Human PIF1 helicase supports DNA replication and cell growth under oncogenic-stress

Oncotarget

Volumn 5, Issue 22, 2014, Pages 11381-11398

  Gagou, Mary E ^a   Ganesh, Anil ^a   Phear, Geraldine ^a   Robinson, Darren ^b   Petermann, Eva ^c   Cox, Angela ^a   Meuth, Mark ^a  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

^b UNIVERSITY OF SHEFFIELD   (United Kingdom)

^c UNIVERSITY OF BIRMINGHAM   (United Kingdom)

Author keywords

Helicases; Human cells; Oncogenes; Replication stress

Indexed keywords

DNA HELICASE; PIF1 PROTEIN; UNCLASSIFIED DRUG; PIF1 PROTEIN, HUMAN; RAS PROTEIN; SMALL INTERFERING RNA;

ARTICLE; CARCINOGENESIS; CELL GROWTH; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; DNA REPLICATION; DNA SYNTHESIS; ENZYME ACTIVITY; HUMAN; HUMAN CELL; MITOSIS INHIBITION; PROTEIN DEPLETION; S PHASE CELL CYCLE CHECKPOINT; DEFICIENCY; FIBROBLAST; GENETIC TRANSFECTION; GENETICS; GENOMIC INSTABILITY; HCT116 CELL LINE; METABOLISM; ONCOGENE; PHYSIOLOGY; TRANSFORMED CELL LINE;

CELL GROWTH PROCESSES; CELL LINE, TRANSFORMED; DNA HELICASES; DNA REPLICATION; FIBROBLASTS; GENOMIC INSTABILITY; HCT116 CELLS; HUMANS; ONCOGENES; RAS PROTEINS; RNA, SMALL INTERFERING; TRANSFECTION;

EID: 84917708918     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.2501     Document Type: Article

References (65)

