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Collagen signaling and matrix stiffness regulate multipotency in glandular epithelial stem cells in mice

Author

Listed:
  • Chen Jiang

    (Université Libre de Bruxelles (ULB))

  • Alessia Centonze

    (Université Libre de Bruxelles (ULB))

  • Yura Song

    (Université Libre de Bruxelles (ULB))

  • Antonius Chrisnandy

    (Ecole Polytechnique Fédérale de Lausanne (EPFL))

  • Elisavet Tika

    (Université Libre de Bruxelles (ULB))

  • Saba Rezakhani

    (Ecole Polytechnique Fédérale de Lausanne (EPFL))

  • Zahra Zahedi

    (Université Libre de Bruxelles (ULB))

  • Gaëlle Bouvencourt

    (Université Libre de Bruxelles (ULB))

  • Christine Dubois

    (Université Libre de Bruxelles (ULB))

  • Alexandra Van Keymeulen

    (Université Libre de Bruxelles (ULB))

  • Matthias Lütolf

    (Ecole Polytechnique Fédérale de Lausanne (EPFL)
    School of Basic Science (SB), EPFL
    Pharma Research and Early Development (pRED), F. Hoffmann-La Roche Ltd)

  • Alejandro Sifrim

    (University of Leuven, KU Leuven)

  • Cédric Blanpain

    (Université Libre de Bruxelles (ULB)
    Université Libre de Bruxelles (ULB))

Abstract

Glandular epithelia, including mammary gland (MG) and prostate, are composed of luminal and basal cells. During embryonic development, glandular epithelia arise from multipotent stem cells (SCs) that are replaced after birth by unipotent basal and unipotent luminal SCs. Different conditions, such as basal cell transplantation, luminal cell ablation, and oncogene expression can reinduce adult basal SC (BaSCs) multipotency in different glandular epithelia. The mechanisms regulating the reactivation of multipotency are incompletely understood. Here, we have found that Collagen I expression is commonly upregulated in BaSCs across the different multipotent conditions. Increasing collagen concentration or stiffness of the extracellular matrix (ECM) promotes BaSC multipotency in MG and prostate organoids. Single cell RNA-seq of MG organoids in stiff conditions have uncovered the importance of β1 integrin/FAK/AP-1 axis in the regulation of BaSC multipotency. Altogether our study uncovers the key role of Collagen signaling and ECM stiffness in the regulation of multipotency in glandular epithelia.

Suggested Citation

  • Chen Jiang & Alessia Centonze & Yura Song & Antonius Chrisnandy & Elisavet Tika & Saba Rezakhani & Zahra Zahedi & Gaëlle Bouvencourt & Christine Dubois & Alexandra Van Keymeulen & Matthias Lütolf & Al, 2024. "Collagen signaling and matrix stiffness regulate multipotency in glandular epithelial stem cells in mice," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-54843-5
    DOI: 10.1038/s41467-024-54843-5
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    1. Shany Koren & Linsey Reavie & Joana Pinto Couto & Duvini De Silva & Michael B. Stadler & Tim Roloff & Adrian Britschgi & Tobias Eichlisberger & Hubertus Kohler & Olulanu Aina & Robert D. Cardiff & Moh, 2015. "PIK3CAH1047R induces multipotency and multi-lineage mammary tumours," Nature, Nature, vol. 525(7567), pages 114-118, September.
    2. Alessia Centonze & Shuheng Lin & Elisavet Tika & Alejandro Sifrim & Marco Fioramonti & Milan Malfait & Yura Song & Aline Wuidart & Jens Van Herck & Anne Dannau & Gaelle Bouvencourt & Christine Dubois , 2020. "Heterotypic cell–cell communication regulates glandular stem cell multipotency," Nature, Nature, vol. 584(7822), pages 608-613, August.
    3. Bhupinder Pal & Yunshun Chen & François Vaillant & Paul Jamieson & Lavinia Gordon & Anne C. Rios & Stephen Wilcox & Naiyang Fu & Kevin He Liu & Felicity C. Jackling & Melissa J. Davis & Geoffrey J. Li, 2017. "Construction of developmental lineage relationships in the mouse mammary gland by single-cell RNA profiling," Nature Communications, Nature, vol. 8(1), pages 1-14, December.
    4. Matthias P. Lutolf & Penney M. Gilbert & Helen M. Blau, 2009. "Designing materials to direct stem-cell fate," Nature, Nature, vol. 462(7272), pages 433-441, November.
    5. Alexandra Van Keymeulen & Ana Sofia Rocha & Marielle Ousset & Benjamin Beck & Gaëlle Bouvencourt & Jason Rock & Neha Sharma & Sophie Dekoninck & Cédric Blanpain, 2011. "Distinct stem cells contribute to mammary gland development and maintenance," Nature, Nature, vol. 479(7372), pages 189-193, November.
    6. Mark Shackleton & François Vaillant & Kaylene J. Simpson & John Stingl & Gordon K. Smyth & Marie-Liesse Asselin-Labat & Li Wu & Geoffrey J. Lindeman & Jane E. Visvader, 2006. "Generation of a functional mammary gland from a single stem cell," Nature, Nature, vol. 439(7072), pages 84-88, January.
    7. Karsten Bach & Sara Pensa & Marta Grzelak & James Hadfield & David J. Adams & John C. Marioni & Walid T. Khaled, 2017. "Differentiation dynamics of mammary epithelial cells revealed by single-cell RNA sequencing," Nature Communications, Nature, vol. 8(1), pages 1-11, December.
    8. Alexandra Van Keymeulen & May Yin Lee & Marielle Ousset & Sylvain Brohée & Sandrine Rorive & Rajshekhar R. Giraddi & Aline Wuidart & Gaëlle Bouvencourt & Christine Dubois & Isabelle Salmon & Christos , 2015. "Reactivation of multipotency by oncogenic PIK3CA induces breast tumour heterogeneity," Nature, Nature, vol. 525(7567), pages 119-123, September.
    9. Sirio Dupont & Leonardo Morsut & Mariaceleste Aragona & Elena Enzo & Stefano Giulitti & Michelangelo Cordenonsi & Francesca Zanconato & Jimmy Le Digabel & Mattia Forcato & Silvio Bicciato & Nicola Elv, 2011. "Role of YAP/TAZ in mechanotransduction," Nature, Nature, vol. 474(7350), pages 179-183, June.
    10. Nikolce Gjorevski & Norman Sachs & Andrea Manfrin & Sonja Giger & Maiia E. Bragina & Paloma Ordóñez-Morán & Hans Clevers & Matthias P. Lutolf, 2016. "Designer matrices for intestinal stem cell and organoid culture," Nature, Nature, vol. 539(7630), pages 560-564, November.
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