Home LiteratureArticle Details
PMID: 14610173 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

ORF73 of herpesvirus Saimiri strain C488 tethers the viral genome to metaphase chromosomes and binds to cis-acting DNA sequences in the terminal repeats.

Journal of virology ·Vol. 77 ·No. 23 ·2003-12-00 ·Pages 12494-506

Verma SC, Robertson ES

Abstract

Kaposi's sarcoma (KS)-associated herpesvirus (KSHV), a human oncogenic gamma-2-herpesvirus, transforms human endothelial cells and establishes latent infection at a low efficiency in vitro. During latent infection, only a limited number of genes are expressed, and the circularized viral genome is maintained as a multicopy episome. Latency-associated nuclear antigen (LANA), exclusively expressed during latency, has been shown to have a multifunctional role in KS pathogenesis. LANA tethers the viral episome to the host chromosome, thus ensuring efficient persistence of the viral genome during successive rounds of cell division. Besides episome maintenance, LANA modulates the expression of genes of various cellular and viral pathways, including those of retinoblastoma protein and p53. Herpesvirus saimiri (HVS), another gamma-2-herpesvirus, primarily infects New World primates. Orf73, encoding the nuclear antigen of HVS, is the positional homolog of the LANA gene, and the ORF73 protein has some sequence homology to KSHV LANA. However, the function of ORF73 of HVS has not been thoroughly investigated. In this report, we show that HVS ORF73 may be important for episome persistence and colocalizes with the HVS genomic DNA on metaphase chromosomes. Furthermore, HVS terminal repeats (TRs) contain a cis-acting sequence similar to that in KSHV TRs, suggesting that the LANA binding sequence is conserved between these two viruses. This cis-acting element is sufficient to bind HVS ORF73 from strains C488 and A11, and plasmids containing the HVS C488 TR element are maintained and replicate in HVS C488 ORF73-expressing cells.

MeSH Terms
Amino Acid Sequence Animals Antibodies, Viral/immunology Base Sequence Callithrix Cell Line, Transformed Chromosomes DNA Replication DNA, Viral/biosynthesis Fluorescent Antibody Technique Genome, Viral Herpesvirus 2, Saimiriine/genetics,immunology Humans Metaphase Molecular Sequence Data Open Reading Frames/immunology Sequence Homology, Amino Acid
Chemicals
Antibodies, Viral DNA, Viral
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Verma Subhash C
Department of Microbiology. Tumor Virology Program, Abramson Comprehensive Cancer Center, School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania 19104, USA.
Robertson Erle S
References (72)
72 references, click to expand
  1. Herpesvirus saimiri strains from three DNA subgroups have different oncogenic potentials in New Zealand white rabbits.
    J Virol. 1989 Sep;63(9):3601-11 PMID: 2547988
  2. Expression of interleukin 2 receptors in T cells transformed by strains of Herpesvirus saimiri representing three DNA subgroups.
    Intervirology. 1989;30(4):213-26 PMID: 2550388
  3. Advanced mammalian gene transfer: high titre retroviral vectors with multiple drug selection markers and a complementary helper-free packaging cell line.
    Nucleic Acids Res. 1990 Jun 25;18(12):3587-96 PMID: 2194165
  4. DNA binding activity is required for EBNA 1-dependent transcriptional activation and DNA replication.
    Virology. 1992 Apr;187(2):591-603 PMID: 1312270
  5. Stable growth transformation of human T lymphocytes by herpesvirus saimiri.
    Proc Natl Acad Sci U S A. 1992 Apr 1;89(7):3116-9 PMID: 1313581
  6. Primary structure of the herpesvirus saimiri genome.
    J Virol. 1992 Aug;66(8):5047-58 PMID: 1321287
  7. Virus-encoded cyclin.
    Mol Cell Biol. 1994 Nov;14(11):7235-44 PMID: 7935438
  8. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice.
    Nucleic Acids Res. 1994 Nov 11;22(22):4673-80 PMID: 7984417
  9. Distinct patterns of viral antigen expression in Epstein-Barr virus and Kaposi's sarcoma-associated herpesvirus coinfected body-cavity-based lymphoma cell lines: potential switches in latent gene expression due to coinfection.
    Virology. 1999 Sep 15;262(1):18-30 PMID: 10489337
  10. Functional dissection of latency-associated nuclear antigen 1 of Kaposi's sarcoma-associated herpesvirus involved in latent DNA replication and transcription of terminal repeats of the viral genome.
    J Virol. 2002 Oct;76(20):10320-31 PMID: 12239308
  11. Protein interactions targeting the latency-associated nuclear antigen of Kaposi's sarcoma-associated herpesvirus to cell chromosomes.
