Structure, function and regulation of CSB: A multi-talented gymnast

Mechanisms of Ageing and Development

Volumn 134, Issue 5-6, 2013, Pages 202-211

  Fan, Ying H ^a   Lake, Robert J ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

ATP dependent chromatin remodeling; Chromatin; CSB; DNA repair; Transcription regulation

Indexed keywords

ADENOSINE TRIPHOSPHATASE; CSB PROTEIN; DNA BINDING PROTEIN; PROTEIN APE1; PROTEIN C JUN; PROTEIN HARP; PROTEIN NEIL1; PROTEIN P53; SINGLE STRANDED DNA; THYROID TRANSCRIPTION FACTOR 1; TRANSCRIPTION FACTOR SNF; TRANSCRIPTION FACTOR SNF2; TRANSCRIPTION FACTOR SWI2; UBIQUITIN; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMATIN STRUCTURE; COCKAYNE SYNDROME; DISEASE ASSOCIATION; DNA CONFORMATION; DNA DAMAGE; DNA PROTEIN COMPLEX; DNA TRANSCRIPTION; ENZYME ACTIVITY; ENZYME REGULATION; ENZYME STRUCTURE; GENE MUTATION; HUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN PROCESSING; PROTEIN TARGETING; UBIQUITINATION;

ANIMALS; CHROMATIN ASSEMBLY AND DISASSEMBLY; DNA HELICASES; DNA REPAIR; DNA REPAIR ENZYMES; HUMANS; STRUCTURE-ACTIVITY RELATIONSHIP; TRANSCRIPTION, GENETIC;

EID: 84878012786     PISSN: 00476374     EISSN: 18726216     Source Type: Journal    
DOI: 10.1016/j.mad.2013.02.004     Document Type: Article

References (82)

1. Alexiadis V., Kadonaga J.T. Strand pairing by Rad54 and Rad51 is enhanced by chromatin. Genes and Development 2002, 16:2767-2771.
2. Anindya R., Mari P.O., Kristensen U., Kool H., Giglia-Mari G., Mullenders L.H., Fousteri M., Vermeulen W., Egly J.M., Svejstrup J.Q. A ubiquitin-binding domain in Cockayne syndrome B required for transcription-coupled nucleotide excision repair. Molecular Cell 2010, 38:637-648.
3. Auble D.T., Hansen K.E., Mueller C.G., Lane W.S., Thorner J., Hahn S. Mot1, a global repressor of RNA polymerase II transcription, inhibits TBP binding to DNA by an ATP-dependent mechanism. Genes and Development 1994, 8:1920-1934.
4. Batenburg N.L., Mitchell T.R., Leach D.M., Rainbow A.J., Zhu X.D. Cockayne syndrome group B protein interacts with TRF2 and regulates telomere length and stability. Nucleic Acids Research 2012.
5. Beerens N., Hoeijmakers J.H., Kanaar R., Vermeulen W., Wyman C. The CSB protein actively wraps DNA. Journal of Biological Chemistry 2005, 280:4722-4729.
6. Berquist B.R., Canugovi C., Sykora P., Wilson D.M., Bohr V.A. Human Cockayne syndrome B protein reciprocally communicates with mitochondrial proteins and promotes transcriptional elongation. Nucleic Acids Research 2012.
7. Berquist B.R., Wilson D.M. Nucleic acid binding activity of human Cockayne syndrome B protein and identification of Ca(2+) as a novel metal cofactor. Journal of Molecular Biology 2009, 391:820-832.
8. Betous R., Mason A.C., Rambo R.P., Bansbach C.E., Badu-Nkansah A., Sirbu B.M., Eichman B.F., Cortez D. SMARCAL1 catalyzes fork regression and Holliday junction migration to maintain genome stability during DNA replication. Genes and Development 2012, 26:151-162.
