Viral immediate-early proteins abrogate the modification by SUMO-1 of PML and Sp100 proteins, correlating with nuclear body disruption

Journal of Virology

Volumn 73, Issue 6, 1999, Pages 5137-5143

  Müller, Stefan ^a   Dejean, Anne ^a  

^a INSTITUT PASTEUR   (France)

Author keywords

[No Author keywords available]

Indexed keywords

IMMEDIATE EARLY PROTEIN; NUCLEAR PROTEIN; UBIQUITIN; VIRUS PROTEIN;

ADENOVIRUS; ARTICLE; CELL NUCLEUS INCLUSION BODY; CONTROLLED STUDY; COVALENT BOND; CYTOMEGALOVIRUS; DNA VIRUS; HELA CELL; HERPES SIMPLEX VIRUS; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROCESSING; VIRUS INFECTION;

EID: 0344299239     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/jvi.73.6.5137-5143.1999     Document Type: Article

References (52)

1. Ahn, J. H., E. J. Brignole III, and G. S. Hayward. 1998. Disruption of PML subnudear domains by the acidic IE1 protein of human cytomegalovirus is mediated through interaction with PML and may modulate a RING finger-dependent cryptic transactivator function of PML. Mol. Cell. Biol. 18:4899-4913.
2. Ahn, J. H., and G. S. Hayward. 1997. 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. 71:4599-4613.
3. Ali, S., Y. Lutz, J. P. Bellocq, M. P. Chenard-Nen, N. Rouyer, and D. Metzger. 1993. Production and characterization of monoclonal antibodies recognising defined regions of the human oestrogen receptor. Hybridoma 12: 391-405.
4. Burkham, J., D. M. Coen, and S. K. Weller. 1998. ND10 protein PML is recruited to herpes simplex virus type 1 prereplicative sites and replication compartments in the presence of viral DNA polymerase. J. Virol. 72:10100-10107.
5. Carvalho, T., J. S. Seeler, K. Ohman, P. Jordan, U. Pettersson, G. Akusjarvi, M. Carmo-Fonseca, and A. Dejean. 1995. Targeting of adenovirus E1A and E4-ORF3 proteins to nuclear matrix-associated PML bodies. J. Cell Biol. 131:45-56.
6. Desbois, C., R. Rousset, F. Bantignies, and P. Jalinot. 1996. Exclusion of Int-6 from PML nuclear bodies by binding to the HTLV-I Tax oncoprotein. Science 273:951-953.
7. 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.
8. De Thé, H., C. Lavau, A. Marchio, C. Chomlenne, L. Degos, and A. Dejean. 1991. The PML-RARα fusion mRNA generated by the t(15;17) translocation in acute promyelocytic leukemia encodes a functionally altered RAR. Cell 66:675-684.
9. Doucas, V., A. M. Ishov, A. Romo, H. Juguilon, M. D. Weitzman, R. M. Evans, and G. G. Maul. 1996. Adenovirus replication is coupled with the dynamic properties of the PML nuclear structure. Genes Dev. 10:196-207.
10. Dyck, J. A., G. G. Maul, W. H. Miller, Jr., J. D. Chen, A. Kakizuka, and R. M. Evaas. 1994. A novel macromolecular structure is a target of the promyelocyte-retinoic acid receptor oncoprotein. Cell 76:333-343.
11. Everett, R. D., P. Freemont, H. Saitoh, M. Dasso, A. Orr, M. Kathoria, and J. Parkinson. 1998. The disruption of ND10 during herpes simplex virus infection correlates with the Vmw110- and proteasome-dependent loss of several PML isoforms. J. Virol. 72:6581-6591.
12. Everett, R. D., and G. G. Maul. 1994. HSV-1 IE protein Vmw110 causes redistribution of PML. EMBO J. 13:5062-5069.
13. Everett, R., P. O'Hare, D. O'Rourke, P. Barlow, and A. Orr. 1995. Point mutations in the herpes simplex virus type 1 Vmw110 RING finger helix affect activation of gene expression, viral growth, and interaction with PML-containing nuclear structures. J. Virol. 69:7339-7344.
14. Goddard, A. D., J. Borrow, P. S. Freemont, and E. Solomon. 1991. Characterization of a zinc finger gene disrupted by the t(15;17) in acute promyelocytic leukemia. Science 254:1371-1374.
