#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Actin-Related Protein Arp6 Influences H2A.Z-Dependent and -Independent Gene Expression and Links Ribosomal Protein Genes to Nuclear Pores


Actin-related proteins are ubiquitous components of chromatin remodelers and are conserved from yeast to man. We have examined the role of the budding yeast actin-related protein Arp6 in gene expression, both as a component of the SWR1 complex (SWR-C) and in its absence. We mapped Arp6 binding sites along four yeast chromosomes using chromatin immunoprecipitation from wild-type and swr1 deleted (swr1Δ) cells. We find that a majority of Arp6 binding sites coincide with binding sites of Swr1, the catalytic subunit of SWR-C, and with the histone H2A variant Htz1 (H2A.Z) deposited by SWR-C. However, Arp6 binding detected at centromeres, the promoters of ribosomal protein (RP) genes, and some telomeres is independent of Swr1 and Htz1 deposition. Given that RP genes and telomeres both show association with the nuclear periphery, we monitored the ability of Arp6 to mediate the localization of chromatin to nuclear pores. Arp6 binding is sufficient to shift a randomly positioned locus to nuclear periphery, even in a swr1Δ strain. Arp6 is also necessary for the pore association of its targeted RP promoters possibly through cell cycle-dependent factors. Loss of Arp6, but not Htz1, leads to an up-regulation of these RP genes. In contrast, the pore-association of GAL1 correlates with Htz1 deposition, and loss of Arp6 reduces both GAL1 activation and peripheral localization. We conclude that Arp6 functions both together with the nucleosome remodeler Swr1 and also without it, to mediate Htz1-dependent and Htz1-independent binding of chromatin domains to nuclear pores. This association is shown to have modulating effects on gene expression.


Vyšlo v časopise: Actin-Related Protein Arp6 Influences H2A.Z-Dependent and -Independent Gene Expression and Links Ribosomal Protein Genes to Nuclear Pores. PLoS Genet 6(4): e32767. doi:10.1371/journal.pgen.1000910
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1000910

Souhrn

Actin-related proteins are ubiquitous components of chromatin remodelers and are conserved from yeast to man. We have examined the role of the budding yeast actin-related protein Arp6 in gene expression, both as a component of the SWR1 complex (SWR-C) and in its absence. We mapped Arp6 binding sites along four yeast chromosomes using chromatin immunoprecipitation from wild-type and swr1 deleted (swr1Δ) cells. We find that a majority of Arp6 binding sites coincide with binding sites of Swr1, the catalytic subunit of SWR-C, and with the histone H2A variant Htz1 (H2A.Z) deposited by SWR-C. However, Arp6 binding detected at centromeres, the promoters of ribosomal protein (RP) genes, and some telomeres is independent of Swr1 and Htz1 deposition. Given that RP genes and telomeres both show association with the nuclear periphery, we monitored the ability of Arp6 to mediate the localization of chromatin to nuclear pores. Arp6 binding is sufficient to shift a randomly positioned locus to nuclear periphery, even in a swr1Δ strain. Arp6 is also necessary for the pore association of its targeted RP promoters possibly through cell cycle-dependent factors. Loss of Arp6, but not Htz1, leads to an up-regulation of these RP genes. In contrast, the pore-association of GAL1 correlates with Htz1 deposition, and loss of Arp6 reduces both GAL1 activation and peripheral localization. We conclude that Arp6 functions both together with the nucleosome remodeler Swr1 and also without it, to mediate Htz1-dependent and Htz1-independent binding of chromatin domains to nuclear pores. This association is shown to have modulating effects on gene expression.