9. Bradsher J., Auriol J., Proietti de Santis L., Iben S., Vonesch J.L., Grummt I., Egly J.M. CSB is a component of RNA pol I transcription. Molecular Cell 2002, 10:819-829.
10. Brosh R.M., Balajee A.S., Selzer R.R., Sunesen M., Proietti de Santis L., Bohr V.A. The ATPase domain but not the acidic region of Cockayne syndrome group B gene product is essential for DNA repair. Molecular Biology of the Cell 1999, 10:3583-3594.
11. Chen W.Y., Wang D.H., Yen R.C., Luo J., Gu W., Baylin S.B. Tumor suppressor HIC1 directly regulates SIRT1 to modulate p53-dependent DNA-damage responses. Cell 2005, 123:437-448.
12. Christiansen M., Stevnsner T., Modin C., Martensen P.M., Brosh R.M., Bohr V.A. Functional consequences of mutations in the conserved SF2 motifs and post-translational phosphorylation of the CSB protein. Nucleic Acids Research 2003, 31:963-973.
13. Christiansen M., Thorslund T., Jochimsen B., Bohr V.A., Stevnsner T. The Cockayne syndrome group B protein is a functional dimer. FEBS Journal 2005, 272:4306-4314.
14. Citterio E., Rademakers S., van Der Horst G.T., van Gool A.J., Hoeijmakers J.H., Vermeulen W. Biochemical and biological characterization of wild-type and ATPase-deficient Cockayne syndrome B repair protein. Journal of Biological Chemistry 1998, 273:11844-11851.
15. Citterio E., van den Boom V., Schnitzler G., Kanaar R., Bonte E., Kingston R.E., Hoeijmakers J.H., Vermeulen W. ATP-dependent chromatin remodeling by the Cockayne syndrome B DNA repair-transcription-coupling factor. Molecular and Cellular Biology 2000, 20:7643-7653.
16. Clapier C.R., Cairns B.R. The biology of chromatin remodeling complexes. Annual Review of Biochemistry 2009, 78:273-304.
17. Colella S., Nardo T., Botta E., Lehmann A.R., Stefanini M. Identical mutations in the CSB gene associated with either Cockayne syndrome or the DeSanctis-cacchione variant of xeroderma pigmentosum. Human Molecular Genetics 2000, 9:1171-1175.
18. Colella S., Nardo T., Mallery D., Borrone C., Ricci R., Ruffa G., Lehmann A.R., Stefanini M. Alterations in the CSB gene in three Italian patients with the severe form of Cockayne syndrome (CS) but without clinical photosensitivity. Human Molecular Genetics 1999, 8:935-941.
19. Dephoure N., Zhou C., Villen J., Beausoleil S.A., Bakalarski C.E., Elledge S.J., Gygi S.P. A quantitative atlas of mitotic phosphorylation. Proceedings of the National Academy of Sciences of the United States of America 2008, 105:10762-10767.
20. Eferl R., Wagner E.F. AP-1: a double-edged sword in tumorigenesis. Nature Reviews Cancer 2003, 3:859-868.
21. Fairman-Williams M.E., Guenther U.P., Jankowsky E. SF1 and SF2 helicases: family matters. Current Opinion in Structural Biology 2010, 20:313-324.
22. Fan H.Y., Narlikar G.J., Kingston R.E. Noncovalent modification of chromatin: different remodeled products with different ATPase domains. Cold Spring Harbor Symposia on Quantitative Biology 2004, 69:183-192.
23. Flaus A., Martin D.M., Barton G.J., Owen-Hughes T. Identification of multiple distinct Snf2 subfamilies with conserved structural motifs. Nucleic Acids Research 2006, 34:2887-2905.
24. Flohr C., Burkle A., Radicella J.P., Epe B. Poly(ADP-ribosyl)ation accelerates DNA repair in a pathway dependent on Cockayne syndrome B protein. Nucleic Acids Research 2003, 31:5332-5337.
