Skip to main content
Nucleic Acids Research logoLink to Nucleic Acids Research
. 1989 Jul 25;17(14):5651–5664. doi: 10.1093/nar/17.14.5651

Transcription of the chicken myb proto-oncogene starts within a CpG island.

M Dvorák 1, P Urbánek 1, P Bartůnĕk 1, V Paces 1, J Vlach 1, V Pecenka 1, L Arnold 1, M Trávnicek 1, J Ríman 1
PMCID: PMC318186  PMID: 2548166

Abstract

The nucleotide sequence of an 8.2-kb DNA fragment from the 5' proximal part of the chicken myb proto-oncogene spanning 1761 nucleotides upstream and 6436 nucleotides downstream from a presumed c-myb initiation codon was determined. A 3.3-kb G + C-rich region found in this sequence had also other features characterizing CpG islands, i.e. no CpG underrepresentation and lack of CpG methylation. In haematopoietic tissues c-myb mRNA synthesis starts in two major regions of the CpG island, namely 98 to 108 and 143 to 145 nucleotides upstream from the c-myb initiation codon. These two regions are in or close to the 124-bp evolutionarily conserved element located in the middle part of the CpG island. No alternative splicing of the 5' end of c-myb mRNA suggested earlier (1,2) was observed. The c-myb promoter contains neither TATA nor CAAT box-like structures at the usual positions. Instead, numerous potential Sp1 factor binding sites were found both upstream and downstream from the transcription initiation sites. Moreover, consensus v-myb protein DNA-binding sites were revealed in the promoter region and in sequences downstream from it.

