Roles and Regulation of H3K4 Methylation During Mammalian Early Embryogenesis and Embryonic Stem Cell Differentiation

Terzi Cizmecioglu, Nihal

doi:10.1007/5584_2023_794

Nihal Terzi Cizmecioglu⁷

Part of the book series: Advances in Experimental Medicine and Biology

1 Altmetric

Abstract

From generation of germ cells, fertilization, and throughout early mammalian embryonic development, the chromatin undergoes significant alterations to enable precise regulation of gene expression and genome use. Methylation of histone 3 lysine 4 (H3K4) correlates with active regions of the genome, and it has emerged as a dynamic mark throughout this timeline. The pattern and the level of H3K4 methylation are regulated by methyltransferases and demethylases. These enzymes, as well as their protein partners, play important roles in early embryonic development and show phenotypes in embryonic stem cell self-renewal and differentiation. The various roles of H3K4 methylation are interpreted by dedicated chromatin reader proteins, linking this modification to broader molecular and cellular phenotypes. In this review, we discuss the regulation of different levels of H3K4 methylation, their distinct accumulation pattern, and downstream molecular roles with an early embryogenesis perspective.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution

Institutional subscriptions

Abbreviations

Ash2L:: Absent Small Or Homeotic-Like
BPTF:: Bromodomain And PHD Domain Transcription Factor
BRPF1/2:: Bromodomain And PHD Finger-Containing Protein 1/2
C/EBPα:: CCAAT/Enhancer Binding Protein (C/EBP), Alpha
CAS9:: CRISPR associated protein 9
CBP:: CREB Binding Protein
CD4:: Cluster of Differentiation 4
ChIP:: Chromatin Immunoprecipitation
c-Myc:: Avian Myelocytomatosis Viral Oncogene Homolog
COMPASS:: Complex Proteins Associated with Set1
CXXC1:: PHD Finger And CXXC Domain-Containing Protein 1
DNMT3A/B/L:: DNA (Cytosine-5-)-Methyltransferase 3 A/B/L
DPY30:: Dumpy-30 Homolog
ESC:: Embryonic stem cell
FAD:: Flavin adenine dinucleotide
H2Az:: Histone variant 2Az
H3:: Histone 3
H3K27ac:: Acetylated Histone 3 Lysine 27
H3K27me3:: Trimethylated Histone 3 Lysine 27
H3K36:: Histone 3 Lysine 36
H3K36me3:: Trimethylated Histone 3 Lysine 36
H3K4:: Histone 3 Lysine 4
H3K4me1:: Monomethylated Histone 3 Lysine 4
H3K4me2:: Dimethylated Histone 3 Lysine 4
H3K4me3:: Trimethylated Histone 3 Lysine 4
H3K9:: Histone 3 Lysine 9
H3K9me3:: Trimethylated Histone 3 Lysine 9
HBO1:: Histone Acetyltransferase Binding To ORC1
Hox:: Homeotic/Homeobox
ICR:: Imprint control region
ING1/2-4/5:: Inhibitor Of Growth Family Member 1/2-4/5
INTS11:: Integrator Complex Subunit 11
IVF:: In vitro fertilization
JARID1A-D:: Jumonji/ARID Domain-Containing Protein 1A-D
KDM1A/B/5A-D:: Lysine Demethylase 1A/B/5A-D
KMT2A-D/F/G:: Lysine Methyltransferase 2A-D/F/G
LSD1/2:: Lysine-specific Histone Demethylase 1/2
MLL1-4:: Mixed-lineage Leukemia 1-4
Mox1:: Mesenchyme Homeobox 1
MOZ/MORF:: Monocytic Leukemic Zinc-finger
NDR:: Nucleosomally depleted region
NO66:: Nucleolar Protein 66
NURF:: Nucleosome Remodeling Factor Complex
Oct4:: Octamer-Binding Protein 4/ POU Class 5 Homeobox 1
PHD:: Plant Homeodomain
PHF19:: PHD Finger Protein 19
P-TEFb:: Cyclin Dependent Kinase 9
RbBP5:: Retinoblastoma binding protein 5
rDNA:: Ribosomal DNA
SET:: Su(var)3-9, Enhancer-of-zeste and Trithorax domain
Set1:: Su(var)3-9, Enhancer-of-zeste and Trithorax domain-containing protein 1
SETD1A/B:: SET domain-containing 1A/B
SIN3:: SIN3 Transcription Regulator Homolog
TAF3:: TATA-Box Binding Protein Associated Factor 3
TF:: Transcription factor
TFIID:: Basal transcription factor IID for RNA polymerase II
TIP60:: Tat Interacting Protein, 60kDa/Lysine Acetyltransferase 5
Trr:: Trithorax-related
Trx:: Trithorax
WDR5:: WD Repeat Domain 5

