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PMID: 10654937 Published · ppublish English Journal Article

Core histone N-termini play an essential role in mitotic chromosome condensation.

The EMBO journal ·Vol. 19 ·No. 3 ·2000-02-01 ·Pages 379-91

de la Barre AE, Gerson V, Gout S, Creaven M, Allis CD, Dimitrov S

Abstract

We have studied the role of core histone tails in the assembly of mitotic chromosomes using Xenopus egg extracts. Incubation of sperm nuclei in the extracts led to the formation of mitotic chromosomes, a process we found to be correlated with phosphorylation of the N-terminal tail of histone H3 at Ser10. When the extracts were supplemented with H1-depleted oligosomes, they were not able to assemble chromosomes. Selective elimination of oligosome histone tails by trypsin digestion resulted in a dramatic decrease in their ability to inhibit chromosome condensation. The chromosome assembly was also inhibited by each of the histone tails with differing efficiency. In addition, we found that nucleosomes were recruiting through the flexible histone tails some chromosome assembly factors, different from topoisomerase II and 13S condensin. These findings demonstrate that histone tails play an essential role in chromosome assembly. We also present evidence that the nucleosomes, through physical association, were able to deplete the extracts from the kinase phosphorylating histone H3 at Ser10, suggesting that this kinase could be important for chromosome condensation.

