Skip to main content
SpringerLink
Log in

Mode of Cell Division as a Regulatory Mechanism for Lung Stem Cell Behavior Compared to Other Systems

  • Chapter
  • First Online:
Lung Stem Cell Behavior

  • 326 Accesses

Abstract

Over the last decade, new insights have been accumulated on the cell fate, behavior, and mode of division of stem/progenitor cells in the respiratory system and many other systems. The balance between symmetric and asymmetric divisions of tissue-specific stem cells is essential for proper organ formation, development, function, and repair/regeneration and, therefore, is tightly controlled. Improper asymmetric cell division can disrupt the tightly regulated morphogenesis of organs, while uncontrolled symmetrical cell division can promote tumor formation. In this chapter, we describe recently accumulated data on the division mode (symmetric vs. asymmetric) of lung stem/progenitor cells. In addition, we describe and compare these division modes and their regulatory mechanisms between the lung and other tissue-specific stem cells in mammals and other organisms, in which these processes are well investigated.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
eBook
USD 16.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 109.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 109.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Ajduk, A., & Zernicka-Goetz, M. (2016). Polarity and cell division orientation in the cleavage embryo: from worm to human. Molecular Human Reproduction, 22, 691–703.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Alexson, T. O., Hitoshi, S., Coles, B., Bernstein, A., & van der Kooy, D. (2006). Notch signaling is required to maintain all neural stem cell populations–irrespective of spatial or temporal niche. Developmental Neuroscience, 28, 34–48.

    Article  CAS  PubMed  Google Scholar 

  • Berdnik, D., Török, T., González-Gaitán, M., & Knoblich, J. A. (2002). The endocytic protein alpha-Adaptin is required for numb-mediated asymmetric cell division in Drosophila. Developmental Cell, 3, 221–231.

    Article  CAS  PubMed  Google Scholar 

  • Berika, M., Elgayyar, M., & El-Hashash, A. H. (2014). Asymmetric cell divisions of stem cells in the lung and other systems. Frontiers in Cell and Development Biology, 2, 33–42.

    Article  Google Scholar 

  • Berika, M., Ku, J., Huang, H., & El-Hashash, A. H. (2016). Gene and signals regulating stem cell fate. In A. El-Hashash (Ed.), Developmental and stem cell biology in health and disease (pp. 36–48). Madison: Bentham Science Publisher, USA.

    Chapter  Google Scholar 

  • Betschinger, J., & Knoblich, J. A. (2004). Dare to be different: Asymmetric cell division in Drosophila, C. elegans and vertebrates. Current Biology, 14, R674–R685.

    Article  CAS  PubMed  Google Scholar 

  • Boitano, S., Safdar, Z., Welsh, D., Bhattacharya, J., & Koval, M. (2004). Cell-cell interactions in regulating lung function. American Journal of Physiology. Lung Cellular and Molecular Physiology, 287, L455–L459.

    Article  CAS  PubMed  Google Scholar 

  • Cayouette, M., & Raff, M. (2002). Asymmetric segregation of Numb: A mechanism for neural specification from Drosophila to mammals. Nature Neuroscience, 5, 1265–1269.

    Article  CAS  PubMed  Google Scholar 

  • Cayouette, M., & Raff, M. (2003). The orientation of cell division influences cell-fate choice in the developing mammalian retina. Development, 130, 2329–2339.

    Article  CAS  PubMed  Google Scholar 

  • Chen, K., Huang, Y., & Chen, J. (2013). Understanding and targeting cancer stem cells: Therapeutic implications and challenges. Acta Pharmacologica Sinica, 34, 732–740.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen, C., Fingerhut, J. M., & Yamashita, Y. M. (2016). The ins(ide) and outs(ide) of asymmetric stem cell division. Current Opinion in Cell Biology, 43, 1–6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Daynac, M., & Petritsch, C. K. (2017). Regulation of asymmetric cell division in mammalian neural stem and cancer precursor cells. In J. P. Tassan & J. Kubiak (Eds.), Asymmetric cell division in development, differentiation and cancer. Results and problems in cell differentiation (Vol. 61). Cham: Springer.

    Google Scholar 

  • Dewey, E. B., Taylor, D. T., & Johnston, C. A. (2015). Cell fate decision making through oriented cell division. Journal of Developmental Biology, 3, 129–157.

    Article  CAS  PubMed  Google Scholar 

  • Doe, C. Q. (2008). Neural stem cells: Balancing self-renewal with differentiation. Development, 135, 1575–1587.

