Skip to main content
SpringerLink
Log in
Book cover

Lung Stem Cell Behavior pp 15–25Cite as

Signals and Molecular Mechanisms Controlling Lung Stem/Progenitor Cell Development and Behavior

  • Chapter
  • First Online:

  • 326 Accesses

Abstract

Better characterization and understanding of lung-specific stem cell behavior could lead to the discovery of new restoration solutions for normal and proper lung morphogenesis, repair, and regeneration. Recent data have accumulated on the behavior of these stem and progenitor cells such as self-renewal, fate, apoptosis, and differentiation into various cell types. Furthermore, many recent studies have focused on the modes of lung stem/progenitor cell division and the regulatory mechanisms of different aspects of lung stem/progenitor cell behavior, growth, and development. In this chapter, we describe recent advances on the factors, signals, and molecular mechanisms that control the self-renewing/proliferation, growth, and fate as well as differentiation of lung stem and progenitor cells.

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

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   84.99
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

Learn about institutional subscriptions

References

  • Abler, L. L., Mansour, S. L., & Sun, X. (2009). Conditional gene inactivation reveals roles for Fgf10 and Fgfr2 in establishing a normal pattern of epithelial branching in the mouse lung. Developmental Dynamics, 238, 1999–2013.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ameis, D., Khoshgoo, N., Iwasiow, B. M., Snarr, P., & Keijzer, R. (2017). MicroRNAs in lung development and disease. Paediatric Respiratory Reviews, 22, 38–43.

    Article  PubMed  Google Scholar 

  • Balasooriya, G., Goschorska, M., Piddini, E., & Rawlins, E. L. (2017). FGFR2 is required for airway basal cell self-renewal and terminal differentiation. Development, 144, 1600–1606.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Balasubramaniam, V., Mervis, C., Maxey, A., Markham, N., & Abman, S. H. (2007). Hyperoxia reduces bone marrow, circulating, and lung endothelial progenitor cells in the developing lung: Implications for the pathogenesis of bronchopulmonary dysplasia. American Journal of Physiology. Lung Cellular and Molecular Physiology, 292, L1073–L1084.

    Article  CAS  PubMed  Google Scholar 

  • Bellusci, S., Grindley, J., Emoto, H., Itoh, N., & Hogan, B. L. (1997). Fibroblast growth factor 10 (FGF10) and branching morphogenesis in the embryonic mouse lung. Development, 124(23), 4867–4878.

    PubMed  CAS  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 

  • Bhaskaran, M., Wang, Y., Zhang, H., et al. (2009). MicroRNA-127 modulates fetal lung development. Physiological Genomics, 37, 268–278.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Buckley, S., Driscoll, B., Anderson, K. D., & Warburton, D. (1997). Cell cycle in alveolar epithelial type II cells: Integration of Matrigel and KGF. The American Journal of Physiology, 273, L572–L580.

    Article  CAS  PubMed  Google Scholar 

  • Buckley, S., Barsky, L., Weinberg, K., & Warburton, D. (2005). In vivo inosine protects alveolar epithelial type 2 cells against hyperoxia-induced DNA damage through MAP kinase signaling. American Journal of Physiology. Lung Cellular and Molecular Physiology, 288, L569–L575.

    Article  CAS  PubMed  Google Scholar 

  • Carraro, G., El-Hashash, A., Guidolin, D., et al. (2009). miR-17 family of microRNAs controls FGF10-mediated embryonic lung epithelial branching morphogenesis through MAPK14 and STAT3 regulation of E-Cadherin distribution. Developmental Biology, 333, 238–250.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen, F., Desai, T. J., Qian, J., Niederreither, K., Lü, J., & Cardoso, W. V. (2007). Inhibition of Tgf beta signaling by endogenous retinoic acid is essential for primary lung bud induction. Development, 134, 2969–2979.

    Article  CAS  PubMed  Google Scholar 

  • Chuang, P. T., Kawcak, T., & McMahon, A. P. (2003). Feedback control of mammalian Hedgehog signaling by the Hedgehog-binding protein, Hip1, modulates Fgf signaling during branching morphogenesis of the lung. Genes & Development, 17, 342–347.

    Article  CAS  Google Scholar 

  • Colvin, J. S., White, A. C., Pratt, S. J., & Ornitz, D. M. (2001). Lung hypoplasia and neonatal death in Fgf9-null mice identify this gene as an essential regulator of lung mesenchyme. Development, 128(11), 2095–2106.