References

Adamo A, Sesé B, Boue S, Castaño J, Paramonov I, Barrero MJ, Belmonte JCI (2011) LSD1 regulates the balance between self-renewal and differentiation in human embryonic stem cells. Nat Cell Biol 13(6):652–659. https://doi.org/10.1038/ncb2246
Article Google Scholar
Albert M, Schmitz SU, Kooistra SM, Malatesta M, Morales Torres C, Rekling JC, Johansen JV, Abarrategui I, Helin K (2013) The histone demethylase Jarid1b ensures faithful mouse development by protecting developmental genes from aberrant H3K4me3. PLoS Genet 9(4):e1003461. https://doi.org/10.1371/journal.pgen.1003461
Article Google Scholar
Andreu-Vieyra CV, Chen R, Agno JE, Glaser S, Anastassiadis K, Stewart AF, Matzuk MM (2010) MLL2 is required in oocytes for bulk histone 3 lysine 4 trimethylation and transcriptional silencing. PLoS Biol 8(8):e1000453. https://doi.org/10.1371/journal.pbio.1000453
Article Google Scholar
Ang Y-S, Tsai S-Y, Lee D-F, Monk J, Su J, Ratnakumar K, Ding J, Ge Y, Darr H, Chang B, Wang J, Rendl M, Bernstein E, Schaniel C, Lemischka IR (2011) Wdr5 mediates self-renewal and reprogramming via the embryonic stem cell core transcriptional network. Cell 145(2):183–197. https://doi.org/10.1016/j.cell.2011.03.003
Article Google Scholar
Arnaudo AM, Garcia BA (2013) Proteomic characterization of novel histone post-translational modifications. Epigenetics Chromatin 6(1):24. https://doi.org/10.1186/1756-8935-6-24
Article Google Scholar
Ashokkumar D, Zhang Q, Much C, Bledau AS, Naumann R, Alexopoulou D, Dahl A, Goveas N, Fu J, Anastassiadis K, Stewart AF, Kranz A (2020) MLL4 is required after implantation whereas MLL3 becomes essential during late gestation. Development. https://doi.org/10.1242/dev.186999
Bai D, Sun J, Chen C, Jia Y, Li Y, Liu K, Zhang Y, Yin J, Liu Y, Han X, Ruan J, Kou X, Zhao Y, Wang H, Wang Z, Chen M, Teng X, Jiang C, Gao S, Liu W (2022) Aberrant H3K4me3 modification of epiblast genes of extraembryonic tissue causes placental defects and implantation failure in mouse IVF embryos. Cell Rep 39(5):110784. https://doi.org/10.1016/j.celrep.2022.110784
Article Google Scholar
Balbasi E, Guven G, Terzi Cizmecioglu N (2021a) Mouse embryonic stem cell culture in serum-containing or 2i conditions, pp 275–294. https://doi.org/10.1007/7651_2021_438
Balbasi E, Sezginmert D, Alganatay C, Terzi Cizmecioglu N (2021b) Directed differentiation of mouse embryonic stem cells to mesoderm, endoderm, and neuroectoderm lineages, pp 295–307. https://doi.org/10.1007/7651_2021_439
Barski A, Cuddapah S, Cui K, Roh T-Y, Schones DE, Wang Z, Wei G, Chepelev I, Zhao K (2007) High-resolution profiling of histone methylations in the human genome. Cell 129(4):823–837. https://doi.org/10.1016/j.cell.2007.05.009
Article Google Scholar
Belhocine M, Simonin M, Abad Flores JD, Cieslak A, Manosalva I, Pradel L, Smith C, Mathieu E-L, Charbonnier G, Martens JHA, Stunnenberg HG, Maqbool MA, Mikulasova A, Russell LJ, Rico D, Puthier D, Ferrier P, Asnafi V, Spicuglia S (2022) Dynamics of broad H3K4me3 domains uncover an epigenetic switch between cell identity and cancer-related genes. Genome Res 32(7):1328–1342. https://doi.org/10.1101/gr.266924.120
Article Google Scholar
Benayoun BA, Pollina EA, Ucar D, Mahmoudi S, Karra K, Wong ED, Devarajan K, Daugherty AC, Kundaje AB, Mancini E, Hitz BC, Gupta R, Rando TA, Baker JC, Snyder MP, Cherry JM, Brunet A (2014) H3K4me3 breadth is linked to cell identity and transcriptional consistency. Cell 158(3):673–688. https://doi.org/10.1016/j.cell.2014.06.027
Article Google Scholar
Bernstein BE, Mikkelsen TS, Xie X, Kamal M, Huebert DJ, Cuff J, Fry B, Meissner A, Wernig M, Plath K, Jaenisch R, Wagschal A, Feil R, Schreiber SL, Lander ES (2006) A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 125(2):315–326. https://doi.org/10.1016/j.cell.2006.02.041
Article Google Scholar
Bertero A, Madrigal P, Galli A, Hubner NC, Moreno I, Burks D, Brown S, Pedersen RA, Gaffney D, Mendjan S, Pauklin S, Vallier L (2015) Activin/nodal signaling and NANOG orchestrate human embryonic stem cell fate decisions by controlling the H3K4me3 chromatin mark. Genes Dev 29(7):702–717. https://doi.org/10.1101/gad.255984.114
Article Google Scholar
Beshiri ML, Holmes KB, Richter WF, Hess S, Islam ABMMK, Yan Q, Plante L, Litovchick L, Gévry N, Lopez-Bigas N, Kaelin WG, Benevolenskaya EV (2012) Coordinated repression of cell cycle genes by KDM5A and E2F4 during differentiation. Proc Natl Acad Sci 109(45):18499–18504. https://doi.org/10.1073/pnas.1216724109
Article Google Scholar
Bledau AS, Schmidt K, Neumann K, Hill U, Ciotta G, Gupta A, Torres DC, Fu J, Kranz A, Stewart AF, Anastassiadis K (2014) The H3K4 methyltransferase Setd1a is first required at the epiblast stage, whereas Setd1b becomes essential after gastrulation. Development 141(5):1022–1035. https://doi.org/10.1242/dev.098152
Article Google Scholar
Boileau RM, Chen KX, Blelloch R (2023) Loss of MLL3/4 decouples enhancer H3K4 monomethylation, H3K27 acetylation, and gene activation during embryonic stem cell differentiation. Genome Biol 24(1):41. https://doi.org/10.1186/s13059-023-02883-3
Article Google Scholar
Brien GL, Gambero G, O’Connell DJ, Jerman E, Turner SA, Egan CM, Dunne EJ, Jurgens MC, Wynne K, Piao L, Lohan AJ, Ferguson N, Shi X, Sinha KM, Loftus BJ, Cagney G, Bracken AP (2012) Polycomb PHF19 binds H3K36me3 and recruits PRC2 and demethylase NO66 to embryonic stem cell genes during differentiation. Nat Struct Mol Biol 19(12):1273–1281. https://doi.org/10.1038/nsmb.2449
Article Google Scholar
Briggs SD, Bryk M, Strahl BD, Cheung WL, Davie JK, Dent SY, Winston F, Allis CD (2001) Histone H3 lysine 4 methylation is mediated by Set1 and required for cell growth and rDNA silencing in Saccharomyces cerevisiae. Genes Dev 15(24):3286–3295. https://doi.org/10.1101/gad.940201
Article Google Scholar
Bryk M, Briggs SD, Strahl BD, Curcio MJ, Allis CD, Winston F (2002) Evidence that Set1, a factor required for methylation of histone H3, regulates rDNA silencing in S. cerevisiae by a Sir2-independent mechanism. Curr Biol 12(2):165–170. https://doi.org/10.1016/S0960-9822(01)00652-2
Article Google Scholar
Burchell. (2011) PLU-1/JARID1B/KDM5B is required for embryonic survival and contributes to cell proliferation in the mammary gland and in ER+ breast cancer cells. Int J Oncol 38(5):1267. https://doi.org/10.3892/ijo.2011.956
Article Google Scholar
Carrozza MJ, Li B, Florens L, Suganuma T, Swanson SK, Lee KK, Shia W-J, Anderson S, Yates J, Washburn MP, Workman JL (2005) Histone H3 methylation by Set2 directs deacetylation of coding regions by Rpd3S to suppress spurious intragenic transcription. Cell 123(4):581–592. https://doi.org/10.1016/j.cell.2005.10.023
Article Google Scholar
Champagne KS, Saksouk N, Peña PV, Johnson K, Ullah M, Yang X, Côté J, Kutateladze TG (2008) The crystal structure of the ING5 PHD finger in complex with an H3K4me3 histone peptide. Proteins Struct Funct Bioinf 72(4):1371–1376. https://doi.org/10.1002/prot.22140
Article Google Scholar
Chang P-Y, Hom RA, Musselman CA, Zhu L, Kuo A, Gozani O, Kutateladze TG, Cleary ML (2010) Binding of the MLL PHD3 finger to histone H3K4me3 is required for MLL-dependent gene transcription. J Mol Biol 400(2):137–144. https://doi.org/10.1016/j.jmb.2010.05.005
Article Google Scholar
Chen K, Chen Z, Wu D, Zhang L, Lin X, Su J, Rodriguez B, Xi Y, Xia Z, Chen X, Shi X, Wang Q, Li W (2015a) Broad H3K4me3 is associated with increased transcription elongation and enhancer activity at tumor-suppressor genes. Nat Genet 47(10):1149–1157. https://doi.org/10.1038/ng.3385
Article Google Scholar
Chen Q, Sinha K, Deng JM, Yasuda H, Krahe R, Behringer RR, de Crombrugghe B (2015b) Mesenchymal deletion of histone demethylase NO66 in mice promotes bone formation. J Bone Miner Res 30(9):1608–1617. https://doi.org/10.1002/jbmr.2494
Article Google Scholar
Christensen J, Agger K, Cloos PAC, Pasini D, Rose S, Sennels L, Rappsilber J, Hansen KH, Salcini AE, Helin K (2007) RBP2 belongs to a family of demethylases, specific for tri-and dimethylated lysine 4 on histone 3. Cell 128(6):1063–1076. https://doi.org/10.1016/j.cell.2007.02.003
Article Google Scholar
Ciccone DN, Su H, Hevi S, Gay F, Lei H, Bajko J, Xu G, Li E, Chen T (2009) KDM1B is a histone H3K4 demethylase required to establish maternal genomic imprints. Nature 461(7262):415–418. https://doi.org/10.1038/nature08315
Article Google Scholar
Clouaire T, Webb S, Skene P, Illingworth R, Kerr A, Andrews R, Lee J-H, Skalnik D, Bird A (2012) Cfp1 integrates both CpG content and gene activity for accurate H3K4me3 deposition in embryonic stem cells. Genes Dev 26(15):1714–1728. https://doi.org/10.1101/gad.194209.112
Article Google Scholar
Core LJ, Waterfall JJ, Lis JT (2008) Nascent RNA sequencing reveals widespread pausing and divergent initiation at human promoters. Science 322(5909):1845–1848. https://doi.org/10.1126/science.1162228
Article Google Scholar
Creech AL, Taylor JE, Maier VK, Wu X, Feeney CM, Udeshi ND, Peach SE, Boehm JS, Lee JT, Carr SA, Jaffe JD (2015) Building the connectivity map of epigenetics: chromatin profiling by quantitative targeted mass spectrometry. Methods 72:57. https://doi.org/10.1016/j.ymeth.2014.10.033
Article Google Scholar
Creyghton MP, Cheng AW, Welstead GG, Kooistra T, Carey BW, Steine EJ, Hanna J, Lodato MA, Frampton GM, Sharp PA, Boyer LA, Young RA, Jaenisch R (2010) Histone H3K27ac separates active from poised enhancers and predicts developmental state. Proc Natl Acad Sci 107(50):21931–21936. https://doi.org/10.1073/pnas.1016071107
Article Google Scholar
Crispatzu G, Rehimi R, Pachano T, Bleckwehl T, Cruz-Molina S, Xiao C, Mahabir E, Bazzi H, Rada-Iglesias A (2021) The chromatin, topological and regulatory properties of pluripotency-associated poised enhancers are conserved in vivo. Nat Commun 12(1):4344. https://doi.org/10.1038/s41467-021-24641-4
Article Google Scholar
Dahl JA, Jung I, Aanes H, Greggains GD, Manaf A, Lerdrup M, Li G, Kuan S, Li B, Lee AY, Preissl S, Jermstad I, Haugen MH, Suganthan R, Bjørås M, Hansen K, Dalen KT, Fedorcsak P, Ren B, Klungland A (2016) Broad histone H3K4me3 domains in mouse oocytes modulate maternal-to-zygotic transition. Nature 537(7621):548–552. https://doi.org/10.1038/nature19360
Article Google Scholar
de Waal E, Mak W, Calhoun S, Stein P, Ord T, Krapp C, Coutifaris C, Schultz RM, Bartolomei MS (2014) In vitro culture increases the frequency of stochastic epigenetic errors at imprinted genes in placental tissues from mouse concepti produced through assisted reproductive technologies. Biol Reprod 90(2). https://doi.org/10.1095/biolreprod.113.114785
Demers C, Chaturvedi C-P, Ranish JA, Juban G, Lai P, Morle F, Aebersold R, Dilworth FJ, Groudine M, Brand M (2007) Activator-mediated recruitment of the MLL2 methyltransferase complex to the β-globin locus. Mol Cell 27(4):573–584. https://doi.org/10.1016/j.molcel.2007.06.022
Article Google Scholar
Denissov S, Hofemeister H, Marks H, Kranz A, Ciotta G, Singh S, Anastassiadis K, Stunnenberg HG, Stewart AF (2014) Mll2 is required for H3K4 trimethylation on bivalent promoters in embryonic stem cells, whereas Mll1 is redundant. Development 141(3):526–537. https://doi.org/10.1242/dev.102681
Article Google Scholar
Dey BK, Stalker L, Schnerch A, Bhatia M, Taylor-Papidimitriou J, Wynder C (2008) The histone demethylase KDM5b/JARID1b plays a role in cell fate decisions by blocking terminal differentiation. Mol Cell Biol 28(17):5312–5327. https://doi.org/10.1128/MCB.00128-08
Article Google Scholar
Dhar SS, Lee S-H, Kan P-Y, Voigt P, Ma L, Shi X, Reinberg D, Lee MG (2012) Trans -tail regulation of MLL4-catalyzed H3K4 methylation by H4R3 symmetric dimethylation is mediated by a tandem PHD of MLL4. Genes Dev 26(24):2749–2762. https://doi.org/10.1101/gad.203356.112
Article Google Scholar
Dorighi KM, Swigut T, Henriques T, Bhanu NV, Scruggs BS, Nady N, Still CD, Garcia BA, Adelman K, Wysocka J (2017) Mll3 and Mll4 facilitate enhancer RNA synthesis and transcription from promoters independently of H3K4 monomethylation. Mol Cell 66(4):568–576.e4. https://doi.org/10.1016/j.molcel.2017.04.018
Article Google Scholar
Dou Y, Milne TA, Tackett AJ, Smith ER, Fukuda A, Wysocka J, Allis CD, Chait BT, Hess JL, Roeder RG (2005) Physical association and coordinate function of the H3 K4 methyltransferase MLL1 and the H4 K16 acetyltransferase MOF. Cell 121(6):873–885. https://doi.org/10.1016/j.cell.2005.04.031
Article Google Scholar
Dou Y, Milne TA, Ruthenburg AJ, Lee S, Lee JW, Verdine GL, Allis CD, Roeder RG (2006) Regulation of MLL1 H3K4 methyltransferase activity by its core components. Nat Struct Mol Biol 13(8):713–719. https://doi.org/10.1038/nsmb1128
Article Google Scholar
Douillet D, Sze CC, Ryan C, Piunti A, Shah AP, Ugarenko M, Marshall SA, Rendleman EJ, Zha D, Helmin KA, Zhao Z, Cao K, Morgan MA, Singer BD, Bartom ET, Smith ER, Shilatifard A (2020) Uncoupling histone H3K4 trimethylation from developmental gene expression via an equilibrium of COMPASS, polycomb and DNA methylation. Nature Genet 52(6):615–625. https://doi.org/10.1038/s41588-020-0618-1
Article Google Scholar
Dreijerink KMA, Mulder KW, Winkler GS, Höppener JWM, Lips CJM, Timmers HT, M. (2006) Menin links estrogen receptor activation to histone H3K4 trimethylation. Cancer Res 66(9):4929–4935. https://doi.org/10.1158/0008-5472.CAN-05-4461
Article Google Scholar
Ernst P, Vakoc CR (2012) WRAD: enabler of the SET1-family of H3K4 methyltransferases. Brief Funct Genomics 11(3):217–226. https://doi.org/10.1093/bfgp/els017
Article Google Scholar
Ernst P, Wang J, Huang M, Goodman RH, Korsmeyer SJ (2001) MLL and CREB bind cooperatively to the nuclear coactivator CREB-binding protein. Mol Cell Biol 21(7):2249–2258. https://doi.org/10.1128/MCB.21.7.2249-2258.2001
Article Google Scholar
Ernst P, Fisher JK, Avery W, Wade S, Foy D, Korsmeyer SJ (2004) Definitive hematopoiesis requires the mixed-lineage leukemia gene. Dev Cell 6(3):437–443. https://doi.org/10.1016/S1534-5807(04)00061-9
Article Google Scholar
Fang R, Barbera AJ, Xu Y, Rutenberg M, Leonor T, Bi Q, Lan F, Mei P, Yuan G-C, Lian C, Peng J, Cheng D, Sui G, Kaiser UB, Shi Y, Shi YG (2010) Human LSD2/KDM1b/AOF1 regulates gene transcription by modulating intragenic H3K4me2 methylation. Mol Cell 39(2):222–233. https://doi.org/10.1016/j.molcel.2010.07.008
Article Google Scholar
Fang L, Zhang J, Zhang H, Yang X, Jin X, Zhang L, Skalnik DG, Jin Y, Zhang Y, Huang X, Li J, Wong J (2016) H3K4 methyltransferase Set1a is A key Oct4 coactivator essential for generation of Oct4 positive inner cell mass. Stem Cells 34(3):565–580. https://doi.org/10.1002/stem.2250
Article Google Scholar
Fossati A, Dolfini D, Donati G, Mantovani R (2011) NF-Y recruits Ash2L to impart H3K4 trimethylation on CCAAT promoters. PLoS One 6(3):e17220. https://doi.org/10.1371/journal.pone.0017220
Article Google Scholar
Foster CT, Dovey OM, Lezina L, Luo JL, Gant TW, Barlev N, Bradley A, Cowley SM (2010) Lysine-specific demethylase 1 regulates the embryonic transcriptome and CoREST stability. Mol Cell Biol 30(20):4851–4863. https://doi.org/10.1128/MCB.00521-10
Article Google Scholar
Froimchuk E, Jang Y, Ge K (2017) Histone H3 lysine 4 methyltransferase KMT2D. Gene 627:337–342. https://doi.org/10.1016/j.gene.2017.06.056
Article Google Scholar
Fuda NJ, Ardehali MB, Lis JT (2009) Defining mechanisms that regulate RNA polymerase II transcription in vivo. Nature 461(7261):186–192. https://doi.org/10.1038/nature08449
Article Google Scholar
Gadue P, Huber TL, Paddison PJ, Keller GM (2006) Wnt and TGF-beta signaling are required for the induction of an in vitro model of primitive streak formation using embryonic stem cells. Proc Natl Acad Sci U S A 103(45):16806–16811. https://doi.org/10.1073/pnas.0603916103