    J Virol. 2002 Nov;76(22):11596-604 PMID: 12388720
  12. The latency-associated nuclear antigen of Kaposi's sarcoma-associated herpesvirus supports latent DNA replication in dividing cells.
    J Virol. 2002 Nov;76(22):11677-87 PMID: 12388727
  13. Identification of herpesvirus-like DNA sequences in AIDS-associated Kaposi's sarcoma.
    Science. 1994 Dec 16;266(5192):1865-9 PMID: 7997879
  14. Detection of herpesvirus-like DNA sequences in Kaposi's sarcoma in patients with and those without HIV infection.
    N Engl J Med. 1995 May 4;332(18):1181-5 PMID: 7700310
  15. Kaposi's sarcoma-associated herpesvirus-like DNA sequences in AIDS-related body-cavity-based lymphomas.
    N Engl J Med. 1995 May 4;332(18):1186-91 PMID: 7700311
  16. Herpes-like sequences in HIV-infected and uninfected Kaposi's sarcoma patients.
    Science. 1995 Apr 28;268(5210):582-3 PMID: 7725108
  17. The DNA sequence of equine herpesvirus 2.
    J Mol Biol. 1995 Jun 9;249(3):520-8 PMID: 7783207
  18. A role for a new herpes virus (KSHV) in different forms of Kaposi's sarcoma.
    Nat Med. 1995 Jul;1(7):707-8 PMID: 7585156
  19. Kaposi's sarcoma-associated herpesvirus infects endothelial and spindle cells.
    Nat Med. 1995 Dec;1(12):1274-8 PMID: 7489408
  20. Primary effusion lymphoma: a distinct clinicopathologic entity associated with the Kaposi's sarcoma-associated herpes virus.
    Blood. 1996 Jul 15;88(2):645-56 PMID: 8695812
  21. Latent nuclear antigen of Kaposi's sarcoma-associated herpesvirus interacts with RING3, a homolog of the Drosophila female sterile homeotic (fsh) gene.
    J Virol. 1999 Dec;73(12):9789-95 PMID: 10559289
  22. The latency-associated nuclear antigen tethers the Kaposi's sarcoma-associated herpesvirus genome to host chromosomes in body cavity-based lymphoma cells.
    Virology. 1999 Nov 25;264(2):254-64 PMID: 10562490
  23. p53 inhibition by the LANA protein of KSHV protects against cell death.
    Nature. 1999 Dec 23-30;402(6764):889-94 PMID: 10622254
  24. HHV-8 is associated with a plasmablastic variant of Castleman disease that is linked to HHV-8-positive plasmablastic lymphoma.
    Blood. 2000 Feb 15;95(4):1406-12 PMID: 10666218
  25. Distinct transcriptional and functional properties of the R transactivator gene orf50 of the transforming herpesvirus saimiri strain C488.
    Virology. 2000 Mar 1;268(1):167-77 PMID: 10683339
  26. Herpesvirus saimiri-transformed macaque T cells are tolerated and do not cause lymphoma after autologous reinfusion.
    Blood. 2000 May 15;95(10):3256-61 PMID: 10807797
  27. Analysis of gene expression in a human cell line stably transduced with herpesvirus saimiri.
    J Virol. 2000 Aug;74(16):7331-7 PMID: 10906186
  28. Carboxy terminus of human herpesvirus 8 latency-associated nuclear antigen mediates dimerization, transcriptional repression, and targeting to nuclear bodies.
    J Virol. 2000 Sep;74(18):8532-40 PMID: 10954554
  29. Human herpesvirus 8 LANA interacts with proteins of the mSin3 corepressor complex and negatively regulates Epstein-Barr virus gene expression in dually infected PEL cells.
    J Virol. 2000 Oct;74(20):9637-45 PMID: 11000236
  30. The latent nuclear antigen of Kaposi sarcoma-associated herpesvirus targets the retinoblastoma-E2F pathway and with the oncogene Hras transforms primary rat cells.
    Nat Med. 2000 Oct;6(10):1121-7 PMID: 11017143
  31. Latency-associated nuclear antigen of Kaposi's sarcoma-associated herpesvirus (human herpesvirus-8) binds ATF4/CREB2 and inhibits its transcriptional activation activity.
    J Gen Virol. 2000 Nov;81(Pt 11):2645-52 PMID: 11038375
  32. Characterization of the herpesvirus saimiri ORF73 gene product.
    J Gen Virol. 2000 Nov;81(Pt 11):2653-8 PMID: 11038376
  33. Modulation of cellular and viral gene expression by the latency-associated nuclear antigen of Kaposi's sarcoma-associated herpesvirus.
