#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

14-3-3 Mediates Histone Cross-Talk during Transcription Elongation in


Post-translational modifications of histone proteins modulate the binding of transcription regulators to chromatin. Studies in Drosophila have shown that the phosphorylation of histone H3 at Ser10 (H3S10ph) by JIL-1 is required specifically during early transcription elongation. 14-3-3 proteins bind H3 only when phosphorylated, providing mechanistic insights into the role of H3S10ph in transcription. Findings presented here show that 14-3-3 functions downstream of H3S10ph during transcription elongation. 14-3-3 proteins localize to active genes in a JIL-1–dependent manner. In the absence of 14-3-3, levels of actively elongating RNA polymerase II are severely diminished. 14-3-3 proteins interact with Elongator protein 3 (Elp3), an acetyltransferase that functions during transcription elongation. JIL-1 and 14-3-3 are required for Elp3 binding to chromatin, and in the absence of either protein, levels of H3K9 acetylation are significantly reduced. These results suggest that 14-3-3 proteins mediate cross-talk between histone phosphorylation and acetylation at a critical step in transcription elongation.


Vyšlo v časopise: 14-3-3 Mediates Histone Cross-Talk during Transcription Elongation in. PLoS Genet 6(6): e32767. doi:10.1371/journal.pgen.1000975
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1000975

Souhrn

Post-translational modifications of histone proteins modulate the binding of transcription regulators to chromatin. Studies in Drosophila have shown that the phosphorylation of histone H3 at Ser10 (H3S10ph) by JIL-1 is required specifically during early transcription elongation. 14-3-3 proteins bind H3 only when phosphorylated, providing mechanistic insights into the role of H3S10ph in transcription. Findings presented here show that 14-3-3 functions downstream of H3S10ph during transcription elongation. 14-3-3 proteins localize to active genes in a JIL-1–dependent manner. In the absence of 14-3-3, levels of actively elongating RNA polymerase II are severely diminished. 14-3-3 proteins interact with Elongator protein 3 (Elp3), an acetyltransferase that functions during transcription elongation. JIL-1 and 14-3-3 are required for Elp3 binding to chromatin, and in the absence of either protein, levels of H3K9 acetylation are significantly reduced. These results suggest that 14-3-3 proteins mediate cross-talk between histone phosphorylation and acetylation at a critical step in transcription elongation.


Zdroje

1. JenuweinT

AllisCD

2001 Translating the histone code. Science 293 1074 1080

2. DanielJA

Pray-GrantMG

GrantPA

2005 Effector proteins for methylated histones: an expanding family. Cell Cycle 4 919 926

3. YangXJ

2004 Lysine acetylation and the bromodomain: a new partnership for signaling. Bioessays 26 1076 1087

4. VermeulenM

MulderKW

DenissovS

PijnappelWW

van SchaikFM

2007 Selective anchoring of TFIID to nucleosomes by trimethylation of histone H3 lysine 4. Cell 131 58 69

5. LeeJS

ShuklaA

SchneiderJ

SwansonSK

WashburnMP

2007 Histone crosstalk between H2B monoubiquitination and H3 methylation mediated by COMPASS. Cell 131 1084 1096

6. ZhangW

DengH

BaoX

LerachS

GirtonJ

2006 The JIL-1 histone H3S10 kinase regulates dimethyl H3K9 modifications and heterochromatic spreading in Drosophila. Development 133 229 235

7. FischleW

TsengBS

DormannHL

UeberheideBM

GarciaBA

2005 Regulation of HP1-chromatin binding by histone H3 methylation and phosphorylation. Nature 438 1116 1122

8. NgHH

RobertF

YoungRA

StruhlK

2003 Targeted recruitment of Set1 histone methylase by elongating Pol II provides a localized mark and memory of recent transcriptional activity. Mol Cell 11 709 719

9. KroganNJ

KimM

TongA

GolshaniA

CagneyG

2003 Methylation of histone H3 by Set2 in Saccharomyces cerevisiae is linked to transcriptional elongation by RNA polymerase II. Mol Cell Biol 23 4207 4218

10. MahadevanLC

WillisAC

BarrattMJ

1991 Rapid histone H3 phosphorylation in response to growth factors, phorbol esters, okadaic acid, and protein synthesis inhibitors. Cell 65 775 783

