Confining euchromatin/heterochromatin territory: jumonji crosses the line
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Heterochromatin is typically highly condensed, gene-poor, and transcriptionally silent, whereas euchromatin is less condensed, gene-rich, and more accessible to transcription. Besides acting as a graveyard for selfish mobile DNA repeats, heterochromatin contributes to important biological functions, such as chromosome segregation during cell division. Multiple features of heterochromatin—including the presence or absence of specific histone modifications, DNA methylation, and small RNAs—have been implicated in distinguishing heterochromatin from euchromatin in various organisms. Cells malfunction if the genome fails to restrict repressive chromatin marks within heterochromatin domains. How euchromatin and heterochromatin territories are confined remains poorly understood. Recent studies from the fission yeast Schizosaccharomyces pombe, the flowering plant Arabidopsis thaliana, and the filamentous fungus Neurospora crassa have revealed a new role for Jumonji C (JmjC) domain-containing proteins in protecting euchromatin from heterochromatin marks.
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H3K9me3 is primarily located within silent, heterochromatic regions.
“H3K9me3 is primarily located within silent, heterochromatic regions (20,37,38)”
From DNA double-strand breaks promote methylation of histone H3 on lysine 9 and transient formation of repressive chromatin (2014) · cites this paper as [37]
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A Novel jmjC Domain Protein Modulates Heterochromatization in Fission Yeast
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Abnormal Chromosome Behavior in Neurospora Mutants Defective in DNA Methylation
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USF1 Recruits Histone Modification Complexes and Is Critical for Maintenance of a Chromatin Barrier
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DNA Methylation Is Independent of RNA Interference in Neurospora
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S. pombe LSD1 Homologs Regulate Heterochromatin Propagation and Euchromatic Gene Transcription
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Dense Nonsymmetrical DNA Methylation Resulting from Repeat-Induced Point Mutation in Neurospora
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DNA Methylation Associated with Repeat-Induced Point Mutation in Neurospora crassa
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Homology-Dependent Gene Silencing Mechanisms in Fungi
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Expression-State Boundaries in the Mating-Type Region of Fission Yeast
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RNAi, heterochromatin and the cell cycle
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Synthesis of Signals for De Novo DNA Methylation in Neurospora crassa
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Mnd2 and Swm1 Are Core Subunits of the Saccharomyces cerevisiae Anaphase-promoting Complex
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Epigenetic Control of a Transposon-Inactivated Gene in Neurospora is Dependent on DNA Methylation
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Replication-competent noninduced proviruses in the latent reservoir increase barrier to HIV-1 cure
Ho, Y.-C., Shan, L., Hosmane, N. N., Wang, J., Laskey, S. B., Rosenbloom, D. I. S., Lai, J., Blankson, J. N., Siliciano, J. D., & Siliciano, R. F. (2013) · Cell · doi:10.1016/j.cell.2013.09.020 · Cited by 1,405 · see citing works
Writing, erasing and reading histone lysine methylations
Hyun, K., Jeon, J., Park, K., & Kim, J. (2017) · Experimental & Molecular Medicine · doi:10.1038/emm.2017.11 · Cited by 1,250 · see citing works
ROS, Cell Senescence, and Novel Molecular Mechanisms in Aging and Age‐Related Diseases
Davalli, P., Mitic, T., Caporali, A., Lauriola, A., & D’Arca, D. (2016) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2016/3565127 · Cited by 1,059 · see citing works
“Indeed, the epigenetic modulation provides the essential and flexible interface between the organisms and the environment, which results in being essential for all the cell functions [122, 123, 129], throughout the lifespan [135–137].”
BackgroundH3K9 methyltransferase G9a and the related molecule GLPPreprint
Shinkai, Y., & Tachibana, M. (2011) · Genes & Development · doi:10.1101/gad.2027411 · Cited by 557 · see citing works
“In Arabidopsis, DNA methylation and H3K9 methylation are functionally interdependent (Jackson et al. 2002; Malagnac et al. 2002; Johnson et al. 2007; Tamaru 2010).”
BackgroundAyrapetov, M. K., Gursoy-Yuzugullu, O., Xu, C., Xu, Y., & Price, B. D. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1403565111 · Cited by 391 · see citing works
“However, because H3K9me3 is primarily located within silent, heterochromatic regions (20, 37, 38), this requirement suggests that Tip60 activity during DNA repair may be restricted to chromatin domains with a high density of H3K9me2/3.”
