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. 2015 Sep;7(9):a025064. doi: 10.1101/cshperspect.a025064

Comprehensive Catalog of Currently Documented Histone Modifications

Yingming Zhao 1, Benjamin A Garcia 2
PMCID: PMC4563710  NIHMSID: NIHMS873521  PMID: 26330523

SUMMARY

Modern techniques in molecular biology, genomics, and mass spectrometry–based proteomics have identified a large number of novel histone posttranslational modifications (PTMs), many of whose functions are still under intense investigation. Here, we catalog histone PTMs under two classes: first, those whose functions have been fairly well studied and, second, those PTMs that have been more recently identified but whose functions remain unclear. We hope that this will be a useful resource for researchers from all biological or technical backgrounds, aiding in their chromatin and epigenetic pursuits.

This extensive summary of all known histone posttranslational modifications, their locations and functions, modifying enzymes, and primary references will be useful to all working in the field of epigenetics.

Histone posttranslational modifications (PTMs) have been linked to a variety of processes, including transcription, DNA replication, and DNA damage (Kouzarides 2007; Murr 2010; for a list of reviews, see Suggested Reviews). The growing list of histone PTMs has exploded in the last several years as a consequence of the considerable advances in available antibody reagents, peptide and protein array technology, and mass spectrometry–based proteomics (Karch et al. 2013). These approaches allow for identification and quantification of histone PTMs from global or more local chromatin states, especially when combined with chromatin immunoprecipitation experiments (Han and Garcia 2013). Here, we attempt to catalog the ever-growing number of histone PTMs that have been studied over the last several years. The tables are broken down into two groups: Section 1 (Tables 1–8) lists the histone PTMs that have been studied more and thus some functional aspects are known concerning the marks; Section 2 (Tables 9–16) lists the histone PTMs that have been detected, but in which rather limited function has been determined. The latter category of histone marks, being in their observed infancy, is very intriguing and represents a large opportunity for the chromatin biology and epigenetics communities to decipher their biological consequences and outcomes in the years to come. Histone acetylation and methylation were first discovered about 50 years ago (Allfrey et al. 1964); however, only in the last decade or so has its physiological function been uncovered. We anticipate that this will serve as a useful resource for those already working in the field, but also as motivation for those newer scientists beginning their research work in this area to continue to push the boundaries of knowledge.

Model organism key
An Aspergillus nidulans
At Arabidopsis thaliana
Bt Bos torus
Ce Caenorhabditis elegans
Dm Drosophila melanogaster
Hs Homo sapiens
Mm Mus musculus
Nc Neurospora crassa
Rn Rattus norvegicus
Sc Saccharomyces cerevisiae
Sp Schizosaccharomyces pombe
Tt Tetrahymena thermophila
Xl Xenopus laevis
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Modification key
ac acetylation mal malonylation
ar1 mono-ADP-ribosylation me1 monomethylation
bio biotinylation me2 dimethylation
but butyrlyation me3 trimethylation
cit citrullination og O-GlcNAcylation
cr crotonylation oh* hydroxylation
for formylation ox* oxidation
gt* glutathionylation ph phosphorylation
hib 2-hydroxyisobutyrylation su SUMOylation
iso isomerization ub ubiquitination
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* XYZ modifications are known to occur on histone proteins but have not been included in these tables at individual amino acid residues.

Table heading key
Site A known histone PTM is indicated, based on the Brno nomenclature (Turner 2005), by the numbered amino acid residue at which it occurs followed by the abbrevation for its chemical modification (see Modification key).
Model Refers to the model organism in which a PTM was characterized.
Enzyme Where known, the histone-modifying enzyme (writer) that transduces a PTM is indicated. Italics specify the valency of modification that an enzyme can catalyze.
Function The associated biological function of a histone PTM is indicated where known.
Reference The key primary references where a PTM and/or its function are described are listed.
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Table 1.

Histone H2A

Site Model Enzyme Function Reference(s)
K5ac Hs, Sc Tip60, p300/CBP, Hat1 Transcriptional activation Yamamoto and Horikoshi 1997; Kimura and Horikoshi 1998; Verreault et al. 1998
K9bio HCS
Biotinidase		 Acetylation and methylation dependent
Involved in cell proliferation, gene silencing, and cellular response to DNA damage		 Stanley et al. 2001; Kothapalli et al. 2005a; Chew et al. 2006
K7ac Sc Hat1, Esa1 Transcriptional activation Suka et al. 2001
K13bio HCS
Biotinidase		 Acetylation and methylation dependent
Involved in cell proliferation, gene silencing, and cellular response to DNA damage		 Stanley et al. 2001; Kothapalli et al. 2005a; Chew et al. 2006
K13ub Mm Rnf168 Part of the DNA damage response to double-stranded DNA breaks Mattiroli et al. 2012; Gatti et al. 2012
K15ub Mm Rnf168 Part of the DNA damage response to double-stranded DNA breaks Mattiroli et al. 2012; Gatti et al. 2012
K63ub Mm Rnf8 Part of the DNA damage response to double-stranded DNA breaks Huen et al. 2007; Mailand et al. 2007
Q105me Sc, Hs Nop1, fibrillarin: me1 Ribosomal gene expression Tessarz et al. 2014
K119ub Dm, Hs dRing, RING1B Polycomb silencing
UV damage response		 Wang et al. 2004; Kapetanaki et al. 2006
S121ph
(S122ph) 		Sc
Sp		 Mec1
PIKK
Bub1		 DNA damage response
Telomere silencing
Chromosomal stability		 Wyatt et al. 2003; Harvey et al. 2005
Kawashima et al. 2010
T125ph Sc Mec1
PIKK		 DNA damage response
Telomere silencing		 Wyatt et al. 2003
K126bio Hs HCS
Biotinidase		 Acetylation and methylation dependent
Involved in cell proliferation, gene silencing, and cellular response to DNA damage.		 Stanley et al. 2001; Kothapalli et al. 2005a; Chew et al. 2006
K126su Sc Transcriptional repression
Blocks histone acetylation and histone ubiquitination		 Nathan et al. 2006
K127bio Hs HCS
Biotinidase		 Acetylation and methylation dependent
Involved in cell proliferation, gene silencing, and cellular response to DNA damage		 Stanley et al. 2001; Kothapalli et al. 2005a; Chew et al. 2006
S128ph
(S129ph) 		Sc Mec1
PIKK		 DNA damage response
Telomere silencing		 Downs et al. 2000; Redon et al. 2003;
Wyatt et al. 2003; Downs et al. 2004
K130bio Hs HCS
Biotinidase		 Acetylation and methylation dependent
Involved in cell proliferation, gene silencing, and cellular response to DNA damage		 Stanley et al. 2001; Kothapalli et al. 2005a; Chew et al. 2006
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Additional H2A modifications: K4ac, K21ac, K74me (Pantazis and Bonner 1981; Song et al. 2003; Aihara et al. 2004).

