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Cell cycle gene regulation dynamics revealed by RNA velocity and deep-learning

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  • Andrea Riba

    (Institut de Génétique et de Biologie Moléculaire et Cellulaire (IGBMC); Université de Strasbourg; Centre National de la Recherche Scientifique (CNRS) UMR 7104; Institut National de la Santé et de la Recherche Médicale (INSERM) UMR-S 1258)

  • Attila Oravecz

    (Institut de Génétique et de Biologie Moléculaire et Cellulaire (IGBMC); Université de Strasbourg; Centre National de la Recherche Scientifique (CNRS) UMR 7104; Institut National de la Santé et de la Recherche Médicale (INSERM) UMR-S 1258)

  • Matej Durik

    (Institut de Génétique et de Biologie Moléculaire et Cellulaire (IGBMC); Université de Strasbourg; Centre National de la Recherche Scientifique (CNRS) UMR 7104; Institut National de la Santé et de la Recherche Médicale (INSERM) UMR-S 1258)

  • Sara Jiménez

    (Institut de Génétique et de Biologie Moléculaire et Cellulaire (IGBMC); Université de Strasbourg; Centre National de la Recherche Scientifique (CNRS) UMR 7104; Institut National de la Santé et de la Recherche Médicale (INSERM) UMR-S 1258)

  • Violaine Alunni

    (Institut de Génétique et de Biologie Moléculaire et Cellulaire (IGBMC); Université de Strasbourg; Centre National de la Recherche Scientifique (CNRS) UMR 7104; Institut National de la Santé et de la Recherche Médicale (INSERM) UMR-S 1258)

  • Marie Cerciat

    (Institut de Génétique et de Biologie Moléculaire et Cellulaire (IGBMC); Université de Strasbourg; Centre National de la Recherche Scientifique (CNRS) UMR 7104; Institut National de la Santé et de la Recherche Médicale (INSERM) UMR-S 1258)

  • Matthieu Jung

    (Institut de Génétique et de Biologie Moléculaire et Cellulaire (IGBMC); Université de Strasbourg; Centre National de la Recherche Scientifique (CNRS) UMR 7104; Institut National de la Santé et de la Recherche Médicale (INSERM) UMR-S 1258)

  • Céline Keime

    (Institut de Génétique et de Biologie Moléculaire et Cellulaire (IGBMC); Université de Strasbourg; Centre National de la Recherche Scientifique (CNRS) UMR 7104; Institut National de la Santé et de la Recherche Médicale (INSERM) UMR-S 1258)

  • William M. Keyes

    (Institut de Génétique et de Biologie Moléculaire et Cellulaire (IGBMC); Université de Strasbourg; Centre National de la Recherche Scientifique (CNRS) UMR 7104; Institut National de la Santé et de la Recherche Médicale (INSERM) UMR-S 1258)

  • Nacho Molina

    (Institut de Génétique et de Biologie Moléculaire et Cellulaire (IGBMC); Université de Strasbourg; Centre National de la Recherche Scientifique (CNRS) UMR 7104; Institut National de la Santé et de la Recherche Médicale (INSERM) UMR-S 1258)

Abstract

Despite the fact that the cell cycle is a fundamental process of life, a detailed quantitative understanding of gene regulation dynamics throughout the cell cycle is far from complete. Single-cell RNA-sequencing (scRNA-seq) technology gives access to these dynamics without externally perturbing the cell. Here, by generating scRNA-seq libraries in different cell systems, we observe cycling patterns in the unspliced-spliced RNA space of cell cycle-related genes. Since existing methods to analyze scRNA-seq are not efficient to measure cycling gene dynamics, we propose a deep learning approach (DeepCycle) to fit these patterns and build a high-resolution map of the entire cell cycle transcriptome. Characterizing the cell cycle in embryonic and somatic cells, we identify major waves of transcription during the G1 phase and systematically study the stages of the cell cycle. Our work will facilitate the study of the cell cycle in multiple cellular models and different biological contexts.

