Home LiteratureArticle Details
PMID: 11160739 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Interactions of herpes simplex virus type 1 with ND10 and recruitment of PML to replication compartments.

Journal of virology ·Vol. 75 ·No. 5 ·2001-03-00 ·Pages 2353-67

Burkham J, Coen DM, Hwang CB, Weller SK

Abstract

Many of the events required for productive herpes simplex virus type 1 (HSV-1) infection occur within globular nuclear domains called replication compartments, whose formation appears to depend on interactions with cellular nuclear domains 10 (ND10). We have previously demonstrated that the formation of HSV-1 replication compartments involves progression through several stages, including the disruption of intact ND10 (stage I to stage II) and the formation of PML-associated prereplicative sites (stage III) and replication compartments (stage IV) (J. Burkham, D. M. Coen, and S. K. Weller, J. Virol. 72:10100-10107, 1998). In this paper, we show that some, but not all, PML isoforms are recruited to stage III foci and replication compartments. Genetic experiments showed that the recruitment of PML isoforms to stage III prereplicative sites and replication compartments requires the localization of the HSV-1 polymerase protein (UL30) to these foci but does not require polymerase catalytic activity. We also examined the stages of viral infection under conditions affecting ND10 integrity. Treatment with factors that increase the stability of ND10, arsenic trioxide and the proteasome inhibitor MG132, inhibited viral disruption of ND10, formation of replication compartments, and production of progeny virus. These results strengthen the previously described correlation between ND10 disruption and productive viral infection.

MeSH Terms
Animals Arsenic Trioxide Arsenicals/pharmacology Cell Line Cell Nucleus Structures/metabolism DNA, Complementary Gene Products, pol/genetics,metabolism Herpes Simplex/virology Herpesvirus 1, Human/drug effects,metabolism,pathogenicity Humans Mutation Neoplasm Proteins/chemistry,genetics,metabolism Nuclear Proteins/metabolism Oxides/pharmacology Promyelocytic Leukemia Protein Protein Isoforms Transcription Factors/chemistry,genetics,metabolism Tumor Suppressor Proteins Virulence Virus Replication
Chemicals
Arsenicals DNA, Complementary Gene Products, pol Neoplasm Proteins Nuclear Proteins Oxides Promyelocytic Leukemia Protein Protein Isoforms Transcription Factors Tumor Suppressor Proteins PML protein, human Arsenic Trioxide
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Burkham J
Department of Microbiology, University of Connecticut Health Center, Farmington, Connecticut 06030, USA.
Coen D M
Hwang C B
Weller S K
References (75)
75 references, click to expand
  1. Conjugation with the ubiquitin-related modifier SUMO-1 regulates the partitioning of PML within the nucleus.
    EMBO J. 1998 Jan 2;17(1):61-70 PMID: 9427741
  2. Nuclear dots: actors on many stages.
    Immunobiology. 1997 Dec;198(1-3):307-31 PMID: 9442402
  3. Resistance to virus infection conferred by the interferon-induced promyelocytic leukemia protein.
    J Virol. 1998 Feb;72(2):1043-51 PMID: 9444998
  4. The promyelocytic leukemia gene product (PML) forms stable complexes with the retinoblastoma protein.
    Mol Cell Biol. 1998 Feb;18(2):1084-93 PMID: 9448006
  5. The ubiquitin-like proteins SMT3 and SUMO-1 are conjugated by the UBC9 E2 enzyme.
    Proc Natl Acad Sci U S A. 1998 Jan 20;95(2):560-4 PMID: 9435231
  6. Polymerases and the replisome: machines within machines.
    Cell. 1998 Feb 6;92(3):295-305 PMID: 9476890
  7. Localization of nascent RNA and CREB binding protein with the PML-containing nuclear body.
    Proc Natl Acad Sci U S A. 1998 Apr 28;95(9):4991-6 PMID: 9560216
  8. The disruption of ND10 during herpes simplex virus infection correlates with the Vmw110- and proteasome-dependent loss of several PML isoforms.
    J Virol. 1998 Aug;72(8):6581-91 PMID: 9658103
  9. Identification of three major sentrinization sites in PML.
    J Biol Chem. 1998 Oct 9;273(41):26675-82 PMID: 9756909
  10. Nuclear domain 10, the site of DNA virus transcription and replication.
    Bioessays. 1998 Aug;20(8):660-7 PMID: 9780840
  11. PML induces a novel caspase-independent death process.
    Nat Genet. 1998 Nov;20(3):259-65 PMID: 9806544
  12. Engineered herpes simplex virus DNA polymerase point mutants: the most highly conserved region shared among alpha-like DNA polymerases is involved in substrate recognition.
