Involvement of Global Genome Repair, Transcription Coupled Repair, and Chromatin Remodeling in UV DNA Damage Response Changes during Development
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.
Vyšlo v časopise:
Involvement of Global Genome Repair, Transcription Coupled Repair, and Chromatin Remodeling in UV DNA Damage Response Changes during Development. PLoS Genet 6(5): e32767. doi:10.1371/journal.pgen.1000941
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1000941
Souhrn
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.
Zdroje
1. HoeijmakersJH
2001 Genome maintenance mechanisms for preventing cancer. Nature 411 366 374
2. NouspikelT
2009 DNA repair in mammalian cells : Nucleotide excision repair: variations on versatility. Cell Mol Life Sci 66 994 1009
3. FousteriM
VermeulenW
van ZeelandAA
MullendersLH
2006 Cockayne syndrome A and B proteins differentially regulate recruitment of chromatin remodeling and repair factors to stalled RNA polymerase II in vivo. Mol Cell 23 471 482
4. TroelstraC
van GoolA
de WitJ
VermeulenW
BootsmaD
1992 ERCC6, a member of a subfamily of putative helicases, is involved in Cockayne's syndrome and preferential repair of active genes. Cell 71 939 953
5. HenningKA
LiL
IyerN
McDanielLD
ReaganMS
1995 The Cockayne syndrome group A gene encodes a WD repeat protein that interacts with CSB protein and a subunit of RNA polymerase II TFIIH. Cell 82 555 564
6. SvejstrupJQ
2007 Contending with transcriptional arrest during RNAPII transcript elongation. Trends Biochem Sci 32 165 171
7. ArakiM
MasutaniC
TakemuraM
UchidaA
SugasawaK
2001 Centrosome protein centrin 2/caltractin 1 is part of the xeroderma pigmentosum group C complex that initiates global genome nucleotide excision repair. J Biol Chem 276 18665 18672
8. SugasawaK
NgJM
MasutaniC
IwaiS
van der SpekPJ
1998 Xeroderma pigmentosum group C protein complex is the initiator of global genome nucleotide excision repair. Mol Cell 2 223 232
9. WakasugiM
KawashimaA
MoriokaH
LinnS
SancarA
2002 DDB accumulates at DNA damage sites immediately after UV irradiation and directly stimulates nucleotide excision repair. J Biol Chem 277 1637 1640
10. VolkerM
MoneMJ
KarmakarP
van HoffenA
SchulW
2001 Sequential assembly of the nucleotide excision repair factors in vivo. Mol Cell 8 213 224
11. GuzderSN
SungP
PrakashL
PrakashS
1998 Affinity of yeast nucleotide excision repair factor 2, consisting of the Rad4 and Rad23 proteins, for ultraviolet damaged DNA. J Biol Chem 273 31541 31546
12. NgJM
VermeulenW
van der HorstGT
BerginkS
SugasawaK
2003 A novel regulation mechanism of DNA repair by damage-induced and RAD23-dependent stabilization of xeroderma pigmentosum group C protein. Genes Dev 17 1630 1645
13. ReardonJT
MuD
SancarA
1996 Overproduction, purification, and characterization of the XPC subunit of the human DNA repair excision nuclease. J Biol Chem 271 19451 19456
14. SugasawaK
MasutaniC
UchidaA
MaekawaT
van der SpekPJ
1996 HHR23B, a human Rad23 homolog, stimulates XPC protein in nucleotide excision repair in vitro. Mol Cell Biol 16 4852 4861
15. de BoerJ
HoeijmakersJH
2000 Nucleotide excision repair and human syndromes. Carcinogenesis 21 453 460
16. van GoolAJ
VerhageR
SwagemakersSM
van de PutteP
BrouwerJ
1994 RAD26, the functional S. cerevisiae homolog of the Cockayne syndrome B gene ERCC6. Embo J 13 5361 5369
17. LeeMH
AhnB
ChoiIS
KooHS
2002 The gene expression and deficiency phenotypes of Cockayne syndrome B protein in Caenorhabditis elegans. FEBS Lett 522 47 51
18. ParkHK
SuhD
HyunM
KooHS
AhnB
2004 A DNA repair gene of Caenorhabditis elegans: a homolog of human XPF. DNA Repair (Amst) 3 1375 1383
19. ParkHK
YookJS
KooHS
ChoiIS
AhnB
2002 The Caenorhabditis elegans XPA homolog of human XPA. Mol Cells 14 50 55
20. AstinJW
O'NeilNJ
KuwabaraPE
