Home LiteratureArticle Details
PMID: 3023843 Published · ppublish English Journal Article

Two modes of c-myb activation in virus-induced mouse myeloid tumors.

Molecular and cellular biology ·Vol. 6 ·No. 2 ·1986-02-00 ·Pages 380-92

Shen-Ong GL, Morse HC, Potter M, Mushinski JF

Abstract

Two modes of disruption of the protooncogene c-myb by viral insertional mutagenesis in mouse myeloid tumor cells are described. The first mode was found in six tumors in which a Moloney murine leukemia virus component had inserted in the same transcriptional orientation upstream of the 5'-most exon with v-myb homology (vE1). cDNA sequence data indicate the presence of a truncated c-myb mRNA that is initiated in the upstream 5' long terminal repeat of the integrated provirus and processed via a cryptic splice donor sequence in the gag region to the splice acceptor site in vE1 of the c-myb gene, thus removing the remaining downstream viral and myb intronic sequences. Unlike most gag-onc transcripts, the gag and myb sequences in the hybrid transcript were not in the same reading frame. It is presumed that the gag sequence provides a cryptic translation initiation site for the novel amino-truncated c-myb protein. The second mode of disruption was by downstream virus insertion at the 3' side of the c-myb, which results in the synthesis of a small (approximately 2 kilobase) myb transcript. The 5' long terminal repeat of the inserted provirus provides a TGA termination codon that results in the elimination of 240 normal c-myb amino acid residues from the carboxyl terminus of the tumor-specific myb protein. These results suggest that truncated myb proteins play a role in neoplastic transformation of myeloid cells.