Zdroje

1. SpectorDL

2003 The dynamics of chromosome organization and gene regulation. Annu Rev Biochem 72 573 608

2. TaddeiA

HedigerF

NeumannFR

BauerC

GasserSM

2004 Separation of silencing from perinuclear anchoring functions in yeast Ku80, Sir4 and Esc1 proteins. EMBO J 23 1301 1312

3. SchneiderR

GrosschedlR

2007 Dynamics and interplay of nuclear architecture, genome organization, and gene expression. Genes Dev 21 3027 3043

4. AkhtarA

GasserS

2007 The nuclear envelope and transcriptional control. Nature Rev 8 507 517

5. BricknerJH

WalterP

2004 Gene recruitment of the activated INO1 locus to the nuclear membrane. PLoS Biol 2 e342 doi:10.1371/journal.pbio.0020342

6. SchmidM

AribG

LaemmliC

NishikawaJ

DurusselT

2006 Nup-PI: the nucleopore-promoter interaction of genes in yeast. Mol Cell 21 379 391

7. TaddeiA

Van HouweG

HedigerF

KalckV

CubizollesF

2006 Nuclear pore association confers optimal expression levels for an inducible yeast gene. Nature 441 774 778

8. MendjanS

TaipaleM

KindJ

HolzH

GebhardtP

2006 Nuclear pore components are involved in the transcriptional regulation of dosage compensation in Drosophila. Mol Cell 21 811 823

9. CasolariJM

BrownCR

KomiliS

WestJ

HieronymusH

SilverPA

2004 Genome-wide localization of the nuclear transport machinery couples transcriptional status and nuclear organization. Cell 117 427 439

10. PedersonT

AebiU

2005 Nuclear actin extends, with no contraction in sight. Mol Biol Cell 16 5055 5060

11. ChuangCH

CarpenterAE

FuchsovaB

JohnsonT

de LanerolleP

2006 Long-range directional movement of an interphase chromosome site. Curr Biol 16 825 831

12. HofmannWA

de LanerolleP

2006 Nuclear actin: to polymerize or not to polymerize. J Cell Biol 172 495 496

13. HofmannWA

JohnsonT

KlapczynskiM

FanJL

de LanerolleP

2006 From transcription to transport: emerging roles for nuclear myosin I. Biochem Cell Biol 84 418 426

14. DundrM

OspinaJK

SungMH

JohnS

UpenderM

2007 Actin-dependent intranuclear repositioning of an active gene locus in vivo. J Cell Biol 179 1095 1103

15. YooY

WuX

GuanJL

2007 A novel role of the actin-nucleating Arp2/3 complex in the regulation of RNA polymerase II-dependent transcription. J Biol Chem 282 7616 7623

16. HuQ

KwonYS

NunezE

CardamoneMD

HuttKR

OhgiKA

2008 Enhancing nuclear receptor-induced transcription requires nuclear motor and LSD1-dependent gene networking in interchromatin granules. Proc Natl Acad Sci U S A 105 19199 19204

17. LuthraR

KerrSC

HarremanMT

ApponiLH

FaskenMB

2007 Actively transcribed GAL genes can be physically linked to the nuclear pore by the SAGA chromatin modifying complex. J Biol Chem 282 3042 3049

18. PochO

WinsorB

1997 Who's who among the Saccharomyces cerevisiae actin-related proteins? A classification and nomenclature proposal for a large family. Yeast 13 1053 1058

19. MullerJ

OmaY

VallarL

FriederichE

PochO

2005 Sequence and Comparative Genomic Analysis of Actin-related Proteins. Mol Biol Cell 16 5736 5748

20. WeberV

HarataM

HauserH

WintersbergerU

1995 The actin-related protein Act3p of Saccharomyces cerevisiae is located in the nucleus. Mol Biol Cell 6 1263 1270

21. GravaS

DumoulinP

MadaniaA

TarassovI

WinsorB

2000 Functional analysis of six genes from chromosomes XIV and XV of Saccharomyces cerevisiae reveals YOR145c as an essential gene and YNL059c/ARP5 as a strain-dependent essential gene encoding nuclear proteins. Yeast 16 1025 1033

22. HarataM

OmaY

TabuchiT

ZhangY

StillmanDJ

2000 Multiple actin-related proteins of Saccharomyces cerevisiae are present in the nucleus. J Biochem (Tokyo) 128 665 671

23. ChenM

ShenX

2007 Nuclear actin and actin-related proteins in chromatin dynamics. Curr Opin Cell Biol 19 326 330

24. KatoM

SasakiM

MizunoS

HarataM

2001 Novel actin-related proteins in vertebrates: similarities of structure and expression pattern to Arp6 localized on Drosophila heterochromatin. Gene 268 133 140