    PubMed  CAS  Google Scholar 

  • Croce, C. M. (2009). Causes and consequences of microRNA dysregulation in cancer. Nature Reviews. Genetics, 10(10), 704–714.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • De Langhe, S. P., Carraro, G., Tefft, D., et al. (2008). Formation and differentiation of multiple mesenchymal lineages during lung development is regulated by beta-catenin signaling. PLoS One, 3, e1516.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • del Moral, P. M., De Langhe, S. P., Sala, F. G., et al. (2006). Differential role of FGF9 on epithelium and mesenchyme in mouse embryonic lung. Developmental Biology, 293, 77–89.

    Article  CAS  PubMed  Google Scholar 

  • Ding, Y., Zhao, R., Zhao, X., Matthay, M. A., Nie, H. G., & Ji, H. L. (2017). ENaCs as both effectors and regulators of MiRNAs in lung epithelial development and regeneration. Cellular Physiology and Biochemistry, 44, 1120–1132.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eblaghie, M. C., Reedy, M., Oliver, T., Mishina, Y., & Hogan, B. L. (2006). Evidence that autocrine signaling through Bmpr1a regulates the proliferation, survival and morphogenetic behavior of distal lung epithelial cells. Developmental Biology, 291, 67–82.

    Article  CAS  PubMed  Google Scholar 

  • El Agha, E., Herold, S., Al Alam, D., et al. (2014). Fgf10-positive cells represent a progenitor cell population during lung development and postnatally. Development, 141, 296–306.

    Article  CAS  PubMed  PubMed Central  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. (2018). Intrinsic vs extrinsic intrinsic regulatory mechanisms of lung stem cell biology and behavior. Journal of Stem Cells, 12, 187–190.

    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 

  • Fan, T., Wang, W., Zhang, B., et al. (2016). Regulatory mechanisms of microRNAs in lung cancer stem cells. SpringerPlus, 5(1), 1762.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Frank, D. B., Peng, T., Zepp, J., et al. (2016). Emergence of a wave of Wnt signaling that regulates lung alveologenesis through controlling epithelial self-renewal and differentiation. Cell Reports, 17, 2312–2325.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gao, X., Vockley, C. M., Pauli, F., et al. (2013). Evidence for multiple roles for grainyheadlike 2 in the establishment and maintenance of human mucociliary airway epithelium. Proceedings of the National Academy of Sciences of the United States of America, 110, 9356–9351.

    Article  PubMed  PubMed Central  Google Scholar 

  • Goss, A. M., Tian, Y., Tsukiyama, T., et al. (2009). Wnt2/2b and beta-catenin signaling are necessary and sufficient to specify lung progenitors in the foregut. Developmental Cell, 17, 290–298.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goss, A. M., Tian, Y., Cheng, L., et al. (2011). Wnt2 signaling is necessary and sufficient to activate the airway smooth muscle program in the lung by regulating myocardin/Mrtf-B and Fgf10 expression. Developmental Biology, 356, 541–552.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gupte, V. V., Ramasamy, S. K., Reddy, R., et al. (2009). Overexpression of fibroblast growth factor-10 during both inflammatory and fibrotic phases attenuates bleomycin-induced pulmonary fibrosis in mice. American Journal of Respiratory and Critical Care Medicine, 180, 424–436.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Harris-Johnson, K. S., Domyan, E. T., Vezina, C. M., et al. (2009). beta-Catenin promotes respiratory progenitor identity in mouse foregut. Proceedings of the National Academy of Sciences of the United States of America, 106, 16287–16292.

    Article  PubMed  PubMed Central  Google Scholar 

  • Hsu, Y. C., Osinski, J., Campbell, C. E., et al. (2011). Mesenchymal nuclear factor I B regulates cell proliferation and epithelial differentiation during lung maturation. Developmental Biology, 354, 242–252.

    Article  CAS  PubMed  PubMed Central  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 

  • Kimura, S., Hara, Y., Pineau, T., et al. (1996). The T/ebp null mouse: Thyroid-specific enhancer-binding protein is essential for the organogenesis of the thyroid, lung, ventral forebrain, and pituitary. Genes & Development, 10, 60–69.

