DNA Damage Stabilizes Interaction of CSB with the Transcription Elongation Machinery

Overview

Journal J Cell Biol

Specialty Cell Biology

Date 2004 Jul 1

PMID 15226310

Citations 78

Authors

Vincent Van den Boom

Elisabetta Citterio

Deborah Hoogstraten

Angelika Zotter

Jean-Marc Egly

Wiggert A van Cappellen

Jan H J Hoeijmakers

Adriaan B Houtsmuller

Wim Vermeulen

Affiliations

Soon will be listed here.

Abstract

The Cockayne syndrome B (CSB) protein is essential for transcription-coupled DNA repair (TCR), which is dependent on RNA polymerase II elongation. TCR is required to quickly remove the cytotoxic transcription-blocking DNA lesions. Functional GFP-tagged CSB, expressed at physiological levels, was homogeneously dispersed throughout the nucleoplasm in addition to bright nuclear foci and nucleolar accumulation. Photobleaching studies showed that GFP-CSB, as part of a high molecular weight complex, transiently interacts with the transcription machinery. Upon (DNA damage-induced) transcription arrest CSB binding these interactions are prolonged, most likely reflecting actual engagement of CSB in TCR. These findings are consistent with a model in which CSB monitors progression of transcription by regularly probing elongation complexes and becomes more tightly associated to these complexes when TCR is active.

Citing Articles

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Differential processing of RNA polymerase II at DNA damage correlates with transcription-coupled repair syndrome severity.

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The ARK2N-CK2 complex initiates transcription-coupled repair through enhancing the interaction of CSB with lesion-stalled RNAPII.

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The chromatin remodeler ERCC6 and the histone chaperone NAP1 are involved in apurinic/apyrimidinic endonuclease-mediated DNA repair.

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Live-cell imaging of endogenous CSB-mScarletI as a sensitive marker for DNA-damage-induced transcription stress.

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References

McNally J, Muller W, Walker D, Wolford R, Hager G . The glucocorticoid receptor: rapid exchange with regulatory sites in living cells. Science. 2000; 287(5456):1262-5. DOI: 10.1126/science.287.5456.1262. View

Houtsmuller A, Rademakers S, Nigg A, Hoogstraten D, Hoeijmakers J, Vermeulen W . Action of DNA repair endonuclease ERCC1/XPF in living cells. Science. 1999; 284(5416):958-61. DOI: 10.1126/science.284.5416.958. View

Le Page F, Kwoh E, Avrutskaya A, Gentil A, Leadon S, Sarasin A . Transcription-coupled repair of 8-oxoguanine: requirement for XPG, TFIIH, and CSB and implications for Cockayne syndrome. Cell. 2000; 101(2):159-71. DOI: 10.1016/s0092-8674(00)80827-2. View

Yu A, Fan H, Liao D, Bailey A, Weiner A . Activation of p53 or loss of the Cockayne syndrome group B repair protein causes metaphase fragility of human U1, U2, and 5S genes. Mol Cell. 2000; 5(5):801-10. DOI: 10.1016/s1097-2765(00)80320-2. View

Citterio E, van den Boom V, Schnitzler G, Kanaar R, Bonte E, Kingston R . ATP-dependent chromatin remodeling by the Cockayne syndrome B DNA repair-transcription-coupling factor. Mol Cell Biol. 2000; 20(20):7643-53. PMC: 86329. DOI: 10.1128/MCB.20.20.7643-7653.2000. View

Jansen L, den Dulk H, Brouns R, de Ruijter M, Brandsma J, Brouwer J . Spt4 modulates Rad26 requirement in transcription-coupled nucleotide excision repair. EMBO J. 2000; 19(23):6498-507. PMC: 305866. DOI: 10.1093/emboj/19.23.6498. View

Hoeijmakers J . Genome maintenance mechanisms for preventing cancer. Nature. 2001; 411(6835):366-74. DOI: 10.1038/35077232. View

Volker M, Mone M, Karmakar P, van Hoffen A, Schul W, Vermeulen W . Sequential assembly of the nucleotide excision repair factors in vivo. Mol Cell. 2001; 8(1):213-24. DOI: 10.1016/s1097-2765(01)00281-7. View

Lee S, Yu S, Prakash L, Prakash S . Requirement for yeast RAD26, a homolog of the human CSB gene, in elongation by RNA polymerase II. Mol Cell Biol. 2001; 21(24):8651-6. PMC: 100025. DOI: 10.1128/MCB.21.24.8651-8656.2001. View

10.

Woudstra E, Gilbert C, Fellows J, Jansen L, Brouwer J, Erdjument-Bromage H . A Rad26-Def1 complex coordinates repair and RNA pol II proteolysis in response to DNA damage. Nature. 2002; 415(6874):929-33. DOI: 10.1038/415929a. View

11.

de Boer J, Andressoo J, de Wit J, Huijmans J, Beems R, van Steeg H . Premature aging in mice deficient in DNA repair and transcription. Science. 2002; 296(5571):1276-9. DOI: 10.1126/science.1070174. View

12.

Van den Boom V, Jaspers N, Vermeulen W . When machines get stuck--obstructed RNA polymerase II: displacement, degradation or suicide. Bioessays. 2002; 24(9):780-4. DOI: 10.1002/bies.10150. View

13.

Bradsher J, Auriol J, Proietti De Santis L, Iben S, Vonesch J, Grummt I . CSB is a component of RNA pol I transcription. Mol Cell. 2002; 10(4):819-29. DOI: 10.1016/s1097-2765(02)00678-0. View

14.

Hoogstraten D, Nigg A, Heath H, Mullenders L, van Driel R, Hoeijmakers J . Rapid switching of TFIIH between RNA polymerase I and II transcription and DNA repair in vivo. Mol Cell. 2002; 10(5):1163-74. DOI: 10.1016/s1097-2765(02)00709-8. View

15.

Kimura H, Sugaya K, Cook P . The transcription cycle of RNA polymerase II in living cells. J Cell Biol. 2002; 159(5):777-82. PMC: 2173384. DOI: 10.1083/jcb.200206019. View

16.

Rademakers S, Volker M, Hoogstraten D, Nigg A, Mone M, van Zeeland A . Xeroderma pigmentosum group A protein loads as a separate factor onto DNA lesions. Mol Cell Biol. 2003; 23(16):5755-67. PMC: 166334. DOI: 10.1128/MCB.23.16.5755-5767.2003. View

17.

Tremeau-Bravard A, Riedl T, Egly J, Dahmus M . Fate of RNA polymerase II stalled at a cisplatin lesion. J Biol Chem. 2003; 279(9):7751-9. DOI: 10.1074/jbc.M309853200. View

18.

Farla P, Hersmus R, Geverts B, Mari P, Nigg A, Dubbink H . The androgen receptor ligand-binding domain stabilizes DNA binding in living cells. J Struct Biol. 2004; 147(1):50-61. DOI: 10.1016/j.jsb.2004.01.002. View

19.

CHANDLER V, Maler B, Yamamoto K . DNA sequences bound specifically by glucocorticoid receptor in vitro render a heterologous promoter hormone responsive in vivo. Cell. 1983; 33(2):489-99. DOI: 10.1016/0092-8674(83)90430-0. View

20.

Bohr V, Smith C, Okumoto D, HANAWALT P . DNA repair in an active gene: removal of pyrimidine dimers from the DHFR gene of CHO cells is much more efficient than in the genome overall. Cell. 1985; 40(2):359-69. DOI: 10.1016/0092-8674(85)90150-3. View