11. NowakSJ

CorcesVG

2000 Phosphorylation of histone H3 correlates with transcriptionally active loci. Genes Dev 14 3003 3013

12. LoWS

DugganL

EmreNC

BelotserkovskyaR

LaneWS

2001 Snf1–a histone kinase that works in concert with the histone acetyltransferase Gcn5 to regulate transcription. Science 293 1142 1146

13. MacdonaldN

WelburnJP

NobleME

NguyenA

YaffeMB

2005 Molecular basis for the recognition of phosphorylated and phosphoacetylated histone h3 by 14-3-3. Mol Cell 20 199 211

14. WinterS

SimboeckE

FischleW

ZupkovitzG

DohnalI

2008 14-3-3 proteins recognize a histone code at histone H3 and are required for transcriptional activation. Embo J 27 88 99

15. ZippoA

SerafiniR

RocchigianiM

PennacchiniS

KrepelovaA

2009 Histone crosstalk between H3S10ph and H4K16ac generates a histone code that mediates transcription elongation. Cell 138 1122 1136

16. WangY

ZhangW

JinY

JohansenJ

JohansenKM

2001 The JIL-1 tandem kinase mediates histone H3 phosphorylation and is required for maintenance of chromatin structure in Drosophila. Cell 105 433 443

17. IvaldiMS

KaramCS

CorcesVG

2007 Phosphorylation of histone H3 at Ser10 facilitates RNA polymerase II release from promoter-proximal pausing in Drosophila. Genes Dev 21 2818 2831

18. CaiW

BaoX

DengH

JinY

GirtonJ

2008 RNA polymerase II-mediated transcription at active loci does not require histone H3S10 phosphorylation in Drosophila. Development 135 2917 2925

19. LabradorM

CorcesVG

2003 Phosphorylation of histone H3 during transcriptional activation depends on promoter structure. Genes Dev 17 43 48

20. BuszczakM

SpradlingAC

2006 The Drosophila P68 RNA helicase regulates transcriptional deactivation by promoting RNA release from chromatin. Genes Dev 20 977 989

21. SchwartzBE

AhmadK

2005 Transcriptional activation triggers deposition and removal of the histone variant H3.3. Genes Dev 19 804 814

22. GrauB

PopescuC

TorrojaL

Ortuno-SahagunD

BorosI

2008 Transcriptional adaptor ADA3 of Drosophila melanogaster is required for histone modification, position effect variegation, and transcription. Mol Cell Biol 28 376 385

23. CiurciuA

TombaczI

PopescuC

BorosI

2009 GAL4 induces transcriptionally active puff in the absence of dSAGA- and ATAC-specific chromatin acetylation in the Drosophila melanogaster polytene chromosome. Chromosoma 118 513 526

24. SuTT

ParryDH

DonahoeB

ChienCT

O'FarrellPH

2001 Cell cycle roles for two 14-3-3 proteins during Drosophila development. J Cell Sci 114 3445 3454

25. ArmstrongJA

PapoulasO

DaubresseG

SperlingAS

LisJT

2002 The Drosophila BRM complex facilitates global transcription by RNA polymerase II. Embo J 21 5245 5254

26. TamkunJW

DeuringR

ScottMP

KissingerM

PattatucciAM

1992 brahma: a regulator of Drosophila homeotic genes structurally related to the yeast transcriptional activator SNF2/SWI2. Cell 68 561 572

27. SrinivasanS

ArmstrongJA

DeuringR

DahlsveenIK

McNeillH

2005 The Drosophila trithorax group protein Kismet facilitates an early step in transcriptional elongation by RNA Polymerase II. Development 132 1623 1635

28. TzivionG

ShenYH

ZhuJ

2001 14-3-3 proteins; bringing new definitions to scaffolding. Oncogene 20 6331 6338

29. WinklerGS

KristjuhanA

Erdjument-BromageH

TempstP

SvejstrupJQ

2002 Elongator is a histone H3 and H4 acetyltransferase important for normal histone acetylation levels in vivo. Proc Natl Acad Sci U S A 99 3517 3522

