Murine gammaherpesvirus 68 ORF75c contains ubiquitin E3 ligase activity and requires PML SUMOylation but not other known cellular PML regulators, CK2 and E6AP, to mediate PML degradation

Virology

Volumn 440, Issue 2, 2013, Pages 140-149

  Sewatanon, Jaturong ^a,b   Ling, Paul D ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b MAHIDOL UNIVERSITY   (Thailand)

Author keywords

Formylglycinamide ribonucleotide amidotransferase (FGARAT); Murine gammaherpesvirus 68; ORF75c; Promyelocytic leukemia protein; SUMO; Viral ubiquitin E3 ligase

Indexed keywords

CASEIN KINASE II; E6 ASSOCIATED VIRUS PROTEIN; PROMYELOCYTIC LEUKEMIA PROTEIN; PROTEASOME; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DNA REPLICATION; EMBRYO; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; FIBROBLAST; GAMMAHERPESVIRINAE; GENE EXPRESSION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MOLECULAR INTERACTION; MOUSE; NONHUMAN; ORF75C GENE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN STABILITY; PROTEIN TARGETING; SUMOYLATION; UBIQUITINATION; UPREGULATION; VIRUS GENE; VIRUS PARTICLE;

ANIMALS; CARBON-NITROGEN LIGASES WITH GLUTAMINE AS AMIDE-N-DONOR; CELL LINE; HOST-PATHOGEN INTERACTIONS; HUMANS; MICE; NUCLEAR PROTEINS; PROTEIN INTERACTION MAPPING; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEOLYSIS; RHADINOVIRUS; SUMOYLATION; TRANSCRIPTION FACTORS; TUMOR SUPPRESSOR PROTEINS; UBIQUITIN-PROTEIN LIGASES;

HUMAN PAPILLOMAVIRUS; MURINAE;

EID: 84876798265     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2013.02.014     Document Type: Article

References (47)

