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PMID: 12177448 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Review

Histone H3 variants specify modes of chromatin assembly.

Ahmad K, Henikoff S

Abstract

Histone variants have been known for 30 years, but their functions and the mechanism of their deposition are still largely unknown. Drosophila has three versions of histone H3. H3 packages the bulk genome, H3.3 marks active chromatin and may be essential for gene regulation, and Cid is the characteristic structural component of centromeric chromatin. We have characterized the properties of these histones by using a Drosophila cell-line system that allows precise analysis of both DNA replication and histone deposition. The deposition of H3 is restricted to replicating DNA. In striking contrast, H3.3 and Cid deposit throughout the cell cycle. Deposition of H3.3 occurs without any corresponding DNA replication. To confirm that the deposition of Cid is also replication-independent (RI), we examined centromere replication in cultured cells and neuroblasts. We found that centromeres replicate out of phase with heterochromatin and display replication patterns that may limit H3 deposition. This confirms that both variants undergo RI deposition, but at different locations in the nucleus. How variant histones accomplish RI deposition is unknown, and raises basic questions about the stability of nucleosomes, the machinery that accomplishes nucleosome assembly, and the functional organization of the nucleus. The different in vivo properties of H3, H3.3, and Cid set the stage for identifying the mechanisms by which they are differentially targeted. Here we suggest that local effects of "open" chromatin and broader effects of nuclear organization help to guide the two different H3 variants to their target sites.

