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Cellular population dynamics shape the route to human pluripotency

Author

Listed:
  • Francesco Panariello

    (Armenise/Harvard Laboratory of Integrative Genomics)

  • Onelia Gagliano

    (University of Padova
    Veneto Institute of Molecular Medicine (VIMM)
    University College London)

  • Camilla Luni

    (ShanghaiTech University
    University of Bologna)

  • Antonio Grimaldi

    (Armenise/Harvard Laboratory of Integrative Genomics)

  • Silvia Angiolillo

    (University of Padova
    Veneto Institute of Molecular Medicine (VIMM))

  • Wei Qin

    (University of Padova
    Veneto Institute of Molecular Medicine (VIMM)
    ShanghaiTech University)

  • Anna Manfredi

    (Armenise/Harvard Laboratory of Integrative Genomics
    NEGEDIA (Next Generation Diagnostic srl))

  • Patrizia Annunziata

    (Armenise/Harvard Laboratory of Integrative Genomics
    NEGEDIA (Next Generation Diagnostic srl))

  • Shaked Slovin

    (Armenise/Harvard Laboratory of Integrative Genomics)

  • Lorenzo Vaccaro

    (Armenise/Harvard Laboratory of Integrative Genomics)

  • Sara Riccardo

    (Armenise/Harvard Laboratory of Integrative Genomics
    NEGEDIA (Next Generation Diagnostic srl))

  • Valentina Bouche

    (Armenise/Harvard Laboratory of Integrative Genomics)

  • Manuela Dionisi

    (Armenise/Harvard Laboratory of Integrative Genomics)

  • Marcello Salvi

    (Armenise/Harvard Laboratory of Integrative Genomics)

  • Sebastian Martewicz

    (ShanghaiTech University)

  • Manli Hu

    (ShanghaiTech University)

  • Meihua Cui

    (ShanghaiTech University)

  • Hannah Stuart

    (University of Padova
    Veneto Institute of Molecular Medicine (VIMM))

  • Cecilia Laterza

    (University of Padova
    Veneto Institute of Molecular Medicine (VIMM))

  • Giacomo Baruzzo

    (University of Padova)

  • Geoffrey Schiebinger

    (University of British Columbia)

  • Barbara Camillo

    (University of Padova
    University of Padova
    University of Padova)

  • Davide Cacchiarelli

    (Armenise/Harvard Laboratory of Integrative Genomics
    University of Naples “Federico II”
    University of Naples “Federico II”)

  • Nicola Elvassore

    (University of Padova
    Veneto Institute of Molecular Medicine (VIMM)
    University College London
    ShanghaiTech University)

Abstract

Human cellular reprogramming to induced pluripotency is still an inefficient process, which has hindered studying the role of critical intermediate stages. Here we take advantage of high efficiency reprogramming in microfluidics and temporal multi-omics to identify and resolve distinct sub-populations and their interactions. We perform secretome analysis and single-cell transcriptomics to show functional extrinsic pathways of protein communication between reprogramming sub-populations and the re-shaping of a permissive extracellular environment. We pinpoint the HGF/MET/STAT3 axis as a potent enhancer of reprogramming, which acts via HGF accumulation within the confined system of microfluidics, and in conventional dishes needs to be supplied exogenously to enhance efficiency. Our data suggest that human cellular reprogramming is a transcription factor-driven process that it is deeply dependent on extracellular context and cell population determinants.