1. Adamson A.L., Kenney S. Epstein-barr virus immediate-early protein BZLF1 is SUMO-1 modified and disrupts promyelocytic leukemia bodies. J. Virol. 2001, 75:2388-2399.
2. Ahn J.H., Hayward G.S. The major immediate-early proteins IE1 and IE2 of human cytomegalovirus colocalize with and disrupt PML-associated nuclear bodies at very early times in infected permissive cells. J. Virol. 1997, 71:4599-4613.
3. Batty E., Jensen K., Freemont P. PML nuclear bodies and their spatial relationships in the mammalian cell nucleus. Front. Biosci. 2009, 14:1182-1196.
4. Bernardi R., Pandolfi P.P. Structure, dynamics and functions of promyelocytic leukaemia nuclear bodies. Nat. Rev. Mol. Cell Biol. 2007, 8:1006-1016.
5. Boutell C., Cuchet-Lourenço D., Vanni E., Orr A., Glass M., McFarlane S., Everett R.D. A viral ubiquitin ligase has substrate preferential SUMO targeted ubiquitin ligase activity that counteracts intrinsic antiviral defence. PLoS Pathog. 2011, 7:e1002245.
6. Chee A.V., Lopez P., Pandolfi P.P., Roizman B. Promyelocytic leukemia protein mediates interferon-based anti-herpes simplex virus 1 effects. J. Virol. 2003, 77:7101-7105.
7. Cheng B.Y.H., Zhi J., Santana A., Khan S., Salinas E., Forrest J.C., Zheng Y., Jaggi S., Leatherwood J., Krug L.T. Tiled microarray identification of novel viral transcript structures and distinct transcriptional profiles during two modes of productive murine gammaherpesvirus 68 infection. J. Virol. 2012, 86:4340-4357.
8. Condemine W., Takahashi Y., Zhu J., Puvion-Dutilleul F., Guegan S., Janin A., de Thé H. Characterization of endogenous human promyelocytic leukemia isoforms. Cancer Res. 2006, 66:6192-6198.
9. Cuchet-Lourenço D., Vanni E., Glass M., Orr A., Everett R.D. Herpes Simplex Virus 1 Ubiquitin Ligase ICP0 interacts with PML Isoform I and induces its SUMO-independent degradation. J. Virol. 2012, 86:11209-11222.
10. Dellaire G., Bazett-Jones D.P. PML nuclear bodies: dynamic sensors of DNA damage and cellular stress. Bioessays 2004, 26:963-977.
11. Evdokimov E., Sharma P., Lockett S.J., Lualdi M., Kuehn M.R. Loss of SUMO1 in mice affects RanGAP1 localization and formation of PML nuclear bodies, but is not lethal as it can be compensated by SUMO2 or SUMO3. J. Cell Sci. 2008, 121:4106-4113.
12. Everett R.D., Chelbi-Alix M.K. PML and PML nuclear bodies: implications in antiviral defence. Biochimie 2007, 89:819-830.
13. Everett R.D., Freemont P., Saitoh H., Dasso M., Orr A., Kathoria M., Parkinson J. The disruption of ND10 during Herpes Simplex Virus infection correlates with the Vmw110 and Proteasome-dependent loss of several PML isoforms. J. Virol. 1998, 6581-6591.
14. Everett R.D., Rechter S., Papior P., Tavalai N., Stamminger T., Orr A. PML contributes to a cellular mechanism of repression of herpes simplex virus type 1 infection that is inactivated by ICP0. J. Virol. 2006, 80:7995-8005.
15. Fu C., Ahmed K., Ding H., Ding X., Lan J., Yang Z., Miao Y., Zhu Y., Shi Y., Zhu J., Huang H., Yao X. Stabilization of PML nuclear localization by conjugation and oligomerization of SUMO-3. Oncogene 2005, 24:5401-5413.
16. Full F., Reuter N., Zielke K., Stamminger T., Ensser A. Herpesvirus saimiri antagonizes nuclear domain 10-instituted intrinsic immunity via an ORF3-mediated selective degradation of cellular protein Sp100. J. Virol. 2012, 86:3541-3553.
17. Gaspar M., Gill M.B., Lösing J.-B., May J.S., Stevenson P.G. Multiple functions for ORF75c in murid herpesvirus-4 infection. PLoS One 2008, 3:e2781.
18. Geoffroy M.-C., Chelbi-Alix M.K. Role of promyelocytic leukemia protein in host antiviral defense. J. Interferon Cytokine Res. 2011, 31:145-158.
19. Gillet L., Adler H., Stevenson P.G. Glycosaminoglycan interactions in murine gammaherpesvirus-68 infection. PLoS One 2007, 2:e347.
20. Jiang Y.-H., Armstrong D., Albrecht U., Atkins C.M., Noebels J.L., Eichele G., Sweatt J.D., Beaudet A.L. Mutation of the Angelman ubiquitin ligase in mice causes increased cytoplasmic p53 and deficits of contextual learning and long-term potentiation. Neuron 1998, 21:799-811.
21. Kamitani T., Kito K., Nguyen H.P., Wada H., Fukuda-Kamitani T., Yeh E.T. Identification of three major sentrinization sites in PML. J. Biol. Chem. 1998, 273:26675-26682.
22. Lallemand-Breitenbach V., de Thé H. PML nuclear bodies. Cold Spring Harbor Perspect. Biol. 2010, 2:a000661.
23. Lallemand-Breitenbach V., Jeanne M., Benhenda S., Nasr R., Lei M., Peres L., Zhou J., Zhu J., Raught B., de Thé H. Arsenic Degrades PML or PML-RARalpha Through a SUMO-Triggered RNF4/Ubiquitin-Mediated Pathway 2008, 10. Nature Publishing Group, 547-555.
24. 3-induced PML or PML/retinoic acid receptor alpha degradation. J. Exp. Med. 2001, 193:1361-1371.
