Home LiteratureArticle Details
PMID: 21925322 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Identification of 67 histone marks and histone lysine crotonylation as a new type of histone modification.

Cell ·Vol. 146 ·No. 6 ·2011-09-16 ·Pages 1016-28

Tan M, Luo H, Lee S, Jin F, Yang JS, Montellier E, Buchou T, Cheng Z, Rousseaux S, Rajagopal N, Lu Z, Ye Z, Zhu Q, Wysocka J, Ye Y, Khochbin S, Ren B, Zhao Y

Abstract

We report the identification of 67 previously undescribed histone modifications, increasing the current number of known histone marks by about 70%. We further investigated one of the marks, lysine crotonylation (Kcr), confirming that it represents an evolutionarily-conserved histone posttranslational modification. The unique structure and genomic localization of histone Kcr suggest that it is mechanistically and functionally different from histone lysine acetylation (Kac). Specifically, in both human somatic and mouse male germ cell genomes, histone Kcr marks either active promoters or potential enhancers. In male germinal cells immediately following meiosis, Kcr is enriched on sex chromosomes and specifically marks testis-specific genes, including a significant proportion of X-linked genes that escape sex chromosome inactivation in haploid cells. These results therefore dramatically extend the repertoire of histone PTM sites and designate Kcr as a specific mark of active sex chromosome-linked genes in postmeiotic male germ cells.

