The Histone Chaperone Facilitates Chromatin Transcription (FACT) Protein Maintains Normal Replication Fork Rates

Overview

Journal J Biol Chem

Specialty Biochemistry

Date 2011 Jul 16

PMID 21757688

Citations 44

Authors

Takuya Abe

Kazuto Sugimura

Yoshifumi Hosono

Yasunari Takami

Motomu Akita

Akari Yoshimura

Shusuke Tada

Tatsuo Nakayama

Hiromu Murofushi

Katsuzumi Okumura

Shunichi Takeda

Masami Horikoshi

Masayuki Seki

Takemi Enomoto

Affiliations

Soon will be listed here.

Abstract

Ordered nucleosome disassembly and reassembly are required for eukaryotic DNA replication. The facilitates chromatin transcription (FACT) complex, a histone chaperone comprising Spt16 and SSRP1, is involved in DNA replication as well as transcription. FACT associates with the MCM helicase, which is involved in DNA replication initiation and elongation. Although the FACT-MCM complex is reported to regulate DNA replication initiation, its functional role in DNA replication elongation remains elusive. To elucidate the functional role of FACT in replication fork progression during DNA elongation in the cells, we generated and analyzed conditional SSRP1 gene knock-out chicken (Gallus gallus) DT40 cells. SSRP1-depleted cells ceased to grow and exhibited a delay in S-phase cell cycle progression, although SSRP1 depletion did not affect the level of chromatin-bound DNA polymerase α or nucleosome reassembly on daughter strands. The tracking length of newly synthesized DNA, but not origin firing, was reduced in SSRP1-depleted cells, suggesting that the S-phase cell cycle delay is mainly due to the inhibition of replication fork progression rather than to defects in the initiation of DNA replication in these cells. We discuss the mechanisms of how FACT promotes replication fork progression in the cells.

Citing Articles

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FACT regulates pluripotency through proximal and distal regulation of gene expression in murine embryonic stem cells.

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The Current Status of SSRP1 in Cancer: Tribulation and Road Ahead.

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SSRP1 affects the growth and apoptosis of gastric cancer cells through AKT pathway.

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FACT maintains nucleosomes during transcription and stem cell viability in adult mice.

Goswami I, Sandlesh P, Stablewski A, Toshkov I, Safina A, Magnitov M EMBO Rep. 2022; 23(4):e53684.

PMID: 35179289 PMC: 8982582. DOI: 10.15252/embr.202153684.

References

Woodward A, Gohler T, Luciani M, Oehlmann M, Ge X, Gartner A . Excess Mcm2-7 license dormant origins of replication that can be used under conditions of replicative stress. J Cell Biol. 2006; 173(5):673-83. PMC: 2063885. DOI: 10.1083/jcb.200602108. View

Gambus A, Jones R, Sanchez-Diaz A, Kanemaki M, van Deursen F, Edmondson R . GINS maintains association of Cdc45 with MCM in replisome progression complexes at eukaryotic DNA replication forks. Nat Cell Biol. 2006; 8(4):358-66. DOI: 10.1038/ncb1382. View

Petermann E, Helleday T, Caldecott K . Claspin promotes normal replication fork rates in human cells. Mol Biol Cell. 2008; 19(6):2373-8. PMC: 2397295. DOI: 10.1091/mbc.e07-10-1035. View

Katsuno Y, Suzuki A, Sugimura K, Okumura K, Zineldeen D, Shimada M . Cyclin A-Cdk1 regulates the origin firing program in mammalian cells. Proc Natl Acad Sci U S A. 2009; 106(9):3184-9. PMC: 2651338. DOI: 10.1073/pnas.0809350106. View

Orphanides G, Wu W, Lane W, Hampsey M, Reinberg D . The chromatin-specific transcription elongation factor FACT comprises human SPT16 and SSRP1 proteins. Nature. 1999; 400(6741):284-8. DOI: 10.1038/22350. View