HCS, holocarboxylase synthetase; PIKK, phosphatidylinositol 3-kinase-related kinase.

Table 2.

Histone H2AX

Site Model Enzyme Function Reference(s)
K13ub Mm Rnf168 Part of the DNA damage response to double-stranded DNA breaks Mattiroli et al. 2012; Gatti et al. 2012; Panier and Durocher 2013
K15ub Mm Rnf168 Part of the DNA damage response to double-stranded DNA breaks Mattiroli et al. 2012; Gatti et al. 2012; Panier and Durocher 2013
K63ub Mm Rnf8 Part of the DNA damage response to double-stranded DNA breaks Huen et al. 2007; Mailand et al. 2007; Panier and Durocher 2013
S139ph Hs, Sc,
Dm, Xl		 ATM
DNA-PK
ATR		 DNA repair
M-phase related
Also known as γH2AX		 Rogakou et al. 1998; Rogakou et al. 1999; Burma et al. 2001; Stiff et al. 2004; Ichijima et al. 2005; Mukherjee et al. 2006; Ward and Chen 2001
Y142ph Hs, Mm WSTF DNA damage Xiao et al. 2009
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ATM, ataxia telangiectasia mutated; PK, protein kinase; ATR, ataxia telangiectasia and Rad3-related; WSTF, Williams–Beuren syndrome transcription factor.

Table 3.

Histone H2B

Site Model Enzyme Function Reference(s)
K5ac Hs Transcriptional activation Puerta et al. 1995; Galasinski et al. 2002
S10ph Sc Ste20 Apoptosis Ahn et al. 2005
S14ph Hs, Mm Mst1/krs2 kinase Apoptosis
Somatic hypermutation and class switch recombination		 Ajiro 2000; Cheung et al. 2003; Odegard et al. 2005
K16su Sc Gene repression Nathan et al. 2006
K17su Sc Gene repression Nathan et al. 2006
S33ph Dm CTK
TAF1		 Transcriptional activation Maile et al. 2004
K34ub Sc MSL2 Transcriptional activation Wu et al. 2011
K120ub Hs RNF20/40 Cell-cycle progression in concert with SAGA for transcriptional activation through H3 methylation, DNA damage response, meiosis Robzyk et al. 2000; Sun and Allis 2002; Kao et al. 2004; Zhu et al. 2005
K123ub Sc Rad6(E2)
Bre1(E3); ub1 		Telomeric silencing by lowering histone methylation at H3K4 and H3K79 Emre et al. 2005
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Table 4.

Histone H3

Site Model Enzyme Function Reference(s)
R2me Hs
Mm		 CARM1; me1, me2a
PRMT5; me1, me2s
PRMT6; me1, me2a
PRMT7; me1, me2s 		Gene expression Chen et al. 1999; Schurter et al. 2001; Greer and Shi 2012
T3ph Hs
At		 Haspin Centromere mitotic spindle function Polioudaki et al. 2004; Dai et al. 2005
K4ac Sc GCN5, RTT109, Sir2, Hst1 Transcription activation at some promoters Guillemette et al. 2011
K4me Sc
Ce
Ds
Hs		 Set1; me3
Set-2; me1–3
Set1; me2/3
SETD1A; me1–3
SETD1B		 rDNA/telomeric silencing (Sc)
Germ cell maintenance