    Article  CAS  Google Scholar 

  • Kimura, S., Ward, J. M., & Minoo, P. (1999). Thyroid-specific enhancer-binding protein/thyroid transcription factor 1 is not required for the initial specification of the thyroid and lung primordia. Biochimie, 81, 321–327.

    Article  CAS  PubMed  Google Scholar 

  • Kugler, M. C., Joyner, A. L., Loomis, C. A., & Munger, J. S. (2015). Sonic hedgehog signaling in the lung. From development to disease. American Journal of Respiratory Cell and Molecular Biology., 52(1), 1–13.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Laresgoiti, U., Nikolić, M. Z., Rao, C., Brady, J. L., et al. (2016). Lung epithelial tip progenitors integrate glucocorticoid- and STAT3-mediated signals to control progeny fate. Development, 143, 3686–3699.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee, J.-H., Bhang, D. H., Beede, A., et al. (2014). Lung stem cell differentiation in mice directed by endothelial cells via a BMP4-NFATc1-thrombospondin-1 axis. Cell, 156, 440–455.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li, C., Xiao, J., Hormi, K., et al. (2002). Wnt5a participates in distal lung morphogenesis. Developmental Biology, 248, 68–81.

    Article  CAS  PubMed  Google Scholar 

  • Liu, Y., & Hogan, B. L. (2002). Differential gene expression in the distal tip endoderm of the embryonic mouse lung. Gene Expression Patterns, 2, 229–233.

    Article  CAS  PubMed  Google Scholar 

  • Lu, Y., Thomson, J. M., Wong, H. Y., Hammond, S. M., & Hogan, B. L. (2007). Transgenic over-expression of the microRNA miR-17-92 cluster promotes proliferation and inhibits differentiation of lung epithelial progenitor cells. Developmental Biology, 310, 442–453.

    Article  CAS  PubMed  PubMed Central  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 

  • Lu, J., & Clark, A. G. (2012). Impact of microRNA regulation on variation in human gene expression. Genome Research, 22(7), 1243–1254.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lüdtke, T. H., Farin, H. F., Rudat, C., et al. (2013). Tbx2 controls lung growth by direct repression of the cell cycle inhibitor genes Cdkn1a and Cdkn1b. PLoS Genetics, 9, e1003189.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miller, B. H., & Wahlestedt, C. (2010). MicroRNA dysregulation in psychiatric disease. Brain Research, 1338, 89–99.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mori, M., Mahoney, J. E., Stupnikov, M. R., et al. (2015). Notch3-Jagged signaling controls the pool of undifferentiated airway progenitors. Development, 142, 258–267.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Morimoto, M., Liu, Z., Cheng, H. T., et al. (2010). Canonical Notch signaling in the developing lung is required for determination of arterial smooth muscle cells and selection of Clara versus ciliated cell fate. Journal of Cell Science, 123, 213–224.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Morrisey, E. E., & Hogan, B. L. M. (2010). Preparing for the first breath: Genetic and cellular mechanisms in lung development. Developmental Cell, 18, 8–23.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nyeng, P., Norgaard, G. A., Kobberup, S., et al. (2008). FGF10 maintains distal lung bud epithelium and excessive signaling leads to progenitor state arrest, distalization, and goblet cell metaplasia. BMC Developmental Biology, 8, 2.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Okubo, T., Knoepfler, P. S., Eisenman, R. N., et al. (2005). N-myc plays an essential role during lung development as a dosage-sensitive regulator of progenitor cell proliferation and differentiation. Development, 132, 1363–1374.

    Article  CAS  PubMed  Google Scholar 

  • Oliver, J. R., Kushwah, R., Wu, J., et al. (2011). Elf3 plays a role in regulating bronchiolar epithelial repair kinetics following Clara cell-specific injury. Laboratory Investigation, 91, 1514–1529.

    Article  CAS  PubMed  Google Scholar 

  • Omran, A., Elimam, D., & Yin, F. (2013). MicroRNAs: New insights into chronic childhood diseases. BioMed Research International, 2013, 291826.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pandit, K. V., & Milosevic, J. (2015). MicroRNA regulatory networks in idiopathic pulmonary fibrosis. Biochemistry and Cell Biology, 93(2), 129–137.

    Article  CAS  PubMed  Google Scholar 

  • Pepicelli, C. V., Lewis, P. M., & McMahon, A. P. (1998). Sonic hedgehog regulates branching morphogenesis in the mammalian lung. Current Biology, 8, 1083–1086.

