Comprehensive Mapping of the C-Terminus of Flap Endonuclease-1 Reveals Distinct Interaction Sites for Five Proteins That Represent Different DNA Replication and Repair Pathways

Journal of Molecular Biology

Volumn 377, Issue 3, 2008, Pages 679-690

  Guo, Zhigang ^a   Chavez, Valerie ^a   Singh, Purnima ^a   Finger, L David ^a   Hang, Haiying ^b   Hegde, Muralidhar L ^c   Shen, Binghui ^a  

^a CITY OF HOPE NATIONAL MEDICAL CENTER   (United States)

^b INSTITUTE OF BIOPHYSICS   (China)

^c University of Texas Medical Branch School of Medicine   (United States)

Author keywords

C terminus; FEN 1; protein protein interaction

Indexed keywords

FLAP ENDONUCLEASE; FLAP ENDONUCLEASE 1; UNCLASSIFIED DRUG;

ARTICLE; CARBOXY TERMINAL SEQUENCE; COMPLEX FORMATION; DNA REPAIR; DNA REPLICATION; GENE MAPPING; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION;

MAMMALIA;

EID: 40649100251     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2007.10.074     Document Type: Article

References (44)

1. M.R. Lieber The FEN-1 family of structure-specific nucleases in eukaryotic DNA replication, recombination and repair BioEssays 19 1997 233 240
2. Y. Liu H.I. Kao R.A. Bambara Flap endonuclease 1: a central component of DNA metabolism Annu. Rev. Biochem. 73 2004 589 615
3. B. Shen P. Singh R. Liu J. Qiu L. Zheng L.D. Finger S. Alas Multiple but dissectible functions of FEN-1 nucleases in nucleic acid processing, genome stability and diseases BioEssays 27 2005 717 729
4. J.J. Harrington M.R. Lieber The characterization of a mammalian DNA structure-specific endonuclease EMBO J. 13 1994 1235 1246
5. X. Wu J. Li X. Li C.L. Hsieh P.M. Burgers M.R. Lieber Processing of branched DNA intermediates by a complex of human FEN-1 and PCNA Nucleic Acids Res. 24 1996 2036 2043
6. I.I. Dianova V.A. Bohr G.L. Dianov Interaction of human AP endonuclease 1 with flap endonuclease 1 and proliferating cell nuclear antigen involved in long-patch base excision repair Biochemistry 40 2001 12639 12644
7. T.A. Ranalli S. Tom R.A. Bambara AP endonuclease 1 coordinates flap endonuclease 1 and DNA ligase I activity in long patch base excision repair J. Biol. Chem. 277 2002 41715 41724
8. J.Z. Parrish C. Yang B. Shen D. Xue CRN-1, a Caenorhabditis elegans FEN-1 homologue, cooperates with CPS-6/EndoG to promote apoptotic DNA degradation EMBO J. 22 2003 3451 3460
9. L. Zheng M. Zhou Q. Chai J. Parrish D. Xue S.M. Patrick Novel function of the flap endonuclease 1 complex in processing stalled DNA replication forks EMBO Rep. 6 2005 83 89
10. P. Singh L. Zheng V. Chavez J. Qiu B. Shen Concerted action of exonuclease and Gap-dependent endonuclease activities of FEN-1 contributes to the resolution of triplet repeat sequences (CTG)n- and (GAA)n-derived secondary structures formed during maturation of Okazaki fragments J. Biol. Chem. 282 2007 3465 3477
11. H.Y. Kang E. Choi S.H. Bae K.H. Lee B.S. Gim H.D. Kim Genetic analyses of Schizosaccharomyces pombe dna2(+) reveal that dna2 plays an essential role in Okazaki fragment metabolism Genetics 155 2000 1055 1067