Article Google Scholar
Gaspar-Maia A, Alajem A, Meshorer E, Ramalho-Santos M (2011) Open chromatin in pluripotency and reprogramming. Nat Rev Mol Cell Biol 12(1):36–47. https://doi.org/10.1038/nrm3036
Article Google Scholar
Giaimo BD, Ferrante F, Herchenröther A, Hake SB, Borggrefe T (2019) The histone variant H2A.Z in gene regulation. Epigenetics Chromatin 12(1):37. https://doi.org/10.1186/s13072-019-0274-9
Article Google Scholar
Glaser S, Schaft J, Lubitz S, Vintersten K, van der Hoeven F, Tufteland KR, Aasland R, Anastassiadis K, Ang S-L, Stewart AF (2006) Multiple epigenetic maintenance factors implicated by the loss of Mll2 in mouse development. Development 133(8):1423–1432. https://doi.org/10.1242/dev.02302
Article Google Scholar
Glaser S, Lubitz S, Loveland KL, Ohbo K, Robb L, Schwenk F, Seibler J, Roellig D, Kranz A, Anastassiadis K, Stewart AF (2009) The histone 3 lysine 4 methyltransferase, Mll2, is only required briefly in development and spermatogenesis. Epigenetics Chromatin 2(1):5. https://doi.org/10.1186/1756-8935-2-5
Article Google Scholar
Grandy RA, Whitfield TW, Wu H, Fitzgerald MP, VanOudenhove JJ, Zaidi SK, Montecino MA, Lian JB, van Wijnen AJ, Stein JL, Stein GS (2016) Genome-wide studies reveal that H3K4me3 modification in bivalent genes is dynamically regulated during the pluripotent cell cycle and stabilized upon differentiation. Mol Cell Biol 36(4):615–627. https://doi.org/10.1128/MCB.00877-15
Article Google Scholar
Guenther MG, Jenner RG, Chevalier B, Nakamura T, Croce CM, Canaani E, Young RA (2005) Global and Hox-specific roles for the MLL1 methyltransferase. Proc Natl Acad Sci 102(24):8603–8608. https://doi.org/10.1073/pnas.0503072102
Article Google Scholar
Guenther MG, Levine SS, Boyer LA, Jaenisch R, Young RA (2007) A chromatin landmark and transcription initiation at most promoters in human cells. Cell 130(1):77–88. https://doi.org/10.1016/j.cell.2007.05.042
Article Google Scholar
Harmeyer KM, Facompre ND, Herlyn M, Basu D (2017) JARID1 histone demethylases: emerging targets in cancer. Trends Cancer 3(10):713–725. https://doi.org/10.1016/j.trecan.2017.08.004
Article Google Scholar
Henckel A, Chebli K, Kota SK, Arnaud P, Feil R (2012) Transcription and histone methylation changes correlate with imprint acquisition in male germ cells. EMBO J 31(3):606–615. https://doi.org/10.1038/emboj.2011.425
Article Google Scholar
Hödl M, Basler K (2012) Transcription in the absence of histone H3.2 and H3K4 methylation. Curr Biol 22(23):2253–2257. https://doi.org/10.1016/j.cub.2012.10.008
Article Google Scholar
Howe FS, Fischl H, Murray SC, Mellor J (2017) Is H3K4me3 instructive for transcription activation? BioEssays 39(1):1–12. https://doi.org/10.1002/bies.201600095
Article Google Scholar
Hu G, Cui K, Northrup D, Liu C, Wang C, Tang Q, Ge K, Levens D, Crane-Robinson C, Zhao K (2013) H2A.Z facilitates access of active and repressive complexes to chromatin in embryonic stem cell self-renewal and differentiation. Cell Stem Cell 12(2):180–192. https://doi.org/10.1016/j.stem.2012.11.003
Article Google Scholar
Hu S, Song A, Peng L, Tang N, Qiao Z, Wang Z, Lan F, Chen FX (2023) H3K4me2/3 modulate the stability of RNA polymerase II pausing. Cell Res 33(5):403–406. https://doi.org/10.1038/s41422-023-00794-3
Article Google Scholar
Hung T, Binda O, Champagne KS, Kuo AJ, Johnson K, Chang HY, Simon MD, Kutateladze TG, Gozani O (2009) ING4 mediates crosstalk between histone H3 K4 trimethylation and H3 acetylation to attenuate cellular transformation. Mol Cell 33(2):248–256. https://doi.org/10.1016/j.molcel.2008.12.016
Article Google Scholar
Irion S, Nostro MC, Kattman SJ, Keller GM (2008) Directed differentiation of pluripotent stem cells: from developmental biology to therapeutic applications. Cold Spring Harb Symp Quant Biol 73:101–110. https://doi.org/10.1101/sqb.2008.73.065
Article Google Scholar
Ishihara T, Griffith OW, Suzuki S, Renfree MB (2022) Presence of H3K4me3 on paternally expressed genes of the paternal genome from sperm to implantation. Front Cell Dev Biol 10. https://doi.org/10.3389/fcell.2022.838684
Iwase S, Brookes E, Agarwal S, Badeaux AI, Ito H, Vallianatos CN, Tomassy GS, Kasza T, Lin G, Thompson A, Gu L, Kwan KY, Chen C, Sartor MA, Egan B, Xu J, Shi Y (2016) A mouse model of X-linked intellectual disability associated with impaired removal of histone methylation. Cell Rep 14(5):1000–1009. https://doi.org/10.1016/j.celrep.2015.12.091
Article Google Scholar
Jain K, Marunde MR, Burg JM, Gloor SL, Joseph FM, Poncha KF, Gillespie ZB, Rodriguez KL, Popova IK, Hall NW, Vaidya A, Howard SA, Taylor HF, Mukhsinova L, Onuoha UC, Patteson EF, Cooke SW, Taylor BC, Weinzapfel EN et al (2023) An acetylation-mediated chromatin switch governs H3K4 methylation read-write capability. elife 12. https://doi.org/10.7554/eLife.82596
Jeong KW, Kim K, Situ AJ, Ulmer TS, An W, Stallcup MR (2011) Recognition of enhancer element–specific histone methylation by TIP60 in transcriptional activation. Nat Struct Mol Biol 18(12):1358–1365. https://doi.org/10.1038/nsmb.2153
Article Google Scholar
Jiang H, Shukla A, Wang X, Chen W, Bernstein BE, Roeder RG (2011) Role for Dpy-30 in ES cell-fate specification by regulation of H3K4 methylation within bivalent domains. Cell 144(4):513–525. https://doi.org/10.1016/j.cell.2011.01.020
Article Google Scholar
Kalkan T, Smith A (2014) Mapping the route from naive pluripotency to lineage specification. Philos Trans R Soc B Biol Sci 369(1657):20130540. https://doi.org/10.1098/rstb.2013.0540
Article Google Scholar
Kang Y, Kim YW, Kang J, Kim A (2021) Histone H3K4me1 and H3K27ac play roles in nucleosome eviction and eRNA transcription, respectively, at enhancers. FASEB J 35(8):e21781. https://doi.org/10.1096/fj.202100488R
Article Google Scholar
Karytinos A, Forneris F, Profumo A, Ciossani G, Battaglioli E, Binda C, Mattevi A (2009) A novel mammalian flavin-dependent histone demethylase. J Biol Chem 284(26):17775–17782. https://doi.org/10.1074/jbc.M109.003087
Article Google Scholar
Kebede AF, Nieborak A, Shahidian LZ, Le Gras S, Richter F, Gómez DA, Baltissen MP, Meszaros G, Magliarelli HDF, Taudt A, Margueron R, Colomé-Tatché M, Ricci R, Daujat S, Vermeulen M, Mittler G, Schneider R (2017) Histone propionylation is a mark of active chromatin. Nat Struct Mol Biol 24(12):1048–1056. https://doi.org/10.1038/nsmb.3490
Article Google Scholar
Keller GM (1995) In vitro differentiation of embryonic stem cells. Curr Opin Cell Biol 7(6):862–869. 0955-0674(95)80071-9 [pii]
Google Scholar
Keogh M-C, Kurdistani SK, Morris SA, Ahn SH, Podolny V, Collins SR, Schuldiner M, Chin K, Punna T, Thompson NJ, Boone C, Emili A, Weissman JS, Hughes TR, Strahl BD, Grunstein M, Greenblatt JF, Buratowski S, Krogan NJ (2005) Cotranscriptional Set2 methylation of histone H3 lysine 36 recruits a repressive Rpd3 complex. Cell 123(4):593–605. https://doi.org/10.1016/j.cell.2005.10.025
Article Google Scholar
Kidder BL, Hu G, Zhao K (2014) KDM5B focuses H3K4 methylation near promoters and enhancers during embryonic stem cell self-renewal and differentiation. Genome Biol 15(2):R32. https://doi.org/10.1186/gb-2014-15-2-r32
Article Google Scholar
Kim J, Singh AK, Takata Y, Lin K, Shen J, Lu Y, Kerenyi MA, Orkin SH, Chen T (2015) LSD1 is essential for oocyte meiotic progression by regulating CDC25B expression in mice. Nat Commun 6(1):10116. https://doi.org/10.1038/ncomms10116
Article Google Scholar
Klose RJ, Yan Q, Tothova Z, Yamane K, Erdjument-Bromage H, Tempst P, Gilliland DG, Zhang Y, Kaelin WG (2007) The retinoblastoma binding protein RBP2 is an H3K4 demethylase. Cell 128(5):889–900. https://doi.org/10.1016/j.cell.2007.02.013
Article Google Scholar