25. Fousteri M., Vermeulen W., van Zeeland A.A., Mullenders L.H. Cockayne syndrome A and B proteins differentially regulate recruitment of chromatin remodeling and repair factors to stalled RNA polymerase II in vivo. Molecular Cell 2006, 23:471-482.
26. Gelbart M.E., Bachman N., Delrow J., Boeke J.D., Tsukiyama T. Genome-wide identification of Isw2 chromatin-remodeling targets by localization of a catalytically inactive mutant. Genes and Development 2005, 19:942-954.
27. Gray L.T., Fong K.K., Pavelitz T., Weiner A.M. Tethering of the conserved piggyBac transposase fusion protein CSB-PGBD3 to chromosomal AP-1 proteins regulates expression of nearby genes in humans. PLoS Genetics 2012, 8:E1002972.
28. Ghosal G., Yuan J., Chen J. The HARP domain dictates the annealing helicase activity of HARP/SMARCAL1. EMBO Reports 2011, 12:574-580.
29. Grüne T., Brzeski J., Eberharter A., Clapier C.R., Corona D.F.V., Becker P.B., Müller C.W. Crystal structure and functional analysis of a nucleosome recognition module of the remodeling factor ISWI. Molecular Cell 2003, 12:449-460.
30. Guetg C., Lienemann P., Sirri V., Grummt I., Hernandez-Verdun D., Hottiger M.O., Fussenegger M., Santoro R. The NoRC complex mediates the heterochromatin formation and stability of silent rRNA genes and centromeric repeats. EMBO Journal 2010, 29:2135-2146.
31. Hanawalt P.C., Spivak G. Transcription-coupled DNA repair: two decades of progress and surprises. Nature Reviews Molecular Cell Biology 2008, 9:958-970.
32. He X., Fan H.Y., Garlick J.D., Kingston R.E. Diverse regulation of SNF2h chromatin remodeling by noncatalytic subunits. Biochemistry 2008.
33. He X., Fan H.Y., Narlikar G.J., Kingston R.E. Human ACF1 alters the remodeling strategy of SNF2h. Journal of Biological Chemistry 2006, 281:28636-28647.
34. Ho L., Crabtree G.R. Chromatin remodelling during development. Nature 2010, 463:474-484.
35. Hogan C., Varga-Weisz P. The regulation of ATP-dependent nucleosome remodelling factors. Mutation Research 2007, 618:41-51.
36. Hopfner K.P., Gerhold C.B., Lakomek K., Wollmann P. Swi2/Snf2 remodelers: hybrid views on hybrid molecular machines. Current Opinion in Structural Biology 2012, 22:225-233.
37. Horn P.J., Peterson C.L. The bromodomain: a regulator of ATP-dependent chromatin remodeling?. Frontiers in Bioscience 2001, 6:D1019-D1023.
38. Imam S.Z., Indig F.E., Cheng W.H., Saxena S.P., Stevnsner T., Kufe D., Bohr V.A. Cockayne syndrome protein B interacts with and is phosphorylated by c-Abl tyrosine kinase. Nucleic Acids Research 2007, 35:4941-4951.
39. Ito T., Levenstein M.E., Fyodorov D.V., Kutach A.K., Kobayashi R., Kadonaga J.T. ACF consists of two subunits, Acf1 and ISWI, that function cooperatively in the ATP-dependent catalysis of chromatin assembly. Genes and Development 1999, 13:1529-1539.
40. Jaakkola E., Mustonen A., Olsen P., Miettinen S., Savuoja T., Raams A., Jaspers N.G., Shao H., Wu B.L., Ignatius J. ERCC6 founder mutation identified in Finnish patients with COFS syndrome. Clinical Genetics 2010, 78:541-547.
41. Kyng K.J., May A., Brosh R.M., Cheng W.H., Chen C., Becker K.G., Bohr V.A. The transcriptional response after oxidative stress is defective in Cockayne syndrome group B cells. Oncogene 2003, 22:1135-1149.