BackgroundEpigenetics and cardiovascular disease
Ordovás, J. M., & Smith, C. E. (2010) · Nature Reviews Cardiology · doi:10.1038/nrcardio.2010.104 · Cited by 402 · see citing works
Targeting the Latent Reservoir for HIV-1
Sengupta, S., & Siliciano, R. F. (2018) · Immunity · doi:10.1016/j.immuni.2018.04.030 · Cited by 333 · see citing works
“Resting CD4+ T cells contain high levels of condensed heterochromatin that limit gene expression (Festenstein et al., 2003; Tamaru 2010).”
The role of chromatin modifications in somatic embryogenesis in plants
De‐la‐Peña, C., Nic-Can, G. I., Galaz-Ávalos, R. M., Avilez-Montalvo, R. N., & Loyola-Vargas, V. M. (2015) · Frontiers in Plant Science · doi:10.3389/fpls.2015.00635 · Cited by 117 · see citing works
“Chromatin organization allows the expression or repression of genes depending on the degree of its compaction in a specific locus (Schones and Zhao, 2008; Tamaru, 2010).”
BackgroundSomatic Embryogenesis Induction in Woody Species: The Future After OMICs Data Assessment
Pais, M. S. (2019) · Frontiers in Plant Science · doi:10.3389/fpls.2019.00240 · Cited by 75 · see citing works
“Chromatin organization induces the expression or repression of genes which depends on the degree of its compaction in a specific locus (Tamaru, 2010).”
BackgroundLee, T., Gurazada, S. G. R., Zhai, J., Li, S., Simon, S. A., Matzke, M. A., Chen, X., & Meyers, B. C. (2012) · Epigenetics · doi:10.4161/epi.20290 · Cited by 73 · see citing works
Evolutionary Epigenomics of Retrotransposon-Mediated Methylation Spreading in Rice
Choi, J. Y., & Purugganan, M. D. (2017) · Molecular Biology and Evolution · doi:10.1093/molbev/msx284 · Cited by 67 · see citing works
“Possible genetic mechanisms from the host and TE that limits the spreading can be seen from the involvement of genes containing the Jumonji C protein domain in regulating the spread of heterochromatic marks in euchromatin boundaries (Tamaru 2010), and TE sequences containing insulator domain and function (Bell et al.”
BackgroundDillon, A. J., Varanasi, V. K., Danilova, T. V., Koo, D., Nakka, S., Peterson, D. E., Tranel, P. J., Friebe, B. R., Gill, B. S., & Jugulam, M. (2016) · PLANT PHYSIOLOGY · doi:10.1104/pp.16.01427 · Cited by 62 · see citing works
Bodetto, S. P., Carouge, D., Fonteneau, M., Dietrich, J., Zwiller, J., & Anglard, P. (2013) · Neuropharmacology · doi:10.1016/j.neuropharm.2013.05.005 · Cited by 59 · see citing works
“(Tamaru, 2010).”
Baute, J., Herman, D., Coppens, F., Block, J. D., Slabbinck, B., Dell’Acqua, M., Pè, M. E., Maere, S., Nelissen, H., & Inzé, D. (2015) · Genome biology · doi:10.1186/s13059-015-0735-9 · Cited by 55 · see citing works
“Some genes are homologs of the Alfin-like family, SET-domain family and DNA methyltransferases, all involved in regulation of chromatin structure in Arabidopsis [62–67], which is essential for normal cell functioning, development and leaf growth [50].”
BackgroundNanoscale Squeezing in Elastomeric Nanochannels for Single Chromatin Linearization
Matsuoka, T., Kim, B. C., Huang, J., Douville, N. J., Thouless, M. D., & Takayama, S. (2012) · Nano Letters · doi:10.1021/nl304063f · Cited by 53 · see citing works
Uwizeye, C., Brisbin, M. M., Gallet, B., Chevalier, F., LeKieffre, C., Schieber, N. L., Falconet, D., Wangpraseurt, D., Schertel, L., Stryhanyuk, H., et al. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2025252118 · Cited by 52 · see citing works
Autoimmune disease: a view of epigenetics and therapeutic targeting
Mu, S., Wang, W., Liu, Q., Ke, N., Li, H., Sun, F., Zhang, J., & Zhu, Z. (2024) · Frontiers in Immunology · doi:10.3389/fimmu.2024.1482728 · Cited by 57 · see citing works
Epigenetic Alterations in Pancreatic Cancer Metastasis
Wang, S. S., Xu, J., Ji, K. Y., & Hwang, C. (2021) · Biomolecules · doi:10.3390/biom11081082 · Cited by 49 · see citing works
“In the heterochromatin state, nucleosomes are highly condensed, preventing TF binding and subsequent RNA polymerase recruitment [27].”