Groth A, Corpet A, Cook A, Roche D, Bartek J, Lukas J . Regulation of replication fork progression through histone supply and demand. Science. 2007; 318(5858):1928-31. DOI: 10.1126/science.1148992. View

Mason P, Struhl K . The FACT complex travels with elongating RNA polymerase II and is important for the fidelity of transcriptional initiation in vivo. Mol Cell Biol. 2003; 23(22):8323-33. PMC: 262413. DOI: 10.1128/MCB.23.22.8323-8333.2003. View

Jackson V . In vivo studies on the dynamics of histone-DNA interaction: evidence for nucleosome dissolution during replication and transcription and a low level of dissolution independent of both. Biochemistry. 1990; 29(3):719-31. DOI: 10.1021/bi00455a019. View

Chin-Ming Tan B, Liu H, Lin C, Lee S . Functional cooperation between FACT and MCM is coordinated with cell cycle and differential complex formation. J Biomed Sci. 2010; 17:11. PMC: 2848000. DOI: 10.1186/1423-0127-17-11. View

10.

Jackson D, 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(6):1285-95. PMC: 2132671. DOI: 10.1083/jcb.140.6.1285. View

11.

Costa A, Ilves I, Tamberg N, Petojevic T, Nogales E, Botchan M . The structural basis for MCM2-7 helicase activation by GINS and Cdc45. Nat Struct Mol Biol. 2011; 18(4):471-7. PMC: 4184033. DOI: 10.1038/nsmb.2004. View

12.

Xin H, Takahata S, Blanksma M, McCullough L, Stillman D, Formosa T . yFACT induces global accessibility of nucleosomal DNA without H2A-H2B displacement. Mol Cell. 2009; 35(3):365-76. PMC: 2748400. DOI: 10.1016/j.molcel.2009.06.024. View

13.

Cao S, Bendall H, Hicks G, Nashabi A, Sakano H, Shinkai Y . The high-mobility-group box protein SSRP1/T160 is essential for cell viability in day 3.5 mouse embryos. Mol Cell Biol. 2003; 23(15):5301-7. PMC: 165710. DOI: 10.1128/MCB.23.15.5301-5307.2003. View

14.

Tyler J, Adams C, Chen S, Kobayashi R, Kamakaka R, Kadonaga J . The RCAF complex mediates chromatin assembly during DNA replication and repair. Nature. 1999; 402(6761):555-60. DOI: 10.1038/990147. View

15.

Corpet A, Almouzni G . Making copies of chromatin: the challenge of nucleosomal organization and epigenetic information. Trends Cell Biol. 2008; 19(1):29-41. DOI: 10.1016/j.tcb.2008.10.002. View

16.

Philpott A, Krude T, Laskey R . Nuclear chaperones. Semin Cell Dev Biol. 2000; 11(1):7-14. DOI: 10.1006/scdb.1999.0346. View

17.

ODonnell A, Brewster N, Kurniawan J, Minard L, Johnston G, Singer R . Domain organization of the yeast histone chaperone FACT: the conserved N-terminal domain of FACT subunit Spt16 mediates recovery from replication stress. Nucleic Acids Res. 2004; 32(19):5894-906. PMC: 528806. DOI: 10.1093/nar/gkh922. View

18.

Quivy J, Gerard A, Cook A, Roche D, Almouzni G . The HP1-p150/CAF-1 interaction is required for pericentric heterochromatin replication and S-phase progression in mouse cells. Nat Struct Mol Biol. 2009; 15(9):972-9. DOI: 10.1038/nsmb.1470. View

19.

Orphanides G, Leroy G, Chang C, Luse D, Reinberg D . FACT, a factor that facilitates transcript elongation through nucleosomes. Cell. 1998; 92(1):105-16. DOI: 10.1016/s0092-8674(00)80903-4. View

20.

Shibahara K, Stillman B . Replication-dependent marking of DNA by PCNA facilitates CAF-1-coupled inheritance of chromatin. Cell. 1999; 96(4):575-85. DOI: 10.1016/s0092-8674(00)80661-3. View