RNA Polymerase II and III Transcription Factors Can Stimulate DNA Replication by Modifying Origin Chromatin Structures

Overview

Journal Nucleic Acids Res

Publisher Oxford University Press

Specialty Biochemistry

Date 2001 Nov 20

PMID 11713306

Citations 10

Authors

K Edler

A Barberis

Affiliations

Soon will be listed here.

Abstract

Many transcription factors are multifunctional and also influence DNA replication. So far, their mechanism of action has remained elusive. Here we show that a DNA-binding protein could rely on the same biochemical activity that activates transcription to stimulate replication from the yeast chromosomal ARS1 origin. Unexpectedly, the ability to stimulate replication from this origin was not restricted to polymerase II transcription factors, but was a property shared by polymerase III factors. Furthermore, activation of replication did not depend on the process of transcription, but rather on the ability of DNA-binding transcription factors to remodel chromatin. The natural ARS1 activator Abf1 and the other transcription factors that stimulated replication remodeled chromatin in a very similar manner. Moreover, the presence of a histone H3 mutant that was previously shown to generally increase transcription also facilitated replication from ARS1 and partially compensated for the absence of a transcription factor. We propose that multifunctional transcription factors work by influencing the chromatin architecture at replication origins so as to generate a structure that is favorable to the initiation of replication.

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References

Brown C, Lechner T, Howe L, Workman J . The many HATs of transcription coactivators. Trends Biochem Sci. 2000; 25(1):15-9. DOI: 10.1016/s0968-0004(99)01516-9. View

Sudarsanam P, Winston F . The Swi/Snf family nucleosome-remodeling complexes and transcriptional control. Trends Genet. 2000; 16(8):345-51. DOI: 10.1016/s0168-9525(00)02060-6. View

Lipford J, Bell S . Nucleosomes positioned by ORC facilitate the initiation of DNA replication. Mol Cell. 2001; 7(1):21-30. DOI: 10.1016/s1097-2765(01)00151-4. View

Thoma F, Bergman L, Simpson R . Nuclease digestion of circular TRP1ARS1 chromatin reveals positioned nucleosomes separated by nuclease-sensitive regions. J Mol Biol. 1984; 177(4):715-33. DOI: 10.1016/0022-2836(84)90046-9. View

Diffley J, Stillman B . Purification of a yeast protein that binds to origins of DNA replication and a transcriptional silencer. Proc Natl Acad Sci U S A. 1988; 85(7):2120-4. PMC: 279940. DOI: 10.1073/pnas.85.7.2120. View

Hatton K, Dhar V, Brown E, Iqbal M, Stuart S, Didamo V . Replication program of active and inactive multigene families in mammalian cells. Mol Cell Biol. 1988; 8(5):2149-58. PMC: 363396. DOI: 10.1128/mcb.8.5.2149-2158.1988. View

Cheng L, Kelly T . Transcriptional activator nuclear factor I stimulates the replication of SV40 minichromosomes in vivo and in vitro. Cell. 1989; 59(3):541-51. DOI: 10.1016/0092-8674(89)90037-8. View

Simpson R . Nucleosome positioning can affect the function of a cis-acting DNA element in vivo. Nature. 1990; 343(6256):387-9. DOI: 10.1038/343387a0. View

Brow D, Guthrie C . Transcription of a yeast U6 snRNA gene requires a polymerase III promoter element in a novel position. Genes Dev. 1990; 4(8):1345-56. DOI: 10.1101/gad.4.8.1345. View

10.

Ten Hagen K, Gilbert D, Willard H, Cohen S . Replication timing of DNA sequences associated with human centromeres and telomeres. Mol Cell Biol. 1990; 10(12):6348-55. PMC: 362910. DOI: 10.1128/mcb.10.12.6348-6355.1990. View

11.

Ferguson B, FANGMAN W . A position effect on the time of replication origin activation in yeast. Cell. 1992; 68(2):333-9. DOI: 10.1016/0092-8674(92)90474-q. View

12.

Marahrens Y, Stillman B . A yeast chromosomal origin of DNA replication defined by multiple functional elements. Science. 1992; 255(5046):817-23. DOI: 10.1126/science.1536007. View

13.

Bell S, Stillman B . ATP-dependent recognition of eukaryotic origins of DNA replication by a multiprotein complex. Nature. 1992; 357(6374):128-34. DOI: 10.1038/357128a0. View

14.

Benard M, Pallotta D, Pierron G . Structure and identity of a late-replicating and transcriptionally active gene. Exp Cell Res. 1992; 201(2):506-13. DOI: 10.1016/0014-4827(92)90301-n. View

15.

MANN R, Grunstein M . Histone H3 N-terminal mutations allow hyperactivation of the yeast GAL1 gene in vivo. EMBO J. 1992; 11(9):3297-306. PMC: 556864. DOI: 10.1002/j.1460-2075.1992.tb05408.x. View

16.

Li R, Botchan M . The acidic transcriptional activation domains of VP16 and p53 bind the cellular replication protein A and stimulate in vitro BPV-1 DNA replication. Cell. 1993; 73(6):1207-21. DOI: 10.1016/0092-8674(93)90649-b. View

17.

He Z, Brinton B, GREENBLATT J, Hassell J, Ingles C . The transactivator proteins VP16 and GAL4 bind replication factor A. Cell. 1993; 73(6):1223-32. DOI: 10.1016/0092-8674(93)90650-f. View

18.

Newlon C, Theis J . The structure and function of yeast ARS elements. Curr Opin Genet Dev. 1993; 3(5):752-8. DOI: 10.1016/s0959-437x(05)80094-2. View

19.

Li R, Botchan M . Acidic transcription factors alleviate nucleosome-mediated repression of DNA replication of bovine papillomavirus type 1. Proc Natl Acad Sci U S A. 1994; 91(15):7051-5. PMC: 44336. DOI: 10.1073/pnas.91.15.7051. View

20.

Diffley J, Cocker J, Dowell S, Rowley A . Two steps in the assembly of complexes at yeast replication origins in vivo. Cell. 1994; 78(2):303-16. DOI: 10.1016/0092-8674(94)90299-2. View