    Article  CAS  PubMed  Google Scholar 

  • Perl, A. K., Wert, S. E., Loudy, D. E., et al. (2005). Conditional recombination reveals distinct subsets of epithelial cells in trachea, bronchi, and alveoli. American Journal of Respiratory Cell and Molecular Biology, 33, v455–v462.

    Article  CAS  Google Scholar 

  • Plantier, L., Marchand-Adam, S., Antico Arciuch, V. G., et al. (2007). Keratinocyte growth factor protects against elastase-induced pulmonary emphysema in mice. American Journal of Physiology. Lung Cellular and Molecular Physiology, 293, L1230–L1239.

    Article  CAS  PubMed  Google Scholar 

  • Popova, A. P., Bentley, J. K., Anyanwu, A. C., et al. (2012). Glycogen synthase kinase-3ß/ß-catenin signaling regulates neonatal lung mesenchymal stromal cell myofibroblastic differentiation. American Journal of Physiology. Lung Cellular and Molecular Physiology, 303, L439–L438.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Que, J., Okubo, T., Goldenring, J. R., et al. (2007). Multiple dose-dependent roles for Sox2 in the patterning and differentiation of anterior foregut endoderm. Development, 134, 2521–2531.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Quiat, D., & Olson, E. N. (2013). MicroRNAs in cardiovascular disease: From pathogenesis to prevention and treatment. The Journal of Clinical Investigation, 123(1), 11–18.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ramasamy, S. K., Mailleux, A. A., Gupte, V. V., et al. (2007). Fgf10 dosage is critical for the amplification of epithelial cell progenitors and for the formation of multiple mesenchymal lineages during lung development. Developmental Biology, 307, 237–247.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ray, P., Devaux, Y., Stolz, D. B., et al. (2003). Inducible expression of keratinocyte growth factor (KGF) in mice inhibits lung epithelial cell death induced by hyperoxia. Proceedings of the National Academy of Sciences of the United States of America, 100, 6098–6103.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reinhart, B. J., Slack, F. J., Basson, M., Pasquinelli, A. E., Bettinger, J. C., Rougvie, A. E., Horvitz, H. R., & Ruvkun, G. (2000). The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans. Nature, 403(6772), 901–906.

    Article  CAS  PubMed  Google Scholar 

  • Rock, J. R., Onaitis, M. W., Rawlins, E. L., et al. (2009). Basal cells as stem cells of the mouse trachea and human airway epithelium. Proceedings of the National Academy of Sciences of the United States of America, 106, 12771–12775.

    Article  PubMed  PubMed Central  Google Scholar 

  • Rutter, M., Wang, J., Huang, Z., et al. (2010). Gli2 influences proliferation in the developing lung through regulation of cyclin expression. American Journal of Respiratory Cell and Molecular Biology, 42, 615–625.

    Article  CAS  PubMed  Google Scholar 

  • Sato, T., van Es, J. H., Snippert, H. J., et al. (2011a). Paneth cells constitute the niche for Lgr5 stem cells in intestinal crypts. Nature, 469, 415–418.

    Article  CAS  PubMed  Google Scholar 

  • Sato, T., Stange, D. E., Ferrante, M., et al. (2011b). Long-term expansion of epithelial organoids from human Colon, adenoma, adenocarcinoma, and Barrett’s epithelium. Gastroenterology, 141, 1762–1772.

    Article  CAS  PubMed  Google Scholar 

  • Sayed, D., & Abdellatif, M. (2011). MicroRNAs in development and disease. Physiological Reviews, 91(3), 827–887.

    Article  CAS  PubMed  Google Scholar 

  • Schittny, J. C. (2017). Development of the lung. Cell and Tissue Research, 367(3), 427–444.

    Article  PubMed  PubMed Central  Google Scholar 

  • Serls, A. E., Doherty, S., Parvatiyar, P., et al. (2005). Different thresholds of fibroblast growth factors pattern the ventral foregut into liver and lung. Development, 132, 35–47.

    Article  CAS  PubMed  Google Scholar 

  • Sgantzis, N., Yiakouvaki, A., Remboutsika, E., et al. (2011). HuR controls lung branching morphogenesis and mesenchymal FGF networks. Developmental Biology, 354, 267–279.

    Article  CAS  PubMed  Google Scholar 

  • Shu, W., Lu, M. M., Zhang, Y., et al. (2007). Foxp2 and Foxp1 cooperatively regulate lung and esophagus development. Development, 134, 1991–2000.

