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Identification of 67 Histone Marks and Histone Lysine Crotonylation as a New Type of Histone Modification
Open accessAbstract
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.
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“Histone crotonylation was previously shown to occur at the promoters or enhancers of gens that are actively transcribed, and play a role in spermatogenesis.111,179”
From Epigenetic regulation in major depression and other stress-related disorders: molecular mechanisms, clinical relevance and therapeutic potential (2023) · cites this paper as [179]
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“A number of functional studies have concentrated on histone lysine-crotonylation (Lys-cr) which is associated with active chromatin and overlaps with known sites of lysine-acetylation (Lys-ac)3,9.”
From Histone deacetylase (HDAC) 1 and 2 complexes regulate both histone acetylation and crotonylation in vivo (2018) · cites this paper as [3]
In the citing paper
“Previous studies failed to detect significant decrotonylase activity for HDAC1/23,18 and this may be because they were using recombinant enzymes generated in isolation.”
From Histone deacetylase (HDAC) 1 and 2 complexes regulate both histone acetylation and crotonylation in vivo (2018) · cites this paper as [3]
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Cites
Chromatin modifications and their function
Kouzarides, T. (2007) · Cell · doi:10.1016/j.cell.2007.02.005 · Cited by 10,883
Crystal structure of the nucleosome core particle at 2.8 Å resolution
Luger, K., Mäder, A. W., Richmond, R. K., Sargent, D. F., & Richmond, T. J. (1997) · Nature · doi:10.1038/38444 · Cited by 9,466
Heintzman, N. D., Stuart, R. K., Hon, G., Fu, Y., Ching, C. W., Hawkins, R. D., Barrera, L. O., Van Calcar, S., Qu, C., Ching, K. A., et al. (2007) · Nature Genetics · doi:10.1038/ng1966 · Cited by 3,398 · cited 1×
“As a control, we compared the Kcr distribution with previously obtained ChIP-seq results for H3K4me3 (marking gene promoters) and H3K4me1 (marking enhancers) distribution (Heintzman et al., 2007).”
ResultSelf-citationHistological and Histopathological Evaluation of the Testis
Russell, L. D., Ettlin, R. A., Hikim, A. P. S., & Clegg, E. D. (1993) · International Journal of Andrology · doi:10.1111/j.1365-2605.1993.tb01156.x · Cited by 2,249
Substrate and Functional Diversity of Lysine Acetylation Revealed by a Proteomics Survey
Kim, S. C., Sprung, R., Chen, Y., Xu, Y., Ball, H., Pei, J., Cheng, T., Kho, Y., Xiao, H., Xiao, L., et al. (2006) · Molecular Cell · doi:10.1016/j.molcel.2006.06.026 · Cited by 1,487
Self-citationHistones and histone modifications
Peterson, C. L., & Laniel, M.-A. (2004) · Current Biology · doi:10.1016/j.cub.2004.07.007 · Cited by 1,313
A PHD finger of NURF couples histone H3 lysine 4 trimethylation with chromatin remodelling
Wysocka, J., Swigut, T., Xiao, H., Milne, T. A., Kwon, S. Y., Landry, J., Kauer, M., Tackett, A. J., Chait, B. T., Badenhorst, P. W., et al. (2006) · Nature · doi:10.1038/nature04815 · Cited by 1,226
Self-citationExtraction, purification and analysis of histones
Shechter, D., Dormann, H. L., Allis, C. D., & Hake, S. B. (2007) · Nature Protocols · doi:10.1038/nprot.2007.202 · Cited by 1,054
Multivalent engagement of chromatin modifications by linked binding modules
Ruthenburg, A. J., Li, H., Patel, D. J., & Allis, C. D. (2007) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2298 · Cited by 1,039
McGhee, J. D., & Felsenfeld, G. (1980) · Annual Review of Biochemistry · doi:10.1146/annurev.bi.49.070180.005343 · Cited by 976
New nomenclature for chromatin-modifying enzymes
Allis, C. D., Berger, S. L., Cote, J., Dent, S., Jenuwien, T., Kouzarides, T., Pillus, L., Reinberg, D., Shi, Y., Shiekhattar, R., et al. (2007) · Cell · doi:10.1016/j.cell.2007.10.039 · Cited by 957
Wysocka, J., Swigut, T., Milne, T. A., Dou, Y., Zhang, X., Burlingame, A. L., Roeder, R. G., Brivanlou, A. H., & Allis, C. D. (2005) · Cell · doi:10.1016/j.cell.2005.03.036 · Cited by 845
Self-citationDistinct epigenomic landscapes of pluripotent and lineage-committed human cells
Hawkins, R. D., Hon, G. C., Lee, L. K., Ngo, Q., Lister, R., Pelizzola, M., Edsall, L. E., Kuan, S., Luu, Y., Klugman, S., et al. (2010) · Cell stem cell · doi:10.1016/j.stem.2010.03.018 · Cited by 806
Self-citationThe key to development: interpreting the histone code?
