Home LiteratureArticle Details
PMID: 15964821 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Centrin 2 stimulates nucleotide excision repair by interacting with xeroderma pigmentosum group C protein.

Molecular and cellular biology ·Vol. 25 ·No. 13 ·2005-07-00 ·Pages 5664-74

Nishi R, Okuda Y, Watanabe E, Mori T, Iwai S, Masutani C, Sugasawa K, Hanaoka F

Abstract

Xeroderma pigmentosum group C (XPC) protein plays a key role in DNA damage recognition in global genome nucleotide excision repair (NER). The protein forms in vivo a heterotrimeric complex involving one of the two human homologs of Saccharomyces cerevisiae Rad23p and centrin 2, a centrosomal protein. Because centrin 2 is dispensable for the cell-free NER reaction, its role in NER has been unclear. Binding experiments with a series of truncated XPC proteins allowed the centrin 2 binding domain to be mapped to a presumed alpha-helical region near the C terminus, and three amino acid substitutions in this domain abrogated interaction with centrin 2. Human cell lines stably expressing the mutant XPC protein exhibited a significant reduction in global genome NER activity. Furthermore, centrin 2 enhanced the cell-free NER dual incision and damaged DNA binding activities of XPC, which likely require physical interaction between XPC and centrin 2. These results reveal a novel vital function for centrin 2 in NER, the potentiation of damage recognition by XPC.

MeSH Terms
Amino Acid Motifs Amino Acid Sequence Calcium-Binding Proteins Cell Cycle Proteins/chemistry,metabolism Cell Line Conserved Sequence DNA/genetics,metabolism DNA Damage/radiation effects DNA Repair DNA-Binding Proteins/chemistry,genetics,metabolism Humans Molecular Sequence Data Mutation Protein Binding Protein Structure, Tertiary Sequence Homology, Amino Acid Ultraviolet Rays Xeroderma Pigmentosum/genetics,metabolism
Chemicals
CETN2 protein, human Calcium-Binding Proteins Cell Cycle Proteins DNA-Binding Proteins XPC protein, human DNA
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
Nishi Ryotaro
Cellular Physiology Laboratory, RIKEN Discovery Research Institute, 2-1 Hirosawa, Wako, Saitama 351-0198, Japan.
Okuda Yuki
Watanabe Eriko
Mori Toshio
Iwai Shigenori
Masutani Chikahide
Sugasawa Kaoru
Hanaoka Fumio
References (75)
75 references, click to expand
  1. How calmodulin binds its targets: sequence independent recognition of amphiphilic alpha-helices.
    Trends Biochem Sci. 1990 Feb;15(2):59-64 PMID: 2186516
  2. Efficient selection for high-expression transfectants with a novel eukaryotic vector.
    Gene. 1991 Dec 15;108(2):193-9 PMID: 1660837
  3. Simultaneous establishment of monoclonal antibodies specific for either cyclobutane pyrimidine dimer or (6-4)photoproduct from the same mouse immunized with ultraviolet-irradiated DNA.
    Photochem Photobiol. 1991 Aug;54(2):225-32 PMID: 1780359
  4. Solution structure of a calmodulin-target peptide complex by multidimensional NMR.
    Science. 1992 May 1;256(5057):632-8 PMID: 1585175
  5. Target enzyme recognition by calmodulin: 2.4 A structure of a calmodulin-peptide complex.
    Science. 1992 Aug 28;257(5074):1251-5 PMID: 1519061
  6. 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):5805-10 PMID: 1454541
  7. Comparative analysis of binding of human damaged DNA-binding protein (XPE) and Escherichia coli damage recognition protein (UvrA) to the major ultraviolet photoproducts: T[c,s]T, T[t,s]T, T[6-4]T, and T[Dewar]T.
    J Biol Chem. 1993 Oct 5;268(28):21301-8 PMID: 8407968
  8. The calcium-binding protein cell division cycle 31 of Saccharomyces cerevisiae is a component of the half bridge of the spindle pole body.
