© The Rockefeller University Press,
0021-9525/1997//5 $5.00
The Journal of Cell Biology, Volume 138, Number 1,
, 1997 5-16
Human Cytomegalovirus Immediate Early Interaction with Host Nuclear Structures: Definition of an Immediate Transcript Environment
Alexander M. Ishov*,
Richard M. Stenberg
, and
Gerd G. Maul*
* The Wistar Institute, Philadelphia, Pennsylvania 19104; and
Department of Microbiology and Immunology, Eastern Virginia Medical School, Norfolk, Virginia 23501
The development of an induced transcript environment was investigated at the supramolecular level through comparative localization of the human cytomegalovirus immediate early (IE) transcripts and specific nuclear domains shortly after infection. Compact aggregates of IE transcripts form only adjacent to nuclear domain 10 (ND10), and the viral protein IE86 accumulates exclusively juxtaposed to the subpopulation of ND10 with transcripts. The stream of transcripts is funneled from ND10 into the spliceosome assembly factor SC35 domain through the accumulation of IE86 protein, which recruits some components of the basal transcription machinery. Concomitantly the IE72 protein binds to ND10 and later disperses them. The domain containing the zinc finger region of IE72 is essential for this dispersal. Positional analysis of proteins IE86 and IE72, IE transcripts, ND10, the spliceosome assembly factor SC35, and basal transcription factors defines spatially and temporally an immediate transcript environment, the basic components of which exist in the cell before viral infection, providing the structural environment for the virus to usurp.
Abbreviations used in this paper: IE, immediate early; HCMV, human cytomegalovirus; PML, promyelocytic leukemia protein; TBP, TATA-binding protein.
Please address all correspondence to Gerd G. Maul, The Wistar Institute, 3601 Spruce Street, Philadelphia, PA 19104. Tel.: (215) 898-3817; Fax: (215) 898-3868; E-mail: Maul{at}wista.wistar.upenn.edu

CiteULike
Complore
Connotea
Del.icio.us
Digg
Facebook
Reddit
Technorati
Twitter What's this?
This article has been cited by other articles:
-
Kapasi, A. J., Clark, C. L., Tran, K., Spector, D. H.
(2009). Recruitment of cdk9 to the Immediate-Early Viral Transcriptosomes during Human Cytomegalovirus Infection Requires Efficient Binding to Cyclin T1, a Threshold Level of IE2 86, and Active Transcription. J. Virol.
83: 5904-5917
[Abstract]
[Full Text]
-
Kyratsous, C. A., Silverstein, S. J.
(2009). Components of Nuclear Domain 10 Bodies Regulate Varicella-Zoster Virus Replication. J. Virol.
83: 4262-4274
[Abstract]
[Full Text]
-
Lin, Z., Yemelyanova, A. V., Gambhira, R., Jagu, S., Meyers, C., Kirnbauer, R., Ronnett, B. M., Gravitt, P. E., Roden, R. B.S.
(2009). Expression Pattern and Subcellular Localization of Human Papillomavirus Minor Capsid Protein L2. Am. J. Pathol.
174: 136-143
[Abstract]
[Full Text]
-
Lukashchuk, V., McFarlane, S., Everett, R. D., Preston, C. M.
(2008). Human Cytomegalovirus Protein pp71 Displaces the Chromatin-Associated Factor ATRX from Nuclear Domain 10 at Early Stages of Infection. J. Virol.
82: 12543-12554
[Abstract]
[Full Text]
-
Ullman, A. J., Hearing, P.
(2008). Cellular Proteins PML and Daxx Mediate an Innate Antiviral Defense Antagonized by the Adenovirus E4 ORF3 Protein. J. Virol.
82: 7325-7335
[Abstract]
[Full Text]
-
Kapasi, A. J., Spector, D. H.
(2008). Inhibition of the Cyclin-Dependent Kinases at the Beginning of Human Cytomegalovirus Infection Specifically Alters the Levels and Localization of the RNA Polymerase II Carboxyl-Terminal Domain Kinases cdk9 and cdk7 at the Viral Transcriptosome. J. Virol.