Margueron, R., Trojer, P., & Reinberg, D. (2005) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2005.01.005 · Cited by 770
Lysine propionylation and butyrylation are novel post-translational modifications in histones
Chen, Y., Sprung, R., Tang, Y., Ball, H., Sangras, B., Kim, S. C., Falck, J. R., Peng, J., Gu, W., & Zhao, Y. (2007) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m700021-mcp200 · Cited by 764
Self-citationBromodomain: an acetyl‐lysine binding domain
Zeng, L., & Zhou, M. (2002) · FEBS Letters · doi:10.1016/s0014-5793(01)03309-9 · Cited by 751
Meiotic sex chromosome inactivation
Turner, J. M. A. (2007) · Development · doi:10.1242/dev.000018 · Cited by 751
Aberrant Epigenetic Landscape in Cancer: How Cellular Identity Goes Awry
Berdasco, M., & Esteller, M. (2010) · Developmental Cell · doi:10.1016/j.devcel.2010.10.005 · Cited by 651
Histone H3.3 is enriched in covalent modifications associated with active chromatin
McKittrick, E., Gafken, P. R., Ahmad, K., & Henikoff, S. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0308092100 · Cited by 520
Role of Jhdm2a in regulating metabolic gene expression and obesity resistance
Tateishi, K., Okada, Y., Kallin, E. M., & Zhang, Y. (2009) · Nature · doi:10.1038/nature07777 · Cited by 442
Histone H1 and its isoforms: Contribution to chromatin structure and function
Happel, N., & Doenecke, D. (2008) · Gene · doi:10.1016/j.gene.2008.11.003 · Cited by 424
Regulated nucleosome mobility and the histone code
Cosgrove, M. S., Boeke, J. D., & Wolberger, C. (2004) · Nature Structural & Molecular Biology · doi:10.1038/nsmb851 · Cited by 421
Postmeiotic Sex Chromatin in the Male Germline of Mice
Namekawa, S. H., Park, P. J., Zhang, L., Shima, J. E., McCarrey, J. R., Griswold, M. D., & Lee, J. T. (2006) · Current Biology · doi:10.1016/j.cub.2006.01.066 · Cited by 396
Chemical derivatization of histones for facilitated analysis by mass spectrometry
Garcia, B. A., Mollah, S., Ueberheide, B. M., Busby, S. A., Muratore‐Schroeder, T. L., Shabanowitz, J., & Hunt, D. F. (2007) · Nature Protocols · doi:10.1038/nprot.2007.106 · Cited by 389
β- N -acetylglucosamine (O-GlcNAc) is part of the histone code
Sakabe, K., Wang, Z., & Hart, G. W. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1009023107 · Cited by 387
Arents, G., & Moudrianakis, E. N. (1993) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.90.22.10489 · Cited by 346
Füllgrabe, J., Kavanagh, E. T., & Joseph, B. (2011) · Oncogene · doi:10.1038/onc.2011.121 · Cited by 322
High Throughput Characterization of Combinatorial Histone Codes
Young, N. L., DiMaggio, P. A., Plazas-Mayorca, M. D., Baliban, R. C., Floudas, C. A., & Garcia, B. A. (2009) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m900238-mcp200 · Cited by 316
Organismal Differences in Post-translational Modifications in Histones H3 and H4
Garcia, B. A., Hake, S. B., Diaz, R. L., Kauer, M., Morris, S. A., Recht, J., Shabanowitz, J., Mishra, N., Strahl, B. D., Allis, C. D., et al. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m607900200 · Cited by 314
The mouse X chromosome is enriched for multicopy testis genes showing postmeiotic expression
Mueller, J. L., Mahadevaiah, S. K., Park, P. J., Warburton, P. E., Page, D. C., & Turner, J. M. A. (2008) · Nature Genetics · doi:10.1038/ng.126 · Cited by 305
Pivôt-Pajot, C., Caron, C., Govin, J., Vion, A., Rousseaux, S., & Khochbin, S. (2003) · Molecular and Cellular Biology · doi:10.1128/mcb.23.15.5354-5365.2003 · Cited by 286
