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Oncogenic Kras induces spatiotemporally specific tissue deformation through converting pulsatile into sustained ERK activation – Nature Cell Biology

  • Bissell, M. J. & Hines, W. C. Why don’t we get more cancer? A proposed role of the microenvironment in restraining cancer progression. Nat. Med. 17, 320–329 (2011).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Schneider, G., Schmidt-Supprian, M., Rad, R. & Saur, D. Tissue-specific tumorigenesis: context matters. Nat. Rev. Cancer 17, 239–253 (2017).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Kakiuchi, N. & Ogawa, S. Clonal expansion in non-cancer tissues. Nat. Rev. Cancer 21, 239–256 (2021).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Amberg, N. et al. Mouse models of nonmelanoma skin cancer. Methods Mol. Biol. 1267, 217–250 (2015).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Lapouge, G. et al. Identifying the cellular origin of squamous skin tumors. Proc. Natl Acad. Sci. USA 108, 7431–7436 (2011).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Latil, M. et al. Cell-type-specific chromatin states differentially prime squamous cell carcinoma tumor-initiating cells for epithelial to mesenchymal transition. Cell Stem Cell 20, 191–204.e195 (2017).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • White, A. C. et al. Stem cell quiescence acts as a tumour suppressor in squamous tumours. Nat. Cell Biol. 16, 99–107 (2014).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • White, A. C. et al. Defining the origins of Ras/p53-mediated squamous cell carcinoma. Proc. Natl Acad. Sci. USA 108, 7425–7430 (2011).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Brown, S. et al. Correction of aberrant growth preserves tissue homeostasis. Nature 548, 334–337 (2017).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Pineda, C. M. et al. Hair follicle regeneration suppresses Ras-driven oncogenic growth. J. Cell Biol. 218, 3212–3222 (2019).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Joost, S. et al. The molecular anatomy of mouse skin during hair growth and rest. Cell Stem Cell 26, 441–457.e447 (2020).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Lee, J. & Tumbar, T. Hairy tale of signaling in hair follicle development and cycling. Semin. Cell Dev. Biol. 23, 906–916 (2012).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Rompolas, P. et al. Live imaging of stem cell and progeny behaviour in physiological hair-follicle regeneration. Nature 487, 496–499 (2012).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Rompolas, P., Mesa, K. R. & Greco, V. Spatial organization within a niche as a determinant of stem-cell fate. Nature 502, 513–518 (2013).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Xin, T., Gonzalez, D., Rompolas, P. & Greco, V. Flexible fate determination ensures robust differentiation in the hair follicle. Nat. Cell Biol. 20, 1361–1369 (2018).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Sequeira, I. & Nicolas, J. F. Redefining the structure of the hair follicle by 3D clonal analysis. Development 139, 3741–3751 (2012).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Morrow, A., Underwood, J., Seldin, L., Hinnant, T. & Lechler, T. Regulated spindle orientation buffers tissue growth in the epidermis. eLife 8, e48482 (2019).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Aikin, T. J., Peterson, A. F., Pokrass, M. J., Clark, H. R. & Regot, S. MAPK activity dynamics regulate non-cell autonomous effects of oncogene expression. eLife 9, e60541 (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Aoki, K. et al. Propagating wave of ERK activation orients collective cell migration. Dev. Cell 43, 305–317.e305 (2017).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • De Simone, A. et al. Control of osteoblast regeneration by a train of Erk activity waves. Nature 590, 129–133 (2021).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Hino, N. et al. ERK-mediated mechanochemical waves direct collective cell polarization. Dev. Cell 53, 646–660.e648 (2020).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Hiratsuka, T. et al. Intercellular propagation of extracellular signal-regulated kinase activation revealed by in vivo imaging of mouse skin. eLife 4, e05178 (2015).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Pokrass, M. J. et al. Cell-cycle-dependent ERK signaling dynamics direct fate specification in the mammalian preimplantation embryo. Dev. Cell 55, 328–340.e325 (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Regot, S., Hughey, J. J., Bajar, B. T., Carrasco, S. & Covert, M. W. High-sensitivity measurements of multiple kinase activities in live single cells. Cell 157, 1724–1734 (2014).