Kranz A, Anastassiadis K (2020) The role of SETD1A and SETD1B in development and disease. Biochim Biophys Acta (BBA) – Gene Regul Mech 1863(8):194578. https://doi.org/10.1016/j.bbagrm.2020.194578
Article Google Scholar
Lalonde M-E, Avvakumov N, Glass KC, Joncas F-H, Saksouk N, Holliday M, Paquet E, Yan K, Tong Q, Klein BJ, Tan S, Yang X-J, Kutateladze TG, Côté J (2013) Exchange of associated factors directs a switch in HBO1 acetyltransferase histone tail specificity. Genes Dev 27(18):2009–2024. https://doi.org/10.1101/gad.223396.113
Article Google Scholar
Landry J, Sharov AA, Piao Y, Sharova LV, Xiao H, Southon E, Matta J, Tessarollo L, Zhang YE, Ko MSH, Kuehn MR, Yamaguchi TP, Wu C (2008) Essential role of chromatin remodeling protein Bptf in early mouse embryos and embryonic stem cells. PLoS Genet 4(10):e1000241. https://doi.org/10.1371/journal.pgen.1000241
Article Google Scholar
Lauberth SM, Nakayama T, Wu X, Ferris AL, Tang Z, Hughes SH, Roeder RG (2013) H3K4me3 interactions with TAF3 regulate preinitiation complex assembly and selective gene activation. Cell 152(5):1021–1036. https://doi.org/10.1016/j.cell.2013.01.052
Article Google Scholar
Lee J-H, Skalnik DG (2005) CpG-binding protein (CXXC finger protein 1) is a component of the mammalian Set1 histone H3-Lys4 methyltransferase complex, the analogue of the yeast Set1/COMPASS complex. J Biol Chem 280(50):41725–41731. https://doi.org/10.1074/jbc.M508312200
Article Google Scholar
Lee J, Kim D-H, Lee S, Yang Q-H, Lee DK, Lee S-K, Roeder RG, Lee JW (2009) A tumor suppressive coactivator complex of p53 containing ASC-2 and histone H3-lysine-4 methyltransferase MLL3 or its paralogue MLL4. Proc Natl Acad Sci 106(21):8513–8518. https://doi.org/10.1073/pnas.0902873106
Article Google Scholar
Lee J-E, Wang C, Xu S, Cho Y-W, Wang L, Feng X, Baldridge A, Sartorelli V, Zhuang L, Peng W, Ge K (2013) H3K4 mono- and di-methyltransferase MLL4 is required for enhancer activation during cell differentiation. elife 2:e01503. https://doi.org/10.7554/eLife.01503
Article Google Scholar
Lee Y-T, Ayoub A, Park S-H, Sha L, Xu J, Mao F, Zheng W, Zhang Y, Cho U-S, Dou Y (2021) Mechanism for DPY30 and ASH2L intrinsically disordered regions to modulate the MLL/SET1 activity on chromatin. Nat Commun 12(1):2953. https://doi.org/10.1038/s41467-021-23268-9
Article Google Scholar
Lewis SL, Tam PPL (2006) Definitive endoderm of the mouse embryo: formation, cell fates, and morphogenetic function. Dev Dyn 235(9):2315–2329. https://doi.org/10.1002/dvdy.20846
Article Google Scholar
Li N, Carrel L (2008) Escape from X chromosome inactivation is an intrinsic property of the Jarid1c locus. Proc Natl Acad Sci 105(44):17055–17060. https://doi.org/10.1073/pnas.0807765105
Article Google Scholar
Li B, Carey M, Workman JL (2007) The role of chromatin during transcription. Cell 128:707. https://doi.org/10.1016/j.cell.2007.01.015
Article Google Scholar
Li N, Dhar SS, Chen T-Y, Kan P-Y, Wei Y, Kim J-H, Chan C-H, Lin H-K, Hung M-C, Lee MG (2016) JARID1D is a suppressor and prognostic marker of prostate cancer invasion and metastasis. Cancer Res 76(4):831–843. https://doi.org/10.1158/0008-5472.CAN-15-0906
Article Google Scholar
Li Q, Mao F, Zhou B, Huang Y, Zou Z, denDekker AD, Xu J, Hou S, Liu J, Dou Y, Rao RC (2020) p53 integrates temporal WDR5 inputs during neuroectoderm and mesoderm differentiation of mouse embryonic stem cells. Cell Rep 30(2):465–480.e6. https://doi.org/10.1016/j.celrep.2019.12.039
Article Google Scholar
Lin W, Cao J, Liu J, Beshiri ML, Fujiwara Y, Francis J, Cherniack AD, Geisen C, Blair LP, Zou MR, Shen X, Kawamori D, Liu Z, Grisanzio C, Watanabe H, Minamishima YA, Zhang Q, Kulkarni RN, Signoretti S et al (2011) Loss of the retinoblastoma binding protein 2 (RBP2) histone demethylase suppresses tumorigenesis in mice lacking Rb1 or Men1. Proc Natl Acad Sci 108(33):13379–13386. https://doi.org/10.1073/pnas.1110104108
Article Google Scholar
Liu X, Wang C, Liu W, Li J, Li C, Kou X, Chen J, Zhao Y, Gao H, Wang H, Zhang Y, Gao Y, Gao S (2016) Distinct features of H3K4me3 and H3K27me3 chromatin domains in pre-implantation embryos. Nature 537(7621):558–562. https://doi.org/10.1038/nature19362
Article Google Scholar
Liu L, Fang Y, Ding X, Zhou W, Terranova R, Zhang Y, Wang H (2023) Wdr5 is essential for fetal erythropoiesis and hematopoiesis. Exp Hematol Oncol 12(1):39. https://doi.org/10.1186/s40164-023-00385-3
Article Google Scholar
Lubitz S, Glaser S, Schaft J, Stewart AF, Anastassiadis K (2007) Increased apoptosis and skewed differentiation in mouse embryonic stem cells lacking the histone methyltransferase Mll2. Mol Biol Cell 18(6):2356–2366. https://doi.org/10.1091/mbc.e06-11-1060
Article Google Scholar
Lv J, Chen K (2016) Broad H3K4me3 as a novel epigenetic signature for normal development and disease. Genomics Proteomics Bioinf 14(5):262–264. https://doi.org/10.1016/j.gpb.2016.09.001
Article Google Scholar
Martin BJE, Brind’Amour J, Kuzmin A, Jensen KN, Liu ZC, Lorincz M, Howe LJ (2021) Transcription shapes genome-wide histone acetylation patterns. Nat Commun 12(1):210. https://doi.org/10.1038/s41467-020-20543-z
Article Google Scholar
Medvedev SP, Shevchenko AI, Zakian SM (2010) Molecular basis of mammalian embryonic stem cell pluripotency and self-renewal. Acta Nat 2(3):30–46
Google Scholar
Metzger E, Wissmann M, Yin N, Müller JM, Schneider R, Peters AHFM, Günther T, Buettner R, Schüle R (2005) LSD1 demethylates repressive histone marks to promote androgen-receptor-dependent transcription. Nature 437(7057):436–439. https://doi.org/10.1038/nature04020
Article Google Scholar
Meyfour A, Pahlavan S, Ansari H, Baharvand H, Salekdeh GH (2019) Down-regulation of a male-specific H3K4 demethylase, KDM5D, impairs cardiomyocyte differentiation. J Proteome Res 18(12):4277–4282. https://doi.org/10.1021/acs.jproteome.9b00395
Article Google Scholar
Mfopou JK, Geeraerts M, Dejene R, Van Langenhoven S, Aberkane A, Van Grunsven LA, Bouwens L (2014) Efficient definitive endoderm induction from mouse embryonic stem cell adherent cultures: a rapid screening model for differentiation studies. Stem Cell Res 12:166. https://doi.org/10.1016/j.scr.2013.10.004
Article Google Scholar
Mikulasova A, Kent D, Trevisan-Herraz M, Karataraki N, Fung KTM, Ashby C, Cieslak A, Yaccoby S, van Rhee F, Zangari M, Thanendrarajan S, Schinke C, Morgan GJ, Asnafi V, Spicuglia S, Brackley CA, Corcoran AE, Hambleton S, Walker BA et al (2022) Epigenomic translocation of H3K4me3 broad domains over oncogenes following hijacking of super-enhancers. Genome Res 32(7):1343–1354. https://doi.org/10.1101/gr.276042.121
Article Google Scholar
Milne TA, Briggs SD, Brock HW, Martin ME, Gibbs D, Allis CD, Hess JL (2002) MLL targets SET domain methyltransferase activity to Hox gene promoters. Mol Cell 10(5):1107–1117. https://doi.org/10.1016/S1097-2765(02)00741-4
Article Google Scholar
Milne TA, Dou Y, Martin ME, Brock HW, Roeder RG, Hess JL (2005) MLL associates specifically with a subset of transcriptionally active target genes. Proc Natl Acad Sci 102(41):14765–14770. https://doi.org/10.1073/pnas.0503630102
Article Google Scholar
Milne TA, Kim J, Wang GG, Stadler SC, Basrur V, Whitcomb SJ, Wang Z, Ruthenburg AJ, Elenitoba-Johnson KSJ, Roeder RG, Allis CD (2010) Multiple interactions recruit MLL1 and MLL1 fusion proteins to the HOXA9 locus in leukemogenesis. Mol Cell 38(6):853–863. https://doi.org/10.1016/j.molcel.2010.05.011
Article Google Scholar
Morey L, Santanach A, Di Croce L (2015) Pluripotency and epigenetic factors in mouse embryonic stem cell fate regulation. Mol Cell Biol 35(16):2716–2728. https://doi.org/10.1128/MCB.00266-15
Article Google Scholar
Morrison EA, Musselman CA (2016) The role of PHD fingers in chromatin signaling. In: Chromatin signaling and diseases. Elsevier, pp 127–147. https://doi.org/10.1016/B978-0-12-802389-1.00007-1
