Abstract
Lymphocytic choriomeningitis virus (LCMV) induces type I interferon (alpha and beta interferon [IFN-alpha and IFN-beta]) upon infection and yet is sensitive to the addition of type II interferon (gamma interferon [IFN-gamma]) to the culture media. This sensitivity is biologically important because it correlates inversely with the ability of certain LCMV strains to persist in mice (D. Moskophidis, M. Battegay, M. A. Bruendler, E. Laine, I. Gresser, and R. M. Zinkernagel, J. Virol. 68:1951-1955, 1994). The cellular oncoprotein PML is induced by both IFN-alpha/beta and IFN-gamma, and PML binds the LCMV Z protein and becomes redistributed within cells from nucleus to cytoplasm upon LCMV infection. In the present study, increased PML expression results in diminished LCMV replication, implicating PML in the IFN sensitivity of LCMV. Virus production in PML -/- murine embryonic fibroblasts (MEF) exceeds virus production in PML +/+ MEF, and this difference is exacerbated by IFN treatment that upregulates PML expression. IFN-gamma also diminishes LCMV production in PML -/- cells; therefore, viral IFN sensitivity is not entirely due to PML. Both viral mRNA production and viral protein production decrease as PML expression increases. Here we propose that PML reduces LCMV transcription through its interaction with the Z protein.
MeSH Terms
Animals
Carrier Proteins/metabolism
Cell Division/drug effects
Interferons/pharmacology
Intracellular Signaling Peptides and Proteins
Lymphocytic choriomeningitis virus/drug effects
Mice
Neoplasm Proteins/physiology
Nuclear Proteins
Promyelocytic Leukemia Protein
RNA, Messenger/analysis
RNA, Viral/analysis
Transcription Factors/physiology
Tumor Suppressor Proteins
Viral Proteins/analysis,genetics
Virus Replication/drug effects
Chemicals
Carrier Proteins
Intracellular Signaling Peptides and Proteins
Neoplasm Proteins
Nuclear Proteins
Pml protein, mouse
Promyelocytic Leukemia Protein
RNA, Messenger
RNA, Viral
Transcription Factors
Tumor Suppressor Proteins
Viral Proteins
p11 Z protein, Lymphocytic choriomeningitis virus
Interferons
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Djavani M
Institute of Human Virology, University of Maryland Biotechnology Center, 725 W. Lombard St., Baltimore, MD 21201, USA.
Rodas J
Lukashevich I S
Horejsh D
Pandolfi P P
Borden K L
Salvato M S
References (20)
20 references, click to expand
-
Interferons and their actions.
Annu Rev Biochem. 1987;56:727-77
PMID: 2441659
-
Distinctive RNA transcriptase, polyadenylic acid polymerase, and polyuridylic acid polymerase activities associated with Pichinde virus.
J Virol. 1979 Apr;30(1):98-107
PMID: 225533
-
Reassessing the hemostatic disorder associated with acute promyelocytic leukemia.
Blood. 1992 Feb 1;79(3):543-53
PMID: 1732003
-
The Tacaribe arenavirus small zinc finger protein is required for both mRNA synthesis and genome replication.
J Virol. 1993 Feb;67(2):807-12
PMID: 8419647
-
Resistance of lymphocytic choriomeningitis virus to alpha/beta interferon and to gamma interferon.
J Virol. 1994 Mar;68(3):1951-5
PMID: 8107255
-
The PML growth-suppressor has an altered expression in human oncogenesis.
Oncogene. 1995 Apr 6;10(7):1315-24
PMID: 7731682
-
The acute promyelocytic leukaemia-associated PML gene is induced by interferon.
Oncogene. 1995 Sep 7;11(5):871-6
PMID: 7545807
-
Induction of the PML protein by interferons in normal and APL cells.
Leukemia. 1995 Dec;9(12):2027-33
PMID: 8609713
-
Transcriptional induction of the PML growth suppressor gene by interferons is mediated through an ISRE and a GAS element.
Oncogene. 1995 Dec 21;11(12):2565-73
PMID: 8545113
-
Completion of the Lassa fever virus sequence and identification of a RING finger open reading frame at the L RNA 5' End.
Virology. 1997 Sep 1;235(2):414-8
PMID: 9281522
-
The promyelocytic leukemia protein PML has a pro-apoptotic activity mediated through its RING domain.
FEBS Lett. 1997 Nov 24;418(1-2):30-4
PMID: 9414089
-
An arenavirus RING (zinc-binding) protein binds the oncoprotein promyelocyte leukemia protein (PML) and relocates PML nuclear bodies to the cytoplasm.
J Virol. 1998 Jan;72(1):758-66
PMID: 9420283
-
Resistance to virus infection conferred by the interferon-induced promyelocytic leukemia protein.
J Virol. 1998 Feb;72(2):1043-51
PMID: 9444998
-
Role of PML in cell growth and the retinoic acid pathway.
Science. 1998 Mar 6;279(5356):1547-51
PMID: 9488655
-
Two RING finger proteins, the oncoprotein PML and the arenavirus Z protein, colocalize with the nuclear fraction of the ribosomal P proteins.
J Virol. 1998 May;72(5):3819-26
PMID: 9557665
-
Cellular factors in the transcription and replication of viral RNA genomes: a parallel to DNA-dependent RNA transcription.
Virology. 1998 Apr 25;244(1):1-12
PMID: 9581772
-
A role for PML and the nuclear body in genomic stability.
Oncogene. 1999 Dec 23;18(56):7941-7
PMID: 10637504
-
The lymphocytic choriomeningitis virus RING protein Z associates with eukaryotic initiation factor 4E and selectively represses translation in a RING-dependent manner.
J Virol. 2000 Apr;74(7):3293-300
PMID: 10708446
-
Interactions between viruses and lymphocytes. I. In vivo replication of lymphocytic choriomeningitis virus in mononuclear cells during both chronic and acute viral infections.
J Immunol. 1978 Oct;121(4):1262-9
PMID: 308960
-
Antiviral actions of interferon. Interferon-regulated cellular proteins and their surprisingly selective antiviral activities.
Virology. 1991 Jul;183(1):1-11
PMID: 1711253