Wuho Is a New Member in Maintaining Genome Stability through its Interaction with Flap Endonuclease 1

PLoS Biology

Volumn 14, Issue 1, 2016, Pages

  Cheng, I Cheng ^a   Chen, Betty Chamay ^a   Shuai, Hung Hsun ^a   Chien, Fan Ching ^b   Chen, Peilin ^c   Hsieh, Tao Shih ^a,d  

^a INSTITUTE OF CELLULAR AND ORGANISMIC BIOLOGY   (Taiwan)

^b NATIONAL CENTRAL UNIVERSITY   (Taiwan)

^c RESEARCH CENTER FOR APPLIED SCIENCES   (Taiwan)

^d DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ATM PROTEIN; CHECKPOINT KINASE 2; CYCLINE; ENDONUCLEASE; FLAP ENDONUCLEASE; FLAP ENDONUCLEASE 1; PEPTIDES AND PROTEINS; PROTEIN P53; PROTEIN WUHO; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; CARRIER PROTEIN; DROSOPHILA PROTEIN; FEN1 PROTEIN, HUMAN; FEN1 PROTEIN, MOUSE; GUANINE NUCLEOTIDE BINDING PROTEIN; WDR4 PROTEIN, HUMAN; WDR4 PROTEIN, MOUSE; WUHO PROTEIN, DROSOPHILA;

ANIMAL CELL; APOPTOSIS; ARTICLE; CONTROLLED STUDY; DNA CLEAVAGE; DNA REPLICATION; DNA STRAND BREAKAGE; DNA SYNTHESIS; DROSOPHILA; EMBRYO; EMBRYO DEATH; ENZYME ACTIVITY; FLUORESCENCE MICROSCOPY; GENE SILENCING; GENOMIC INSTABILITY; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; ANIMAL; DROSOPHILA MELANOGASTER; HCT 116 CELL LINE; KNOCKOUT MOUSE; METABOLISM;

ANIMALS; APOPTOSIS; CARRIER PROTEINS; DNA REPLICATION; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; FLAP ENDONUCLEASES; GENOMIC INSTABILITY; GTP-BINDING PROTEINS; HCT116 CELLS; HUMANS; MICE; MICE, KNOCKOUT; PROLIFERATING CELL NUCLEAR ANTIGEN; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84961345198     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.1002349     Document Type: Article

References (58)

