Skip to main content
NCBI home page
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1983 Dec;80(24):7385–7389. doi: 10.1073/pnas.80.24.7385

Structural organization and expression of human DNA sequences related to the transforming gene of avian myeloblastosis virus.

G Franchini, F Wong-Staal, M A Baluda, C Lengel, S R Tronick
PMCID: PMC389955  PMID: 6324165

Abstract

Bacteriophage libraries of human DNA were screened for sequences homologous to the transforming gene (v-myb) of avian myeloblastosis virus. The three overlapping clones isolated were shown to contain a total of 1.0 kilobase pair (kbp) of sequence related to v-myb distributed over 6.2 kbp. Restriction enzyme mapping and heteroduplex analysis revealed the presence of five myb-related domains interrupted by four stretches of non-homology. To study the extent of human DNA coding sequences that constitute the myb gene homologue, c-myb (human), probes spanning about 30 kbp were prepared from the clones and used to study transcription in a human hematopoietic cell line (MOLT-4). Each of the probes hybridized a 4.5-kilobase transcript, which suggests that either the c-myb (human) gene encompasses 30 kbp or it contains two or more transcription units that each give rise to a mRNA of 4.5 kilobases.

Full text

PDF
7385

Images in this article

7386Image
on p.7386
7387Image
on p.7387
7388Image
on p.7388
7388Image
on p.7388

Selected References

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

  1. Adams S. L., Sobel M. E., Howard B. H., Olden K., Yamada K. M., de Crombrugghe B., Pastan I. Levels of translatable mRNAs for cell surface protein, collagen precursors, and two membrane proteins are altered in Rous sarcoma virus-transformed chick embryo fibroblasts. Proc Natl Acad Sci U S A. 1977 Aug;74(8):3399–3403. doi: 10.1073/pnas.74.8.3399. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Benton W. D., Davis R. W. Screening lambdagt recombinant clones by hybridization to single plaques in situ. Science. 1977 Apr 8;196(4286):180–182. doi: 10.1126/science.322279. [DOI] [PubMed] [Google Scholar]
  3. 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]
  4. Blair D. G., Oskarsson M., Wood T. G., McClements W. L., Fischinger P. J., Vande Woude G. G. Activation of the transforming potential of a normal cell sequence: a molecular model for oncogenesis. Science. 1981 May 22;212(4497):941–943. doi: 10.1126/science.7233190. [DOI] [PubMed] [Google Scholar]
  5. Boyle W. J., Lipsick J. S., Reddy E. P., Baluda M. A. Identification of the leukemogenic protein of avian myeloblastosis virus and of its normal cellular homologue. Proc Natl Acad Sci U S A. 1983 May;80(10):2834–2838. doi: 10.1073/pnas.80.10.2834. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Chang E. H., Furth M. E., Scolnick E. M., Lowy D. R. Tumorigenic transformation of mammalian cells induced by a normal human gene homologous to the oncogene of Harvey murine sarcoma virus. Nature. 1982 Jun 10;297(5866):479–483. doi: 10.1038/297479a0. [DOI] [PubMed] [Google Scholar]
  7. Chang E. H., Gonda M. A., Ellis R. W., Scolnick E. M., Lowy D. R. Human genome contains four genes homologous to transforming genes of Harvey and Kirsten murine sarcoma viruses. Proc Natl Acad Sci U S A. 1982 Aug;79(16):4848–4852. doi: 10.1073/pnas.79.16.4848. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Coffin J. M., Varmus H. E., Bishop J. M., Essex M., Hardy W. D., Jr, Martin G. S., Rosenberg N. E., Scolnick E. M., Weinberg R. A., Vogt P. K. Proposal for naming host cell-derived inserts in retrovirus genomes. J Virol. 1981 Dec;40(3):953–957. doi: 10.1128/jvi.40.3.953-957.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Dalla-Favera R., Bregni M., Erikson J., Patterson D., Gallo R. C., Croce C. M. Human c-myc onc gene is located on the region of chromosome 8 that is translocated in Burkitt lymphoma cells. Proc Natl Acad Sci U S A. 1982 Dec;79(24):7824–7827. doi: 10.1073/pnas.79.24.7824. