DOI: 10.1099/0022-1317-83-1-179. Latent nuclear antigen of Kaposi’s sarcoma herpesvirus/human herpesvirus-8 induces and relocates RING3 to nuclear heterochromatin regions

Latent nuclear antigen of Kaposi’s sarcoma herpesvirus/human herpesvirus-8 induces and relocates RING3 to nuclear heterochromatin regions

10.1099/0022-1317-83-1-179

Crossref journal-article

Microbiology Society

Journal of General Virology (345)

Abstract

LANA, the major latency-associated nuclear antigen of Kaposi’s sarcoma herpesvirus/human herpesvirus-8 (KSHV/HHV-8), binds RING3 protein, one of five human homologues of thefsh(female sterile homeotic) gene product ofDrosophila. In KSHV/HHV-8-infected cells LANA and the viral episomes accumulate in heterochromatin-associated nuclear bodies. Here we show that in several KSHV/HHV-8-negative cell lines derived from carcinomas, sarcomas and lymphomas, RING3 was expressed at low levels, primarily localized to the euchromatin, and dissociated from the chromosomes during mitosis. In contrast, in KSHV/HHV-8-infected body cavity lymphoma cells the bulk of RING3 localizes to the LANA nuclear bodies and remains associated with the chromosomes during cell division. KSHV/HHV-8-infected body cavity lymphoma cells expressed RING3 at much higher levels than cells without the virus. Transfection of full-length LANA, but not the C terminus alone, greatly induced RING3 gene expression, and LANA and RING3 co-localized even in the transfected cells, in the absence of KSHV/HHV-8 viral DNA. High levels of LANA expression led to the disappearance of heterochromatin in both human and mouse cells. We suggest that LANA and RING3 may create a local euchromatic microenvironment around the viral episomes that are anchored to the heterochromatin.

Authors 8

Karin Mattsson (first)
Csaba Kiss (additional)
Georgina M. Platt (additional)
Guy R. Simpson (additional)
Elena Kashuba (additional)
George Klein (additional)
Thomas F. Schulz (additional)
Laszlo Szekely (additional)