25. JinJ

CaiY

LiB

ConawayRC

WorkmanJL

2005 In and out: histone variant exchange in chromatin. Trends Biochem Sci 30 680 687

26. OhfuchiE

KatoM

SasakiM

SugimotoK

OmaY

2006 Vertebrate Arp6, a novel nuclear actin-related protein, interacts with heterochromatin protein 1. Eur J Cell Biol 85 411 421

27. CaiY

JinJ

FlorensL

SwansonSK

KuschT

2005 The mammalian YL1 protein is a shared subunit of the TRRAP/TIP60 histone acetyltransferase and SRCAP complexes. J Biol Chem 280 13665 13670

28. WuWH

AlamiS

LukE

WuCH

SenS

2005 Swc2 is a widely conserved H2AZ-binding module essential for ATP-dependent histone exchange. Nat Struct Mol Biol 12 1064 1071

29. KroganNJ

KeoghMC

DattaN

SawaC

RyanOW

2003 A Snf2 family ATPase complex required for recruitment of the histone H2A variant Htz1. Mol Cell 12 1565 1576

30. MizuguchiG

ShenX

LandryJ

WuWH

SenS

2004 ATP-driven exchange of histone H2AZ variant catalyzed by SWR1 chromatin remodeling complex. Science 303 343 348

31. AdamM

RobertF

LarochelleM

GaudreauL

2001 H2A.Z is required for global chromatin integrity and for recruitment of RNA polymerase II under specific conditions. Mol Cell Biol 21 6270 6279

32. GuillemetteB

BatailleAR

GevryN

AdamM

BlanchetteM

2005 Variant histone H2A.Z is globally localized to the promoters of inactive yeast genes and regulates nucleosome positioning. PLoS Biol 3 e384 doi:10.1371/journal.pbio.0030384

33. LiB

PattendenSG

LeeD

GutierrezJ

ChenJ

2005 Preferential occupancy of histone variant H2AZ at inactive promoters influences local histone modifications and chromatin remodeling. Proc Natl Acad Sci U S A 102 18385 18390

34. RaisnerRM

HartleyPD

MeneghiniMD

BaoMZ

LiuCL

2005 Histone variant H2A.Z marks the 5′ ends of both active and inactive genes in euchromatin. Cell 123 233 248

35. ZhangH

RobertsDN

CairnsBR

2005 Genome-wide dynamics of Htz1, a histone H2A variant that poises repressed/basal promoters for activation through histone loss. Cell 123 219 231

36. MillarCB

XuF

ZhangK

GrunsteinM

2006 Acetylation of H2AZ Lys 14 is associated with genome-wide gene activity in yeast. Genes Dev 20 711 722

37. MeneghiniMD

WuM

MadhaniHD

2003 Conserved histone variant H2A.Z protects euchromatin from the ectopic spread of silent heterochromatin. Cell 112 725 736

38. BabiarzJE

HalleyJE

RineJ

2006 Telomeric heterochromatin boundaries require NuA4- dependent acetylation of histone variant H2A.Z in Saccharomyces cerevisiae. Genes Dev 20 700 710

39. GalarneauL

NouraniA

BoudreaultAA

ZhangY

HeliotL

2000 Multiple links between the NuA4 histone acetyltransferase complex and epigenetic control of transcription. Mol Cell 5 927 937

40. SunadaR

GorzerI

OmaY

YoshidaT

SukaN

2005 The nuclear actin-related protein Act3p/Arp4p is involved in the dynamics of chromatin-modulating complexes. Yeast 22 753 768

41. KroganNJ

BaetzK

KeoghMC

DattaN

SawaC

2004 Regulation of chromosome stability by the histone H2A variant Htz1, the Swr1 chromatin remodeling complex, and the histone acetyltransferase NuA4. Proc Natl Acad Sci U S A 101 13513 13518

42. AoyamaN

OkaA

KitayamaK

KurumizakaH

HarataM

2008 The actin-related protein hArp8 accumulates on the mitotic chromosomes and functions in chromosome alignment. Exp Cell Res 314 859 868

