Initiation of DNA Repair Mediated by a Stalled RNA Polymerase IIO

Overview

Journal EMBO J

Specialties Biotechnology
Molecular Biology

Date 2006 Jan 13

PMID 16407975

Citations 72

Authors

Jean-Philippe Laine

Jean-Marc Egly

Affiliations

Soon will be listed here.

Abstract

The transcription-coupled repair (TCR) pathway preferentially repairs DNA damage located in the transcribed strand of an active gene. To gain insight into the coupling mechanism between transcription and repair, we have set up an in vitro system in which we isolate an elongating RNA pol IIO, which is stalled in front of a cisplatin adduct. This immobilized RNA pol IIO is used as 'bait' to sequentially recruit TFIIH, XPA, RPA, XPG and XPF repair factors in an ATP-dependent manner. This RNA pol IIO/repair complex allows the ATP-dependent removal of the lesion only in the presence of CSB, while the latter does not promote dual incision in an XPC-dependent nucleotide excision repair reaction. In parallel to the dual incision, the repair factors also allow the partial release of RNA pol IIO. In this 'minimal TCR system', the RNA pol IIO can effectively act as a loading point for all the repair factors required to eliminate a transcription-blocking lesion.

Citing Articles

STK19 positions TFIIH for cell-free transcription-coupled DNA repair.

Mevissen T, Kummecke M, Schmid E, Farnung L, Walter J Cell. 2024; 187(25):7091-7106.e24.

PMID: 39547228 PMC: 11645862. DOI: 10.1016/j.cell.2024.10.020.

The histone demethylase JMJ27 acts during the UV-induced modulation of H3K9me2 landscape and facilitates photodamage repair.

Johann To Berens P, Peter J, Koechler S, Bruggeman M, Staerck S, Molinier J Nat Plants. 2024; 10(11):1698-1709.

PMID: 39367258 DOI: 10.1038/s41477-024-01814-9.

STK19 positions TFIIH for cell-free transcription-coupled DNA repair.

Mevissen T, Kummecke M, Schmid E, Farnung L, Walter J bioRxiv. 2024; .

PMID: 39091863 PMC: 11291053. DOI: 10.1101/2024.07.22.604623.

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

Luo Y, Li J, Li X, Lin H, Mao Z, Xu Z Proc Natl Acad Sci U S A. 2024; 121(24):e2404383121.

PMID: 38843184 PMC: 11181095. DOI: 10.1073/pnas.2404383121.

Persistent TFIIH binding to non-excised DNA damage causes cell and developmental failure.

Muniesa-Vargas A, Davo-Martinez C, Ribeiro-Silva C, van der Woude M, Thijssen K, Haspels B Nat Commun. 2024; 15(1):3490.

PMID: 38664429 PMC: 11045817. DOI: 10.1038/s41467-024-47935-9.

References

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

Araujo S, Tirode F, Coin F, Pospiech H, Syvaoja J, Stucki M . Nucleotide excision repair of DNA with recombinant human proteins: definition of the minimal set of factors, active forms of TFIIH, and modulation by CAK. Genes Dev. 2000; 14(3):349-59. PMC: 316364. View

Reardon J, Sancar A . Molecular anatomy of the human excision nuclease assembled at sites of DNA damage. Mol Cell Biol. 2002; 22(16):5938-45. PMC: 133982. DOI: 10.1128/MCB.22.16.5938-5945.2002. View

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

Frit P, Kwon K, Coin F, Auriol J, Dubaele S, Salles B . Transcriptional activators stimulate DNA repair. Mol Cell. 2002; 10(6):1391-401. DOI: 10.1016/s1097-2765(02)00732-3. View

Svejstrup J . Rescue of arrested RNA polymerase II complexes. J Cell Sci. 2003; 116(Pt 3):447-51. DOI: 10.1242/jcs.00271. View

Groisman R, Polanowska J, Kuraoka I, Sawada J, Saijo M, Drapkin R . The ubiquitin ligase activity in the DDB2 and CSA complexes is differentially regulated by the COP9 signalosome in response to DNA damage. Cell. 2003; 113(3):357-67. DOI: 10.1016/s0092-8674(03)00316-7. View

Riedl T, Hanaoka F, Egly J . The comings and goings of nucleotide excision repair factors on damaged DNA. EMBO J. 2003; 22(19):5293-303. PMC: 204472. DOI: 10.1093/emboj/cdg489. View

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

10.

Tapias A, Auriol J, Forget D, Enzlin J, Scharer O, Coin F . Ordered conformational changes in damaged DNA induced by nucleotide excision repair factors. J Biol Chem. 2004; 279(18):19074-83. PMC: 4494833. DOI: 10.1074/jbc.M312611200. View

11.

Van den Boom V, Citterio E, Hoogstraten D, Zotter A, Egly J, van Cappellen W . DNA damage stabilizes interaction of CSB with the transcription elongation machinery. J Cell Biol. 2004; 166(1):27-36. PMC: 2172148. DOI: 10.1083/jcb.200401056. View

12.

Wade M, Chu E . Effects of DNA damaging agents on cultured fibroblasts derived from patients with Cockayne syndrome. Mutat Res. 1979; 59(1):49-60. DOI: 10.1016/0027-5107(79)90194-5. View

13.

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

14.

Mellon I, Spivak G, HANAWALT P . Selective removal of transcription-blocking DNA damage from the transcribed strand of the mammalian DHFR gene. Cell. 1987; 51(2):241-9. DOI: 10.1016/0092-8674(87)90151-6. View

15.

Venema J, van Hoffen A, Natarajan A, van Zeeland A, Mullenders L . The residual repair capacity of xeroderma pigmentosum complementation group C fibroblasts is highly specific for transcriptionally active DNA. Nucleic Acids Res. 1990; 18(3):443-8. PMC: 333446. DOI: 10.1093/nar/18.3.443. View

16.

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

17.

Nakatsu Y, Asahina H, Citterio E, Rademakers S, Vermeulen W, Kamiuchi S . XAB2, a novel tetratricopeptide repeat protein involved in transcription-coupled DNA repair and transcription. J Biol Chem. 2000; 275(45):34931-7. DOI: 10.1074/jbc.M004936200. View

18.

Sugasawa K, Okamoto T, Shimizu Y, Masutani C, Iwai S, Hanaoka F . A multistep damage recognition mechanism for global genomic nucleotide excision repair. Genes Dev. 2001; 15(5):507-21. PMC: 312644. DOI: 10.1101/gad.866301. View

19.

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

20.

Missura M, Buterin T, Hindges R, Hubscher U, Kasparkova J, Brabec V . Double-check probing of DNA bending and unwinding by XPA-RPA: an architectural function in DNA repair. EMBO J. 2001; 20(13):3554-64. PMC: 125508. DOI: 10.1093/emboj/20.13.3554. View