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Li, S., Balmain, A. & Counter, C. M. A model for RAS mutation patterns in cancers: finding the sweet spot. Nat. Rev. Cancer 18, 767–777 (2018).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Johnson, H. E. & Toettcher, J. E. Signaling dynamics control cell fate in the early Drosophila embryo. Dev. Cell 48, 361–370.e363 (2019).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Marshall, C. J. Specificity of receptor tyrosine kinase signaling: transient versus sustained extracellular signal-regulated kinase activation. Cell 80, 179–185 (1995).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Gagliardi, P. A. et al. Collective ERK/Akt activity waves orchestrate epithelial homeostasis by driving apoptosis-induced survival. Dev. Cell 56, 1712–1726.e1716 (2021).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Pond, K. W. et al. Live-cell imaging in human colonic monolayers reveals ERK waves limit the stem cell compartment to maintain epithelial homeostasis. eLife 11, e78837 (2022).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Valon, L. et al. Robustness of epithelial sealing is an emerging property of local ERK feedback driven by cell elimination. Dev. Cell 56, 1700–1711.e1708 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Bugaj, L. J. et al. Cancer mutations and targeted drugs can disrupt dynamic signal encoding by the Ras-Erk pathway. Science 361, eaao3048 (2018).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Dessauges, C. et al. Optogenetic actuator – ERK biosensor circuits identify MAPK network nodes that shape ERK dynamics. Mol. Syst. Biol. 18, e10670 (2022).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Hiratsuka, T., Bordeu, I., Pruessner, G. & Watt, F. M. Regulation of ERK basal and pulsatile activity control proliferation and exit from the stem cell compartment in mammalian epidermis. Proc. Natl Acad. Sci. USA 117, 17796–17807 (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Aoki, K. et al. Stochastic ERK activation induced by noise and cell-to-cell propagation regulates cell density-dependent proliferation. Mol. Cell 52, 529–540 (2013).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Sugawara, K. et al. Spatial and temporal control of laminin-332 (5) and -511 (10) expression during induction of anagen hair growth. J. Histochem. Cytochem. 55, 43–55 (2007).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Rezza, A. et al. Signaling networks among stem cell precursors, transit-amplifying progenitors, and their niche in developing hair follicles. Cell Rep. 14, 3001–3018 (2016).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Tumbar, T. et al. Defining the epithelial stem cell niche in skin. Science 303, 359–363 (2004).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Mesa, K. R. et al. Niche-induced cell death and epithelial phagocytosis regulate hair follicle stem cell pool. Nature 522, 94–97 (2015).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Madisen, L. et al. A robust and high-throughput Cre reporting and characterization system for the whole mouse brain. Nat. Neurosci. 13, 133–140 (2010).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Jackson, E. L. et al. Analysis of lung tumor initiation and progression using conditional expression of oncogenic K-ras. Genes Dev. 15, 3243–3248 (2001).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Chen, X. et al. Endogenous expression of Hras(G12V) induces developmental defects and neoplasms with copy number imbalances of the oncogene. Proc. Natl Acad. Sci. USA 106, 7979–7984 (2009).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Barker, N. et al. Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature 449, 1003–1007 (2007).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Muller-Rover, S. et al. A comprehensive guide for the accurate classification of murine hair follicles in distinct hair cycle stages. J. Invest. Dermatol. 117, 3–15 (2001).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Chi, W., Wu, E. & Morgan, B. A. Dermal papilla cell number specifies hair size, shape and cycling and its reduction causes follicular decline. Development 140, 1676–1683 (2013).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Greco, V. et al. A two-step mechanism for stem cell activation during hair regeneration. Cell Stem Cell 4, 155–169 (2009).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar