Home LiteratureArticle Details
PMID: 10563794 Published · ppublish English Journal Article Research Support, U.S. Gov't, Non-P.H.S.

Interactions of human nucleotide excision repair protein XPA with DNA and RPA70 Delta C327: chemical shift mapping and 15N NMR relaxation studies.

Biochemistry ·Vol. 38 ·No. 46 ·1999-11-16 ·Pages 15116-28

Buchko GW, Daughdrill GW, de Lorimier R, Rao B K, Isern NG, Lingbeck JM, Taylor JS, Wold MS, Gochin M, Spicer LD, Lowry DF, Kennedy MA

Abstract

Human XPA is an essential component in the multienzyme nucleotide excision repair (NER) pathway. The solution structure of the minimal DNA binding domain of XPA (XPA-MBD: M98-F219) was recently determined [Buchko et al. (1998) Nucleic Acids Res. 26, 2779-2788, Ikegami et al. (1998) Nat. Struct. Biol. 5, 701-706] and shown to consist of a compact zinc-binding core and a loop-rich C-terminal subdomain connected by a linker sequence. Here, the solution structure of XPA-MBD was further refined using an entirely new class of restraints based on pseudocontact shifts measured in cobalt-substituted XPA-MBD. Using this structure, the surface of XPA-MBD which interacts with DNA and a fragment of the largest subunit of replication protein A (RPA70 Delta C327: M1-Y326) was determined using chemical shift mapping. DNA binding in XPA-MBD was highly localized in the loop-rich subdomain for DNA with or without a lesion [dihydrothymidine (dhT) or 6-4-thymidine-cytidine (64TC)], or with DNA in single- or double-stranded form, indicating that the character of the lesion itself is not the driving force for XPA binding DNA. RPA70 Delta C327 was found to contact regions in both the zinc-binding and loop-rich subdomains. Some overlap of the DNA and RPA70 Delta C327 binding regions was observed in the loop-rich subdomain, indicating a possible cooperative DNA-binding mode between XPA and RPA70 Delta C327. To complement the chemical shift mapping data, the backbone dynamics of free XPA-MBD and XPA-MBD bound to DNA oligomers containing dhT or 64TC lesions were investigated using 15N NMR relaxation data. The dynamic analyses for the XPA-MBD complexes with DNA revealed localized increases and decreases in S2 and an increase in the global correlation time. Regions of XPA-MBD with the largest increases in S2 overlapped regions having the largest chemical shifts changes upon binding DNA, indicating that the loop-rich subdomain becomes more rigid upon binding DNA. Interestingly, S2 decreased for some residues in the zinc-binding core upon DNA association, indicating a possible concerted structural rearrangement on binding DNA.