Suggested Citation

  • Andrea Riba & Attila Oravecz & Matej Durik & Sara Jiménez & Violaine Alunni & Marie Cerciat & Matthieu Jung & Céline Keime & William M. Keyes & Nacho Molina, 2022. "Cell cycle gene regulation dynamics revealed by RNA velocity and deep-learning," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-30545-8
    DOI: 10.1038/s41467-022-30545-8
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    References listed on IDEAS

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    1. Zehua Liu & Huazhe Lou & Kaikun Xie & Hao Wang & Ning Chen & Oscar M. Aparicio & Michael Q. Zhang & Rui Jiang & Ting Chen, 2017. "Reconstructing cell cycle pseudo time-series via single-cell transcriptome data," Nature Communications, Nature, vol. 8(1), pages 1-9, December.
    2. Gioele La Manno & Ruslan Soldatov & Amit Zeisel & Emelie Braun & Hannah Hochgerner & Viktor Petukhov & Katja Lidschreiber & Maria E. Kastriti & Peter Lönnerberg & Alessandro Furlan & Jean Fan & Lars E, 2018. "RNA velocity of single cells," Nature, Nature, vol. 560(7719), pages 494-498, August.
    3. Yifan Zhao & Huiyu Cai & Zuobai Zhang & Jian Tang & Yue Li, 2021. "Learning interpretable cellular and gene signature embeddings from single-cell transcriptomic data," Nature Communications, Nature, vol. 12(1), pages 1-15, December.
    4. Hee Won Yang & Mingyu Chung & Takamasa Kudo & Tobias Meyer, 2017. "Competing memories of mitogen and p53 signalling control cell-cycle entry," Nature, Nature, vol. 549(7672), pages 404-408, September.
    5. Shih-Yin Tsai & Rene Opavsky & Nidhi Sharma & Lizhao Wu & Shan Naidu & Eric Nolan & Enrique Feria-Arias & Cynthia Timmers & Jana Opavska & Alain de Bruin & Jean-Leon Chong & Prashant Trikha & Soledad , 2008. "Mouse development with a single E2F activator," Nature, Nature, vol. 454(7208), pages 1137-1141, August.
    6. Gökcen Eraslan & Lukas M. Simon & Maria Mircea & Nikola S. Mueller & Fabian J. Theis, 2019. "Single-cell RNA-seq denoising using a deep count autoencoder," Nature Communications, Nature, vol. 10(1), pages 1-14, December.
    7. Mahé Raccaud & Elias T. Friman & Andrea B. Alber & Harsha Agarwal & Cédric Deluz & Timo Kuhn & J. Christof M. Gebhardt & David M. Suter, 2019. "Mitotic chromosome binding predicts transcription factor properties in interphase," Nature Communications, Nature, vol. 10(1), pages 1-16, December.
    8. Shaoheng Liang & Fang Wang & Jincheng Han & Ken Chen, 2020. "Latent periodic process inference from single-cell RNA-seq data," Nature Communications, Nature, vol. 11(1), pages 1-8, December.
    9. Jiarui Ding & Anne Condon & Sohrab P. Shah, 2018. "Interpretable dimensionality reduction of single cell transcriptome data with deep generative models," Nature Communications, Nature, vol. 9(1), pages 1-13, December.
    10. Yifan Zhao & Huiyu Cai & Zuobai Zhang & Jian Tang & Yue Li, 2021. "Publisher Correction: Learning interpretable cellular and gene signature embeddings from single-cell transcriptomic data," Nature Communications, Nature, vol. 12(1), pages 1-1, December.
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    Cited by:

    1. Jiachen Li & Xiaoyong Pan & Ye Yuan & Hong-Bin Shen, 2024. "TFvelo: gene regulation inspired RNA velocity estimation," Nature Communications, Nature, vol. 15(1), pages 1-15, December.

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