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. 1987 Jan 12;15(1):87–103. doi: 10.1093/nar/15.1.87

Replication of proto-oncogenes early during the S phase in mammalian cell lines.

M A Iqbal, J Chinsky, V Didamo, C L Schildkraut
PMCID: PMC340399  PMID: 3469620

Abstract

Members of several classes of proto-oncogenes replicate during the first third of S-phase in two human (K562 erythroleukemia and HeLa), one Chinese hamster (CHO) and eight mouse cell lines. These cell lines exhibit a variety of specialized functions characteristic of pre-B and B cells, T cells and erythroid cells. The proto-oncogenes studied include fos, myc, myb, abl, fes, fms, mos, raf, rel, sis, Ha-ras, Ki-ras, and N-ras. In K562 cells, amplified and rearranged c-abl genes show a pattern of temporal replication during S that is similar to the pattern observed for the 5' breakpoint cluster region (bcr) and the amplified C lambda light chain immunoglobulin genes. The c-Ki-ras related sequences in CHO cells provide one example of late replicating proto-oncogene sequences that are present in multiple copies. The cellular gene N-myc replicates late during S in some of these cell lines. In three pre-B cell lines in which N-myc specific transcripts have been detected, N-myc replicates earlier in the S phase than in the other cell lines studied here.