MeSH Terms
Amino Acid Sequence Animals Base Sequence Cell Line Cell Transformation, Neoplastic Cloning, Molecular DNA Transposable Elements Genes, Viral Mice Mice, Inbred BALB C Moloney murine leukemia virus/genetics Mutation Neoplasms, Experimental/microbiology Nucleic Acid Hybridization Proto-Oncogene Proteins/genetics Proto-Oncogene Proteins c-myb Proto-Oncogenes Transcription, Genetic
Chemicals
DNA Transposable Elements Proto-Oncogene Proteins Proto-Oncogene Proteins c-myb
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Shen-Ong G L
Morse H C
Potter M
Mushinski J F
References (64)
64 references, click to expand
  1. Activation of the c-myb locus by viral insertional mutagenesis in plasmacytoid lymphosarcomas.
    Science. 1984 Nov 30;226(4678):1077-80 PMID: 6093260
  2. Leukemic transformation with avian myeloblastosis virus: present status.
    Curr Top Microbiol Immunol. 1975;71:79-101 PMID: 172289
  3. A novel method to map transcripts: evidence for homology between an adenovirus mRNA and discrete multiple regions of the viral genome.
    Cell. 1977 Sep;12(1):23-36 PMID: 198139
  4. Sizing and mapping of early adenovirus mRNAs by gel electrophoresis of S1 endonuclease-digested hybrids.
    Cell. 1977 Nov;12(3):721-32 PMID: 922889
  5. DNA sequencing with chain-terminating inhibitors.
    Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463-7 PMID: 271968
  6. Three new types of viral oncogene of cellular origin specific for haematopoietic cell transformation.
    Nature. 1979 Oct 11;281(5731):452-5 PMID: 226888
  7. A versatile primer for DNA sequencing in the M13mp2 cloning system.
    Gene. 1980 Jun;10(1):69-73 PMID: 6250947
  8. Three new types of viral oncogenes in defective avian leukemia viruses. I. Specific nucleotide sequences of cellular origin correlate with specific transformation.
    Cold Spring Harb Symp Quant Biol. 1980;44 Pt 2,:1215-23 PMID: 6253195
  9. Genetic structure of avian myeloblastosis virus, released from transformed myeloblasts as a defective virus particle.
    Proc Natl Acad Sci U S A. 1980 Sep;77(9):5120-4 PMID: 6159639
  10. Cellular sequences are present in the presumptive avian myeloblastosis virus genome.
    Proc Natl Acad Sci U S A. 1980 Sep;77(9):5177-81 PMID: 6254063
  11. Analysis of avian leukosis virus DNA and RNA in bursal tumours: viral gene expression is not required for maintenance of the tumor state.
    Cell. 1981 Feb;23(2):311-22 PMID: 6258797
  12. Avian leukosis virus-induced tumors have common proviral integration sites and synthesize discrete new RNAs: oncogenesis by promoter insertion.
    Cell. 1981 Feb;23(2):323-34 PMID: 6258798
  13. The genome and the intracellular RNAs of avian myeloblastosis virus.
    Cell. 1981 Jan;23(1):279-90 PMID: 6260378
  14. Activation of a cellular onc gene by promoter insertion in ALV-induced lymphoid leukosis.
    Nature. 1981 Apr 9;290(5806):475-80 PMID: 6261142
  15. On the mechanism of retrovirus-induced avian lymphoid leukosis: deletion and integration of the proviruses.
    Proc Natl Acad Sci U S A. 1981 Jun;78(6):3418-22 PMID: 6267589
  16. Myeloid and erythroid neoplastic responses to avian defective leukemia viruses in chickens and in quail.
    Virology. 1981 Sep;113(2):765-8 PMID: 6267807
  17. Oligonucleotide directed mutagenesis of the human beta-globin gene: a general method for producing specific point mutations in cloned DNA.
    Nucleic Acids Res. 1981 Aug 11;9(15):3647-56 PMID: 7279669
  18. Genomes of murine leukemia viruses isolated from wild mice.
    J Virol. 1981 Sep;39(3):777-91 PMID: 6270351
  19. Possible role of flanking nucleotides in recognition of the AUG initiator codon by eukaryotic ribosomes.
    Nucleic Acids Res. 1981 Oct 24;9(20):5233-52 PMID: 7301588
  20. Vertebrate DNAs contain nucleotide sequences related to the transforming gene of avian myeloblastosis virus.
    J Virol. 1981 Nov;40(2):450-5 PMID: 6275098
  21. Multiple arrangements of viral DNA and an activated host oncogene in bursal lymphomas.
    Nature. 1982 Jan 21;295(5846):209-14 PMID: 6276760
  22. Nuclear localization and DNA binding of the transforming gene product of avian myelocytomatosis virus.
    Nature. 1982 Mar 18;296(5854):262-9 PMID: 6278322
  23. Form and function of retroviral proviruses.
    Science. 1982 May 21;216(4548):812-20 PMID: 6177038
  24. The molecular genetics of cellular oncogenes.
    Annu Rev Genet. 1984;18:553-612 PMID: 6397126
  25. DNA-binding activity is associated with purified myb proteins from AMV and E26 viruses and is temperature-sensitive for E26 ts mutants.
    Cell. 1985 Apr;40(4):983-90 PMID: 2985272
  26. Isolation of the proto-oncogene c-myb from D. melanogaster.
    Cell. 1985 Jun;41(2):449-56 PMID: 3921261
  27. Friend murine leukemia virus-immortalized myeloid cells are converted into tumorigenic cell lines by Abelson leukemia virus.
    Proc Natl Acad Sci U S A. 1985 May;82(10):3306-10 PMID: 2987918
  28. Malignant transformation of a growth factor-dependent myeloid cell line by Abelson virus without evidence of an autocrine mechanism.
    Cell. 1985 Jul;41(3):677-83 PMID: 2988782
  29. Neoplastic transformation of mast cells by Abelson-MuLV: abrogation of IL-3 dependence by a nonautocrine mechanism.
    Cell. 1985 Jul;41(3):685-93 PMID: 2988783
  30. 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
  31. Removal of a 67-base-pair sequence in the noncoding region of protooncogene fos converts it to a transforming gene.
    Proc Natl Acad Sci U S A. 1985 Aug;82(15):4987-91 PMID: 2991903
