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. 1990 Aug;87(16):6039–6043. doi: 10.1073/pnas.87.16.6039

A human cellular sequence implicated in trk oncogene activation is DNA damage inducible.

R Ben-Ishai 1, R Scharf 1, R Sharon 1, I Kapten 1
PMCID: PMC54467  PMID: 1696715

Abstract

Xeroderma pigmentosum cells, which are deficient in the repair of UV light-induced DNA damage, have been used to clone DNA-damage-inducible transcripts in human cells. The cDNA clone designated pC-5 hybridizes on RNA gel blots to a 1-kilobase transcript, which is moderately abundant in nontreated cells and whose synthesis is enhanced in human cells following UV irradiation or treatment with several other DNA-damaging agents. UV-enhanced transcription of C-5 RNA is transient and occurs at lower fluences and to a greater extent in DNA-repair-deficient than in DNA-repair-proficient cells. Southern blot analysis indicates that the C-5 gene belongs to a multigene family. A cDNA clone containing the complete coding sequence of C-5 was isolated. Sequence analysis revealed that it is homologous to a human cellular sequence encoding the amino-terminal activating sequence of the trk-2h chimeric oncogene [Kozma, S. C., Redmond, S. M. S., Xiao-Chang, F., Saurer, S. M., Groner, B. & Hynes, N. E. (1988) EMBO J. 7, 147-154]. The presence of DNA-damage-responsive sequences at the 5' end of a chimeric oncogene could result in enhanced expression of the oncogene in response to carcinogens.

