Deciphering alternative splicing patterns during cell fate transition of fast chemical reprogramming

Abstract Background Alternative splicing (AS) is a substantial contributor to the high complexity of transcriptomes in multicellular eukaryotes. Fast chemical reprogramming (FCR) system is an innovative approach that facilitates the rapid transition of somatic cells into induced pluripotent stem cel...

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Main Authors: Yunkun Lu, Kainan Lin, Yeling Ruan, Junjie Li, Huizhen Zhang, Tianyuan Pan, Qianqian Wang, Lianyu Lin, Sijie Feng
Format: Article
Language:English
Published: BMC 2025-06-01
Series:BMC Biology
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Online Access:https://doi.org/10.1186/s12915-025-02264-1
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author Yunkun Lu
Kainan Lin
Yeling Ruan
Junjie Li
Huizhen Zhang
Tianyuan Pan
Qianqian Wang
Lianyu Lin
Sijie Feng
author_facet Yunkun Lu
Kainan Lin
Yeling Ruan
Junjie Li
Huizhen Zhang
Tianyuan Pan
Qianqian Wang
Lianyu Lin
Sijie Feng
author_sort Yunkun Lu
collection DOAJ
description Abstract Background Alternative splicing (AS) is a substantial contributor to the high complexity of transcriptomes in multicellular eukaryotes. Fast chemical reprogramming (FCR) system is an innovative approach that facilitates the rapid transition of somatic cells into induced pluripotent stem cells (iPSCs). Results In this study, we used the FCR system to delve into the dynamics of AS during cell fate transition. The trajectory of FCR, as characterized by gene expression profiles, consistently aligned with that observed in AS patterns, revealing a complex interplay between AS and gene expression regulation. Additionally, we discovered that the exon exclusion events were more prevalent than the exon inclusion events, indicating a predominant mode of splicing regulation during FCR. Compared to transcription factor-induced reprogramming (TFR), FCR showed a distinct AS pattern, underscoring the unique regulatory mechanisms governing AS in each reprogramming system. Further investigation uncovered polypyrimidine tract-binding protein 3 (Ptbp3) as an important splicing factor, possibly participating in epigenetic regulation in late stage of FCR by affecting AS of epigenetic regulators. Moreover, we found an abundance of intron retention events caused by decrease in spliceosome activity, potentially contributing to the downregulation of key diapause-related genes in the middle and late stages of FCR. Conclusions This research provided a comprehensive characterization of AS during FCR, highlighting the pivotal roles of AS in regulating cell fate transitions. Our findings advanced the understanding of the molecular mechanisms governing cell fate decisions and offered new insights into the potential of FCR for regenerative medicine and therapeutic applications.
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spelling doaj-art-b7ef8e169ba1442d8bcf0a689ece9a602025-08-20T03:21:05ZengBMCBMC Biology1741-70072025-06-0123111610.1186/s12915-025-02264-1Deciphering alternative splicing patterns during cell fate transition of fast chemical reprogrammingYunkun Lu0Kainan Lin1Yeling Ruan2Junjie Li3Huizhen Zhang4Tianyuan Pan5Qianqian Wang6Lianyu Lin7Sijie Feng8Department of General Surgery, Sir Run-Run Shaw Hospital, Zhejiang University School of MedicineDepartment of General Surgery, Sir Run-Run Shaw Hospital, Zhejiang University School of MedicineDepartment of Head and Neck Surgery, Sir Run-Run Shaw Hospital, Zhejiang University School of MedicineSchool of Medicine, Henan Polytechnic UniversitySchool of Medicine, Henan Polytechnic UniversityDepartment of General Medicine, the First Affiliated Hospital of Zhejiang University School of MedicineDepartment of General Surgery, Sir Run-Run Shaw Hospital, Zhejiang University School of MedicineCollege of Life Science, Fujian Agriculture and Forestry UniversityDepartment of General Surgery, Sir Run-Run Shaw Hospital, Zhejiang University School of MedicineAbstract Background Alternative splicing (AS) is a substantial contributor to the high complexity of transcriptomes in multicellular eukaryotes. Fast chemical reprogramming (FCR) system is an innovative approach that facilitates the rapid transition of somatic cells into induced pluripotent stem cells (iPSCs). Results In this study, we used the FCR system to delve into the dynamics of AS during cell fate transition. The trajectory of FCR, as characterized by gene expression profiles, consistently aligned with that observed in AS patterns, revealing a complex interplay between AS and gene expression regulation. Additionally, we discovered that the exon exclusion events were more prevalent than the exon inclusion events, indicating a predominant mode of splicing regulation during FCR. Compared to transcription factor-induced reprogramming (TFR), FCR showed a distinct AS pattern, underscoring the unique regulatory mechanisms governing AS in each reprogramming system. Further investigation uncovered polypyrimidine tract-binding protein 3 (Ptbp3) as an important splicing factor, possibly participating in epigenetic regulation in late stage of FCR by affecting AS of epigenetic regulators. Moreover, we found an abundance of intron retention events caused by decrease in spliceosome activity, potentially contributing to the downregulation of key diapause-related genes in the middle and late stages of FCR. Conclusions This research provided a comprehensive characterization of AS during FCR, highlighting the pivotal roles of AS in regulating cell fate transitions. Our findings advanced the understanding of the molecular mechanisms governing cell fate decisions and offered new insights into the potential of FCR for regenerative medicine and therapeutic applications.https://doi.org/10.1186/s12915-025-02264-1Alternative splicingFast chemical reprogrammingCell fate transitionDiapause-like state
spellingShingle Yunkun Lu
Kainan Lin
Yeling Ruan
Junjie Li
Huizhen Zhang
Tianyuan Pan
Qianqian Wang
Lianyu Lin
Sijie Feng
Deciphering alternative splicing patterns during cell fate transition of fast chemical reprogramming
BMC Biology
Alternative splicing
Fast chemical reprogramming
Cell fate transition
Diapause-like state
title Deciphering alternative splicing patterns during cell fate transition of fast chemical reprogramming
title_full Deciphering alternative splicing patterns during cell fate transition of fast chemical reprogramming
title_fullStr Deciphering alternative splicing patterns during cell fate transition of fast chemical reprogramming
title_full_unstemmed Deciphering alternative splicing patterns during cell fate transition of fast chemical reprogramming
title_short Deciphering alternative splicing patterns during cell fate transition of fast chemical reprogramming
title_sort deciphering alternative splicing patterns during cell fate transition of fast chemical reprogramming
topic Alternative splicing
Fast chemical reprogramming
Cell fate transition
Diapause-like state
url https://doi.org/10.1186/s12915-025-02264-1
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