1. Brosh RM Jr. DNA helicases involved in DNA repair and their roles in cancer. Nat Rev Cancer. 2013; 13:542-558.
2. Ellis NA, Groden J, Ye T-Z, Straughen J, Lennon DJ, Ciocci S, Proytcheva M, German J. The Bloom's syndrome gene product is homologous to RecQ helicases. Cell. 1995; 83:655-666.
3. Kudlow BA, Kennedy BK, Monnat RJ Jr. Werner and Hutchinson-Gilford progeria syndromes: mechanistic basis of human progeroid diseases. Nat Rev Mol Cell Biol. 2007; 8:394-404.
4. Kitao S, Shimamoto A, Goto M, Miller RW, Smithson WA, Lindor NM, Furuichi Y. Mutations in RECQL4 cause a subset of cases of Rothmund-Thomson syndrome. Nat Genet. 1999; 22:82-84.
5. Litman R, Peng M, Jin Z, Zhang F, Zhang J, Powell S, Andeassen PR, Cantor SB. BACH1 is critical for homologous recombination and appears to be the Fanconi anemia gene product FANCJ. Cancer Cell. 2005; 8:255-265.
6. Schulz VP, Zakian VA. The saccharomyces PIF1 DNA helicase inhibits telomere elongation and de novo telomere formation. Cell. 1994; 76:145-155.
7. Budd ME, Reis CC, Smith S, Myung K, Campbell JL. Evidence suggesting that Pif1 helicase functions in DNA replication with the Dna2helicase/nuclease and DNA polymerase delta. Mol Cell Biol. 2006; 26:2490-2500.
8. Ribeyre C, Lopes J, Boulé J-B, Piazza A, Guédin A, Zakian VA, Mergny JL, Nicolas A. The yeast Pif1 helicase prevents genomic instability caused by G-quadruplex-forming CEB1 sequences in vivo. PLoS Genet. 2009; 5:e1000475.
9. Paeschke K, Bochman ML, Garcia PD, Cejka P, Friedman KL, Kowalczykowski SC, Zakian VA. Pif1 family helicases suppress genome instability at G-quadruplex motifs. Nature. 2013; 497:458-462.
10. Sabouri N, McDonald KR, Webb CJ, Cristea IM, Zakian VA. DNA replication through hard-to-replicate sites, including both highly transcribed RNA Pol II and Pol III genes, requires the S. pombe Pfh1 helicase. Genes Dev. 2012; 26:581-593.
11. Steinacher R, Osman F, Dalgaard JZ, Lorenz A, Whitby MC. The DNA helicase Pfh1 promotes fork merging at replication termination sites to ensure genome stability. Genes Dev. 2012; 26:594-602.
12. Saini N, Ramakrishnan S, Elango R, Ayyar S, Zhang Y, Deem A, Ira G, Haber JE, Lobachev KS, Malkova A. Migrating bubble during break-induced replication drives conservative DNA synthesis. Nature. 2013; 502: 389-392.
13. Wilson MA, Kwon Y, Xu Y, Chung W-H, Chi P, Niu H Mayle R, Chen X, Malkova A, Sung P, Ira G Pif1 helicase and Polδ promote recombination-coupled DNA synthesis via bubble migration. Nature. 2013; 502:393-396.
14. Ivessa AS, Zhou JQ, Zakian VA. The Saccharomyces Pif1p DNA helicase and the highly related Rrm3p have opposite effects on replication fork progression in ribosomal DNA. Cell. 2000; 100:479-489.
15. Boulé J-B, Zakian VA. Roles of Pif1-like helicases in the maintenance of genomic stability. Nucleic Acids Res. 2006; 34:4147-4153.
16. Bochman ML, Sabouri N, Zakian VA. Unwinding the functions of the Pif1 family helicases. DNA Repair (Amst). 2010; 9:237-249.
17. Snow BE, Mateyak M, Paderova J, Wakeham A, Iorio C, Zakian V, Squire J, Harrington L. Murine Pif1 interacts with telomerase and is dispensable for telomere function in vivo. Mol Cell Biol. 2007; 27:1017-1026.
18. Zhou J-Q, Qi H, Schulz VP, Mateyak MK, Monson EK, Zakian VA. Schizosaccharomyces pombe pfh1+ encodes an essential 5" to 3" DNA helicase that is a member of the PIF1 subfamily of DNA helicases. Mol Biol Cell. 2002; 13:2180-2191.
19. Futami K, Shimamoto A, Furuichi Y. Mitochondrial and nuclear localization of human Pif1 helicase. Biol Pharm Bull. 2007; 30:1685-1692.
20. Mateyak MK, Zakian VA. Human PIF helicase is cell cycle regulated and associates with telomerase. Cell Cycle. 2006; 5:2796-2804.
21. Zhang D-H, Zhou B, Huang Y, Xu L-X, Zhou J-Q. The human Pif1 helicase, a potential Escherichia coli RecD homologue, inhibits telomerase activity. Nucleic Acids Res. 2006; 34:1393-1404.
22. Kazak L, Reyes A, Duncan AL, Rorbach J, Wood SR, Brea-Calvo G, Gammage PA, Robinson AJ, Minczuk M, Holt IJ. Alternative translation initiation augments the human mitochondrial proteome. Nucleic Acids Res. 2013; 41:2354-2369.