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Selected References

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

  1. Angel P., Baumann I., Stein B., Delius H., Rahmsdorf H. J., Herrlich P. 12-O-tetradecanoyl-phorbol-13-acetate induction of the human collagenase gene is mediated by an inducible enhancer element located in the 5'-flanking region. Mol Cell Biol. 1987 Jun;7(6):2256–2266. doi: 10.1128/mcb.7.6.2256. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Angel P., Pöting A., Mallick U., Rahmsdorf H. J., Schorpp M., Herrlich P. Induction of metallothionein and other mRNA species by carcinogens and tumor promoters in primary human skin fibroblasts. Mol Cell Biol. 1986 May;6(5):1760–1766. doi: 10.1128/mcb.6.5.1760. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Barnes D., Clayton L., Chumbley G., MacLeod A. R. Activation of the trk oncogene by alternatively spliced muscle and non-muscle tropomyosin sequences. Oncogene. 1989 Feb;4(2):259–262. [PubMed] [Google Scholar]
  4. Ben-Ishai R., Sharon R., Rothman M., Miskin R. DNA repair and induction of plasminogen activator in human fetal cells treated with ultraviolet light. Carcinogenesis. 1984 Mar;5(3):357–362. doi: 10.1093/carcin/5.3.357. [DOI] [PubMed] [Google Scholar]
  5. Birnboim H. C. Rapid extraction of high molecular weight RNA from cultured cells and granulocytes for Northern analysis. Nucleic Acids Res. 1988 Feb 25;16(4):1487–1497. doi: 10.1093/nar/16.4.1487. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Büscher M., Rahmsdorf H. J., Litfin M., Karin M., Herrlich P. Activation of the c-fos gene by UV and phorbol ester: different signal transduction pathways converge to the same enhancer element. Oncogene. 1988 Sep;3(3):301–311. [PubMed] [Google Scholar]
  7. Canaani D., Naiman T., Teitz T., Berg P. Immortalization of xeroderma pigmentosum cells by simian virus 40 DNA having a defective origin of DNA replication. Somat Cell Mol Genet. 1986 Jan;12(1):13–20. doi: 10.1007/BF01560723. [DOI] [PubMed] [Google Scholar]
  8. Chang L. S., Pan S., Pater M. M., Di Mayorca G. Differential requirement for SV40 early genes in immortalization and transformation of primary rat and human embryonic cells. Virology. 1985 Oct 30;146(2):246–261. doi: 10.1016/0042-6822(85)90008-x. [DOI] [PubMed] [Google Scholar]
  9. Cleaver J. E., Bootsma D. Xeroderma pigmentosum: biochemical and genetic characteristics. Annu Rev Genet. 1975;9:19–38. doi: 10.1146/annurev.ge.09.120175.000315. [DOI] [PubMed] [Google Scholar]
  10. Feinberg A. P., Vogelstein B. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem. 1983 Jul 1;132(1):6–13. doi: 10.1016/0003-2697(83)90418-9. [DOI] [PubMed] [Google Scholar]
  11. Fornace A. J., Jr, Alamo I., Jr, Hollander M. C. DNA damage-inducible transcripts in mammalian cells. Proc Natl Acad Sci U S A. 1988 Dec;85(23):8800–8804. doi: 10.1073/pnas.85.23.8800. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Fornace A. J., Jr, Schalch H., Alamo I., Jr Coordinate induction of metallothioneins I and II in rodent cells by UV irradiation. Mol Cell Biol. 1988 Nov;8(11):4716–4720. doi: 10.1128/mcb.8.11.4716. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Giallongo A., Yon J., Fried M. Ribosomal protein L7a is encoded by a gene (Surf-3) within the tightly clustered mouse surfeit locus. Mol Cell Biol. 1989 Jan;9(1):224–231. doi: 10.1128/mcb.9.1.224. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Glazer P. M., Greggio N. A., Metherall J. E., Summers W. C. UV-induced DNA-binding proteins in human cells. Proc Natl Acad Sci U S A. 1989 Feb;86(4):1163–1167. doi: 10.1073/pnas.86.4.1163. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Gubler U., Hoffman B. J. A simple and very efficient method for generating cDNA libraries. Gene. 1983 Nov;25(2-3):263–269. doi: 10.1016/0378-1119(83)90230-5. [DOI] [PubMed] [Google Scholar]
  16. Hanahan D. Studies on transformation of Escherichia coli with plasmids. J Mol Biol. 1983 Jun 5;166(4):557–580. doi: 10.1016/s0022-2836(83)80284-8. [DOI] [PubMed] [Google Scholar]
  17. Hanawalt P. C. Concepts and models for DNA repair: from Escherichia coli to mammalian cells. Environ Mol Mutagen. 1989;14 (Suppl 16):90–98. doi: 10.1002/em.2850140617. [DOI] [PubMed] [Google Scholar]
  18. Hollander M. C., Fornace A. J., Jr Induction of fos RNA by DNA-damaging agents. Cancer Res. 1989 Apr 1;49(7):1687–1692. [PubMed] [Google Scholar]
