KBG syndrome-associated protein ANKRD11 regulates SETD5 expression to modulate rRNA levels and translation

Summary: ANKRD11 haploinsufficiency is implicated in KBG syndrome, characterized by intellectual disability, autism spectrum disorders, and skeletal abnormalities. While SETD5 mutations are linked to a distinct clinical disorder, they also appear in KBG-like cases, suggesting shared molecular pathwa...

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Main Authors: Shoko Sashiyama, Tadashi Nakagawa, Makiko Nakagawa, Masaki Hosogane, Yasuaki Watanabe, Honoka Ashitomi, Kazusa Yamane, Norihiro Shibuya, Toshiro Moroishi, Keiko Nakayama, Toru Hosoi
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Language:English
Published: Elsevier 2025-06-01
Series:iScience
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Online Access:http://www.sciencedirect.com/science/article/pii/S2589004225009605
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author Shoko Sashiyama
Tadashi Nakagawa
Makiko Nakagawa
Masaki Hosogane
Yasuaki Watanabe
Honoka Ashitomi
Kazusa Yamane
Norihiro Shibuya
Toshiro Moroishi
Keiko Nakayama
Toru Hosoi
author_facet Shoko Sashiyama
Tadashi Nakagawa
Makiko Nakagawa
Masaki Hosogane
Yasuaki Watanabe
Honoka Ashitomi
Kazusa Yamane
Norihiro Shibuya
Toshiro Moroishi
Keiko Nakayama
Toru Hosoi
author_sort Shoko Sashiyama
collection DOAJ
description Summary: ANKRD11 haploinsufficiency is implicated in KBG syndrome, characterized by intellectual disability, autism spectrum disorders, and skeletal abnormalities. While SETD5 mutations are linked to a distinct clinical disorder, they also appear in KBG-like cases, suggesting shared molecular pathways. Here, we show that ANKRD11-deficient neural cells exhibit reduced ribosomal RNA (rRNA) and translation. Although ANKRD11 primarily localizes outside the nucleolus, where rDNA transcription occurs, it indirectly promotes rRNA expression by upregulating SETD5, a transcriptional activator of rRNA. Mechanistically, ANKRD11 interacts with the Setd5 promoter and recruits WDR5, a component of the histone H3 lysine 4 (H3K4) methyltransferase complex involved in transcriptional activation. Correspondingly, reduced H3K4 methylation on the Setd5 promoter correlates with diminished SETD5 expression in ANKRD11-deficient cells. Overexpression of ANKRD11 or SETD5 restores rRNA levels and translational activity. These findings underscore the role of the ANKRD11-SETD5 axis in alleviating KBG syndrome pathogenesis, offering insights into potential therapeutic targets.
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spelling doaj-art-db0f58d043294be3aa613bfdee67429a2025-08-20T02:00:50ZengElsevieriScience2589-00422025-06-0128611269910.1016/j.isci.2025.112699KBG syndrome-associated protein ANKRD11 regulates SETD5 expression to modulate rRNA levels and translationShoko Sashiyama0Tadashi Nakagawa1Makiko Nakagawa2Masaki Hosogane3Yasuaki Watanabe4Honoka Ashitomi5Kazusa Yamane6Norihiro Shibuya7Toshiro Moroishi8Keiko Nakayama9Toru Hosoi10Department of Clinical Pharmacology, Faculty of Pharmaceutical Sciences, Sanyo-Onoda City University, Sanyo-Onoda 756-0884, Japan; Department of Molecular and Medical Pharmacology, Faculty of Life Sciences, Kumamoto University, Kumamoto 860-8556, JapanDepartment of Clinical Pharmacology, Faculty of Pharmaceutical Sciences, Sanyo-Onoda City University, Sanyo-Onoda 756-0884, Japan; Division of Cell Proliferation, ART, Graduate School of Medicine, Tohoku University, Sendai 980-8575, Japan; Corresponding authorDivision of Cell Proliferation, ART, Graduate School of Medicine, Tohoku University, Sendai 980-8575, Japan; Institute of Gene Research, Yamaguchi University Science Research Center, Ube 755-8505, Japan; Advanced Technology Institute, Life Science Division, Yamaguchi University, Yamaguchi 755-8611, JapanDivision of Cell