Transcriptional activation (All)		 Briggs et al. 2001; Roguev et al. 2001; Nagy et al. 2002; Bryk et al. 2002; Bernstein et al. 2002; Santos-Rosa et al. 2002; Lee and Skalnik 2005; Lee et al. 2007; Xiao et al. 2011
Tt Transcriptional activation Strahl et al. 1999
Ds
Hs		 Trx
MLL; me1–3
MLL2		 Trithorax activation
Gene activation		 Milne et al. 2002; Nakamura et al. 2002; Greer and Shi 2012
Ds
Hs		 Trr
MLL3; me1–3
MLL4		 Enhancer function Herz et al. 2013
Ce
Ds
Hs		 Ash-2; me1–3
Ash1; me3
ASH1L; me1/3 		Germ cell specification
Trithorax activation
Gene activation		 Beisel et al. 2002; Xiao et al. 2011
Hs SETD7; me1 Transcriptional activation Wang et al. 2001a; Nishioka et al. 2002a; Wilson et al. 2002; Zegerman et al. 2002
Hs SMYD3; me2/3 Transcriptional activation Hamamoto et al. 2004
Mm Meisetz; me3 Meiotic prophase progression Hayashi et al. 2005
T6ph Hs PKCβ Inhibits AR-dependent transcription Metzger et al. 2010
R8me Hs PRMT5; me1, me2s Transcriptional repression Pal et al. 2004
K9ac Sc SAGA
GCN5		 Transcriptional activation Grant et al. 1999
Hs SRC1 Nuclear receptor coactivator Spencer et al. 1997; Schubeler et al. 2000; Vaquero et al. 2004
Dm Transcriptional activation Nowak and Corces 2000
K9me Sp Clr4; me1, me2 Centromeric and mating-type silencing Bannister et al. 2001; Nakayama et al. 2001
Nc Dim5; me3 DNA methylation Tamaru and Selker 2001
Ce Met-2; me3
Mes-2; me3 		Germ cells Bessler et al. 2010
Dm Su(var)3–9; me2/3 Dominant PEV modifier Czermin et al. 2001; Schotta et al. 2002; Ebert et al. 2004
At KRYPTONITE; me2 DNA methylation Jackson et al. 2002; Jackson et al. 2004
Mm Suv39h1; me2/3
Suv39h2; me2/3 		Pericentric heterochromatin O’Carroll et al. 2000; Rea et al. 2000; Lachner et al. 2001; Peters et al. 2001
Hs SUV39H1; me3 Rb-mediated silencing Nielsen et al. 2001; Vandel et al. 2001
Hs, Mm ESET; me2/me3
(SETDB1)		 Transcriptional repression Schultz et al. 2002; Yang et al. 2002; Dodge et al. 2004; Wang et al. 2004
Mm, Hs G9a; me1/me2 Transcriptional repression
Imprinting		 Tachibana et al. 2001, 2002; Ogawa et al. 2002; Xin et al. 2003
Hs EHMT1/GLP; me1/me2 Transcriptional repression Ogawa et al. 2002; Tachibana et al. 2005
Hs PRDM2/RIZ1; me2 Tumor suppression and response to female sex hormones Kim et al. 2003; Carling et al. 2004
S10ph Sc Snf1 Transcriptional activation Lo et al. 2001
Dm Jil-1 Transcriptional up-regulation of male X-chromosome Jin et al. 1999; Wang et al. 2001c
Hs Rsk2
Msk1
Msk2		 Transcriptional activation of immediate early genes (in concert with H3-K14 acetylation) Sassone-Corsi et al. 1999; Thomson et al. 1999; Cheung et al. 2000; Clayton et al. 2000
Hs IKKα Transcriptional up-regulation Anest et al. 2003; Yamamoto et al. 2003
Sc, Ce Ip11/AuroraB Mitotic chromosome condensation Hendzel et al. 1997; Wei et al. 1999; Hsu et al. 2000
An NIMA Mitotic chromosome condensation De Souza et al. 2000
Hs, Ce Fyn kinase UVB-induced MAP kinase pathway He et al. 2005
T11ph Hs Dlk/ZIP Mitosis-specific phosphorylation Preuss et al. 2003
K14ac Sc, Tt, Mm Gcn5 Transcriptional activation Brownell et al. 1996; Kuo et al. 1996
Hs, Dm TAFII230
TAFII250		 Transcriptional activation Mizzen et al. 1996
Hs p300 Transcriptional activation Schiltz et al. 1999
Hs PCAF Transcriptional activation Schiltz et al. 1999
Mm SRC1 Nuclear receptor coactivator Spencer et al. 1997
R17me Hs, Mm CARM1; me1, me2a Transcriptional activation (in concert with H3-K18/23 acetylation) Chen et al. 1999; Schurter et al. 2001; Bauer et al. 2002; Daujat et al. 2002
K18ac Sc SAGA
Ada
GCN5		 Transcriptional activation Grant et al. 1999
Hs p300 Transcriptional activation Schiltz et al. 1999
Hs CBP Transcriptional activation (in concert with H3-R17 methylation) Daujat et al. 2002
K23ac Sc SAGA Transcriptional activation Grant et al. 1999
Hs CBP Transcriptional activation (in concert with H3-R17 methylation) Daujat et al. 2002
R26me Hs CARM1; me1, me2a In vitro methylation site Chen et al. 1999; Schurter et al. 2001
K27ac Sc, Dm CBP, P300, GCN5 Enhancer function, gene expression Tie et al. 2009; Suka et al. 2001; Creyghton et al. 2010
K27me Hs, Dm E(z)/EZH2; me3 Polycomb repression
Early B-cell development
X-chromosome inactivation		 Cao et al. 2002; Czermin et al. 2002; Kuzmichev et al. 2002; Muller et al. 2002; Su et al. 2003
S28ph Hs Aurora-B Mitotic chromosome condensation Goto et al. 1999; Goto et al. 2002
Hs MSK1 UVB-induced phosphorylation Zhong et al. 2001
K36me Sc Set2; me2 Gene repression Strahl et al. 2002; Kizer et al. 2005; Sun et al. 2005
Nc Set2; me2 Transcription activation Adhvaryu et al. 2005
Sp Set2; me2 Transcription elongation Morris et al. 2005
Ce MES-4; me2
MET-1; me3 		Dosage compensation in germline
Meiosis		 Bender et al. 2006; Andersen and Horvitz 2007
Dm MES4; me3
SET2; me3 		Transcription elongation Bell et al. 2007
Hs, Mm SETD2; me1–3
NSD1–3; me1, me2 		Transcription activation Edmunds et al. 2008
Wang et al. 2007
K36ac Sc, Mm, Hs GCN5 Promoter mark on active genes Morris et al. 2007
P38iso Sc Fpr4 Gene expression Nelson et al. 2006
Y41ph Hs JAK2 Gene expression Dawson et al. 2009
R43me Hs CARM1, PRMT6; me2a Transcriptional activation Casadio et al. 2013
T45ph Sc, Hs Cdc7, PKC DNA replication; apoptosis Baker et al. 2010; Hurd et al. 2009
K56ac Sc SPT10 Transcriptional activation; DNA damage Xu et al. 2005; Ozdemir et al. 2005; Masumoto et al. 2005
K56me Hs G9a; me1 DNA replication Yu et al. 2012
Hs Suv39h; me3 Heterochromatin Jack et al. 2013
K64ac Hs/Mm p300 Nucleosome dynamics and transcription Di Cerbo et al. 2014
K64me Mm me3 Pericentric heterochromatin Daujat et al. 2009
K79me Sc, Hs Dot1/DOT1L; me1–3 Telomeric silencing, pachytene checkpoint
DNA damage response		 Feng et al. 2002; Lacoste et al. 2002; Ng et al. 2002; van Leeuwen et al. 2002; Greer and Shi 2012
T80ph Hs Mitosis Hammond et al. 2014
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Table 5.