Chapter Google Scholar
Morrison EA, Bowerman S, Sylvers KL, Wereszczynski J, Musselman CA (2018) The conformation of the histone H3 tail inhibits association of the BPTF PHD finger with the nucleosome. elife 7. https://doi.org/10.7554/eLife.31481
Myrick DA, Christopher MA, Scott AM, Simon AK, Donlin-Asp PG, Kelly WG, Katz DJ (2017) KDM1A/LSD1 regulates the differentiation and maintenance of spermatogonia in mice. PLoS One 12(5):e0177473. https://doi.org/10.1371/journal.pone.0177473
Article Google Scholar
Nady N, Lemak A, Walker JR, Avvakumov GV, Kareta MS, Achour M, Xue S, Duan S, Allali-Hassani A, Zuo X, Wang Y-X, Bronner C, Chédin F, Arrowsmith CH, Dhe-Paganon S (2011) Recognition of multivalent histone states associated with heterochromatin by UHRF1 protein. J Biol Chem 286(27):24300–24311. https://doi.org/10.1074/jbc.M111.234104
Article Google Scholar
Ng HH, Robert F, Young RA, Struhl K (2003) Targeted recruitment of Set1 histone methylase by elongating pol II provides a localized mark and memory of recent transcriptional activity. Mol Cell 11(3):709–719. https://doi.org/10.1016/S1097-2765(03)00092-3
Article Google Scholar
Nightingale KP, Gendreizig S, White DA, Bradbury C, Hollfelder F, Turner BM (2007) Cross-talk between histone modifications in response to histone deacetylase inhibitors. J Biol Chem 282(7):4408–4416. https://doi.org/10.1074/jbc.M606773200
Article Google Scholar
Nislow C, Ray E, Pillus L (1997) SET1, a yeast member of the trithorax family, functions in transcriptional silencing and diverse cellular processes. Mol Biol Cell 8(12):2421–2436. https://doi.org/10.1091/mbc.8.12.2421
Article Google Scholar
Nostro MC, Cheng X, Keller GM, Gadue P (2008) Wnt, activin, and BMP signaling regulate distinct stages in the developmental pathway from embryonic stem cells to blood. Cell Stem Cell 2:60. https://doi.org/10.1016/j.stem.2007.10.011
Article Google Scholar
Ntorla A, Burgoyne JR (2021) The regulation and function of histone crotonylation. Front Cell Dev Biol 9. https://doi.org/10.3389/fcell.2021.624914
Ooi SKT, Qiu C, Bernstein E, Li K, Jia D, Yang Z, Erdjument-Bromage H, Tempst P, Lin S-P, Allis CD, Cheng X, Bestor TH (2007) DNMT3L connects unmethylated lysine 4 of histone H3 to de novo methylation of DNA. Nature 448(7154):714–717. https://doi.org/10.1038/nature05987
Article Google Scholar
Orkin SH, Hochedlinger K (2011) Chromatin connections to pluripotency and cellular reprogramming. Cell 145(6):835–850. https://doi.org/10.1016/j.cell.2011.05.019
Article Google Scholar
Orkin SH, Wang J, Kim J, Chu J, Rao S, Theunissen TW, Shen X, Levasseur DN (2008) The transcriptional network controlling pluripotency in ES cells. Cold Spring Harb Symp Quant Biol 73(0):195–202. https://doi.org/10.1101/sqb.2008.72.001
Article Google Scholar
Outchkourov NS, Muiño JM, Kaufmann K, van Ijcken WFJ, Koerkamp MJG, van Leenen D, de Graaf P, Holstege FCP, Grosveld FG, Timmers HTM (2013) Balancing of histone H3K4 methylation states by the Kdm5c/SMCX histone demethylase modulates promoter and enhancer function. Cell Rep 3(4):1071–1079. https://doi.org/10.1016/j.celrep.2013.02.030
Article Google Scholar
Patel SR, Kim D, Levitan I, Dressler GR (2007) The BRCT-domain containing protein PTIP links PAX2 to a histone H3, lysine 4 methyltransferase complex. Dev Cell 13(4):580–592. https://doi.org/10.1016/j.devcel.2007.09.004
Article Google Scholar
Patel A, Dharmarajan V, Vought VE, Cosgrove MS (2009) On the mechanism of multiple lysine methylation by the human mixed lineage leukemia protein-1 (MLL1) core complex. J Biol Chem 284(36):24242–24256. https://doi.org/10.1074/jbc.M109.014498
Article Google Scholar
Pekowska A, Benoukraf T, Ferrier P, Spicuglia S (2010) A unique H3K4me2 profile marks tissue-specific gene regulation. Genome Res 20(11):1493–1502. https://doi.org/10.1101/gr.109389.110
Article Google Scholar
Pekowska A, Benoukraf T, Zacarias-Cabeza J, Belhocine M, Koch F, Holota H, Imbert J, Andrau J-C, Ferrier P, Spicuglia S (2011) H3K4 tri-methylation provides an epigenetic signature of active enhancers. EMBO J 30(20):4198–4210. https://doi.org/10.1038/emboj.2011.295
Article Google Scholar
Peña PV, Davrazou F, Shi X, Walter KL, Verkhusha VV, Gozani O, Zhao R, Kutateladze TG (2006) Molecular mechanism of histone H3K4me3 recognition by plant homeodomain of ING2. Nature 442(7098):100–103. https://doi.org/10.1038/nature04814
Article Google Scholar
Placek K, Hu G, Cui K, Zhang D, Ding Y, Lee J-E, Jang Y, Wang C, Konkel JE, Song J, Liu C, Ge K, Chen W, Zhao K (2017) MLL4 prepares the enhancer landscape for Foxp3 induction via chromatin looping. Nat Immunol 18(9):1035–1045. https://doi.org/10.1038/ni.3812
Article Google Scholar
Poreba E, Lesniewicz K, Durzynska J (2020) Aberrant activity of histone–lysine N-methyltransferase 2 (KMT2) complexes in oncogenesis. Int J Mol Sci 21(24):9340. https://doi.org/10.3390/ijms21249340
Article Google Scholar
Qin S, Jin L, Zhang J, Liu L, Ji P, Wu M, Wu J, Shi Y (2011) Recognition of unmodified histone H3 by the first PHD finger of bromodomain-PHD finger protein 2 provides insights into the regulation of histone acetyltransferases Monocytic leukemic zinc-finger protein (MOZ) and MOZ-related factor (MORF). J Biol Chem 286(42):36944–36955. https://doi.org/10.1074/jbc.M111.244400
Article Google Scholar
Rada-Iglesias A, Bajpai R, Swigut T, Brugmann SA, Flynn RA, Wysocka J (2011) A unique chromatin signature uncovers early developmental enhancers in humans. Nature 470(7333):279–283. https://doi.org/10.1038/nature09692
Article Google Scholar
Rahl PB, Lin CY, Seila AC, Flynn RA, McCuine S, Burge CB, Sharp PA, Young RA (2010) C-Myc regulates transcriptional pause release. Cell 141(3):432–445. https://doi.org/10.1016/j.cell.2010.03.030
Article Google Scholar
Ruthenburg AJ, Allis CD, Wysocka J (2007) Methylation of lysine 4 on histone H3: intricacy of writing and reading a single epigenetic mark. Mol Cell 25(1):15–30. https://doi.org/10.1016/j.molcel.2006.12.014
Article Google Scholar
Santos-Rosa H, Schneider R, Bannister AJ, Sherriff J, Bernstein BE, Emre NCT, Schreiber SL, Mellor J, Kouzarides T (2002) Active genes are tri-methylated at K4 of histone H3. Nature 419(6905):407–411. https://doi.org/10.1038/nature01080
Article Google Scholar
Scandaglia M, Lopez-Atalaya JP, Medrano-Fernandez A, Lopez-Cascales MT, del Blanco B, Lipinski M, Benito E, Olivares R, Iwase S, Shi Y, Barco A (2017) Loss of Kdm5c causes spurious transcription and prevents the fine-tuning of activity-regulated enhancers in neurons. Cell Rep 21(1):47–59. https://doi.org/10.1016/j.celrep.2017.09.014
Article Google Scholar
Schmidt K, Zhang Q, Tasdogan A, Petzold A, Dahl A, Arneth BM, Slany R, Fehling HJ, Kranz A, Stewart AF, Anastassiadis K (2018) The H3K4 methyltransferase Setd1b is essential for hematopoietic stem and progenitor cell homeostasis in mice. elife 7. https://doi.org/10.7554/eLife.27157
Schneider J, Wood A, Lee J-S, Schuster R, Dueker J, Maguire C, Swanson SK, Florens L, Washburn MP, Shilatifard A (2005) Molecular regulation of histone H3 trimethylation by COMPASS and the regulation of gene expression. Mol Cell 19(6):849–856. https://doi.org/10.1016/j.molcel.2005.07.024
Article Google Scholar
Seila AC, Calabrese JM, Levine SS, Yeo GW, Rahl PB, Flynn RA, Young RA, Sharp PA (2008) Divergent transcription from active promoters. Science 322(5909):1849–1851. https://doi.org/10.1126/science.1162253
Article Google Scholar
Sezginmert D, Terzi Cizmecioglu N (2023) Histone proteomics implicates H3K36me2 and its regulators in mouse embryonic stem cell pluripotency exit and lineage choice. Turk J Biochem 48(4):351–361. https://doi.org/10.1515/tjb-2023-0030
Article Google Scholar