Proliferation, ART, Graduate School of Medicine, Tohoku University, Sendai 980-8575, JapanDivision of Cell Proliferation, ART, Graduate School of Medicine, Tohoku University, Sendai 980-8575, Japan; Department of Neurology, Tohoku University Graduate School of Medicine, Sendai 980-8575, JapanDepartment of Clinical Pharmacology, Faculty of Pharmaceutical Sciences, Sanyo-Onoda City University, Sanyo-Onoda 756-0884, JapanDepartment of Clinical Pharmacology, Faculty of Pharmaceutical Sciences, Sanyo-Onoda City University, Sanyo-Onoda 756-0884, JapanDepartment of Pharmacology, Faculty of Pharmaceutical Sciences, Sanyo-Onoda City University, Sanyo-Onoda 756-0884, JapanDepartment of Molecular and Medical Pharmacology, Faculty of Life Sciences, Kumamoto University, Kumamoto 860-8556, Japan; Center for Metabolic Regulation of Healthy Aging, Faculty of Life Sciences, Kumamoto University, Kumamoto 860-8556, Japan; Division of Cellular Dynamics, Medical Research Laboratory, Institute of Science Tokyo, 1-5-45 Yushima, Bunkyo-ku, Tokyo 113-8510, JapanDivision of Cell Proliferation, ART, Graduate School of Medicine, Tohoku University, Sendai 980-8575, Japan; Research Infrastructure Management Center, Institute of Science Tokyo, 1-5-45 Yushima, Bunkyo-ku, Tokyo 113-8510, JapanDepartment of Clinical Pharmacology, Faculty of Pharmaceutical Sciences, Sanyo-Onoda City University, Sanyo-Onoda 756-0884, JapanSummary: ANKRD11 haploinsufficiency is implicated in KBG syndrome, characterized by intellectual disability, autism spectrum disorders, and skeletal abnormalities. While SETD5 mutations are linked to a distinct clinical disorder, they also appear in KBG-like cases, suggesting shared molecular pathways. Here, we show that ANKRD11-deficient neural cells exhibit reduced ribosomal RNA (rRNA) and translation. Although ANKRD11 primarily localizes outside the nucleolus, where rDNA transcription occurs, it indirectly promotes rRNA expression by upregulating SETD5, a transcriptional activator of rRNA. Mechanistically, ANKRD11 interacts with the Setd5 promoter and recruits WDR5, a component of the histone H3 lysine 4 (H3K4) methyltransferase complex involved in transcriptional activation. Correspondingly, reduced H3K4 methylation on the Setd5 promoter correlates with diminished SETD5 expression in ANKRD11-deficient cells. Overexpression of ANKRD11 or SETD5 restores rRNA levels and translational activity. These findings underscore the role of the ANKRD11-SETD5 axis in alleviating KBG syndrome pathogenesis, offering insights into potential therapeutic targets.http://www.sciencedirect.com/science/article/pii/S2589004225009605Molecular biologyCell biology
spellingShingle Shoko Sashiyama
Tadashi Nakagawa
Makiko Nakagawa
Masaki Hosogane
Yasuaki Watanabe
Honoka Ashitomi
Kazusa Yamane
Norihiro Shibuya
Toshiro Moroishi
Keiko Nakayama
Toru Hosoi
KBG syndrome-associated protein ANKRD11 regulates SETD5 expression to modulate rRNA levels and translation
iScience
Molecular biology
Cell biology
title KBG syndrome-associated protein ANKRD11 regulates SETD5 expression to modulate rRNA levels and translation
title_full KBG syndrome-associated protein ANKRD11 regulates SETD5 expression to modulate rRNA levels and translation
title_fullStr KBG syndrome-associated protein ANKRD11 regulates SETD5 expression to modulate rRNA levels and translation
title_full_unstemmed KBG syndrome-associated protein ANKRD11 regulates SETD5 expression to modulate rRNA levels and translation
title_short KBG syndrome-associated protein ANKRD11 regulates SETD5 expression to modulate rRNA levels and translation
title_sort kbg syndrome associated protein ankrd11 regulates setd5 expression to modulate rrna levels and translation
topic Molecular biology
Cell biology
url http://www.sciencedirect.com/science/article/pii/S2589004225009605
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