  19. Huxley C., Williams T., Fried M. One of the tightly clustered genes of the mouse surfeit locus is a highly expressed member of a multigene family whose other members are predominantly processed pseudogenes. Mol Cell Biol. 1988 Sep;8(9):3898–3905. doi: 10.1128/mcb.8.9.3898. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Kartasova T., van de Putte P. Isolation, characterization, and UV-stimulated expression of two families of genes encoding polypeptides of related structure in human epidermal keratinocytes. Mol Cell Biol. 1988 May;8(5):2195–2203. doi: 10.1128/mcb.8.5.2195. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Kozma S. C., Redmond S. M., Fu X. C., Saurer S. M., Groner B., Hynes N. E. Activation of the receptor kinase domain of the trk oncogene by recombination with two different cellular sequences. EMBO J. 1988 Jan;7(1):147–154. doi: 10.1002/j.1460-2075.1988.tb02794.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Lambert M. E., Ronai Z. A., Weinstein I. B., Garrels J. I. Enhancement of major histocompatibility class I protein synthesis by DNA damage in cultured human fibroblasts and keratinocytes. Mol Cell Biol. 1989 Feb;9(2):847–850. doi: 10.1128/mcb.9.2.847. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Mallick U., Rahmsdorf H. J., Yamamoto N., Ponta H., Wegner R. D., Herrlich P. 12-O-tetradecanoylphorbol 13-acetate-inducible proteins are synthesized at an increased rate in Bloom syndrome fibroblasts. Proc Natl Acad Sci U S A. 1982 Dec;79(24):7886–7890. doi: 10.1073/pnas.79.24.7886. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Martin-Zanca D., Hughes S. H., Barbacid M. A human oncogene formed by the fusion of truncated tropomyosin and protein tyrosine kinase sequences. 1986 Feb 27-Mar 5Nature. 319(6056):743–748. doi: 10.1038/319743a0. [DOI] [PubMed] [Google Scholar]
  25. Mezzina M., Nocentini S., Sarasin A. DNA ligase activity in carcinogen-treated human fibroblasts. Biochimie. 1982 Aug-Sep;64(8-9):743–748. doi: 10.1016/s0300-9084(82)80122-3. [DOI] [PubMed] [Google Scholar]
  26. Miskin R., Ben-Ishai R. Induction of plasminogen activator by UV light in normal and xeroderma pigmentosum fibroblasts. Proc Natl Acad Sci U S A. 1981 Oct;78(10):6236–6240. doi: 10.1073/pnas.78.10.6236. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Okayama H., Berg P. A cDNA cloning vector that permits expression of cDNA inserts in mammalian cells. Mol Cell Biol. 1983 Feb;3(2):280–289. doi: 10.1128/mcb.3.2.280. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Oskam R., Coulier F., Ernst M., Martin-Zanca D., Barbacid M. Frequent generation of oncogenes by in vitro recombination of TRK protooncogene sequences. Proc Natl Acad Sci U S A. 1988 May;85(9):2964–2968. doi: 10.1073/pnas.85.9.2964. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Ronai Z. A., Okin E., Weinstein I. B. Ultraviolet light induces the expression of oncogenes in rat fibroblast and human keratinocyte cells. Oncogene. 1988 Feb;2(2):201–204. [PubMed] [Google Scholar]
  30. Rotem N., Axelrod J. H., Miskin R. Induction of urokinase-type plasminogen activator by UV light in human fetal fibroblasts is mediated through a UV-induced secreted protein. Mol Cell Biol. 1987 Feb;7(2):622–631. doi: 10.1128/mcb.7.2.622. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. 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]
  32. Sarasin A. SOS response in mammalian cells. Cancer Invest. 1985;3(2):163–174. doi: 10.3109/07357908509017499. [DOI] [PubMed] [Google Scholar]
  33. Sarkar S., Dasgupta U. B., Summers W. C. Error-prone mutagenesis detected in mammalian cells by a shuttle vector containing the supF gene of Escherichia coli. Mol Cell Biol. 1984 Oct;4(10):2227–2230. doi: 10.1128/mcb.4.10.2227. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Schorpp M., Mallick U., Rahmsdorf H. J., Herrlich P. UV-induced extracellular factor from human fibroblasts communicates the UV response to nonirradiated cells. Cell. 1984 Jul;37(3):861–868. doi: 10.1016/0092-8674(84)90421-5. [DOI] [PubMed] [Google Scholar]
  35. Vos J. M., Hanawalt P. C. DNA interstrand cross-links promote chromosomal integration of a selected gene in human cells. Mol Cell Biol. 1989 Jul;9(7):2897–2905. doi: 10.1128/mcb.9.7.2897. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Walker G. C. Inducible DNA repair systems. Annu Rev Biochem. 1985;54:425–457. doi: 10.1146/annurev.bi.54.070185.002233. [DOI] [PubMed] [Google Scholar]
  37. Witkin E. M. Ultraviolet mutagenesis and inducible DNA repair in Escherichia coli. Bacteriol Rev. 1976 Dec;40(4):869–907. doi: 10.1128/br.40.4.869-907.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Yancopoulos G. D., Blackwell T. K., Suh H., Hood L., Alt F. W. Introduced T cell receptor variable region gene segments recombine in pre-B cells: evidence that B and T cells use a common recombinase. Cell. 1986 Jan 31;44(2):251–259. doi: 10.1016/0092-8674(86)90759-2. [DOI] [PubMed] [Google Scholar]
  39. Ziemiecki A., Müller R. G., Fu X. C., Hynes N. E., Kozma S. Oncogenic activation of the human trk proto-oncogene by recombination with the ribosomal large subunit protein L7a. EMBO J. 1990 Jan;9(1):191–196. doi: 10.1002/j.1460-2075.1990.tb08095.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. van Duin M., Westerveld A., Hoeijmakers J. H. UV stimulation of DNA-mediated transformation of human cells. Mol Cell Biol. 1985 Apr;5(4):734–741. doi: 10.1128/mcb.5.4.734. [DOI] [PMC free article] [PubMed] [Google Scholar]

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