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Dalla-Favera R., Franchini G., Martinotti S., Wong-Staal F., Gallo R. C., Croce C. M. Chromosomal assignment of the human homologues of feline sarcoma virus and avian myeloblastosis virus onc genes. Proc Natl Acad Sci U S A. 1982 Aug;79(15):4714–4717. doi: 10.1073/pnas.79.15.4714. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Dalla-Favera R., Gelmann E. P., Gallo R. C., Wong-Staal F. A human onc gene homologous to the transforming gene (v-sis) of simian sarcoma virus. Nature. 1981 Jul 2;292(5818):31–35. doi: 10.1038/292031a0. [DOI] [PubMed] [Google Scholar]
  12. DeFeo D., Gonda M. A., Young H. A., Chang E. H., Lowy D. R., Scolnick E. M., Ellis R. W. Analysis of two divergent rat genomic clones homologous to the transforming gene of Harvey murine sarcoma virus. Proc Natl Acad Sci U S A. 1981 Jun;78(6):3328–3332. doi: 10.1073/pnas.78.6.3328. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Der C. J., Krontiris T. G., Cooper G. M. Transforming genes of human bladder and lung carcinoma cell lines are homologous to the ras genes of Harvey and Kirsten sarcoma viruses. Proc Natl Acad Sci U S A. 1982 Jun;79(11):3637–3640. doi: 10.1073/pnas.79.11.3637. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Eva A., Robbins K. C., Andersen P. R., Srinivasan A., Tronick S. R., Reddy E. P., Ellmore N. W., Galen A. T., Lautenberger J. A., Papas T. S. Cellular genes analogous to retroviral onc genes are transcribed in human tumour cells. Nature. 1982 Jan 14;295(5845):116–119. doi: 10.1038/295116a0. [DOI] [PubMed] [Google Scholar]
  15. Franchini G., Even J., Sherr C. J., Wong-Staal F. onc sequences (v-fes) of Snyder-Theilen feline sarcoma virus are derived from noncontiguous regions of a cat cellular gene (c-fes). Nature. 1981 Mar 12;290(5802):154–157. doi: 10.1038/290154a0. [DOI] [PubMed] [Google Scholar]
  16. Franchini G., Gelmann E. P., Dalla-Favera R., Gallo R. C., Wong-Staal F. Human gene (c-fes) related to the onc sequences of Snyder-Theilen feline sarcoma virus. Mol Cell Biol. 1982 Aug;2(8):1014–1019. doi: 10.1128/mcb.2.8.1014. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Fritsch E. F., Lawn R. M., Maniatis T. Molecular cloning and characterization of the human beta-like globin gene cluster. Cell. 1980 Apr;19(4):959–972. doi: 10.1016/0092-8674(80)90087-2. [DOI] [PubMed] [Google Scholar]
  18. Fung Y. K., Lewis W. G., Crittenden L. B., Kung H. J. 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):357–368. doi: 10.1016/0092-8674(83)90417-8. [DOI] [PubMed] [Google Scholar]
  19. Gallo R. C., Wong-Staal F. Retroviruses as etiologic agents of some animal and human leukemias and lymphomas and as tools for elucidating the molecular mechanism of leukemogenesis. Blood. 1982 Sep;60(3):545–557. [PubMed] [Google Scholar]
  20. Goff S. P., Gilboa E., Witte O. N., Baltimore D. Structure of the Abelson murine leukemia virus genome and the homologous cellular gene: studies with cloned viral DNA. Cell. 1980 Dec;22(3):777–785. doi: 10.1016/0092-8674(80)90554-1. [DOI] [PubMed] [Google Scholar]
  21. 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]
  22. Groffen J., Heisterkamp N., Grosveld F., Van de Ven W., Stephenson J. R. Isolation of human oncogene sequences (v-fes homolog) from a cosmid library. Science. 1982 Jun 4;216(4550):1136–1138. doi: 10.1126/science.6281890. [DOI] [PubMed] [Google Scholar]
  23. Harper M. E., Franchini G., Love J., Simon M. I., Gallo R. C., Wong-Staal F. Chromosomal sublocalization of human c-myb and c-fes cellular onc genes. Nature. 1983 Jul 14;304(5922):169–171. doi: 10.1038/304169a0. [DOI] [PubMed] [Google Scholar]
  24. Hayata I., Oshimura M., Minowada J., Sandberg A. A. Chromosomal banding of cultured T and B lymphocytes. In Vitro. 1975 Nov-Dec;11(6):361–368. doi: 10.1007/BF02616372. [DOI] [PubMed] [Google Scholar]