    J Cell Biol. 1993 Oct;123(2):405-16 PMID: 8408222
  9. Preferential binding of the xeroderma pigmentosum group A complementing protein to damaged DNA.
    Biochemistry. 1993 Nov 16;32(45):12096-104 PMID: 8218288
  10. Molecular cloning and centrosomal localization of human caltractin.
    Proc Natl Acad Sci U S A. 1993 Dec 1;90(23):11039-43 PMID: 8248209
  11. Centrin plays an essential role in microtubule severing during flagellar excision in Chlamydomonas reinhardtii.
    J Cell Biol. 1994 Mar;124(5):795-805 PMID: 8120100
  12. UV-induced ubiquitylation of XPC protein mediated by UV-DDB-ubiquitin ligase complex.
    Cell. 2005 May 6;121(3):387-400 PMID: 15882621
  13. Mutational analysis of centrin: an EF-hand protein associated with three distinct contractile fibers in the basal body apparatus of Chlamydomonas.
    J Cell Biol. 1992 Dec;119(6):1613-24 PMID: 1361488
  14. Nucleotide excision repair of DNA with recombinant human proteins: definition of the minimal set of factors, active forms of TFIIH, and modulation by CAK.
    Genes Dev. 2000 Feb 1;14(3):349-59 PMID: 10673506
  15. C-terminal half of human centrin 2 behaves like a regulatory EF-hand domain.
    Biochemistry. 2003 Feb 18;42(6):1439-50 PMID: 12578356
  16. Calmodulin target database.
    J Struct Funct Genomics. 2000;1(1):8-14 PMID: 12836676
  17. A novel regulation mechanism of DNA repair by damage-induced and RAD23-dependent stabilization of xeroderma pigmentosum group C protein.
    Genes Dev. 2003 Jul 1;17(13):1630-45 PMID: 12815074
  18. The comings and goings of nucleotide excision repair factors on damaged DNA.
    EMBO J. 2003 Oct 1;22(19):5293-303 PMID: 14517266
  19. Xeroderma pigmentosum group C protein possesses a high affinity binding site to human centrin 2 and calmodulin.
    J Biol Chem. 2003 Oct 10;278(41):40252-61 PMID: 12890685
  20. In vivo recruitment of XPC to UV-induced cyclobutane pyrimidine dimers by the DDB2 gene product.
    J Biol Chem. 2003 Nov 21;278(47):46906-10 PMID: 12944386
  21. CENTRIN2 modulates homologous recombination and nucleotide excision repair in Arabidopsis.
    Plant Cell. 2004 Jun;16(6):1633-43 PMID: 15155891
  22. A new, tenth subunit of TFIIH is responsible for the DNA repair syndrome trichothiodystrophy group A.
    Nat Genet. 2004 Jul;36(7):714-9 PMID: 15220921
  23. Relative levels of the two mammalian Rad23 homologs determine composition and stability of the xeroderma pigmentosum group C protein complex.
    DNA Repair (Amst). 2004 Oct 5;3(10):1285-95 PMID: 15336624
  24. A rapid, sensitive, and specific method for the determination of protein in dilute solution.
    Anal Biochem. 1973 Dec;56(2):502-14 PMID: 4128882
  25. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding.
    Anal Biochem. 1976 May 7;72:248-54 PMID: 942051
  26. Differential expression and cellular distribution of centrin isoforms during human ciliated cell differentiation in vitro.
    J Cell Sci. 2000 Apr;113 ( Pt 8):1355-64 PMID: 10725219
  27. Reconstitution of damage DNA excision reaction from SV40 minichromosomes with purified nucleotide excision repair proteins.
    Mutat Res. 2000 Mar 20;459(2):147-60 PMID: 10725665
  28. The xeroderma pigmentosum group C protein complex XPC-HR23B plays an important role in the recruitment of transcription factor IIH to damaged DNA.
    J Biol Chem. 2000 Mar 31;275(13):9870-5 PMID: 10734143
  29. Cation- and peptide-binding properties of human centrin 2.
    FEBS Lett. 2000 Apr 28;472(2-3):208-12 PMID: 10788612
  30. Stable binding of human XPC complex to irradiated DNA confers strong discrimination for damaged sites.
    J Mol Biol. 2000 Jul 7;300(2):275-90 PMID: 10873465
  31. A multistep damage recognition mechanism for global genomic nucleotide excision repair.
    Genes Dev. 2001 Mar 1;15(5):507-21 PMID: 11238373
  32. Strong functional interactions of TFIIH with XPC and XPG in human DNA nucleotide excision repair, without a preassembled repairosome.
