A replicator-specific binding protein essential for site-specific initiation of DNA replication in mammalian cells

Nature Communications

Volumn 7, Issue , 2016, Pages

  Zhang, Ya ^a   Huang, Liang ^a   Fu, Haiqing ^a   Smith, Owen K ^a   Lin, Chii Mei ^a   Utani, Koichi ^a   Rao, Mishal ^a   Reinhold, William C ^a   Redon, Christophe E ^a   Ryan, Michael ^b   Kim, Ryangguk ^b   You, Yang ^a   Hanna, Harlington ^a   Boisclair, Yves ^c   Long, Qiaoming ^c   Aladjem, Mirit I ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b In Silico Solutions   (United States)

^c Department of Obstetrics Gynecology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; DNA BINDING PROTEIN; HEMOGLOBIN BETA CHAIN; REPLICATION INITIATION DETERMINANT PROTEIN; UNCLASSIFIED DRUG; PROTEIN BINDING;

CHEMICAL BINDING; CHROMOSOME; DNA; EMBRYO; HOMINID; MAMMAL; POLYMER; PROTEIN; RODENT;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DNA REPLICATION; DNA REPLICATION ORIGIN; EMBRYO; FIBROBLAST; GENE LOCUS; MAMMAL CELL; MOUSE; NONHUMAN; NUCLEOTIDE BINDING SITE; PROTEIN DNA BINDING; PROTEIN MOTIF; REGULATOR GENE; ANIMAL; BIOLOGICAL MODEL; CELL LINE; CYTOLOGY; GENOME; HUMAN; MAMMAL; MAMMALIAN EMBRYO; METABOLISM; NUCLEOTIDE SEQUENCE;

MAMMALIA; MURINAE;

ANIMALS; BASE SEQUENCE; CELL LINE; DNA REPLICATION; DNA-BINDING PROTEINS; EMBRYO, MAMMALIAN; FIBROBLASTS; GENETIC LOCI; GENOME; HUMANS; LOCUS CONTROL REGION; MAMMALS; MICE; MODELS, BIOLOGICAL; PROTEIN BINDING; REPLICATION ORIGIN;

EID: 84976345852     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms11748     Document Type: Article

References (65)