82: 394-407
[Abstract]
[Full Text]
-
Park, J.-J., Kim, Y.-E., Pham, H. T., Kim, E. T., Chung, Y.-H., Ahn, J.-H.
(2007). Functional interaction of the human cytomegalovirus IE2 protein with histone deacetylase 2 in infected human fibroblasts. J. Gen. Virol.
88: 3214-3223
[Abstract]
[Full Text]
-
Sourvinos, G., Tavalai, N., Berndt, A., Spandidos, D. A., Stamminger, T.
(2007). Recruitment of Human Cytomegalovirus Immediate-Early 2 Protein onto Parental Viral Genomes in Association with ND10 in Live-Infected Cells. J. Virol.
81: 10123-10136
[Abstract]
[Full Text]
-
Luo, M. H., Rosenke, K., Czornak, K., Fortunato, E. A.
(2007). Human Cytomegalovirus Disrupts both Ataxia Telangiectasia Mutated Protein (ATM)- and ATM-Rad3-Related Kinase-Mediated DNA Damage Responses during Lytic Infection. J. Virol.
81: 1934-1950
[Abstract]
[Full Text]
-
Binnie, A., Castelo-Branco, P., Monks, J., Proudfoot, N. J.
(2006). Homologous gene sequences mediate transcription-domain formation. J. Cell Sci.
119: 3876-3887
[Abstract]
[Full Text]
-
Ueno, T., Eizuru, Y., Katano, H., Kurata, T., Sata, T., Irie, S., Ogawa-Goto, K.
(2006). Novel Real-Time Monitoring System for Human Cytomegalovirus- Infected Cells In Vitro That Uses a Green Fluorescent Protein-PML-Expressing Cell Line.. Antimicrob. Agents Chemother.
50: 2806-2813
[Abstract]
[Full Text]
-
Tavalai, N., Papior, P., Rechter, S., Leis, M., Stamminger, T.
(2006). Evidence for a Role of the Cellular ND10 Protein PML in Mediating Intrinsic Immunity against Human Cytomegalovirus Infections.. J. Virol.
80: 8006-8018
[Abstract]
[Full Text]
-
Negorev, D. G., Vladimirova, O. V., Ivanov, A., Rauscher, F. III, Maul, G. G.
(2006). Differential role of sp100 isoforms in interferon-mediated repression of herpes simplex virus type 1 immediate-early protein expression.. J. Virol.
80: 8019-8029
[Abstract]
[Full Text]
-
Cantrell, S. R., Bresnahan, W. A.
(2006). Human Cytomegalovirus (HCMV) UL82 Gene Product (pp71) Relieves hDaxx-Mediated Repression of HCMV Replication.. J. Virol.
80: 6188-6191
[Abstract]
[Full Text]
-
Park, M.-Y., Kim, Y.-E., Seo, M.-R., Lee, J.-R., Lee, C. H., Ahn, J.-H.
(2006). Interactions among Four Proteins Encoded by the Human Cytomegalovirus UL112-113 Region Regulate Their Intranuclear Targeting and the Recruitment of UL44 to Prereplication Foci. J. Virol.
80: 2718-2727
[Abstract]
[Full Text]
-
Tamrakar, S., Kapasi, A. J., Spector, D. H.
(2005). Human Cytomegalovirus Infection Induces Specific Hyperphosphorylation of the Carboxyl-Terminal Domain of the Large Subunit of RNA Polymerase II That Is Associated with Changes in the Abundance, Activity, and Localization of cdk9 and cdk7. J. Virol.
79: 15477-15493
[Abstract]
[Full Text]
-
White, E. A., Spector, D. H.
(2005). Exon 3 of the Human Cytomegalovirus Major Immediate-Early Region Is Required for Efficient Viral Gene Expression and for Cellular Cyclin Modulation. J. Virol.
79: 7438-7452
[Abstract]
[Full Text]
-
Cantrell, S. R., Bresnahan, W. A.
(2005). Interaction between the Human Cytomegalovirus UL82 Gene Product (pp71) and hDaxx Regulates Immediate-Early Gene Expression and Viral Replication. J. Virol.