1. Kornberg A, Baker TA, DNA Replication. New York: Freeman; 1992.
2. O'Donnell M, Langston L, Stillman B, Principles and concepts of DNA replication in bacteria, archaea, and eukarya. Cold Spring Harbor perspectives in biology. 2013;5(7). Epub 2013/07/03. doi: 5/7/a010108 [pii] doi: 10.1101/cshperspect.a010108 23818497; PubMed Central PMCID: PMC3685895.
3. Liu Y, Kao HI, Bambara RA, Flap endonuclease 1: a central component of DNA metabolism. Annual review of biochemistry. 2004;73:589–615. doi: 10.1146/annurev.biochem.73.012803.092453 15189154.
4. Shen B, Singh P, Liu R, Qiu J, Zheng L, Finger LD, et al. Multiple but dissectible functions of FEN-1 nucleases in nucleic acid processing, genome stability and diseases. BioEssays: news and reviews in molecular, cellular and developmental biology. 2005;27(7):717–29. doi: 10.1002/bies.20255 15954100.
5. Balakrishnan L, Bambara RA, Flap Endonuclease 1. Annual review of biochemistry. 2013;82:119–38. doi: 10.1146/annurev-biochem-072511-122603 23451868.
6. Brutlag D, Atkinson MR, Setlow P, Kornberg A, An active fragment of DNA polymerase produced by proteolytic cleavage. Biochem Biophys Res Commun. 1969;37(6):982–9. Epub 1969/12/04. doi: 0006-291X(69)90228-9 [pii]. 4982877.
7. Klett RP, Cerami A, Reich E, Exonuclease VI, a new nuclease activity associated with E. coli DNA polymerase. Proc Natl Acad Sci U S A. 1968;60(3):943–50. 4875807; PubMed Central PMCID: PMC225144.
8. Harrington JJ, Lieber MR, The characterization of a mammalian DNA structure-specific endonuclease. EMBO J. 1994;13(5):1235–46. 8131753; PubMed Central PMCID: PMC394933.
9. Lieber MR, The FEN-1 family of structure-specific nucleases in eukaryotic DNA replication, recombination and repair. BioEssays: news and reviews in molecular, cellular and developmental biology. 1997;19(3):233–40. doi: 10.1002/bies.950190309 9080773.
10. Klungland A, Lindahl T, Second pathway for completion of human DNA base excision-repair: reconstitution with purified proteins and requirement for DNase IV (FEN1). EMBO J. 1997;16(11):3341–8. doi: 10.1093/emboj/16.11.3341 9214649; PubMed Central PMCID: PMC1169950.
11. Zheng L, Zhou M, Chai Q, Parrish J, Xue D, Patrick SM, et al. Novel function of the flap endonuclease 1 complex in processing stalled DNA replication forks. EMBO reports. 2005;6(1):83–9. doi: 10.1038/sj.embor.7400313 15592449; PubMed Central PMCID: PMC1299223.
12. Larsen E, Gran C, Saether BE, Seeberg E, Klungland A, Proliferation failure and gamma radiation sensitivity of Fen1 null mutant mice at the blastocyst stage. Mol Cell Biol. 2003;23(15):5346–53. 12861020; PubMed Central PMCID: PMC165721.
13. Kucherlapati M, Yang K, Kuraguchi M, Zhao J, Lia M, Heyer J, et al. Haploinsufficiency of Flap endonuclease (Fen1) leads to rapid tumor progression. Proc Natl Acad Sci U S A. 2002;99(15):9924–9. doi: 10.1073/pnas.152321699 12119409; PubMed Central PMCID: PMC126601.
14. Brosh RM, Jr.von Kobbe C, Sommers JA, Karmakar P, Opresko PL, Piotrowski J, et al. Werner syndrome protein interacts with human flap endonuclease 1 and stimulates its cleavage activity. EMBO J. 2001;20(20):5791–801. doi: 10.1093/emboj/20.20.5791 11598021; PubMed Central PMCID: PMC125684.
15. Imamura O, Campbell JL, The human Bloom syndrome gene suppresses the DNA replication and repair defects of yeast dna2 mutants. Proc Natl Acad Sci U S A. 2003;100(14):8193–8. Epub 2003/06/27. doi: 10.1073/pnas.1431624100 1431624100 [pii]. 12826610; PubMed Central PMCID: PMC166205.
16. Tom S, Henricksen LA, Bambara RA, Mechanism whereby proliferating cell nuclear antigen stimulates flap endonuclease 1. J Biol Chem. 2000;275(14):10498–505. Epub 2000/04/01. 10744741.
17. Wang W, Brandt P, Rossi ML, Lindsey-Boltz L, Podust V, Fanning E, et al. The human Rad9-Rad1-Hus1 checkpoint complex stimulates flap endonuclease 1. Proc Natl Acad Sci U S A. 2004;101(48):16762–7. doi: 10.1073/pnas.0407686101 15556996; PubMed Central PMCID: PMC534749.
18. Hasan S, Stucki M, Hassa PO, Imhof R, Gehrig P, Hunziker P, et al. Regulation of human flap endonuclease-1 activity by acetylation through the transcriptional coactivator p300. Mol Cell. 2001;7(6):1221–31. Epub 2001/06/30. doi: S1097-2765(01)00272-6 [pii]. 11430825.