MeSH Terms
Centromere Chromatin/metabolism DNA Replication Histones/chemistry,metabolism
Chemicals
Chromatin Histones
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Ahmad Kami
Fred Hutchinson Cancer Research Center, 1100 Fairview Avenue North, A1-162, Seattle, WA 98109, USA.
Henikoff Steven
References (60)
60 references, click to expand
  1. Heterochromatic deposition of centromeric histone H3-like proteins.
    Proc Natl Acad Sci U S A. 2000 Jan 18;97(2):716-21 PMID: 10639145
  2. The centromere paradox: stable inheritance with rapidly evolving DNA.
    Science. 2001 Aug 10;293(5532):1098-102 PMID: 11498581
  3. Distinct protein interaction domains and protein spreading in a complex centromere.
    Genes Dev. 2000 Apr 1;14(7):783-91 PMID: 10766735
  4. Centromere identity in Drosophila is not determined in vivo by replication timing.
    J Cell Biol. 2001 Aug 20;154(4):683-90 PMID: 11514585
  5. Specification of kinetochore-forming chromatin by the histone H3 variant CENP-A.
    J Cell Sci. 2001 Oct;114(Pt 19):3529-42 PMID: 11682612
  6. Domain organization at the centromere and neocentromere.
    Dev Cell. 2001 Aug;1(2):165-77 PMID: 11702777
  7. Chromatin assembly factor I and Hir proteins contribute to building functional kinetochores in S. cerevisiae.
    Genes Dev. 2002 Jan 1;16(1):85-100 PMID: 11782447
  8. Ctf3p, the Mis6 budding yeast homolog, interacts with Mcm22p and Mcm16p at the yeast outer kinetochore.
    Genes Dev. 2002 Jan 1;16(1):101-13 PMID: 11782448
  9. X-chromosome silencing in the germline of C. elegans.
    Development. 2002 Jan;129(2):479-92 PMID: 11807039
  10. Recurrent evolution of DNA-binding motifs in the Drosophila centromeric histone.
    Proc Natl Acad Sci U S A. 2002 Feb 5;99(3):1449-54 PMID: 11805302
  11. Nuclear architecture and spatial positioning help establish transcriptional states of telomeres in yeast.
    Nat Cell Biol. 2002 Mar;4(3):214-21 PMID: 11862215
  12. Conserved organization of centromeric chromatin in flies and humans.
    Dev Cell. 2002 Mar;2(3):319-30 PMID: 11879637
  13. Heterochromatin: new possibilities for the inheritance of structure.
    Curr Opin Genet Dev. 2002 Apr;12(2):178-87 PMID: 11893491
  14. The contribution of nuclear compartmentalization to gene regulation.
    Cell. 2002 Feb 22;108(4):513-21 PMID: 11909522
  15. Nucleosome remodeling induced by RNA polymerase II: loss of the H2A/H2B dimer during transcription.
    Mol Cell. 2002 Mar;9(3):541-52 PMID: 11931762
  16. Genome-wide location and regulated recruitment of the RSC nucleosome-remodeling complex.
    Genes Dev. 2002 Apr 1;16(7):806-19 PMID: 11937489
  17. CENP-I is essential for centromere function in vertebrate cells.
    Dev Cell. 2002 Apr;2(4):463-76 PMID: 11970896
  18. Centromeric localization and adaptive evolution of an Arabidopsis histone H3 variant.
    Plant Cell. 2002 May;14(5):1053-66 PMID: 12034896
  19. The histone variant H3.3 marks active chromatin by replication-independent nucleosome assembly.
    Mol Cell. 2002 Jun;9(6):1191-200 PMID: 12086617
  20. Yeast centromere DNA is in a unique and highly ordered structure in chromosomes and small circular minichromosomes.
    Cell. 1982 Jun;29(2):305-17 PMID: 6288253
  21. Common features of analogous replacement histone H3 genes in animals and plants.
    J Mol Evol. 1996 Sep;43(3):194-206 PMID: 8703085
  22. The localization of histone H3.3 in germ line chromatin of Drosophila males as established with a histone H3.3-specific antiserum.
    Chromosoma. 1997 Nov;106(6):335-47 PMID: 9362542
  23. Immunolocalization of CENP-A suggests a distinct nucleosome structure at the inner kinetochore plate of active centromeres.
    Curr Biol. 1997 Nov 1;7(11):901-4 PMID: 9382805
  24. Centromeres: the missing link in the development of human artificial chromosomes.
    Curr Opin Genet Dev. 1998 Apr;8(2):219-25 PMID: 9610413
  25. A mutation in NPS1/STH1, an essential gene encoding a component of a novel chromatin-remodeling complex RSC, alters the chromatin structure of Saccharomyces cerevisiae centromeres.
    Nucleic Acids Res. 1998 Jul 1;26(13):3286-92 PMID: 9628931
  26. Replication-dependent marking of DNA by PCNA facilitates CAF-1-coupled inheritance of chromatin.
    Cell. 1999 Feb 19;96(4):575-85 PMID: 10052459
  27. A histone-H3-like protein in C. elegans.
    Nature. 1999 Oct 7;401(6753):547-8 PMID: 10524621
  28. Histone rearrangements accompany nuclear differentiation and dedifferentiation in Tetrahymena.
    Dev Biol. 1984 Feb;101(2):282-94 PMID: 6692982
  29. Changes in histones H2A and H3 variant composition in differentiating and mature rat brain cortical neurons.
    Dev Biol. 1987 Sep;123(1):51-8 PMID: 3622934
  30. Time of replication of yeast centromeres and telomeres.
    Cell. 1988 Aug 12;54(4):505-13 PMID: 3042152