79: 7792-7802
[Abstract]
[Full Text]
-
Ghazal, P., Visser, A. E., Gustems, M., Garcia, R., Borst, E. M., Sullivan, K., Messerle, M., Angulo, A.
(2005). Elimination of ie1 Significantly Attenuates Murine Cytomegalovirus Virulence but Does Not Alter Replicative Capacity in Cell Culture. J. Virol.
79: 7182-7194
[Abstract]
[Full Text]
-
Everett, R. D., Murray, J.
(2005). ND10 Components Relocate to Sites Associated with Herpes Simplex Virus Type 1 Nucleoprotein Complexes during Virus Infection. J. Virol.
79: 5078-5089
[Abstract]
[Full Text]
-
Ching, R. W., Dellaire, G., Eskiw, C. H., Bazett-Jones, D. P.
(2005). PML bodies: a meeting place for genomic loci?. J. Cell Sci.
118: 847-854
[Abstract]
[Full Text]
-
Tang, Q., Li, L., Maul, G. G.
(2005). Mouse Cytomegalovirus Early M112/113 Proteins Control the Repressive Effect of IE3 on the Major Immediate-Early Promoter. J. Virol.
79: 257-263
[Abstract]
[Full Text]
-
Preston, C. M., Nicholl, M. J.
(2005). Human Cytomegalovirus Tegument Protein pp71 Directs Long-Term Gene Expression from Quiescent Herpes Simplex Virus Genomes. J. Virol.
79: 525-535
[Abstract]
[Full Text]
-
Isomura, H., Tsurumi, T., Stinski, M. F.
(2004). Role of the Proximal Enhancer of the Major Immediate-Early Promoter in Human Cytomegalovirus Replication. J. Virol.
78: 12788-12799
[Abstract]
[Full Text]
-
Lee, H.-R., Ahn, J.-H.
(2004). Sumoylation of the major immediate-early IE2 protein of human cytomegalovirus Towne strain is not required for virus growth in cultured human fibroblasts. J. Gen. Virol.
85: 2149-2154
[Abstract]
[Full Text]
-
Rosenke, K., Fortunato, E. A.
(2004). Bromodeoxyuridine-Labeled Viral Particles as a Tool for Visualization of the Immediate-Early Events of Human Cytomegalovirus Infection. J. Virol.
78: 7818-7822
[Abstract]
[Full Text]
-
Lee, H.-R., Kim, D.-J., Lee, J.-M., Choi, C. Y., Ahn, B.-Y., Hayward, G. S., Ahn, J.-H.
(2004). Ability of the Human Cytomegalovirus IE1 Protein To Modulate Sumoylation of PML Correlates with Its Functional Activities in Transcriptional Regulation and Infectivity in Cultured Fibroblast Cells. J. Virol.
78: 6527-6542
[Abstract]
[Full Text]
-
Everett, R. D., Sourvinos, G., Leiper, C., Clements, J. B., Orr, A.
(2004). Formation of Nuclear Foci of the Herpes Simplex Virus Type 1 Regulatory Protein ICP4 at Early Times of Infection: Localization, Dynamics, Recruitment of ICP27, and Evidence for the De Novo Induction of ND10-Like Complexes. J. Virol.
78: 1903-1917
[Abstract]
[Full Text]
-
Becker, K. A., Florin, L., Sapp, C., Maul, G. G., Sapp, M.
(2004). Nuclear Localization but Not PML Protein Is Required for Incorporation of the Papillomavirus Minor Capsid Protein L2 into Virus-Like Particles. J. Virol.
78: 1121-1128
[Abstract]
[Full Text]
-
Eskiw, C. H., Dellaire, G., Mymryk, J. S., Bazett-Jones, D. P.
(2003). Size, position and dynamic behavior of PML nuclear bodies following cell stress as a paradigm for supramolecular trafficking and assembly. J. Cell Sci.
116: 4455-4466
[Abstract]
[Full Text]
-
Tang, Q., Li, L., Ishov, A. M., Revol, V., Epstein, A. L., Maul, G. G.
(2003). Determination of Minimum Herpes Simplex Virus Type 1 Components Necessary To Localize Transcriptionally Active DNA to ND10. J. Virol.