Suggested Citation

  • Francesco Panariello & Onelia Gagliano & Camilla Luni & Antonio Grimaldi & Silvia Angiolillo & Wei Qin & Anna Manfredi & Patrizia Annunziata & Shaked Slovin & Lorenzo Vaccaro & Sara Riccardo & Valenti, 2023. "Cellular population dynamics shape the route to human pluripotency," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-37270-w
    DOI: 10.1038/s41467-023-37270-w
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    as
    1. Xiaodong Liu & John F. Ouyang & Fernando J. Rossello & Jia Ping Tan & Kathryn C. Davidson & Daniela S. Valdes & Jan Schröder & Yu B. Y. Sun & Joseph Chen & Anja S. Knaupp & Guizhi Sun & Hun S. Chy & Z, 2020. "Reprogramming roadmap reveals route to human induced trophoblast stem cells," Nature, Nature, vol. 586(7827), pages 101-107, October.
    2. Paul J. Tesar & Josh G. Chenoweth & Frances A. Brook & Timothy J. Davies & Edward P. Evans & David L. Mack & Richard L. Gardner & Ronald D. G. McKay, 2007. "New cell lines from mouse epiblast share defining features with human embryonic stem cells," Nature, Nature, vol. 448(7150), pages 196-199, July.
    3. Junyue Cao & Malte Spielmann & Xiaojie Qiu & Xingfan Huang & Daniel M. Ibrahim & Andrew J. Hill & Fan Zhang & Stefan Mundlos & Lena Christiansen & Frank J. Steemers & Cole Trapnell & Jay Shendure, 2019. "The single-cell transcriptional landscape of mammalian organogenesis," Nature, Nature, vol. 566(7745), pages 496-502, February.
    4. Kazutoshi Takahashi & Koji Tanabe & Mari Ohnuki & Megumi Narita & Aki Sasaki & Masamichi Yamamoto & Michiko Nakamura & Kenta Sutou & Kenji Osafune & Shinya Yamanaka, 2014. "Induction of pluripotency in human somatic cells via a transient state resembling primitive streak-like mesendoderm," Nature Communications, Nature, vol. 5(1), pages 1-9, May.
    5. Onelia Gagliano & Camilla Luni & Yan Li & Silvia Angiolillo & Wei Qin & Francesco Panariello & Davide Cacchiarelli & Joseph S. Takahashi & Nicola Elvassore, 2021. "Synchronization between peripheral circadian clock and feeding-fasting cycles in microfluidic device sustains oscillatory pattern of transcriptome," Nature Communications, Nature, vol. 12(1), pages 1-12, December.
    6. Jacob Hanna & Krishanu Saha & Bernardo Pando & Jeroen van Zon & Christopher J. Lengner & Menno P. Creyghton & Alexander van Oudenaarden & Rudolf Jaenisch, 2009. "Direct cell reprogramming is a stochastic process amenable to acceleration," Nature, Nature, vol. 462(7273), pages 595-601, December.
    7. Shinya Yamanaka, 2009. "Elite and stochastic models for induced pluripotent stem cell generation," Nature, Nature, vol. 460(7251), pages 49-52, July.
    8. Salah Mahmoudi & Elena Mancini & Lucy Xu & Alessandra Moore & Fereshteh Jahanbani & Katja Hebestreit & Rajini Srinivasan & Xiyan Li & Keerthana Devarajan & Laurie Prélot & Cheen Euong Ang & Yohei Shib, 2019. "Heterogeneity in old fibroblasts is linked to variability in reprogramming and wound healing," Nature, Nature, vol. 574(7779), pages 553-558, October.
    9. Carla Boccaccio & Margherita Andò & Luca Tamagnone & Alberto Bardelli & Paolo Michieli & Carlo Battistini & Paolo M. Comoglio, 1998. "Induction of epithelial tubules by growth factor HGF depends on the STAT pathway," Nature, Nature, vol. 391(6664), pages 285-288, January.
    10. Hongwei Chen & Irène Aksoy & Fabrice Gonnot & Pierre Osteil & Maxime Aubry & Claire Hamela & Cloé Rognard & Arnaud Hochard & Sophie Voisin & Emeline Fontaine & Magali Mure & Marielle Afanassieff & Elo, 2015. "Reinforcement of STAT3 activity reprogrammes human embryonic stem cells to naive-like pluripotency," Nature Communications, Nature, vol. 6(1), pages 1-17, November.
    11. Jordan A. Ramilowski & Tatyana Goldberg & Jayson Harshbarger & Edda Kloppmann & Marina Lizio & Venkata P. Satagopam & Masayoshi Itoh & Hideya Kawaji & Piero Carninci & Burkhard Rost & Alistair R. R. F, 2015. "A draft network of ligand–receptor-mediated multicellular signalling in human," Nature Communications, Nature, vol. 6(1), pages 1-12, November.
    12. Alexander M. Tsankov & Hongcang Gu & Veronika Akopian & Michael J. Ziller & Julie Donaghey & Ido Amit & Andreas Gnirke & Alexander Meissner, 2015. "Transcription factor binding dynamics during human ES cell differentiation," Nature, Nature, vol. 518(7539), pages 344-349, February.
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