Abstract
The bovine papillomavirus E5 transforming protein appears to activate both the epidermal growth factor receptor (EGF-R) and the platelet-derived growth factor receptor (PDGF-R) by a ligand-independent mechanism. To further investigate the ability of E5 to activate receptors of different classes and to determine whether this stimulation occurs through the extracellular domain required for ligand activation, we constructed chimeric genes encoding PDGF-R and EGF-R by interchanging the extracellular, membrane, and cytoplasmic coding domains. Chimeras were transfected into NIH 3T3 and CHO(LR73) cells. All chimeras expressed stable protein which, upon addition of the appropriate ligand, could be activated as assayed by tyrosine autophosphorylation and biological transformation. Cotransfection of E5 with the wild-type and chimeric receptors resulted in the ligand-independent activation of receptors, provided that a receptor contained either the transmembrane domain of the PDGF-R or the cytoplasmic domain of the EGF-R. Chimeric receptors that contained both of these domains exhibited the highest level of E5-induced biochemical and biological stimulation. These results imply that E5 activates the PDGF-R and EGR-R by two distinct mechanisms, neither of which specifically involves the extracellular domain of the receptor. Consistent with the biochemical and biological activation data, coimmunoprecipitation studies demonstrated that E5 formed a complex with any chimera that contained a PDGF-R transmembrane domain or an EGF-R cytoplasmic domain, with those chimeras containing both domains demonstrating the greatest efficiency of complex formation. These results suggest that although different domains of the PDGF-R and EGF-R are required for E5 activation, both receptors are activated directly by formation of an E5-containing complex.
MeSH Terms
3T3 Cells
Animals
Bovine papillomavirus 1/genetics,metabolism
CHO Cells
Cell Division/drug effects
Cell Line
Cell Transformation, Neoplastic
Cholera Toxin/pharmacology
Cloning, Molecular
Cricetinae
ErbB Receptors/genetics,isolation & purification,metabolism
Humans
Macromolecular Substances
Mice
Models, Structural
Oncogene Proteins, Viral/isolation & purification,metabolism
Protein Binding
Receptors, Platelet-Derived Growth Factor/genetics,isolation & purification,metabolism
Recombinant Fusion Proteins/isolation & purification,metabolism
Transfection
Chemicals
Macromolecular Substances
Oncogene Proteins, Viral
Recombinant Fusion Proteins
oncogene protein E5, Bovine papillomavirus type 1
Cholera Toxin
ErbB Receptors
Receptors, Platelet-Derived Growth Factor
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Cohen B D
Laboratory of Cellular Oncology, National Cancer Institute, Bethesda, Maryland 20892.
Goldstein D J
Rutledge L
Vass W C
Lowy D R
Schlegel R
Schiller J T
References (30)
30 references, click to expand
-
The normal erbB-2 product is an atypical receptor-like tyrosine kinase with constitutive activity in the absence of ligand.
New Biol. 1990 Nov;2(11):992-1003
PMID: 1983208
-
Bovine papillomavirus E5 oncoprotein binds to the 16K component of vacuolar H(+)-ATPases.
Nature. 1991 Jul 25;352(6333):347-9
PMID: 1649407
-
A glutamine residue in the membrane-associating domain of the bovine papillomavirus type 1 E5 oncoprotein mediates its binding to a transmembrane component of the vacuolar H(+)-ATPase.
J Virol. 1992 Jan;66(1):405-13
PMID: 1370089
-
Human papillomavirus type 16 E5 gene stimulates the transforming activity of the epidermal growth factor receptor.
Oncogene. 1992 Jan;7(1):27-32
PMID: 1311063
-
The erythropoietin receptor transmembrane region is necessary for activation by the Friend spleen focus-forming virus gp55 glycoprotein.
Mol Cell Biol. 1992 Jul;12(7):2949-57
PMID: 1320192
-
Analysis of the influences of the E5 transforming protein on kinetic parameters of epidermal growth factor binding and metabolism.
J Cell Physiol. 1992 Aug;152(2):253-63
PMID: 1639860
-
Stable association between the bovine papillomavirus E5 transforming protein and activated platelet-derived growth factor receptor in transformed mouse cells.