15. Greaves, R. F., and E. S. Mocarski. 1998. Defective growth correlates with reduced accumulation of a viral DNA replication protein after low-multiplicity infection by a human cytomegalovirus iel mutant. J. Virol. 72:366-379.
16. Guldner, H. H., C. Szostecki, T. Grötzinger, and H. Will. 1992. IFN enhance expression of Sp100, an autoantigen in primary biliary cirrhosis. J. Immunol. 149:4067-4073.
17. Hodges, M., C. Tissot, K. Howe, D. Grimwade, and P. S. Freemont. 1998. Structure, organization, and dynamics of promyelocytic leukemia protein nuclear bodies. Am. J. Hum. Genet. 63:297-304.
18. Ishov, A. M., and G. G. Maul. 1996. The periphery of nuclear domain 10 (ND10) as site of DNA virus deposition. J. Cell Biol. 134:815-826.
19. Ishov, A. M., R. M. Stenberg, and G. G. Maul. 1997. Human cytomegalovirus immediate early interaction with host nuclear structures: definition of an immediate transcript environment. J. Cell Biol. 138:5-16.
20. Kakizuka, A., W. H. Miller, Jr., K. Umesono, R. P. Warrell, Jr., S. R. Frankel, V. V. Murty, E. Dmitrovsky, and R. M. Evans. 1991. Chromosomal translocation t(15;17) in human acute promyelocytic leukemia fuses RAR alpha with a novel putative transcription factor, PML. Cell 66:663-674.
21. Kamitani, T., H. P. Nguyen, K. Kito, T. Fukuda-Kamitani, and E. T. Yeh. 1998. Covalent modification of PML by the sentrin family of ubiquitin-like proteins. J. Biol. Chem. 273:3117-3720.
22. Kastner, P., A. Perez, Y. Lutz, C. Rochette-Egly, M. P. Gaub, B. Durand, M. Lanotte, R. Berger, and P. Chambon. 1992. Structure, localization and transcriptional properties of two classes of retinoic acid receptor a fusion proteins in acute promyelocytic leukemia (APL): structural similarities with a new family of oncoproteins. EMBO J. 11:629-642.
23. Kelly, C., R. van Driel, and G. W. Wllkinson. 1995. Disruption of PML-associated nuclear bodies during human cytomegalovirus infection. J. Gen. Virol. 76:2887-2893.
24. Koken, M. H., F. Puvion-Dutilleul, M. C. Guillemin, A. Viron, G. Linares-Cruz, N. Stuurman, L. de Jong, C. Szostecki, F. Calvo, C. Chomienne, L. Degos, E. Puvion, and H. de Thé. 1994. The t(15;17) translocation alters a nuclear body in a retinoic acid-reversible fashion. EMBO J. 13:1073-1083.
25. Korioth, F., G. G. Maul, B. Plachter, T. Stamminger, and J. Frey. 1996. The nuclear domain 10 (ND10) is disrupted by the human cytomegalovirus gene product IE1. Exp. Cell Res. 229:155-158.
26. Lamond, A. I., and W. C. Earnshaw. 1998. Structure and function in the nucleus. Science 280:547-553.
27. Lavau, C., A. Marchio, M. Fagioli, J. Jansen, B. Falini, P. Lebon, F. Grosveld, P. P. Pandolfi, P. G. Pelicci, and A. Dejean. 1995. The acute-promyelocytic leukaemia-associated PML gene is induced by interferon. Oncogene 11:871-876.
28. Lehming, N., A. Le Saux, J. Schuller, and M. Ptashne. 1998. Chromatin components as part of a putative transcriptional repressing complex. Proc. Natl. Acad. Sci. USA 95:7322-7326.
29. 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.
30. 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.
31. Maul, G. 1998. Nuclear domain 10, the site of DNA virus transcription and replication. Bioessays 20:660-667.
32. Maul, G. G., and R. D. Everett. 1994. The nuclear location of PML, a cellular member of the C3HC4 zinc-binding domain protein family, is rearranged during herpes simplex virus infection by the C3HC4 viral protein ICP0. J. Gen. Virol. 75:1223-1233.
33. Maul, G. G., H. H. Guldner, and J. G. Spivack. 1993. Modification of discrete nuclear domains induced by herpes simplex virus type 1 immediate early gene 1 product (ICP0). J. Gen. Virol. 74:2679-2690.
34. Maul, G. G., A. M. Ishov, and R. D. Everett. 1996. Nuclear domain 10 as preexisting potential replication start sites of herpes simplex virus type-1. Virology 217:67-75.