30. Pozuelo RubioM

GeraghtyKM

WongBH

WoodNT

CampbellDG

2004 14-3-3-affinity purification of over 200 human phosphoproteins reveals new links to regulation of cellular metabolism, proliferation and trafficking. Biochem J 379 395 408

31. WittschiebenBO

OteroG

de BizemontT

FellowsJ

Erdjument-BromageH

1999 A novel histone acetyltransferase is an integral subunit of elongating RNA polymerase II holoenzyme. Mol Cell 4 123 128

32. HanQ

LuJ

DuanJ

SuD

HouX

2008 Gcn5- and Elp3-induced histone H3 acetylation regulates hsp70 gene transcription in yeast. Biochem J 409 779 788

33. WittschiebenBO

FellowsJ

DuW

StillmanDJ

SvejstrupJQ

2000 Overlapping roles for the histone acetyltransferase activities of SAGA and elongator in vivo. EMBO J 19 3060 3068

34. WalkerJ

KwonSY

BadenhorstP

McNeillH

SvejstrupJQ

2009 Role of Elongator Subunit Elp3 in Drosophila Melanogaster Larval Development and Tumorigenesis. Submitted

35. LiW

SkoulakisEM

DavisRL

PerrimonN

1997 The Drosophila 14-3-3 protein Leonardo enhances Torso signaling through D-Raf in a Ras 1-dependent manner. Development 124 4163 4171

36. SkoulakisEM

DavisRL

1998 14-3-3 proteins in neuronal development and function. Mol Neurobiol 16 269 284

37. ChangHC

RubinGM

1997 14-3-3 epsilon positively regulates Ras-mediated signaling in Drosophila. Genes Dev 11 1132 1139

38. KarimFD

ChangHC

TherrienM

WassarmanDA

LavertyT

1996 A screen for genes that function downstream of Ras1 during Drosophila eye development. Genetics 143 315 329

39. AcevedoSF

TsigkariKK

GrammenoudiS

SkoulakisEM

2007 In vivo functional specificity and homeostasis of Drosophila 14-3-3 proteins. Genetics 177 239 253

40. BjorkGR

HuangB

PerssonOP

BystromAS

2007 A conserved modified wobble nucleoside (mcm5s2U) in lysyl-tRNA is required for viability in yeast. Rna 13 1245 1255

41. HuangB

JohanssonMJ

BystromAS

2005 An early step in wobble uridine tRNA modification requires the Elongator complex. Rna 11 424 436

42. MahadevanLC

ClaytonAL

HazzalinCA

ThomsonS

2004 Phosphorylation and acetylation of histone H3 at inducible genes: two controversies revisited. Novartis Found Symp 259 102 111; discussion 111-104, 163-109

43. CheungP

TannerKG

CheungWL

Sassone-CorsiP

DenuJM

2000 Synergistic coupling of histone H3 phosphorylation and acetylation in response to epidermal growth factor stimulation. Mol Cell 5 905 915

44. ClaytonAL

MahadevanLC

2003 MAP kinase-mediated phosphoacetylation of histone H3 and inducible gene regulation. FEBS Lett 546 51 58

45. ThomsonS

ClaytonAL

MahadevanLC

2001 Independent dynamic regulation of histone phosphorylation and acetylation during immediate-early gene induction. Mol Cell 8 1231 1241

46. MuseGW

GilchristDA

NechaevS

ShahR

ParkerJS

2007 RNA polymerase is poised for activation across the genome. Nat Genet 39 1507 1511

47. ZeitlingerJ

StarkA

KellisM

HongJW

NechaevS

2007 RNA polymerase stalling at developmental control genes in the Drosophila melanogaster embryo. Nat Genet 39 1512 1516

48. GuentherMG

LevineSS

BoyerLA

JaenischR

YoungRA

2007 A chromatin landmark and transcription initiation at most promoters in human cells. Cell 130 77 88

49. BoehmAK

SaundersA

WernerJ

LisJT

2003 Transcription factor and polymerase recruitment, modification, and movement on dhsp70 in vivo in the minutes following heat shock. Mol Cell Biol 23 7628 7637

Štítky
Genetika Reprodukčná medicína

Článok vyšiel v časopise

PLOS Genetics


2010 Číslo 6
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#