42. Lake R.J., Basheer A., Fan H.Y. Reciprocally regulated chromatin association of Cockayne syndrome protein B and p53 protein. Journal of Biological Chemistry 2011, 286:34951-34958.
43. Lake R.J., Geyko A., Hemashettar G., Zhao Y., Fan H.Y. UV-induced association of the CSB remodeling protein with chromatin requires ATP-dependent relief of N-terminal autorepression. Molecular Cell 2010, 37:235-246.
44. Latini P., Frontini M., Caputo M., Gregan J., Cipak L., Filippi S., Kumar V., Velez-Cruz R., Stefanini M., Proietti-de-Santis L. CSA and CSB proteins interact with p53 and regulate its Mdm2-dependent ubiquitination. Cell Cycle 2011, 10:3719-3730.
45. Laugel V., Dalloz C., Durand M., Sauvanaud F., Kristensen U., Vincent M.C., Pasquier L., Odent S., Cormier-Daire V., Gener B., Tobias E.S., Tolmie J.L., Martin-Coignard D., Drouin-Garraud V., Heron D., Journel H., Raffo E., Vigneron J., Lyonnet S., Murday V., Gubser-Mercati D., Funalot B., Brueton L., Sanchez Del Pozo J., Munoz E., Gennery A.R., Salih M., Noruzinia M., Prescott K., Ramos L., Stark Z., Fieggen K., Chabrol B., Sarda P., Edery P., Bloch-Zupan A., Fawcett H., Pham D., Egly J.M., Lehmann A.R., Sarasin A., Dollfus H. Mutation update for the CSB/ERCC6 and CSA/ERCC8 genes involved in Cockayne syndrome. Human Mutation 2010, 31:113-126.
46. Madison J.M., Winston F. Evidence that Spt3 functionally interacts with Mot1, TFIIA, and TATA-binding protein to confer promoter-specific transcriptional control in Saccharomyces cerevisiae. Molecular and Cellular Biology 1997, 17:287-295.
47. Mallery D.L., Tanganelli B., Colella S., Steingrimsdottir H., van Gool A.J., Troelstra C., Stefanini M., Lehmann A.R. Molecular analysis of mutations in the CSB (ERCC6) gene in patients with Cockayne syndrome. American Journal of Human Genetics 1998, 62:77-85.
48. Mathonnet G., Leger C., Desnoyers J., Drouin R., Therrien J.P., Drobetsky E.A. UV wavelength-dependent regulation of transcription-coupled nucleotide excision repair in p53-deficient human cells. Proceedings of the National Academy of Sciences of the United States of America 2003, 100:7219-7224.
49. Matsuoka S., Ballif B.A., Smogorzewska A., Mcdonald E.R., Hurov K.E., Luo J., Bakalarski C.E., Zhao Z., Solimini N., Lerenthal Y., Shiloh Y., Gygi S.P., Elledge S.J. ATM and ATR substrate analysis reveals extensive protein networks responsive to DNA damage. Science 2007, 316:1160-1166.
50. Muftuoglu M., de Souza-Pinto N.C., Dogan A., Aamann M., Stevnsner T., Rybanska I., Kirkali G., Dizdaroglu M., Bohr V.A. Cockayne syndrome group B protein stimulates repair of formamidopyrimidines by NEIL1 DNA glycosylase. Journal of Biological Chemistry 2009, 284:9270-9279.
51. Muftuoglu M., Selzer R., Tuo J., Brosh R.M., Bohr V.A. Phenotypic consequences of mutations in the conserved motifs of the putative helicase domain of the human Cockayne syndrome group B gene. Gene 2002, 283:27-40.
52. Muftuoglu M., Sharma S., Thorslund T., Stevnsner T., Soerensen M.M., Brosh R.M., Bohr V.A. Cockayne syndrome group B protein has novel strand annealing and exchange activities. Nucleic Acids Research 2006, 34:295-304.