    Article  CAS  PubMed  Google Scholar 

  • Drummond, M. L., & Prehoda, K. E. (2016). Molecular control of atypical Protein Kinase C: Tipping the balance between self-renewal and differentiation. Journal of Molecular Biology, 428, 1455–1464.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Duncan, A. W., Rattis, F. M., DiMascio, L. N., et al. (2005). Integration of Notch and Wnt signaling in hematopoietic stem cell maintenance. Nature Immunology, 6, 314–322.

    Article  CAS  PubMed  Google Scholar 

  • El-Hashash, A. H. (2013). Lung stem cells: Mechanisms of behavior, development and regeneration. Anatomy and Physiology, 3, 119–128.

    Article  Google Scholar 

  • El-Hashash, A. H. (2015). Asymmetric cell divisions of stem/progenitor cells. In D. David Warburton (Ed.), Stem cells, tissue engineering and regenerative medicine (pp. 41–58). New Jersey: World Scientific Publishing.

    Chapter  Google Scholar 

  • El-Hashash, A. H., & Warburton, D. (2011). Cell polarity and spindle orientation in the distal epithelium of embryonic lung. Developmental Dynamics, 240, 441–445.

    Article  PubMed  PubMed Central  Google Scholar 

  • El-Hashash, A. H., & Warburton, D. (2012). Numb expression and asymmetric versus symmetric cell division in embryonic distal lung epithelium. Journal of Histochemistry and Cytochemistry, 60, 675–682.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • El-Hashash, A., Turcatel, G., Alam, D., Buckley, S., Bellusci, S., & Warburton, D. (2011c). Eya1 controls cell polarity, spindle orientation, cell fate and Notch signaling in distal embryonic lung epithelium. Development, 138, 1395–1407.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Elshahawy, S., Ibrahim, A., Soliman, S., Berika, M., & El-Hashash, A. H. (2016). Behavior and asymmetric cell divisions of stem cells. In A. El-Hashash (Ed.), Developmental and stem cell biology in health and disease (pp. 81–104). Madison: Bentham Science Publisher, USA.

    Google Scholar 

  • Florian, M. C., & Geiger, H. (2010). Concise review: Polarity in stem cells, disease, and aging. Stem Cells (Dayton, Ohio), 28(9), 1623–1629.

    Article  Google Scholar 

  • Frise, E., Knoblich, J. A., Younger-Shepherd, S., et al. (1996). The Drosophila Numb protein inhibits signaling of the Notch receptor during cell-cell interaction in sensory organ lineage. Proceedings of the National Academy of Sciences of the United States of America, 93, 11925–11932.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fu, Y., Li, H., & Hao, X. (2017). The self-renewal signaling pathways utilized by gastric cancer stem cells. Tumor Biology, 1–7.

    Google Scholar 

  • Giebel, B., & Wodarz, A. (2012). Notch signaling: Numb makes the difference. Curr Biol, 22, R133–R135.

    Article  CAS  PubMed  Google Scholar 

  • Goldstein, B., & Macara, I. G. (2007). The PAR proteins: Fundamental players in animal cell polarization. Developmental Cell, 13, 609–622.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gómez-López, S., Lerner, R. G., & Petritsch, C. (2014). Asymmetric cell division of stem and progenitor cells during homeostasis and cancer. Cellular and Molecular Life Sciences, 71, 575–597.

    Article  CAS  PubMed  Google Scholar 

  • Gulino, A., Di Marcotullio, L., & Screpanti, I. (2010). The multiple functions of Numb. Experimental Cell Research, 316, 900–906.

    Article  CAS  PubMed  Google Scholar 

  • Guo, M., Jan, L. Y., & Jan, Y. N. (1996). Control of daughter cell fates during asymmetric division: Interaction of Numb and Notch. Neuron, 17, 27–41.

    Article  PubMed  Google Scholar 

  • Haydar, T. F., Ang, E., Jr., & Rakic, P. (2003). Mitotic spindle rotation and mode of cell division in the developing telencephalon. Proceedings of the National Academy of Sciences of the United States of America, 100, 2890–2895.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Homem, C. C., & Knoblich, J. A. (2012). Drosophila neuroblasts: A model for stem cell biology. Development, 139, 4297–4310.

    Article  CAS  PubMed  Google Scholar 

  • Huttner, W. B., & Kosodo, Y. (2005). Symmetric versus asymmetric cell division during neurogenesis in the developing vertebrate central nervous system. Current Opinion in Cell Biology, 17, 648–657.