MeSH Terms
Adenosine Triphosphatases/metabolism Animals Bisbenzimidazole Cell Extracts Chromosomes/chemistry DNA/metabolism DNA Topoisomerases, Type II/metabolism DNA-Binding Proteins/metabolism Histones/chemistry,genetics Male Microscopy, Fluorescence Mitosis Multiprotein Complexes Mutation Nuclear Proteins/metabolism Nucleosomes/metabolism Oocytes Phosphorylation Protein Kinases/metabolism Recombinant Fusion Proteins/genetics,metabolism Spermatozoa Trypsin/metabolism Xenopus
Chemicals
Cell Extracts DNA-Binding Proteins Histones Multiprotein Complexes Nuclear Proteins Nucleosomes Recombinant Fusion Proteins condensin complexes DNA Protein Kinases Trypsin Adenosine Triphosphatases DNA Topoisomerases, Type II Bisbenzimidazole
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
de la Barre A E
Laboratoire de Biologie Moléculaire et Cellulaire de la Différenciation, équipe Mécanismes d'Assemblage du Matériel Génétique, INSERM U 309, Institut Albert Bonniot, Domaine de la Merci, 38706 La Tronche, Cedex, France.
Gerson V
Gout S
Creaven M
Allis C D
Dimitrov S
References (46)
46 references, click to expand
  1. Crystal structure of the nucleosome core particle at 2.8 A resolution.
    Nature. 1997 Sep 18;389(6648):251-60 PMID: 9305837
  2. SMC-mediated chromosome mechanics: a conserved scheme from bacteria to vertebrates?
    Genes Dev. 1999 Jan 1;13(1):11-9 PMID: 9887095
  3. Histone H3 and H4 N-termini interact with SIR3 and SIR4 proteins: a molecular model for the formation of heterochromatin in yeast.
    Cell. 1995 Feb 24;80(4):583-92 PMID: 7867066
  4. Chromatin superstructure-dependent crosslinking with DNA of the histone H5 residues Thr1, His25 and His62.
    J Mol Biol. 1990 Jan 20;211(2):479-91 PMID: 2106584
  5. Mitotic chromosome condensation.
    Annu Rev Cell Dev Biol. 1996;12:305-33 PMID: 8970729
  6. Remodeling sperm chromatin in Xenopus laevis egg extracts: the role of core histone phosphorylation and linker histone B4 in chromatin assembly.
    J Cell Biol. 1994 Aug;126(3):591-601 PMID: 8045925
  7. Cleavage of structural proteins during the assembly of the head of bacteriophage T4.
    Nature. 1970 Aug 15;227(5259):680-5 PMID: 5432063
  8. Anaphase is initiated by proteolysis rather than by the inactivation of maturation-promoting factor.
    Cell. 1993 Jul 2;73(7):1393-402 PMID: 8391932
  9. Stable nucleosome positioning and complete repression by the yeast alpha 2 repressor are disrupted by amino-terminal mutations in histone H4.
    Genes Dev. 1992 Mar;6(3):411-25 PMID: 1547940
  10. Nucleoplasmin remodels sperm chromatin in Xenopus egg extracts.
    Cell. 1992 May 29;69(5):759-67 PMID: 1591776
  11. The histone tails of the nucleosome.
    Curr Opin Genet Dev. 1998 Apr;8(2):140-6 PMID: 9610403
  12. Untangling the role of DNA topoisomerase II in mitotic chromosome structure and function.
    Bioessays. 1997 Feb;19(2):97-9 PMID: 9046238
  13. Condensins, chromosome condensation protein complexes containing XCAP-C, XCAP-E and a Xenopus homolog of the Drosophila Barren protein.
    Cell. 1997 May 16;89(4):511-21 PMID: 9160743
  14. Resolving the role of topoisomerase II in chromatin structure and function.
    Trends Cell Biol. 1995 Sep;5(9):348-54 PMID: 14732077
  15. Chromosome condensation induced by fostriecin does not require p34cdc2 kinase activity and histone H1 hyperphosphorylation, but is associated with enhanced histone H2A and H3 phosphorylation.
    EMBO J. 1995 Mar 1;14(5):976-85 PMID: 7889943
  16. Fine resolution of histones by two-dimensional polyacrylamide gel electrophoresis: developmental implications.
    Methods. 1997 May;12(1):57-61 PMID: 9169195
  17. Histone acetylation and chromatin assembly: a single escort, multiple dances?
    Cell. 1996 Oct 4;87(1):5-8 PMID: 8858142
  18. Elasticity and structure of eukaryote chromosomes studied by micromanipulation and micropipette aspiration.
    J Cell Biol. 1997 Oct 6;139(1):1-12 PMID: 9314524
  19. The nucleosomal core histone octamer at 3.1 A resolution: a tripartite protein assembly and a left-handed superhelix.
    Proc Natl Acad Sci U S A. 1991 Nov 15;88(22):10148-52 PMID: 1946434
  20. Nucleosome assembly: the CAF and the HAT.
    Curr Opin Cell Biol. 1996 Jun;8(3):369-73 PMID: 8743889
  21. Sperm decondensation in Xenopus egg cytoplasm is mediated by nucleoplasmin.
    Cell. 1991 May 17;65(4):569-78 PMID: 2032284