    J Virol. 1990 Dec;64(12):5883-90 PMID: 2173770
  13. Localization of p53, retinoblastoma and host replication proteins at sites of viral replication in herpes-infected cells.
    Nature. 1991 Jan 31;349(6308):429-31 PMID: 1671528
  14. Polymerization activity of an alpha-like DNA polymerase requires a conserved 3'-5' exonuclease active site.
    Mol Cell Biol. 1991 Sep;11(9):4786-95 PMID: 1652064
  15. Chromosomal translocation t(15;17) in human acute promyelocytic leukemia fuses RAR alpha with a novel putative transcription factor, PML.
    Cell. 1991 Aug 23;66(4):663-74 PMID: 1652368
  16. Visualizing DNA replication sites in the cell nucleus.
    Semin Cell Biol. 1991 Apr;2(2):103-15 PMID: 1742475
  17. Alternative splicing of PML transcripts predicts coexpression of several carboxy-terminally different protein isoforms.
    Oncogene. 1992 Jun;7(6):1083-91 PMID: 1594241
  18. Direct repeats of the herpes simplex virus a sequence promote nonconservative homologous recombination that is not dependent on XPF/ERCC4.
    J Virol. 1997 Sep;71(9):6842-9 PMID: 9261409
  19. Effects of mutations in the Exo III motif of the herpes simplex virus DNA polymerase gene on enzyme activities, viral replication, and replication fidelity.
    J Virol. 1997 Oct;71(10):7791-8 PMID: 9311864
  20. Stable overexpression of PML alters regulation of cell cycle progression in HeLa cells.
    Carcinogenesis. 1997 Nov;18(11):2063-9 PMID: 9395203
  21. Cell-cycle regulation of DNA damage-induced expression of the suppressor gene PML.
    Biochem Biophys Res Commun. 1997 Nov 26;240(3):640-6 PMID: 9398618
  22. Evidence for covalent modification of the nuclear dot-associated proteins PML and Sp100 by PIC1/SUMO-1.
    J Cell Biol. 1997 Dec 29;139(7):1621-34 PMID: 9412458
  23. 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. 1998 Dec;72(12):10100-7 PMID: 9811750
  24. Trivalent antimonials induce degradation of the PML-RAR oncoprotein and reorganization of the promyelocytic leukemia nuclear bodies in acute promyelocytic leukemia NB4 cells.
    Blood. 1998 Dec 1;92(11):4308-16 PMID: 9834237
  25. A viral activator of gene expression functions via the ubiquitin-proteasome pathway.
    EMBO J. 1998 Dec 15;17(24):7161-9 PMID: 9857173
  26. Herpes simplex virus type 1 immediate-early protein vmw110 induces the proteasome-dependent degradation of the catalytic subunit of DNA-dependent protein kinase.
    J Virol. 1999 Jan;73(1):650-7 PMID: 9847370
  27. SUMO-1 modification of the acute promyelocytic leukaemia protein PML: implications for nuclear localisation.
    J Cell Sci. 1999 Feb;112 ( Pt 3):381-93 PMID: 9885291
  28. Herpes virus induced proteasome-dependent degradation of the nuclear bodies-associated PML and Sp100 proteins.
    Oncogene. 1999 Jan 28;18(4):935-41 PMID: 10023669
  29. Specific destruction of kinetochore protein CENP-C and disruption of cell division by herpes simplex virus immediate-early protein Vmw110.
    EMBO J. 1999 Mar 15;18(6):1526-38 PMID: 10075924
  30. Viral immediate-early proteins abrogate the modification by SUMO-1 of PML and Sp100 proteins, correlating with nuclear body disruption.
    J Virol. 1999 Jun;73(6):5137-43 PMID: 10233977
  31. Smt3, a SUMO-1 homolog, is conjugated to Cdc3, a component of septin rings at the mother-bud neck in budding yeast.
    Biochem Biophys Res Commun. 1999 Jun 16;259(3):582-7 PMID: 10364461
  32. PIC-1/SUMO-1-modified PML-retinoic acid receptor alpha mediates arsenic trioxide-induced apoptosis in acute promyelocytic leukemia.
    Mol Cell Biol. 1999 Jul;19(7):5170-8 PMID: 10373566
  33. Telomerase-negative immortalized human cells contain a novel type of promyelocytic leukemia (PML) body.
    Cancer Res. 1999 Sep 1;59(17):4175-9 PMID: 10485449
  34. Clinical effects and in vitro studies of trifluorothymidine combined with interferon-alpha for treatment of drug-resistant and -sensitive herpes simplex virus infections.
