Cited by 406Developmental Biology and Gene RegulationMicrotubule and mitosis dynamicsSkin and Cellular Biology Research

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Asymmetric cell divisions promote Notch-dependent epidermal differentiation

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Williams, Scott E., Beronja, Slobodan, Pasolli, H. Amalia, Fuchs, Elaine·2011·Nature

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Abstract

Stem and progenitor cells use asymmetric cell divisions to balance proliferation and differentiation. Evidence from invertebrates shows that this process is regulated by proteins asymmetrically distributed at the cell cortex during mitosis: Par3-Par6-aPKC, which confer polarity, and Gα(i)-LGN/AGS3-NuMA-dynein/dynactin, which govern spindle positioning. Here we focus on developing mouse skin, where progenitor cells execute a switch from symmetric to predominantly asymmetric divisions concomitant with stratification. Using in vivo skin-specific lentiviral RNA interference, we investigate spindle orientation regulation and provide direct evidence that LGN (also called Gpsm2), NuMA and dynactin (Dctn1) are involved. In compromising asymmetric cell divisions, we uncover profound defects in stratification, differentiation and barrier formation, and implicate Notch signalling as an important effector. Our study demonstrates the efficacy of applying RNA interference in vivo to mammalian systems, and the ease of uncovering complex genetic interactions, here to gain insights into how changes in spindle orientation are coupled to establishing proper tissue architecture during skin development.

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A Lentiviral RNAi Library for Human and Mouse Genes Applied to an Arrayed Viral High-Content Screen
Moffat, J., Grueneberg, D. A., Yang, X., Kim, S. Y., Kloepfer, A. M., Hinkle, G., Piqani, B., Eisenhaure, T., Luo, B., Grenier, J. K., et al. (2006) · Cell · doi:10.1016/j.cell.2006.01.040 · Cited by 1,801
Mechanisms of Asymmetric Stem Cell Division
Knoblich, J. A. (2008) · Cell · doi:10.1016/j.cell.2008.02.007 · Cited by 1,057
Asymmetric cell divisions promote stratification and differentiation of mammalian skin
Lechler, T., & Fuchs, E. (2005) · Nature · doi:10.1038/nature03922 · Cited by 998
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Scratching the surface of skin development
Fuchs, E. (2007) · Nature · doi:10.1038/nature05659 · Cited by 930
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Rangarajan, A., Talora, C., Okuyama, R., Nicolas, M., Mammucari, C., Oh, H., Aster, J. C., Krishna, S., METZGER, D., Chambon, P., et al. (2001) · The EMBO Journal · doi:10.1093/emboj/20.13.3427 · Cited by 867
A single type of progenitor cell maintains normal epidermis
Clayton, E., Doupé, D. P., Klein, A. M., Winton, D. J., Simons, B. D., & Jones, P. H. (2007) · Nature · doi:10.1038/nature05574 · Cited by 853
Notch signaling controls multiple steps of pancreatic differentiation
Murtaugh, L. C., Stanger, B. Z., Kwan, K. M., & Melton, D. A. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2436557100 · Cited by 782
Asymmetric distribution of numb protein during division of the sensory organ precursor cell confers distinct fates to daughter cells
Rhyu, M. S., Jan, L. Y., & Jan, Y. N. (1994) · Cell · doi:10.1016/0092-8674(94)90112-0 · Cited by 770
The magical touch: genome targeting in epidermal stem cells induced by tamoxifen application to mouse skin.
Vasioukhin, V., Degenstein, L., Wise, B., & Fuchs, E. (1999) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.96.15.8551 · Cited by 691
Self-citation
Neuroepithelial progenitors undergo LGN-dependent planar divisions to maintain self-renewability during mammalian neurogenesis
Konno, D., Shioi, G., Shitamukai, A., Mori, A., Kiyonari, H., Miyata, T., & Matsuzaki, F. (2007) · Nature Cell Biology · doi:10.1038/ncb1673 · Cited by 534