MeSH Terms
Animals Gene Expression Regulation HeLa Cells Histone Code Histones/chemistry,metabolism Humans Lysine/metabolism Male Meiosis Mice Protein Processing, Post-Translational Testis/cytology,metabolism
Chemicals
Histones Lysine
Authors & Affiliations
18 authors, click to expand affiliations / ORCID
Tan Minjia
Ben May Department of Cancer Research, The University of Chicago, Chicago, IL 60637, USA.
Luo Hao
Lee Sangkyu
Jin Fulai
Yang Jeong Soo
Montellier Emilie
Buchou Thierry
Cheng Zhongyi
Rousseaux Sophie
Rajagopal Nisha
Lu Zhike
Ye Zhen
Zhu Qin
Wysocka Joanna
Ye Yang
Khochbin Saadi
Ren Bing
Zhao Yingming
References (37)
37 references, click to expand
  1. Chromatin modifications and their function.
    Cell. 2007 Feb 23;128(4):693-705 PMID: 17320507
  2. From meiosis to postmeiotic events: the secrets of histone disappearance.
    FEBS J. 2010 Feb;277(3):599-604 PMID: 20015078
  3. The tale beyond the tail: histone core domain modifications and the regulation of chromatin structure.
    Nucleic Acids Res. 2006 May 19;34(9):2653-62 PMID: 16714444
  4. Deposition-related histone acetylation in micronuclei of conjugating Tetrahymena.
    Proc Natl Acad Sci U S A. 1985 Dec;82(23):8048-52 PMID: 3865215
  5. Meiotic sex chromosome inactivation.
    Development. 2007 May;134(10):1823-31 PMID: 17329371
  6. Mass spectrometry analysis of Arabidopsis histone H3 reveals distinct combinations of post-translational modifications.
    Nucleic Acids Res. 2004 Dec 14;32(22):6511-8 PMID: 15598823
  7. Chemical derivatization of histones for facilitated analysis by mass spectrometry.
    Nat Protoc. 2007;2(4):933-8 PMID: 17446892
  8. Aberrant epigenetic landscape in cancer: how cellular identity goes awry.
    Dev Cell. 2010 Nov 16;19(5):698-711 PMID: 21074720
  9. Transition nuclear proteins are required for normal chromatin condensation and functional sperm development.
    Genesis. 2004 Apr;38(4):200-13 PMID: 15083521
  10. Characterization of histones and their post-translational modifications by mass spectrometry.
    Curr Opin Chem Biol. 2007 Feb;11(1):66-73 PMID: 17157550
  11. WDR5 associates with histone H3 methylated at K4 and is essential for H3 K4 methylation and vertebrate development.
    Cell. 2005 Jun 17;121(6):859-72 PMID: 15960974
  12. Nucleosome structure.
    Annu Rev Biochem. 1980;49:1115-56 PMID: 6996562
  13. PTMap--a sequence alignment software for unrestricted, accurate, and full-spectrum identification of post-translational modification sites.
    Proc Natl Acad Sci U S A. 2009 Jan 20;106(3):761-6 PMID: 19136633
  14. The key to development: interpreting the histone code?
    Curr Opin Genet Dev. 2005 Apr;15(2):163-76 PMID: 15797199
  15. Regulated hyperacetylation of core histones during mouse spermatogenesis: involvement of histone deacetylases.
    Eur J Cell Biol. 2000 Dec;79(12):950-60 PMID: 11152286
  16. Mass spectrometric mapping of linker histone H1 variants reveals multiple acetylations, methylations, and phosphorylation as well as differences between cell culture and tissue.
    Mol Cell Proteomics. 2007 Jan;6(1):72-87 PMID: 17043054
  17. Topography of the histone octamer surface: repeating structural motifs utilized in the docking of nucleosomal DNA.
    Proc Natl Acad Sci U S A. 1993 Nov 15;90(22):10489-93 PMID: 8248135
  18. Integrated approach for manual evaluation of peptides identified by searching protein sequence databases with tandem mass spectra.
    J Proteome Res. 2005 May-Jun;4(3):998-1005 PMID: 15952748
  19. Bromodomain: an acetyl-lysine binding domain.
    FEBS Lett. 2002 Feb 20;513(1):124-8 PMID: 11911891
  20. In vivo residue-specific histone methylation dynamics.
    J Biol Chem. 2010 Jan 29;285(5):3341-50 PMID: 19940157
  21. Postmeiotic sex chromatin in the male germline of mice.
    Curr Biol. 2006 Apr 4;16(7):660-7 PMID: 16581510
  22. Mapping post-translational modifications of the histone variant MacroH2A1 using tandem mass spectrometry.
    Mol Cell Proteomics. 2006 Jan;5(1):194-203 PMID: 16210244
  23. Beta-N-acetylglucosamine (O-GlcNAc) is part of the histone code.
    Proc Natl Acad Sci U S A. 2010 Nov 16;107(46):19915-20 PMID: 21045127
  24. Multivalent engagement of chromatin modifications by linked binding modules.
    Nat Rev Mol Cell Biol. 2007 Dec;8(12):983-94 PMID: 18037899
  25. Substrate and functional diversity of lysine acetylation revealed by a proteomics survey.
    Mol Cell. 2006 Aug;23(4):607-18 PMID: 16916647
  26. The mouse X chromosome is enriched for multicopy testis genes showing postmeiotic expression.
    Nat Genet. 2008 Jun;40(6):794-9 PMID: 18454149
  27. Distinct and predictive chromatin signatures of transcriptional promoters and enhancers in the human genome.
    Nat Genet. 2007 Mar;39(3):311-8 PMID: 17277777
  28. The role of histones in chromatin remodelling during mammalian spermiogenesis.
    Eur J Biochem. 2004 Sep;271(17):3459-69 PMID: 15317581
  29. Mechanisms of epigenetic inheritance.
    Curr Opin Cell Biol. 2007 Jun;19(3):266-72 PMID: 17466502
  30. A new insight into male genome reprogramming by histone variants and histone code.
    Cell Cycle. 2008 Nov 15;7(22):3499-502 PMID: 19001855
  31. Crystal structure of the nucleosome core particle at 2.8 A resolution.
    Nature. 1997 Sep 18;389(6648):251-60 PMID: 9305837
  32. Pervasive combinatorial modification of histone H3 in human cells.
    Nat Methods. 2007 Jun;4(6):487-9 PMID: 17529979
  33. Histone onco-modifications.
    Oncogene. 2011 Aug 4;30(31):3391-403 PMID: 21516126
  34. Regulated nucleosome mobility and the histone code.
    Nat Struct Mol Biol. 2004 Nov;11(11):1037-43 PMID: 15523479
  35. Regulation of intra-S phase checkpoint by ionizing radiation (IR)-dependent and IR-independent phosphorylation of SMC3.
    J Biol Chem. 2008 Jul 11;283(28):19176-83 PMID: 18442975
  36. Distinct epigenomic landscapes of pluripotent and lineage-committed human cells.
    Cell Stem Cell. 2010 May 7;6(5):479-91 PMID: 20452322
  37. A PHD finger of NURF couples histone H3 lysine 4 trimethylation with chromatin remodelling.
    Nature. 2006 Jul 6;442(7098):86-90 PMID: 16728976
Article Info
Journal
Cell
Abbr.
Cell
ISSN
1097-4172
DOI
10.1016/j.cell.2011.08.008
Published
2011-09-16
Pages
1016-28
Language
English
Region
United States
NLM ID
0413066
PMCID
PMC3176443
Subset
IM
Grants
NCI NIH HHS · R01 CA126832 · United States
NCI NIH HHS · R01 CA126832-06 · United States
NIDDK NIH HHS · R01 DK082664 · United States
NIDDK NIH HHS · R01 DK082664-04 · United States
Corrections
CommentIn
PMID: 21946920
External Links
PubMed source DOI: 10.1016/j.cell.2011.08.008 PMC Full Text View journal details
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2