Histone H3.3

Site Model Enzyme Function Reference(s)
K4me Dm me1, me2, me3 Transcriptional activation McKittrick et al. 2004
K9me Dm me1, me2 Transcriptional repression McKittrick et al. 2004
K9ac Dm, Hs Transcriptional activation McKittrick et al. 2004; Hake et al. 2006
K14me Dm me1, me2 McKittrick et al. 2004
K14ac Dm, Hs Transcriptional activation McKittrick et al. 2004; Hake et al. 2006
K18ac Hs Transcriptional activation Hake et al. 2006
K23ac Hs Transcriptional activation Hake et al. 2006
K27me Dm me1, me2, me3 Transcriptional repression McKittrick et al. 2004
S31ph Mammals Mitosis-specific phosphorylation Hake et al. 2005
K36me Dm, Hs me1, me2, me3 Transcriptional activation McKittrick et al. 2004; Hake et al. 2006
K37me Dm me1, me2 McKittrick et al. 2004
K79me Dm, Hs me1, me2 Transcriptional activation McKittrick et al. 2004; Hake et al. 2006
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Table 6.

CEN-H3/CENP-A

Site Model Enzyme Function Reference
G1me3 Hs RCC1 Mitosis Bailey et al. 2013
S7ph Hs Mitosis Zeitlin et al. 2001
S16ph Hs Chromosome segregation during mitosis Bailey et al. 2013
S18ph Hs Chromosome segregation during mitosis Bailey et al. 2013
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Table 7.

Histone H4

Site Model Enzyme Function Reference(s)
S1ph Hs, Sc Casein kinase II DNA damage response Ruiz-Carrillo et al. 1975; Cheung et al. 2005; van Attikum and Gasser 2005
R3me Hs, Sc PRMT1; me1, me2a
PRMT5; me1, me2s
PRMT6; me1, me2a
PRMT7; me1, me2s 		Transcriptional activation Wang et al. 2001b; Strahl et al. 2001; Greer and Shi 2012
K5ac Tt, Dm, Hs Hat1 Histone deposition Sobel et al. 1995; Parthun et al. 1996; Taplick et al. 1998; Kruhlak et al. 2001
Sc Esa1/NuA4 Cell-cycle progression Smith et al. 1998; Allard et al. 1999; Clarke et al. 1999; Miranda et al. 2006; Bird et al. 2002
Hs, Mm ATF2 Sequence-specific transcription factor Kawasaki et al. 2000a
Hs p300 Transcriptional activation Schiltz et al. 1999; Turner and Fellows 1989
K5me Hs Smyd3; me1 Contributes to cancer phenotype Van Aller et al. 2012
K8ac Hs, Mm Y-ATF2 Excluded from Xi
Sequence-specific transcription factor		 Jeppesen and Turner 1993; Choy et al. 2001; Kruhlak et al. 2001; Kawasaki et al. 2000b
Hs PCAF/ p300 Transcriptional activation Schiltz et al. 1999; Turner and Fellows 1989
K8me Sc SET5; me1 Stress response Green et al. 2012
K12ac Sc, Hs Hat1 Excluded from Xi
Histone deposition		 Jeppesen and Turner 1993; Kleff et al. 1995; Sobel et al. 1995; Parthun et al. 1996; Chang et al. 1997; Kruhlak et al. 2001; Turner and Fellows 1989
Sc NuA4 Mitotic and meiotic progression Choy et al. 2001
K12me Sc SET5; me1 Stress response Green et al. 2012
K12bio Hs HCS
Biotinidase		 Decrease in response to DNA double-strand breaks
Effects on cell proliferation		 Stanley et al. 2001; Kothapalli et al. 2005a,b
K16ac Mm Excluded from Xi
Cell-cycle-dependent acetylation		 Jeppesen and Turner 1993; Taplick et al. 1998
Dm MOF Transcriptional up-regulation of male X chromosome Akhtar and Becker 2000; Hsu et al. 2000
Hs, Mm ATF2 Sequence-specific transcription factor Kawasaki et al. 2000a; Turner 2000; Kruhlak et al. 2001; Turner and Fellows 1989; Vaquero et al. 2004
K20me Mm, Dm Suv4–20h1; me2, me3
Suv4–20h2; me2, me3 		Gene silencing Schotta et al. 2004
Hs, Dm SETD8/Pr-SET7;
me1 		Transcriptional silencing
Mitotic condensation		 Fang et al. 2002; Nishioka et al. 2002b; Rice et al. 2002
Dm Ash1; me2 Trithorax activation in concert with H3K4 and H3K9 methylation Beisel et al. 2002
K59me Sc Silent chromatin formation Zhang et al. 2003
K59su Hs SUMO-1
SUMO-3		 Transcriptional repression Shiio and Eisenman 2003
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Table 8.