MeSH Terms
Binding Sites DNA/chemistry,metabolism DNA Repair DNA Replication DNA, Single-Stranded/chemistry,metabolism DNA-Binding Proteins/chemistry,metabolism Humans Nitrogen Isotopes Nuclear Magnetic Resonance, Biomolecular Oligodeoxyribonucleotides/chemistry,metabolism Peptide Fragments/chemistry,metabolism Protein Conformation RNA-Binding Proteins/chemistry,metabolism Replication Protein A Solutions Thermodynamics Xeroderma Pigmentosum Group A Protein
Chemicals
DNA, Single-Stranded DNA-Binding Proteins Nitrogen Isotopes Oligodeoxyribonucleotides Peptide Fragments RNA-Binding Proteins RPA1 protein, human Replication Protein A Solutions XPA protein, human Xeroderma Pigmentosum Group A Protein DNA
Authors & Affiliations
12 authors, click to expand affiliations / ORCID
Buchko G W
Pacific Northwest National Laboratories, Environmental Molecular Sciences Laboratory, Richland, Washington 99352, USA.
Daughdrill G W
de Lorimier R
Rao B K
Isern N G
Lingbeck J M
Taylor J S
Wold M S
Gochin M
Spicer L D
Lowry D F
Kennedy M A
References (58)
58 references, click to expand
  1. Interactions of the transcription/DNA repair factor TFIIH and XP repair proteins with DNA lesions in a cell-free repair assay.
    J Mol Biol. 1998 Aug 14;281(2):211-8 PMID: 9698541
  2. Reconstitution of human DNA repair excision nuclease in a highly defined system.
    J Biol Chem. 1995 Feb 10;270(6):2415-8 PMID: 7852297
  3. Overproduction, purification, and characterization of the XPC subunit of the human DNA repair excision nuclease.
    J Biol Chem. 1996 Aug 9;271(32):19451-6 PMID: 8702634
  4. Reaction mechanism of human DNA repair excision nuclease.
    J Biol Chem. 1996 Apr 5;271(14):8285-94 PMID: 8626523
  5. Resonance assignments, solution structure, and backbone dynamics of the DNA- and RPA-binding domain of human repair factor XPA.
    J Biochem. 1999 Mar;125(3):495-506 PMID: 10050037
  6. Backbone dynamics of a free and phosphopeptide-complexed Src homology 2 domain studied by 15N NMR relaxation.
    Biochemistry. 1994 May 17;33(19):5984-6003 PMID: 7514039
  7. Recognition of DNA adducts by human nucleotide excision repair. Evidence for a thermodynamic probing mechanism.
    J Biol Chem. 1996 Oct 11;271(41):25089-98 PMID: 8810263
  8. Theoretical aspects of DNA-protein interactions: co-operative and non-co-operative binding of large ligands to a one-dimensional homogeneous lattice.
    J Mol Biol. 1974 Jun 25;86(2):469-89 PMID: 4416620
  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. Replication protein A interactions with DNA. 1. Functions of the DNA-binding and zinc-finger domains of the 70-kDa subunit.
    Biochemistry. 1999 Mar 30;38(13):3963-73 PMID: 10194308
  11. RPA involvement in the damage-recognition and incision steps of nucleotide excision repair.
    Nature. 1995 Apr 6;374(6522):566-9 PMID: 7700386
  12. Characterization of gamma-radiation induced decomposition products of thymidine-containing dinucleoside monophosphates by nuclear magnetic resonance spectroscopy.
    J Biomol Struct Dyn. 1993 Feb;10(4):747-62 PMID: 8466677
  13. Self-association and backbone dynamics of the hck SH2 domain in the free and phosphopeptide-complexed forms.
    Biochemistry. 1998 May 19;37(20):7119-26 PMID: 9585523
  14. Specific association between the human DNA repair proteins XPA and ERCC1.
    Proc Natl Acad Sci U S A. 1994 May 24;91(11):5012-6 PMID: 8197174
  15. Backbone 1H and 15N resonance assignments of the N-terminal SH3 domain of drk in folded and unfolded states using enhanced-sensitivity pulsed field gradient NMR techniques.
    J Biomol NMR. 1994 Nov;4(6):845-58 PMID: 7812156
  16. Solution-state structure of the Dewar pyrimidinone photoproduct of thymidylyl-(3'----5')-thymidine.
    Biochemistry. 1988 Sep 20;27(19):7206-15 PMID: 3207670
  17. Analysis of a human DNA excision repair gene involved in group A xeroderma pigmentosum and containing a zinc-finger domain.
    Nature. 1990 Nov 1;348(6296):73-6 PMID: 2234061
  18. Characterization of NADP+ binding to perdeuterated MurB: backbone atom NMR assignments and chemical-shift changes.
    J Mol Biol. 1997 Apr 18;267(5):1223-46 PMID: 9150408
  19. The Japan Society of Human Genetics Award Lecture. Molecular analysis of xeroderma pigmentosum group A gene.
    Jpn J Hum Genet. 1993 Mar;38(1):1-14 PMID: 8504220
  20. The general transcription-repair factor TFIIH is recruited to the excision repair complex by the XPA protein independent of the TFIIE transcription factor.
    J Biol Chem. 1995 Mar 3;270(9):4896-902 PMID: 7876263
  21. Investigation of protein motions via relaxation measurements.
    Methods Enzymol. 1994;239:563-96 PMID: 7830599
  22. The three operators of the lac operon cooperate in repression.
    EMBO J. 1990 Apr;9(4):973-9 PMID: 2182324
  23. Mapping of the binding interfaces of the proteins of the bacterial phosphotransferase system, HPr and IIAglc.
    Biochemistry. 1993 Jan 12;32(1):32-7 PMID: 8418852
  24. An affinity of human replication protein A for ultraviolet-damaged DNA.
    J Biol Chem. 1996 May 17;271(20):11607-10 PMID: 8690733
  25. Backbone dynamics of proteins as studied by 15N inverse detected heteronuclear NMR spectroscopy: application to staphylococcal nuclease.
    Biochemistry. 1989 Nov 14;28(23):8972-9 PMID: 2690953
  26. Gene synthesis machines: DNA chemistry and its uses.