12. R. Prasad G.L. Dianov V.A. Bohr S.H. Wilson FEN1 stimulation of DNA polymerase beta mediates an excision step in mammalian long patch base excision repair J. Biol. Chem. 275 2000 4460 4466
13. R. Gary K. Kim H.L. Cornelius M.S. Park Y. Matsumoto Proliferating cell nuclear antigen facilitates excision in long-patch base excision repair J. Biol. Chem. 274 1999 4354 4363
14. B. Ahn J.A. Harrigan F.E. Indig D.M. Wilson 3rd V.A. Bohr Regulation of WRN helicase activity in human base excision repair J. Biol. Chem. 279 2004 53465 53474
15. W. Wang P. Brandt M.L. Rossi L. Lindsey-Boltz V. Podust E. Fanning The human Rad9–Rad1–Hus1 checkpoint complex stimulates flap endonuclease 1 Proc. Natl Acad. Sci. USA 101 2004 16762 16767
16. E.R. Parrilla-Castellar S.J. Arlander L. Karnitz Dial 9-1-1 for DNA damage: the Rad9–Hus1–Rad1 (9-1-1) clamp complex DNA Repair (Amst) 3 2004 1009 1014
17. M. Kalinowska W. Garncarz M. Pietrowska W.T. Garrard P. Widlak Regulation of the human apoptotic DNase/RNase endonuclease G: involvement of Hsp70 and ATP Apoptosis 10 2005 821 830
18. P. Widlak L.Y. Li X. Wang W.T. Garrard Action of recombinant human apoptotic endonuclease G on naked DNA and chromatin substrates: cooperation with exonuclease and DNase I J. Biol. Chem. 276 2001 48404 48409
19. J. Cote J. Renaud A. Ruiz-Carrillo Recognition of (dG)n.(dC)n sequences by endonuclease G. Characterization of the calf thymus nuclease J. Biol. Chem. 264 1989 3301 3310
20. M. Gerschenson K.L. Houmiel R.L. Low Endonuclease G from mammalian nuclei is identical to the major endonuclease of mitochondria Nucleic Acids Res. 23 1995 88 97
21. S. Ikeda K. Ozaki Action of mitochondrial endonuclease G on DNA damaged by l- ascorbic acid, peplomycin, and cis -diamminedichloroplatinum (II) Biochem. Biophys. Res. Commun. 235 1997 291 294
22. E. Friedrich-Heineken U. Hubscher The Fen1 extrahelical 3′-flap pocket is conserved from archaea to human and regulates DNA substrate specificity Nucleic Acids Res. 32 2004 2520 2528
23. M. Stucki Z.O. Jonsson U. Hubscher In euyotic flap endonuclease 1, the C terminus is essential for substrate binding J. Biol. Chem. 276 2001 7843 7849
24. J. Qiu X. Li G. Frank B. Shen Cell cycle-dependent and DNA damage-inducible nuclear localization of FEN-1 nuclease is consistent with its dual functions in DNA replication and repair J. Biol. Chem. 276 2001 4901 4908
25. R. Gary D.L. Ludwig H.L. Cornelius M.A. MacInnes M.S. Park The DNA repair endonuclease XPG binds to proliferating cell nuclear antigen (PCNA) and shares sequence elements with the PCNA-binding regions of FEN-1 and cyclin-dependent kinase inhibitor p21 J. Biol. Chem. 272 1997 24522 24529
26. E. Warbrick D.P. Lane D.M. Glover L.S. Cox Homologous regions of Fen1 and p21Cip1 compete for binding to the same site on PCNA: a potential mechanism to co-ordinate DNA replication and repair Oncogene 14 1997 2313 2321
27. S. Sharma J.A. Sommers R.K. Gary E. Friedrich-Heineken U. Hubscher R.M. Brosh Jr. The interaction site of Flap Endonuclease-1 with WRN helicase suggests a coordination of WRN and PCNA Nucleic Acids Res. 33 2005 6769 6781
