#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

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

Štítky
Genetika Reprodukčná medicína

Článok vyšiel v časopise

PLOS Genetics


2010 Číslo 5
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Aktuální možnosti diagnostiky a léčby litiáz
nový kurz
Autori: MUDr. Tomáš Ürge, PhD.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#