Histone H1

Site Model Enzyme Function Reference(s)
E2arn Rn PARP-1; ar1 Involved in neurotrophic activity Ogata et al. 1980b; Visochek et al. 2005
T10ph Hs Mitosis specific
Transcriptional activation H1b		 Chadee et al. 1995; Garcia et al. 2004; Sarg et al. 2006
E14arn Rn PARP-1; ar1 Involved in neurotrophic activity Ogata et al. 1980b; Visochek et al. 2005
S17ph Hs Interphase specific
Transcriptional activation H1b		 Chadee et al. 1995; Garcia et al. 2004; Sarg et al. 2006
K26me Hs EZH2; me2 Mediates HP1 binding Kuzmichev et al. 2004; Daujat et al. 2005
S27ph Hs EZH2; me2 Blocks HP1 binding Garcia et al. 2004; Daujat et al. 2005
R54cit Mm PADI4 Cellular reprogramming/nucleosome binding Christophorou et al. 2014
T137ph Hs Mitosis specific
Transcriptional activation H1b		 Chadee et al. 1995; Garcia et al. 2004; Sarg et al. 2006
T154ph Hs Mitosis specific
Transcriptional activation H1b		 Chadee et al. 1995; Garcia et al. 2004; Sarg et al. 2006
S172ph Hs Interphase specific
Transcriptional activation H1b		 Chadee et al. 1995; Garcia et al. 2004; Sarg et al. 2006
S188ph Hs Interphase specific
Transcriptional activation H1b		 Chadee et al. 1995; Garcia et al. 2004; Sarg et al. 2006
K213ar Rn PARP-1; ar1 Involved in neurotrophic activity Ogata et al. 1980b; Visochek et al. 2005
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Table 9.

Histone H2Aa,b

Site Model Method Reference(s)
S1ph Mm Au Pantazis and Bonner 1981
R3me3 Mm MS Tweedie-Cullen et al. 2012
K5hib Mm MS Dai et al. 2014
K9me1; me2; suc; hib Hs; Mm; Hs; Hs MS Tan et al. 2011; Tweedie-Cullen et al. 2012; Xie et al. 2012; Dai et al. 2014
R11me1, me2 Hs MS Waldmann et al. 2011
K13me1, ac; suc Bt; Sc MS Zhang et al. 2003; Xie et al. 2012
K15ac Bt MS Zhang et al. 2003
K21suc Sc MS Xie et al. 2012
R29me1, me2 Hs MS/Ab Waldmann et al. 2011
K36ac, suc; for; hib; cr Hs/Dm; Hs/Mm; Mm; Hs/Mm MS Xie et al. 2012; Wisniewski et al. 2008; Dai et al. 2014; Tan et al. 2011
Y39oh Hs MS Tan et al. 2011
R42me1 Hs; Hs MS/Ab Tan et al. 2011
R71me1 Mm MS Tweedie-Cullen et al. 2012
K74ac, me1; hib Mm; Mm MS Tweedie-Cullen et al. 2012; Dai et al. 2014
K75me1; hib Bt; Mm MS Zhang et al. 2003; Dai et al. 2014
R77me1 Bt MS Zhang et al. 2003
T79ac Mm MS Tweedie-Cullen et al. 2012
R88me1 Hs MS Tan et al. 2011
K95cr, but, pr, me1, me2; for; ub; suc; hib Mm; Hs/Mm; Mm; Hs; Hs/Mm MS Tweedie-Cullen et al. 2012; Wisniewski et al. 2008; Tweedie-Cullen et al. 2009; Xie et al. 2012; Dai et al. 2014
K99me1; me2 Mm; Mm MS Tweedie-Cullen et al. 2012; Tweedie-Cullen et al. 2009
T101og Hs MS/Ab Sakabe et al. 2010
K118for, me1, cr; for; ub, me2; hib Hs/Mm; Hs/Mm; Mm; Mm MS Tan et al. 2011; Wisniewski et al. 2008; Tweedie-Cullen et al. 2009; Dai et al. 2014
K119cr; mal Hs; Sc MS Tan et al. 2011; Xie et al. 2012
T120ph Dm Ab Aihara et al. 2004
K125me1, cr; me2, pr; ub Hs; Mm; Mm MS Tan et al. 2011; Tweedie-Cullen et al. 2012; Tweedie-Cullen et al. 2009
K127ac Mm MS Tweedie-Cullen et al. 2012
K129ac Mm MS Tweedie-Cullen et al. 2012
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aCarbonylation of H2A has been detected in Rn indirectly by Sharma et al. (2006).

b5-Hydroxylation of lysine residues has been reported for canonical histones (H2A, H2B, H3, and H4) by Unoki et al. (2013).

Table 10.

Histone H2AX

Site Model Method Reference
K118ub Mm MS Tweedie-Cullen et al. 2009
K119ub Mm MS Tweedie-Cullen et al. 2009
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Table 11.

Histone H2A.Z

Site Model Method Reference(s)
K4ac; me1 Hs; Hs/Mm MS; MS/Ab Tweedie-Cullen et al. 2009; Binda et al. 2013
K7ac; me1 Hs; Hs/Mm MS; MS/Ab Bonenfant et al. 2006; Binda et al. 2013
K11ac Hs MS Bonenfant et al. 2006
K13ac Mm MS Tweedie-Cullen et al. 2009
K120ub Mm MS Ku et al. 2012
K121ub Mm MS Ku et al. 2012
K125ub Mm MS Ku et al. 2012
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Table 12.

Histone macroH2A

Site Model Method Reference(s)
K17me1 Hs MS Chu et al. 2006
K115ub Hs MS Ogawa et al. 2005; Chu et al. 2006
K122me2 Hs MS Chu et al. 2006
T128ph Hs MS/Ab Chu et al. 2006; Bernstein et al. 2008
K238me1 Hs MS Chu et al. 2006
K238me2 Hs MS Chu et al. 2006
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Table 13.