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Xu, C., Xiao, G., ZHANG, B.-Z., Wang, M., Wang, J., Liu, D., Zhang, J., Ren, H., & Sun, X. (2018) · Gene Therapy · doi:10.1038/gt.2017.98 · Cited by 55
Oral keratinocyte stem/progenitor cells: specific markers, molecular signaling pathways and potential uses.
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Ying, Z., Sandoval, M., & Beronja, S. (2018) · Nature Cell Biology · doi:10.1038/s41556-018-0218-9 · Cited by 53
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Günschmann, C., Stachelscheid, H., Akyüz, M. D., Schmitz, A., Missero, C., Brüning, J. C., & Niessen, C. M. (2013) · Developmental Cell · doi:10.1016/j.devcel.2013.05.017 · Cited by 53
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Macara, I. G., & McCaffrey, L. M. (2013) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2013.0012 · Cited by 51
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Wen, W., & Zhang, M. (2017) · Journal of Molecular Biology · doi:10.1016/j.jmb.2017.09.013 · Cited by 53
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Luxenburg, C., & Zaidel‐Bar, R. (2019) · Experimental Cell Research · doi:10.1016/j.yexcr.2019.03.016 · Cited by 53
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Asymmetric Cell Divisions in the Epidermis
Poulson, N. D., & Lechler, T. (2012) · International review of cytology · doi:10.1016/b978-0-12-394306-4.00012-5 · Cited by 48
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Kranjec, C., Holleywood, C., Libert, D. M., Griffin, H. M., Mahmood, R., Isaacson, E. R., & Doorbar, J. (2017) · The Journal of Pathology · doi:10.1002/path.4917 · Cited by 48
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Blumer, J., Öner, Ş. S., & Lanier, S. M. (2011) · Acta Physiologica · doi:10.1111/j.1748-1716.2011.02327.x · Cited by 46
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Mey, J. D., & Freund, J. (2013) · Tissue Barriers · doi:10.4161/tisb.24965 · Cited by 49
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Magnusson, J. P., & Frisén, J. (2016) · Development · doi:10.1242/dev.133975 · Cited by 46
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Bañón‐Rodríguez, I., Gálvez-Santisteban, M., Vergarajauregui, S., Bosch‐Fortea, M., Borreguero-Pascual, A., & Martín‐Belmonte, F. (2014) · The EMBO Journal · doi:10.1002/embj.201385946 · Cited by 45
Divide and polarize: recent advances in the molecular mechanism regulating epithelial tubulogenesis
Rodriguez-Fraticelli, A., Gálvez-Santisteban, M., & Martín‐Belmonte, F. (2011) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2011.07.002 · Cited by 44
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Tame, M. A., Raaijmakers, J. A., van den Broek, B., Lindqvist, A., Jalink, K., & Medema, R. H. (2014) · Cell Cycle · doi:10.4161/cc.28031 · Cited by 43
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Sjöqvist, M., Antfolk, D., Ferraris, S. E., Rraklli, V., Haga, C., Antila, C., Mutvei, A. P., Imanishi, S. Y., Holmberg, J., Jin, S., et al. (2014) · Cell Research · doi:10.1038/cr.2014.34 · Cited by 42
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Zhou, C., Jiang, H., Zhang, Z., Zhang, G., Wang, H., Zhang, Q., Sun, P., Xiang, R., & Yang, S. (2017) · Oncotarget · doi:10.18632/oncotarget.17077 · Cited by 42
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Chiu, C. W. N., Monat, C., Robitaille, M., Lacomme, M., Daulat, A. M., MacLeod, G. D. A. H., McNeill, H., Cayouette, M., & Angers, S. (2016) · Developmental Cell · doi:10.1016/j.devcel.2015.12.016 · Cited by 36
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Analysis and modeling of mitotic spindle orientations in three dimensions
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Dainichi, T., Hayden, M. S., Park, S., Oh, H.-J., Seeley, J. J., Grinberg‐Bleyer, Y., Beck, K. M., Miyachi, Y., Kabashima, K., Hashimoto, T., et al. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.04.051 · Cited by 36
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Torii, T., Ogawa, Y., Liu, C., Ho, T. S., Hamdan, H., Wang, C.-C., Osés-Prieto, J. A., Burlingame, A. L., & Rasband, M. N. (2019) · The Journal of Cell Biology · doi:10.1083/jcb.201907048 · Cited by 37
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Dewey, E. B., Taylor, D. T., & Johnston, C. A. (2015) · Journal of Developmental Biology · doi:10.3390/jdb3040129 · Cited by 35
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Fiore, V. F., Almagro, J., & Fuchs, E. V. (2025) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-024-00821-0 · Cited by 36
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Li, J., Cheng, L., & Jiang, H. (2019) · Molecular Biology of the Cell · doi:10.1091/mbc.e19-04-0227 · Cited by 33
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Lough, K. J., Byrd, K. M., Descovich, C. P., Spitzer, D. C., Bergman, A. J., Beaudoin, G. M. J., Reichardt, L. F., & Williams, S. E. (2019) · eLife · doi:10.7554/elife.49249 · Cited by 31
Self-citation
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Xu, K., Wu, X., Shapiro, E., Huang, H., Zhang, L., Hickling, D. R., Deng, Y., Lee, P., Li, J., Lepor, H., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0029372 · Cited by 33
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Ali, N., Gomes, M., Bauer, R., Brodesser, S., Niemann, C., & Iden, S. (2016) · Journal of Investigative Dermatology · doi:10.1016/j.jid.2016.07.011 · Cited by 32
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RETRACTED ARTICLE: p53 destabilizing protein skews asymmetric division and enhances NOTCH activation to direct self-renewal of TICs
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Self-citation

Authors: Williams, S. E., Beronja, S., Pasolli, H. A., & Fuchs, E.
Affiliations: Howard Hughes Medical Institute (US)
Corresponding author: Fuchs, Elaine
ORCID: Williams, Scott E.
Beronja, Slobodan
Pasolli, H. Amalia
Fuchs, Elaine
Venue: Nature
Publisher: Springer Science and Business Media LLC
Published: 2011-02
Volume: 470
Issue: 7334
Pages: 353-358
ISSN: 0028-0836 (ISSN-L)
1476-4687
DOI: 10.1038/nature09793
PMC: PMC3077085
OpenAlex: W2038970717
Cited by: 406
References: 51
Citations by year: 2026: 9 · 2025: 13 · 2024: 8 · 2023: 13 · 2022: 14 · 2021: 24 · 2020: 32 · 2019: 31 · 2018: 26 · 2017: 21 · 2016: 36 · 2015: 29 · 2014: 35 · 2013: 36 · 2012: 45
FWCI: 19.37
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.springer.com/tdm (tdm)
Locations: Nature (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
RePEc: Research Papers in Economics (submittedVersion)
Funders: Howard Hughes Medical Institute
American Cancer Society
National Institutes of Health (2r01ar050452-21)
National Institute of Arthritis and Musculoskeletal and Skin Diseases (R01AR027883, R01 AR27883, R37AR027883, R01-AR050452)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Microtubule and mitosis dynamics
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Skin and Cellular Biology Research
Keywords: asymmetric cell division, Notch signaling, epidermal differentiation, epidermal stratification, spindle orientation, lateral geniculate nucleus, NUMA, dynactin, DCTN1, skin development, basal progenitor cells, cell polarity, skin barrier formation
MeSH terms: Dynactin Complex, Epidermal Cells, Animals, Carrier Proteins, Cell Differentiation, Cell Division, Cells, Cultured, Female, Male, Microtubule-Associated Proteins, Spindle Apparatus, Nuclear Proteins, Skin, Signal Transduction, Keratinocytes, Cell Cycle Proteins, Mice, Receptors, Notch, Gene Knockdown Techniques

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Asymmetric cell divisions promote Notch-dependent epidermal differentiation

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