    Article  CAS  PubMed  Google Scholar 

  • Ibrahim, A., & El-Hashash, A. H. (2015). Lung stem cell behavior in development and regeneration. Edorium Journal of Stem Cell Research and Therapy, 1, 1–13.

    Google Scholar 

  • Juven-Gershon, T., Shifman, O., Unger, T., et al. (1998). The Mdm2 oncoprotein interacts with the cell fate regulator Numb. Molecular and Cellular Biology, 18, 3974–3982.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Knoblich, J. A. (2001). Asymmetric cell division during animal development. Nature Reviews. Molecular Cell Biology, 2, 11–20.

    Article  CAS  PubMed  Google Scholar 

  • Knoblich, J. A. (2010). Asymmetric cell division: Recent developments and their implications for tumour biology. Nature Reviews. Molecular Cell Biology, 11, 849–860.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kosodo, Y., Röper, K., Haubensak, W., et al. (2004). Asymmetric distribution of the apical plasma membrane during neurogenic divisions of mammalian neuroepithelial cells. The EMBO Journal, 23, 2314–2324.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ku, J., & El-Hashash, A. H. (2016). Molecular control of the mode of cell division: A view from mammalian lung epithelial stem cells. A Journal of Anatomy, 3, 3–6.

    Google Scholar 

  • Lechler, T., & Fuchs, E. (2005). Asymmetric cell divisions promote stratification and differentiation of mammalian skin. Nature, 437, 275–280.

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu, K., Lin, Q., Wei, Y., et al. (2015). Gαs regulates asymmetric cell division of cortical progenitors by controlling Numb mediated Notch signaling suppression. Neuroscience Letters, 597, 97–103.

    Article  CAS  PubMed  Google Scholar 

  • Lu, Y., Okubo, T., Rawlins, E., et al. (2008). Epithelial progenitor cells of the embryonic lung and the role of microRNAs in their proliferation. Proceedings of the American Thoracic Society, 5, 300–304.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nelson, W. J. (2003a). Epithelial cell polarity from the outside looking in. News in Physiological Sciences, 18, 143–146.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Nelson, W. J. (2003b). Adaptation of core mechanisms to generate cell polarity. Nature, 422, 766–774.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Noctor, S. C., Martínez-Cerdeño, V., Ivic, L., et al. (2004). Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases. Nature Neuroscience, 7, 136–144.

    Article  CAS  PubMed  Google Scholar 

  • Overeem, A. W., Bryant, D. M., & van IJzendoorn, S. C. (2015). Mechanisms of apical-basal axis orientation and epithelial lumen positioning. Trends in Cell Biology, 25, 476–485.

    Article  CAS  PubMed  Google Scholar 

  • Pece, S., Confalonieri, S. R., Romano, P., et al. (2011). NUMB-ing down cancer by more than just a NOTCH. Biochimica et Biophysica Acta, 1815, 26–43.

    PubMed  CAS  Google Scholar 

  • Peng, Y., & Axelrod, J. D. (2012). Asymmetric protein localization in planar cell polarity: Mechanisms, puzzles and challenges. Current Topics in Developmental Biology, 101, 33–53.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rawlins, E. L. (2008). Lung epithelial progenitor cells: Lessons from development. Proceedings of the American Thoracic Society, 5, 675–681.

    Article  PubMed  PubMed Central  Google Scholar 

  • Rawlins, E. L., & Hogan, B. L. (2006). Epithelial stem cells of the lung: Privileged few or opportunities for many? Development, 133, 2455–2465.

    Article  CAS  PubMed  Google Scholar 

  • Rawlins, E. L., Clark, C. P., Xue, Y., et al. (2009a). The Id2+ distal tip lung epithelium contains individual multipotent embryonic progenitor cells. Development, 136, 3741–3745.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rawlins, E. L., Okubo, T., Xue, Y., et al. (2009b). The role of Scgb1a1+ Clara cells in the long-term maintenance and repair of lung airway, but not alveolar, epithelium. Cell Stem Cell, 4, 525–534.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Roignot, J., Peng, X., & Mostov, K. (2013). Polarity in mammalian epithelial morphogenesis. Cold Spring Harbor Perspectives in Biology, 5, a013789.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shi, W., Xu, J., & Warburton, D. (2009). Development, repair and fibrosis: What is common and why it matters. Respirology, 14, 656–655.