Sha Q-Q, Zhu Y-Z, Xiang Y, Yu J-L, Fan X-Y, Li Y-C, Wu Y-W, Shen L, Fan H-Y (2021) Role of CxxC-finger protein 1 in establishing mouse oocyte epigenetic landscapes. Nucleic Acids Res 49(5):2569–2582. https://doi.org/10.1093/nar/gkab107
Article Google Scholar
Shao G-B, Chen J-C, Zhang L-P, Huang P, Lu H-Y, Jin J, Gong A-H, Sang J-R (2014) Dynamic patterns of histone H3 lysine 4 methyltransferases and demethylases during mouse preimplantation development. In Vitro Cell Dev Biol Anim 50(7):603–613. https://doi.org/10.1007/s11626-014-9741-6
Article Google Scholar
Shen X, Hu K, Cheng G, Xu L, Chen Z, Du P, Zhuang Z (2019) KDM5D inhibit epithelial-mesenchymal transition of gastric cancer through demethylation in the promoter of Cul4A in male. J Cell Biochem 120(8):12247–12258. https://doi.org/10.1002/jcb.27308
Article Google Scholar
Shi Y, Lan F, Matson C, Mulligan P, Whetstine JR, Cole PA, Casero RA, Shi Y (2004) Histone demethylation mediated by the nuclear amine oxidase homolog LSD1. Cell 119(7):941–953. https://doi.org/10.1016/j.cell.2004.12.012
Article Google Scholar
Shi X, Hong T, Walter KL, Ewalt M, Michishita E, Hung T, Carney D, Peña P, Lan F, Kaadige MR, Lacoste N, Cayrou C, Davrazou F, Saha A, Cairns BR, Ayer DE, Kutateladze TG, Shi Y, Côté J et al (2006) ING2 PHD domain links histone H3 lysine 4 methylation to active gene repression. Nature 442(7098):96–99. https://doi.org/10.1038/nature04835
Article Google Scholar
Shinsky SA, Monteith KE, Viggiano S, Cosgrove MS (2015) Biochemical reconstitution and phylogenetic comparison of human SET1 family core complexes involved in histone methylation. J Biol Chem 290(10):6361–6375. https://doi.org/10.1074/jbc.M114.627646
Article Google Scholar
Sims RJ, Reinberg D (2006) Histone H3 Lys 4 methylation: caught in a bind? Genes Dev 20(20):2779–2786. https://doi.org/10.1101/gad.1468206
Article Google Scholar
Sinha KM, Yasuda H, Coombes MM, Dent SYR, de Crombrugghe B (2010) Regulation of the osteoblast-specific transcription factor Osterix by NO66, a Jumonji family histone demethylase. EMBO J 29(1):68–79. https://doi.org/10.1038/emboj.2009.332
Article Google Scholar
Smith E, Shilatifard A (2010) The chromatin signaling pathway: diverse mechanisms of recruitment of histone-modifying enzymes and varied biological outcomes. Mol Cell 40(5):689–701. https://doi.org/10.1016/j.molcel.2010.11.031
Article Google Scholar
Smith E, Shilatifard A (2014) Enhancer biology and enhanceropathies. Nat Struct Mol Biol 21(3):210–219. https://doi.org/10.1038/nsmb.2784
Article Google Scholar
Stewart KR, Veselovska L, Kim J, Huang J, Saadeh H, Tomizawa S, Smallwood SA, Chen T, Kelsey G (2015) Dynamic changes in histone modifications precede de novo DNA methylation in oocytes. Genes Dev 29(23):2449–2462. https://doi.org/10.1101/gad.271353.115
Article Google Scholar
Stoller JZ, Huang L, Tan CC, Huang F, Zhou DD, Yang J, Gelb BD, Epstein JA (2010) Ash2l interacts with Tbx1 and is required during early embryogenesis. Exp Biol Med 235(5):569–576. https://doi.org/10.1258/ebm.2010.009318
Article Google Scholar
Stützer A, Liokatis S, Kiesel A, Schwarzer D, Sprangers R, Söding J, Selenko P, Fischle W (2016) Modulations of DNA contacts by linker histones and post-translational modifications determine the mobility and modifiability of nucleosomal H3 tails. Mol Cell 61(2):247–259. https://doi.org/10.1016/j.molcel.2015.12.015
Article Google Scholar
Tang Z, Chen W-Y, Shimada M, Nguyen UTT, Kim J, Sun X-J, Sengoku T, McGinty RK, Fernandez JP, Muir TW, Roeder RG (2013) SET1 and p300 act synergistically, through coupled histone modifications, in transcriptional activation by p53. Cell 154(2):297–310. https://doi.org/10.1016/j.cell.2013.06.027
Article Google Scholar
Terranova R, Agherbi H, Boned A, Meresse S, Djabali M (2006) Histone and DNA methylation defects at Hox genes in mice expressing a SET domain-truncated form of Mll. Proc Natl Acad Sci 103(17):6629–6634. https://doi.org/10.1073/pnas.0507425103
Article Google Scholar
Terzi N, Churchman LS, Vasiljeva L, Weissman J, Buratowski S (2011) H3K4 Trimethylation by Set1 promotes efficient termination by the Nrd1-Nab3-Sen1 pathway. Mol Cell Biol 31(17):3569–3583. https://doi.org/10.1128/MCB.05590-11
Article Google Scholar
Tyagi S, Chabes AL, Wysocka J, Herr W (2007) E2F activation of S phase promoters via association with HCF-1 and the MLL family of histone H3K4 methyltransferases. Mol Cell 27(1):107–119. https://doi.org/10.1016/j.molcel.2007.05.030
Article Google Scholar
Ullius A, Luscher-Firzlaff J, Costa IG, Walsemann G, Forst AH, Gusmao EG, Kapelle K, Kleine H, Kremmer E, Vervoorts J, Luscher B (2014) The interaction of MYC with the trithorax protein ASH2L promotes gene transcription by regulating H3K27 modification. Nucleic Acids Res 42(11):6901–6920. https://doi.org/10.1093/nar/gku312
Article Google Scholar
Vermeulen M, Mulder KW, Denissov S, Pijnappel WWMP, van Schaik FMA, Varier RA, Baltissen MPA, Stunnenberg HG, Mann M, Timmers HTM (2007) Selective anchoring of TFIID to nucleosomes by trimethylation of histone H3 lysine 4. Cell 131(1):58–69. https://doi.org/10.1016/j.cell.2007.08.016
Article Google Scholar
Vilhais-Neto GC, Fournier M, Plassat J-L, Sardiu ME, Saraf A, Garnier J-M, Maruhashi M, Florens L, Washburn MP, Pourquié O (2017) The WHHERE coactivator complex is required for retinoic acid-dependent regulation of embryonic symmetry. Nat Commun 8(1):728. https://doi.org/10.1038/s41467-017-00593-6
Article Google Scholar
Voigt P, LeRoy G, Drury WJ, Zee BM, Son J, Beck DB, Young NL, Garcia BA, Reinberg D (2012) Asymmetrically modified nucleosomes. Cell 151(1):181–193. https://doi.org/10.1016/j.cell.2012.09.002
Article Google Scholar
Voigt P, Tee W-W, Reinberg D (2013) A double take on bivalent promoters. Genes Dev 27(12):1318–1338. https://doi.org/10.1101/gad.219626.113
Article Google Scholar
Voss AK, Collin C, Dixon MP, Thomas T (2009) Moz and retinoic acid coordinately regulate H3K9 acetylation, Hox gene expression, and segment identity. Dev Cell 17(5):674–686. https://doi.org/10.1016/j.devcel.2009.10.006
Article Google Scholar
Wan M, Liang J, Xiong Y, Shi F, Zhang Y, Lu W, He Q, Yang D, Chen R, Liu D, Barton M, Songyang Z (2013) The Trithorax group protein Ash2l is essential for pluripotency and maintaining open chromatin in embryonic stem cells. J Biol Chem 288(7):5039–5048. https://doi.org/10.1074/jbc.M112.424515
Article Google Scholar
Wang J, Scully K, Zhu X, Cai L, Zhang J, Prefontaine GG, Krones A, Ohgi KA, Zhu P, Garcia-Bassets I, Liu F, Taylor H, Lozach J, Jayes FL, Korach KS, Glass CK, Fu X-D, Rosenfeld MG (2007) Opposing LSD1 complexes function in developmental gene activation and repression programmes. Nature 446(7138):882–887. https://doi.org/10.1038/nature05671
Article Google Scholar
Wang Z, Zang C, Rosenfeld JA, Schones DE, Barski A, Cuddapah S, Cui K, Roh T-Y, Peng W, Zhang MQ, Zhao K (2008) Combinatorial patterns of histone acetylations and methylations in the human genome. Nat Genet 40(7):897–903. https://doi.org/10.1038/ng.154
Article Google Scholar
Wang J, Hevi S, Kurash JK, Lei H, Gay F, Bajko J, Su H, Sun W, Chang H, Xu G, Gaudet F, Li E, Chen T (2009a) The lysine demethylase LSD1 (KDM1) is required for maintenance of global DNA methylation. Nat Genet 41(1):125–129. https://doi.org/10.1038/ng.268
Article Google Scholar
Wang P, Lin C, Smith ER, Guo H, Sanderson BW, Wu M, Gogol M, Alexander T, Seidel C, Wiedemann LM, Ge K, Krumlauf R, Shilatifard A (2009b) Global analysis of H3K4 methylation defines MLL family member targets and points to a role for MLL1-mediated H3K4 methylation in the regulation of transcriptional initiation by RNA polymerase II. Mol Cell Biol 29(22):6074–6085. https://doi.org/10.1128/MCB.00924-09
Article Google Scholar
