Disruption of PML subnuclear 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

Molecular and Cellular Biology

Volumn 18, Issue 8, 1998, Pages 4899-4913

  Ahn, Jin Hyun ^a   Brignole III, Edward J ^a   Hayward, Gary S ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; DNA; IMMEDIATE EARLY PROTEIN; RETINOBLASTOMA PROTEIN;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; COMPLEX FORMATION; CONTROLLED STUDY; DNA SYNTHESIS; HUMAN; HUMAN CELL; HUMAN CYTOMEGALOVIRUS; MITOSIS; NONHUMAN; POINT MUTATION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN LOCALIZATION; VERO CELL;

EID: 0031877790     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.18.8.4899     Document Type: Article

References (78)

1. 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.
2. Ahn, J.-H., C.-J. Chiou, and G. S. Hayward. 1998. Evaluation and mapping of the DNA binding and oligomerization domains of the IE2 regulatory protein of human cytomegalovirus using yeast one and two hybrid interaction assays. Gene 210:25-36.
3. Ahn, J.-H. Unpublished data.
4. Ascoli, C. A., and G. G. Maul. 1991. Identification of a novel nuclear domain. J. Cell Biol. 112:785-795.
5. 1H-nuclear magnetic resonance spectroscopy. J. Mol. Biol. 237:201-211.
6. 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 leukemia. Oncogene 13:971-982.
7. Borden, K. L. B., M. N. Boddy, J. Lally, N. J. O'Reilly, S. Martin, K. Howe, E. Solomon, and P. S. Freemont. 1995. The solution structure of the RING finger domain from the acute promyelocytic leukaemia proto-oncogene PML. EMBO J. 14:1532-1541.
8. Britt, W. J., and C. A. Alford. 1996. Cytomegalovirus, p. 2493-2523. In B. N. Fields, D. M. Knipe, and P. M. Howley (ed.), Fields virology, 3rd ed. Lippincott-Raven Publishers, Philadelphia, Pa.
9. 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.
10. Chang, Y.-N., K.-T. Jeang, T. Lietman, and G. S. Hayward. 1995. Structural organization of the spliced immediate-early gene complex that encodes the major acidic nuclear (IE1) and trans-activator (IE2) proteins of African green monkey cytomegalovirus. J. Biomed. Sci. 2:105-130.
11. Cherrington, J. M., and E. S. Mocarski. 1989. Human cytomegalovirus IE1 transactivates the promoter-enhancer via an 18-base-pair repeat element. J. Virol. 63:1435-1440.
12. Cherrington, J. M., E. L. Khoury, and E. S. Mocarski. 1991. Human cytomegalovirus ie2 negatively regulates alpha gene expression via a short target sequence near the transcription start site. J. Virol. 65:887-896.
13. Chiou, C.-J., J. Zong, I. Waheed, and G. S. Hayward. 1993. Identification and mapping of dimerization and DNA-binding domains in the C terminus of the IE2 regulatory protein of human cytomegalovirus. J. Virol. 67:6201-6214.
14. Ciufo, D., and G. S. Hayward. Evaluation of colocalization interactions between the herpes simplex virus IE110 nuclear regulatory protein and the cellular PML and SP100 proteins in infected and DNA-transfected cells. Submitted for publication.
15. Ciufo, D., and G. S. Hayward. Unpublished data.
16. de The, H., C. Lavau, A. Marchio, C. Chomienne, L. Degos, and A. Dejean. 1991. The PML-RARα fusion mRNA generated by the t(15;17) translocation of acute promyelocytic leukemia encodes a functionally altered RAR. Cell 66:675-684.
17. 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.
18. Doucas, V., and R. M. Evans. 1996. The PML nuclear compartment and cancer. Biochem. Biophys. Acta 1288:M25-M29.
19. Doucas, V., J. P. Brockes, M. Yaniv, H. de The, and A. Dejean. 1993. The PML-retinoic acid receptor α translocation converts the receptor from an inhibitor to a retinoic acid-dependent activator of transcription factor AP-1. Proc. Natl. Acad. Sci. USA 90:9345-9349.
20. Durfee, T., K. Becherer, P. L. Chen, S. H. Yeh, Y. Yang, A. Kilburn, W. H. Lee, and S. J. Elledge. 1993. The retinoblastoma protein associates with the protein phosphatase type 1 catalytic subunit. Genes Dev. 7:555-569.