BackgroundEarly-life stress interactions with the epigenome
Lewis, C. R., & Olive, M. F. (2014) · Behavioural Pharmacology · doi:10.1097/fbp.0000000000000057 · Cited by 51 · see citing works
“Chromatin can exist in the form of heterochromatin or euchromatin (Tamaru, 2010).”
BackgroundRezazadeh, S., Yang, D. X., Biashad, S. A., Firsanov, D., Takasugi, M., Gilbert, M. B., Tombline, G., Bhanu, N. V., Garcia, B. A., Seluanov, A., et al. (2020) · Aging · doi:10.18632/aging.103567 · Cited by 42 · see citing works
Programmed Genome Rearrangements in Tetrahymena
Yao, M.-C., Chao, J., & Cheng, C.-Y. (2014) · Microbiology Spectrum · doi:10.1128/microbiolspec.mdna3-0012-2014 · Cited by 43 · see citing works
“We suggest that flanking regulatory sequences set boundaries for heterochromatin, similar to chromatin boundary elements in other eukaryotes (92, 93).”
BackgroundSinton, M. C., Hay, D. C., & Drake, A. J. (2019) · Clinical Epigenetics · doi:10.1186/s13148-019-0702-5 · Cited by 44 · see citing works
Hsiao, F., Frouard, J., Gramatica, A., Xie, G., Telwatte, S., Lee, G. Q., Roychoudhury, P., Schwarzer, R., Luo, X., Yukl, S. A., et al. (2020) · PLoS Pathogens · doi:10.1371/journal.ppat.1008450 · Cited by 43 · see citing works
“Of the 1,207 unique proviral integration sites that were identified, the vast majority were in genic regions (S7A Fig), which tend to reside within open regions of the genome [39, 40].”
The Emerging Roles of ATP-Dependent Chromatin Remodeling Enzymes in Nucleotide Excision Repair
Czaja, W., Mao, P., & Smerdon, M. J. (2012) · International Journal of Molecular Sciences · doi:10.3390/ijms130911954 · Cited by 40 · see citing works
“Euchromatin is decondensed, more accessible and generally associated with active transcription [7].”
BackgroundCai, W., Chen, Y., Zhang, L., Fang, X., & Wang, W. (2022) · Biotechnology for Biofuels and Bioproducts · doi:10.1186/s13068-022-02132-y · Cited by 40 · see citing works
“crassa, DNA Methylation Modulators (DMMs) prevent aberrant spreading of DNA methylation from normally methylated A:T-rich DNA to nearby genes [15, 16].”
BackgroundInfluentialStephens, V. R., Rumph, J. T., Ameli, S., Bruner‐Tran, K. L., & Osteen, K. G. (2022) · Frontiers in Physiology · doi:10.3389/fphys.2021.807685 · Cited by 40 · see citing works
“Historically, DNA was thought to be solely responsible for transferring phenotypic information from parent to offspring.”
BackgroundInfluentialSchuler, N., & Rübe, C. E. (2013) · PLoS ONE · doi:10.1371/journal.pone.0063932 · Cited by 37 · see citing works
“well as methylation of histone 3 at lysine 4 (H3K4me) [9].”
BackgroundStrategies for Natural Product Discovery by Unlocking Cryptic Biosynthetic Gene Clusters in Fungi
Hur, J. Y., Jeong, E., Kim, Y. C., & Lee, S. R. (2023) · Separations · doi:10.3390/separations10060333 · Cited by 36 · see citing works
Targeting epigenetics: A novel promise for Alzheimer’s disease treatment
Jeremic, D., Jiménez‐Díaz, L., & Navarro‐López, J. D. (2023) · Ageing Research Reviews · doi:10.1016/j.arr.2023.102003 · Cited by 36 · see citing works
Epigenetics: spotlight on type 2 diabetes and obesity
Desiderio, A., Spinelli, R., Ciccarelli, M., Nigro, C., Miele, C., Bèguinot, F., & Raciti, G. A. (2016) · Journal of Endocrinological Investigation · doi:10.1007/s40618-016-0473-1 · Cited by 33 · see citing works
“On the other hand, euchromatin exhibits lower levels of DNA methylation, and is typically enriched in acetylation of lysine residues at histones H3 and H4 and in mono- and tri-methylation of H3-Lys4 (Table 1) [27, 28].”
