A 127 kDa component of a UV-damaged DNA-binding complex, which is defective in some xeroderma pigmentosum group E patients, is homologous to a slime mold protein (original) (raw)

Abstract

A cDNA which encodes a approximately 127 kDa UV-damaged DNA-binding (UV-DDB) protein with high affinity for (6-4)pyrimidine dimers [Abramic', M., Levine, A.S. & Protic', M., J. Biol. Chem. 266: 22493-22500, 1991] has been isolated from a monkey cell cDNA library. The presence of this protein in complexes bound to UV-damaged DNA was confirmed by immunoblotting. The human cognate of the UV-DDB gene was localized to chromosome 11. UV-DDB mRNA was expressed in all human tissues examined, including cells from two patients with xeroderma pigmentosum (group E) that are deficient in UV-DDB activity, which suggests that the binding defect in these cells may reside in a dysfunctional UV-DDB protein. Database searches have revealed significant homology of the UV-DDB protein sequence with partial sequences of yet uncharacterized proteins from Dictyostelium discoideum (44% identity over 529 amino acids) and Oryza sativa (54% identity over 74 residues). According to our results, the UV-DDB polypeptide belongs to a highly conserved, structurally novel family of proteins that may be involved in the early steps of the UV response, e.g., DNA damage recognition.

