JMJD1A is a signal-sensing scaffold that regulates acute chromatin dynamics via SWI/SNF association for thermogenesis

Yohei Abe, Royhan Rozqie, Yoshihiro Matsumura, Takeshi Kawamura, Ryo Nakaki, Yuya Tsurutani, Kyoko Tanimura-Inagaki, Akira Shiono, Kenta Magoori, Kanako Nakamura, Shotaro Ogi, Shingo Kajimura, Hiroshi Kimura, Toshiya Tanaka, Kiyoko Fukami, Timothy Osborne, Tatsuhiko Kodama, Hiroyuki Aburatani, Takeshi Inagaki, Juro Sakai

Research output: Contribution to journalArticle

Abstract

Histone 3 lysine 9 (H3K9) demethylase JMJD1A regulates β-adrenergic-induced systemic metabolism and body weight control. Here we show that JMJD1A is phosphorylated at S265 by protein kinase A (PKA), and this is pivotal to activate the β1-adrenergic receptor gene (Adrb1) and downstream targets including Ucp1 in brown adipocytes (BATs). Phosphorylation of JMJD1A by PKA increases its interaction with the SWI/SNF nucleosome remodelling complex and DNA-bound PPAR 3. This complex confers β-adrenergic-induced rapid JMJD1A recruitment to target sites and facilitates long-range chromatin interactions and target gene activation. This rapid gene induction is dependent on S265 phosphorylation but not on demethylation activity. Our results show that JMJD1A has two important roles in regulating hormone-stimulated chromatin dynamics that modulate thermogenesis in BATs. In one role, JMJD1A is recruited to target sites and functions as a cAMP-responsive scaffold that facilitates long-range chromatin interactions, and in the second role, JMJD1A demethylates H3K9 di-methylation.

Original languageEnglish (US)
Article number7052
JournalNature Communications
Volume6
DOIs
StatePublished - May 7 2015
Externally publishedYes

Fingerprint

chromatin
Thermogenesis
adrenergics
Scaffolds
Brown Adipocytes
Chromatin
Phosphorylation
Genes
Association reactions
genes
Cyclic AMP-Dependent Protein Kinases
Adrenergic Agents
phosphorylation
Weight control
Peroxisome Proliferator-Activated Receptors
Methylation
Nucleosomes
proteins
Metabolism
body weight

ASJC Scopus subject areas

  • Chemistry(all)
  • Biochemistry, Genetics and Molecular Biology(all)
  • Physics and Astronomy(all)

Cite this

JMJD1A is a signal-sensing scaffold that regulates acute chromatin dynamics via SWI/SNF association for thermogenesis. / Abe, Yohei; Rozqie, Royhan; Matsumura, Yoshihiro; Kawamura, Takeshi; Nakaki, Ryo; Tsurutani, Yuya; Tanimura-Inagaki, Kyoko; Shiono, Akira; Magoori, Kenta; Nakamura, Kanako; Ogi, Shotaro; Kajimura, Shingo; Kimura, Hiroshi; Tanaka, Toshiya; Fukami, Kiyoko; Osborne, Timothy; Kodama, Tatsuhiko; Aburatani, Hiroyuki; Inagaki, Takeshi; Sakai, Juro.

In: Nature Communications, Vol. 6, 7052, 07.05.2015.

Research output: Contribution to journalArticle

Abe, Y, Rozqie, R, Matsumura, Y, Kawamura, T, Nakaki, R, Tsurutani, Y, Tanimura-Inagaki, K, Shiono, A, Magoori, K, Nakamura, K, Ogi, S, Kajimura, S, Kimura, H, Tanaka, T, Fukami, K, Osborne, T, Kodama, T, Aburatani, H, Inagaki, T & Sakai, J 2015, 'JMJD1A is a signal-sensing scaffold that regulates acute chromatin dynamics via SWI/SNF association for thermogenesis', Nature Communications, vol. 6, 7052. https://doi.org/10.1038/ncomms8052
Abe, Yohei ; Rozqie, Royhan ; Matsumura, Yoshihiro ; Kawamura, Takeshi ; Nakaki, Ryo ; Tsurutani, Yuya ; Tanimura-Inagaki, Kyoko ; Shiono, Akira ; Magoori, Kenta ; Nakamura, Kanako ; Ogi, Shotaro ; Kajimura, Shingo ; Kimura, Hiroshi ; Tanaka, Toshiya ; Fukami, Kiyoko ; Osborne, Timothy ; Kodama, Tatsuhiko ; Aburatani, Hiroyuki ; Inagaki, Takeshi ; Sakai, Juro. / JMJD1A is a signal-sensing scaffold that regulates acute chromatin dynamics via SWI/SNF association for thermogenesis. In: Nature Communications. 2015 ; Vol. 6.
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