    J Infect Dis. 1992 Jul;166(1):108-12 PMID: 1318909
  35. A monoclonal antibody recognizing nuclear matrix-associated nuclear bodies.
    J Cell Sci. 1992 Apr;101 ( Pt 4):773-84 PMID: 1527179
  36. IFN enhance expression of Sp100, an autoantigen in primary biliary cirrhosis.
    J Immunol. 1992 Dec 15;149(12):4067-73 PMID: 1281200
  37. Nuclear dot antigens may specify transcriptional domains in the nucleus.
    Mol Cell Biol. 1993 Oct;13(10):6170-9 PMID: 8413218
  38. Retention of the herpes simplex virus type 1 (HSV-1) UL37 protein on single-stranded DNA columns requires the HSV-1 ICP8 protein.
    J Virol. 1994 Jan;68(1):521-5 PMID: 8254765
  39. Modification of discrete nuclear domains induced by herpes simplex virus type 1 immediate early gene 1 product (ICP0).
    J Gen Virol. 1993 Dec;74 ( Pt 12):2679-90 PMID: 8277273
  40. A novel macromolecular structure is a target of the promyelocyte-retinoic acid receptor oncoprotein.
    Cell. 1994 Jan 28;76(2):333-43 PMID: 8293467
  41. Effect of the acute promyelocytic leukemia PML/RAR alpha protein on differentiation and survival of myeloid precursors.
    Leukemia. 1994 Apr;8 Suppl 1:S7-11 PMID: 8152308
  42. 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. 1994 Jun;75 ( Pt 6):1223-33 PMID: 8207389
  43. PML, a growth suppressor disrupted in acute promyelocytic leukemia.
    Mol Cell Biol. 1994 Oct;14(10):6858-67 PMID: 7935403
  44. HSV-1 IE protein Vmw110 causes redistribution of PML.
    EMBO J. 1994 Nov 1;13(21):5062-9 PMID: 7957072
  45. Characterization of a new monoclonal antibody (PG-M3) directed against the aminoterminal portion of the PML gene product: immunocytochemical evidence for high expression of PML proteins on activated macrophages, endothelial cells, and epithelia.
    Blood. 1995 Apr 1;85(7):1871-80 PMID: 7535592
  46. Sequestration of PML and Sp100 proteins in an intranuclear viral structure during herpes simplex virus type 1 infection.
    Exp Cell Res. 1995 Dec;221(2):448-61 PMID: 7493645
  47. Nuclear domain 10 as preexisting potential replication start sites of herpes simplex virus type-1.
    Virology. 1996 Mar 1;217(1):67-75 PMID: 8599237
  48. Functional order of assembly of herpes simplex virus DNA replication proteins into prereplicative site structures.
    J Virol. 1996 Mar;70(3):1759-67 PMID: 8627698
  49. Effect of PML and PML-RAR on the transactivation properties and subcellular distribution of steroid hormone receptors.
    Mol Endocrinol. 1995 Dec;9(12):1791-803 PMID: 8614415
  50. In vitro studies on cellular and molecular mechanisms of arsenic trioxide (As2O3) in the treatment of acute promyelocytic leukemia: As2O3 induces NB4 cell apoptosis with downregulation of Bcl-2 expression and modulation of PML-RAR alpha/PML proteins.
    Blood. 1996 Aug 1;88(3):1052-61 PMID: 8704214
  51. Nuclear domain 10 (ND10) associated proteins are also present in nuclear bodies and redistribute to hundreds of nuclear sites after stress.
    J Cell Biochem. 1995 Dec;59(4):498-513 PMID: 8749719
  52. Interferon augments PML and PML/RAR alpha expression in normal myeloid and acute promyelocytic cells and cooperates with all-trans retinoic acid to induce maturation of a retinoid-resistant promyelocytic cell line.
    Blood. 1996 Nov 15;88(10):3926-36 PMID: 8916959
  53. The PML and PML/RARalpha domains: from autoimmunity to molecular oncology and from retinoic acid to arsenic.
    Exp Cell Res. 1996 Dec 15;229(2):253-60 PMID: 8986606
  54. Formation of herpes simplex virus type 1 replication compartments by transfection: requirements and localization to nuclear domain 10.
    J Virol. 1997 Mar;71(3):2390-9 PMID: 9032376
  55. Assembly of complete, functionally active herpes simplex virus DNA replication compartments and recruitment of associated viral and cellular proteins in transient cotransfection assays.