    Mol Cell Biol. 2001 Apr;21(7):2281-91 PMID: 11259578
  33. Diversity of the damage recognition step in the global genomic nucleotide excision repair in vitro.
    Mutat Res. 2001 Apr 4;485(3):219-27 PMID: 11267833
  34. Structure of the gating domain of a Ca2+-activated K+ channel complexed with Ca2+/calmodulin.
    Nature. 2001 Apr 26;410(6832):1120-4 PMID: 11323678
  35. Genome maintenance mechanisms for preventing cancer.
    Nature. 2001 May 17;411(6835):366-74 PMID: 11357144
  36. Centrosome protein centrin 2/caltractin 1 is part of the xeroderma pigmentosum group C complex that initiates global genome nucleotide excision repair.
    J Biol Chem. 2001 Jun 1;276(22):18665-72 PMID: 11279143
  37. Phosphorylation of centrin during the cell cycle and its role in centriole separation preceding centrosome duplication.
    J Biol Chem. 2001 Jun 8;276(23):20774-80 PMID: 11279195
  38. Sequential assembly of the nucleotide excision repair factors in vivo.
    Mol Cell. 2001 Jul;8(1):213-24 PMID: 11511374
  39. Structural basis for the activation of anthrax adenylyl cyclase exotoxin by calmodulin.
    Nature. 2002 Jan 24;415(6870):396-402 PMID: 11807546
  40. How nucleotide excision repair protects against cancer.
    Nat Rev Cancer. 2001 Oct;1(1):22-33 PMID: 11900249
  41. Centrin-2 is required for centriole duplication in mammalian cells.
    Curr Biol. 2002 Aug 6;12(15):1287-92 PMID: 12176356
  42. A molecular mechanism for DNA damage recognition by the xeroderma pigmentosum group C protein complex.
    DNA Repair (Amst). 2002 Jan 22;1(1):95-107 PMID: 12509299
  43. The carboxy-terminal domain of the XPC protein plays a crucial role in nucleotide excision repair through interactions with transcription factor IIH.
    DNA Repair (Amst). 2002 Jun 21;1(6):449-61 PMID: 12509233
  44. DNA bending by the human damage recognition complex XPC-HR23B.
    DNA Repair (Amst). 2003 Mar 1;2(3):325-36 PMID: 12547395
  45. Striated flagellar roots: isolation and partial characterization of a calcium-modulated contractile organelle.
    J Cell Biol. 1984 Sep;99(3):962-70 PMID: 6381510
  46. Yeast gene required for spindle pole body duplication: homology of its product with Ca2+-binding proteins.
    Proc Natl Acad Sci U S A. 1986 Aug;83(15):5512-6 PMID: 3526331
  47. Purification and characterization of a basal body-associated Ca2+-binding protein.
    J Cell Biol. 1988 Jul;107(1):121-31 PMID: 3292538
  48. Recombinant replication protein A: expression, complex formation, and functional characterization.
    J Biol Chem. 1994 Apr 15;269(15):11121-32 PMID: 8157639
  49. Purification and cloning of a nucleotide excision repair complex involving the xeroderma pigmentosum group C protein and a human homologue of yeast RAD23.
    EMBO J. 1994 Apr 15;13(8):1831-43 PMID: 8168482
  50. Cloning of a cDNA encoding human centrin, an EF-hand protein of centrosomes and mitotic spindle poles.
    J Cell Sci. 1994 Jan;107 ( Pt 1):9-16 PMID: 8175926
  51. DNA repair defect in xeroderma pigmentosum group C and complementing factor from HeLa cells.
    J Biol Chem. 1994 Sep 9;269(36):22749-57 PMID: 8077226
  52. XPG endonuclease makes the 3' incision in human DNA nucleotide excision repair.
    Nature. 1994 Sep 29;371(6496):432-5 PMID: 8090225
  53. Reconstitution of human DNA repair excision nuclease in a highly defined system.
    J Biol Chem. 1995 Feb 10;270(6):2415-8 PMID: 7852297
  54. Human DNA repair excision nuclease. Analysis of the roles of the subunits involved in dual incisions by using anti-XPG and anti-ERCC1 antibodies.