Histone H2B

Site Model Method Reference(s)
E2arn Rn Au Ogata et al. 1980a
K5me1; cr; for; hib; suc Bt; Hs; Hs/Mm; Hs/Mm; Hs MS Zhang et al. 2003; Tan et al. 2011; Wisniewski et al. 2008; Dai et al. 2014; Weinert et al. 2013
S6ph Mm MS Tweedie-Cullen et al. 2009
K11ac; cr Sc; Hs/Mm MS Jiang et al. 2007; Tan et al. 2011
K12me1, cr; me3; hib Hs; Mm; Mm MS Tan et al. 2011; Tweedie-Cullen et al. 2012; Dai et al. 2014
K15ac; me1, cr  Hs MS Tan et al. 2011
K16ac; cr Sc; Hs MS Jiang et al. 2007; Tan et al. 2011
T19ac Mm MS Tweedie-Cullen et al. 2012
K20me1, cr; hib Hs; Mm MS Tan et al. 2011; Dai et al. 2014
K21but Sc MS Zhang et al. 2009
K23me1, cr; me2; hib Hs; Bt; Mm MS Tan et al. 2011; Zhang et al. 2003; Dai et al. 2014
K24hib Mm MS Dai et al. 2014
K34for; cr; suc; me1; hib Hs/Mm; Hs/Mm; Sc/Hs; Mm; Mm MS Wisniewski et al. 2008; Tan et al. 2011; Xie et al. 2012; Tweedie-Cullen et al. 2012; Dai et al. 2014
S36og Hs MS/Ab Sakabe et al. 2010
K37me1 Sc MS Zhang et al. 2009
E38me2 Sc MS Zhang et al. 2009
Y37oh Hs MS Tan et al. 2011
K43me1; for; hib; suc Bt; Hs/Mm; Mm; Hs MS Zhang et al. 2003; Wisniewski et al. 2008; Dai et al. 2014; Weinert et al. 2013
K46for; suc; hib Hs/Mm; Sc/Dm; Hs/Mm MS Wisniewski et al. 2008; Xie et al. 2012; Dai et al. 2014
K57me1; ac; hib Hs; Mm; Mm MS Tan et al. 2011; Tweedie-Cullen et al. 2012; Dai et al. 2014
E64me2 Sc MS Zhang et al. 2009
S76ph Mm MS Tweedie-Cullen et al. 2009
K79me1 Hs MS Tan et al. 2011
K85ac; me1; suc; hib Bt; Hs; Hs; Hs/Mm MS Zhang et al. 2003; Tan et al. 2011; Weinert et al. 2013; Dai et al. 2014
S88ph Mm MS Tweedie-Cullen et al. 2009
T89ph Mm MS Tweedie-Cullen et al. 2009
S92ph Mm MS Tweedie-Cullen et al. 2009
K99me1 Hs MS Tan et al. 2011
K108for; cr; ub, ac; hib; suc Hs/Mm; Mm; Mm; Hs/Mm; Mm MS Wisniewski et al. 2008; Tweedie-Cullen et al. 2012; Tweedie-Cullen et al. 2009; Dai et al. 2014; Park et al. 2013
S113ph Mm MS Tweedie-Cullen et al. 2009
K116for, me1; suc, mal; ac; hib; cr Hs; Hs/Dm; Mm; Hs/Mm; Mm MS Tan et al. 2011; Xie et al. 2012; Tweedie-Cullen et al. 2012; Dai et al. 2014; Montellier et al. 2013
K120for; suc; ac, ub; hib Hs; Hs/Dm/Mm; Mm; Hs/Mm MS Tan et al. 2011; Xie et al. 2012; Tweedie-Cullen et al. 2009; Dai et al. 2014
K125ac Mm MS Tweedie-Cullen et al. 2012
Open in a new tab

Also, 5-hydroxylation of lysine residues has been reported (Unoki et al. 2013).

Table 14.

Histone H3

Site Model Method Reference(s)
K4cr; hib; ac Hs/Mm; Mm; Hs MS Tan et al. 2011; Dai et al. 2014; Garcia et al. 2007
T6ac Tt MS Britton et al. 2013
K9cr; hib Hs/Mm; Mm MS Tan et al. 2011; Dai et al. 2014
S10ac; og Sc/Mm/Hs MS; Ab; Ab Britton et al. 2013; Zhang et al. 2011
K14suc; but; hib Hs; Sc; Mm MS Xie et al. 2012; Zhang et al. 2009; Dai et al. 2014
K18cr; for; me1; hib Hs/Mm; Hs/Mm; Mm; Mm MS Tan et al. 2011; Wisniewski et al. 2008; Garcia et al. 2005; Dai et al. 2014
T22ac Sc/Dm/Hs MS Britton et al. 2013
K23cr; for; pr; hib; suc Hs/Mm; Hs/Mm; Sc; Hs/Mm; Mm MS Tan et al. 2011; Wisniewski et al. 2008; Zhang et al. 2009; Dai et al. 2014; Park et al. 2013
K27cr; but; hib; suc Hs/Mm; Sc; Mm; Mm MS Tan et al. 2011; Zhang et al. 2009; Dai et al. 2014; Park et al. 2013
S28ac Mm MS Britton et al. 2013
T32og Hs MS Fong et al. 2012
K36hib Mm MS Dai et al. 2014
R52me1 Sc/Bt MS Hyland et al. 2005
R53me1 Sc/Bt MS Hyland et al. 2005
Y54ac Tet MS Britton et al. 2013
K56cr, for; suc, mal; pr; ub; hib Hs/Mm; Dm/Mm/Hs; Sc; Mm; Hs/Mm MS Tan et al. 2011; Xie et al. 2012; Zhang et al. 2009; Tweedie-Cullen et al. 2009; Dai et al. 2014
E59me2 Sc MS Zhang et al. 2009
R63me1 Hs/Mm MS Tan et al. 2011
K64for; hib; ac, me1 Hs/Mm; Mm; Sc, Hs MS Wisniewski et al. 2008; Dai et al. 2014; Garcia et al. 2007
K79suc; for; cr; ub; hib; ac Sc/Dm/Mm/Hs; Hs/Mm; Mm; Mm; Hs/Mm; Hs MS Xie et al. 2012; Wisniewski et al. 2008; Tweedie-Cullen et al. 2012; Tweedie-Cullen et al. 2009; Dai et al. 2014; Garcia et al. 2007
T80ac Mm MS Tweedie-Cullen et al. 2012
R83me1, me2 Mm MS Tweedie-Cullen et al. 2012
S86ph Mm MS Tweedie-Cullen et al. 2012
T107ph Mm MS Tweedie-Cullen et al. 2012
C110gt Hs/Mm Indirect chemical labeling Garcia-Gimenez et al. 2013
K115ac; but Sc/Bt; Mm MS Hyland et al. 2005; Tweedie-Cullen et al. 2012
T118ph Sc/Bt MS Hyland et al. 2005
R128me1 Hs/Mm MS Tan et al. 2011
K122suc; for; me2; hib; cr Hs; Hs/Mm; Mm; Hs/Mm; Mm MS Tan et al. 2011; Wisniewski et al. 2008; Tweedie-Cullen et al. 2009; Dai et al. 2014; Montellier et al. 2013
K134me1 Mm MS Tweedie-Cullen et al. 2012
Open in a new tab