4111

Images in this article

Selected References

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

  1. Abramić M., Levine A. S., Protić M. Purification of an ultraviolet-inducible, damage-specific DNA-binding protein from primate cells. J Biol Chem. 1991 Nov 25;266(33):22493–22500. [PubMed] [Google Scholar]
  2. Adams M. D., Kelley J. M., Gocayne J. D., Dubnick M., Polymeropoulos M. H., Xiao H., Merril C. R., Wu A., Olde B., Moreno R. F. Complementary DNA sequencing: expressed sequence tags and human genome project. Science. 1991 Jun 21;252(5013):1651–1656. doi: 10.1126/science.2047873. [DOI] [PubMed] [Google Scholar]
  3. Aebersold R. H., Leavitt J., Saavedra R. A., Hood L. E., Kent S. B. Internal amino acid sequence analysis of proteins separated by one- or two-dimensional gel electrophoresis after in situ protease digestion on nitrocellulose. Proc Natl Acad Sci U S A. 1987 Oct;84(20):6970–6974. doi: 10.1073/pnas.84.20.6970. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Akrigg D., Attwood T. K., Bleasby A. J., Findlay J. B., North A. C., Maughan N. A., Parry-Smith D. J., Perkins D. N., Wootton J. C. SERPENT--an information storage and analysis resource for protein sequences. Comput Appl Biosci. 1992 Jun;8(3):295–296. doi: 10.1093/bioinformatics/8.3.295. [DOI] [PubMed] [Google Scholar]
  5. Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J. Basic local alignment search tool. J Mol Biol. 1990 Oct 5;215(3):403–410. doi: 10.1016/S0022-2836(05)80360-2. [DOI] [PubMed] [Google Scholar]
  6. Altschul S. F., Lipman D. J. Protein database searches for multiple alignments. Proc Natl Acad Sci U S A. 1990 Jul;87(14):5509–5513. doi: 10.1073/pnas.87.14.5509. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Bootsma D., Hoeijmakers J. H. DNA repair. Engagement with transcription. Nature. 1993 May 13;363(6425):114–115. doi: 10.1038/363114a0. [DOI] [PubMed] [Google Scholar]
  8. Brash D. E., Rudolph J. A., Simon J. A., Lin A., McKenna G. J., Baden H. P., Halperin A. J., Pontén J. A role for sunlight in skin cancer: UV-induced p53 mutations in squamous cell carcinoma. Proc Natl Acad Sci U S A. 1991 Nov 15;88(22):10124–10128. doi: 10.1073/pnas.88.22.10124. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Bronner C. E., Welker D. L., Deering R. A. Mutations affecting sensitivity of the cellular slime mold Dictyostelium discoideum to DNA-damaging agents. Mutat Res. 1992 Sep;274(3):187–200. doi: 10.1016/0921-8777(92)90065-b. [DOI] [PubMed] [Google Scholar]
  10. Chirgwin J. M., Przybyla A. E., MacDonald R. J., Rutter W. J. Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease. Biochemistry. 1979 Nov 27;18(24):5294–5299. doi: 10.1021/bi00591a005. [DOI] [PubMed] [Google Scholar]
  11. Chu G., Chang E. Cisplatin-resistant cells express increased levels of a factor that recognizes damaged DNA. Proc Natl Acad Sci U S A. 1990 May;87(9):3324–3327. doi: 10.1073/pnas.87.9.3324. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Chu G., Chang E. Xeroderma pigmentosum group E cells lack a nuclear factor that binds to damaged DNA. Science. 1988 Oct 28;242(4878):564–567. doi: 10.1126/science.3175673. [DOI] [PubMed] [Google Scholar]
  13. Eker A. P., Vermeulen W., Miura N., Tanaka K., Jaspers N. G., Hoeijmakers J. H., Bootsma D. Xeroderma pigmentosum group A correcting protein from calf thymus. Mutat Res. 1992 Sep;274(3):211–224. doi: 10.1016/0921-8777(92)90067-d. [DOI] [PubMed] [Google Scholar]
  14. Friedberg E. C. Xeroderma pigmentosum, Cockayne's syndrome, helicases, and DNA repair: what's the relationship? Cell. 1992 Dec 11;71(6):887–889. doi: 10.1016/0092-8674(92)90384-o. [DOI] [PubMed] [Google Scholar]
  15. Ghosh D. TFD: the transcription factors database. Nucleic Acids Res. 1992 May 11;20 (Suppl):2091–2093. doi: 10.1093/nar/20.suppl.2091. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Hirschfeld S., Levine A. S., Ozato K., Protić M. A constitutive damage-specific DNA-binding protein is synthesized at higher levels in UV-irradiated primate cells. Mol Cell Biol. 1990 May;10(5):2041–2048. doi: 10.1128/mcb.10.5.2041. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Hoeijmakers J. H. How relevant is the Escherichia coli UvrABC model for excision repair in eukaryotes? J Cell Sci. 1991 Dec;100(Pt 4):687–691. doi: 10.1242/jcs.100.4.687. [DOI] [PubMed] [Google Scholar]
  18. Hwang B. J., Chu G. Purification and characterization of a human protein that binds to damaged DNA. Biochemistry. 1993 Feb 16;32(6):1657–1666. doi: 10.1021/bi00057a033. [DOI] [PubMed] [Google Scholar]
  19. Johansen T., Moens U., Holm T., Fjose A., Krauss S. Zebrafish pou[c]: a divergent POU family gene ubiquitously expressed during embryogenesis. Nucleic Acids Res. 1993 Feb 11;21(3):475–483. doi: 10.1093/nar/21.3.475. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Karlin S., Altschul S. F. Methods for assessing the statistical significance of molecular sequence features by using general scoring schemes. Proc Natl Acad Sci U S A. 1990 Mar;87(6):2264–2268. doi: 10.1073/pnas.87.6.2264. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Kataoka H., Fujiwara Y. UV damage-specific DNA-binding protein in xeroderma pigmentosum complementation group E. Biochem Biophys Res Commun. 1991 Mar 29;175(3):1139–1143. doi: 10.1016/0006-291x(91)91684-5. [DOI] [PubMed] [Google Scholar]
  22. Keeney S., Wein H., Linn S. Biochemical heterogeneity in xeroderma pigmentosum complementation group E. Mutat Res. 1992 Jan;273(1):49–56. doi: 10.1016/0921-8777(92)90049-9. [DOI] [PubMed] [Google Scholar]