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“…depending on PTMs: transcriptionally active genes are associated with a lesscondensed, nucleosome-depleted and accessible chromatin known as euchromatin while transcriptionally silent genes are linked to highly-condensed and inaccessible chromatin regions called heterochromatin (Tamaru, 2010).”
BackgroundGenetics and epigenetics purpose in nonalcoholic fatty liver disease
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“active transcription and contain housekeeping genes, otherwise crucial for basic cell functions [15].”
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“Another antisilencing factor is the JMJ-domain protein Epe1 from Schizosaccharomyces pombe, which is required for heterochromatin boundary formation (Trewick et al., 2007; Tamaru, 2010).”
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“Several JmjC domain-containing proteins, such as DMM-1 in Neurospora crassa, Epe1 in Schizosaccharomyces pombe, and IBM1 in Arabidopsis thaliana, have been shown to regulate the boundary of heterochromatin (29, 48, 66, 71).”
BackgroundFunctional crosstalk between chromatin and hypoxia signalling
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“…be tightly packed as heterochromatin containing an array of condensed nucleosomes that prevent access of factors involved in process such as transcription and translation to genomic DNA, or loosely wound as euchromatin, which provides active sequences to further translation and replication [245].”
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“While transcription of the provirus in resting CD4 T cells and monocytes can be restricted by epigenetic modifications and chromatin structure [17,51], limiting levels of essential host factors for HIV-1 transcription, such as P-TEFb [52], also greatly contribute to the low permissivity of resting CD4 T cells and mono…”
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Micro- and nanofluidic technologies for epigenetic profiling
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“Heterochromatin is highly condensed, gene poor, rich in transposons or other parasitic genomic elements and generally transcriptionally silent, whereas euchromatin is less condensed, gene-rich, and more easily transcribed (Huisinga et al. 2006; Kind and van Steensel 2010; Tamaru 2010).”
BackgroundImplication of the Mediterranean diet on the human epigenome
Kenanoğlu, S., Gökçe, N., Akalın, H., Ergören, M. Ç., Beccari, T., Bertelli, M., & Dündar, M. (2022) · Journal of preventive medicine and hygiene · doi:10.15167/2421-4248/jpmh2022.63.2s3.2746 · Cited by 17 · see citing works
“Euchromatin is a highly loosely condensed form that is transcriptionally active and provides the environment for DNA-regulatory processes, while heterochromatin is often defined as its tightly condensed transcriptionally inactive form, devoid of DNA-regulatory activity [10].”
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“Chromatin is composed of DNA and histones, of which two main types can be distinguished: the gene-poor, transcriptionally less active heterochromatin and the gene-rich euchromatin, which is accessible for transcription [8].”
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“Euchromatin is typically gene rich, less condensed, and transcriptionally accessible, while heterochromatin is gene poor, highly condensed, and transcriptionally repressed (Tamaru 2010).”
Identification of novel genes associated with HIV-1 latency by analysis of histone modifications
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“Additionally, gene expression of HIV-1 latency can be dynamically regulated through epigenetic changes in chromatin structure surrounding and within integrated HIV-1 provirus [7, 8].”
Enhancer prediction with histone modification marks using a hybrid neural network model
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Chromatin: the old and young of it
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“Heterochromatin is typically associated with genes that are silenced, as the tightly wrapped DNA is dif fi cult to access for transcription, while euchromatin is associated with active gene expression (Tamaru, 2010).”
BackgroundControlling the balance between chromosome break repair pathways
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Negative regulation of floral transition in Arabidopsis by HOS15-PWR-HDA9 complex
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“On the contrary, chromatin becomes compacted with histone deacetylation, hindering the interaction of transcription factors with the promoters and repressing the expression of genes (Tamaru, 2010; Park et al., 2018a).”
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The histone code of the fungal genus Aspergillus uncovered by evolutionary and proteomic analyses
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“Histone demethylase activity has not been detected for DMM-1 [140] or Epe1 [141] in N. crassa , while KDM2 can demethylate H3K36me1/2 in mouse [142] and JMJD6/PKDM11 is an arginine demethylase in Arabidopsis [143].”
Interplay between epigenome and 3D chromatin structure
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“In contrast, heterochromatin regions, marked by repressive modifications, such as H3K9 and H3K27 methylation, are predominantly compact, and serve as barriers to transcriptional machinery (13).”