53. Newman J.C., Bailey A.D., Fan H.Y., Pavelitz T., Weiner A.M. An abundant evolutionarily conserved CSB-PiggyBac fusion protein expressed in Cockayne syndrome. PLoS Genetics 2008, 4:E1000031.
54. Newman J.C., Bailey A.D., Weiner A.M. Cockayne syndrome group B protein (CSB) plays a general role in chromatin maintenance and remodeling. Proceedings of the National Academy of Science 2006, 103:9613-9618.
55. Nousiainen M., Sillje H.H., Sauer G., Nigg E.A., Korner R. Phosphoproteome analysis of the human mitotic spindle. Proceedings of the National Academy of Sciences of the United States of America 2006, 103:5391-5396.
56. Phelan M.L., Sif S., Narlikar G.J., Kingston R.E. Reconstitution of a core chromatin remodeling complex from SWI/SNF subunits. Molecular Cell 1999, 3:247-253.
57. Pyle A.M. Translocation and unwinding mechanisms of RNA and DNA helicases. Annual Review of Biophysics 2008, 37:317-336.
58. Racki L.R., Yang J.G., Naber N., Partensky P.D., Acevedo A., Purcell T.J., Cooke R., Cheng Y., Narlikar G.J. The chromatin remodeller ACF acts as a dimeric motor to space nucleosomes. Nature 2009, 462:1016-1021.
59. Richmond E., Peterson C.L. Functional analysis of the DNA-stimulated ATPase domain of yeast SWI2/SNF2. Nucleic Acids Research 1996, 24:3685-3692.
60. Sakai A., Sakasai R., Kakeji Y., Kitao H., Maehara Y. PARP and CSB modulate the processing of transcription-mediated DNA strand breaks. Genes and Genetic Systems 2012, 87:265-272.
61. Selby C.P., Sancar A. Structure and function of transcription-repair coupling factor. II. Catalytic properties. Journal of Biological Chemistry 1995, 270:4890-4895.
62. Selby C.P., Sancar A. Human transcription-repair coupling factor CSB/ERCC6 is a DNA-stimulated ATPase but is not a helicase and does not disrupt the ternary transcription complex of stalled RNA polymerase II. Journal of Biological Chemistry 1997, 272:1885-1890.
63. Selzer R.R., Nyaga S., Tuo J., May A., Muftuoglu M., Christiansen M., Citterio E., Brosh R.M., Bohr V.A. Differential requirement for the ATPase domain of the Cockayne syndrome group B gene in the processing of UV-induced DNA damage and 8-oxoguanine lesions in human cells. Nucleic Acids Research 2002, 30:782-793.
64. Sif S., Stukenberg P.T., Kirschner M.W., Kingston R.E. Mitotic inactivation of a human SWI/SNF chromatin remodeling complex. Genes and Development 1998, 12:2842-2851.
65. Thoma N.H., Czyzewski B.K., Alexeev A.A., Mazin A.V., Kowalczykowski S.C., Pavletich N.P. Structure of the SWI2/SNF2 chromatin-remodeling domain of eukaryotic Rad54. Nature Structural & Molecular Biology 2005, 12:350-356.
66. Thorslund T., von Kobbe C., Harrigan J.A., Indig F.E., Christiansen M., Stevnsner T., Bohr V.A. Cooperation of the Cockayne syndrome group B protein and poly(ADP-ribose) polymerase 1 in the response to oxidative stress. Molecular and Cellular Biology 2005, 25:7625-7636.
67. Troelstra C., van Gool A., de Wit J., Vermeulen W., Bootsma D., Hoeijmakers J.H. ERCC6, a member of a subfamily of putative helicases, is involved in Cockayne's syndrome and preferential repair of active genes. Cell 1992, 71:939-953.
