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
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Genetika Reprodukčná medicínaČlánok vyšiel v časopise
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