Proc Natl Acad Sci U S A. 1992 Aug 1;89(15):6736-40
PMID: 1323117
-
The BPV-1 E5 protein, the 16 kDa membrane pore-forming protein and the PDGF receptor exist in a complex that is dependent on hydrophobic transmembrane interactions.
EMBO J. 1992 Dec;11(13):4851-9
PMID: 1334459
-
A quantitative in vitro focus assay for bovine papilloma virus.
Virology. 1980 Jun;103(2):369-75
PMID: 6247821
-
Rous sarcoma virus transformed cells are resistant to cyclic AMP.
J Cell Physiol. 1982 Apr;111(1):42-8
PMID: 6282904
-
Animal papillomaviruses.
Microbiol Rev. 1982 Jun;46(2):191-207
PMID: 6289064
-
Simian sarcoma virus onc gene, v-sis, is derived from the gene (or genes) encoding a platelet-derived growth factor.
Science. 1983 Jul 15;221(4607):275-7
PMID: 6304883
-
Platelet-derived growth factor is structurally related to the putative transforming protein p28sis of simian sarcoma virus.
Nature. 1983 Jul 7-13;304(5921):35-9
PMID: 6306471
-
Human epidermal growth factor receptor cDNA sequence and aberrant expression of the amplified gene in A431 epidermoid carcinoma cells.
Nature. 1984 May 31-Jun 6;309(5967):418-25
PMID: 6328312
-
Characterization of the polypeptide composition of human factor VIII:C and the nucleotide sequence and expression of the human kidney cDNA.
DNA. 1985 Oct;4(5):333-49
PMID: 3935400
-
E5 open reading frame of bovine papillomavirus type 1 encodes a transforming gene.
J Virol. 1986 Jan;57(1):1-6
PMID: 3001335
-
The E5 transforming gene of bovine papillomavirus encodes a small, hydrophobic polypeptide.
Science. 1986 Jul 25;233(4762):464-7
PMID: 3014660
-
Genetic and biochemical definition of the bovine papillomavirus E5 transforming protein.
EMBO J. 1987 Aug;6(8):2381-5
PMID: 2822390
-
Cell proliferative response to vaccinia virus is mediated by VGF.
Virology. 1988 May;164(1):182-92
PMID: 3363864
-
Increased tyrosine kinase activity associated with the protein encoded by the activated neu oncogene.
Proc Natl Acad Sci U S A. 1988 Aug;85(15):5394-8
PMID: 2899890
-
44-amino-acid E5 transforming protein of bovine papillomavirus requires a hydrophobic core and specific carboxyl-terminal amino acids.
Mol Cell Biol. 1988 Oct;8(10):4071-8
PMID: 2847028
-
Retroviruses expressing different levels of the normal epidermal growth factor receptor: biological properties and new bioassay.
J Cell Biochem. 1989 Feb;39(2):153-66
PMID: 2565908
-
The E5 oncoprotein of bovine papillomavirus is oriented asymmetrically in Golgi and plasma membranes.
Virology. 1989 May;170(1):334-9
PMID: 2541554
-
Neu receptor dimerization.
Nature. 1989 Jun 22;339(6226):587
PMID: 2567498
-
The bovine papillomavirus E5 transforming protein can stimulate the transforming activity of EGF and CSF-1 receptors.
Cell. 1989 Oct 6;59(1):21-32
PMID: 2551505
-
Transforming activity of a 16-amino-acid segment of the bovine papillomavirus E5 protein linked to random sequences of hydrophobic amino acids.
J Virol. 1989 Nov;63(11):4515-9
PMID: 2552136
-
The E5 oncoprotein of bovine papillomavirus binds to a 16 kd cellular protein.
EMBO J. 1990 Jan;9(1):137-45
PMID: 1688529
-
Distribution and specific identification of papillomavirus major capsid protein epitopes by immunocytochemistry and epitope scanning of synthetic peptides.
J Infect Dis. 1990 Dec;162(6):1263-9
PMID: 1700026
-
Activation of the platelet-derived growth factor receptor by the bovine papillomavirus E5 transforming protein.
EMBO J. 1991 Apr;10(4):845-55
PMID: 1849073
-
Tumorigenic transformation of murine keratinocytes by the E5 genes of bovine papillomavirus type 1 and human papillomavirus type 16.
J Virol. 1991 Dec;65(12):7078-83
PMID: 1658398