Skip to main content
SpringerLink
Log in

Interaction of Epithelial Cells and Basement Membrane in the Regulation of EMT Exemplified in Chicken Embryo Gastrulation

  • Chapter
  • First Online:
New Principles in Developmental Processes

  • 985 Accesses

Abstract

Epithelial–mesenchymal transition (EMT) is a process in which epithelial cells are converted into mesenchymal cells. It plays crucial roles in the formation of complex organs and in tissue repair during animal development. After EMT, cells acquire migratory and invasive properties, which can contribute to organ fibrosis and cancer metastasis. However, the precise cellular mechanisms that govern EMT in various in vivo contexts are poorly understood. Gastrulation is a process through which the three embryonic germ layers are formed. During this process, epithelial cells in the epiblast layer dynamically change their shape and ingress through the primitive streak to become mesoderm or endoderm. EMT occurs during this gastrulation process, and in this chapter, I describe the key principles of EMT and characterize EMT in the primitive streak during chicken gastrulation. Gastrulation EMT is a multistep process that includes the dissociation of cell–cell contact, the loss of epithelial polarity, and the degradation of the basement membrane (BM). Our recent studies indicate that epiblast/BM interaction requires basally localized RhoA activity, and CLASP- and dystroglycan-mediated cortical microtubule anchoring, the disruption of which causes BM degradation during gastrulation EMT.

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

Access this chapter

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 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
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

  • Acloque H, Adams MS, Fishwick K, Bronner-Fraser M, Nieto MA (2009) Epithelial–mesenchymal transitions: the importance of changing cell state in development and disease. J Clin Invest 119(6):1438–1449. doi:10.1172/JCI38019, pii: 38019

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Akhmanova A, Stehbens SJ, Yap AS (2009) Touch, grasp, deliver and control: functional cross-talk between microtubules and cell adhesions. Traffic 10(3):268–274. doi:10.1111/j.1600-0854.2008.00869.x, pii: TRA869

    Article  CAS  PubMed  Google Scholar 

  • Alev C, Wu Y, Kasukawa T, Jakt LM, Ueda HR, Sheng G (2010) Transcriptomic landscape of the primitive streak. Development (Camb) 137(17):2863–2874. doi:10.1242/dev.053462, pii: dev.053462

    Article  CAS  Google Scholar 

  • Bacallao R, Antony C, Dotti C, Karsenti E, Stelzer EH, Simons K (1989) The subcellular organization of Madin-Darby canine kidney cells during the formation of a polarized epithelium. J Cell Biol 109(6 Pt 1):2817–2832

    Article  CAS  PubMed  Google Scholar 

  • Bortier H, Callebaut M, van Nueten E, Vakaet L (2001) Autoradiographic evidence for the sliding of the upper layer over the basement membrane in chicken blastoderms during gastrulation. Eur J Morphol 39(2):91–98

    Article  CAS  PubMed  Google Scholar 

  • Cao X, Surma MA, Simons K (2012) Polarized sorting and trafficking in epithelial cells. Cell Res 22(5):793–805. doi:10.1038/cr.2012.64, pii: cr201264

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Chuai M, Hughes D, Weijer CJ (2012) Collective epithelial and mesenchymal cell migration during gastrulation. Curr Genomics 13(4):267–277. doi:10.2174/138920212800793357, pii: CG-13-267

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • De Craene B, Berx G (2013) Regulatory networks defining EMT during cancer initiation and progression. Nat Rev Cancer 13(2):97–110. doi:10.1038/nrc3447, pii: nrc3447

    Article  PubMed  Google Scholar 

  • England MA, Wakely J (1977) Scanning electron microscopy of the development of the mesoderm layer in chick embryos. Anat Embryol (Berl) 150(3):291–300

    Article  CAS  Google Scholar 

  • Fuse T, Kanai Y, Kanai-Azuma M, Suzuki M, Nakamura K, Mori H, Hayashi Y, Mishina M (2004) Conditional activation of RhoA suppresses the epithelial to mesenchymal transition at the primitive streak during mouse gastrulation. Biochem Biophys Res Commun 318(3):665–672. doi:10.1016/j.bbrc.2004.04.076, pii: S0006291X04007934

    Article  CAS  PubMed  Google Scholar 

  • Hardy KM, Yatskievych TA, Konieczka J, Bobbs AS, Antin PB (2011) FGF signalling through RAS/MAPK and PI3K pathways regulates cell movement and gene expression in the chicken primitive streak without affecting E-cadherin expression. BMC Dev Biol 11:20. doi:10.1186/1471-213X-11-20, pii: 1471-213X-11-20