  23. Khan A. S., Wilcox A. S., Polymeropoulos M. H., Hopkins J. A., Stevens T. J., Robinson M., Orpana A. K., Sikela J. M. Single pass sequencing and physical and genetic mapping of human brain cDNAs. Nat Genet. 1992 Nov;2(3):180–185. doi: 10.1038/ng1192-180. [DOI] [PubMed] [Google Scholar]
  24. Kondo S., Fukuro S., Mamada A., Kawada A., Satoh Y., Fujiwara Y. Assignment of three patients with xeroderma pigmentosum to complementation group E and their characteristics. J Invest Dermatol. 1988 Feb;90(2):152–157. doi: 10.1111/1523-1747.ep12462130. [DOI] [PubMed] [Google Scholar]
  25. Kondo S., Mamada A., Miyamoto C., Keong C. H., Satoh Y., Fujiwara Y. Late onset of skin cancers in 2 xeroderma pigmentosum group F siblings and a review of 30 Japanese xeroderma pigmentosum patients in groups D, E and F. Photodermatol. 1989 Apr;6(2):89–95. [PubMed] [Google Scholar]
  26. Kozak M. Point mutations define a sequence flanking the AUG initiator codon that modulates translation by eukaryotic ribosomes. Cell. 1986 Jan 31;44(2):283–292. doi: 10.1016/0092-8674(86)90762-2. [DOI] [PubMed] [Google Scholar]
  27. Legerski R., Peterson C. Expression cloning of a human DNA repair gene involved in xeroderma pigmentosum group C. Nature. 1992 Sep 3;359(6390):70–73. doi: 10.1038/359070a0. [DOI] [PubMed] [Google Scholar]
  28. McLenigan M., Levine A. S., Protić M. Differential expression of pyrimidine dimer-binding proteins in normal and UV light-treated vertebrate cells. Photochem Photobiol. 1993 Apr;57(4):655–662. doi: 10.1111/j.1751-1097.1993.tb02932.x. [DOI] [PubMed] [Google Scholar]
  29. Mitchell D. L., Nairn R. S. The biology of the (6-4) photoproduct. Photochem Photobiol. 1989 Jun;49(6):805–819. doi: 10.1111/j.1751-1097.1989.tb05578.x. [DOI] [PubMed] [Google Scholar]
  30. Mitchell D. L. The relative cytotoxicity of (6-4) photoproducts and cyclobutane dimers in mammalian cells. Photochem Photobiol. 1988 Jul;48(1):51–57. doi: 10.1111/j.1751-1097.1988.tb02785.x. [DOI] [PubMed] [Google Scholar]
  31. O'Donovan A., Wood R. D. Identical defects in DNA repair in xeroderma pigmentosum group G and rodent ERCC group 5. Nature. 1993 May 13;363(6425):185–188. doi: 10.1038/363185a0. [DOI] [PubMed] [Google Scholar]
  32. Protić-Sabljić M., Tuteja N., Munson P. J., Hauser J., Kraemer K. H., Dixon K. UV light-induced cyclobutane pyrimidine dimers are mutagenic in mammalian cells. Mol Cell Biol. 1986 Oct;6(10):3349–3356. doi: 10.1128/mcb.6.10.3349. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Robins P., Jones C. J., Biggerstaff M., Lindahl T., Wood R. D. Complementation of DNA repair in xeroderma pigmentosum group A cell extracts by a protein with affinity for damaged DNA. EMBO J. 1991 Dec;10(12):3913–3921. doi: 10.1002/j.1460-2075.1991.tb04961.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Roza L., Vermeulen W., Bergen Henegouwen J. B., Eker A. P., Jaspers N. G., Lohman P. H., Hoeijmakers J. H. Effects of microinjected photoreactivating enzyme on thymine dimer removal and DNA repair synthesis in normal human and xeroderma pigmentosum fibroblasts. Cancer Res. 1990 Mar 15;50(6):1905–1910. [PubMed] [Google Scholar]
  35. Scherly D., Nouspikel T., Corlet J., Ucla C., Bairoch A., Clarkson S. G. Complementation of the DNA repair defect in xeroderma pigmentosum group G cells by a human cDNA related to yeast RAD2. Nature. 1993 May 13;363(6425):182–185. doi: 10.1038/363182a0. [DOI] [PubMed] [Google Scholar]
  36. Stone K. L., Williams K. R. High-performance liquid chromatographic peptide mapping and amino acid analysis in the sub-nanomole range. J Chromatogr. 1986 May 30;359:203–212. doi: 10.1016/0021-9673(86)80074-7. [DOI] [PubMed] [Google Scholar]
  37. Studier F. W., Rosenberg A. H., Dunn J. J., Dubendorff J. W. Use of T7 RNA polymerase to direct expression of cloned genes. Methods Enzymol. 1990;185:60–89. doi: 10.1016/0076-6879(90)85008-c. [DOI] [PubMed] [Google Scholar]
  38. Tempst P., Link A. J., Riviere L. R., Fleming M., Elicone C. Internal sequence analysis of proteins separated on polyacrylamide gels at the submicrogram level: improved methods, applications and gene cloning strategies. Electrophoresis. 1990 Jul;11(7):537–553. doi: 10.1002/elps.1150110704. [DOI] [PubMed] [Google Scholar]
  39. Tempst P., Riviere L. Examination of automated polypeptide sequencing using standard phenyl isothiocyanate reagent and subpicomole high-performance liquid chromatographic analysis. Anal Biochem. 1989 Dec;183(2):290–300. doi: 10.1016/0003-2697(89)90482-x. [DOI] [PubMed] [Google Scholar]
  40. Thielmann H. W., Popanda O., Edler L., Jung E. G. Clinical symptoms and DNA repair characteristics of xeroderma pigmentosum patients from Germany. Cancer Res. 1991 Jul 1;51(13):3456–3470. [PubMed] [Google Scholar]
  41. Treiber D. K., Chen Z., Essigmann J. M. An ultraviolet light-damaged DNA recognition protein absent in xeroderma pigmentosum group E cells binds selectively to pyrimidine (6-4) pyrimidone photoproducts. Nucleic Acids Res. 1992 Nov 11;20(21):5805–5810. doi: 10.1093/nar/20.21.5805. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Van Houten B. Nucleotide excision repair in Escherichia coli. Microbiol Rev. 1990 Mar;54(1):18–51. doi: 10.1128/mr.54.1.18-51.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Van Houten B. Nucleotide excision repair in Escherichia coli. Microbiol Rev. 1990 Mar;54(1):18–51. doi: 10.1128/mr.54.1.18-51.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Zelle B., Lohman P. H. Repair of UV-endonuclease-susceptible sites in the 7 complementation groups of xeroderma pigmentosum A through G. Mutat Res. 1979 Sep;62(2):363–368. doi: 10.1016/0027-5107(79)90091-5. [DOI] [PubMed] [Google Scholar]