  31. In vivo studies on the dynamics of histone-DNA interaction: evidence for nucleosome dissolution during replication and transcription and a low level of dissolution independent of both.
    Biochemistry. 1990 Jan 23;29(3):719-31 PMID: 1692479
  32. A view of interphase chromosomes.
    Science. 1990 Dec 14;250(4987):1533-40 PMID: 2274784
  33. The centromere-kinetochore complex: a repeat subunit model.
    J Cell Biol. 1991 Jun;113(5):1091-110 PMID: 1828250
  34. The regulation of histone synthesis in the cell cycle.
    Annu Rev Biochem. 1991;60:827-61 PMID: 1883210
  35. A Drosophila melanogaster H3.3 cDNA encodes a histone variant identical with the vertebrate H3.3.
    Gene. 1991 Nov 15;107(2):341-2 PMID: 1748304
  36. Dynamic organization of DNA replication in mammalian cell nuclei: spatially and temporally defined replication of chromosome-specific alpha-satellite DNA sequences.
    J Cell Biol. 1992 Mar;116(5):1095-110 PMID: 1740468
  37. Histone synthesis and turnover in alfalfa. Fast loss of highly acetylated replacement histone variant H3.2.
    J Biol Chem. 1993 Mar 5;268(7):4912-7 PMID: 8444869
  38. A histone octamer can step around a transcribing polymerase without leaving the template.
    Cell. 1994 Jan 28;76(2):371-82 PMID: 8293470
  39. Structural analysis of alpha-satellite DNA and centromere proteins using extended chromatin and chromosomes.
    Hum Mol Genet. 1994 May;3(5):697-709 PMID: 8081355
  40. A mutation in CSE4, an essential gene encoding a novel chromatin-associated protein in yeast, causes chromosome nondisjunction and cell cycle arrest at mitosis.
    Genes Dev. 1995 Mar 1;9(5):573-86 PMID: 7698647
  41. Structure and expression of histone H3.3 genes in Drosophila melanogaster and Drosophila hydei.
    Genome. 1995 Jun;38(3):586-600 PMID: 7557364
  42. Heterogeneity of eukaryotic replicons, replicon clusters, and replication foci.
    Chromosoma. 2000 Mar;108(8):471-84 PMID: 10794569
  43. De novo nucleosome assembly: new pieces in an old puzzle.
    Genes Dev. 2000 Jun 15;14(12):1430-8 PMID: 10859162
  44. Requirement of Mis6 centromere connector for localizing a CENP-A-like protein in fission yeast.
    Science. 2000 Jun 23;288(5474):2215-9 PMID: 10864871
  45. Histone-histone interactions and centromere function.
    Mol Cell Biol. 2000 Aug;20(15):5700-11 PMID: 10891506
  46. Tension on chromosomes increases the number of kinetochore microtubules but only within limits.
    J Cell Sci. 2000 Nov;113 Pt 21:3815-23 PMID: 11034909
  47. Characterisation of transcriptionally active and inactive chromatin domains in neurons.
    J Cell Sci. 2000 Dec;113 Pt 24:4463-74 PMID: 11082040
  48. Chromatin assembly at kinetochores is uncoupled from DNA replication.
    J Cell Biol. 2000 Nov 27;151(5):1113-8 PMID: 11086012
  49. The human SWI/SNF-B chromatin-remodeling complex is related to yeast rsc and localizes at kinetochores of mitotic chromosomes.
    Proc Natl Acad Sci U S A. 2000 Nov 21;97(24):13015-20 PMID: 11078522
  50. Chromatin-bound PCNA complex formation triggered by DNA damage occurs independent of the ATM gene product in human cells.
    Nucleic Acids Res. 2001 Mar 15;29(6):1341-51 PMID: 11239001
  51. A solid foundation: functional specialization of centromeric chromatin.
    Curr Opin Genet Dev. 2001 Apr;11(2):182-8 PMID: 11250142
  52. The hinge and chromo shadow domain impart distinct targeting of HP1-like proteins.
    Mol Cell Biol. 2001 Apr;21(7):2555-69 PMID: 11259603
  53. Centromeres are specialized replication domains in heterochromatin.
    J Cell Biol. 2001 Apr 2;153(1):101-10 PMID: 11285277
  54. Modulation of a transcription factor counteracts heterochromatic gene silencing in Drosophila.
    Cell. 2001 Mar 23;104(6):839-47 PMID: 11290322
  55. Unfolding individual nucleosomes by stretching single chromatin fibers with optical tweezers.
    Nat Struct Biol. 2001 Jul;8(7):606-10 PMID: 11427891
  56. Chromatin organization and its relation to replication and histone acetylation during the cell cycle in barley.
    Chromosoma. 2001 May;110(2):83-92 PMID: 11453558
  57. The role of Drosophila CID in kinetochore formation, cell-cycle progression and heterochromatin interactions.
    Nat Cell Biol. 2001 Aug;3(8):730-9 PMID: 11483958
  58. Determining centromere identity: cyclical stories and forking paths.
    Nat Rev Genet. 2001 Aug;2(8):584-96 PMID: 11483983
  59. Translating the histone code.
    Science. 2001 Aug 10;293(5532):1074-80 PMID: 11498575
  60. Integrated cytogenetic map of chromosome arm 4S of A. thaliana: structural organization of heterochromatic knob and centromere region.
    Cell. 2000 Feb 4;100(3):367-76 PMID: 10676818
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
2002-12-10
Epub
2002-00-12
Pages
16477-84
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC139911
Subset
IM
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