M. Lai.2008. Transcription of subgenomic mRNA of hepatitis delta virus requires a modified hepatitis delta antigen that is distinct from antigenomic RNA synthesis. J. Virol. 82:9409-9416.
49. Wang, J. G., J. Cullen, and S. M. Lemon.1992. Immunoblot analysis demonstrates that the large and small forms of hepatitis delta virus antigen have different C-terminal amino acid sequences. J. Gen. Virol. 73:183-188.
50. Wilson, V. G., and D. Rangasamy.2001. Viral interaction with the host cell sumoylation system. Virus Res. 81:17-27.
51. Wong, S. K., and D. W. Lazinski.2002. Replicating hepatitis delta virus RNA is edited in the nucleus by the small form of ADAR1. Proc. Natl. Acad. Sci. USA 99:15118-15123.
52. Wu, Y. C., A. F. Deyrieux, and V. G. Wilson.2007. Papillomaviruses and the host SUMOylation system. Biochem. Soc. Trans. 35:1433-1435.
53. Xue, Y., F. Zhou, C. Fu, Y. Xu, and X. Yao.2006. SUMOsp: a web server for sumoylation site prediction. Nucleic Acids Res. 34:254-257.
54. Yang, C. K., J. H. Kim, D. K. Ann, and M. R. Stallcup.2008. Differential regulation of the two transcriptional activation domains of the coiled-coil coactivator CoCoA by sumoylation. BMC Mol. Biol. 9:1-12.
55. Yurchenko, V., Z. Xue, and M. J. Sadofsky.2006. SUMO modification of human XRCC4 regulates its localization and function in DNA double-strand break repair. Mol. Cell. Biol. 26:1786-1794.
56. Zhao, J.2007. Sumoylation regulates diverse biological processes. Cell. Mol. Life Sci. 64:3017-3033.