35. Maul, G. G., E. Yu, A. M. Ishov, and A. L. Epstein. 1995. Nuclear domain 10 (ND10) associated proteins are also present in nuclear bodies and redistribute to hundreds of nuclear sites after stress. J. Cell. Biochem. 59:498-513.
36. Mazeron, M. C., G. Jahn, and B. Plachter. 1992. Monoclonal antibody E-13 (M-810) to human cytomegalovirus recognizes an epitope encoded by exon 2 of the major immediate early gene. J. Gen. Virol. 73:2699-2703.
37. Mocarski, E. S., G. W. Kemble, J. M. Lyle, and R. F. Greaves. 1996. A deletion mutant in the human cytomegalovirus gene encoding IE1(491aa) is replication defective due to a failure in autoregulation. Proc. Natl. Acad. Sci. USA 93:11321-11326.
38. Müller, S., and A. Dejean. Unpublished data.
39. Müller, S., M. J. Matunis, and A. Dejean. 1998. Conjugation with the ubiquitin-relaled modifier SUMO-1 regulates the partitioning of PML within the nucleus. EMBO J. 17:61-70.
40. Pandolfi, P. P., F. Grignani, M. Alcalay, A. Mencarelli, A. Biondi, F. Lo Coco, F. Grignani, and P. G. Pelicci. 1991. Structure and origin of the acute promyelocytic leukemia myl/RARα cDNA and characterization of its retinoid-binding and transactivation properties. Oncogene 6:1285-1292.
41. Quignon, F., F. De Bels, M. Koken, J. Feunteun, J. C. Ameisen, and H. de Thé. 1998. PML induces a novel caspase-independent death process. Nat. Genet. 20:259-265.
42. Reddy, B. A., L. D. Etkin, and P. S. Freemont. 1992. A novel zinc finger coiled-coil domain in a family of nuclear proteins. Trends Biochem. Sci. 17: 344-345.
43. Seeler, J. S., A. Marchio, D. Sitterlin, C. Transy, and A. Dejean. 1998. Interaction of SP100 with HP1 proteins: a link between the promyelocytic leukemia-associated nuclear bodies and the chromatin compartment. Proc. Natl. Acad. Sci. USA 95:7316-7321.
44. Skinner, P. J., B. T. Koshy, C. J. Cummings, I. A. Klement, K. Helin, A. Servadio, H. Y. Zoghbi, and H. T. Orr. 1997. Ataxin-1 with an expanded glutamine tract alters nuclear matrix-associated structures. Nature 389:971-974.
45. Stadler, M., M. K. Chelbi-Alix, M. H. M. Koken, L. Venturini, C. Lee, A. Saïb, F. Quignon, L. Pelicano, M. C. Guillemin, C. Schindler, and H. de Thé. 1995. Transcriptional induction of the PML growth suppressor gene by interferons is mediated through an ISRE and a GAS element. Oncogene 11: 2565-2573.
46. Stenberg, R. M., D. R. Thomson, and M. F. Stinski. 1984. Structural analysis of the major immediate early gene of human cytomegalovirus. J. Virol. 49: 190-199.
47. Sternsdorf, T., K. Jensen, and H. Will. 1997. Evidence for covalent modification of the nuclear dot-associated proteins PML and Sp100 by PIC1/ SUMO-1. J. Cell Biol. 139:1621-1634.
48. Szostecki, C., H. H. Guldner, H. J. Netter, and H. Will. 1990. Isolation and characterization of cDNA encoding a human nuclear antigen predominantly recognized by autoantibodies from patients with primary biliary cirrhosis. J. Immunol. 145:4338-4347.
49. Wang, Z. G., D. Ruggero, S. Ronchetti, S. Zhong, M. Gaboli, R. Rivi, and P. P. Pandolfi. 1998. Pm1 is essential for multiple apoptotic pathways. Nat. Genet. 20:266-272.
50. 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.
51. Weis, K., S. Rambaud, C. Lavau, J. Jansen, T. Carvalho, M. Carmo-Fonseca, A. Lamond, and A. Dejean. 1994. Retinoic acid regulates aberrant nuclear localization of PML-RAR alpha in acute promyelocytic leukemia cells. Cell 76:345-356.
52. Zhu, J., M. H. Koken, F. Quignon, M. K. Chelbi-Alix, L. Degos, Z. Y. Wang, Z. Chen, and H. de Thé. 1997. Arsenic-induced PML targeting onto nuclear bodies: implications for the treatment of acute promyelocytic leukemia. Proc. Natl. Acad. Sci. USA 94:3978-3983.