21. Dyck, J. A., G. G. Maul, W. H. Miller, J. D. Chen, A. Kakizuka, and R. M. Evans. 1994. A novel macromolecular structure is a target of the promyelocyte-retinoic acid receptor oncoprotein. Cell 76:333-343.
22. Everett, R. D., and G. G. Maul. 1994. HSV-1 IE protein Vmw110 causes redistribution of PML. EMBO J. 13:5062-5069.
23. Everett, R. D., G. G. Maul, A. Orr, and M. Elliott. 1995. The cellular RING finger protein PML is not a functional counterpart of the herpes simplex virus type 1 RING finger protein Vmw110. J. Gen. Virol. 76:791-798.
24. Everett, R. D., M. Meredith, A. Orr, A. Cross, M. Kathoria, and J. Parkinson. 1997. A novel ubiquitin-specific protease is dynamically associated with PML nuclear domain and binds to a herpesvirus regulatory protein. EMBO J. 16:556-577.
25. Fields, S., and O.-K. Song. 1989. A novel genetic system to detect protein-protein interactions. Nature 340:245-246.
26. Ghazal, P., and J. A. Nelson. 1993. Transcription factors and viral regulatory proteins as potential mediators of human cytomegalovirus pathogenesis. Springer-Verlag, Berlin, Germany.
27. 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.
28. 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 ie1 mutant. J. Virol. 72:366-379.
29. Grignani, F., M. Fagioli, P. F. Ferrucci, M. Alcalay, and P. G. Pelicci. 1993. The molecular genetics of acute promyelocytic leukaemia. Blood Rev. 7:87-93.
30. Guarente, L., and M. Ptashne. 1981. Fusion of Escherichia coli lacZ to the cytochrome c gene of Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 78:2199-2203.
31. Hagemeier, C., R. Caswell, G. Hayhurst, J. Sinclair, and T. Kouzarides. 1994. Functional interaction between the HCMV IE2 transactivator and the retinoblastoma protein. EMBO J. 13:2897-2903.
32. Hayhurst, G. P., L. A. Bryant, R. C. Caswell, S. M. Walker, and J. H. Sinclair. 1995. CCAAT box-dependent activation of the TATA-less human DNA polymerase α promoter by the human cytomegalovirus 72-kilodalton major immediate-early protein. J. Virol. 69:182-188.
33. He, L.-Z., C. Tribioli, R. Rivi, D. Peruzzi, P. G. Pelicci, V. Soares, G. Cattoretti, and P. P. Pandolfi. 1997. Acute leukemia with promyelocytic features in PML/RARα transgenic mice. Proc. Natl. Acad. Sci. USA 94: 5302-5307.
34. Hermiston, T. W., C. L. Malone, P. R. Witte, and M. F. Stinski. 1987. Identification and characterization of the human cytomegalovirus immediate-early region 2 gene that stimulates gene expression from an inducible promoter, J. Virol. 61:3214-3221.
35. Honess, R. W., U. A. Gompels, M. Craxton, K. R. Cameron, R. Staden, B. G. Barrell, Y.-N. Chang, and G. S. Hayward. 1989. Global and local deviation from expected frequencies of CpG-dinucleotides in herpes virus DNAs may be diagnostic of differences in the states of their latent genomes. J. Gen. Virol. 70:837-855.
36. Hsieh, J. J.-D., and S. D. Hayward. 1995. Masking of the CBF1/RBPJκ transcriptional repressor domain by Epstein-Barr virus EBNA2. Science 268:560-563.
37. Isbov, A. M., R. M. Stenberg, and G. G. Maul. 1997. Human cytomegalovirus immediate early interaction with host nuclear structures: Definition of an immediate transcription environment. J. Cell Biol. 138:5-16.
38. 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.
39. Kakizuka, A., W. H. Miller, Jr., K. Umesono, R. P. Warrell, Jr., S. R. Frankel, V. V. V. S. Murty, E. Dmitrovsky, and R. M. Evans. 1991. Chromosomal translocation t(15;17) in human acute promyelocytic leukemia fuses RARα with a novel putative transcription factor. Cell 66:663-674.
40. Kastner, P., A. Pevez, Y. Lute, 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 α fusion proteins in acute promyleocytic leukemia (APL); structural similarities with a new family of oncoproteins. EMBO J. 11:629-642.