43. KatouY

KanohY

BandoM

NoguchiH

TanakaH

2003 S-phase checkpoint proteins Tof1 and Mrc1 form a stable replication-pausing complex. Nature 424 1078 1083

44. WuWH

WuCH

LadurnerA

MizuguchiG

WeiD

2009 N terminus of Swr1 binds to histone H2AZ and provides a platform for subunit assembly in the chromatin remodeling complex. J Biol Chem 284 6200 6207

45. PaseroP

DunckerBP

SchwobE

GasserSM

1999 A role for the Cdc7 kinase regulatory subunit Dbf4p in the formation of initiation-competent origins of replication. Genes Dev 13 2159 2176

46. KoborMS

VenkatasubrahmanyamS

MeneghiniMD

GinJW

JenningsJL

2004 A protein complex containing the conserved Swi2/Snf2-related ATPase Swr1p deposits histone variant H2A.Z into euchromatin. PLoS Biol 2 e131 doi:10.1371/journal.pbio.0020131

47. GligorisT

ThireosG

TzamariasD

2007 The Tup1 corepressor directs Htz1 deposition at a specific promoter nucleosome marking the GAL1 gene for rapid activation. Mol Cell Biol 27 4198 4205

48. DoyeV

WepfR

HurtEC

1994 A novel nuclear pore protein Nup133p with distinct roles in poly(A)+ RNA transport and nuclear pore distribution. EMBO J 13 6062 6075

49. SchoberH

FerreiraH

KalckV

GehlenLR

GasserSM

2009 Yeast telomerase and the SUN domain protein Mps3 anchor telomeres and repress subtelomeric recombination. Genes Dev 23 928 938

50. HedigerF

NeumannFR

Van HouweG

DubranaK

GasserSM

2002 Live imaging of telomeres: yKu and Sir proteins define redundant telomere-anchoring pathways in yeast. Curr Biol 12 2076 2089

51. DieppoisG

IglesiasN

StutzF

2006 Cotranscriptional recruitment to the mRNA export receptor Mex67p contributes to nuclear pore anchoring of activated genes. Mol Cell Biol 26 7858 7870

52. VinciguerraP

IglesiasN

CamblongJ

ZenklusenD

StutzF

2005 Perinuclear Mlp proteins downregulate gene expression in response to a defect in mRNA export. EMBO J 24 813 823

53. OeffingerM

WeiKE

RogersR

DeGrasseJA

ChaitBT

2007 Comprehensive analysis of diverse ribonucleoprotein complexes. Nat Methods 4 951 956

54. ShiaWJ

LiB

WorkmanJL

2006 SAS-mediated acetylation of histone H4 Lys 16 is required for H2A.Z incorporation at subtelomeric regions in Saccharomyces cerevisiae. Genes Dev 20 2507 2512

55. MartinDE

PowersT

HallMN

2006 Regulation of ribosome biogenesis: where is TOR? Cell Metab 4 259 260

56. HallDB

WadeJT

StruhlK

2006 An HMG protein, Hmo1, associates with promoters of many ribosomal protein genes and throughout the rRNA gene locus in Saccharomyces cerevisiae. Mol Cell Biol 26 3672 3679

57. ZhaoY

McIntoshKB

RudraD

SchawalderS

ShoreD

2006 Fine-structure analysis of ribosomal protein gene transcription. Mol Cell Biol 26 4853 4862

58. CollinsSR

MillerKM

MaasNL

RoguevA

FillinghamJ

2007 Functional dissection of protein complexes involved in yeast chromosome biology using a genetic interaction map. Nature 446 806 810

59. KasaharaK

OhtsukiK

KiS

AoyamaK

TakahashiH

2007 Assembly of regulatory factors on rRNA and ribosomal protein genes in Saccharomyces cerevisiae. Mol Cell Biol 27 6686 6705

60. CabalGG

GenovesioA

Rodriguez-NavarroS

ZimmerC

GadalO

2006 SAGA interacting factors confine sub-diffusion of transcribed genes to the nuclear envelope. Nature 441 770 773

61. BricknerDG

CajigasI

Fondufe-MittendorfY

AhmedS

LeePC

2007 H2A.Z-mediated localization of genes at the nuclear periphery confers epigenetic memory of previous transcriptional state. PLoS Biol 5 e81 doi:10.1371/journal.pbio.0050081