    J Biol Chem. 1995 Sep 1;270(35):20862-9 PMID: 7657672
  55. XPC and human homologs of RAD23: intracellular localization and relationship to other nucleotide excision repair complexes.
    Nucleic Acids Res. 1996 Jul 1;24(13):2551-9 PMID: 8692695
  56. PHD: predicting one-dimensional protein structure by profile-based neural networks.
    Methods Enzymol. 1996;266:525-39 PMID: 8743704
  57. HHR23B, a human Rad23 homolog, stimulates XPC protein in nucleotide excision repair in vitro.
    Mol Cell Biol. 1996 Sep;16(9):4852-61 PMID: 8756644
  58. Xeroderma pigmentosum group F caused by a defect in a structure-specific DNA repair endonuclease.
    Cell. 1996 Sep 6;86(5):811-22 PMID: 8797827
  59. Most of centrin in animal cells is not centrosome-associated and centrosomal centrin is confined to the distal lumen of centrioles.
    J Cell Sci. 1996 Dec;109 ( Pt 13):3089-102 PMID: 9004043
  60. Open complex formation around a lesion during nucleotide excision repair provides a structure for cleavage by human XPG protein.
    EMBO J. 1997 Feb 3;16(3):625-38 PMID: 9034344
  61. The non-catalytic function of XPG protein during dual incision in human nucleotide excision repair.
    J Biol Chem. 1997 Jun 20;272(25):16030-4 PMID: 9188507
  62. Identification of a new mammalian centrin gene, more closely related to Saccharomyces cerevisiae CDC31 gene.
    Proc Natl Acad Sci U S A. 1997 Aug 19;94(17):9141-6 PMID: 9256449
  63. The role of calcium in the regulation of apoptosis.
    Biochem Biophys Res Commun. 1997 Oct 20;239(2):357-66 PMID: 9344835
  64. Characterization of reaction intermediates of human excision repair nuclease.
    J Biol Chem. 1997 Nov 14;272(46):28971-9 PMID: 9360969
  65. Two human homologs of Rad23 are functionally interchangeable in complex formation and stimulation of XPC repair activity.
    Mol Cell Biol. 1997 Dec;17(12):6924-31 PMID: 9372924
  66. Mechanism of open complex and dual incision formation by human nucleotide excision repair factors.
    EMBO J. 1997 Nov 3;16(21):6559-73 PMID: 9351836
  67. Expression of centrin isoforms in the mammalian retina.
    Exp Cell Res. 1998 Jul 10;242(1):10-7 PMID: 9665797
  68. Xeroderma pigmentosum group C protein complex is the initiator of global genome nucleotide excision repair.
    Mol Cell. 1998 Aug;2(2):223-32 PMID: 9734359
  69. Differential regulation of centrin genes during ciliogenesis in human tracheal epithelial cells.
    Am J Physiol. 1998 Dec;275(6 Pt 1):L1145-56 PMID: 9843852
  70. Molecular mechanism of nucleotide excision repair.
    Genes Dev. 1999 Apr 1;13(7):768-85 PMID: 10197977
  71. Effect of DNA lesions on transcription elongation.
    Biochimie. 1999 Jan-Feb;81(1-2):139-46 PMID: 10214918
  72. Characterization of DNA recognition by the human UV-damaged DNA-binding protein.
    J Biol Chem. 1999 Jul 9;274(28):20027-33 PMID: 10391953
  73. Molecular cloning of cDNA for caltractin, a basal body-associated Ca2+-binding protein: homology in its protein sequence with calmodulin and the yeast CDC31 gene product.
    J Cell Biol. 1988 Jul;107(1):133-40 PMID: 2839516
  74. The centrin-based cytoskeleton of Chlamydomonas reinhardtii: distribution in interphase and mitotic cells.
    J Cell Biol. 1988 Aug;107(2):635-41 PMID: 3047144
  75. Centrin-mediated microtubule severing during flagellar excision in Chlamydomonas reinhardtii.
    J Cell Biol. 1989 May;108(5):1751-60 PMID: 2654141
Article Info
Journal
Molecular and cellular biology
Abbr.
Mol Cell Biol
ISSN
0270-7306
Published
2005-07-00
Pages
5664-74
Language
English
Region
United States
NLM ID
8109087
PMCID
PMC1156980
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]