19. Henneke G, Koundrioukoff S, Hubscher U, Phosphorylation of human Fen1 by cyclin-dependent kinase modulates its role in replication fork regulation. Oncogene. 2003;22(28):4301–13. Epub 2003/07/11. doi: 10.1038/sj.onc.1206606 1206606 [pii]. 12853968.
20. Guo Z, Kanjanapangka J, Liu N, Liu S, Liu C, Wu Z, et al. Sequential posttranslational modifications program FEN1 degradation during cell-cycle progression. Mol Cell. 2012;47(3):444–56. Epub 2012/07/04. doi: S1097-2765(12)00487-X [pii] doi: 10.1016/j.molcel.2012.05.042 22749529; PubMed Central PMCID: PMC3518404.
21. Wu J, Hou JH, Hsieh TS, . A new Drosophila gene wh (wuho) with WD40 repeats is essential for spermatogenesis and has maximal expression in hub cells. Dev Biol. 2006;296(1):219–30. Epub 2006/06/10. doi: S0012-1606(06)00756-1 [pii] doi: 10.1016/j.ydbio.2006.04.459 16762337; PubMed Central PMCID: PMC2055424.
22. Leulliot N, Chaillet M, Durand D, Ulryck N, Blondeau K, van Tilbeurgh H, Structure of the yeast tRNA m7G methylation complex. Structure. 2008;16(1):52–61. doi: 10.1016/j.str.2007.10.025 18184583.
23. Stirnimann CU, Petsalaki E, Russell RB, Muller CW, WD40 proteins propel cellular networks. Trends Biochem Sci. 2010;35(10):565–74. Epub 2010/05/11. doi: S0968-0004(10)00072-1 [pii] doi: 10.1016/j.tibs.2010.04.003 20451393.
24. Alexandrov A, Martzen MR, Phizicky EM, Two proteins that form a complex are required for 7-methylguanosine modification of yeast tRNA. RNA. 2002;8(10):1253–66. Epub 2002/10/31. 12403464; PubMed Central PMCID: PMC1370335.
25. Abraham RT, Cell cycle checkpoint signaling through the ATM and ATR kinases. Genes Dev. 2001;15(17):2177–96. doi: 10.1101/gad.914401 11544175.
26. Lavin MF, ATM and the Mre11 complex combine to recognize and signal DNA double-strand breaks. Oncogene. 2007;26(56):7749–58. doi: 10.1038/sj.onc.1210880 18066087.
27. Zilfou JT, Lowe SW, Tumor suppressive functions of p53. Cold Spring Harbor perspectives in biology. 2009;1(5):a001883. doi: 10.1101/cshperspect.a001883 20066118; PubMed Central PMCID: PMC2773645.
28. Unger T, Sionov RV, Moallem E, Yee CL, Howley PM, Oren M, et al. Mutations in serines 15 and 20 of human p53 impair its apoptotic activity. Oncogene. 1999;18(21):3205–12. Epub 1999/06/08. doi: 10.1038/sj.onc.1202656 10359526.
29. She QB, Bode AM, Ma WY, Chen NY, Dong Z, Resveratrol-induced activation of p53 and apoptosis is mediated by extracellular-signal-regulated protein kinases and p38 kinase. Cancer Res. 2001;61(4):1604–10. 11245472.
30. Chipuk JE, Kuwana T, Bouchier-Hayes L, Droin NM, Newmeyer DD, Schuler M, et al. Direct activation of Bax by p53 mediates mitochondrial membrane permeabilization and apoptosis. Science. 2004;303(5660):1010–4. doi: 10.1126/science.1092734 14963330.
31. Miyashita T, Reed JC, Tumor suppressor p53 is a direct transcriptional activator of the human bax gene. Cell. 1995;80(2):293–9. 7834749.
32. Oda E, Ohki R, Murasawa H, Nemoto J, Shibue T, Yamashita T, et al. Noxa, a BH3-only member of the Bcl-2 family and candidate mediator of p53-induced apoptosis. Science. 2000;288(5468):1053–8. 10807576.
33. Hengartner MO, The biochemistry of apoptosis. Nature. 2000;407(6805):770–6. doi: 10.1038/35037710 11048727.
34. Salvesen GS, Ashkenazi A, Snapshot: caspases. Cell. 2011;147(2):476–e1. doi: 10.1016/j.cell.2011.09.030 22000022.
35. Levine AJ, p53, the cellular gatekeeper for growth and division. Cell. 1997;88(3):323–31. 9039259.
36. Bunz F, Dutriaux A, Lengauer C, Waldman T, Zhou S, Brown JP, et al. Requirement for p53 and p21 to sustain G2 arrest after DNA damage. Science. 1998;282(5393):1497–501. 9822382.
37. Cartlidge RA, Knebel A, Peggie M, Alexandrov A, Phizicky EM, Cohen P, The tRNA methylase METTL1 is phosphorylated and inactivated by PKB and RSK in vitro and in cells. EMBO J. 2005;24(9):1696–705. doi: 10.1038/sj.emboj.7600648 15861136; PubMed Central PMCID: PMC1142581.
38. Alexandrov A, Grayhack EJ, Phizicky EM, tRNA m7G methyltransferase Trm8p/Trm82p: evidence linking activity to a growth phenotype and implicating Trm82p in maintaining levels of active Trm8p. RNA. 2005;11(5):821–30. Epub 2005/04/07. doi: rna.2030705 [pii] doi: 10.1261/rna.2030705 15811913; PubMed Central PMCID: PMC1370766.
39. Li X, Li J, Harrington J, Lieber MR, Burgers PM, Lagging strand DNA synthesis at the eukaryotic replication fork involves binding and stimulation of FEN-1 by proliferating cell nuclear antigen. J Biol Chem. 1995;270(38):22109–12. 7673186.