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Selected References

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

  1. Alt F., Rosenberg N., Lewis S., Thomas E., Baltimore D. Organization and reorganization of immunoglobulin genes in A-MULV-transformed cells: rearrangement of heavy but not light chain genes. Cell. 1981 Dec;27(2 Pt 1):381–390. doi: 10.1016/0092-8674(81)90421-9. [DOI] [PubMed] [Google Scholar]
  2. Bishop J. M. Cellular oncogenes and retroviruses. Annu Rev Biochem. 1983;52:301–354. doi: 10.1146/annurev.bi.52.070183.001505. [DOI] [PubMed] [Google Scholar]
  3. Braunstein J. D., Schulze D., DelGiudice T., Furst A., Schildkraut C. L. The temporal order of replication of murine immunoglobulin heavy chain constant region sequences corresponds to their linear order in the genome. Nucleic Acids Res. 1982 Nov 11;10(21):6887–6902. doi: 10.1093/nar/10.21.6887. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Burke W., Fangman W. L. Temporal order in yeast chromosome replication. Cell. 1975 Jul;5(3):263–269. doi: 10.1016/0092-8674(75)90101-4. [DOI] [PubMed] [Google Scholar]
  5. Calza R. E., Eckhardt L. A., DelGiudice T., Schildkraut C. L. Changes in gene position are accompanied by a change in time of replication. Cell. 1984 Mar;36(3):689–696. doi: 10.1016/0092-8674(84)90349-0. [DOI] [PubMed] [Google Scholar]
  6. Campisi J., Gray H. E., Pardee A. B., Dean M., Sonenshein G. E. Cell-cycle control of c-myc but not c-ras expression is lost following chemical transformation. Cell. 1984 Feb;36(2):241–247. doi: 10.1016/0092-8674(84)90217-4. [DOI] [PubMed] [Google Scholar]
  7. Chattopadhyay S. K., Chang E. H., Lander M. R., Ellis R. W., Scolnick E. M., Lowy D. R. Amplification and rearrangement of onc genes in mammalian species. Nature. 1982 Mar 25;296(5855):361–363. doi: 10.1038/296361a0. [DOI] [PubMed] [Google Scholar]
  8. Chen I. S., Mak T. W., O'Rear J. J., Temin H. M. Characterization of reticuloendotheliosis virus strain T DNA and isolation of a novel variant of reticuloendotheliosis virus strain T by molecular cloning. J Virol. 1981 Dec;40(3):800–811. doi: 10.1128/jvi.40.3.800-811.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Collins S. J., Groudine M. T. Rearrangement and amplification of c-abl sequences in the human chronic myelogenous leukemia cell line K-562. Proc Natl Acad Sci U S A. 1983 Aug;80(15):4813–4817. doi: 10.1073/pnas.80.15.4813. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Curran T., Peters G., Van Beveren C., Teich N. M., Verma I. M. FBJ murine osteosarcoma virus: identification and molecular cloning of biologically active proviral DNA. J Virol. 1982 Nov;44(2):674–682. doi: 10.1128/jvi.44.2.674-682.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. D'Andrea A. D., Tantravahi U., Lalande M., Perle M. A., Latt S. A. High resolution analysis of the timing of replication of specific DNA sequences during S phase of mammalian cells. Nucleic Acids Res. 1983 Jul 25;11(14):4753–4774. doi: 10.1093/nar/11.14.4753. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. DePinho R. A., Legouy E., Feldman L. B., Kohl N. E., Yancopoulos G. D., Alt F. W. Structure and expression of the murine N-myc gene. Proc Natl Acad Sci U S A. 1986 Mar;83(6):1827–1831. doi: 10.1073/pnas.83.6.1827. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Ellis R. W., DeFeo D., Maryak J. M., Young H. A., Shih T. Y., Chang E. H., Lowy D. R., Scolnick E. M. Dual evolutionary origin for the rat genetic sequences of Harvey murine sarcoma virus. J Virol. 1980 Nov;36(2):408–420. doi: 10.1128/jvi.36.2.408-420.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Ellis R. W., Defeo D., Shih T. Y., Gonda M. A., Young H. A., Tsuchida N., Lowy D. R., Scolnick E. M. The p21 src genes of Harvey and Kirsten sarcoma viruses originate from divergent members of a family of normal vertebrate genes. Nature. 1981 Aug 6;292(5823):506–511. doi: 10.1038/292506a0. [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. George D. L., Scott A. F., de Martinville B., Francke U. Amplified DNA in Y1 mouse adrenal tumor cells: isolation of cDNAs complementary to an amplified c-Ki-ras gene and localization of homologous sequences to mouse chromosome 6. Nucleic Acids Res. 1984 Mar 26;12(6):2731–2743. doi: 10.1093/nar/12.6.2731. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. 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]
  18. Greenberg M. E., Ziff E. B. Stimulation of 3T3 cells induces transcription of the c-fos proto-oncogene. Nature. 1984 Oct 4;311(5985):433–438. doi: 10.1038/311433a0. [DOI] [PubMed] [Google Scholar]
  19. Grisham J. W., Greenberg D. S., Kaufman D. G., Smith G. J. Cycle-related toxicity and transformation in 10T1/2 cells treated with N-methyl-N'-nitro-N-nitrosoguanidine. Proc Natl Acad Sci U S A. 1980 Aug;77(8):4813–4817. doi: 10.1073/pnas.77.8.4813. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Grosveld G., Verwoerd T., van Agthoven T., de Klein A., Ramachandran K. L., Heisterkamp N., Stam K., Groffen J. The chronic myelocytic cell line K562 contains a breakpoint in bcr and produces a chimeric bcr/c-abl transcript. Mol Cell Biol. 1986 Feb;6(2):607–616. doi: 10.1128/mcb.6.2.607. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Hamlin J. L., Biedler J. L. Replication pattern of a large homogenously staining chromosome region in antifolate-resistant Chinese hamster cell lines. J Cell Physiol. 1981 Apr;107(1):101–114. doi: 10.1002/jcp.1041070112. [DOI] [PubMed] [Google Scholar]
  22. Heisterkamp N., Stephenson J. R., Groffen J., Hansen P. F., de Klein A., Bartram C. R., Grosveld G. Localization of the c-ab1 oncogene adjacent to a translocation break point in chronic myelocytic leukaemia. Nature. 1983 Nov 17;306(5940):239–242. doi: 10.1038/306239a0. [DOI] [PubMed] [Google Scholar]