25. Ling P.D., Peng R.S., Nakajima A., Yu J.H., Tan J., Moses S.M., Yang W.-H., Zhao B., Kieff E., Bloch K.D., Bloch D.B. Mediation of Epstein-Barr virus EBNA-LP transcriptional coactivation by Sp100. EMBO J. 2005, 24:3565-3575.
26. Ling P.D., Tan J., Sewatanon J., Peng R. Murine gammaherpesvirus 68 open reading frame 75c tegument protein induces the degradation of PML and is essential for production of infectious virus. J. Virol. 2008, 82:8000-8012.
27. Louria-Hayon I., Alsheich-Bartok O., Levav-Cohen Y., Silberman I., Berger M., Grossman T., Matentzoglu K., Jiang Y.-H., Müller S., Scheffner M., Haupt S., Haupt Y. E6AP promotes the degradation of the PML tumor suppressor. Cell Death Differ. 2009, 16:1156-1166.
28. Marcos-Villar L., Lopitz-Otsoa F., Gallego P., Muñoz-Fontela C., González-Santamaría J., Campagna M., Shou-Jiang G., Rodriguez M.S., Rivas C. Kaposi's sarcoma-associated herpesvirus protein LANA2 disrupts PML oncogenic domains and inhibits PML-mediated transcriptional repression of the survivin gene. J. Virol. 2009, 83:8849-8858.
29. Martinez-Guzman D., Rickabaugh T., Wu T.-T., Brown H., Cole S., Song M.J., Tong L., Sun R. Transcription program of murine gammaherpesvirus 68. J. Virol. 2003, 77:10488-10503.
30. Nash A.A., Dutia B.M., Stewart J.P., Davison A.J. Natural history of murine gamma-herpesvirus infection. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2001, 356:569-579.
31. Negorev D., Maul G.G. Cellular proteins localized at and interacting within ND10/PML nuclear bodies/PODs suggest functions of a nuclear depot. Oncogene 2001, 20:7234-7242.
32. Nichol J.N., Petruccelli L.A., Miller W.H. Expanding PML's functional repertoire through post-translational mechanisms. Front. Biosci. 2009, 14:2293-2306.
33. Ozato K., Shin D.-M., Chang T.-H., Morse H.C. TRIM family proteins and their emerging roles in innate immunity. Nat. Rev. Immunol. 2008, 8:849-860.
34. Percherancier Y., Germain-Desprez D., Galisson F., Mascle X.H., Dianoux L., Estephan P., Chelbi-Alix M.K., Aubry M. Role of SUMO in RNF4-mediated promyelocytic leukemia protein (PML) degradation: sumoylation of PML and phospho-switch control of its SUMO binding domain dissected in living cells. J. Biol. Chem. 2009, 284:16595-16608.
35. Reineke E.L., Kao H.-Y. Targeting promyelocytic leukemia protein: a means to regulating PML nuclear bodies. Int. J. Biol. Sci. 2009, 5:366-376.
36. Rochford R., Lutzke M.L., Alfinito R.S., Clavo A., Cardin R.D. Kinetics of murine gammaherpesvirus 68 gene expression following infection of murine cells in culture and in mice. J. Virol. 2001, 75:4955-4963.
37. Ruzzene M., Penzo D., Pinna L.A. Protein kinase CK2 inhibitor 4,5,6,7-tetrabromobenzotriazole (TBB) induces apoptosis and caspase-dependent degradation of haematopoietic lineage cell-specific protein 1 (HS1) in Jurkat cells. Biochem. J. 2002, 364:41-47.
38. Salomoni P., Pandolfi P.P. The role of PML in tumor suppression. Cell 2002, 108:165-170.
39. Scaglioni P.P., Yung T.M., Cai L.F., Erdjument-Bromage H., Kaufman A.J., Singh B., Teruya-Feldstein J., Tempst P., Pandolfi P.P. A CK2-dependent mechanism for degradation of the PML tumor suppressor. Cell 2006, 126:269-283.
40. Simas J.P., Efstathiou S. Murine gammaherpesvirus 68: a model for the study of gammaherpesvirus pathogenesis. Trends Microbiol. 1998, 6:276-282.
41. Sivachandran N., Cao J.Y., Frappier L. Epstein-Barr virus nuclear antigen 1 Hijacks the host kinase CK2 to disrupt PML nuclear bodies. J. Virol. 2010, 84:11113-11123.
42. Sivachandran N., Sarkari F., Frappier L. Epstein-Barr nuclear antigen 1 contributes to nasopharyngeal carcinoma through disruption of PML nuclear bodies. PLoS Pathog. 2008, 4:e1000170.
43. Tatham M.H., Geoffroy M.-C., Shen L., Plechanovova A., Hattersley N., Jaffray E.G., Palvimo J.J., Hay R.T. RNF4 is a Poly-SUMO-specific E3 Ubiquitin Ligase Required For Arsenic-Induced PML Degradation 2008, 10. Nature Publishing Group, 538-546.
44. Tavalai N., Papior P., Rechter S., Leis M., Stamminger T. Evidence for a role of the cellular ND10 protein PML in mediating intrinsic immunity against human cytomegalovirus infections. J. Virol. 2006, 80:8006-8018.
45. Tsai K., Thikmyanova N., Wojcechowskyj J.A., Delecluse H.-J., Lieberman P.M. EBV tegument protein BNRF1 disrupts DAXX-ATRX to activate viral early gene transcription. PLoS Pathog. 2011, 7:e1002376.
46. Yu Y., Wang S.E., Hayward G.S. The KSHV immediate-early transcription factor RTA encodes ubiquitin E3 ligase activity that targets IRF7 for proteosome-mediated degradation. Immunity 2005, 22:59-70.
47. Zhong S., Müller S., Ronchetti S., Freemont P.S., Dejean A., Pandolfi P.P. Role of SUMO-1-modified PML in nuclear body formation. Blood 2000, 95:2748-2752.