Also, 5-hydroxylation of lysine residues has been reported (Unoki et al. 2013).

Table 15.

Histone H4

Site Model Method Reference(s)
R3me3 Mm MS Tweedie-Cullen et al. 2012
K5cr; me3; pr, but; hib Mm/Hs; Mm; Hs; Mm MS Tan et al. 2011; Tweedie-Cullen et al. 2012; Chen et al. 2007; Dai et al. 2014
K8cr; pr, but; hib Mm/Hs; Hs; Mm MS; MS; MS/Ab Tan et al. 2011; Chen et al. 2007; Dai et al. 2014
K12cr; for; suc; pr, but; hib Mm/Hs; Hs; Hs; Mm MS Tan et al. 2011; Wisniewski et al. 2008; Xie et al. 2012; Chen et al. 2007; Dai et al. 2014
K16cr, me1; pr; pr, but; hib Mm/Hs; Mm; Hs; Mm MS Tan et al. 2011; Tweedie-Cullen et al. 2012; Chen et al. 2007; Dai et al. 2014
R17me1, me2 Mm MS Tweedie-Cullen et al. 2012
R17me1, me2, me3 Mm MS Tweedie-Cullen et al. 2012
K20ac Sc MS Garcia et al. 2007
K31for; suc; hib; me1; pr Hs; Sc/Dm/Mm/Hs; Hs/Mm; Hs/Mm/Sc; Hs MS Tan et al. 2011; Xie et al. 2012; Dai et al. 2014; Garcia et al. 2007; Chen et al. 2007
R23me3 Mm MS Tweedie-Cullen et al. 2012
R35me1 Hs MS Tan et al. 2011
K44pr; hib Hs; Mm MS Chen et al. 2007; Dai et al. 2014
S47og; ph Hs; Sc/Bt MS/Ab; MS Sakabe et al. 2010; Hyland et al. 2005
Y51oh Hs MS Tan et al. 2011
R55me1 Hs MS Tan et al. 2011
K59me1, for; hib Hs; Mm/Hs; Mm MS Tan et al. 2011; Wisniewski et al. 2008; Dai et al. 2014
R67me1 Hs MS Tan et al. 2011
K77me1; suc; for; hib; ac; pr; cr Hs; Sc/Dm/Mm/Hs; Mm/Hs; Hs/Mm; Sc/Bt; Hs; Mm MS Tan et al. 2011; Xie et al. 2012; Wisniewski et al. 2008; Dai et al. 2014; Hyland et al. 2005; Chen et al. 2007; Montellier et al. 2013
K79for; suc, ac; hib; pr Hs; Dm/Mm; Mm; Hs/Mm; Hs MS Wisniewski et al. 2008; Xie et al. 2012; Tweedie-Cullen et al. 2012; Dai et al. 2014; Chen et al. 2007
Y88ox; ph Hs; Mm MS Tan et al. 2011; Tweedie-Cullen et al. 2009
K91ac; for; suc; cr; hib; pr Hs; Hs; Dm/Mm/Hs; Mm; Hs/Mm; Hs MS Tan et al. 2011; Wisniewski et al. 2008; Xie et al. 2012; Tweedie-Cullen et al. 2012; Dai et al. 2014; Chen et al. 2007
R92me1 Sc/Bt MS Hyland et al. 2005
Open in a new tab

Also, 5-hydroxylation of lysine residues has been reported (Unoki et al. 2013).

Table 16.