Self-citationIdentification of novel histone post-translational modifications by peptide mass fingerprinting
Zhang, L., Eugeni, E. E., Parthun, M. R., & Freitas, M. A. (2003) · Chromosoma · doi:10.1007/s00412-003-0244-6 · Cited by 274
In Vivo Residue-specific Histone Methylation Dynamics
Zee, B. M., Levin, R. S., Xu, B., LeRoy, G., Wingreen, N. S., & Garcia, B. A. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.063784 · Cited by 270
Hazzouri, M., Pivôt-Pajot, C., Faure, A.-K., Usson, Y., Pelletier, R., Sèle, B., Khochbin, S., & Rousseaux, S. (2000) · European Journal of Cell Biology · doi:10.1078/0171-9335-00123 · Cited by 267
Self-citationJohnson, L. M. (2004) · Nucleic Acids Research · doi:10.1093/nar/gkh992 · Cited by 258
The role of histones in chromatin remodelling during mammalian spermiogenesis
Govin, J., Caron, C., Lestrat, C., Rousseaux, S., & Khochbin, S. (2004) · European Journal of Biochemistry · doi:10.1111/j.1432-1033.2004.04266.x · Cited by 255
Self-citationPervasive combinatorial modification of histone H3 in human cells
Garcia, B. A., Pesavento, J. J., Mizzen, C. A., & Kelleher, N. L. (2007) · Nature Methods · doi:10.1038/nmeth1052 · Cited by 243
Mechanisms of epigenetic inheritance
Martin, C., & Zhang, Y. (2007) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2007.04.002 · Cited by 239
Wiśniewski, J. R., Zougman, A., Krüger, S., & Mann, M. (2006) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m600255-mcp200 · Cited by 233
Mersfelder, E. L., & Parthun, M. R. (2006) · Nucleic Acids Research · doi:10.1093/nar/gkl338 · Cited by 221
Differential histone modifications mark mouse imprinting control regions during spermatogenesis
Delaval, K., Govin, J., Cerqueira, F., Rousseaux, S., Khochbin, S., & Feil, R. (2007) · The EMBO Journal · doi:10.1038/sj.emboj.7601513 · Cited by 218
Self-citationSnapShot: Histone-Modifying Enzymes
Kouzarides, T. (2007) · Cell · doi:10.1016/j.cell.2007.11.005 · Cited by 213
Jiang, T., Zhou, X., Taghizadeh, K., Dong, M., & Dedon, P. C. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0606775103 · Cited by 209
Kotaja, N., Kimmins, S., Brancorsini, S., Hentsch, D., Vonesch, J., Davidson, I., Parvinen, M., & Sassone‐Corsi, P. (2004) · Nature Methods · doi:10.1038/nmeth1204-249 · Cited by 196
Zhao, M., Shirley, C. R., Hayashi, S., Marcon, L., Mohapatra, B., Suganuma, R., Behringer, R. R., Boissonneault, G., Yanagimachi, R., & Meistrich, M. L. (2004) · genesis · doi:10.1002/gene.20019 · Cited by 194
From meiosis to postmeiotic events: The secrets of histone disappearance
Gaucher, J., Reynoird, N., Montellier, E., Boussouar, F., Rousseaux, S., & Khochbin, S. (2009) · FEBS Journal · doi:10.1111/j.1742-4658.2009.07504.x · Cited by 178
Self-citationChen, Y., Kwon, S. W., Kim, S. C., & Zhao, Y. (2005) · Journal of Proteome Research · doi:10.1021/pr049754t · Cited by 177
Self-citationBBAP Monoubiquitylates Histone H4 at Lysine 91 and Selectively Modulates the DNA Damage Response
Yan, Q., Dutt, S., Xu, R., Graves, K., Juszczyński, P., Manis, J. P., & Shipp, M. A. (2009) · Molecular Cell · doi:10.1016/j.molcel.2009.08.019 · Cited by 171
Wiśniewski, J. R., Zougman, A., & Mann, M. (2008) · Nucleic Acids Research · doi:10.1093/nar/gkm1057 · Cited by 163
Characterization of histones and their post-translational modifications by mass spectrometry
Garcia, B. A., Shabanowitz, J., & Hunt, D. F. (2006) · Current Opinion in Chemical Biology · doi:10.1016/j.cbpa.2006.11.022 · Cited by 143
Deposition-related histone acetylation in micronuclei of conjugating Tetrahymena.