77: 5821-5828
[Abstract]
[Full Text]
-
Everett, R. D., Sourvinos, G., Orr, A.
(2003). Recruitment of Herpes Simplex Virus Type 1 Transcriptional Regulatory Protein ICP4 into Foci Juxtaposed to ND10 in Live, Infected Cells. J. Virol.
77: 3680-3689
[Abstract]
[Full Text]
-
Berthoux, L., Towers, G. J., Gurer, C., Salomoni, P., Pandolfi, P. P., Luban, J.
(2003). As2O3 Enhances Retroviral Reverse Transcription and Counteracts Ref1 Antiviral Activity. J. Virol.
77: 3167-3180
[Abstract]
[Full Text]
-
Imai, N., Matsuda, N., Tanaka, K., Nakano, A., Matsumoto, S., Kang, W.
(2002). Ubiquitin Ligase Activities of Bombyx mori Nucleopolyhedrovirus RING Finger Proteins. J. Virol.
77: 923-930
[Abstract]
[Full Text]
-
Tang, Q., Maul, G. G.
(2002). Mouse Cytomegalovirus Immediate-Early Protein 1 Binds with Host Cell Repressors To Relieve Suppressive Effects on Viral Transcription and Replication during Lytic Infection. J. Virol.
77: 1357-1367
[Abstract]
[Full Text]
-
Ishov, A. M., Vladimirova, O. V., Maul, G. G.
(2002). Daxx-Mediated Accumulation of Human Cytomegalovirus Tegument Protein pp71 at ND10 Facilitates Initiation of Viral Infection at These Nuclear Domains. J. Virol.
76: 7705-7712
[Abstract]
[Full Text]
-
Marshall, K. R., Rowley, K. V., Rinaldi, A., Nicholson, I. P., Ishov, A. M., Maul, G. G., Preston, C. M.
(2002). Activity and intracellular localization of the human cytomegalovirus protein pp71. J. Gen. Virol.
83: 1601-1612
[Abstract]
[Full Text]
-
Gravel, A., Gosselin, J., Flamand, L.
(2002). Human Herpesvirus 6 Immediate-Early 1 Protein Is a Sumoylated Nuclear Phosphoprotein Colocalizing with Promyelocytic Leukemia Protein-associated Nuclear Bodies. J. Biol. Chem.
277: 19679-19687
[Abstract]
[Full Text]
-
Fortunato, E. A., Sanchez, V., Yen, J. Y., Spector, D. H.
(2002). Infection of Cells with Human Cytomegalovirus during S Phase Results in a Blockade to Immediate-Early Gene Expression That Can Be Overcome by Inhibition of the Proteasome. J. Virol.
76: 5369-5379
[Abstract]
[Full Text]
-
Hofmann, H., Sindre, H., Stamminger, T.
(2002). Functional Interaction between the pp71 Protein of Human Cytomegalovirus and the PML-Interacting Protein Human Daxx. J. Virol.
76: 5769-5783
[Abstract]
[Full Text]
-
Gawn, J. M., Greaves, R. F.
(2002). Absence of IE1 p72 Protein Function during Low-Multiplicity Infection by Human Cytomegalovirus Results in a Broad Block to Viral Delayed-Early Gene Expression. J. Virol.
76: 4441-4455
[Abstract]
[Full Text]
-
Shiels, C., Islam, S. A., Vatcheva, R., Sasieni, P., Sternberg, M. J. E., Freemont, P. S., Sheer, D.
(2002). PML bodies associate specifically with the MHC gene cluster in interphase nuclei. J. Cell Sci.
114: 3705-3716
[Abstract]
[Full Text]
-
Xu, Y., Ahn, J.-H., Cheng, M., apRhys, C. M., Chiou, C.-J., Zong, J., Matunis, M. J., Hayward, G. S.
(2001). Proteasome-Independent Disruption of PML Oncogenic Domains (PODs), but Not Covalent Modification by SUMO-1, Is Required for Human Cytomegalovirus Immediate-Early Protein IE1 To Inhibit PML-Mediated Transcriptional Repression. J. Virol.
