Functional and mechanistic studies of XPC DNA-repair complex as transcriptional coactivator in embryonic stem cells

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 18, 2015, Pages E2317-E2326

  Cattoglio, Claudia ^a   Zhang, Elisa T ^a   Grubisic, Ivan ^a,b   Chiba, Kunitoshi ^a   Fong, Yick W ^c   Tjian, Robert ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

ChIP seq; Pluripotency; Protein protein interactions; RNA seq; Transcription

Indexed keywords

CALCIUM BINDING PROTEIN; CENTRIN EF HAND PROTEIN 2; NUCLEIC ACID BINDING PROTEIN; OCTAMER TRANSCRIPTION FACTOR 4; RAD23 HOMOLOG B; TRANSCRIPTION FACTOR SOX2; UNCLASSIFIED DRUG; XERODERMA PIGMENTOSUM GROUP C PROTEIN; DNA BINDING PROTEIN; IMMUNOGLOBULIN G; PROTEIN BINDING; RAD23B PROTEIN, MOUSE; SOX2 PROTEIN, MOUSE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR SOX; XPC PROTEIN, HUMAN;

ANIMAL CELL; ARTICLE; BINDING SITE; COMPLEX FORMATION; DNA REPAIR; EMBRYONIC STEM CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; TRANSCRIPTION INITIATION; ANIMAL; CELL DIFFERENTIATION; CELL LINEAGE; CHEMISTRY; CYTOLOGY; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENOME; HEK293 CELL LINE; HUMAN; KNOCKOUT MOUSE; LENTIVIRINAE; METABOLISM; PLURIPOTENT STEM CELL;

MURINAE;

ANIMALS; BINDING SITES; CELL DIFFERENTIATION; CELL LINEAGE; DNA REPAIR; DNA-BINDING PROTEINS; EMBRYONIC STEM CELLS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENOME; HEK293 CELLS; HUMANS; IMMUNOGLOBULIN G; LENTIVIRUS; MICE; MICE, KNOCKOUT; PLURIPOTENT STEM CELLS; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; SOXB1 TRANSCRIPTION FACTORS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 84928964006     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1505569112     Document Type: Article

References (73)