  22. Core histone hyperacetylation co-maps with generalized DNase I sensitivity in the chicken beta-globin chromosomal domain.
    EMBO J. 1994 Apr 15;13(8):1823-30 PMID: 8168481
  23. A direct link between core histone acetylation and transcriptionally active chromatin.
    EMBO J. 1988 May;7(5):1395-402 PMID: 3409869
  24. Histone acetylation: chromatin in action.
    Trends Biochem Sci. 1997 Apr;22(4):128-32 PMID: 9149532
  25. Phosphorylation and activation of 13S condensin by Cdc2 in vitro.
    Science. 1998 Oct 16;282(5388):487-90 PMID: 9774278
  26. Phosphorylation of histone H3 at serine 10 is correlated with chromosome condensation during mitosis and meiosis in Tetrahymena.
    Proc Natl Acad Sci U S A. 1998 Jun 23;95(13):7480-4 PMID: 9636175
  27. Phosphorylation-induced rearrangement of the histone H3 NH2-terminal domain during mitotic chromosome condensation.
    J Cell Biol. 1999 Apr 19;145(2):225-35 PMID: 10209020
  28. SMC protein complexes and higher-order chromosome dynamics.
    Curr Opin Cell Biol. 1998 Jun;10(3):317-22 PMID: 9640531
  29. Reversible histone modifications and the chromosome cell cycle.
    Bioessays. 1992 Jan;14(1):9-16 PMID: 1312335
  30. Topoisomerase II does not play a scaffolding role in the organization of mitotic chromosomes assembled in Xenopus egg extracts.
    J Cell Biol. 1993 Feb;120(3):601-12 PMID: 8381118
  31. A heterodimeric coiled-coil protein required for mitotic chromosome condensation in vitro.
    Cell. 1994 Nov 4;79(3):449-58 PMID: 7954811
  32. Chromosome condensation in Xenopus mitotic extracts without histone H1.
    Science. 1993 Dec 24;262(5142):2033-5 PMID: 8266099
  33. ATP-dependent positive supercoiling of DNA by 13S condensin: a biochemical implication for chromosome condensation.
    Cell. 1997 Aug 22;90(4):625-34 PMID: 9288743
  34. Persistent interactions of core histone tails with nucleosomal DNA following acetylation and transcription factor binding.
    Mol Cell Biol. 1998 Nov;18(11):6293-304 PMID: 9774646
  35. Mitosis-specific phosphorylation of histone H3 initiates primarily within pericentromeric heterochromatin during G2 and spreads in an ordered fashion coincident with mitotic chromosome condensation.
    Chromosoma. 1997 Nov;106(6):348-60 PMID: 9362543
  36. Histone H3 phosphorylation is required for the initiation, but not maintenance, of mammalian chromosome condensation.
    J Cell Sci. 1998 Dec;111 ( Pt 23):3497-506 PMID: 9811564
  37. The N tails of histones H3 and H4 adopt a highly structured conformation in the nucleosome.
    J Mol Biol. 1997 Oct 31;273(3):503-8 PMID: 9356240
  38. Targeting chromatin disruption: Transcription regulators that acetylate histones.
    Cell. 1996 Mar 22;84(6):817-9 PMID: 8601304
  39. Phosphorylation of histone H3 is required for proper chromosome condensation and segregation.
    Cell. 1999 Apr 2;97(1):99-109 PMID: 10199406
  40. Characterization of topoisomerase II-DNA interaction and identification of a DNA-binding domain by ultraviolet laser crosslinking.
    FEBS Lett. 1996 Feb 12;380(1-2):127-32 PMID: 8603720
  41. Elasticity measurements show the existence of thin rigid cores inside mitotic chromosomes.
    J Cell Biol. 1999 Apr 19;145(2):215-23 PMID: 10209019
  42. Systems for the study of nuclear assembly, DNA replication, and nuclear breakdown in Xenopus laevis egg extracts.
    Methods Cell Biol. 1991;35:449-68 PMID: 1664032
  43. Role of histone tails in nucleosome remodeling by Drosophila NURF.
    EMBO J. 1997 Aug 1;16(15):4717-26 PMID: 9303316
  44. pEg7, a new Xenopus protein required for mitotic chromosome condensation in egg extracts.
    J Cell Biol. 1998 Dec 14;143(6):1437-46 PMID: 9852142
  45. Formation in vitro of sperm pronuclei and mitotic chromosomes induced by amphibian ooplasmic components.
    Science. 1983 May 13;220(4598):719-21 PMID: 6601299
  46. Nuclear assembly is independent of linker histones.
    Proc Natl Acad Sci U S A. 1994 Dec 20;91(26):12477-81 PMID: 7809061
Article Info
Journal
The EMBO journal
Abbr.
EMBO J
ISSN
0261-4189
DOI
10.1093/emboj/19.3.379
Published
2000-02-01
Pages
379-91
Language
English
Region
England
NLM ID
8208664
PMCID
PMC305575
Subset
IM
External Links
PubMed source DOI: 10.1093/emboj/19.3.379 PMC Full Text View journal details
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