Histone H2A C-Terminus Regulates Chromatin Dynamics, Remodeling, and Histone H1 Binding

English version České info

The tails of histone proteins are central players for all chromatin-mediated processes. Whereas the N-terminal histone tails have been studied extensively, little is known about the function of the H2A C-terminus. Here, we show that the H2A C-terminal tail plays a pivotal role in regulating chromatin structure and dynamics. We find that cells expressing C-terminally truncated H2A show increased stress sensitivity. Moreover, both the complete and the partial deletion of the tail result in increased histone exchange kinetics and nucleosome mobility in vivo and in vitro. Importantly, our experiments reveal that the H2A C-terminus is required for efficient nucleosome translocation by ISWI-type chromatin remodelers and acts as a novel recognition module for linker histone H1. Thus, we suggest that the H2A C-terminal tail has a bipartite function: stabilisation of the nucleosomal core particle, as well as mediation of the protein interactions that control chromatin dynamics and conformation.

Vyšlo v časopise: Histone H2A C-Terminus Regulates Chromatin Dynamics, Remodeling, and Histone H1 Binding. PLoS Genet 6(12): e32767. doi:10.1371/journal.pgen.1001234
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1001234

Souhrn

Zdroje

1. KhorasanizadehS

2004 The nucleosome: from genomic organization to genomic regulation. Cell 116 259 272

2. LugerK

MaderAW

RichmondRK

SargentDF

RichmondTJ

1997 Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature 389 251 260

3. KouzaridesT

2007 Chromatin modifications and their function. Cell 128 693 705

4. NarlikarGJ

FanHY

KingstonRE

2002 Cooperation between complexes that regulate chromatin structure and transcription. Cell 108 475 487

5. TsukudaT

FlemingAB

NickoloffJA

OsleyMA

2005 Chromatin remodelling at a DNA double-strand break site in Saccharomyces cerevisiae. Nature 438 379 383

6. van AttikumH

GasserSM

2005 ATP-dependent chromatin remodeling and DNA double-strand break repair. Cell Cycle 4 1011 1014

7. GodfreyJE

EickbushTH

MoudrianakisEN

1980 Reversible association of calf thymus histones to form the symmetrical octamer (H2AH2BH3H4)2: a case of a mixed-associating system. Biochemistry 19 1339 1346

8. KimuraH

CookPR

2001 Kinetics of core histones in living human cells: little exchange of H3 and H4 and some rapid exchange of H2B. J Cell Biol 153 1341 1353

9. WoodcockCL

SkoultchiAI

FanY

2006 Role of linker histone in chromatin structure and function: H1 stoichiometry and nucleosome repeat length. Chromosome Res 14 17 25

10. ZhouYB

GerchmanSE

RamakrishnanV

TraversA

MuyldermansS

1998 Position and orientation of the globular domain of linker histone H5 on the nucleosome. Nature 395 402 405

11. BharathMM

ChandraNR

RaoMR

2003 Molecular modeling of the chromatosome particle. Nucleic Acids Res 31 4264 4274

12. BrownDT

IzardT

MisteliT

2006 Mapping the interaction surface of linker histone H1(0) with the nucleosome of native chromatin in vivo. Nat Struct Mol Biol 13 250 255

13. FanL

RobertsVA

2006 Complex of linker histone H5 with the nucleosome and its implications for chromatin packing. Proc Natl Acad Sci U S A 103 8384 8389

14. SyedSH

Goutte-GattatD

BeckerN

MeyerS

ShuklaMS

2010 Single-base resolution mapping of H1-nucleosome interactions and 3D organization of the nucleosome. Proc Natl Acad Sci U S A 107 9620 9625

15. KepperN

FoethkeD

StehrR

WedemannG

RippeK

2008 Nucleosome geometry and internucleosomal interactions control the chromatin fiber conformation. Biophys J 95 3692 3705

16. LeeKM

HayesJJ

1998 Linker DNA and H1-dependent reorganization of histone-DNA interactions within the nucleosome. Biochemistry 37 8622 8628

17. MeshorerE

YellajoshulaD

GeorgeE

ScamblerPJ

BrownDT

2006 Hyperdynamic plasticity of chromatin proteins in pluripotent embryonic stem cells. Dev Cell 10 105 116

18. GoldbergAD

BanaszynskiLA

NohKM

LewisPW

ElsaesserSJ

2010 Distinct factors control histone variant H3.3 localization at specific genomic regions. Cell 140 678 691

19. RaghuramN

CarreroG

Th'ngJ

HendzelMJ

2009 Molecular dynamics of histone H1. Biochem Cell Biol 87 189 206

20. DouY

BowenJ

LiuY

GorovskyMA

2002 Phosphorylation and an ATP-dependent process increase the dynamic exchange of H1 in chromatin. J Cell Biol 158 1161 1170

21. HigashiT

MatsunagaS

IsobeK

MorimotoA

ShimadaT

2007 Histone H2A mobility is regulated by its tails and acetylation of core histone tails. Biochem Biophys Res Commun 357 627 632

22. BoulardM

GautierT

MbeleGO

GersonV

HamicheA

2006 The NH2 tail of the novel histone variant H2BFWT exhibits properties distinct from conventional H2B with respect to the assembly of mitotic chromosomes. Mol Cell Biol 26 1518 1526

23. GrothA

CorpetA

CookAJ

RocheD

BartekJ

2007 Regulation of replication fork progression through histone supply and demand. Science 318 1928 1931

24. SzutsD

2004 Cell cycle arrest at the initiation step of human chromosomal DNA replication causes DNA damage. Journal of Cell Science 117 4897 4908

