Home LiteratureArticle Details
PMID: 20439749 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Structure and identification of ADP-ribose recognition motifs of APLF and role in the DNA damage response.

Li GY, McCulloch RD, Fenton AL, Cheung M, Meng L, Ikura M, Koch CA

Abstract

Poly(ADP-ribosyl)ation by poly(ADP-ribose) polymerases regulates the interaction of many DNA damage and repair factors with sites of DNA strand lesions. The interaction of these factors with poly(ADP-ribose) (PAR) is mediated by specific domains, including the recently identified PAR-binding zinc finger (PBZ) domain. However, the mechanism governing these interactions is unclear. To better understand the PBZ-PAR interaction, we performed a detailed examination of the representative PBZ-containing protein involved in the DNA damage response, aprataxin polynucleotide-kinase-like factor (APLF), which possesses two tandem PBZ domains. Here we present structural and biochemical studies that identify Y381/Y386 and Y423/Y428 residues in the conserved C(M/P)Y and CYR motifs within each APLF PBZ domain that are critical for the interaction with the adenine ring of ADP-ribose. Basic residues (R387 and R429 in the first and second PBZ domains, respectively) coordinate additional interactions with the phosphate backbone of ADP-ribose, suggesting that APLF binds to multiple ADP-ribose residues along PAR polymers. These C(M/P)Y and CYR motifs form a basic/hydrophobic pocket within a variant zinc finger structure and are required for APLF recruitment to sites of DNA damage in vivo.