28. S. Sakurai K. Kitano H. Yamaguchi K. Hamada K. Okada K. Fukuda Structural basis for recruitment of human flap endonuclease 1 to PCNA EMBO J. 24 2005 683 693
29. B. Shen J. Qiu D. Hosfield J.A. Tainer Flap endonuclease homologs in archaebacteria exist as independent proteins Trends Biochem. Sci. 23 1998 171 173
30. G. Frank J. Qiu L. Zheng B. Shen Stimulation of eukaryotic flap endonuclease-1 activities by proliferating cell nuclear antigen (PCNA) is independent of its in vitro interaction via a consensus PCNA binding region J. Biol. Chem. 276 2001 36295 36302
31. H.J. Dyson P.E. Wright Intrinsically unstructured proteins and their functions Nat. Rev., Mol. Cell Biol. 6 2005 197 208
32. S.L. Berger Histone modifications in transcriptional regulation Curr. Opin. Genet. Dev. 12 2002 142 148
33. S. Jergic K. Ozawa N.K. Williams X.C. Su D.D. Scott S.M. Hamdan The unstructured C-terminus of the tau subunit of Escherichia coli DNA polymerase III holoenzyme is the site of interaction with the alpha subunit Nucleic Acids Res. 35 2007 2813 2824
34. B.R. Chapados D.J. Hosfield S. Han J. Qiu B. Yelent B. Shen J.A. Tainer Structural basis for FEN-1 substrate specificity and PCNA-mediated activation in DNA replication and repair Cell 116 2004 39 50
35. R.M. Brosh Jr. C. von Kobbe J.A. Sommers P. Karmakar P.L. Opresko J. Piotrowski Werner syndrome protein interacts with human flap endonuclease 1 and stimulates its cleavage activity EMBO J. 20 2001 5791 5801
36. M.A. Burtelow P.M. Roos-Mattjus M. Rauen J.R. Babendure L.M. Karnitz Reconstitution and molecular analysis of the hRad9–hHus1–hRad1 (9-1-1) DNA damage responsive checkpoint complex J. Biol. Chem. 276 2001 25903 25909
37. C. Venclovas M.P. Thelen Structure-based predictions of Rad1, Rad9, Hus1 and Rad17 participation in sliding clamp and clamp-loading complexes Nucleic Acids Res. 28 2000 2481 2493
38. Y. Shiomi A. Shinozaki D. Nakada K. Sugimoto J. Usukura C. Obuse T. Tsurimoto Clamp and clamp loader structures of the human checkpoint protein complexes, Rad9-1-1 and Rad17-RFC Genes Cells 7 2002 861 868
39. L. Wiederhold J.B. Leppard P. Kedar F. Karimi-Busheri A. Rasouli-Nia M. Weinfeld AP endonuclease-independent DNA base excision repair in human cells Mol. Cell 15 2004 209 220
40. X.V. Gomes P.M. Burgers Two modes of FEN1 binding to PCNA regulated by DNA EMBO J. 19 2000 3811 3821
41. L. Zheng H. Dai J. Qiu Q. Huang B. Shen Disruption of the FEN-1/PCNA interaction results in DNA replication defects, pulmonary hypoplasia, pancytopenia, and newborn lethality in mice Mol. Cell. Biol. 27 2007 3176 3186
42. R. Liu J. Qiu L.D. Finger L. Zheng B. Shen The DNA–protein interaction modes of FEN-1 with gap substrates and their implication in preventing duplication mutations Nucleic Acids Res. 34 2006 1772 1784
43. L. Xia L. Zheng H.W. Lee S.E. Bates L. Federico B. Shen T.R. O'Connor Human 3-methyladenine-DNA glycosylase: effect of sequence context on excision, association with PCNA, and stimulation by AP endonuclease J. Mol. Biol. 346 2005 1259 1274
44. R.M. Brosh Jr H.C. Driscoll G.L. Dianov J.A. Sommers Biochemical characterization of the WRN–FEN-1 functional interaction Biochemistry 41 2002 12204 12216