    Article  PubMed  PubMed Central  Google Scholar 

  • Shinin, V., Gayraud-Morel, B., Gomes, D., & Tajbakhsh, S. (2006). Asymmetric division and cosegregation of template DNA strands in adult muscle satellite cells. Nature Cell Biology, 8, 677–687.

    Article  CAS  PubMed  Google Scholar 

  • Tepass, U. (2012). The apical polarity protein network in Drosophila epithelial cells: Regulation of polarity, junctions, morphogenesis, cell growth, and survival. Annual Review of Cell and Developmental Biology, 28, 655–685.

    Article  CAS  PubMed  Google Scholar 

  • Tuncay, H., & Ebnet, K. (2016). Cell adhesion molecule control of planar spindle orientation. Cellular and Molecular Life Sciences, 73, 1195–1207.

    Article  CAS  PubMed  Google Scholar 

  • Vorhagen, S., & Niessen, C. M. (2014). Mammalian aPKC/Par polarity complex mediated regulation of epithelial division orientation and cell fate. Experimental Cell Research, 328, 296–302.

    Article  CAS  PubMed  Google Scholar 

  • Wang, C., Chang, K. C., Somers, G., et al. (2009). Protein phosphatase 2A regulates self-renewal of Drosophila neural stem cells. Development, 136, 2287–2296.

    Article  CAS  PubMed  Google Scholar 

  • Warburton, D. (2008). Developmental biology: Order in the lung. Nature, 453, 73–75.

    Article  CAS  Google Scholar 

  • Warburton, D., Schwarz, M., Tefft, D., et al. (2000). The molecular basis of lung morphogenesis. Mech Dev, 92, 55–81.

    Article  CAS  PubMed  Google Scholar 

  • Warburton, D., Perin, L., Defilippo, R., et al. (2008). Stem/progenitor cells in lung development, injury repair, and regeneration. Proceedings of the American Thoracic Society, 5, 703–706.

    Article  PubMed  PubMed Central  Google Scholar 

  • Warburton, D., El-Hashash, A., Carraro, G., et al. (2010). Lung organogenesis. Current Topics in Developmental Biology, 90, 73–158.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wodarz, A. (2002). Establishing cell polarity in development. Nature Cell Biology, 4, E39–E44.

    Article  CAS  PubMed  Google Scholar 

  • Woods, D. F., Wu, J. W., & Bryant, P. J. (1997). Localization of proteins to the apico-lateral junctions of Drosophila epithelia. Developmental Genetics, 20, 111–118.

    Article  CAS  PubMed  Google Scholar 

  • Yamashita, Y. M., Yuan, H., Cheng, J., et al. (2010). Polarity in stem cell division: Asymmetric stem cell division in tissue homeostasis. Cold Spring Harbor Perspectives in Biology, 2, a001313.

    Article  PubMed  PubMed Central  Google Scholar 

  • Yan, B., Omar, F. M., Das, K., et al. (2008). Characterization of Numb expression in astrocytomas. Neuropathology, 28, 479–484.

    Article  PubMed  Google Scholar 

  • Yang, S., Ma, K., Geng, Z., et al. (2015). Oriented cell division: New roles in guiding skin wound repair and regeneration. Bioscience Reports, 35, 6.

    Article  CAS  Google Scholar 

  • Zhou, Q., Law, A. C., Rajagopal, J., et al. (2007). A multipotent progenitor domain guides pancreatic organogenesis. Developmental Cell, 13, 103–114.

    Article  CAS  PubMed  Google Scholar 

  • Zimdahl, B., Ito, T., Blevins, A., et al. (2014). Lis1 regulates asymmetric division in hematopoietic stem cells and in leukemia. Nature Genetics, 46, 245–252.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. The University of Edinburgh-Zhejiang International campus (UoE-ZJU Institute), and Centre of Stem Cell and Regenerative Medicine Schools of Medicine & Basic Medicine, Zhejiang University, Haining, Zhejiang, China

    Ahmed El-Hashash

Authors
  1. Ahmed El-Hashash
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

Copyright information

© 2018 Springer International Publishing AG, part of Springer Nature

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

El-Hashash, A. (2018). Mode of Cell Division as a Regulatory Mechanism for Lung Stem Cell Behavior Compared to Other Systems. In: Lung Stem Cell Behavior. Springer, Cham. https://doi.org/10.1007/978-3-319-95279-6_5

Download citation

Publish with us

Policies and ethics

Search

Navigation