1. Mechali, M. Eukaryotic DNA replication origins: many choices for appropriate answers. Nat. Rev. Mol. Cell Biol. 11, 728-738 (2010).
2. Bielinsky, A. K. Replication origins: why do we need so many? Cell Cycle 2, 307-309 (2003).
3. Aladjem, M. I. Replication in context: dynamic regulation of DNA replication patterns in metazoans. Nat. Rev. Genet. 8, 588-600 (2007).
4. Martin, M. M. et al. Genome-wide depletion of replication initiation events in highly transcribed regions. Genome Res. 21, 1822-1832 (2011).
5. Gilbert, D. M. et al. Space and time in the nucleus: developmental control of replication timing and chromosome architecture. Cold Spring Harb. Symp. Quant. Biol. 75, 143-153 (2010).
6. Lunyak, V. V., Ezrokhi, M., Smith, H. S. & Gerbi, S. A. Developmental changes in the Sciara II/9A initiation zone for DNA replication. Mol. Cell Biol. 22, 8426-8437 (2002).
7. Cayrou, C. et al. Genome-scale analysis of metazoan replication origins reveals their organization in specific but flexible sites defined by conserved features. Genome Res. 21, 1438-1449 (2011).
8. DePamphilis, M. L. et al. Regulating the licensing of DNA replication origins in metazoa. Curr. Opin. Cell. Biol. 18, 231-239 (2006).
9. Blow, J. J. & Dutta, A. Preventing re-replication of chromosomal DNA. Nat. Rev. Mol. Cell Biol. 6, 476-486 (2005).
10. Masai, H., Matsumoto, S., You, Z., Yoshizawa-Sugata, N. & Oda, M. Eukaryotic chromosome DNA replication: where, when, and how? Annu. Rev. Biochem. 79, 89-130 (2010).
11. Mendez, J. & Stillman, B. Perpetuating the double helix: molecular machines at eukaryotic DNA replication origins. Bioessays 25, 1158-1167 (2003).
12. Vashee, S. et al. Sequence-independent DNA binding and replication initiation by the human origin recognition complex. Genes Dev. 17, 1894-1908 (2003).
13. Remus, D., Beall, E. L. & Botchan, M. R. DNA topology, not DNA sequence, is a critical determinant for Drosophila ORC-DNA binding. EMBO J. 23, 897-907 (2004).
14. Eaton, M. L., Galani, K., Kang, S., Bell, S. P. & MacAlpine, D. M. Conserved nucleosome positioning defines replication origins. Genes Dev. 24, 748-753 (2010).
15. Lubelsky, Y. et al. Pre-replication complex proteins assemble at regions of low nucleosome occupancy within the Chinese hamster dihydrofolate reductase initiation zone. Nucleic Acids Res. 39, 3141-3155 (2011).
16. Dellino, G. I. et al. Genome-wide mapping of human DNA-replication origins: Levels of transcription at ORC1 sites regulate origin selection and replication timing. Genome Res. 23, 1-11 (2013).
17. Jacob, F. & Brenner, S. On the regulation of DNA synthesis in bacteria: The hypothesis of the replicon. C. R. Hebd Seances Acad. Sci. 256, 298-300 (1963).
18. Besnard, E. et al. Unraveling cell type-specific and reprogrammable human replication origin signatures associated with G-quadruplex consensus motifs. Nat. Struct. Mol. Biol. 19, 837-844 (2012).
19. Schepers, A. & Papior, P. Why are we where we are? Understanding replication origins and initiation sites in eukaryotes using ChIP-Approaches. Chromosome Res. 18, 63-77 (2010).
20. Chowdhury, A. et al. The DNA unwinding element binding protein DUE-B interacts with Cdc45 in preinitiation complex formation. Mol. Cell Biol. 30, 1495-1507 (2010).
21. Thangavel, S. et al. Human RECQ1 and RECQ4 helicases play distinct roles in DNA replication initiation. Mol. Cell Biol. 30, 1382-1396 (2010).
22. Giri, S. et al. The preRC protein ORCA organizes heterochromatin by assembling histone H3 lysine 9 methyltransferases on chromatin. eLife 4, e06496 (2015).
23. Miotto, B. & Struhl, K. JNK1 phosphorylation of Cdt1 inhibits recruitment of HBO1 histone acetylase and blocks replication licensing in response to stress. Mol. Cell 44, 62-71 (2011).
24. Farhang-Fallah, J., Yin, X., Trentin, G., Cheng, A. M. & Rozakis-Adcock, M. Cloning and characterization of PHIP, a novel insulin receptor substrate-1 pleckstrin homology domain interacting protein. J. Biol. Chem. 275, 40492-40497 (2000).
25. Podcheko, A. et al. Identification of a WD40 repeat-containing isoform of PHIP as a novel regulator of beta-cell growth and survival. Mol. Cell Biol. 27, 6484-6496 (2007).
26. Li, S. et al. The full-length isoform of the mouse pleckstrin homology domain-interacting protein (PHIP) is required for postnatal growth. FEBS Lett. 584, 4121-4127 (2010).
27. De Semir, D. et al. Pleckstrin homology domain-interacting protein (PHIP) as a marker and mediator of melanoma metastasis. Proc. Natl Acad. Sci. USA 109, 7067-7072 (2012).
28. Jin, J., Arias, E. E., Chen, J., Harper, J. W. & Walter, J. C. A family of diverse Cul4-Ddb1-interacting proteins includes Cdt2, which is required for S phase destruction of the replication factor Cdt1. Mol. Cell 23, 709-721 (2006).
29. Raman, M., Havens, C. G., Walter, J. C. & Harper, J. W. A genome-wide screen identifies p97 as an essential regulator of DNA damage-dependent CDT1 destruction. Mol. Cell 44, 72-84 (2011).
30. Franz, A. et al. CDC-48/p97 coordinates CDT-1 degradation with GINS chromatin dissociation to ensure faithful DNA replication. Mol. Cell 44, 85-96 (2011).
31. Aladjem, M. I., Rodewald, L. W., Kolman, J. L. & Wahl, G. M. Genetic dissection of a mammalian replicator in the human beta-globin locus. Science 281, 1005-1009 (1998).
32. Henning, K. A. et al. Human artificial chromosomes generated by modification of a yeast artificial chromosome containing both human alpha satellite and single-copy DNA sequences. Proc. Natl Acad. Sci. USA 96, 592-597 (1999).
33. Kitsberg, D., Selig, S., Keshet, I. & Cedar, H. Replication structure of the human beta-globin gene domain. Nature 366, 588-590 (1993).
