Global Analysis of the Relationship between JIL-1 Kinase and Transcription

English version České info

The ubiquitous tandem kinase JIL-1 is essential for Drosophila development. Its role in defining decondensed domains of larval polytene chromosomes is well established, but its involvement in transcription regulation has remained controversial. For a first comprehensive molecular characterisation of JIL-1, we generated a high-resolution, chromosome-wide interaction profile of the kinase in Drosophila cells and determined its role in transcription. JIL-1 binds active genes along their entire length. The presence of the kinase is not proportional to average transcription levels or polymerase density. Comparison of JIL-1 association with elongating RNA polymerase and a variety of histone modifications suggests two distinct targeting principles. A basal level of JIL-1 binding can be defined that correlates best with the methylation of histone H3 at lysine 36, a mark that is placed co-transcriptionally. The additional acetylation of H4K16 defines a second state characterised by approximately twofold elevated JIL-1 levels, which is particularly prominent on the dosage-compensated male X chromosome. Phosphorylation of the histone H3 N-terminus by JIL-1 in vitro is compatible with other tail modifications. In vivo, phosphorylation of H3 at serine 10, together with acetylation at lysine 14, creates a composite histone mark that is enriched at JIL-1 binding regions. Its depletion by RNA interference leads to a modest, but significant, decrease of transcription from the male X chromosome. Collectively, the results suggest that JIL-1 participates in a complex histone modification network that characterises active, decondensed chromatin. We hypothesise that one specific role of JIL-1 may be to reinforce, rather than to establish, the status of active chromatin through the phosphorylation of histone H3 at serine 10.

Vyšlo v časopise: Global Analysis of the Relationship between JIL-1 Kinase and Transcription. PLoS Genet 7(3): e32767. doi:10.1371/journal.pgen.1001327
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1001327

Souhrn

Zdroje

1. 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

2. JinY

WangY

WalkerDL

DongH

ConleyC

1999 JIL-1: a novel chromosomal tandem kinase implicated in transcriptional regulation in Drosophila. Mol Cell 4 129 135

3. BaoX

CaiW

DengH

ZhangW

KrencikR

2008 The COOH-terminal domain of the JIL-1 histone H3S10 kinase interacts with histone H3 and is required for correct targeting to chromatin. J Biol Chem 283 32741 32750

4. DengH

ZhangW

BaoX

MartinJN

GirtonJ

2005 The JIL-1 kinase regulates the structure of Drosophila polytene chromosomes. Chromosoma 114 173 182

5. DengH

BaoX

CaiW

BlacketerMJ

BelmontAS

2008 Ectopic histone H3S10 phosphorylation causes chromatin structure remodeling in Drosophila. Development 135 699 705

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. LerachS

ZhangW

BaoX

DengH

GirtonJ

2006 Loss-of-function alleles of the JIL-1 kinase are strong suppressors of position effect variegation of the wm4 allele in Drosophila. Genetics 173 2403 2406

8. BaoX

DengH

JohansenJ

GirtonJ

JohansenKM

2007 Loss-of-function alleles of the JIL-1 histone H3S10 kinase enhance position-effect variegation at pericentric sites in Drosophila heterochromatin. Genetics 176 1355 1358

9. EbertA

SchottaG

LeinS

KubicekS

KraussV

2004 Su(var) genes regulate the balance between euchromatin and heterochromatin in Drosophila. Genes Dev 18 2973 2983

10. DengH

BaoX

ZhangW

GirtonJ

JohansenJ

2007 Reduced levels of Su(var)3-9 but not Su(var)2-5 (HP1) counteract the effects on chromatin structure and viability in loss-of-function mutants of the JIL-1 histone H3S10 kinase. Genetics 177 79 87

11. DengH

CaiW

WangC

LerachS

DelattreM

2010 JIL-1 AND SU(VAR)3-7 Interact Genetically and Counteract Each Other's Effect on Position Effect Variegation in Drosophila. Genetics

12. VermeulenL

BergheWV

BeckIM

De BosscherK

HaegemanG

2009 The versatile role of MSKs in transcriptional regulation. Trends Biochem Sci 34 311 318

13. 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

14. VicentGP

BallareC

NachtAS

ClausellJ

Subtil-RodriguezA

2006 Induction of progesterone target genes requires activation of Erk and Msk kinases and phosphorylation of histone H3. Mol Cell 24 367 381

15. 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

16. ZippoA

SerafiniR

RocchigianiM

PennacchiniS

KrepelovaA

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

17. KaramCS

KellnerWA

TakenakaN

ClemmonsAW

CorcesVG

2010 14-3-3 Mediates Histone Cross-Talk during Transcription Elongation in Drosophila. PLoS Genet 6 e1000975 doi:10.1371/journal.pgen.1000975

