RNPS1 in PSAP complex controls periodic pre-mRNA splicing over the cell cycle

Summary: Cell cycle progression requires periodic gene expression through splicing control. However, the splicing factor that directly controls this cell cycle-dependent splicing remains unknown. Cell cycle-dependent expression of the AURKB (aurora kinase B) gene is essential for chromosome segregat...

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Main Authors: Kazuhiro Fukumura, Akio Masuda, Jun-ichi Takeda, Osamu Nagano, Hideyuki Saya, Kinji Ohno, Akila Mayeda
Format: Article
Language:English
Published: Elsevier 2024-12-01
Series:iScience
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Online Access:http://www.sciencedirect.com/science/article/pii/S2589004224026257
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author Kazuhiro Fukumura
Akio Masuda
Jun-ichi Takeda
Osamu Nagano
Hideyuki Saya
Kinji Ohno
Akila Mayeda
author_facet Kazuhiro Fukumura
Akio Masuda
Jun-ichi Takeda
Osamu Nagano
Hideyuki Saya
Kinji Ohno
Akila Mayeda
author_sort Kazuhiro Fukumura
collection DOAJ
description Summary: Cell cycle progression requires periodic gene expression through splicing control. However, the splicing factor that directly controls this cell cycle-dependent splicing remains unknown. Cell cycle-dependent expression of the AURKB (aurora kinase B) gene is essential for chromosome segregation and cytokinesis. We previously reported that RNPS1 is essential to maintain precise splicing in AURKB intron 5. Here we show that RNPS1 plays this role in PSAP complex with PNN and SAP18, but not ASAP complex with ACIN1 and SAP18. Whole-transcriptome sequencing of RNPS1- and PNN-deficient cells indicated that RNPS1, either alone or as PSAP complex, is an essential splicing factor for a subset of introns. Remarkably, protein expression of RNPS1, but not PNN, is coordinated with cyclical splicing in PSAP-controlled introns including AURKB intron 5. The ubiquitin-proteasome pathway is involved in the periodic decrease of RNPS1 protein level. RNPS1 is a key factor that controls periodic splicing during the cell cycle.
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publishDate 2024-12-01
publisher Elsevier
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series iScience
spelling doaj-art-bd659f5b8d9847ee811636773b24743e2024-12-22T05:29:14ZengElsevieriScience2589-00422024-12-012712111400RNPS1 in PSAP complex controls periodic pre-mRNA splicing over the cell cycleKazuhiro Fukumura0Akio Masuda1Jun-ichi Takeda2Osamu Nagano3Hideyuki Saya4Kinji Ohno5Akila Mayeda6Division of Gene Regulation, Oncology Innovation Center, Fujita Health University, Toyoake, Aichi 470-1192, Japan; Corresponding authorDivision of Neurogenetics, Center for Neurological Disease and Cancer, Nagoya University Graduate School of Medicine, Nagoya, Aichi 466-8550, JapanDivision of Neurogenetics, Center for Neurological Disease and Cancer, Nagoya University Graduate School of Medicine, Nagoya, Aichi 466-8550, JapanDivision of Gene Regulation, Oncology Innovation Center, Fujita Health University, Toyoake, Aichi 470-1192, JapanDivision of Gene Regulation, Oncology Innovation Center, Fujita Health University, Toyoake, Aichi 470-1192, JapanDivision of Neurogenetics, Center for Neurological Disease and Cancer, Nagoya University Graduate School of Medicine, Nagoya, Aichi 466-8550, Japan; Graduate School of Nutritional Sciences, Nagoya University of Arts and Sciences, Nisshin, Aichi 470-0196, JapanDivision of Gene Regulation, Oncology Innovation Center, Fujita Health University, Toyoake, Aichi 470-1192, Japan; xFOREST Therapeutics Co., Ltd., Kajii-cho, Kamigyo-ku, Kyoto 602-0841, Japan; Corresponding authorSummary: Cell cycle progression requires periodic gene expression through splicing control. However, the splicing factor that directly controls this cell cycle-dependent splicing remains unknown. Cell cycle-dependent expression of the AURKB (aurora kinase B) gene is essential for chromosome segregation and cytokinesis. We previously reported that RNPS1 is essential to maintain precise splicing in AURKB intron 5. Here we show that RNPS1 plays this role in PSAP complex with PNN and SAP18, but not ASAP complex with ACIN1 and SAP18. Whole-transcriptome sequencing of RNPS1- and PNN-deficient cells indicated that RNPS1, either alone or as PSAP complex, is an essential splicing factor for a subset of introns. Remarkably, protein expression of RNPS1, but not PNN, is coordinated with cyclical splicing in PSAP-controlled introns including AURKB intron 5. The ubiquitin-proteasome pathway is involved in the periodic decrease of RNPS1 protein level. RNPS1 is a key factor that controls periodic splicing during the cell cycle.http://www.sciencedirect.com/science/article/pii/S2589004224026257Cell biologyCellular physiologyMolecular biologyProperties of biomolecules
spellingShingle Kazuhiro Fukumura
Akio Masuda
Jun-ichi Takeda
Osamu Nagano
Hideyuki Saya
Kinji Ohno
Akila Mayeda
RNPS1 in PSAP complex controls periodic pre-mRNA splicing over the cell cycle
iScience
Cell biology
Cellular physiology
Molecular biology
Properties of biomolecules
title RNPS1 in PSAP complex controls periodic pre-mRNA splicing over the cell cycle
title_full RNPS1 in PSAP complex controls periodic pre-mRNA splicing over the cell cycle
title_fullStr RNPS1 in PSAP complex controls periodic pre-mRNA splicing over the cell cycle
title_full_unstemmed RNPS1 in PSAP complex controls periodic pre-mRNA splicing over the cell cycle
title_short RNPS1 in PSAP complex controls periodic pre-mRNA splicing over the cell cycle
title_sort rnps1 in psap complex controls periodic pre mrna splicing over the cell cycle
topic Cell biology
Cellular physiology
Molecular biology
Properties of biomolecules
url http://www.sciencedirect.com/science/article/pii/S2589004224026257
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