    Science. 1985 Oct 18;230(4723):281-5 PMID: 3863253
  27. Correlation between dynamics and high affinity binding in an SH2 domain interaction.
    Biochemistry. 1996 Jan 16;35(2):361-8 PMID: 8555205
  28. 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
  29. Identification of a damaged-DNA binding domain of the XPA protein.
    Mutat Res. 1996 Jan 2;362(1):87-95 PMID: 8538652
  30. Simultaneous acquisition of [13C,15N]- and [15N,15N]-separated 4D gradient-enhanced NOESY spectra in proteins.
    J Biomol NMR. 1994 Sep;4(5):673-87 PMID: 7919953
  31. Human nucleotide excision repair protein XPA: expression and NMR backbone assignments of the 14.7 kDa minimal damaged DNA binding domain (Met98-Phe219).
    J Biomol NMR. 1997 Oct;10(3):313-4 PMID: 9390412
  32. The XPA protein is a zinc metalloprotein with an ability to recognize various kinds of DNA damage.
    Mutat Res. 1994 Nov;315(3):229-37 PMID: 7526200
  33. DNA repair protein XPA binds replication protein A (RPA).
    J Biol Chem. 1995 Feb 24;270(8):4152-7 PMID: 7876167
  34. 15N NMR relaxation studies of the FK506 binding protein: backbone dynamics of the uncomplexed receptor.
    Biochemistry. 1993 Sep 7;32(35):9000-10 PMID: 7690248
  35. DNA excision-repair defect of xeroderma pigmentosum prevents removal of a class of oxygen free radical-induced base lesions.
    Proc Natl Acad Sci U S A. 1993 Jul 1;90(13):6335-9 PMID: 8327515
  36. Structural features of the minimal DNA binding domain (M98-F219) of human nucleotide excision repair protein XPA.
    Nucleic Acids Res. 1998 Jun 1;26(11):2779-88 PMID: 9592168
  37. The DNA damage-recognition problem in human and other eukaryotic cells: the XPA damage binding protein.
    Biochem J. 1997 Nov 15;328 ( Pt 1):1-12 PMID: 9359827
  38. NMR studies of mobility within protein structure.
    Eur J Biochem. 1989 Aug 15;183(3):479-97 PMID: 2673776
  39. Order of assembly of human DNA repair excision nuclease.
    J Biol Chem. 1999 Jun 25;274(26):18759-68 PMID: 10373492
  40. Chemical shift mapping of the RNA-binding interface of the multiple-RBD protein sex-lethal.
    Biochemistry. 1997 Nov 25;36(47):14306-17 PMID: 9398148
  41. Discovering high-affinity ligands for proteins: SAR by NMR.
    Science. 1996 Nov 29;274(5292):1531-4 PMID: 8929414
  42. Binding of human single-stranded DNA binding protein to DNA damaged by the anticancer drug cis-diamminedichloroplatinum (II).
    Cancer Res. 1992 Nov 15;52(22):6375-9 PMID: 1423284
  43. Chemical shift as a probe of molecular interfaces: NMR studies of DNA binding by the three amino-terminal zinc finger domains from transcription factor IIIA.
    J Biomol NMR. 1998 Jul;12(1):51-71 PMID: 9729788
  44. An interaction between the DNA repair factor XPA and replication protein A appears essential for nucleotide excision repair.
    Mol Cell Biol. 1995 Oct;15(10):5396-402 PMID: 7565690
  45. Structural features of protein-nucleic acid recognition sites.
    Biochemistry. 1999 Feb 16;38(7):1999-2017 PMID: 10026283
  46. Protein structure refinement based on paramagnetic NMR shifts: applications to wild-type and mutant forms of cytochrome c.
    Protein Sci. 1995 Feb;4(2):296-305 PMID: 7757018
  47. Requirement for the replication protein SSB in human DNA excision repair.
    Nature. 1991 Feb 7;349(6309):538-41 PMID: 1992355
  48. 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):3913-21 PMID: 1935910
  49. Backbone dynamics of Escherichia coli ribonuclease HI: correlations with structure and function in an active enzyme.
    J Mol Biol. 1995 Feb 10;246(1):144-63 PMID: 7531772
  50. Contrasting structural impacts induced by cis-syn cyclobutane dimer and (6-4) adduct in DNA duplex decamers: implication in mutagenesis and repair activity.
    Photochem Photobiol. 1995 Jul;62(1):44-50 PMID: 7638271
  51. Human nucleotide excision repair protein XPA: extended X-ray absorption fine-structure evidence for a metal-binding domain.
    Protein Sci. 1998 Sep;7(9):1970-5 PMID: 9761477
  52. Solution structure of the DNA- and RPA-binding domain of the human repair factor XPA.
    Nat Struct Biol. 1998 Aug;5(8):701-6 PMID: 9699634
  53. Analysis of the backbone dynamics of interleukin-1 beta using two-dimensional inverse detected heteronuclear 15N-1H NMR spectroscopy.
    Biochemistry. 1990 Aug 14;29(32):7387-401 PMID: 2223770
  54. Excision repair in mammalian cells.
    J Biol Chem. 1995 Jul 7;270(27):15915-8 PMID: 7608140
  55. Structural analysis of human replication protein A. Mapping functional domains of the 70-kDa subunit.
    J Biol Chem. 1995 Mar 3;270(9):4534-43 PMID: 7876222
  56. Touring protein fold space with Dali/FSSP.
    Nucleic Acids Res. 1998 Jan 1;26(1):316-9 PMID: 9399863
  57. Nucleotide excision repair in mammalian cells.
    J Biol Chem. 1997 Sep 19;272(38):23465-8 PMID: 9295277
  58. Assignment of the non-exchangeable proton resonances of d(C-G-C-G-A-A-T-T-C-G-C-G) using two-dimensional nuclear magnetic resonance methods.
    J Mol Biol. 1983 Dec 15;171(3):319-36 PMID: 6317867
Article Info
Journal
Biochemistry
Abbr.
Biochemistry
ISSN
0006-2960
Published
1999-11-16
Pages
15116-28
Language
English
Region
United States
NLM ID
0370623
PMCID
PMC4251892
Subset
IM
Grants
NIGMS NIH HHS · R01 GM044721 · United States
NIGMS NIH HHS · R29 GM053164-05 · United States
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]