Full text

PDF
5651

Images in this article

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Akiyama Y., Kato S. Two cell lines from lymphomas of Marek's disease. Biken J. 1974 Sep;17(3):105–116. [PubMed] [Google Scholar]
  2. Anderson S. Shotgun DNA sequencing using cloned DNase I-generated fragments. Nucleic Acids Res. 1981 Jul 10;9(13):3015–3027. doi: 10.1093/nar/9.13.3015. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Aviv H., Leder P. Purification of biologically active globin messenger RNA by chromatography on oligothymidylic acid-cellulose. Proc Natl Acad Sci U S A. 1972 Jun;69(6):1408–1412. doi: 10.1073/pnas.69.6.1408. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bading H., Hansen J., Moelling K. Selective DNA binding of the human cellular myb protein isolated by immunoaffinity chromatography using a monoclonal antibody. Oncogene. 1987;1(4):395–401. [PubMed] [Google Scholar]
  5. Bender T. P., Kuehl W. M. Murine myb protooncogene mRNA: cDNA sequence and evidence for 5' heterogeneity. Proc Natl Acad Sci U S A. 1986 May;83(10):3204–3208. doi: 10.1073/pnas.83.10.3204. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bender T. P., Thompson C. B., Kuehl W. M. Differential expression of c-myb mRNA in murine B lymphomas by a block to transcription elongation. Science. 1987 Sep 18;237(4821):1473–1476. doi: 10.1126/science.3498214. [DOI] [PubMed] [Google Scholar]
  7. Bergmann D. G., Souza L. M., Baluda M. A. Vertebrate DNAs contain nucleotide sequences related to the transforming gene of avian myeloblastosis virus. J Virol. 1981 Nov;40(2):450–455. doi: 10.1128/jvi.40.2.450-455.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Biedenkapp H., Borgmeyer U., Sippel A. E., Klempnauer K. H. Viral myb oncogene encodes a sequence-specific DNA-binding activity. Nature. 1988 Oct 27;335(6193):835–837. doi: 10.1038/335835a0. [DOI] [PubMed] [Google Scholar]
  9. Bird A. P. CpG-rich islands and the function of DNA methylation. Nature. 1986 May 15;321(6067):209–213. doi: 10.1038/321209a0. [DOI] [PubMed] [Google Scholar]
  10. Boyle W. J., Lipsick J. S., Baluda M. A. Antibodies to the evolutionarily conserved amino-terminal region of the v-myb-encoded protein detect the c-myb protein in widely divergent metazoan species. Proc Natl Acad Sci U S A. 1986 Jul;83(13):4685–4689. doi: 10.1073/pnas.83.13.4685. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Bucher P., Trifonov E. N. Compilation and analysis of eukaryotic POL II promoter sequences. Nucleic Acids Res. 1986 Dec 22;14(24):10009–10026. doi: 10.1093/nar/14.24.10009. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Chen J. H. Expression of endogenous avian myeloblastosis virus information in different chicken cells. J Virol. 1980 Oct;36(1):162–170. doi: 10.1128/jvi.36.1.162-170.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem. 1987 Apr;162(1):156–159. doi: 10.1006/abio.1987.9999. [DOI] [PubMed] [Google Scholar]
  14. Cleveland J. L., Huleihel M., Bressler P., Siebenlist U., Akiyama L., Eisenman R. N., Rapp U. R. Negative regulation of c-myc transcription involves myc family proteins. Oncogene Res. 1988;3(4):357–375. [PubMed] [Google Scholar]
  15. Coll J., Saule S., Martin P., Raes M. B., Lagrou C., Graf T., Beug H., Simon I. E., Stehelin D. The cellular oncogenes c-myc, c-myb and c-erb are transcribed in defined types of avian hematopoietic cells. Exp Cell Res. 1983 Nov;149(1):151–162. doi: 10.1016/0014-4827(83)90388-9. [DOI] [PubMed] [Google Scholar]
  16. Craig R. W., Bloch A. Early decline in c-myb oncogene expression in the differentiation of human myeloblastic leukemia (ML-1) cells induced with 12-O-tetradecanoylphorbol-13-acetate. Cancer Res. 1984 Feb;44(2):442–446. [PubMed] [Google Scholar]
  17. Deininger P. L. Random subcloning of sonicated DNA: application to shotgun DNA sequence analysis. Anal Biochem. 1983 Feb 15;129(1):216–223. doi: 10.1016/0003-2697(83)90072-6. [DOI] [PubMed] [Google Scholar]
  18. Dvorák M., Bartůnek P., Pecenka V., Urbánek P., Trávnícek M. A search for c-myb gene regulatory sequences: cloning and restriction analysis of the 18-kb BamHI fragment of chicken chromosomal DNA, containing the 5' part of the c-myb gene. Folia Biol (Praha) 1989;35(2):102–109. [PubMed] [Google Scholar]
  19. Dvorák M., Trávnícek M., Sulová A., Ríman J. Two exons specific for the myb proto-oncogene found upstream from the avian myeloblastosis virus-transduced myb sequences. Folia Biol (Praha) 1987;33(1):1–10. [PubMed] [Google Scholar]
  20. Gardiner-Garden M., Frommer M. CpG islands in vertebrate genomes. J Mol Biol. 1987 Jul 20;196(2):261–282. doi: 10.1016/0022-2836(87)90689-9. [DOI] [PubMed] [Google Scholar]
  21. Gerondakis S., Bishop J. M. Structure of the protein encoded by the chicken proto-oncogene c-myb. Mol Cell Biol. 1986 Nov;6(11):3677–3684. doi: 10.1128/mcb.6.11.3677. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Gewirtz A. M., Calabretta B. A c-myb antisense oligodeoxynucleotide inhibits normal human hematopoiesis in vitro. Science. 1988 Dec 2;242(4883):1303–1306. doi: 10.1126/science.2461588. [DOI] [PubMed] [Google Scholar]
  23. Gonda T. J., Gough N. M., Dunn A. R., de Blaquiere J. Nucleotide sequence of cDNA clones of the murine myb proto-oncogene. EMBO J. 1985 Aug;4(8):2003–2008. doi: 10.1002/j.1460-2075.1985.tb03884.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Gonda T. J., Metcalf D. Expression of myb, myc and fos proto-oncogenes during the differentiation of a murine myeloid leukaemia. Nature. 1984 Jul 19;310(5974):249–251. doi: 10.1038/310249a0. [DOI] [PubMed] [Google Scholar]