18. 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

19. 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

20. StraubT

BeckerPB

2007 Dosage compensation: the beginning and end of generalization. Nat Rev Genet 8 47 57

21. GelbartME

KurodaMI

2009 Drosophila dosage compensation: a complex voyage to the X chromosome. Development 136 1399 1410

22. JinY

WangY

JohansenJ

JohansenKM

2000 JIL-1, a chromosomal kinase implicated in regulation of chromatin structure, associates with the male specific lethal (MSL) dosage compensation complex. J Cell Biol 149 1005 1010

23. AlekseyenkoAA

LarschanE

LaiWR

ParkPJ

KurodaMI

2006 High-resolution ChIP-chip analysis reveals that the Drosophila MSL complex selectively identifies active genes on the male X chromosome. Genes Dev 20 848 857

24. GilfillanGD

StraubT

de WitE

GreilF

LammR

2006 Chromosome-wide gene-specific targeting of the Drosophila dosage compensation complex. Genes Dev 20 858 870

25. GelbartME

LarschanE

PengS

ParkPJ

KurodaMI

2009 Drosophila MSL complex globally acetylates H4K16 on the male X chromosome for dosage compensation. Nat Struct Mol Biol 16 825 832

26. PrestelM

FellerC

StraubT

MitlöhnerH

BeckerPB

2010 The activation potential of MOF is constrained for doasege compensation. Molecular Cell 38 815 826

27. Shogren-KnaakM

IshiiH

SunJM

PazinMJ

DavieJR

2006 Histone H4-K16 acetylation controls chromatin structure and protein interactions. Science 311 844 847

28. ZhangY

OliverB

2010 An evolutionary consequence of dosage compensation on Drosophila melanogaster female X-chromatin structure? BMC Genomics 11 6

29. StraubT

GrimaudC

GilfillanGD

MitterwegerA

BeckerPB

2008 The chromosomal high-affinity binding sites for the Drosophila dosage compensation complex. PLoS Genet 4 e1000302 doi:10.1371/journal.pgen.1000302

30. LarschanE

AlekseyenkoAA

GortchakovAA

PengS

LiB

2007 MSL complex is attracted to genes marked by H3K36 trimethylation using a sequence-independent mechanism. Mol Cell 28 121 133

31. LeeJS

ShilatifardA

2007 A site to remember: H3K36 methylation a mark for histone deacetylation. Mutat Res 618 130 134

32. Villar-GareaA

ImhofA

2008 Fine mapping of posttranslational modifications of the linker histone H1 from Drosophila melanogaster. PLoS ONE 3 e1553 doi:10.1371/journal.pone.0001553

33. BoekeJ

RegnardC

CaiW

JohansenJ

JohansenKM

2010 Phosphorylation of SU(VAR)3-9 by the chromosomal kinase JIL-1. PLoS ONE 5 e10042 doi:10.1371/journal.pone.0010042

34. GietR

GloverDM

2001 Drosophila aurora B kinase is required for histone H3 phosphorylation and condensin recruitment during chromosome condensation and to organize the central spindle during cytokinesis. J Cell Biol 152 669 682

35. NowakSJ

CorcesVG

2004 Phosphorylation of histone H3: a balancing act between chromosome condensation and transcriptional activation. Trends Genet 20 214 220

36. GadeaBB

RudermanJV

2005 Aurora kinase inhibitor ZM447439 blocks chromosome-induced spindle assembly, the completion of chromosome condensation, and the establishment of the spindle integrity checkpoint in Xenopus egg extracts. Mol Biol Cell 16 1305 1318

37. Morales-MuliaS

ScholeyJM

2005 Spindle pole organization in Drosophila S2 cells by dynein, abnormal spindle protein (Asp), and KLP10A. Mol Biol Cell 16 3176 3186

38. ClaytonAL

HazzalinCA

MahadevanLC

2006 Enhanced histone acetylation and transcription: a dynamic perspective. Mol Cell 23 289 296

39. ClaytonAL

RoseS

BarrattMJ

MahadevanLC

2000 Phosphoacetylation of histone H3 on c-fos- and c-jun-associated nucleosomes upon gene activation. EMBO J 19 3714 3726

40. BrunmeirR

LaggerS

SimboeckE

SawickaA

EggerG

2010 Epigenetic regulation of a murine retrotransposon by a dual histone modification mark. PLoS Genet 6 e1000927 doi:10.1371/journal.pgen.1000927

41. PeteschSJ

LisJT

2008 Rapid, transcription-independent loss of nucleosomes over a large chromatin domain at Hsp70 loci. Cell 134 74 84

42. ZinkD

ParoR

1995 Drosophila Polycomb-group regulated chromatin inhibits the accessibility of a trans-activator to its target DNA. EMBO J 14 5660 5671

