Abstract
We have previously shown that avian leukosis virus (ALV) induces erythroblastosis by insertional activation of the c-erbB gene. In 25% of the ALV-induced leukemic samples we have analyzed, acute retroviruses that have captured the activated erbB oncogene were released. The unusually high frequency at which erbB transduction occurs makes this an ideal system for studying the mechanism of oncogene transduction. In addition, these leukemic samples provide a rich source for the isolation of novel erbB-transducing viruses. We report here our characterization of several new erbB-transducing proviruses. The 5' recombination points of all these viruses mapped to the same intron in which proviral insertions cluster, supporting the hypothesis that transduction begins with proviral insertion near the oncogene. The 3' recombination points usually occurred within the 3' untranslated region downstream from the termination codon of the c-erbB gene. Three of the erbB-containing proviruses were molecularly cloned and analyzed in detail. Two of them were capable of releasing acute viruses, and interestingly, both retained poly(A) tracts of erbB messages in their genomes. A stretch of six adenosine residues in the ALV env gene appeared to mediate the 3' recombination events required for the generation of these viruses. These data provide further insight into the mechanism by which oncogenes are transduced into retroviral genomes.
MeSH Terms
Animals
Avian Leukosis Virus/genetics,physiology
Base Sequence
Chickens
Genes, Viral
Introns
Leukemia, Erythroblastic, Acute/etiology,genetics
Leukemia, Experimental/etiology,genetics
Models, Genetic
Molecular Sequence Data
Oncogenes
Poly A/genetics
Proto-Oncogene Proteins/genetics
Proviruses/genetics
RNA, Messenger/genetics
RNA, Viral/genetics
Transduction, Genetic
Chemicals
Proto-Oncogene Proteins
RNA, Messenger
RNA, Viral
Poly A
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Raines M A
Department of Molecular Biology and Microbiology, School of Medicine, Case Western Reserve University, Cleveland, Ohio 44106.
Maihle N J
Moscovici C
Crittenden L
Kung H J
References (32)
32 references, click to expand
-
Purification of biologically active globin messenger RNA by chromatography on oligothymidylic acid-cellulose.
Proc Natl Acad Sci U S A. 1972 Jun;69(6):1408-12
PMID: 4504350
-
Efficient packaging of readthrough RNA in ALV: implications for oncogene transduction.
Science. 1987 May 15;236(4803):845-8
PMID: 3033828
-
DNA sequencing with chain-terminating inhibitors.
Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463-7
PMID: 271968
-
Avian oncovirus mutant (SE21Q1b) deficient in genomic RNA: characterization of a deletion in the provirus.
J Virol. 1980 Nov;36(2):450-6
PMID: 6253670
-
Generation of novel, biologically active Harvey sarcoma viruses via apparent illegitimate recombination.
J Virol. 1981 Apr;38(1):136-50
PMID: 7241647
-
Formation of infectious progeny virus after insertion of herpes simplex thymidine kinase gene into DNA of an avian retrovirus.
Cell. 1981 Oct;26(1 Pt 1):67-77
PMID: 6276009
-
Transduction of a cellular oncogene: the genesis of Rous sarcoma virus.
Proc Natl Acad Sci U S A. 1983 May;80(9):2519-23
PMID: 6302692
-
Activation of the cellular oncogene c-erbB by LTR insertion: molecular basis for induction of erythroblastosis by avian leukosis virus.
Cell. 1983 Jun;33(2):357-68
PMID: 6305505
-
Identification of a sequence likely to be required for avian retroviral packaging.
Virology. 1983 Jul 30;128(2):505-11
PMID: 6310871
-
The erbB gene of avian erythroblastosis virus is a member of the src gene family.
Cell. 1983 Nov;35(1):71-8
PMID: 6313229
-
Site-specific mutagenesis of avian erythroblastosis virus: erb-B is required for oncogenicity.
Virology. 1983 Oct 15;130(1):155-78
PMID: 6195816
-
Lambda replacement vectors carrying polylinker sequences.