62. DilworthDJ

TackettAJ

RogersRS

YiEC

ChristmasRH

2005 The mobile nucleoporin Nup2p and chromatin-bound Prp20p function in endogenous NPC-mediated transcriptional control. J Cell Biol 171 955 965

63. FischerT

StrasserK

RaczA

Rodriguez-NavarroS

OppizziM

2002 The mRNA export machinery requires the novel Sac3p-Thp1p complex to dock at the nucleoplasmic entrance of the nuclear pores. EMBO J 21 5843 5852

64. HieronymusH

SilverPA

2003 Genome-wide analysis of RNA-protein interactions illustrates specificity of the mRNA export machinery. Nat Genet 33 155 161

65. KroganNJ

CagneyG

YuH

ZhongG

GuoX

2006 Global landscape of protein complexes in the yeast Saccharomyces cerevisiae. Nature 440 637 643

66. ZhaoY

SohnJH

WarnerJR

2003 Autoregulation in the biosynthesis of ribosomes. Mol Cell Biol 23 699 707

67. PresuttiC

CiafréSA

BozzoniI

1991 The ribosomal protein L2 in S. cerevisiae controls the level of accumulation of its own mRNA. EMBO J 10 2215 2221

68. LiZ

PaulovichAG

WoolfordJLJr

1995 Feedback inhibition of the yeast ribosomal protein gene CRY2 is mediated by the nucleotide sequence and secondary structure of CRY2 pre- mRNA. Mol Cell Biol 15 6454 6464

69. TashevaES

RoufaDJ

1995 Regulation of human RPS14 transcription by intronic antisense RNAs and ribosomal protein S14. Genes Dev 9 304 316

70. RougemailleM

DieppoisG

Kisseleva-RomanovaE

GudipatiRK

LemoineS

2008 THO/Sub2p functions to coordinate 3′-end processing with gene-nuclear pore association. Cell 135 308 321

71. NagaiS

DubranaK

Tsai-PflugfelderM

DavidsonMB

RobertsTM

2008 Functional targeting of DNA damage to a nuclear pore-associated SUMO-dependent ubiquitin ligase. Science 322 597 602

72. AbdallahP

LucianoP

RungeKW

LisbyM

GéliV

2009 A two-step model for senescence triggered by a single critically short telomere. Nat Cell Biol 11 988 993

73. KalocsayM

HillerNJ

JentschS

2009 Chromosome-wide Rad51 spreading and SUMO-H2A.Z-dependent chromosome fixation in response to a persistent DNA double-strand break. Mol Cell 33 335 343

74. OzaP

JaspersenSL

MieleA

DekkerJ

PetersonCL

2009 Mechanisms that regulate localization of a DNA double-strand break to the nuclear periphery. Genes Dev 23 912 927

75. LeeK

KangMJ

KwonSJ

KwonYK

KimKW

2007 Expansion of chromosome territories with chromatin decompaction in BAF53-depleted interphase cells. Mol Biol Cell 18 4013 4023

76. LongtineMS

McKenzieA3rd

DemariniDJ

ShahNG

WachA

1998 Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14 953 961

77. HedigerF

DubranaK

GasserSM

2002 Myosin-like proteins 1 and 2 are not required for silencing or telomere anchoring, but act in the Tel1 pathway of telomere length control. J Struct Biol 140 79 91

78. IyerVR

HorakCE

ScafeCS

BotsteinD

SnyderM

2001 Genomic binding sites of the yeast cell-cycle transcription factors SBF and MBF. Nature 409 533 538

79. IwahashiH

KitagawaE

SuzukiY

UedaY

IshizawaYH

2007 Evaluation of toxicity of the mycotoxin citrinin using yeast ORF DNA microarray and Oligo DNA microarray. BMC genomics 8 95

80. ShimadaK

OmaY

SchlekerT

KugouK

OhtaK

2008 Ino80 chromatin remodeling complex promotes recovery of stalled replication forks. Curr Biol 18 566 575

81. HedigerF

TaddeiA

NeumannFR

GasserSM

2004 Methods for visualizing chromatin dynamics in living yeast. Methods Enzymol 375 345 365

Štítky
Genetika Reprodukčná medicína

Článok vyšiel v časopise

PLOS Genetics


2010 Číslo 4
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#