MeSH Terms
Adenosine Diphosphate Ribose/metabolism Amino Acid Sequence DNA Damage DNA Repair/genetics DNA-(Apurinic or Apyrimidinic Site) Lyase Magnetic Resonance Spectroscopy Models, Molecular Molecular Sequence Data Nucleotides/metabolism Phosphoproteins/chemistry,genetics,metabolism Poly-ADP-Ribose Binding Proteins Protein Conformation Sequence Alignment Signal Transduction/genetics,physiology
Chemicals
Nucleotides Phosphoproteins Poly-ADP-Ribose Binding Proteins Adenosine Diphosphate Ribose APLF protein, human DNA-(Apurinic or Apyrimidinic Site) Lyase
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Li Guang-Yao
Ontario Cancer Institute, 610 University Avenue, Toronto, ON, Canada M5G 2M9.
McCulloch Richard D
Fenton Amanda L
Cheung Melissa
Meng Li
Ikura Mitsuhiko
Koch C Anne
References (29)
29 references, click to expand
  1. Human Xip1 (C2orf13) is a novel regulator of cellular responses to DNA strand breaks.
    J Biol Chem. 2007 Jul 6;282(27):19638-43 PMID: 17507382
  2. The molecular architecture of the mammalian DNA repair enzyme, polynucleotide kinase.
    Mol Cell. 2005 Mar 4;17(5):657-70 PMID: 15749016
  3. Biochemical properties and function of poly(ADP-ribose) glycohydrolase.
    Biochimie. 1995;77(6):433-8 PMID: 7578425
  4. The macro domain is an ADP-ribose binding module.
    EMBO J. 2005 Jun 1;24(11):1911-20 PMID: 15902274
  5. Xrcc4 physically links DNA end processing by polynucleotide kinase to DNA ligation by DNA ligase IV.
    EMBO J. 2004 Oct 1;23(19):3874-85 PMID: 15385968
  6. The ataxia-oculomotor apraxia 1 gene product has a role distinct from ATM and interacts with the DNA strand break repair proteins XRCC1 and XRCC4.
    DNA Repair (Amst). 2004 Nov 2;3(11):1493-502 PMID: 15380105
  7. RECOORD: a recalculated coordinate database of 500+ proteins from the PDB using restraints from the BioMagResBank.
    Proteins. 2005 Jun 1;59(4):662-72 PMID: 15822098
  8. DNA-induced alpha-helix capping in conserved linker sequences is a determinant of binding affinity in Cys(2)-His(2) zinc fingers.
    J Mol Biol. 2000 Jan 28;295(4):719-27 PMID: 10656784
  9. Recognition of the mRNA AU-rich element by the zinc finger domain of TIS11d.
    Nat Struct Mol Biol. 2004 Mar;11(3):257-64 PMID: 14981510
  10. Poly(ADP-ribose)-binding zinc finger motifs in DNA repair/checkpoint proteins.
    Nature. 2008 Jan 3;451(7174):81-5 PMID: 18172500
  11. APLF (C2orf13) is a novel component of poly(ADP-ribose) signaling in mammalian cells.
    Mol Cell Biol. 2008 Jul;28(14):4620-8 PMID: 18474613
  12. Structures of zinc finger domains from transcription factor Sp1. Insights into sequence-specific protein-DNA recognition.
    J Biol Chem. 1997 Mar 21;272(12):7801-9 PMID: 9065444
  13. Zinc finger proteins: new insights into structural and functional diversity.
    Curr Opin Struct Biol. 2001 Feb;11(1):39-46 PMID: 11179890
  14. Solution structures of the two PBZ domains from human APLF and their interaction with poly(ADP-ribose).
    Nat Struct Mol Biol. 2010 Feb;17(2):241-3 PMID: 20098424
  15. APLF (C2orf13) facilitates nonhomologous end-joining and undergoes ATM-dependent hyperphosphorylation following ionizing radiation.
    DNA Repair (Amst). 2008 Feb 1;7(2):292-302 PMID: 18077224
  16. Poly(ADP-ribosyl)ation reactions in the regulation of nuclear functions.
    Biochem J. 1999 Sep 1;342 ( Pt 2):249-68 PMID: 10455009
  17. Multiple RNA binding domains (RBDs) just don't add up.
    Nucleic Acids Res. 1995 Mar 11;23(5):725-8 PMID: 7535921
  18. Crystallography & NMR system: A new software suite for macromolecular structure determination.
    Acta Crystallogr D Biol Crystallogr. 1998 Sep 1;54(Pt 5):905-21 PMID: 9757107
  19. A novel human AP endonuclease with conserved zinc-finger-like motifs involved in DNA strand break responses.
    EMBO J. 2007 Apr 18;26(8):2094-103 PMID: 17396150
  20. Torsion angle dynamics for NMR structure calculation with the new program DYANA.
    J Mol Biol. 1997 Oct 17;273(1):283-98 PMID: 9367762
  21. Structural classification of zinc fingers: survey and summary.
    Nucleic Acids Res. 2003 Jan 15;31(2):532-50 PMID: 12527760
  22. APLF (C2orf13) is a novel human protein involved in the cellular response to chromosomal DNA strand breaks.
    Mol Cell Biol. 2007 May;27(10):3793-803 PMID: 17353262
  23. A new XRCC1-containing complex and its role in cellular survival of methyl methanesulfonate treatment.
    Mol Cell Biol. 2004 Oct;24(19):8356-65 PMID: 15367657
  24. A macrodomain-containing histone rearranges chromatin upon sensing PARP1 activation.
    Nat Struct Mol Biol. 2009 Sep;16(9):923-9 PMID: 19680243
  25. Proteome-wide identification of poly(ADP-ribose) binding proteins and poly(ADP-ribose)-associated protein complexes.
    Nucleic Acids Res. 2008 Dec;36(22):6959-76 PMID: 18981049
  26. The acute myeloid leukemia fusion protein AML1-ETO targets E proteins via a paired amphipathic helix-like TBP-associated factor homology domain.
    Proc Natl Acad Sci U S A. 2006 Jul 5;103(27):10242-10247 PMID: 16803958
  27. Poly(ADP-ribosyl)ated chromatin domains: access granted.
    J Cell Sci. 2004 Feb 29;117(Pt 6):815-25 PMID: 14963022
  28. The protein kinase CK2 facilitates repair of chromosomal DNA single-strand breaks.
    Cell. 2004 Apr 2;117(1):17-28 PMID: 15066279
  29. HADDOCK: a protein-protein docking approach based on biochemical or biophysical information.
    J Am Chem Soc. 2003 Feb 19;125(7):1731-7 PMID: 12580598
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
1091-6490
Published
2010-05-18
Epub
2010-00-03
Pages
9129-34
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC2889080
Subset
IM
Grants
Canadian Institutes of Health Research · Canada
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]