References 27 Referenced 51

10.1126/science.284.5414.641 / Science / Efficient persistence of extrachromosomal KSHV DNA mediated by latency-associated nuclear antigen by Ballestas (1999)
10.3109/10425179209020804 / DNA Sequence / A homologue of the Drosophila female sterile homeotic (fsh) gene in the class II region of the human MHC by Beck (1992)
10.3109/10425179609015640 / DNA Sequence / Organisation and functions of class II genes and molecules by Beck (1996)
10.1016/S0065-230X(08)60739-3 / Advances in Cancer Research / Kaposi’s sarcoma-associated herpesvirus by Boshoff (1998)
10.1006/viro.1999.9999 / Virology / The latency-associated nuclear antigen tethers the Kaposi’s sarcoma-associated herpesvirus genome to host chromosomes in body cavity-based lymphoma cells by Cotter (1999)
10.1128/MCB.20.17.6537-6549.2000 / Molecular and Cellular Biology / A bromodomain protein, MCAP, associates with mitotic chromosomes and affects G2-to-M transition by Dey (2000)
10.1038/20974 / Nature / Structure and ligand of a histone acetyltransferase bromodomain by Dhalluin (1999)
10.1073/pnas.96.8.4546 / Proceedings of the National Academy of Sciences, USA / Distribution of human herpesvirus-8 latently infected cells in Kaposi’s sarcoma, multicentric Castleman’s disease, and primary effusion lymphoma by Dupin (1999)
10.1128/JVI.61.12.3870-3878.1987 / Journal of Virology / Monoclonal and polyclonal antibodies against Epstein–Barr virus nuclear antigen 5 (EBNA-5) detect multiple protein species in Burkitt’s lymphoma and lymphoblastoid cell lines by Finke (1987)
10.1038/47266 / Nature / p53 inhibition by the LANA protein of KSHV protects against cell death by Friborg (1999)
10.1097/00129039-199909000-00009 / Applied Immunohistochemistry & Molecular Morphology / Computer programs that allow fast acquisition, visualization and overlap quantitation of fluorescent 3D microscopic objects using nearest neighbor deconvolution algorithm by Holmvall (1999)
10.1006/geno.1997.5000 / Genomics / Identification and characterization of BRDT: a testis-specific gene related to the bromodomain genes RING3 and Drosophila fsh by Jones (1997)
10.1016/S0002-9440(10)65097-3 / American Journal of Pathology / High expression of HHV-8-encoded ORF73 protein in spindle-shaped cells of Kaposi’s sarcoma by Katano (1999)
10.1172/JCI119804 / Journal of Clinical Investigation / Identification of the gene encoding the major latency-associated nuclear antigen of the Kaposi’s sarcoma-associated herpesvirus by Kedes (1997)
{'key': 'R15', 'first-page': '19', 'article-title': 'Identification of a major latent nuclear antigen, LNA-1, in the human herpesvirus 8 genome', 'volume': '1', 'author': 'Kellam', 'year': '1997', 'journal-title': 'Journal of Human Virology'} / Journal of Human Virology / Identification of a major latent nuclear antigen, LNA-1, in the human herpesvirus 8 genome by Kellam (1997)
10.1128/JVI.74.20.9637-9645.2000 / Journal of Virology / 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 by Krithivas (2000)
10.4049/jimmunol.166.3.1945 / Journal of Immunology / Host responses to Plasmodium yoelii hepatic stages: a paradigm in host–parasite interaction by Lau (2001)
10.1073/pnas.86.10.3738 / Proceedings of the National Academy of Sciences, USA / Cloning and molecular characterization of the trithorax locus of Drosophila melanogaster by Mozer (1989)
10.1128/JVI.73.12.9789-9795.1999 / Journal of Virology / Latent nuclear antigen of Kaposi’s sarcoma-associated herpesvirus interacts with RING3, a homolog of the Drosophila female sterile homeotic (fsh) gene by Platt (1999)
10.1099/0022-1317-82-2-345 / Journal of General Virology / Proteasome inhibitor induces nucleolar translocation of the EBV-encoded EBNA-5 by Pokrovskaja (2001)
10.1038/80459 / Nature Medicine / The latent nuclear antigen of Kaposi sarcoma-associated herpesvirus targets the retinoblastoma–E2F pathway and with the oncogene Hras transforms primary rat cells by Radkov (2000)
10.1128/JVI.71.8.5915-5921.1997 / Journal of Virology / 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 by Rainbow (1997)
10.1128/JVI.75.1.458-468.2001 / Journal of Virology / Modulation of the cellular and viral gene expression by the latency-associated nuclear antigen of Kaposi’s sarcoma-associated herpesvirus by Renne (2001)
10.1242/jcs.111.23.3541 / Journal of Cell Science / Expression and potential role of Fsrg1, a murine bromodomain-containing homologue of the Drosophila gene female sterile homeotic by Rhee (1998)
10.1099/0022-1317-79-6-1445 / Journal of General Virology / Restricted expression of Epstein–Barr virus (EBV)-encoded, growth transformation-associated antigens in an EBV- and human herpesvirus type 8-carrying body cavity lymphoma line by Szekely (1998)
10.1099/0022-1317-80-11-2889 / Journal of General Virology / Human herpesvirus-8-encoded LNA-1 accumulates in heterochromatin-associated nuclear bodies by Szekely (1999)
10.1006/geno.1998.5262 / Genomics / Nucleotide sequence of the ring3 gene in the class II region of the mouse MHC and its abundant expression in testicular germ cells by Taniguchi (1998)

Dates

Type	When
Created	10 years ago (Aug. 26, 2015, 12:26 p.m.)
Deposited	3 years, 3 months ago (May 20, 2022, 7:44 p.m.)
Indexed	11 months, 2 weeks ago (Sept. 15, 2024, 5:21 a.m.)
Issued	23 years, 8 months ago (Jan. 1, 2002)
Published	23 years, 8 months ago (Jan. 1, 2002)
Published Print	23 years, 8 months ago (Jan. 1, 2002)

Funders 0

None

BibTeX

@article{Mattsson_2002, title={Latent nuclear antigen of Kaposi’s sarcoma herpesvirus/human herpesvirus-8 induces and relocates RING3 to nuclear heterochromatin regions}, volume={83}, ISSN={1465-2099}, url={http://dx.doi.org/10.1099/0022-1317-83-1-179}, DOI={10.1099/0022-1317-83-1-179}, number={1}, journal={Journal of General Virology}, publisher={Microbiology Society}, author={Mattsson, Karin and Kiss, Csaba and Platt, Georgina M. and Simpson, Guy R. and Kashuba, Elena and Klein, George and Schulz, Thomas F. and Szekely, Laszlo}, year={2002}, month=jan, pages={179–188} }

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  "ISSN": [
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