2008 Nucleotide excision repair and the degradation of RNA pol II by the Caenorhabditis elegans XPA and Rsp5 orthologues, RAD-3 and WWP-1. DNA Repair (Amst) 7 267 280
21. HartmanPS
HermanRK
1982 Radiation-sensitive mutants of Caenorhabditis elegans. Genetics 102 159 178
22. StergiouL
DoukoumetzidisK
SendoelA
HengartnerMO
2007 The nucleotide excision repair pathway is required for UV-C-induced apoptosis in Caenorhabditis elegans. Cell Death Differ 14 1129 1138
23. YoudsJL
O'NeilNJ
RoseAM
2006 Homologous recombination is required for genome stability in the absence of DOG-1 in Caenorhabditis elegans. Genetics 173 697 708
24. MasutaniC
ArakiM
SugasawaK
van der SpekPJ
YamadaA
1997 Identification and characterization of XPC-binding domain of hHR23B. Mol Cell Biol 17 6915 6923
25. NishiR
OkudaY
WatanabeE
MoriT
IwaiS
2005 Centrin 2 stimulates nucleotide excision repair by interacting with xeroderma pigmentosum group C protein. Mol Cell Biol 25 5664 5674
26. MasutaniC
SugasawaK
YanagisawaJ
SonoyamaT
UiM
1994 Purification and cloning of a nucleotide excision repair complex involving the xeroderma pigmentosum group C protein and a human homologue of yeast RAD23. Embo J 13 1831 1843
27. GartnerA
MilsteinS
AhmedS
HodgkinJ
HengartnerMO
2000 A conserved checkpoint pathway mediates DNA damage–induced apoptosis and cell cycle arrest in C. elegans. Mol Cell 5 435 443
28. GumiennyTL
LambieE
HartwiegE
HorvitzHR
HengartnerMO
1999 Genetic control of programmed cell death in the Caenorhabditis elegans hermaphrodite germline. Development 126 1011 1022
29. HubbardEJ
GreensteinD
2000 The Caenorhabditis elegans gonad: a test tube for cell and developmental biology. Dev Dyn 218 2 22
30. HartmanPS
1984 UV irradiation of wild type and radiation-sensitive mutants of the nematode Caenorhabditis elegans: fertilities, survival, and parental effects. Photochem Photobiol 39 169 175
31. CadetJ
SageE
DoukiT
2005 Ultraviolet radiation-mediated damage to cellular DNA. Mutat Res 571 3 17
32. WadeSL
PooreyK
BekiranovS
AubleDT
2009 The Snf1 kinase and proteasome-associated Rad23 regulate UV-responsive gene expression. Embo J 28 2919 2931
33. DantumaNP
HeinenC
HoogstratenD
2009 The ubiquitin receptor Rad23: at the crossroads of nucleotide excision repair and proteasomal degradation. DNA Repair (Amst) 8 449 460
34. LuijsterburgMS
DinantC
LansH
StapJ
WiernaszE
2009 Heterochromatin protein 1 is recruited to various types of DNA damage. J Cell Biol 185 577 586
35. DinantC
HoutsmullerAB
VermeulenW
2008 Chromatin structure and DNA damage repair. Epigenetics Chromatin 1 9
36. WangGG
AllisCD
ChiP
2007 Chromatin remodeling and cancer, Part II: ATP-dependent chromatin remodeling. Trends Mol Med 13 373 380
37. CitterioE
Van Den BoomV
SchnitzlerG
KanaarR
BonteE
2000 ATP-dependent chromatin remodeling by the Cockayne syndrome B DNA repair-transcription-coupling factor. Mol Cell Biol 20 7643 7653
38. AndersenEC
LuX
HorvitzHR
2006 C. elegans ISWI and NURF301 antagonize an Rb-like pathway in the determination of multiple cell fates. Development 133 2695 2704
39. ShiY
MelloC
1998 A CBP/p300 homolog specifies multiple differentiation pathways in Caenorhabditis elegans. Genes Dev 12 943 955
40. HakimiMA
BocharDA
SchmiesingJA
DongY
BarakOG
2002 A chromatin remodelling complex that loads cohesin onto human chromosomes. Nature 418 994 998
41. ChanRC
ChanA
JeonM
WuTF
PasqualoneD
2003 Chromosome cohesion is regulated by a clock gene paralogue TIM-1. Nature 423 1002 1009
42. SawaH
KouikeH
OkanoH
2000 Components of the SWI/SNF complex are required for asymmetric cell division in C. elegans. Mol Cell 6 617 624
43. CuiM
FayDS
HanM
2004 lin-35/Rb cooperates with the SWI/SNF complex to control Caenorhabditis elegans larval development. Genetics 167 1177 1185
44. MuellerJP
SmerdonMJ