75: 10683-10695
[Abstract]
[Full Text]
-
Bell, P., Montaner, L. J., Maul, G. G.
(2001). Accumulation and Intranuclear Distribution of Unintegrated Human Immunodeficiency Virus Type 1 DNA. J. Virol.
75: 7683-7691
[Abstract]
[Full Text]
-
Ahn, J.-H., Xu, Y., Jang, W.-J., Matunis, M. J., Hayward, G. S.
(2001). Evaluation of Interactions of Human Cytomegalovirus Immediate-Early IE2 Regulatory Protein with Small Ubiquitin-Like Modifiers and Their Conjugation Enzyme Ubc9. J. Virol.
75: 3859-3872
[Abstract]
[Full Text]
-
Burkham, J., Coen, D. M., Hwang, C. B. C., Weller, S. K.
(2001). Interactions of Herpes Simplex Virus Type 1 with ND10 and Recruitment of PML to Replication Compartments. J. Virol.
75: 2353-2367
[Abstract]
[Full Text]
-
Wu, F. Y., Ahn, J.-H., Alcendor, D. J., Jang, W.-J., Xiao, J., Hayward, S. D., Hayward, G. S.
(2001). Origin-Independent Assembly of Kaposi's Sarcoma-Associated Herpesvirus DNA Replication Compartments in Transient Cotransfection Assays and Association with the ORF-K8 Protein and Cellular PML. J. Virol.
75: 1487-1506
[Abstract]
[Full Text]
-
(2001). Prespliceosomal Assembly on Microinjected Precursor mRNA Takes Place in Nuclear Speckles. Mol. Biol. Cell
12: 393-406
[Abstract]
[Full Text]
-
Bell, P., Lieberman, P. M., Maul, G. G.
(2000). Lytic but Not Latent Replication of Epstein-Barr Virus Is Associated with PML and Induces Sequential Release of Nuclear Domain 10 Proteins. J. Virol.
74: 11800-11810
[Abstract]
[Full Text]
-
Angulo, A., Ghazal, P., Messerle, M.
(2000). The Major Immediate-Early Gene ie3 of Mouse Cytomegalovirus Is Essential for Viral Growth. J. Virol.
74: 11129-11136
[Abstract]
[Full Text]
-
Tang, Q., Bell, P., Tegtmeyer, P., Maul, G. G.
(2000). Replication but Not Transcription of Simian Virus 40 DNA Is Dependent on Nuclear Domain 10. J. Virol.
74: 9694-9700
[Abstract]
[Full Text]
-
Bloch, D. B., Nakajima, A., Gulick, T., Chiche, J.-D., Orth, D., de la Monte, S. M., Bloch, K. D.
(2000). Sp110 Localizes to the PML-Sp100 Nuclear Body and May Function as a Nuclear Hormone Receptor Transcriptional Coactivator. Mol. Cell. Biol.
20: 6138-6146
[Abstract]
[Full Text]
-
Bell, P., Brazas, R., Ganem, D., Maul, G. G.
(2000). Hepatitis Delta Virus Replication Generates Complexes of Large Hepatitis Delta Antigen and Antigenomic RNA That Affiliate with and Alter Nuclear Domain 10. J. Virol.
74: 5329-5336
[Abstract]
[Full Text]
-
Gong, L., Millas, S., Maul, G. G., Yeh, E. T. H.
(2000). Differential Regulation of Sentrinized Proteins by a Novel Sentrin-specific Protease. J. Biol. Chem.
275: 3355-3359
[Abstract]
[Full Text]
-
Melcak, I., Koberna, K., Malínský, J.
(2000). Nuclear pre-mRNA Compartmentalization: Trafficking of Released Transcripts to Splicing Factor Reservoirs. Mol. Biol. Cell
11: 497-510
[Abstract]
[Full Text]
-
Boisvert, F.-M., Hendzel, M. J., Bazett-Jones, D. P.
(2000). Promyelocytic Leukemia (Pml) Nuclear Bodies Are Protein Structures That Do Not Accumulate RNA. JCB
148: 283-292
[Abstract]
[Full Text]
-
Bass, H., Nagar, S, Hanley-Bowdoin, L, Robertson, D
(2000). Chromosome condensation induced by geminivirus infection of mature plant cells. J. Cell Sci.