41. Kelly, C., R. V. Driel, and G. W. G. Wilkinson. 1995. Disruption of PML-associated nuclear bodies during human cytomegalovirus infection. J. Gen. Virol. 76:2887-2893.
42. Koken, M. H., A. Reid, F. Quignon, M. K. Chelbi-Alix, J. M. Davies, J. H. S. Kabarowski, J. Zhu, S. Dong, S.-J. Chen, Z. Chen, C. C. Tan, J. Licht, S. Waxman, H. de The, and A. Zelent. 1997. Leukemia-associated retinoic acid receptor α fusion partner, PML and PLZF, heterodimerize and colocalize to nuclear bodies. Proc. Natl. Acad. Sci. USA 94:10255-10260.
43. Koken, M. H., F. Puvion-Dutilleul, M. C. Guillemin, A. Viron, G. Linares-Cruz, N. Stuurman, L. De Jong, C. Szostechi, F. Calvo, C. Chomienne, L. Degos, E. Puvion, and H. de The. 1994. The t(15:17) translocation alters a nuclear body in a retinoic acid-reversible fashion. EMBO J. 13:1073-1083.
44. Koken, M. H., G. Linares-Cruz, F. Quignon, A. Viron, M. K. Chelbi-Alix, J. Sobczak-Thepot, L. Juhlin, L. Degos, F. Calvo, and H. de The. 1995. The PML growth suppressor has an altered expression in human oncogenesis. Oncogene 10:1315-1324.
45. 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.
46. LaFemina, R. L., and G. S. Hayward. 1980. Structural organization of the DNA molecules from human cytomegalovirus. ICN-UCLA Symp. Mol. Biol. 18:39-55.
47. LaFemina, R. L., and G. S. Hayward. 1988. Differences in cell type-specific blocks to immediate early gene expression and DNA replication of human, simian and murine cytomegalovirus. J. Gen. Virol. 69:355-374.
48. LaFemina, R. L., M. C. Pizzorno, J. D. Mosca, and G. S. Hayward. 1989. Expression of the acidic nuclear immediate-early protein (IE1) of human cytomegalovirus in stable cell lines and its preferential association with metaphase chromosomes. Virology 172:584-600.
49. Lang, D., and T. Stamminger. 1993. The 86-kilodalton IE-2 protein of human cytomegalovirus is a sequence-specific DNA-binding protein that interacts directly with the negative autoregulatory response element located near the cap site of the IE-1/2 enhancer-promoter. J. Virol. 67:323-331.
50. Le, X.-F., P. Yang, and K.-S. Chang. 1996. Analysis of the growth and transformation suppressor domains of promyelocytic leukemia gene, PML. J. Biol. Chem. 271:130-135.
51. Lillie, J. W., and M. R. Green. 1989. Transcription activation by the adenovirus E1A protein. Nature 338:39-44.
52. Liu, B., and M. F. Stinski. 1992. Human cytomegalovirus contains a tegument protein that enhances transcription from promoters with upstream ATF and AP-1 cis-acting elements. J. Virol. 66:4434-4444.
53. Liu, B., T. W. Hermiston, and M. F. Stinski. 1991. A "cis"-acting element in the major immediate-early (IE) promoter of human cytomegalovirus is required for negative regulation by IE2. J. Virol. 65:897-903.
54. Liu, J.-H., Z.-M. Mu, and K.-S. Chang. 1995. PML suppresses oncogenic transformation of NIH/3T3 cells by activated neu. J. Exp. Med. 181:1965-1973.
55. 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.
56. 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.
57. 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.
58. 491aa is replication defective due to a failure in autoregulation. Proc. Natl. Acad. Sci. USA 93:11321-11326.
59. Mocarski, E. S., Jr. 1996. Cytomegalovirus and their replication, p. 2447-2492. In B. N. Fields, D. M. Knipe, and P. M. Howley (ed.), Fields virology, 3rd ed. Lippincott-Raven Publishers, Philadelphia, Pa.
60. Mu, Z. M., K. V. Chin, J. H. Liu, G. Lozano, and K.-S. Chang. 1994. PML, a growth suppressor disrupted in acute promyelocytic leukemia. Mol. Cell. Biol. 14:6858-6867.