1. Hirai H, Karian P, Kikyo N (2011) Regulation of embryonic stem cell self-renewal and pluripotency by leukaemia inhibitory factor. Biochem J 438(1):11-23.
2. Kunath T, et al. (2007) FGF stimulation of the Erk1/2 signalling cascade triggers transition of pluripotent embryonic stem cells from self-renewal to lineage commitment. Development 134(16):2895-2902.
3. Hackett JA, Surani MA (2014) Regulatory principles of pluripotency: From the ground state up. Cell Stem Cell 15(4):416-430.
4. Martello G, Smith A (2014) The nature of embryonic stem cells. Annu Rev Cell Dev Biol 30:647-675.
5. Fong YW, Cattoglio C, Yamaguchi T, Tjian R (2012) Transcriptional regulation by coactivators in embryonic stem cells. Trends Cell Biol 22(6):292-298.
6. Ghosal S, Das S, Chakrabarti J (2013) Long noncoding RNAs: New players in the molecular mechanism for maintenance and differentiation of pluripotent stem cells. Stem Cells Dev 22(16):2240-2253.
7. Orkin SH, Hochedlinger K (2011) Chromatin connections to pluripotency and cellular reprogramming. Cell 145(6):835-850.
8. Liu Z, Scannell DR, Eisen MB, Tjian R (2011) Control of embryonic stem cell lineage commitment by core promoter factor, TAF3. Cell 146(5):720-731.
9. Maston GA, et al. (2012) Non-canonical TAF complexes regulate active promoters in human embryonic stem cells. eLife 1:e00068.
10. Pijnappel WW, et al. (2013) A central role for TFIID in the pluripotent transcription circuitry. Nature 495(7442):516-519.
11. Fong YW, et al. (2011) A DNA repair complex functions as an Oct4/Sox2 coactivator in embryonic stem cells. Cell 147(1):120-131.
12. Fong YW, Ho JJ, Inouye C, Tjian R (2014) The dyskerin ribonucleoprotein complex as an OCT4/SOX2 coactivator in embryonic stem cells. eLife 3:3.
13. Sugasawa K, et al. (1998) Xeroderma pigmentosum group C protein complex is the initiator of global genome nucleotide excision repair. Mol Cell 2(2):223-232.
14. Fousteri M, Mullenders LH (2008) Transcription-coupled nucleotide excision repair in mammalian cells: Molecular mechanisms and biological effects. Cell Res 18(1): 73-84.
15. Ng JM, et al. (2003) A novel regulation mechanism of DNA repair by damage-induced and RAD23-dependent stabilization of xeroderma pigmentosum group C protein. Genes Dev 17(13):1630-1645.
16. Bergink S, et al. (2012) Recognition of DNA damage by XPC coincides with disruption of the XPC-RAD23 complex. J Cell Biol 196(6):681-688.
17. Nishi R, et al. (2005) Centrin 2 stimulates nucleotide excision repair by interacting with xeroderma pigmentosum group C protein. Mol Cell Biol 25(13):5664-5674.
18. Bunick CG, Miller MR, Fuller BE, Fanning E, Chazin WJ (2006) Biochemical and structural domain analysis of xeroderma pigmentosum complementation group C protein. Biochemistry 45(50):14965-14979.
19. Uchida A, et al. (2002) The carboxy-terminal domain of the XPC protein plays a crucial role in nucleotide excision repair through interactions with transcription factor IIH. DNA Repair (Amst) 1(6):449-461.
20. Le May N, Fradin D, Iltis I, Bougnères P, Egly JM (2012) XPG and XPF endonucleases trigger chromatin looping and DNA demethylation for accurate expression of activated genes. Mol Cell 47(4):622-632.
21. Le May N, et al. (2010) NER factors are recruited to active promoters and facilitate chromatin modification for transcription in the absence of exogenous genotoxic attack. Mol Cell 38(1):54-66.
22. Creyghton MP, et al. (2010) Histone H3K27ac separates active from poised enhancers and predicts developmental state. Proc Natl Acad Sci USA 107(50):21931-21936.
23. Kagey MH, et al. (2010) Mediator and cohesin connect gene expression and chromatin architecture. Nature 467(7314):430-435.
24. Marson A, et al. (2008) Connecting microRNA genes to the core transcriptional regulatory circuitry of embryonic stem cells. Cell 134(3):521-533.
25. Loh YH, et al. (2006) The Oct4 and Nanog transcription network regulates pluripotency in mouse embryonic stem cells. Nat Genet 38(4):431-440.
26. Chew JL, et al. (2005) Reciprocal transcriptional regulation of Pou5f1 and Sox2 via the Oct4/Sox2 complex in embryonic stem cells. Mol Cell Biol 25(14):6031-6046.
27. Chen J, et al. (2014) Single-molecule dynamics of enhanceosome assembly in embryonic stem cells. Cell 156(6):1274-1285.
28. Niwa H, Miyazaki J, Smith AG (2000) Quantitative expression of Oct-3/4 defines differentiation, dedifferentiation or self-renewal of ES cells. Nat Genet 24(4):372-376.
29. Fong H, Hohenstein KA, Donovan PJ (2008) Regulation of self-renewal and pluripotency by Sox2 in human embryonic stem cells. Stem Cells 26(8):1931-1938.
30. Adachi K, Suemori H, Yasuda SY, Nakatsuji N, Kawase E (2010) Role of SOX2 in maintaining pluripotency of human embryonic stem cells. Genes Cells 15(5):455-470.
31. Cinelli P, et al. (2008) Expression profiling in transgenic FVB/N embryonic stem cells overexpressing STAT3. BMC Dev Biol 8:57.
32. Ye S, Li P, Tong C, Ying QL (2013) Embryonic stem cell self-renewal pathways converge on the transcription factor Tfcp2l1. EMBO J 32(19):2548-2560.
33. Hall J, et al. (2009) Oct4 and LIF/Stat3 additively induce Krüppel factors to sustain embryonic stem cell self-renewal. Cell Stem Cell 5(6):597-609.
34. de Waard H, et al. (2008) Cell-type-specific consequences of nucleotide excision repair deficiencies: Embryonic stem cells versus fibroblasts. DNA Repair (Amst) 7(10):1659-1669.
35. Prabhu VV, et al. (2012) Therapeutic targeting of the p53 pathway in cancer stem cells. Expert Opin Ther Targets 16(12):1161-1174.
36. Matoba R, et al. (2006) Dissecting Oct3/4-regulated gene networks in embryonic stem cells by expression profiling. PLoS ONE 1:e26.
37. Ziani S, et al. (2014) Sequential and ordered assembly of a large DNA repair complex on undamaged chromatin. J Cell Biol 206(5):589-598.
38. Yasuda G, et al. (2007) In vivo destabilization and functional defects of the xeroderma pigmentosum C protein caused by a pathogenic missense mutation. Mol Cell Biol 27(19):6606-6614.
39. Araújo SJ, Nigg EA, Wood RD (2001) Strong functional interactions of TFIIH with XPC and XPG in human DNA nucleotide excision repair, without a preassembled repairosome. Mol Cell Biol 21(7):2281-2291.
40. Koch F, et al. (2011) Transcription initiation platforms and GTF recruitment at tissue-specific enhancers and promoters. Nat Struct Mol Biol 18(8):956-963.
41. Ito S, Yamane M, Ohtsuka S, Niwa H (2014) The C-terminal region of Xpc is dispensable for the transcriptional activity of Oct3/4 in mouse embryonic stem cells. FEBS Lett 588(7):1128-1135.
42. Sands AT, Abuin A, Sanchez A, Conti CJ, Bradley A (1995) High susceptibility to ultraviolet-induced carcinogenesis in mice lacking XPC. Nature 377(6545):162-165.
43. Cheo DL, et al. (1997) Characterization of defective nucleotide excision repair in XPC mutant mice. Mutat Res 374(1):1-9.
44. Dantuma NP, Heinen C, Hoogstraten D (2009) The ubiquitin receptor Rad23: At the crossroads of nucleotide excision repair and proteasomal degradation. DNA Repair (Amst) 8(4):449-460.
45. Durairaj G, Kaiser P (2014) The 26S proteasome and initiation of gene transcription. Biomolecules 4(3):827-847.
46. Szutorisz H, Georgiou A, Tora L, Dillon N (2006) The proteasome restricts permissive transcription at tissue-specific gene loci in embryonic stem cells. Cell 127(7):1375-1388.
47. Wade SL, Poorey K, Bekiranov S, Auble DT (2009) The Snf1 kinase and proteasome-associated Rad23 regulate UV-responsive gene expression. EMBO J 28(19):2919-2931.
48. Ng JM, et al. (2002) Developmental defects and male sterility in mice lacking the ubiquitin-like DNA repair gene mHR23B. Mol Cell Biol 22(4):1233-1245.
49. Bergink S, et al. (2013) Erythropoietic defect associated with reduced cell proliferation in mice lacking the 26S proteasome shuttling factor Rad23b. Mol Cell Biol 33(19):3879-3892.
50. Ng SY, Bogu GK, Soh BS, Stanton LW (2013) The long noncoding RNA RMST interacts with SOX2 to regulate neurogenesis. Mol Cell 51(3):349-359.
51. Cech TR, Steitz JA (2014) The noncoding RNA revolution-trashing old rules to forge new ones. Cell 157(1):77-94.
52. Schwartz JC, Wang X, Podell ER, Cech TR (2013) RNA seeds higher-order assembly of FUS protein. Cell Reports 5(4):918-925.
53. Kwon I, et al. (2013) Phosphorylation-regulated binding of RNA polymerase II to fibrous polymers of low-complexity domains. Cell 155(5):1049-1060.
54. Davidovich C, et al. (2015) Toward a consensus on the binding specificity and promiscuity of PRC2 for RNA. Mol Cell 57(3):552-558.
55. Fazzio TG, Huff JT, Panning B (2008) An RNAi screen of chromatin proteins identifies Tip60-p400 as a regulator of embryonic stem cell identity. Cell 134(1):162-174.
56. Ang YS, et al. (2011) Wdr5 mediates self-renewal and reprogramming via the embryonic stem cell core transcriptional network. Cell 145(2):183-197.
57. Ding L, et al. (2009) A genome-scale RNAi screen for Oct4 modulators defines a role of the Paf1 complex for embryonic stem cell identity. Cell Stem Cell 4(5):403-415.
58. Thompson NE, Steinberg TH, Aronson DB, Burgess RR (1989) Inhibition of in vivo and in vitro transcription by monoclonal antibodies prepared against wheat germ RNA polymerase II that react with the heptapeptide repeat of eukaryotic RNA polymerase II. J Biol Chem 264(19):11511-11520.
59. Huang W, Sherman BT, Lempicki RA (2009) Bioinformatics enrichment tools: Paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res 37(1):1-13.
60. Huang W, Sherman BT, Lempicki RA (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4(1):44-57.
61. Blankenberg D, et al. (2010) Galaxy: a web-based genome analysis tool for experimentalists. Curr Protoc Mol Biol Chapter 19:Unit 19.10.11-21.
62. Giardine B, et al. (2005) Galaxy: A platform for interactive large-scale genome analysis. Genome Res 15(10):1451-1455.
63. Goecks J, Nekrutenko A, Taylor J; Galaxy Team (2010) Galaxy: A comprehensive approach for supporting accessible, reproducible, and transparent computational research in the life sciences. Genome Biol 11(8):R86.
64. Dull T, et al. (1998) A third-generation lentivirus vector with a conditional packaging system. J Virol 72(11):8463-8471.
65. Amendola M, Venneri MA, Biffi A, Vigna E, Naldini L (2005) Coordinate dual-gene transgenesis by lentiviral vectors carrying synthetic bidirectional promoters. Nat Biotechnol 23(1):108-116.
66. Lombardo A, et al. (2007) Gene editing in human stem cells using zinc finger nucleases and integrase-defective lentiviral vector delivery. Nat Biotechnol 25(11):1298-1306.
67. Ortolan TG, Chen L, Tongaonkar P, Madura K (2004) Rad23 stabilizes Rad4 from degradation by the Ub/proteasome pathway. Nucleic Acids Res 32(22):6490-6500.
68. Trapnell C, et al. (2012) Differential gene and transcript expression analysis of RNAseq experiments with TopHat and Cufflinks. Nat Protoc 7(3):562-578.
69. Edgar R, Domrachev M, Lash AE (2002) Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res 30(1):207-210.
70. Chen X, et al. (2008) Integration of external signaling pathways with the core transcriptional network in embryonic stem cells. Cell 133(6):1106-1117.
71. Thorvaldsdóttir H, Robinson JT, Mesirov JP (2013) Integrative Genomics Viewer (IGV): High-performance genomics data visualization and exploration. Brief Bioinform 14(2):178-192.
72. Robinson JT, et al. (2011) Integrative genomics viewer. Nat Biotechnol 29(1):24-26.
73. Min JH, Pavletich NP (2007) Recognition of DNA damage by the Rad4 nucleotide excision repair protein. Nature 449(7162):570-575.