25. FerreiraH

SomersJ

WebsterR

FlausA

Owen-HughesT

2007 Histone tails and the H3 alphaN helix regulate nucleosome mobility and stability. Mol Cell Biol 27 4037 4048

26. DundrM

Hoffmann-RohrerU

HuQ

GrummtI

RothblumLI

2002 A kinetic framework for a mammalian RNA polymerase in vivo. Science 298 1623 1626

27. KandaT

SullivanKF

WahlGM

1998 Histone-GFP fusion protein enables sensitive analysis of chromosome dynamics in living mammalian cells. Curr Biol 8 377 385

28. KappesF

BurgerK

BaackM

FackelmayerFO

GrussC

2001 Subcellular localization of the human proto-oncogene protein DEK. J Biol Chem 276 26317 26323

29. RoseSM

GarrardWT

1984 Differentiation-dependent chromatin alterations precede and accompany transcription of immunoglobulin light chain genes. J Biol Chem 259 8534 8544

30. FlausA

Owen-HughesT

2003 Dynamic properties of nucleosomes during thermal and ATP-driven mobilization. Mol Cell Biol 23 7767 7779

31. FlausA

RichmondTJ

1998 Positioning and stability of nucleosomes on MMTV 3'LTR sequences. Journal of Molecular Biology 275 427 441

32. MeerssemanG

PenningsS

BradburyEM

1992 Mobile nucleosomes–a general behavior. Embo J 11 2951 2959

33. HamicheA

SandaltzopoulosR

GdulaDA

WuC

1999 ATP-dependent histone octamer sliding mediated by the chromatin remodeling complex NURF. Cell 97 833 842

34. LängstG

BeckerPB

2001 ISWI induces nucleosome sliding on nicked DNA. Molecular Cell 8 1085 1092

35. StrohnerR

WachsmuthM

DachauerK

MazurkiewiczJ

HochstatterJ

2005 A ‘loop recapture’ mechanism for ACF-dependent nucleosome remodeling. Nat Struct Mol Biol 12 683 690

36. RippeK

SchraderA

RiedeP

StrohnerR

LehmannE

2007 DNA sequence- and conformation-directed positioning of nucleosomes by chromatin-remodeling complexes. Proc Natl Acad Sci U S A 104 15635 15640

37. EberharterA

VetterI

FerreiraR

BeckerPB

2004 ACF1 improves the effectiveness of nucleosome mobilization by ISWI through PHD-histone contacts. Embo J 23 4029 4039

38. ThastromA

LowaryPT

WidlundHR

CaoH

KubistaM

1999 Sequence motifs and free energies of selected natural and non-natural nucleosome positioning DNA sequences. J Mol Biol 288 213 229

39. FinkM

ImholzD

ThomaF

2007 Contribution of the serine 129 of histone H2A to chromatin structure. Mol Cell Biol 27 3589 3600

40. KruhlakMJ

CelesteA

DellaireG

Fernandez-CapetilloO

MullerWG

2006 Changes in chromatin structure and mobility in living cells at sites of DNA double-strand breaks. J Cell Biol 172 823 834

41. LiJ

LangstG

GrummtI

2006 NoRC-dependent nucleosome positioning silences rRNA genes. Embo J 25 5735 5741

42. ZhangZ

ReeseJC

2004 Ssn6-Tup1 requires the ISW2 complex to position nucleosomes in Saccharomyces cerevisiae. Embo J 23 2246 2257

43. ParnellTJ

HuffJT

CairnsBR

2008 RSC regulates nucleosome positioning at Pol II genes and density at Pol III genes. Embo J 27 100 110

44. KaraczynAA

ChengRYS

BuzardGS

HartleyJ

EspositoD

2009 Truncation of histone H2A's C-terminal tail, as is typical for Ni(II)-assisted specific peptide bond hydrolysis, has gene expression altering effects. Ann Clin Lab Sci 39 251 262

45. KimK

ChoiJ

HeoK

KimH

LevensD

2008 Isolation and characterization of a novel H1.2 complex that acts as a repressor of p53-mediated transcription. J Biol Chem 283 9113 9126

46. WolffeAP

1998 Chromatin Structure and Function: Academic Press

47. LugerK

RechsteinerTJ

RichmondTJ

1999 Expression and purification of recombinant histones and nucleosome reconstitution. Methods Mol Biol 119 1 16

48. LängstG

BonteEJ

CoronaDF

BeckerPB

1999 Nucleosome movement by CHRAC and ISWI without disruption or trans-displacement of the histone octamer. Cell 97 843 852

49. BrehmA

LängstG

KehleJ

ClapierCR

ImhofA

2000 dMi-2 and ISWI chromatin remodelling factors have distinct nucleosome binding and mobilization properties. EMBO J 19 4332 4341

50. FlausA

Owen-HughesT

2003 Mechanisms for nucleosome mobilization. Biopolymers 68 563 578

51. FrankenNA

RodermondHM

StapJ

HavemanJ

van BreeC

2006 Clonogenic assay of cells in vitro. Nat Protoc 1 2315 2319

52. DaujatS

ZeisslerU

WaldmannT

HappelN

SchneiderR

2005 HP1 binds specifically to Lys26-methylated histone H1.4, whereas simultaneous Ser27 phosphorylation blocks HP1 binding. J Biol Chem 280 38090 38095

53. O'NeillLP

KeohaneAM

LavenderJS

McCabeV

HeardE

1999 A developmental switch in H4 acetylation upstream of Xist plays a role in X chromosome inactivation. Embo J 18 2897 2907

54. HeoK

KimB

KimK

ChoiJ

KimH

2007 Isolation and characterization of proteins associated with histone H3 tails in vivo. J Biol Chem 282 15476 15483