113: 1149-1160
[Abstract]
-
Ahn, J.-H., Jang, W.-J., Hayward, G. S.
(1999). The Human Cytomegalovirus IE2 and UL112-113 Proteins Accumulate in Viral DNA Replication Compartments That Initiate from the Periphery of Promyelocytic Leukemia Protein-Associated Nuclear Bodies (PODs or ND10). J. Virol.
73: 10458-10471
[Abstract]
[Full Text]
-
Kim, Y. H., Choi, C. Y., Kim, Y.
(1999). Covalent modification of the homeodomain-interacting protein kinase 2 (HIPK2) by the ubiquitin-like protein SUMO-1. Proc. Natl. Acad. Sci. USA
96: 12350-12355
[Abstract]
[Full Text]
-
Ishov, A. M., Sotnikov, A. G., Negorev, D., Vladimirova, O. V., Neff, N., Kamitani, T., Yeh, E. T.H., Strauss, J. F. III, Maul, G. G.
(1999). Pml Is Critical for Nd10 Formation and Recruits the Pml-Interacting Protein Daxx to This Nuclear Structure When Modified by Sumo-1. JCB
147: 221-234
[Abstract]
[Full Text]
-
Müller, S., Dejean, A.
(1999). Viral Immediate-Early Proteins Abrogate the Modification by SUMO-1 of PML and Sp100 Proteins, Correlating with Nuclear Body Disruption. J. Virol.
73: 5137-5143
[Abstract]
[Full Text]
-
Snaar, S. P., Vincent, M., Dirks, R. W.
(1999). RNA Polymerase II Localizes at Sites of Human Cytomegalovirus Immediate-early RNA Synthesis and Processing. J. Histochem. Cytochem.
47: 245-254
[Abstract]
[Full Text]
-
Okano, K., Mikhailov, V. S., Maeda, S.
(1999). Colocalization of Baculovirus IE-1 and Two DNA-Binding Proteins, DBP and LEF-3, to Viral Replication Factories. J. Virol.
73: 110-119
[Abstract]
[Full Text]
-
Vallian, S., Chin, K.-V., Chang, K.-S.
(1998). The Promyelocytic Leukemia Protein Interacts with Sp1 and Inhibits Its Transactivation of the Epidermal Growth Factor Receptor Promoter. Mol. Cell. Biol.
18: 7147-7156
[Abstract]
[Full Text]
-
Burkham, J., Coen, D. M., Weller, S. K.
(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
[Abstract]
[Full Text]
-
Hendzel, M. J., Kruhlak, M. J., Bazett-Jones, D. P.
(1998). Organization of Highly Acetylated Chromatin around Sites of Heterogeneous Nuclear RNA Accumulation. Mol. Biol. Cell
9: 2491-2507
[Abstract]
[Full Text]
-
Everett, R. D., Freemont, P., Saitoh, H., Dasso, M., Orr, A., Kathoria, M., Parkinson, J.
(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
[Abstract]
[Full Text]
-
Ahn, J.-H., Brignole, E. J. III, Hayward, G. S.
(1998). 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. Mol. Cell. Biol.
18: 4899-4913
[Abstract]
[Full Text]
-
LaMorte, V. J., Dyck, J. A., Ochs, R. L., Evans, R. M.
(1998). Localization of nascent RNA and CREB binding protein with the PML-containing nuclear body. Proc. Natl. Acad. Sci. USA
95: 4991-4996
[Abstract]
[Full Text]
-
Samaniego, L. A., Neiderhiser, L., DeLuca, N. A.
(1998). Persistence and Expression of the Herpes Simplex Virus Genome in the Absence of Immediate-Early Proteins. J. Virol.
72: 3307-3320
[Abstract]
[Full Text]
-
Hirose, E, Nakashima, N, Sekiguchi, T, Nishimoto, T
(1998). RagA is a functional homologue of S. cerevisiae Gtr1p involved in the Ran/Gsp1-GTPase pathway. J. Cell Sci.
111: 11-21
[Abstract]