34. Wang, L. et al. The human beta-globin replication initiation region consists of two modular independent replicators. Mol. Cell Biol. 24, 3373-3386 (2004).
35. Fu, H. et al. Preventing gene silencing with human replicators. Nat. Biotechnol. 24, 572-576 (2006).
36. Dhar, V., Mager, D., Iqbal, A. & Schildkraut, C. L. The coordinate replication of the human beta-globin gene domain reflects its transcriptional activity and nuclease hypersensitivity. Mol. Cell Biol. 8, 4958-4965 (1988).
37. Driscoll, M. C., Dobkin, C. S. & Alter, B. P. Gamma delta beta-Thalassemia due to a de novo mutation deleting the 5' beta-globin gene activation-region hypersensitive sites. Proc. Natl Acad. Sci. USA 86, 7470-7474 (1989).
38. Forrester, W. C. et al. A deletion of the human beta-globin locus activation region causes a major alteration in chromatin structure and replication across the entire beta-globin locus. Genes Dev. 4, 1637-1649 (1990).
39. Epner, E., Forrester, W. C. & Groudine, M. Asynchronous DNA replication within the human beta-globin gene locus. Proc. Natl Acad. Sci. USA 85, 8081-8085 (1988).
40. Simon, I. et al. Developmental regulation of DNA replication timing at the human beta globin locus. EMBO J. 20, 6150-6157 (2001).
41. Kamath, S. & Leffak, M. Multiple sites of replication initiation in the human beta-globin gene locus. Nucleic Acids Res. 29, 809-817 (2001).
42. Djeliova, V., Russev, G. & Anachkova, B. DNase I sensitive site in the core region of the human beta-globin origin of replication. J. Cell Biochem. 87, 279-283 (2002).
43. Francino, M. P. & Ochman, H. Strand symmetry around the beta-globin origin of replication in primates. Mol. Biol. Evol. 17, 416-422 (2000).
44. Karmakar, S., Mahajan, M. C., Schulz, V., Boyapaty, G. & Weissman, S. M. A multiprotein complex necessary for both transcription and DNA replication at the beta-globin locus. EMBO J. 29, 3260-3271 (2010).
45. Schneider, U., Schwenk, H. U. & Bornkamm, G. Characterization of EBV-genome negative 'null' and 'T' cell lines derived from children with acute lymphoblastic leukemia and leukemic transformed non-Hodgkin lymphoma. Int. J. Cancer 19, 621-626 (1977).
46. Huang, L. et al. Prevention of transcriptional silencing by a replicator-binding complex consisting of SWI/SNF, MeCP1, and hnRNP C1/C2. Mol. Cell Biol. 31, 3472-3484 (2011).
47. Shankavaram, U. T. et al. CellMiner: A relational database and query tool for the NCI-60 cancer cell lines. BMC Genomics 10, 277 (2009).
48. Wei, X. et al. Exome sequencing identifies GRIN2A as frequently mutated in melanoma. Nat. Genet. 43, 442-446 (2011).
49. Aladjem, M. I. et al. Participation of the human beta-globin locus control region in initiation of DNA replication. Science 270, 815-819 (1995).
50. Noordermeer, D. & de Laat, W. Joining the loops: beta-globin gene regulation. IUBMB Life 60, 824-833 (2008).
51. Cadoret, J. C. et al. Genome-wide studies highlight indirect links between human replication origins and gene regulation. Proc. Natl Acad. Sci. USA 105, 15837-15842 (2008).
52. Cayrou, C., Coulombe, P. & Mechali, M. Programming DNA replication origins and chromosome organization. Chromosome Res. 18, 137-145 (2010).
53. Seiler, J. A., Conti, C., Syed, A., Aladjem, M. I. & Pommier, Y. The intra-Sphase checkpoint affects both DNA replication initiation and elongation: single-cell and-DNA fiber analyses. Mol. Cell Biol. 27, 5806-5818 (2007).
54. Yun, W. J. et al. The hematopoietic regulator TAL1 is required for chromatin looping between the beta-globin LCR and human gamma-globin genes to activate transcription. Nucleic Acids Res. 42, 4283-4293 (2014).
55. Fu, H. et al. Methylation of histone H3 on lysine 79 associates with a group of replication origins and helps limit DNA replication once per cell cycle. PLoS Genet. 9, e1003542 (2013).
56. DePamphilis, M. L. Replication origins in metazoan chromosomes: fact or fiction? Bioessays 21, 5-16 (1999).
57. Donley, N., Smith, L. & Thayer, M. J. ASAR15, a cis-Acting locus that controls chromosome-wide replication timing and stability of human chromosome 15. PLoS Genet. 11, e1004923 (2015).
58. Liu, S. et al. RING finger and WD repeat domain 3 (RFWD3) associates with replication protein A (RPA) and facilitates RPA-mediated DNA damage response. J. Biol. Chem. 286, 22314-22322 (2011).
59. McCall, C. M. et al. Human immunodeficiency virus type 1 Vpr-binding protein VprBP, a WD40 protein associated with the DDB1-CUL4 E3 ubiquitin ligase, is essential for DNA replication and embryonic development. Mol. Cell Biol. 28, 5621-5633 (2008).
60. Blow, J. J., Ge, X. Q. & Jackson, D. A. How dormant origins promote complete genome replication. Trends Biochem. Sci. 36, 405-414 (2011).
61. Debatisse, M., Le Tallec, B., Letessier, A., Dutrillaux, B. & Brison, O. Common fragile sites: mechanisms of instability revisited. Trends Genet. 28, 22-32 (2012).
62. Fu, H. et al. The DNA repair endonuclease Mus81 facilitates fast DNA replication in the absence of exogenous damage. Nat. Commun. 6, 6746 (2015).
63. Shimura, T. et al. Bloom's syndrome helicase and Mus81 are required to induce transient double-strand DNA breaks in response to DNA replication stress. J. Mol. Biol. 375, 1152-1164 (2008).
64. Scherf, U. et al. A gene expression database for the molecular pharmacology of cancer. Nat. Genet. 24, 236-244 (2000).
65. Markova, E. N., Kantidze, O. L. & Razin, S. V. Transcriptional regulation and spatial organisation of the human AML1/RUNX1 gene. J. Cell. Biochem. 112, 1997-2005 (2011).