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“…JmjC-domainproteins and unmethylated DNA, especially intheCHG context,andmightsuggest aroleinprevent-ing heterochromatin marks from spreading into euchromatin like in other species, such as JmjC-domain proteins DMM-1 in Neurospora crassa and Epe1 in Schizosaccharomyces pombe (Tamaru 2010).”
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“verts euchromatin into heterochromatin [61,62].”
Chromatin Modifications in Plants
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“In contrast, genes located in euchromatin regions generally exhibit higher expression levels than those located in heterochromatin regions [30,31].”
Review of the geometrical developments in GEANT4-DNA: From a biological perspective
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“In this context it is interesting to note that JmjC proteins from several organisms function in preventing spreading of silencing from heterochromatic regions [60], including the Schizosaccharomyces pombe protein Epe1 which has a catalytic site mutation identical to the one in Gis1 [3,61].”
BackgroundA review of epigenetics in human consciousness
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“Two forms of chromatin exist: (1) heterochromatin—a tightly compacted form which is genetically inactive and (2) euchromatin—a more loosely compacted form which is genetically active because it is accessible to DNA transcription factors (Tamaru, 2010).”
BackgroundRole of DNA methylation in genome stability
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Unraveling the complexity of the histone code: implications for gene regulation and disease
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“Conversely, euchromatin regions contain DNA that is less constricted and more amenable to being accessible to transcription factors for gene expression [2, 5, 8].”
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“However, recent studies suggest otherwise, i.e., heterochromatin contributes to important roles in cellular functions, such as transcriptions, chromosome segregation and long-range chromatin interactions (see reviews by Grewal and Jia 80 ; Tamaru 81 ).”
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“In both classes of heterochromatin, histones are hypo-acetylated, resulting in the inaccessibility of DNA to transcription machinery [4].”
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A Primer on Epigenetic Changes: The More We Know, the More We Find in Fetuses and Infants
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“Much experimental progress has been made in understanding the regulation of sharp boundaries between euchromatin and hete-rochromatin (Li and Zhou, 2013; Tamaru, 2010; Wang et al., 2012; Wang et al., 2014).”
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“tional part of the chromatin; it replicates early at the beginning of S faze, being R positive bands from bands marked chromosomes [51].”
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A Model of Transcriptional Activation of DNA by Loosening of Chromatin Structure
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“These modifications give rise to chromatin with different states of compaction, namely euchromatin, facultative heterochromatin, or constitutive heterochromatin, all providing different levels of DNA accessibility [52].”
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“• Heterochromatin vs. Heterochromatin : Heterochromatin in all chromosomes consists of highly condensed, repetitive, and transcriptionally inactive regions that show similarities across different chromosomes [60,72].”
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“In contrast, heterochromatin represents a more condensed chromatin state that limits DNA accessibility and is generally linked to transcriptional repression (TaMaru 2010).”
Small molecules effective for disruption of HIV-1 latency
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“Since nuclear chromatin is a obligatory substrate for the realization of metabolic functions of cells, its structural-functional transformations, which predetermine the modification of DNA and histone proteins, are very important [19, 20].”
Background
- Authors
- Tamaru, H.
- Affiliations
- Gregor Mendel Institute of Molecular Plant Biology (AT)
- Corresponding author
- Tamaru, Hisashi
- Venue
- Genes & Development
- Publisher
- Cold Spring Harbor Laboratory
- Published
- 2010-07-15
- Volume
- 24
- Issue
- 14
- Pages
- 1465-1478
- ISSN
- 0890-9369 (ISSN-L)
- 1549-5477
- PMC
- PMC2904936
- OpenAlex
- W2163949420
- Cited by
- 118
- References
- 160
- Citations by year
- 2026: 5 · 2025: 3 · 2024: 12 · 2023: 17 · 2022: 11 · 2021: 7 · 2020: 4 · 2019: 8 · 2018: 3 · 2017: 5 · 2016: 6 · 2015: 7 · 2014: 7 · 2013: 9 · 2012: 9
- Type
- posted content
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Genes & Development (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Austrian Science Fund
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Chromosomal and Genetic Variations
- Keywords
- heterochromatin, euchromatin, histone modifications, DNA methylation, small RNA, heterochromatinization, Schizosaccharomyces pombe, Arabidopsis thaliana, Neurospora crassa
- MeSH terms
- Animals, Heterochromatin, Humans, Neurospora crassa, Nuclear Proteins, Schizosaccharomyces, Arabidopsis, Protein Structure, Tertiary, Euchromatin
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