61. Pandolfi, P. P., F. Grignani, M. Alcalay, A. Mencarelli, A. Biondi, F. LoCoco, F. Grignani, and P. G. Pellicci. 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.
62. Pizzorno, M. C., and G. S. Hayward. 1990. The IE2 gene products of human cytomegalovirus specifically down-regulate expression from the major immediate-early promoter through a target sequence located near the cap site. J. Virol. 64:6154-6165.
63. Pizzorno, M. C., M.-A. Mullen, Y.-N. Chang, and G. S. Hayward. 1991. The functionally active IE2 immediate-early regulatory protein of human cytomegalovirus is an 80-kilodalton polypeptide that contains two distinct activator domains and a duplicated nuclear localization signal. J. Virol. 65:3839-3852.
64. Pizzorno, M. C., P. O'Hare, L. Sha, R. L. LaFemina, and G. S. Hayward. 1988. trans-activation and autoregulation of gene expression by the immediate-early region 2 gene products of human cytomegalovirus. J. Virol. 62:1167-1179.
65. Puvion-Dutilleul, F., M. K. Chelbi-Alix, M. Koken, F. Quignon, E. Puvion, and H. de The. 1995. Adenovirus infection induces rearrangements in the intranuclear distribution of the nuclear body-associated PML protein. Exp. Cell Res. 218:9-16.
66. Rose, M. D., F. Winston, and P. Hieter. 1990. Methods in yeast genetics. A laboratory course manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
67. Spaete, R. R., and E. S. Mocarski. 1987. Insertion and deletion mutagenesis of the human cytomegalovirus genome. Proc. Natl. Acad. Sci. USA 84:7213-7217.
68. Stadler, M., M. K. Chelbi-Alix, M. H. Koken, L. Venturini, C. Lee, A. Saib, F. Quignon, L. Pelicano, M. C. Guillemin, and C. Schindler. 1995. Transcriptional induction of the PML growth suppressor gene by interferons is mediated through an ISRE and a GAS element. Oncogene 11:2565-2573.
69. Stenberg, R. M., P. R. Witte, and M. F. Stinski. 1985. Multiple spliced and unspliced transcripts from human cytomegalovirus immediate-early region 2 and evidence for a common initiation site within immediate-early region 1. J. Virol. 56:665-675.
70. Stinski, M. F., D. R. Thomsen, R. M. Stenberg, and L. C. Goldstein. 1983. Organization and expression of the immediate early genes of human cytomegalovirus. J. Virol. 46:1-14.
71. Stuurman, N., A. De Graaf, A. Floore, A. Josso, B. Humbel, L. De Jong, and R. Van Driel. 1992. A monoclonal antibody recognizing nuclear matrix associated nuclear bodies. J. Cell Sci. 101:773-784.
72. Szekely, L., K. Pokrovskaja, W.-Q. Jiang, H. de The, N. Ringertz, and G. Klein. 1996. The Epstein-Barr virus-encoded nuclear antigen EBNA-5 accumulates in PML-containing bodies. J. Virol. 70:2562-2568.
73. Szostecki, C., H. H. Guldner, H. T. Netter, and H. Will. 1990. Isolation and characterization of cDNA encoding a human nuclear antigen predominantly recognized by autoantibodies from patients with cirrhosis. J. Immunol. 145:4338-4347.
74. Wang, Y., J. E. Finan, J. M. Middeldrop, and S. D. Hayward. 1997. P32/TAP, a cellular protein that interacts with EBNA-1 of Epstein-Barr virus. Virology 236:18-29.
75. Weis, K., S. Rambaud, C. Lavau, J. Janseu, 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.
76. Wilkinson, G. W. G., and A. Akrigg. 1992. Constitutive and enhanced expression from the CMV major IE promoter in a defective adenovirus vector. Nucleic Acids Res. 20:2233-2239.
77. Zhong, L. 1997. Role of herpes simplex virus type-1 (HSV-1) immediate early proteins in intranuclear compartmentalization during HSV-1 infection. Ph.D. thesis. Johns Hopkins University, Baltimore, Md.
78. Zhong, L., and G. S. Hayward. The herpes simplex virus IE68(ICP22) immediate-early protein is associated with novel nuclear punctate structures and causes the disruption of both cellular PML oncogenic domains and spliceosome domains. Submitted for publication.