23. Gu Y, Masuda Y, Kamiya K. Biochemical analysis of human PIF1 helicase and functions of its N-terminal domain. Nucleic Acids Res. 2008; 36:6295-6308.
24. George T, Wen Q, Griffiths R, Ganesh A, Meuth M, Sanders CM. Human Pif1 helicase unwinds synthetic DNA structures resembling stalled DNA replication forks. Nucleic Acids Res. 2009; 37:6491-6502.
25. Sanders CM. Human Pif1 helicase is a G-quadruplex DNA-binding protein with G-quadruplex DNA-unwinding activity. Biochem J. 2010; 430:119-128.
26. Gagou ME, Ganesh A, Thompson R, Phear G, Sanders C, Meuth M. Suppression of apoptosis by PIF1 helicase in human tumor cells. Cancer Res. 2011; 71:4998-5008.
27. Bartkova J, Rezaei N, Liontos M, Karakaidos P, Kletsas D, Issaeva N, Vassiliou LV, Kolettas E, Niforou K, Zoumpourlis VC, Takaoka M, Nakagawa H, Tort F, et al. Oncogene-induced senescence is part of the tumorigenesis barrier imposed by DNA damage checkpoints. Nature. 2006; 444:633-637.
28. Di Micco R, Fumagalli M, Cicalese A, Piccinin S, Gasparini P, Luise C, Schurra C, Garre M, Nuciforo PG, Bensimon A, Maestro R, Pelicci PG, d'Adda di Fagagna F. Oncogene-induced senescence is a DNA damage response triggered by DNA hyper-replication. Nature. 2006; 444:638-642.
29. Pylayeva-Gupta Y, Grabocka E, Bar-Sagi D. RAS oncogenes: weaving a tumorigenic web. Nat Rev Cancer. 2011; 11:761-774.
30. Jackson DA, Pombo A. Replicon clusters are stable units of chromosome structure: evidence that nuclear organization contributes to the efficient activation and propagation of S phase in human cells. J Cell Biol. 1998; 140: 1285-1295.
31. Petermann E, Maya-Mendoza A, Zachos G, Gillespie DA, Jackson DA, Caldecott KW. Chk1 requirement for high global rates of replication fork progression during normal vertebrate S phase. Mol Cell Biol. 2006; 26: 3319-3326.
32. Conti C, Saccà B, Herrick J, Lalou C, Pommier Y, Bensimon A. Replication fork velocities at adjacent replication origins are coordinately modified during DNA replication in human cells. Mol Biol Cell. 2007; 18:3059-3067.
33. Paeschke K, Capra JA, Zakian VA. DNA replication through G-quadruplex motifs is promoted by the Saccharomyces cerevisiae Pif1 DNA helicase. Cell. 2011; 145:678-691.
34. Zhou W-J, Deng R, Zhang X-Y, Feng G-K, Gu L-Q, Zhu X-F. G-quadruplex ligand SYUIQ-5 induces autophagy by telomere damage and TRF2 delocalization in cancer cells. Mol Cancer Ther. 2009; 8:3203-3213.
35. Zhang W-J, Ou T-M, Lu Y-J, Huang Y-Y, Wu W-B, Huang Z-S, Zhou JL, Wong KY, Gu LQ. 9-Substituted berberine derivatives as G-quadruplex stabilizing ligands in telomeric DNA. Bioorg Med Chem. 2007; 15:5493-5501.
36. Ou T-M, Lin J, Lu Y-J, Hou J-Q, Tan J-H, Chen S-H, Li Z, Li YP, Li D, Gu LQ, Huang ZS. Inhibition of cell proliferation by quindoline derivative (SYUIQ-05) through its preferential interaction with c-myc promoter G-quadruplex. J Med Chem. 2011; 54:5671-5679.
37. Ma Y, Ou T-M, Hou J-Q, Lu Y-J, Tan J-H, Gu L-Q, Huang ZS. 9-N-Substituted berberine derivatives: stabilization of G-quadruplex DNA and down-regulation of oncogene c-myc. Bioorg Med Chem. 2008; 16:7582-7591.
38. Newman TJ, Mamun MA, Nieduszynski CA, Blow JJ. Replisome stall events have shaped the distribution of replication origins in the genomes of yeasts. Nucleic Acids Res. 2013; 41:9705-9718.
39. Denko NC, Giaccia AJ, Stringer JR, Stambrook PJ. The human Ha-ras oncogene induces genomic instability in murine fibroblasts within one cell cycle. Proc Natl Acad Sci USA. 1994; 91:5124-5128.
40. Bester AC, Roniger M, Oren YS, Im MM, Sarni D, Chaoat M, Bensimon A, Zamir G, Shewach DS, Kerem B. Nucleotide deficiency promotes genomic instability in early stages of cancer development. Cell. 2011; 145:435-446.
41. Petermann E, Orta ML, Issaeva N, Schultz N, Helleday T. Hydroxyurea-stalled replication forks become progressively inactivated and require two different RAD51-mediated pathways for restart and repair. Mol Cell. 2010; 37:492-502.