  25. Hayward W. S., Neel B. G., Astrin S. M. Activation of a cellular onc gene by promoter insertion in ALV-induced lymphoid leukosis. Nature. 1981 Apr 9;290(5806):475–480. doi: 10.1038/290475a0. [DOI] [PubMed] [Google Scholar]
  26. Hieter P. A., Max E. E., Seidman J. G., Maizel J. V., Jr, Leder P. Cloned human and mouse kappa immunoglobulin constant and J region genes conserve homology in functional segments. Cell. 1980 Nov;22(1 Pt 1):197–207. doi: 10.1016/0092-8674(80)90168-3. [DOI] [PubMed] [Google Scholar]
  27. Houck C. M., Rinehart F. P., Schmid C. W. A ubiquitous family of repeated DNA sequences in the human genome. J Mol Biol. 1979 Aug 15;132(3):289–306. doi: 10.1016/0022-2836(79)90261-4. [DOI] [PubMed] [Google Scholar]
  28. Klein G. The role of gene dosage and genetic transpositions in carcinogenesis. Nature. 1981 Nov 26;294(5839):313–318. doi: 10.1038/294313a0. [DOI] [PubMed] [Google Scholar]
  29. 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]
  30. Leprince D., Saule S., de Taisne C., Gegonne A., Begue A., Righi M., Stehelin D. The human DNA locus related to the oncogene myb of avian myeloblastosis virus (AMV): molecular cloning and structural characterization. EMBO J. 1983;2(7):1073–1078. doi: 10.1002/j.1460-2075.1983.tb01548.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Minowada J., Onuma T., Moore G. E. Rosette-forming human lymphoid cell lines. I. Establishment and evidence for origin of thymus-derived lymphocytes. J Natl Cancer Inst. 1972 Sep;49(3):891–895. [PubMed] [Google Scholar]
  32. Mushinski J. F., Potter M., Bauer S. R., Reddy E. P. DNA rearrangement and altered RNA expression of the c-myb oncogene in mouse plasmacytoid lymphosarcomas. Science. 1983 May 20;220(4599):795–798. doi: 10.1126/science.6687762. [DOI] [PubMed] [Google Scholar]
  33. NOWELL P. C., HUNGERFORD D. A. CHROMOSOME CHANGES IN HUMAN LEUKEMIA AND A TENTATIVE ASSESSMENT OF THEIR SIGNIFICANCE. Ann N Y Acad Sci. 1964 Feb 28;113:654–662. doi: 10.1111/j.1749-6632.1964.tb40697.x. [DOI] [PubMed] [Google Scholar]
  34. Nishikura K., ar-Rushdi A., Erikson J., Watt R., Rovera G., Croce C. M. Differential expression of the normal and of the translocated human c-myc oncogenes in B cells. Proc Natl Acad Sci U S A. 1983 Aug;80(15):4822–4826. doi: 10.1073/pnas.80.15.4822. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Oskarsson M., McClements W. L., Blair D. G., Maizel J. V., Vande Woude G. F. Properties of a normal mouse cell DNA sequence (sarc) homologous to the src sequence of Moloney sarcoma virus. Science. 1980 Mar 14;207(4436):1222–1224. doi: 10.1126/science.6243788. [DOI] [PubMed] [Google Scholar]
  36. Parada L. F., Tabin C. J., Shih C., Weinberg R. A. Human EJ bladder carcinoma oncogene is homologue of Harvey sarcoma virus ras gene. Nature. 1982 Jun 10;297(5866):474–478. doi: 10.1038/297474a0. [DOI] [PubMed] [Google Scholar]
  37. Parker R. C., Varmus H. E., Bishop J. M. Cellular homologue (c-src) of the transforming gene of Rous sarcoma virus: isolation, mapping, and transcriptional analysis of c-src and flanking regions. Proc Natl Acad Sci U S A. 1981 Sep;78(9):5842–5846. doi: 10.1073/pnas.78.9.5842. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Payne G. S., Bishop J. M., Varmus H. E. Multiple arrangements of viral DNA and an activated host oncogene in bursal lymphomas. Nature. 1982 Jan 21;295(5846):209–214. doi: 10.1038/295209a0. [DOI] [PubMed] [Google Scholar]
  39. Perbal B., Cline J. M., Hillyard R. L., Baluda M. A. Organization of chicken DNA sequences homologous to the transforming gene of avian myeloblastosis virus. II. Isolation and characterization of lambda proto-amv DNA recombinant clones from a library of leukemic chicken DNA. J Virol. 1983 Mar;45(3):925–940. doi: 10.1128/jvi.45.3.925-940.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Prakash K., McBride O. W., Swan D. C., Devare S. G., Tronick S. R., Aaronson S. A. Molecular cloning and chromosomal mapping of a human locus related to the transforming gene of Moloney murine sarcoma virus. Proc Natl Acad Sci U S A. 1982 Sep;79(17):5210–5214. doi: 10.1073/pnas.79.17.5210. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Robins T., Bister K., Garon C., Papas T., Duesberg P. Structural relationship between a normal chicken DNA locus and the transforming gene of the avian acute leukemia virus MC29. J Virol. 1982 Feb;41(2):635–642. doi: 10.1128/jvi.41.2.635-642.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Rowley J. D. Letter: A new consistent chromosomal abnormality in chronic myelogenous leukaemia identified by quinacrine fluorescence and Giemsa staining. Nature. 1973 Jun 1;243(5405):290–293. doi: 10.1038/243290a0. [DOI] [PubMed] [Google Scholar]
  43. Rushlow K. E., Lautenberger J. A., Papas T. S., Baluda M. A., Perbal B., Chirikjian J. G., Reddy E. P. Nucleotide sequence of the transforming gene of avian myeloblastosis virus. Science. 1982 Jun 25;216(4553):1421–1423. doi: 10.1126/science.6283631. [DOI] [PubMed] [Google Scholar]
  44. Santos E., Tronick S. R., Aaronson S. A., Pulciani S., Barbacid M. T24 human bladder carcinoma oncogene is an activated form of the normal human homologue of BALB- and Harvey-MSV transforming genes. Nature. 1982 Jul 22;298(5872):343–347. doi: 10.1038/298343a0. [DOI] [PubMed] [Google Scholar]
  45. Shalloway D., Zelenetz A. D., Cooper G. M. Molecular cloning and characterization of the chicken gene homologous to the transforming gene of Rous sarcoma virus. Cell. 1981 May;24(2):531–541. doi: 10.1016/0092-8674(81)90344-5. [DOI] [PubMed] [Google Scholar]
  46. Southern E. M. Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol. 1975 Nov 5;98(3):503–517. doi: 10.1016/s0022-2836(75)80083-0. [DOI] [PubMed] [Google Scholar]
  47. Souza L. M., Strommer J. N., Hillyard R. L., Komaromy M. C., Baluda M. A. Cellular sequences are present in the presumptive avian myeloblastosis virus genome. Proc Natl Acad Sci U S A. 1980 Sep;77(9):5177–5181. doi: 10.1073/pnas.77.9.5177. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Thomas P. S. Hybridization of denatured RNA and small DNA fragments transferred to nitrocellulose. Proc Natl Acad Sci U S A. 1980 Sep;77(9):5201–5205. doi: 10.1073/pnas.77.9.5201. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Trus M. D., Sodroski J. G., Haseltine W. A. Isolation and characterization of a human locus homologous to the transforming gene (v-fes) of feline sarcoma virus. J Biol Chem. 1982 Mar 25;257(6):2730–2733. [PubMed] [Google Scholar]
  50. Vennström B., Bishop J. M. Isolation and characterization of chicken DNA homologous to the two putative oncogenes of avian erythroblastosis virus. Cell. 1982 Jan;28(1):135–143. doi: 10.1016/0092-8674(82)90383-x. [DOI] [PubMed] [Google Scholar]
  51. Wahl G. M., Stern M., Stark G. R. Efficient transfer of large DNA fragments from agarose gels to diazobenzyloxymethyl-paper and rapid hybridization by using dextran sulfate. Proc Natl Acad Sci U S A. 1979 Aug;76(8):3683–3687. doi: 10.1073/pnas.76.8.3683. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Watson R., Oskarsson M., Vande Woude G. F. Human DNA sequence homologous to the transforming gene (mos) of Moloney murine sarcoma virus. Proc Natl Acad Sci U S A. 1982 Jul;79(13):4078–4082. doi: 10.1073/pnas.79.13.4078. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Watson R., Oskarsson M., Vande Woude G. F. Human DNA sequence homologous to the transforming gene (mos) of Moloney murine sarcoma virus. Proc Natl Acad Sci U S A. 1982 Jul;79(13):4078–4082. doi: 10.1073/pnas.79.13.4078. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. 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]
  55. Westin E. H., Wong-Staal F., Gelmann E. P., Dalla-Favera R., Papas T. S., Lautenberger J. A., Eva A., Reddy E. P., Tronick S. R., Aaronson S. A. Expression of cellular homologues of retroviral onc genes in human hematopoietic cells. Proc Natl Acad Sci U S A. 1982 Apr;79(8):2490–2494. doi: 10.1073/pnas.79.8.2490. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES