title: Involvement of global genome repair, transcription coupled repair, and chromatin remodeling in UV DNA damage response changes during development.
abstract: Nucleotide Excision Repair (NER), which removes a variety of helix-distorting lesions from DNA, is initiated by two distinct DNA damage-sensing mechanisms. Transcription Coupled Repair (TCR) removes damage from the active strand of transcribed genes and depends on the SWI/SNF family protein CSB. Global Genome Repair (GGR) removes damage present elsewhere in the genome and depends on damage recognition by the XPC/RAD23/Centrin2 complex. Currently, it is not well understood to what extent both pathways contribute to genome maintenance and cell survival in a developing organism exposed to UV light. Here, we show that eukaryotic NER, initiated by two distinct subpathways, is well conserved in the nematode Caenorhabditis elegans. In C. elegans, involvement of TCR and GGR in the UV-induced DNA damage response changes during development. In germ cells and early embryos, we find that GGR is the major pathway contributing to normal development and survival after UV irradiation, whereas in later developmental stages TCR is predominantly engaged. Furthermore, we identify four ISWI/Cohesin and four SWI/SNF family chromatin remodeling factors that are implicated in the UV damage response in a developmental stage dependent manner. These in vivo studies strongly suggest that involvement of different repair pathways and chromatin remodeling proteins in UV-induced DNA repair depends on developmental stage of cells.
authors.affiliation: Department of Genetics, Medical Genetics Center, Erasmus MC, Rotterdam, The Netherlands.
authors.forename: Hannes
authors.initials: H
authors.lastname: Lans
authors.forename: Jurgen A
authors.initials: JA
authors.lastname: Marteijn
authors.forename: Björn
authors.initials: B
authors.lastname: Schumacher
authors.forename: Jan H J
authors.initials: JH
authors.lastname: Hoeijmakers
authors.forename: Gert
authors.initials: G
authors.lastname: Jansen
authors.forename: Wim
authors.initials: W
authors.lastname: Vermeulen
mesh_terms: D000818:Animals; D017173:Caenorhabditis elegans / Q000235:genetics* / Q000254:growth & development* / Q000378:metabolism; D029742:Caenorhabditis elegans Proteins / Q000235:genetics / Q000378:metabolism; D042002:Chromatin Assembly and Disassembly / Q000528:radiation effects*; D004249:DNA Damage / Q000528:radiation effects*; D053843:DNA Mismatch Repair / Q000528:radiation effects*; D005260:Female; D018507:Gene Expression Regulation, Developmental / Q000528:radiation effects; D008297:Male; D014466:Ultraviolet Rays
chemical_list: D029742:Caenorhabditis elegans Proteins
references.citation: EMBO J. 2001 Apr 17;20(8):2004-14
references.pmid: 11296233
references.citation: Mol Cell. 2001 Jul;8(1):213-24
references.pmid: 11511374
references.citation: Dev Dyn. 2000 May;218(1):2-22
references.pmid: 10822256
references.citation: J Biol Chem. 2001 Jun 1;276(22):18665-72
references.pmid: 11279143
references.citation: Genetics. 2006 Jun;173(2):697-708
references.pmid: 16547095
references.citation: Mol Cell Biol. 2006 Apr;26(7):2661-74
references.pmid: 16537910
references.citation: DNA Repair (Amst). 2004 Oct 5;3(10):1375-83
references.pmid: 15336632
references.citation: Mol Cell Biol. 1996 May;16(5):2361-8
references.pmid: 8628303
references.citation: Mol Cell. 2006 Aug;23(4):471-82
references.pmid: 16916636
references.citation: Genetics. 1982 Oct;102(2):159-78
references.pmid: 7152245
references.citation: FEBS Lett. 2002 Jul 3;522(1-3):47-51
references.pmid: 12095617
references.citation: Nature. 2003 Jun 26;423(6943):1002-9
references.pmid: 12827206
references.citation: Mol Cell Biol. 1996 Sep;16(9):4852-61
references.pmid: 8756644
references.citation: EMBO J. 1994 Nov 15;13(22):5361-9
references.pmid: 7957102
references.citation: Trends Biochem Sci. 2007 Apr;32(4):165-71
references.pmid: 17349792
references.citation: Mol Cell Biol. 2000 Mar;20(5):1562-70
references.pmid: 10669734
references.citation: Mol Cell Biol. 1997 Dec;17(12):6915-23
references.pmid: 9372923
references.citation: Mol Cell Biol. 2002 Oct;22(19):6779-87
references.pmid: 12215535
references.citation: Carcinogenesis. 2000 Mar;21(3):453-60
references.pmid: 10688865
references.citation: DNA Repair (Amst). 2008 Feb 1;7(2):267-80
references.pmid: 18053776
references.citation: DNA Repair (Amst). 2008 Oct 1;7(10):1659-69
references.pmid: 18634906
references.citation: Mol Cell Biol. 2005 Jul;25(13):5664-74
references.pmid: 15964821
references.citation: Genes Dev. 1998 Apr 1;12(7):943-55
references.pmid: 9531533
references.citation: J Cell Biol. 2009 May 18;185(4):577-86
references.pmid: 19451271
references.citation: Genetics. 2004 Jul;167(3):1177-85
references.pmid: 15280233
references.citation: Cell Mol Life Sci. 2009 Mar;66(6):994-1009
references.pmid: 19153657
references.citation: Mutat Res. 1991 Jul;249(1):37-54
references.pmid: 2067542
references.citation: Trends Mol Med. 2007 Sep;13(9):373-80
references.pmid: 17822959
references.citation: Cell. 1995 Aug 25;82(4):555-64
references.pmid: 7664335
references.citation: Genes Dev. 2003 Feb 15;17(4):443-8
references.pmid: 12600937
references.citation: J Biol Chem. 1998 Nov 20;273(47):31541-6
references.pmid: 9813069
references.citation: Oncogene. 1996 Aug 15;13(4):823-31
references.pmid: 8761304
references.citation: Photochem Photobiol. 1984 Feb;39(2):169-75
references.pmid: 6709723
references.citation: Mol Cell Biol. 2000 Oct;20(20):7643-53
references.pmid: 11003660
references.citation: EMBO J. 1994 Apr 15;13(8):1831-43
references.pmid: 8168482
references.citation: Dev Biol. 1983 Nov;100(1):64-119
references.pmid: 6684600
references.citation: J Biol Chem. 1996 Aug 9;271(32):19451-6
references.pmid: 8702634
references.citation: Mol Cell. 2000 Sep;6(3):617-24
references.pmid: 11030341
references.citation: Mutat Res. 2005 Apr 1;571(1-2):3-17
references.pmid: 15748634
references.citation: Nature. 2002 Aug 29;418(6901):994-8
references.pmid: 12198550
references.citation: Oncogene. 2000 May 18;19(22):2714-20
references.pmid: 10851071
references.citation: J Biol Chem. 2002 Jan 18;277(3):1637-40
references.pmid: 11705987
references.citation: Cell Cycle. 2008 Apr 15;7(8):1067-74
references.pmid: 18414052
references.citation: Nat Struct Mol Biol. 2006 Oct;13(10):902-7
references.pmid: 17013386
references.citation: Genetics. 1974 May;77(1):71-94
references.pmid: 4366476
references.citation: Genetics. 2006 Jul;173(3):1301-17
references.pmid: 16702421
references.citation: DNA Repair (Amst). 2009 Apr 5;8(4):449-60
references.pmid: 19223247
references.citation: EMBO J. 2009 Oct 7;28(19):2919-31
references.pmid: 19680226
references.citation: Development. 2006 Jul;133(14):2695-704
references.pmid: 16774993
references.citation: Genome Biol. 2007;8(5):R70
references.pmid: 17472752
references.citation: Mol Cell. 2000 Mar;5(3):435-43
references.pmid: 10882129
references.citation: Cell. 1992 Dec 11;71(6):939-53
references.pmid: 1339317
references.citation: Genes Dev. 2002 Mar 1;16(5):571-82
references.pmid: 11877377
references.citation: Genes Dev. 2002 Mar 1;16(5):560-70
references.pmid: 11877376
references.citation: Cell Death Differ. 2007 Jun;14(6):1129-38
references.pmid: 17347667
references.citation: Nature. 2001 May 17;411(6835):366-74
references.pmid: 11357144
references.citation: Genes Dev. 2003 Jul 1;17(13):1630-45
references.pmid: 12815074
references.citation: Mol Cell Biol. 1994 Sep;14(9):6135-42
references.pmid: 8065346
references.citation: Development. 1999 Feb;126(5):1011-22
references.pmid: 9927601
references.citation: Mol Cells. 2002 Aug 31;14(1):50-5
references.pmid: 12243352
references.citation: J Cell Sci. 2007 Mar 15;120(Pt 6):1104-12
references.pmid: 17327276
references.citation: Curr Biol. 2006 Jul 11;16(13):1344-50
references.pmid: 16824923
references.citation: Genetics. 1989 Jun;122(2):379-85
references.pmid: 2767423
references.citation: Epigenetics Chromatin. 2008 Nov 12;1(1):9
references.pmid: 19014481
references.citation: Mol Cell. 1998 Aug;2(2):223-32
references.pmid: 9734359