42. Hanada K, Budzowska M, Davies SL, van Drunen E, Onizawa H, Beverloo HB, Maas A, Essers J, Hickson ID, Kanaar R. The structure-specific endonuclease Mus81 contributes to replication restart by generating double-strand DNA breaks. Nat Struct Mol Biol. 2007; 14:1096-1104. www.impactjournals.com/oncotarget 11398 Oncotarget
43. Ge XQ, Blow JJ. Chk1 inhibits replication factory activation but allows dormant origin firing in existing factories. J Cell Biol. 2010; 191:1285-1297.
44. Mirkin EV, Mirkin SM. Replication fork stalling at natural impediments. Microbiol Mol Biol Rev. 2007; 71:13-35.
45. Mirkin SM. DNA replication: driving past four-stranded snags. Nature. 2013; 497:449-450.
46. Tarsounas M, Tijsterman M. Genomes and G-quadruplexes: for better or for worse. J Mol Biol. 2013; 425:4782-4789.
47. Rodriguez R, Miller KM, Forment JV, Bradshaw CR, Nikan M, Britton S, Oelschlaegel T, Xhemalce B, Balasubramanian S, Jackson SP. Small-molecule-induced DNA damage identifies alternative DNA structures in human genes. Nat Chem Biol. 2012; 8:301-310.
48. Lopes J, Piazza A, Bermejo R, Kriegsman B, Colosio A, Teulade-Fichou M-P, Foiani M, Nicolas A. G-quadruplexinduced instability during leading-strand replication. EMBO J. 2011; 30:4033-4046.
49. Langston LD, O'Donnell M. DNA replication: keep moving and don't mind the gap. Mol Cell. 2006; 23:155-160.
50. Labib K, Hodgson B. Replication fork barriers: pausing for a break or stalling for time?. EMBO Rep. 2007; 8:346-353.
51. Branzei D, Foiani M. Maintaining genome stability at the replication fork. Nat Rev Mol Cell Biol. 2010; 11:208-219.
52. Davies SL, North PS, Hickson ID. Role for BLM in replication-fork restart and suppression of origin firing after replicative stress. Nat Struct Mol Biol. 2007; 14:677-679.
53. Franchitto A, Pirzio LM, Prosperi E, Sapora O, Bignami M, Pichierri P. Replication fork stalling in WRN-deficient cells is overcome by prompt activation of a MUS81dependent pathway. J Cell Biol. 2008; 183:241-252.
54. Schwab RA, Nieminuszczy J, Shin-ya K, Niedzwiedz W. FANCJ couples replication past natural fork barriers with maintenance of chromatin structure. J Cell Biol. 2013; 201:33-48.
55. Sung P, Klein H. Mechanism of homologous recombination: mediators and helicases take on regulatory functions. Nat Rev Mol Cell Biol. 2006; 7:739-750.
56. Petermann E, Helleday T. Pathways of mammalian replication fork restart. Nat Rev Mol Cell Biol. 2010; 11:683-687.
57. Ge XQ, Jackson DA, Blow JJ. Dormant origins licensed by excess Mcm2-7 are required for human cells to survive replicative stress. Genes Dev. 2007; 21:3331-3341.
58. Jones RM, Mortusewicz O, Afzal I, Lorvellec MGarcía P, Helleday T, Petermann E. Increased replication initiation and conflicts with transcription underlie Cyclin E-induced replication stress. Oncogene. 2013; 32:3744-3753.
59. Besnard E, Babled A, Lapasset L, Milhavet O, Parrinello H, Dantec C, Marin JM, Lemaitre JM. Unraveling cell typespecific and reprogrammable human replication origin signatures associated with G-quadruplex consensus motifs. Nat Struct Mol Biol. 2012; 19:837-844.
60. Hoshina S, Yura K, Teranishi H, Kiyasu N, Tominaga A, Kadoma H, Nakatsuka A, Kunichika T, Obuse C, Waga S. Human Origin Recognition Complex Binds Preferentially to G-Quadruplex-Preferable RNA and Single-Stranded DNA. J Biol Chem. 2013; 288:30161-30171.
61. Daigo Y, Nakamura Y, Tsunoda T. Cdc45l as tumor marker and therapeutic target for cancer. Google Patents. 2011; ~17.
62. Boos D, Frigola J, Diffley JFX. Activation of the replicative DNA helicase: breaking up is hard to do. Curr Opin Cell Biol. 2012; 24:423-430.
63. Rodriguez R, Gagou ME, Meuth M. Apoptosis induced by replication inhibitors in Chk1-depleted cells is dependent upon the helicase cofactor Cdc45. Cell Death & Differentiation. 2008; 15:889-898.
64. Bolderson E, Scorah J, Helleday T, Smythe C, Meuth M. ATM is required for the cellular response to thymidine induced replication fork stress. Hum Mol Genet. 2004; 13:2937-2945.
65. Hautbergue GM, Hung M-L, Walsh MJ, Snijders AP, Chang C-T, Jones R, Ponting CP, Dickman MJ, Wilson SA. UIF, a New mRNA Export Adaptorthat Works Together with REF/ALY, Requires FACT for Recruitment to mRNA. Current Biology. 2009; 19:1918-1924