  23. Hollis G. F., Hieter P. A., McBride O. W., Swan D., Leder P. Processed genes: a dispersed human immunoglobulin gene bearing evidence of RNA-type processing. Nature. 1982 Mar 25;296(5855):321–325. doi: 10.1038/296321a0. [DOI] [PubMed] [Google Scholar]
  24. Iqbal M. A., Plumb M., Stein J., Stein G., Schildkraut C. L. Coordinate replication of members of the multigene family of core and H1 human histone genes. Proc Natl Acad Sci U S A. 1984 Dec;81(24):7723–7727. doi: 10.1073/pnas.81.24.7723. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Jakobovits A., Schwab M., Bishop J. M., Martin G. R. Expression of N-myc in teratocarcinoma stem cells and mouse embryos. Nature. 1985 Nov 14;318(6042):188–191. doi: 10.1038/318188a0. [DOI] [PubMed] [Google Scholar]
  26. Jansen H. W., Lurz R., Bister K., Bonner T. I., Mark G. E., Rapp U. R. Homologous cell-derived oncogenes in avian carcinoma virus MH2 and murine sarcoma virus 3611. Nature. 1984 Jan 19;307(5948):281–284. doi: 10.1038/307281a0. [DOI] [PubMed] [Google Scholar]
  27. Kellems R. E., Harper M. E., Smith L. M. Amplified dihydrofolate reductase genes are located in chromosome regions containing DNA that replicates during the first half of S-phase. J Cell Biol. 1982 Feb;92(2):531–539. doi: 10.1083/jcb.92.2.531. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Kirsch I. R., Ravetch J. V., Kwan S. P., Max E. E., Ney R. L., Leder P. Multiple immunoglobulin switch region homologies outside the heavy chain constant region locus. Nature. 1981 Oct 15;293(5833):585–587. doi: 10.1038/293585a0. [DOI] [PubMed] [Google Scholar]
  29. Kohl N. E., Gee C. E., Alt F. W. Activated expression of the N-myc gene in human neuroblastomas and related tumors. Science. 1984 Dec 14;226(4680):1335–1337. doi: 10.1126/science.6505694. [DOI] [PubMed] [Google Scholar]
  30. Kohl N. E., Kanda N., Schreck R. R., Bruns G., Latt S. A., Gilbert F., Alt F. W. Transposition and amplification of oncogene-related sequences in human neuroblastomas. Cell. 1983 Dec;35(2 Pt 1):359–367. doi: 10.1016/0092-8674(83)90169-1. [DOI] [PubMed] [Google Scholar]
  31. Lavi S. Carcinogen-mediated amplification of viral DNA sequences in simian virus 40-transformed Chinese hamster embryo cells. Proc Natl Acad Sci U S A. 1981 Oct;78(10):6144–6148. doi: 10.1073/pnas.78.10.6144. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Mariani B. D., Schimke R. T. Gene amplification in a single cell cycle in Chinese hamster ovary cells. J Biol Chem. 1984 Feb 10;259(3):1901–1910. [PubMed] [Google Scholar]
  33. Murray M. J., Cunningham J. M., Parada L. F., Dautry F., Lebowitz P., Weinberg R. A. The HL-60 transforming sequence: a ras oncogene coexisting with altered myc genes in hematopoietic tumors. Cell. 1983 Jul;33(3):749–757. doi: 10.1016/0092-8674(83)90017-x. [DOI] [PubMed] [Google Scholar]
  34. 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]
  35. Perbal B., Baluda M. A. Avian myeloblastosis virus transforming gene is related to unique chicken DNA regions separated by at least one intervening sequence. J Virol. 1982 Jan;41(1):250–257. doi: 10.1128/jvi.41.1.250-257.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Robbins K. C., Devare S. G., Aaronson S. A. Molecular cloning of integrated simian sarcoma virus: genome organization of infectious DNA clones. Proc Natl Acad Sci U S A. 1981 May;78(5):2918–2922. doi: 10.1073/pnas.78.5.2918. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Santos E., Martin-Zanca D., Reddy E. P., Pierotti M. A., Della Porta G., Barbacid M. Malignant activation of a K-ras oncogene in lung carcinoma but not in normal tissue of the same patient. Science. 1984 Feb 17;223(4637):661–664. doi: 10.1126/science.6695174. [DOI] [PubMed] [Google Scholar]
  38. Schimke R. T. Gene amplification in cultured animal cells. Cell. 1984 Jul;37(3):705–713. doi: 10.1016/0092-8674(84)90406-9. [DOI] [PubMed] [Google Scholar]
  39. Selden J. R., Emanuel B. S., Wang E., Cannizzaro L., Palumbo A., Erikson J., Nowell P. C., Rovera G., Croce C. M. Amplified C lambda and c-abl genes are on the same marker chromosome in K562 leukemia cells. Proc Natl Acad Sci U S A. 1983 Dec;80(23):7289–7292. doi: 10.1073/pnas.80.23.7289. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Silverstone A., Sun L., Witte O. N., Baltimore D. Biosynthesis of murine terminal deoxynucleotidyltransferase. J Biol Chem. 1980 Jan 25;255(2):791–796. [PubMed] [Google Scholar]
  41. Stanton L. W., Watt R., Marcu K. B. Translocation, breakage and truncated transcripts of c-myc oncogene in murine plasmacytomas. Nature. 1983 Jun 2;303(5916):401–406. doi: 10.1038/303401a0. [DOI] [PubMed] [Google Scholar]
  42. Sukumar S., Pulciani S., Doniger J., DiPaolo J. A., Evans C. H., Zbar B., Barbacid M. A transforming ras gene in tumorigenic guinea pig cell lines initiated by diverse chemical carcinogens. Science. 1984 Mar 16;223(4641):1197–1199. doi: 10.1126/science.6322298. [DOI] [PubMed] [Google Scholar]
  43. Tlsty T. D., Brown P. C., Schimke R. T. UV radiation facilitates methotrexate resistance and amplification of the dihydrofolate reductase gene in cultured 3T6 mouse cells. Mol Cell Biol. 1984 Jun;4(6):1050–1056. doi: 10.1128/mcb.4.6.1050. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. 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]
  45. Zimmerman K. A., Yancopoulos G. D., Collum R. G., Smith R. K., Kohl N. E., Denis K. A., Nau M. M., Witte O. N., Toran-Allerand D., Gee C. E. Differential expression of myc family genes during murine development. 1986 Feb 27-Mar 5Nature. 319(6056):780–783. doi: 10.1038/319780a0. [DOI] [PubMed] [Google Scholar]

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