Abstract
LMP-1, the Epstein-Barr virus latent membrane protein 1, is the only protein encoded by the virus that has been shown to have the properties of a transforming oncogene in rodent fibroblasts such as Rat-1 cells. LMP-1 is phosphorylated and proteolytically cleaved in Rat-1 cells in a manner similar to that seen in human lymphocytes. In this study, we demonstrate that all three major domains of LMP-1 (N-terminal, transmembrane, and C-terminal domains) are required for the ability to transform Rat-1 cells in culture, as assayed by loss of contact inhibition. This study is the first demonstration of a functional role for the C-terminal domain of LMP-1. Our analysis suggests that there are at least three distinct regions of the C terminus involved in signalling. Amino acids 306 to 334, which generate a toxic signal in the absence of amino acids 334 to 364, and the last 23 amino acids, 364 to 386, are essential for transformation. Biochemical analysis of the LMP-1 mutants with the three domains deleted indicate that the mutant N-terminal with the domain deleted is phosphorylated normally but is inefficiently cleaved compared with the wild-type LMP-1. The mutant with the transmembrane domain deleted is also phosphorylated but is not cleaved, showing that phosphorylation of LMP-1 does not require membrane association. The nontransforming mutant with the C-terminal domain deleted that lacks the last 23 amino acids is phosphorylated and cleaved. Therefore, these processing events alone are insufficient to generate a transforming signal.
MeSH Terms
Amino Acid Sequence
Animals
Cell Line
DNA Mutational Analysis
Herpesvirus 4, Human/genetics,metabolism
Molecular Sequence Data
Oncogene Proteins, Viral/genetics,metabolism
Phenotype
Plasmids/genetics
Protein Precursors/genetics,metabolism
Protein Processing, Post-Translational
Protein Sorting Signals/genetics,metabolism
Rats
Transfection
Transformation, Genetic
Viral Matrix Proteins/genetics,metabolism
Chemicals
EBV-associated membrane antigen, Epstein-Barr virus
Oncogene Proteins, Viral
Protein Precursors
Protein Sorting Signals
Viral Matrix Proteins
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Moorthy R K
Department of Pathology, Tufts University School of Medicine, Boston, Massachusetts 02111.
Thorley-Lawson D A
References (19)
19 references, click to expand
-
An Epstein-Barr virus transforming protein associates with vimentin in lymphocytes.
Mol Cell Biol. 1987 Jul;7(7):2299-308
PMID: 3039344
-
Phenotypes of Epstein-Barr virus LMP1 deletion mutants indicate transmembrane and amino-terminal cytoplasmic domains necessary for effects in B-lymphoma cells.
J Virol. 1992 Jul;66(7):4612-6
PMID: 1318423
-
Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications.
Proc Natl Acad Sci U S A. 1979 Sep;76(9):4350-4
PMID: 388439
-
Nucleotide sequence of an mRNA transcribed in latent growth-transforming virus infection indicates that it may encode a membrane protein.
J Virol. 1984 Aug;51(2):411-9
PMID: 6086953
-
A membrane protein encoded by Epstein-Barr virus in latent growth-transforming infection.
Proc Natl Acad Sci U S A. 1984 Nov;81(22):7207-11
PMID: 6095274
-
Epstein-Barr virus-encoded protein found in plasma membranes of transformed cells.
J Virol. 1985 Sep;55(3):710-20
PMID: 2991591
-
An EBV membrane protein expressed in immortalized lymphocytes transforms established rodent cells.
Cell. 1985 Dec;43(3 Pt 2):831-40
PMID: 3000618
-
Orientation and patching of the latent infection membrane protein encoded by Epstein-Barr virus.
J Virol. 1986 Apr;58(1):233-7
PMID: 3005654
-
Posttranslational processing of an Epstein-Barr virus-encoded membrane protein expressed in cells transformed by Epstein-Barr virus.
J Virol. 1987 Mar;61(3):866-75
PMID: 3027413
-
Posttranslational processing of the Epstein-Barr virus-encoded p63/LMP protein.
J Virol. 1987 Jul;61(7):2100-8
PMID: 3035211
-
The truncated form of the Epstein-Barr virus latent-infection membrane protein expressed in virus replication does not transform rodent fibroblasts.
J Virol. 1988 Jul;62(7):2337-46
PMID: 2836616
-
Transformation of Balb 3T3 cells by the BNLF-1 gene of Epstein-Barr virus.
Oncogene. 1988 May;2(5):461-7
PMID: 2836780
-
Adrenergic receptors.
Adv Second Messenger Phosphoprotein Res. 1988;21:1-10
PMID: 2843210
-
The multiple membrane-spanning segments of the BNLF-1 oncogene from Epstein-Barr virus are required for transformation.
Oncogene. 1989 Jan;4(1):67-74
PMID: 2536919
-
The transforming domain alone of the latent membrane protein of Epstein-Barr virus is toxic to cells when expressed at high levels.
J Virol. 1989 Jun;63(6):2469-75
PMID: 2542565
-
Processing of the Epstein-Barr virus-encoded latent membrane protein p63/LMP.
J Virol. 1990 Feb;64(2):829-37
PMID: 2153246
-
Transformation by the oncogenic latent membrane protein correlates with its rapid turnover, membrane localization, and cytoskeletal association.
J Virol. 1991 Jun;65(6):3246-58
PMID: 1827846
-
Epstein-Barr virus latent membrane protein expression in Hodgkin and Reed-Sternberg cells.
Proc Natl Acad Sci U S A. 1991 Jun 1;88(11):4766-70
PMID: 1647016
-
A new technique for the assay of infectivity of human adenovirus 5 DNA.
Virology. 1973 Apr;52(2):456-67
PMID: 4705382