  32. Correlation of cell-surface phenotype with the establishment of interleukin 3-dependent cell lines from wild-mouse murine leukemia virus-induced neoplasms.
    Proc Natl Acad Sci U S A. 1985 Oct;82(19):6687-91 PMID: 2995979
  33. Expression of the Rous sarcoma virus pol gene by ribosomal frameshifting.
    Science. 1985 Dec 13;230(4731):1237-42 PMID: 2416054
  34. A set of synthetic oligodeoxyribonucleotide primers for DNA sequencing in the plasmid vector pBR322.
    Gene. 1981 Dec;16(1-3):21-6 PMID: 6282692
  35. Nucleotide sequence of the transforming gene of avian myeloblastosis virus.
    Science. 1982 Jun 25;216(4553):1421-3 PMID: 6283631
  36. Eukaryotic ribosomes can recognize preproinsulin initiation codons irrespective of their position relative to the 5' end of mRNA.
    Nature. 1982 Sep 16;299(5880):221-6 PMID: 6955600
  37. A new pair of M13 vectors for selecting either DNA strand of double-digest restriction fragments.
    Gene. 1982 Oct;19(3):269-76 PMID: 6295880
  38. Many tumors induced by the mouse mammary tumor virus contain a provirus integrated in the same region of the host genome.
    Cell. 1982 Nov;31(1):99-109 PMID: 6297757
  39. Novel myc oncogene RNA from abortive immunoglobulin-gene recombination in mouse plasmacytomas.
    Cell. 1982 Dec;31(2 Pt 1):443-52 PMID: 6819085
  40. Nucleotide sequence of the retroviral leukemia gene v-myb and its cellular progenitor c-myb: the architecture of a transduced oncogene.
    Cell. 1982 Dec;31(2 Pt 1):453-63 PMID: 6297766
  41. Transformation of both erythroid and myeloid cells by E26, an avian leukemia virus that contains the myb gene.
    Cell. 1982 Dec;31(3 Pt 2):643-53 PMID: 6297778
  42. Structure and transcription of the cellular homolog (c-myb) of the avian myeloblastosis virus transforming gene (v-myb).
    J Virol. 1983 Apr;46(1):212-20 PMID: 6298458
  43. Analysis of FBJ-MuSV provirus and c-fos (mouse) gene reveals that viral and cellular fos gene products have different carboxy termini.
    Cell. 1983 Apr;32(4):1241-55 PMID: 6301687
  44. DNA rearrangement and altered RNA expression of the c-myb oncogene in mouse plasmacytoid lymphosarcomas.
    Science. 1983 May 20;220(4599):795-8 PMID: 6687762
  45. Comparison of initiation of protein synthesis in procaryotes, eucaryotes, and organelles.
    Microbiol Rev. 1983 Mar;47(1):1-45 PMID: 6343825
  46. Complete nucleotide sequence of a human c-onc gene: deduced amino acid sequence of the human c-fos protein.
    Proc Natl Acad Sci U S A. 1983 Jun;80(11):3183-7 PMID: 6574479
  47. Expression of c-myc RNA in bursal lymphoma cell lines: identification of c-myc-encoded proteins by hybrid-selected translation.
    Cell. 1983 Jun;33(2):335-44 PMID: 6190569
  48. The product of the retroviral transforming gene v-myb is a truncated version of the protein encoded by the cellular oncogene c-myb.
    Cell. 1983 Jun;33(2):345-55 PMID: 6305504
  49. Tumorigenesis by mouse mammary tumor virus: evidence for a common region for provirus integration in mammary tumors.
    Cell. 1983 Jun;33(2):369-77 PMID: 6305506
  50. Characterization of the hemopoietic target cells for the avian leukemia virus E26.
    Virology. 1983 Aug;129(1):65-78 PMID: 6310886
  51. RNA splicing: three themes with variations.
    Cell. 1983 Oct;34(3):713-6 PMID: 6354470
  52. The erbB gene of avian erythroblastosis virus is a member of the src gene family.
    Cell. 1983 Nov;35(1):71-8 PMID: 6313229
  53. Transduction of c-myb into avian myeloblastosis virus: locating points of recombination within the cellular gene.
    J Virol. 1983 Dec;48(3):565-72 PMID: 6195355
  54. Tripartite structure of the avian erythroblastosis virus E26 transforming gene.
    Nature. 1983 Nov 24-30;306(5941):391-5 PMID: 6316155
  55. A putative second cell-derived oncogene of the avian leukaemia retrovirus E26.
    Nature. 1983 Nov 24-30;306(5941):395-7 PMID: 6316156
  56. The protein products of the myc and myb oncogenes and adenovirus E1a are structurally related.
    Nature. 1983 Dec 22-1984 Jan 4;306(5945):803-6 PMID: 6656884
  57. Mode of proviral activation of a putative mammary oncogene (int-1) on mouse chromosome 15.
    Nature. 1984 Jan 12-18;307(5947):131-6 PMID: 6318122
  58. c-fos protein can induce cellular transformation: a novel mechanism of activation of a cellular oncogene.
    Cell. 1984 Jan;36(1):51-60 PMID: 6607118
  59. Transcriptional interference in avian retroviruses--implications for the promoter insertion model of leukaemogenesis.
    Nature. 1984 Jan 19-25;307(5948):241-5 PMID: 6363938
  60. Close similarity of epidermal growth factor receptor and v-erb-B oncogene protein sequences.
    Nature. 1984 Feb 9-15;307(5951):521-7 PMID: 6320011
  61. Structural organization and expression of human DNA sequences related to the transforming gene of avian myeloblastosis virus.
    Proc Natl Acad Sci U S A. 1983 Dec;80(24):7385-9 PMID: 6324165
  62. Initiation of translation at internal AUG codons in mammalian cells.
    Nature. 1984 May 3-9;309(5963):82-5 PMID: 6717585
  63. Subcellular localization of proteins encoded by oncogenes of avian myeloblastosis virus and avian leukemia virus E26 and by chicken c-myb gene.
    Cell. 1984 Jun;37(2):537-47 PMID: 6327074
  64. Avian myeloblastosis virus and E26 virus oncogene products are nuclear proteins.
    Proc Natl Acad Sci U S A. 1984 Jul;81(14):4265-9 PMID: 6087315
Article Info
Journal
Molecular and cellular biology
Abbr.
Mol Cell Biol
ISSN
0270-7306
Published
1986-02-00
Pages
380-92
Language
English
Region
United States
NLM ID
8109087
PMCID
PMC367527
Subset
IM
Databases
GENBANK
M13138
Corrections
ErratumIn
-
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com