  25. Gonda T. J., Sheiness D. K., Bishop J. M. Transcripts from the cellular homologs of retroviral oncogenes: distribution among chicken tissues. Mol Cell Biol. 1982 Jun;2(6):617–624. doi: 10.1128/mcb.2.6.617. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Hahn S. L., Hahn M., Hayward W. S. Structural organization of upstream exons and distribution of transcription start sites in the chicken c-myb gene. Mol Cell Biol. 1989 Feb;9(2):837–843. doi: 10.1128/mcb.9.2.837. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Klempnauer K. H., Bonifer C., Sippel A. E. Identification and characterization of the protein encoded by the human c-myb proto-oncogene. EMBO J. 1986 Aug;5(8):1903–1911. doi: 10.1002/j.1460-2075.1986.tb04443.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Klempnauer K. H., Gonda T. J., Bishop J. M. 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):453–463. doi: 10.1016/0092-8674(82)90138-6. [DOI] [PubMed] [Google Scholar]
  29. Klempnauer K. H. Interaction of myb proteins with nuclear matrix in vitro. Oncogene. 1988 Jun;2(6):545–551. [PubMed] [Google Scholar]
  30. Klempnauer K. H., Sippel A. E. Subnuclear localization of proteins encoded by the oncogene v-myb and its cellular homolog c-myb. Mol Cell Biol. 1986 Jan;6(1):62–69. doi: 10.1128/mcb.6.1.62. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Klempnauer K. H., Symonds G., Evan G. I., Bishop J. M. 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):537–547. doi: 10.1016/0092-8674(84)90384-2. [DOI] [PubMed] [Google Scholar]
  32. Majello B., Kenyon L. C., Dalla-Favera R. Human c-myb protooncogene: nucleotide sequence of cDNA and organization of the genomic locus. Proc Natl Acad Sci U S A. 1986 Dec;83(24):9636–9640. doi: 10.1073/pnas.83.24.9636. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Maxam A. M., Gilbert W. Sequencing end-labeled DNA with base-specific chemical cleavages. Methods Enzymol. 1980;65(1):499–560. doi: 10.1016/s0076-6879(80)65059-9. [DOI] [PubMed] [Google Scholar]
  34. Pecenka V., Dvorák M., Karafiát V., Sloncová E., Hlozánek I., Trávnícek M., Ríman J. Avian nephroblastomas induced by a retrovirus (MAV-2) lacking oncogene. II. Search for common sites of proviral integration in tumour DNA. Folia Biol (Praha) 1988;34(3):147–169. [PubMed] [Google Scholar]
  35. Pecenka V., Dvorák M., Trávnícek M. Avian nephroblastomas induced by a retrovirus (MAV-2) lacking oncogene. I. Construction of MAV-1 and MAV-2 proviral restriction maps and preparation of specific proviral molecular subclones. Folia Biol (Praha) 1988;34(3):129–146. [PubMed] [Google Scholar]
  36. Peters C. W., Sippel A. E., Vingron M., Klempnauer K. H. Drosophila and vertebrate myb proteins share two conserved regions, one of which functions as a DNA-binding domain. EMBO J. 1987 Oct;6(10):3085–3090. doi: 10.1002/j.1460-2075.1987.tb02616.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Rosson D., Reddy E. P. Nucleotide sequence of chicken c-myb complementary DNA and implications for myb oncogene activation. Nature. 1986 Feb 13;319(6054):604–606. doi: 10.1038/319604a0. [DOI] [PubMed] [Google Scholar]
  38. Roussel M., Saule S., Lagrou C., Rommens C., Beug H., Graf T., Stehelin D. Three new types of viral oncogene of cellular origin specific for haematopoietic cell transformation. Nature. 1979 Oct 11;281(5731):452–455. doi: 10.1038/281452a0. [DOI] [PubMed] [Google Scholar]
  39. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Sheiness D., Gardinier M. Expression of a proto-oncogene (proto-myb) in hemopoietic tissues of mice. Mol Cell Biol. 1984 Jul;4(7):1206–1212. doi: 10.1128/mcb.4.7.1206. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Slamon D. J., Boone T. C., Murdock D. C., Keith D. E., Press M. F., Larson R. A., Souza L. M. Studies of the human c-myb gene and its product in human acute leukemias. Science. 1986 Jul 18;233(4761):347–351. doi: 10.1126/science.3014652. [DOI] [PubMed] [Google Scholar]
  42. Soret J., Vellard M., Martinerie C., Perbal B. Organization of 5'-proximal c-myb exons in chicken DNA. Implications for c-myb tissue-specific transcription. FEBS Lett. 1988 May 9;232(1):227–234. doi: 10.1016/0014-5793(88)80422-8. [DOI] [PubMed] [Google Scholar]
  43. Thomas P. S. Hybridization of denatured RNA transferred or dotted nitrocellulose paper. Methods Enzymol. 1983;100:255–266. doi: 10.1016/0076-6879(83)00060-9. [DOI] [PubMed] [Google Scholar]
  44. Tocík Z., Arnold L., Smrt J. Automated 3'-H-phosphonate synthesis of oligodeoxyribonucleotides using amidine protected purine synthons. Nucleic Acids Symp Ser. 1987;(18):193–196. [PubMed] [Google Scholar]
  45. Urbánek P., Dvorák M., Bartunek P., Pecenka V., Paces V., Trávnícek M. Nucleotide sequence of chicken myb proto-oncogene promoter region: detection of an evolutionarily conserved element. Nucleic Acids Res. 1988 Dec 23;16(24):11521–11530. doi: 10.1093/nar/16.24.11521. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Vlach J., Dvorak M., Bartunek P., Pecenka V., Travnicek M., Sponar J. Supercoil-induced Z-DNA formation within 5'-end of chicken myb proto-oncogene. Biochem Biophys Res Commun. 1989 Feb 15;158(3):737–742. doi: 10.1016/0006-291x(89)92783-6. [DOI] [PubMed] [Google Scholar]
  47. Watson R. J. A transcriptional arrest mechanism involved in controlling constitutive levels of mouse c-myb mRNA. Oncogene. 1988 Mar;2(3):267–272. [PubMed] [Google Scholar]
  48. Watson R. J., Dyson P. J., McMahon J. Multiple c-myb transcript cap sites are variously utilized in cells of mouse haemopoietic origin. EMBO J. 1987 Jun;6(6):1643–1651. doi: 10.1002/j.1460-2075.1987.tb02413.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Westin E. H., Gallo R. C., Arya S. K., Eva A., Souza L. M., Baluda M. A., Aaronson S. A., Wong-Staal F. Differential expression of the amv gene in human hematopoietic cells. Proc Natl Acad Sci U S A. 1982 Apr;79(7):2194–2198. doi: 10.1073/pnas.79.7.2194. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Nucleic Acids Research are provided here courtesy of Oxford University Press

RESOURCES