43. KelleyRL

WangJ

BellL

KurodaMI

1997 Sex lethal controls dosage compensation in Drosophila by a non-splicing mechanism. Nature 387 195 199

44. DahlsveenIK

GilfillanGD

ShelestVI

LammR

BeckerPB

2006 Targeting determinants of dosage compensation in Drosophila. PLoS Genet 2 e5 doi:10.1371/journal.pgen.0020005

45. FilionGJ

van BemmelJG

BraunschweigU

TalhoutW

KindJ

2010 Systematic protein location mapping reveals five principal chromatin types in Drosophila cells. Cell 143 212 224

46. KindJ

VaquerizasJM

GebhardtP

GentzelM

LuscombeNM

2008 Genome-wide analysis reveals MOF as a key regulator of dosage compensation and gene expression in Drosophila. Cell 133 813 828

47. RajaSJ

CharapitsaI

ConradT

VaquerizasJM

GebhardtP

2010 The nonspecific lethal complex is a transcriptional regulator in Drosophila. Molecular Cell 38 827 841

48. CiurciuA

KomonyiO

BorosIM

2008 Loss of ATAC-specific acetylation of histone H4 at Lys12 reduces binding of JIL-1 to chromatin and phosphorylation of histone H3 at Ser10. J Cell Sci 121 3366 3372

49. SuganumaT

GutierrezJL

LiB

FlorensL

SwansonSK

2008 ATAC is a double histone acetyltransferase complex that stimulates nucleosome sliding. Nat Struct Mol Biol 15 364 372

50. LoWS

TrievelRC

RojasJR

DugganL

HsuJY

2000 Phosphorylation of serine 10 in histone H3 is functionally linked in vitro and in vivo to Gcn5-mediated acetylation at lysine 14. Mol Cell 5 917 926

51. 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

52. ReaS

EisenhaberF

O'CarrollD

StrahlBD

SunZW

2000 Regulation of chromatin structure by site-specific histone H3 methyltransferases. Nature 406 593 599

53. ZippoA

De RobertisA

SerafiniR

OlivieroS

2007 PIM1-dependent phosphorylation of histone H3 at serine 10 is required for MYC-dependent transcriptional activation and oncogenic transformation. Nat Cell Biol 9 932 944

54. WinterS

FischleW

SeiserC

2008 Modulation of 14-3-3 interaction with phosphorylated histone H3 by combinatorial modification patterns. Cell Cycle 7 1336 1342

55. FudaNJ

ArdehaliMB

LisJT

2009 Defining mechanisms that regulate RNA polymerase II transcription in vivo. Nature 461 186 192

56. HagerGL

McNallyJG

MisteliT

2009 Transcription dynamics. Mol Cell 35 741 753

57. WijgerdeM

GrosveldF

FraserP

1995 Transcription complex stability and chromatin dynamics in vivo. Nature 377 209 213

58. FischleW

TsengBS

DormannHL

UeberheideBM

GarciaBA

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

59. HirotaT

LippJJ

TohBH

PetersJM

2005 Histone H3 serine 10 phosphorylation by Aurora B causes HP1 dissociation from heterochromatin. Nature 438 1176 1180

60. BaoX

ZhangW

KrencikR

DengH

WangY

2005 The JIL-1 kinase interacts with lamin Dm0 and regulates nuclear lamina morphology of Drosophila nurse cells. J Cell Sci 118 5079 5087

61. NegreN

HennetinJ

SunLV

LavrovS

BellisM

2006 Chromosomal distribution of PcG proteins during Drosophila development. PLoS Biol 4 e170 doi:10.1371/journal.pbio.0040170

62. GilfillanGD

KonigC

DahlsveenIK

PrakouraN

StraubT

2007 Cumulative contributions of weak DNA determinants to targeting the Drosophila dosage compensation complex. Nucleic Acids Res 35 3561 3572

63. TusherVG

TibshiraniR

ChuG

2001 Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci U S A 98 5116 5121

64. EfronB

2007 Correlation and large scale simultaneous significance testing. Jour Amer Stat Assoc 102 99 103

65. HumburgP

BulgerD

StoneG

2008 Parameter estimation for robust HMM analysis of ChIP-chip data. BMC Bioinformatics 9 343

66. StraubT

NeumannMF

PrestelM

KremmerE

KaetherC

2005 Stable chromosomal association of MSL2 defines a dosage-compensated nuclear compartment. Chromosoma 114 352 364

67. RisauW

SaumweberH

SymmonsP

1981 Monoclonal antibodies against a nuclear membrane protein of Drosophila. Localization by indirect immunofluorescence and detection of antigen using a new protein blotting procedure. Exp Cell Res 133 47 54

68. 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