Wang Z, Song J, Milne TA, Wang GG, Li H, Allis CD, Patel DJ (2010) Pro isomerization in MLL1 PHD3-bromo cassette connects H3K4me readout to CyP33 and HDAC-mediated repression. Cell 141(7):1183–1194. https://doi.org/10.1016/j.cell.2010.05.016
Article Google Scholar
Wang C, Lee J-E, Lai B, Macfarlan TS, Xu S, Zhuang L, Liu C, Peng W, Ge K (2016) Enhancer priming by H3K4 methyltransferase MLL4 controls cell fate transition. Proc Natl Acad Sci 113(42):11871–11876. https://doi.org/10.1073/pnas.1606857113
Article Google Scholar
Wang H, Fan Z, Shliaha PV, Miele M, Hendrickson RC, Jiang X, Helin K (2023) H3K4me3 regulates RNA polymerase II promoter-proximal pause-release. Nature 615(7951):339–348. https://doi.org/10.1038/s41586-023-05780-8
Article Google Scholar
White MD, Plachta N (2020) Specification of the first mammalian cell lineages in vivo and in vitro. Cold Spring Harb Perspect Biol 12(4):a035634. https://doi.org/10.1101/cshperspect.a035634
Article Google Scholar
Whyte WA, Bilodeau S, Orlando DA, Hoke HA, Frampton GM, Foster CT, Cowley SM, Young RA (2012) Enhancer decommissioning by LSD1 during embryonic stem cell differentiation. Nature 482(7384):221–225. https://doi.org/10.1038/nature10805
Article Google Scholar
Wu M, Wang PF, Lee JS, Martin-Brown S, Florens L, Washburn M, Shilatifard A (2008) Molecular regulation of H3K4 Trimethylation by Wdr82, a component of human Set1/COMPASS. Mol Cell Biol 28(24):7337–7344. https://doi.org/10.1128/MCB.00976-08
Article Google Scholar
Wu X, Wu X, Xie W (2023) Activation, decommissioning, and dememorization: enhancers in a life cycle. Trends Biochem Sci 48(8):673–688. https://doi.org/10.1016/j.tibs.2023.04.005
Article Google Scholar
Wysocka J, Myers MP, Laherty CD, Eisenman RN, Herr W (2003) Human Sin3 deacetylase and trithorax-related Set1/Ash2 histone H3-K4 methyltransferase are tethered together selectively by the cell-proliferation factor HCF-1. Genes Dev 17(7):896–911. https://doi.org/10.1101/gad.252103
Article Google Scholar
Wysocka J, Swigut T, Milne TA, Dou Y, Zhang X, Burlingame AL, Roeder RG, Brivanlou AH, Allis CD (2005) WDR5 associates with histone H3 methylated at K4 and is essential for H3 K4 methylation and vertebrate development. Cell 121(6):859–872. https://doi.org/10.1016/j.cell.2005.03.036
Article Google Scholar
Xie L, Pelz C, Wang W, Bashar A, Varlamova O, Shadle S, Impey S (2011) KDM5B regulates embryonic stem cell self-renewal and represses cryptic intragenic transcription. EMBO J 30(8):1473–1484. https://doi.org/10.1038/emboj.2011.91
Article Google Scholar
Xie G, Lee J-E, Senft AD, Park Y-K, Jang Y, Chakraborty S, Thompson JJ, McKernan K, Liu C, Macfarlan TS, Rocha PP, Peng W, Ge K (2023) MLL3/MLL4 methyltransferase activities control early embryonic development and embryonic stem cell differentiation in a lineage-selective manner. Nat Genet 55(4):693–705. https://doi.org/10.1038/s41588-023-01356-4
Article Google Scholar
Xu C, Liu K, Lei M, Yang A, Li Y, Hughes TR, Min J (2018) DNA sequence recognition of human CXXC domains and their structural determinants. Structure 26(1):85–95.e3. https://doi.org/10.1016/j.str.2017.11.022
Article Google Scholar
Yagi H, Deguchi K, Aono A, Tani Y, Kishimoto T, Komori T (1998) Growth disturbance in fetal liver hematopoiesis of Mll-mutant mice. Blood 92(1):108–117
Google Scholar
Yang Z, Augustin J, Hu J, Jiang H (2015) Physical interactions and functional coordination between the Core subunits of Set1/Mll complexes and the reprogramming factors. PLoS One 10(12):e0145336. https://doi.org/10.1371/journal.pone.0145336
Article Google Scholar
Yang Z, Shah K, Khodadadi-Jamayran A, Jiang H (2016) Dpy30 is critical for maintaining the identity and function of adult hematopoietic stem cells. J Exp Med 213(11):2349–2364. https://doi.org/10.1084/jem.20160185
Article Google Scholar
Yang X, Hu B, Hou Y, Qiao Y, Wang R, Chen Y, Qian Y, Feng S, Chen J, Liu C, Peng G, Tang F, Jing N (2018) Silencing of developmental genes by H3K27me3 and DNA methylation reflects the discrepant plasticity of embryonic and extraembryonic lineages. Cell Res 28(5):593–596. https://doi.org/10.1038/s41422-018-0010-1
Article Google Scholar
Ying Q-L, Stavridis M, Griffiths D, Li M, Smith A (2003) Conversion of embryonic stem cells into neuroectodermal precursors in adherent monoculture. Nat Biotechnol 21(2):183–186. https://doi.org/10.1038/nbt780
Article Google Scholar
Yu BD, Hess JL, Horning SE, Brown GAJ, Korsmeyer SJ (1995) Altered Hox expression and segmental identity in Mll-mutant mice. Nature 378(6556):505–508. https://doi.org/10.1038/378505a0
Article Google Scholar
Yu BD, Hanson RD, Hess JL, Horning SE, Korsmeyer SJ (1998) MLL, a mammalian trithorax- group gene, functions as a transcriptional maintenance factor in morphogenesis. Proc Natl Acad Sci 95(18):10632–10636. https://doi.org/10.1073/pnas.95.18.10632
Article Google Scholar
Zeng C, Chen J, Cooke EW, Subuddhi A, Roodman ET, Chen FX, Cao K (2023) Demethylase-independent roles of LSD1 in regulating enhancers and cell fate transition. Nat Commun 14(1):4944. https://doi.org/10.1038/s41467-023-40606-1
Article Google Scholar
Zhang L, Mitch WE (2020) NO66 suppresses muscle protein synthesis by a demethylase mechanism. FASEB J 34(S1):1–1. https://doi.org/10.1096/fasebj.2020.34.s1.00706
Article Google Scholar
Zhang Y, Jurkowska R, Soeroes S, Rajavelu A, Dhayalan A, Bock I, Rathert P, Brandt O, Reinhardt R, Fischle W, Jeltsch A (2010) Chromatin methylation activity of Dnmt3a and Dnmt3a/3L is guided by interaction of the ADD domain with the histone H3 tail. Nucleic Acids Res 38(13):4246–4253. https://doi.org/10.1093/nar/gkq147
Article Google Scholar
Zhang J, Dominguez-Sola D, Hussein S, Lee J-E, Holmes AB, Bansal M, Vlasevska S, Mo T, Tang H, Basso K, Ge K, Dalla-Favera R, Pasqualucci L (2015) Disruption of KMT2D perturbs germinal center B cell development and promotes lymphomagenesis. Nat Med 21(10):1190–1198. https://doi.org/10.1038/nm.3940
Article Google Scholar
Zhang B, Zheng H, Huang B, Li W, Xiang Y, Peng X, Ming J, Wu X, Zhang Y, Xu Q, Liu W, Kou X, Zhao Y, He W, Li C, Chen B, Li Y, Wang Q, Ma J et al (2016) Allelic reprogramming of the histone modification H3K4me3 in early mammalian development. Nature 537(7621):553–557. https://doi.org/10.1038/nature19361
Article Google Scholar
Zhao T, Hong Y, Ming G, Song H (2020) Loss of chromatin modulator Dpy30 compromises proliferation and differentiation of postnatal neural stem cells. J Mol Cell Biol 12(1):2–3. https://doi.org/10.1093/jmcb/mjz041
Article Google Scholar
Zhao L, Huang N, Mencius J, Li Y, Xu Y, Zheng Y, He W, Li N, Zheng J, Zhuang M, Quan S, Chen Y (2022) DPY30 acts as an ASH2L-specific stabilizer to stimulate the enzyme activity of MLL family methyltransferases on different substrates. iScience 25(9):104948. https://doi.org/10.1016/j.isci.2022.104948
Article Google Scholar
Zhou T, Cheng X, He Y, Xie Y, Xu F, Xu Y, Huang W (2022) Function and mechanism of histone β-hydroxybutyrylation in health and disease. Front Immunol 13. https://doi.org/10.3389/fimmu.2022.981285

Download references

Author information

Authors and Affiliations

Department of Biological Sciences, Middle East Technical University, Ankara, Turkey
Nihal Terzi Cizmecioglu

Authors

Nihal Terzi Cizmecioglu
View author publications
You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Nihal Terzi Cizmecioglu .

Rights and permissions

Reprints and permissions

Copyright information

About this chapter

Cite this chapter

Terzi Cizmecioglu, N. (2024). Roles and Regulation of H3K4 Methylation During Mammalian Early Embryogenesis and Embryonic Stem Cell Differentiation. In: Advances in Experimental Medicine and Biology(). Springer, Cham. https://doi.org/10.1007/5584_2023_794

Download citation

DOI: https://doi.org/10.1007/5584_2023_794
Published: 18 January 2024
Publisher Name: Springer, Cham

Publish with us

Policies and ethics