Incorporation of histone H3.1 suppresses the lineage potential of skeletal muscle

Akihito Harada; Kazumitsu Maehara; Yuko Sato; Daijiro Konno; Taro Tachibana; Hiroshi Kimura; Yasuyuki Ohkawa

doi:10.1093/nar/gku1346

Incorporation of histone H3.1 suppresses the lineage potential of skeletal muscle

Akihito Harada, Kazumitsu Maehara, Yuko Sato, Daijiro Konno, Taro Tachibana, Hiroshi Kimura, Yasuyuki Ohkawa

Medical Research Center Initiative for High Depth Omics

Research output: Contribution to journal › Article › peer-review

32 Citations (Scopus)

Abstract

Lineage potential is triggered by lineage-specific transcription factors in association with changes in the chromatin structure. Histone H3.3 variant is thought to play an important role in the regulation of lineage-specific genes. To elucidate the function of H3.3 in myogenic differentiation, we forced the expression of GFP-H3.1 to alter the balance between H3.1 and H3.3 in mouse C2C12 cells that could be differentiated into myotubes. GFP-H3.1 replaced H3.3 in the regulatory regions of skeletal muscle (SKM) genes and induced a decrease of H3K4 trimethylation (H3K4me3) and increase of H3K27 trimethylation (H3K27me3). Similar results were obtained by H3.3 knockdown. In contrast, MyoD-dependent H3.3 incorporation into SKM genes in fibroblasts induced an increase of H3K4me3 and H3K27me3. In mouse embryos, a bivalent modification of H3K4me3 and H3K27me3 was formed on H3.3-incorporated SKM genes before embryonic skeletal muscle differentiation. These results suggest that lineage potential is established through a selective incorporation of specific H3 variants that governs the balance of histone modifications.

Original language	English
Pages (from-to)	775-786
Number of pages	12
Journal	Nucleic acids research
Volume	43
Issue number	2
DOIs	https://doi.org/10.1093/nar/gku1346
Publication status	Published - Jan 30 2015

All Science Journal Classification (ASJC) codes

Genetics

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10.1093/nar/gku1346

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title = "Incorporation of histone H3.1 suppresses the lineage potential of skeletal muscle",

abstract = "Lineage potential is triggered by lineage-specific transcription factors in association with changes in the chromatin structure. Histone H3.3 variant is thought to play an important role in the regulation of lineage-specific genes. To elucidate the function of H3.3 in myogenic differentiation, we forced the expression of GFP-H3.1 to alter the balance between H3.1 and H3.3 in mouse C2C12 cells that could be differentiated into myotubes. GFP-H3.1 replaced H3.3 in the regulatory regions of skeletal muscle (SKM) genes and induced a decrease of H3K4 trimethylation (H3K4me3) and increase of H3K27 trimethylation (H3K27me3). Similar results were obtained by H3.3 knockdown. In contrast, MyoD-dependent H3.3 incorporation into SKM genes in fibroblasts induced an increase of H3K4me3 and H3K27me3. In mouse embryos, a bivalent modification of H3K4me3 and H3K27me3 was formed on H3.3-incorporated SKM genes before embryonic skeletal muscle differentiation. These results suggest that lineage potential is established through a selective incorporation of specific H3 variants that governs the balance of histone modifications.",

author = "Akihito Harada and Kazumitsu Maehara and Yuko Sato and Daijiro Konno and Taro Tachibana and Hiroshi Kimura and Yasuyuki Ohkawa",

note = "Funding Information: JSPS KAKENHI [23310134, 25116010, 25118518, 25132709 and 26290064 to Y.O.]; Grant-in-Aid for JSPS Fellows [25·4024 to A.H.] (http://www.jsps.go.jp/ j-grantsinaid/). Funding for open access charge: JSPS KAKENHI [23310134, 25116010, 25118518, 25132709 and 26290064 to Y.O.]; Grant-in-Aid for JSPS Fellows [25·4024 to A.H.] (http://www.jsps.go.jp/j-grantsinaid/). Conflict of interest statement. None declared. Publisher Copyright: {\textcopyright} 2015 The Author(s).",

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doi = "10.1093/nar/gku1346",

language = "English",

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T1 - Incorporation of histone H3.1 suppresses the lineage potential of skeletal muscle

AU - Harada, Akihito

AU - Maehara, Kazumitsu

AU - Sato, Yuko

AU - Konno, Daijiro

AU - Tachibana, Taro

AU - Kimura, Hiroshi

AU - Ohkawa, Yasuyuki

N1 - Funding Information: JSPS KAKENHI [23310134, 25116010, 25118518, 25132709 and 26290064 to Y.O.]; Grant-in-Aid for JSPS Fellows [25·4024 to A.H.] (http://www.jsps.go.jp/ j-grantsinaid/). Funding for open access charge: JSPS KAKENHI [23310134, 25116010, 25118518, 25132709 and 26290064 to Y.O.]; Grant-in-Aid for JSPS Fellows [25·4024 to A.H.] (http://www.jsps.go.jp/j-grantsinaid/). Conflict of interest statement. None declared. Publisher Copyright: © 2015 The Author(s).

PY - 2015/1/30

Y1 - 2015/1/30

N2 - Lineage potential is triggered by lineage-specific transcription factors in association with changes in the chromatin structure. Histone H3.3 variant is thought to play an important role in the regulation of lineage-specific genes. To elucidate the function of H3.3 in myogenic differentiation, we forced the expression of GFP-H3.1 to alter the balance between H3.1 and H3.3 in mouse C2C12 cells that could be differentiated into myotubes. GFP-H3.1 replaced H3.3 in the regulatory regions of skeletal muscle (SKM) genes and induced a decrease of H3K4 trimethylation (H3K4me3) and increase of H3K27 trimethylation (H3K27me3). Similar results were obtained by H3.3 knockdown. In contrast, MyoD-dependent H3.3 incorporation into SKM genes in fibroblasts induced an increase of H3K4me3 and H3K27me3. In mouse embryos, a bivalent modification of H3K4me3 and H3K27me3 was formed on H3.3-incorporated SKM genes before embryonic skeletal muscle differentiation. These results suggest that lineage potential is established through a selective incorporation of specific H3 variants that governs the balance of histone modifications.

AB - Lineage potential is triggered by lineage-specific transcription factors in association with changes in the chromatin structure. Histone H3.3 variant is thought to play an important role in the regulation of lineage-specific genes. To elucidate the function of H3.3 in myogenic differentiation, we forced the expression of GFP-H3.1 to alter the balance between H3.1 and H3.3 in mouse C2C12 cells that could be differentiated into myotubes. GFP-H3.1 replaced H3.3 in the regulatory regions of skeletal muscle (SKM) genes and induced a decrease of H3K4 trimethylation (H3K4me3) and increase of H3K27 trimethylation (H3K27me3). Similar results were obtained by H3.3 knockdown. In contrast, MyoD-dependent H3.3 incorporation into SKM genes in fibroblasts induced an increase of H3K4me3 and H3K27me3. In mouse embryos, a bivalent modification of H3K4me3 and H3K27me3 was formed on H3.3-incorporated SKM genes before embryonic skeletal muscle differentiation. These results suggest that lineage potential is established through a selective incorporation of specific H3 variants that governs the balance of histone modifications.

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JO - Nucleic acids research

JF - Nucleic acids research

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ER -

Incorporation of histone H3.1 suppresses the lineage potential of skeletal muscle

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