68. van Den Boom V., Citterio E., Hoogstraten D., Zotter A., Egly J.M., van Cappellen W.A., Hoeijmakers J.H., Houtsmuller A.B., Vermeulen W. DNA damage stabilizes interaction of CSB with the transcription elongation machinery. Journal of Cell Biology 2004, 166:27-36.
69. van Gool A.J., Citterio E., Rademakers S., van Os R., Vermeulen W., Constantinou A., Egly J.M., Bootsma D., Hoeijmakers J.H. The Cockayne syndrome B protein, involved in transcription-coupled DNA repair, resides in an RNA polymerase II-containing complex. EMBO Journal 1997, 16:5955-5965.
70. van Steensel B., Smogorzewska A., de Lange T. TRF2 protects human telomeres from end-to-end fusions. Cell 1998, 92:401-413.
71. Wang X.W., Yeh H., Schaeffer L., Roy R., Moncollin V., Egly J.M., Wang Z., Freidberg E.C., Evans M.K., Taffe B.G., et al. p53 modulation of TFIIH-associated nucleotide excision repair activity. Nature Genetics 1995, 10:188-195.
72. Wollmann P., Cui S., Viswanathan R., Berninghausen O., Wells M.N., Moldt M., Witte G., Butryn A., Wendler P., Beckmann R., Auble D.T., Hopfner K.P. Structure and mechanism of the Swi2/Snf2 remodeller Mot1 in complex with its substrate TBP. Nature 2011, 475:403-407.
73. Wong H.K., Muftuoglu M., Beck G., Imam S.Z., Bohr V.A., Wilson D.M. Cockayne syndrome B protein stimulates apurinic endonuclease 1 activity and protects against agents that introduce base excision repair intermediates. Nucleic Acids Research 2007, 35:4103-4113.
74. Wu J.I., Lessard J., Olave I.A., Qiu Z., Ghosh A., Graef I.A., Crabtree G.R. Regulation of dendritic development by neuron-specific chromatin remodeling complexes. Neuron 2007, 56:94-108.
75. Wu Y., Brosh R.M. Distinct roles of RECQ1 in the maintenance of genomic stability. DNA Repair (Amst) 2010, 9:315-324.
76. Xie W., Ling T., Zhou Y., Feng W., Zhu Q., Stunnenberg H.G., Grummt I., Tao W. The chromatin remodeling complex NuRD establishes the poised state of rRNA genes characterized by bivalent histone modifications and altered nucleosome positions. Proceedings of the National Academy of Sciences of the United States of America 2012.
77. Yu A., Bailey A.D., Weiner A.M. Metaphase fragility of the human RNU1 and RNU2 loci is induced by actinomycin D through a p53-dependent pathway. Human Molecular Genetics 1998, 7:609-617.
78. Yu A., Fan H.Y., Liao D., Bailey A.D., Weiner A.M. Activation of p53 or loss of the Cockayne syndrome group B repair protein causes metaphase fragility of human U1, U2, and 5S genes. Molecular Cell 2000, 5:801-810.
79. Yu L.R., Zhu Z., Chan K.C., Issaq H.J., Dimitrov D.S., Veenstra T.D. Improved titanium dioxide enrichment of phosphopeptides from HeLa cells and high confident phosphopeptide identification by cross-validation of MS/MS and MS/MS/MS spectra. Journal of Proteome Research 2007, 6:4150-4162.
80. Yuan X., Feng W., Imhof A., Grummt I., Zhou Y. Activation of RNA polymerase I transcription by Cockayne syndrome group B protein and histone methyltransferase G9a. Molecular Cell 2007, 27:585-595.
81. Yusufzai T., Kadonaga J.T. HARP is an ATP-driven annealing helicase. Science 2008, 322:748-750.
82. Zhang Z., Fan H.Y., Goldman J.A., Kingston R.E. Homology-driven chromatin remodeling by human RAD54. Nature Structural & Molecular Biology 2007, 14:397-405.