    J Virol. 2001 Jan;75(1):458-68 PMID: 11119614
  34. Differential regulation of the overlapping Kaposi's sarcoma-associated herpesvirus vGCR (orf74) and LANA (orf73) promoters.
    J Virol. 2001 Feb;75(4):1798-807 PMID: 11160678
  35. Kaposi's sarcoma-associated herpesvirus latency-associated nuclear antigen 1 mediates episome persistence through cis-acting terminal repeat (TR) sequence and specifically binds TR DNA.
    J Virol. 2001 Apr;75(7):3250-8 PMID: 11238851
  36. Close but distinct regions of human herpesvirus 8 latency-associated nuclear antigen 1 are responsible for nuclear targeting and binding to human mitotic chromosomes.
    J Virol. 2001 Apr;75(8):3948-59 PMID: 11264383
  37. The latency-associated nuclear antigen of Kaposi's sarcoma-associated herpesvirus transactivates the telomerase reverse transcriptase promoter.
    J Biol Chem. 2001 Jun 22;276(25):22971-8 PMID: 11313352
  38. DNA binding and modulation of gene expression by the latency-associated nuclear antigen of Kaposi's sarcoma-associated herpesvirus.
    J Virol. 2001 Sep;75(17):7882-92 PMID: 11483733
  39. The transcriptional activity of cAMP response element-binding protein-binding protein is modulated by the latency associated nuclear antigen of Kaposi's sarcoma-associated herpesvirus.
    J Biol Chem. 2001 Aug 17;276(33):31016-22 PMID: 11425857
  40. Latency-associated nuclear antigen encoded by Kaposi's sarcoma-associated herpesvirus interacts with Tat and activates the long terminal repeat of human immunodeficiency virus type 1 in human cells.
    J Virol. 2001 Sep;75(18):8761-71 PMID: 11507221
  41. The Kaposi's sarcoma-associated herpesvirus latency-associated nuclear antigen binds to specific sequences at the left end of the viral genome through its carboxy-terminus.
    Virology. 2001 Dec 20;291(2):241-59 PMID: 11878894
  42. Latency-associated nuclear antigen (LANA) cooperatively binds to two sites within the terminal repeat, and both sites contribute to the ability of LANA to suppress transcription and to facilitate DNA replication.
    J Biol Chem. 2002 Jul 26;277(30):27401-11 PMID: 12015325
  43. The terminal repeats and latency-associated nuclear antigen of herpesvirus saimiri are essential for episomal persistence of the viral genome.
    J Gen Virol. 2002 Sep;83(Pt 9):2269-78 PMID: 12185282
  44. The seroepidemiology of human herpesvirus 8 (Kaposi's sarcoma-associated herpesvirus): distribution of infection in KS risk groups and evidence for sexual transmission.
    Nat Med. 1996 Aug;2(8):918-24 PMID: 8705863
  45. KSHV antibodies among Americans, Italians and Ugandans with and without Kaposi's sarcoma.
    Nat Med. 1996 Aug;2(8):925-8 PMID: 8705864
  46. Regulation of the herpesvirus saimiri oncogene stpC, similar to that of T-cell activation genes, in growth-transformed human T lymphocytes.
    J Virol. 1996 Sep;70(9):6012-9 PMID: 8709223
  47. Kaposi's sarcoma-associated herpesvirus infection prior to onset of Kaposi's sarcoma.
    AIDS. 1996 Feb;10(2):175-80 PMID: 8838705
  48. Nucleotide sequence of the Kaposi sarcoma-associated herpesvirus (HHV8).
    Proc Natl Acad Sci U S A. 1996 Dec 10;93(25):14862-7 PMID: 8962146
  49. Oncogenic forms of NOTCH1 lacking either the primary binding site for RBP-Jkappa or nuclear localization sequences retain the ability to associate with RBP-Jkappa and activate transcription.
    J Biol Chem. 1997 Apr 25;272(17):11336-43 PMID: 9111040
  50. The cyclin encoded by Kaposi's sarcoma-associated herpesvirus stimulates cdk6 to phosphorylate the retinoblastoma protein and histone H1.
    J Virol. 1997 Jun;71(6):4193-8 PMID: 9151805
  51. The 222- to 234-kilodalton latent nuclear protein (LNA) of Kaposi's sarcoma-associated herpesvirus (human herpesvirus 8) is encoded by orf73 and is a component of the latency-associated nuclear antigen.
    J Virol. 1997 Aug;71(8):5915-21 PMID: 9223481
  52. A role for natural simian immunodeficiency virus and human immunodeficiency virus type 1 nef alleles in lymphocyte activation.