    J Virol. 1997 Apr;71(4):3146-60 PMID: 9060678
  56. Assembly of herpes simplex virus replication proteins at two distinct intranuclear sites.
    Virology. 1997 Mar 3;229(1):113-25 PMID: 9123852
  57. Arsenic-induced PML targeting onto nuclear bodies: implications for the treatment of acute promyelocytic leukemia.
    Proc Natl Acad Sci U S A. 1997 Apr 15;94(8):3978-83 PMID: 9108090
  58. Use of arsenic trioxide (As2O3) in the treatment of acute promyelocytic leukemia (APL): I. As2O3 exerts dose-dependent dual effects on APL cells.
    Blood. 1997 May 1;89(9):3345-53 PMID: 9129041
  59. Herpes simplex virus type 1 prereplicative sites are a heterogeneous population: only a subset are likely to be precursors to replication compartments.
    J Virol. 1997 Jun;71(6):4771-81 PMID: 9151871
  60. Human cytomegalovirus immediate early interaction with host nuclear structures: definition of an immediate transcript environment.
    J Cell Biol. 1997 Jul 14;138(1):5-16 PMID: 9214377
  61. A dynamic connection between centromeres and ND10 proteins.
    J Cell Sci. 1999 Oct;112 ( Pt 20):3443-54 PMID: 10504293
  62. Herpes simplex virus ICP0 mutants are hypersensitive to interferon.
    J Virol. 2000 Feb;74(4):2052-6 PMID: 10644380
  63. Promyelocytic leukemia (PML) nuclear bodies are protein structures that do not accumulate RNA.
    J Cell Biol. 2000 Jan 24;148(2):283-92 PMID: 10648561
  64. Review: properties and assembly mechanisms of ND10, PML bodies, or PODs.
    J Struct Biol. 2000 Apr;129(2-3):278-87 PMID: 10806078
  65. Cross-reactivity of the anti-PML antibody PG-M3 with the herpes simplex virus type 1 immediate early protein ICP4.
    J Gen Virol. 2000 Jul;81(Pt 7):1773-7 PMID: 10859383
  66. Interferon coordinately inhibits the disruption of PML-positive ND10 and immediate-early gene expression by herpes simplex virus.
    J Interferon Cytokine Res. 2000 Sep;20(9):805-15 PMID: 11032400
  67. Further evidence for a non-random chromosomal abnormality in acute promyelocytic leukemia.
    Int J Cancer. 1977 Dec 15;20(6):869-72 PMID: 271143
  68. Monoclonal antibodies to herpes simplex virus type 1 proteins, including the immediate-early protein ICP 4.
    Infect Immun. 1981 Dec;34(3):684-92 PMID: 6277788
  69. Genetic analysis of temperature-sensitive mutants which define the gene for the major herpes simplex virus type 1 DNA-binding protein.
    J Virol. 1983 Jan;45(1):354-66 PMID: 6296442
  70. Fine mapping and molecular cloning of mutations in the herpes simplex virus DNA polymerase locus.
    J Virol. 1984 Jan;49(1):236-47 PMID: 6317891
  71. The intranuclear location of a herpes simplex virus DNA-binding protein is determined by the status of viral DNA replication.
    Cell. 1984 Apr;36(4):857-68 PMID: 6323024
  72. Sensitivity of arabinosyladenine-resistant mutants of herpes simplex virus to other antiviral drugs and mapping of drug hypersensitivity mutations to the DNA polymerase locus.
    J Virol. 1985 Feb;53(2):477-88 PMID: 2982032
  73. Expression of herpes simplex virus type 1 DNA polymerase gene by in vitro translation and effects of gene deletions on activity.
    J Virol. 1988 Sep;62(9):3224-32 PMID: 2841474
  74. Progressive esophagitis from acyclovir-resistant herpes simplex. Clinical roles for DNA polymerase mutants and viral heterogeneity?
    Ann Intern Med. 1989 Dec 1;111(11):893-9 PMID: 2554768
  75. Isolation and characterization of herpes simplex virus mutants containing engineered mutations at the DNA polymerase locus.
    J Virol. 1990 May;64(5):2208-16 PMID: 2157881
Article Info
Journal
Journal of virology
Abbr.
J Virol
ISSN
0022-538X
DOI
10.1128/JVI.75.5.2353-2367.2001
Published
2001-03-00
Pages
2353-67
Language
English
Region
United States
NLM ID
0113724
PMCID
PMC114819
Subset
IM
Grants
NIDCR NIH HHS · R01 DE010051 · United States
NIAID NIH HHS · AI19838 · United States
PHS HHS · A121747 · United States
NIDCR NIH HHS · R01DE10051 · United States
NIAID NIH HHS · R01 AI019838 · United States
External Links
PubMed source DOI: 10.1128/JVI.75.5.2353-2367.2001 PMC Full Text View journal details
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2