1996 Rad23 is required for transcription-coupled repair and efficient overrall repair in Saccharomyces cerevisiae. Mol Cell Biol 16 2361 2368
45. VerhageR
ZeemanAM
de GrootN
GleigF
BangDD
1994 The RAD7 and RAD16 genes, which are essential for pyrimidine dimer removal from the silent mating type loci, are also required for repair of the nontranscribed strand of an active gene in Saccharomyces cerevisiae. Mol Cell Biol 14 6135 6142
46. MatsumotoM
YaginumaK
IgarashiA
ImuraM
HasegawaM
2007 Perturbed gap-filling synthesis in nucleotide excision repair causes histone H2AX phosphorylation in human quiescent cells. J Cell Sci 120 1104 1112
47. de WaardH
SonneveldE
de WitJ
Esveldt-van LangeR
HoeijmakersJH
2008 Cell-type-specific consequences of nucleotide excision repair deficiencies: Embryonic stem cells versus fibroblasts. DNA Repair (Amst) 7 1659 1669
48. ConfortiG
NardoT
D'IncalciM
StefaniniM
2000 Proneness to UV-induced apoptosis in human fibroblasts defective in transcription coupled repair is associated with the lack of Mdm2 transactivation. Oncogene 19 2714 2720
49. LjungmanM
ZhangF
1996 Blockage of RNA polymerase as a possible trigger for u.v. light-induced apoptosis. Oncogene 13 823 831
50. ClejanI
BoerckelJ
AhmedS
2006 Developmental modulation of nonhomologous end joining in Caenorhabditis elegans. Genetics 173 1301 1317
51. NouspikelT
HanawaltPC
2000 Terminally differentiated human neurons repair transcribed genes but display attenuated global DNA repair and modulation of repair gene expression. Mol Cell Biol 20 1562 1570
52. MeyerJN
BoydWA
AzzamGA
HaugenAC
FreedmanJH
2007 Decline of nucleotide excision repair capacity in aging Caenorhabditis elegans. Genome Biol 8 R70
53. SulstonJE
SchierenbergE
WhiteJG
ThomsonJN
1983 The embryonic cell lineage of the nematode Caenorhabditis elegans. Dev Biol 100 64 119
54. StewartHI
RosenbluthRE
BaillieDL
1991 Most ultraviolet irradiation induced mutations in the nematode Caenorhabditis elegans are chromosomal rearrangements. Mutat Res 249 37 54
55. van HaaftenG
RomeijnR
PothofJ
KooleW
MullendersLH
2006 Identification of conserved pathways of DNA-damage response and radiation protection by genome-wide RNAi. Curr Biol 16 1344 1350
56. PothofJ
van HaaftenG
ThijssenK
KamathRS
FraserAG
2003 Identification of genes that protect the C. elegans genome against mutations by genome-wide RNAi. Genes Dev 17 443 448
57. UraK
ArakiM
SaekiH
MasutaniC
ItoT
2001 ATP-dependent chromatin remodeling facilitates nucleotide excision repair of UV-induced DNA lesions in synthetic dinucleosomes. Embo J 20 2004 2014
58. KimST
XuB
KastanMB
2002 Involvement of the cohesin protein, Smc1, in Atm-dependent and independent responses to DNA damage. Genes Dev 16 560 570
59. YazdiPT
WangY
ZhaoS
PatelN
LeeEY
2002 SMC1 is a downstream effector in the ATM/NBS1 branch of the human S-phase checkpoint. Genes Dev 16 571 582
60. Klochendler-YeivinA
PicarskyE
YanivM
2006 Increased DNA damage sensitivity and apoptosis in cells lacking the Snf5/Ini1 subunit of the SWI/SNF chromatin remodeling complex. Mol Cell Biol 26 2661 2674
61. GongF
FahyD
LiuH
WangW
SmerdonMJ
2008 Role of the mammalian SWI/SNF chromatin remodeling complex in the cellular response to UV damage. Cell Cycle 7 1067 1074
62. GongF
FahyD
SmerdonMJ
2006 Rad4–Rad23 interaction with SWI/SNF links ATP-dependent chromatin remodeling with nucleotide excision repair. Nat Struct Mol Biol 13 902 907
63. HaraR
SancarA
2002 The SWI/SNF chromatin-remodeling factor stimulates repair by human excision nuclease in the mononucleosome core particle. Mol Cell Biol 22 6779 6787
64. BrennerS
1974 The genetics of Caenorhabditis elegans. Genetics 77 71 94
65. HartmanPS
HeveloneJ
DwarakanathV
MitchellDL
1989 Excision repair of UV radiation-induced DNA damage in Caenorhabditis elegans. Genetics 122 379 385
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