Allis, C. D., Chicoine, L., Richman, R., & Schulman, I. G. (1985) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.82.23.8048 · Cited by 141
Freitas, M. A., Sklenar, A. R., & Parthun, M. R. (2004) · Journal of Cellular Biochemistry · doi:10.1002/jcb.20106 · Cited by 140
Chen, Y., Chen, W., Cobb, M. H., & Zhao, Y. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0811739106 · Cited by 102
Self-citationChew, Y. C., Camporeale, G., Kothapalli, N. R., Sarath, G., & Zempleni, J. (2005) · The Journal of Nutritional Biochemistry · doi:10.1016/j.jnutbio.2005.05.003 · Cited by 98
Modifications of Human Histone H3 Variants during Mitosis
Garcia, B. A., Barber, C. M., Hake, S. B., Ptak, C., Turner, F. B., Busby, S. A., Shabanowitz, J., Moran, R. G., Allis, C. D., & Hunt, D. F. (2005) · Biochemistry · doi:10.1021/bi050906n · Cited by 96
Luo, H., Li, Y., Mu, J.-J., Zhang, J., Tonaka, T., Hamamori, Y., Jung, S. Y., Wáng, Y., & Qin, J. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m802299200 · Cited by 80
Self-citationFeixia Chu, C., Nusinow, D. A., Chalkley, R. J., Plath, K., Panning, B., & Burlingame, A. L. (2005) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m500285-mcp200 · Cited by 78
A new insight into male genome reprogramming by histone variants and histone code
Boussouar, F., Rousseaux, S., & Khochbin, S. (2008) · Cell Cycle · doi:10.4161/cc.7.22.6975 · Cited by 47
Self-citationMapping of Lysine Monomethylation of Linker Histones in Human Breast and Its Cancer
Lu, A., Zougman, A., Pudełko, M., Bębenek, M., Ziolkowski, P. P., Mann, M., & Wiśniewski, J. R. (2009) · Journal of Proteome Research · doi:10.1021/pr9000652 · Cited by 28
MS/MS/MS Reveals False Positive Identification of Histone Serine Methylation
Zhang, J., Chen, Y., Zhang, Z., Xing, G., Wysocka, J., & Zhao, Y. (2009) · Journal of Proteome Research · doi:10.1021/pr900864s · Cited by 20
Self-citationNelson, M. A., Foxwell, A. R., Tyrer, P. C., & Dean, R. T. (2006) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2006.10.004 · Cited by 16
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Metadata
- Authors
- Tan, M., Luo, H., Lee, S., Jin, F., Yang, J. S., 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.
- Affiliations
- University of Chicago (US)
- University of California San Diego (US)
- Inserm (FR)
- Chinese Academy of Sciences (CN)
- Stanford Medicine (US)
- Corresponding author
- Zhao, Yingming
- ORCID
- Venue
- Cell
- Publisher
- Elsevier BV
- Published
- 2011-09
- Volume
- 146
- Issue
- 6
- Pages
- 1016-1028
- ISSN
- 0092-8674 (ISSN-L)
- PMC
- PMC3176443
- OpenAlex
- W2115862579
- Cited by
- 1,902
- References
- 61
- Citations by year
- 2026: 114 · 2025: 144 · 2024: 144 · 2023: 140 · 2022: 127 · 2021: 143 · 2020: 119 · 2019: 108 · 2018: 121 · 2017: 111 · 2016: 138 · 2015: 133 · 2014: 136 · 2013: 110 · 2012: 104
- FWCI
- 46.19
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Cell (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- Funders
- Agence Nationale de la Recherche
- Institut National Du Cancer
- National Institutes of Health
- Direction de l’hospitalisation et de l’offre de Soins
- National Cancer Institute (R01CA126832)
- National Institute of Diabetes and Digestive and Kidney Diseases (R01DK082664)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Cancer-related gene regulation
- Keywords
- histone modifications, lysine acetylation, male germ cells, sex chromosome inactivation, X-linked genes, testis-specific genes, enhancers, promoter, meiosis, sex chromosomes
- MeSH terms
- Animals, Gene Expression Regulation, HeLa Cells, Histones, Humans, Lysine, Male, Meiosis, Protein Processing, Post-Translational, Testis, Histone Code, Mice
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