J Mol Biol. 1983 Nov 15;170(4):827-42
PMID: 6315951
-
Retrovirus transduction: generation of infectious retroviruses expressing dominant and selectable genes is associated with in vivo recombination and deletion events.
Mol Cell Biol. 1983 Dec;3(12):2180-90
PMID: 6318087
-
Expression of complete chicken thymidine kinase gene inserted in a retrovirus vector.
Mol Cell Biol. 1984 Apr;4(4):749-54
PMID: 6325895
-
Autophosphorylation sites on the epidermal growth factor receptor.
Nature. 1984 Oct 4-10;311(5985):483-5
PMID: 6090945
-
The four C-terminal amino acids of the v-erbA polypeptide are encoded by an intronic sequence of the v-erbB oncogene.
Virology. 1985 Jan 15;140(1):179-82
PMID: 2981452
-
The molecular genetics of cellular oncogenes.
Annu Rev Genet. 1984;18:553-612
PMID: 6397126
-
High-frequency transduction of c-erbB in avian leukosis virus-induced erythroblastosis.
J Virol. 1985 May;54(2):295-303
PMID: 2985798
-
c-erbB activation in avian leukosis virus-induced erythroblastosis: clustered integration sites and the arrangement of provirus in the c-erbB alleles.
Proc Natl Acad Sci U S A. 1985 Apr;82(8):2287-91
PMID: 2986110
-
c-erbB activation in ALV-induced erythroblastosis: novel RNA processing and promoter insertion result in expression of an amino-truncated EGF receptor.
Cell. 1985 Jul;41(3):719-26
PMID: 2988784
-
Rous-associated virus 1-induced erythroleukemic cells exhibit a weakly transformed phenotype in vitro and release c-erbB-containing retroviruses unable to transform fibroblasts.
J Virol. 1986 Mar;57(3):1127-38
PMID: 3005614
-
Characterization of a myc-containing retrovirus generated by propagation of an MH2 viral subgenomic RNA.
J Virol. 1986 Mar;57(3):1191-4
PMID: 3951018
-
The role of RNA molecules in transduction of the proto-oncogene c-fps.
Cell. 1986 Mar 28;44(6):935-40
PMID: 2420470
-
A new acute transforming feline retrovirus and relationship of its oncogene v-kit with the protein kinase gene family.
Nature. 1986 Apr 3-9;320(6061):415-21
PMID: 3007997
-
A conserved cis-acting sequence in the 5' leader of avian sarcoma virus RNA is required for packaging.
J Virol. 1986 Jul;59(1):163-7
PMID: 3012114
-
Differential transcription from the long terminal repeats of integrated avian leukosis virus DNA.
J Virol. 1986 Nov;60(2):497-505
PMID: 3021984
-
A single amino acid substitution in v-erbB confers a thermolabile phenotype to ts167 avian erythroblastosis virus-transformed erythroid cells.
Mol Cell Biol. 1986 May;6(5):1751-9
PMID: 2878364
-
Activation of the cellular src gene by transducing retrovirus.
Mol Cell Biol. 1986 Jul;6(7):2420-8
PMID: 3097513
-
c-erbB activation in avian leukosis virus-induced erythroblastosis: multiple epidermal growth factor receptor mRNAs are generated by alternative RNA processing.
Mol Cell Biol. 1986 Sep;6(9):3128-33
PMID: 3023963
-
Activation of oncogenicity of the c-rel proto-oncogene.
Mol Cell Biol. 1986 Dec;6(12):4709-16
PMID: 3025667
-
Structure of the feline c-fes/fps proto-oncogene: genesis of a retroviral oncogene.
J Virol. 1987 Jun;61(6):2009-16
PMID: 3553615
-
Detection of specific sequences among DNA fragments separated by gel electrophoresis.
J Mol Biol. 1975 Nov 5;98(3):503-17
PMID: 1195397