    J Virol. 1997 Aug;71(8):6094-9 PMID: 9223503
  53. Primary structure of the alcelaphine herpesvirus 1 genome.
    J Virol. 1997 Sep;71(9):6517-25 PMID: 9261371
  54. The superantigen-homologous viral immediate-early gene ie14/vsag in herpesvirus saimiri-transformed human T cells.
    J Virol. 1997 Dec;71(12):9124-33 PMID: 9371569
  55. Identification of minimal oriP of Epstein-Barr virus required for DNA replication.
    J Biochem. 1998 Jan;123(1):175-81 PMID: 9504426
  56. Herpesvirus saimiri transforms human T-cell clones to stable growth without inducing resistance to apoptosis.
    J Virol. 1998 Apr;72(4):3138-45 PMID: 9525639
  57. Modified Hirt procedure for rapid purification of extrachromosomal DNA from mammalian cells.
    Biotechniques. 1998 May;24(5):760-2 PMID: 9591124
  58. A cluster of latently expressed genes in Kaposi's sarcoma-associated herpesvirus.
    J Virol. 1998 Oct;72(10):8309-15 PMID: 9733875
  59. Distribution of human herpesvirus-8 latently infected cells in Kaposi's sarcoma, multicentric Castleman's disease, and primary effusion lymphoma.
    Proc Natl Acad Sci U S A. 1999 Apr 13;96(8):4546-51 PMID: 10200299
  60. Transcriptional analysis of human herpesvirus-8 open reading frames 71, 72, 73, K14, and 74 in a primary effusion lymphoma cell line.
    Virology. 1999 Apr 25;257(1):84-94 PMID: 10208923
  61. Efficient persistence of extrachromosomal KSHV DNA mediated by latency-associated nuclear antigen.
    Science. 1999 Apr 23;284(5414):641-4 PMID: 10213686
  62. High expression of HHV-8-encoded ORF73 protein in spindle-shaped cells of Kaposi's sarcoma.
    Am J Pathol. 1999 Jul;155(1):47-52 PMID: 10393835
  63. Chromosome binding site of latency-associated nuclear antigen of Kaposi's sarcoma-associated herpesvirus is essential for persistent episome maintenance and is functionally replaced by histone H1.
    J Virol. 2002 Dec;76(24):12917-24 PMID: 12438617
  64. The latency-associated nuclear antigen of Kaposi's sarcoma-associated herpesvirus permits replication of terminal repeat-containing plasmids.
    J Virol. 2003 Feb;77(4):2779-83 PMID: 12552022
  65. Selective extraction of polyoma DNA from infected mouse cell cultures.
    J Mol Biol. 1967 Jun 14;26(2):365-9 PMID: 4291934
  66. An apparently new herpesvirus from primary kidney cultures of the squirrel monkey (Saimiri sciureus).
    Lab Anim Care. 1968 Jun;18(3):374-81 PMID: 4233372
  67. Herpesvirus saimiri DNA in tumor cells--deleted sequences and sequence rearrangements.
    J Virol. 1981 Aug;39(2):497-509 PMID: 6268839
  68. Detection of circular and linear herpesvirus DNA molecules in mammalian cells by gel electrophoresis.
    J Virol. 1984 Apr;50(1):248-54 PMID: 6321792
  69. Classification of herpesvirus saimiri into three groups based on extreme variation in a DNA region required for oncogenicity.
    J Virol. 1984 Dec;52(3):938-44 PMID: 6092721
  70. Stable replication of plasmids derived from Epstein-Barr virus in various mammalian cells.
    Nature. 1985 Feb 28-Mar 6;313(6005):812-5 PMID: 2983224
  71. Random association of Epstein-Barr virus genomes with host cell metaphase chromosomes in Burkitt's lymphoma-derived cell lines.
    J Virol. 1985 Oct;56(1):328-32 PMID: 2993664
  72. Sequence-specific DNA binding of the Epstein-Barr virus nuclear antigen (EBNA-1) to clustered sites in the plasmid maintenance region.
    Cell. 1985 Oct;42(3):859-68 PMID: 2996781
Article Info
Journal
Journal of virology
Abbr.
J Virol
ISSN
0022-538X
Published
2003-12-00
Pages
12494-506
Language
English
Region
United States
NLM ID
0113724
PMCID
PMC262571
Subset
IM
Grants
NCI NIH HHS · R01 CA091792 · United States
NCI NIH HHS · CA072510 · United States
NCI NIH HHS · CA091792 · United States
NIDCR NIH HHS · DE01436 · United States
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