Histone H1

Site Model Method Reference(s)
S1ph Hs MS Garcia et al. 2004
E2arn Rn Au Ogata et al. 1980b
T3ph Hs MS Garcia et al. 2004
K12me1 Hs MS Lu et al. 2009
E14arn Rn Au Ogata et al. 1980b
K16ac; me1, me2; for Hs/Mm;
Hs/Mm		 MS Wisniewski et al. 2007
Wisniewski et al. 2008
T17ph Hs MS Garcia et al. 2004
K21ac; me1 Hs; Mm MS Wisniewski et al. 2007; Tweedie-Cullen et al. 2012
K22hib Mm MS Dai et al. 2014
K25hib Mm MS Dai et al. 2014
K26hib Mm MS Dai et al. 2014
S30ph Hs MS Garcia et al. 2004
K33ac; me2, for; cr; ub; hib Hs; Mm; Hs/Mm; Mm; Mm MS Wisniewski et al. 2007; Tweedie-Cullen et al. 2012; Tan et al. 2011; Tweedie-Cullen et al. 2009
S35ph; ac Hs; Mm MS Garcia et al. 2004; Tweedie-Cullen et al. 2012
K45ac,ub; hib; for; suc Hs; Hs; Hs/Mm; Mm MS Wisniewski et al. 2007; Dai et al. 2014; Wisniewski et al. 2008; Park et al. 2013
K48ac Hs MS Wisniewski et al. 2007
S50ac Mm MS Tweedie-Cullen et al. 2012
K51ac; me1; hib Hs; Mm; Hs/Mm MS Wisniewski et al. 2007; Tweedie-Cullen et al. 2012; Dai et al. 2014
K54me1 Hs MS Tan et al. 2011
K62ac; for; hib; suc Hs; Hs/Mm; Hs/Mm; Hs MS Garcia et al. 2004; Wisniewski et al. 2008; Dai et al. 2014; Weinert et al. 2013
K63ac; me1; for; cr; hib Hs; Hs; Hs/Mm; Hs/Mm; Hs MS Wisniewski et al. 2007; Lu et al. 2009; Wisniewski et al. 2008; Tan et al. 2011; Dai et al. 2014
K64ac Hs MS Tan et al. 2011
K66for Hs/Mm MS Wisniewski et al. 2008
S72ph Hs MS Garcia et al. 2004
Y73oh Hs MS Tan et al. 2011
K74for; hib Hs/Mm; Mm MS Wisniewski et al. 2008; Dai et al. 2014
K80hib Mm MS Dai et al. 2014
K81me1 Hs MS Lu et al. 2009
K83for Hs MS Tan et al. 2011
K84for; cr; hib Hs/Mm; Hs/Mm; Hs/Mm MS Wisniewski et al. 2008; Tan et al. 2011; Dai et al. 2014
K85ac Hs MS Wisniewski et al. 2007
S87pha Hs MS Garcia et al. 2004
K87fora Hs MS Wisniewski et al. 2007
K89ac, for; cr; suc; hib Hs; Hs; Mm; Hs MS Wisniewski et al. 2007; Tan et al. 2011; Park et al. 2013; Dai et al. 2014
K92me1 Hs MS Tan et al. 2011
K96ac; me1; me2; for; cr; hib; suc Hs; Hs; Mm; Hs/Mm; Hs; Hs/Mm; Mm MS Wisniewski et al. 2007; Lu et al. 2009; Tweedie-Cullen et al. 2012; Wisniewski et al. 2008; Tan et al. 2011; Dai et al. 2014; Park et al. 2013
K101me1 Hs MS Lu et al. 2009
K105me1; suc Hs; Mm MS Lu et al. 2009; Park et al. 2013
K107me1 Hs MS Lu et al. 2009
K109me2; for; hib Mm; Hs/Mm; Mm MS Tweedie-Cullen et al. 2012; Wisniewski et al. 2008; Dai et al. 2014
S112ac Mm MS Tweedie-Cullen et al. 2012
K118me1 Hs MS Lu et al. 2009
K120hib; suc Mm; Mm MS Dai et al. 2014; Park et al. 2013
K128hib Mm MS Dai et al. 2014
K131me1 Hs MS Tan et al. 2011
K135hib Mm MS Dai et al. 2014
K140for Hs/Mm MS Wisniewski et al. 2008
T145ph Hs MS Garcia et al. 2004
T146ph Hs MS Garcia et al. 2004
K147me1; hib Hs; Mm MS Lu et al. 2009; Dai et al. 2014
K150me1 Hs MS Tan et al. 2011
K158cr; hib Hs/Mm; Mm MS Tan et al. 2011; Dai et al. 2014
K159for Hs/Mm MS Wisniewski et al. 2008
T164ph Hs MS Wisniewski et al. 2007
K167cr; hib Hs; Mm MS Tan et al. 2011; Dai et al. 2014
T179ph Hs MS Garcia et al. 2004
K187me1 Hs MS/Ab Weiss et al. 2010
K201me1 Hs MS Tan et al. 2011
K212hib Mm MS Dai et al. 2014
K226me1 Hs MS Tan et al. 2011
Open in a new tab

Pham (2000) found an enzyme that ubiquitinates histone H1

aH1S87 and H1K87 represent different histone H1 variants.

1. MORE-STUDIED HISTONE PTMS

The tables in this section list histone modifications with known functions and modifying enzymes, and primary references are indicated wherever possible (up until 2014). Distinct modification states are indicated in italics in the Enzyme column.

Additional modifications with currently unknown function are listed in Section 2. These modifications were obtained from a combination of sources.

The tables that constitute Section 1 have been extended from Appendix 2 in Allis et al. (2007) by Ben Garcia and Yingming Zhao, with additional input from Le Hehuang, Monika Lachner, and Marie-Laure Caparros. That appendix was based on an original setup from Lachner et al. (2003) and significantly extended by Roopsha Sengupta, Mario Richter, and Marie-Laure Caparros and verified by Patrick Trojer.

The histone modifications follow the nomenclature as proposed by Turner (2005).

2. LESS-STUDIED HISTONE PTMS

Methods key
The method by which novel histone modifications have been identified is indicated by the following abbreviations:
Ab antibody
Au autoradiography
MS mass spectrometry
Open in a new tab

These tables reflect modification sites that have been detected, but where no function has been assigned.

Footnotes

Editors: C. David Allis, Marie-Laure Caparros, Thomas Jenuwein, Danny Reinberg, and Monika Lachner

Additional Perspectives on Epigenetics available at www.cshperspectives.org

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