    Article  CAS  PubMed  Google Scholar 

  • Snitow, M., Lu, M., Cheng, L., et al. (2016). Ezh2 restricts the smooth muscle lineage during mouse lung mesothelial development. Development, 143, 3733–3741.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sountoulidis, A., Stavropoulos, A., Giaglis, S., et al. (2012). Activation of the canonical bone morphogenetic protein (BMP) pathway during lung morphogenesis and adult lung tissue repair. PLoS One, 7, e41460.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Spurlin, J. W., III, & Nelson, C. M. (2017). Building branched tissue structures: From single cell guidance to coordinated construction. Philosophical Transactions of the Royal Society B, 372, 20150527.

    Article  CAS  Google Scholar 

  • Stevens, T., Phan, S., Frid, M. G., et al. (2008). Lung vascular cell heterogeneity: Endothelium, smooth muscle, and fibroblasts. Proceedings of the American Thoracic Society, 5, 783–791.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Takahashi, Y., Izumi, Y., Kohno, M., et al. (2010). Thyroid transcription factor-1 influences the early phase of compensatory lung growth in adult mice. American Journal of Respiratory and Critical Care Medicine, 181, 1397–1406.

    Article  CAS  PubMed  Google Scholar 

  • Tefft, D., Lee, M., Smith, S., et al. (2002). mSprouty2 inhibits FGF10-activated MAP kinase by differentially binding to upstream target proteins. American Journal of Physiology. Lung Cellular and Molecular Physiology, 283, L700–L706.

    Article  CAS  PubMed  Google Scholar 

  • Tefft, D., De Langhe, S. P., Del Moral, P. M., et al. (2005). A novel function for the protein tyrosine phosphatase Shp2 during lung branching morphogenesis. Developmental Biology, 282, 422–431.

    Article  CAS  PubMed  Google Scholar 

  • Tian, Y., Zhang, Y., Hurd, L., Hannenhalli, S., Liu, F., Lu, M. M., & Morrisey, E. E. (2011). Regulation of lung endoderm progenitor cell behavior by miR302/367. Development, 138, 1235–1245.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tuder, R. M., & Yun, J. H. (2008). Vascular endothelial growth factor the lung: friend or foe. Current Opinion in Pharmacology, 8(3), 255–260 PMC. Web. 20 Feb. 2018.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Volckaert, T., Campbell, A., Dill, E., et al. (2013). Localized Fgf10 expression is not required for lung branching morphogenesis but prevents differentiation of epithelial progenitors. Development, 140, 3731–3742.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wan, H., Dingle, S., Xu, Y., et al. (2005). Compensatory roles of Foxa1 and Foxa2 during lung morphogenesis. The Journal of Biological Chemistry, 280, 13809–13816.

    Article  CAS  PubMed  Google Scholar 

  • Wang, Y., Tian, Y., Morley, M. P., et al. (2013). Development and regeneration of Sox2+ endoderm progenitors are regulated by a Hdac1/2- Bmp4/Rb1 regulatory pathway. Developmental Cell, 24, 345–358.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang, X., Wang, Y., Snitow, M. E., et al. (2016). Expression of histone deacetylase 3 instructs alveolar type I cell differentiation by regulating a Wnt signaling niche in the lung. Developmental Biology, 414, 161–169.

    Article  CAS  PubMed  PubMed Central  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., 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 

  • Watson, J. K., Rulands, S., Wilkinson, A. C., et al. (2015). Clonal dynamics reveal two distinct populations of basal cells in slow-turnover airway epithelium. Cell Reports, 12, 90–101.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Weaver, M., Yingling, J. M., Dunn, N. R., et al. (1999). Bmp signaling regulates proximal-distal differentiation of endoderm in mouse lung development. Development, 126, 4005–4015.

    PubMed  CAS  Google Scholar 

  • Yin, Y., Wang, F., & Ornitz, D. M. (2011). Mesothelial- and epithelial-derived FGF9 have distinct functions in the regulation of lung development. Development, 138, 3169–3177.

    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). Signals and Molecular Mechanisms Controlling Lung Stem/Progenitor Cell Development and Behavior. In: Lung Stem Cell Behavior. Springer, Cham. https://doi.org/10.1007/978-3-319-95279-6_3

Download citation

Publish with us

Policies and ethics

Search

Navigation