40. Warbrick E, PCNA binding through a conserved motif. BioEssays: news and reviews in molecular, cellular and developmental biology. 1998;20(3):195–9. doi: 10.1002/(SICI)1521-1878(199803)20:3<195::AID-BIES2>3.0.CO;2-R 9631646.
41. Moldovan GL, Pfander B, Jentsch S, PCNA, the maestro of the replication fork. Cell. 2007;129(4):665–79. doi: 10.1016/j.cell.2007.05.003 17512402.
42. Zheng L, Dai H, Qiu J, Huang Q, Shen B, Disruption of the FEN-1/PCNA interaction results in DNA replication defects, pulmonary hypoplasia, pancytopenia, and newborn lethality in mice. Mol Cell Biol. 2007;27(8):3176–86. doi: 10.1128/MCB.01652-06 17283043; PubMed Central PMCID: PMC1899923.
43. van de Linde S, Loschberger A, Klein T, Heidbreder M, Wolter S, Heilemann M, et al. Direct stochastic optical reconstruction microscopy with standard fluorescent probes. Nat Protoc. 2011;6(7):991–1009. Epub 2011/07/02. doi: 10.1038/nprot.2011.336 21720313.
44. Dungrawala H, Rose KL, Bhat KP, Mohni KN, Glick GG, Couch FB, et al. The Replication Checkpoint Prevents Two Types of Fork Collapse without Regulating Replisome Stability. Mol Cell. 2015;59(6):998–1010. doi: 10.1016/j.molcel.2015.07.030 26365379; PubMed Central PMCID: PMC4575883.
45. Harrington JJ, Lieber MR, DNA structural elements required for FEN-1 binding. J Biol Chem. 1995;270(9):4503–8. 7876218.
46. Kao HI, Henricksen LA, Liu Y, Bambara RA, Cleavage specificity of Saccharomyces cerevisiae flap endonuclease 1 suggests a double-flap structure as the cellular substrate. J Biol Chem. 2002;277(17):14379–89. doi: 10.1074/jbc.M110662200 11825897.
47. Michaud J, Kudoh J, Berry A, Bonne-Tamir B, Lalioti MD, Rossier C, et al. Isolation and characterization of a human chromosome 21q22.3 gene (WDR4) and its mouse homologue that code for a WD-repeat protein. Genomics. 2000;68(1):71–9. Epub 2000/08/22. doi: 10.1006/geno.2000.6258 S0888-7543(00)96258-X [pii]. 10950928.
48. Chen CK, Chan NL, Wang AH, The many blades of the beta-propeller proteins: conserved but versatile. Trends Biochem Sci. 2011;36(10):553–61. Epub 2011/09/20. doi: S0968-0004(11)00115-0 [pii] doi: 10.1016/j.tibs.2011.07.004 21924917.
49. Smith TF, Gaitatzes C, Saxena K, Neer EJ, The WD repeat: a common architecture for diverse functions. Trends Biochem Sci. 1999;24(5):181–5. Epub 1999/05/14. doi: S0968-0004(99)01384-5 [pii]. 10322433.
50. Wu X, Li J, Li X, Hsieh CL, Burgers PM, Lieber MR, Processing of branched DNA intermediates by a complex of human FEN-1 and PCNA. Nucleic Acids Res. 1996;24(11):2036–43. 8668533; PubMed Central PMCID: PMC145902.
51. Sharma S, Sommers JA, Wu L, Bohr VA, Hickson ID, Brosh RM, JrStimulation of flap endonuclease-1 by the Bloom's syndrome protein. J Biol Chem. 2004;279(11):9847–56. doi: 10.1074/jbc.M309898200 14688284.
52. Cheng IC, Lee HJ, Wang TC, Multiple factors conferring high radioresistance in insect Sf9 cells. Mutagenesis. 2009;24(3):259–69. doi: 10.1093/mutage/gep005 19264841.
53. Lakso M, Pichel JG, Gorman JR, Sauer B, Okamoto Y, Lee E, et al. Efficient in vivo manipulation of mouse genomic sequences at the zygote stage. Proc Natl Acad Sci U S A. 1996;93(12):5860–5. Epub 1996/06/11. 8650183; PubMed Central PMCID: PMC39152.
54. Shen B, Nolan JP, Sklar LA, Park MS, Essential amino acids for substrate binding and catalysis of human flap endonuclease 1. J Biol Chem. 1996;271(16):9173–6. 8621570.
55. Adams SR, Campbell RE, Gross LA, Martin BR, Walkup GK, Yao Y, et al. New biarsenical ligands and tetracysteine motifs for protein labeling in vitro and in vivo: synthesis and biological applications. J Am Chem Soc. 2002;124(21):6063–76. Epub 2002/05/23. doi: ja017687n [pii]. 12022841.
56. Heyduk T, Lee JC, Application of fluorescence energy transfer and polarization to monitor Escherichia coli cAMP receptor protein and lac promoter interaction. Proc Natl Acad Sci U S A. 1990;87(5):1744–8. Epub 1990/03/01. 2155424; PubMed Central PMCID: PMC53559.
57. Best MD, Click chemistry and bioorthogonal reactions: unprecedented selectivity in the labeling of biological molecules. Biochemistry. 2009;48(28):6571–84. doi: 10.1021/bi9007726 19485420.
58. Nolan JP, Shen B, Park MS, Sklar LA, Kinetic analysis of human flap endonuclease-1 by flow cytometry. Biochemistry. 1996;35(36):11668–76. doi: 10.1021/bi952840+ 8794747.