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hay ED (1968) Organization and fine structure of epithelium and mesenchyme in the developing chick embryo. In: Epithelial–mesenchymal interactions. 18th Hahnemann symposium. Williams & Wilkins, Baltimore

    Google Scholar 

  • Hay ED (2005) The mesenchymal cell, its role in the embryo, and the remarkable signaling mechanisms that create it. Dev Dyn 233(3):706–720. doi:10.1002/dvdy.20345

    Article  CAS  PubMed  Google Scholar 

  • Hugo H, Ackland ML, Blick T, Lawrence MG, Clements JA, Williams ED, Thompson EW (2007) Epithelial–mesenchymal and mesenchymal–epithelial transitions in carcinoma progression. J Cell Physiol 213(2):374–383. doi:10.1002/jcp.21223

    Article  CAS  PubMed  Google Scholar 

  • Jaffe AB, Hall A (2005) Rho GTPases: biochemistry and biology. Annu Rev Cell Dev Biol 21:247–269. doi:10.1146/annurev.cellbio.21.020604.150721

    Article  CAS  PubMed  Google Scholar 

  • Lawson A, Schoenwolf GC (2001) Cell populations and morphogenetic movements underlying formation of the avian primitive streak and organizer. Genesis 29(4):188–195. doi:10.1002/gene.1023

    Article  CAS  PubMed  Google Scholar 

  • Lim J, Thiery JP (2012) Epithelial–mesenchymal transitions: insights from development. Development (Camb) 139(19):3471–3486. doi:10.1242/dev.071209, pii: 139/19/3471

    Article  CAS  Google Scholar 

  • Lopez-Novoa JM, Nieto MA (2009) Inflammation and EMT: an alliance towards organ fibrosis and cancer progression. EMBO Mol Med 1(6–7):303–314. doi:10.1002/emmm.200900043

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Mani SA, Guo W, Liao MJ, Eaton EN, Ayyanan A, Zhou AY, Brooks M, Reinhard F, Zhang CC, Shipitsin M, Campbell LL, Polyak K, Brisken C, Yang J, Weinberg RA (2008) The epithelial–mesenchymal transition generates cells with properties of stem cells. Cell 133(4):704–715. doi:10.1016/j.cell.2008.03.027, pii: S0092-8674(08)00444-3

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Mimori-Kiyosue Y (2011) Shaping microtubules into diverse patterns: molecular connections for setting up both ends. Cytoskeleton (Hoboken) 68(11):603–618. doi:10.1002/cm.20540

    Article  CAS  Google Scholar 

  • Nakaya Y, Sheng G (2008) Epithelial to mesenchymal transition during gastrulation: an embryological view. Dev Growth Differ 50(9):755–766. doi:10.1111/j.1440-169X.2008.01070.x, pii: DGD1070

    Article  CAS  PubMed  Google Scholar 

  • Nakaya Y, Sheng G (2009) An amicable separation: chick’s way of doing EMT. Cell Adh Migr 3(2):160–163, pii: 7373

    Article  PubMed Central  PubMed  Google Scholar 

  • Nakaya Y, Sheng G (2013) EMT in developmental morphogenesis. Cancer Lett. doi:10.1016/j.canlet.2013.02.037; pii: S0304-3835(13)00163-8

  • Nakaya Y, Kuroda S, Katagiri YT, Kaibuchi K, Takahashi Y (2004) Mesenchymal–epithelial transition during somitic segmentation is regulated by differential roles of Cdc42 and Rac1. Dev Cell 7(3):425–438. doi:10.1016/j.devcel.2004.08.003, pii: S1534580704002783

    Article  CAS  PubMed  Google Scholar 

  • Nakaya Y, Sukowati EW, Wu Y, Sheng G (2008) RhoA and microtubule dynamics control cell-basement membrane interaction in EMT during gastrulation. Nat Cell Biol 10(7):765–775. doi:10.1038/ncb1739, pii: ncb1739

    Article  CAS  PubMed  Google Scholar 

  • Nakaya Y, Sukowati EW, Alev C, Nakazawa F, Sheng G (2011) Involvement of dystroglycan in epithelial–mesenchymal transition during chick gastrulation. Cells Tissues Organs 193(1–2):64–73. doi:10.1159/000320165, pii: 000320165

    Article  CAS  PubMed  Google Scholar 

  • Nakaya Y, Sukowati EW, Sheng G (2013) Epiblast integrity requires CLASP and dystroglycan-mediated microtubule anchoring to basal cortex. J Cell Biol 202(4):637–651

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ozdamar B, Bose R, Barrios-Rodiles M, Wang HR, Zhang Y, Wrana JL (2005) Regulation of the polarity protein Par6 by TGF-beta receptors controls epithelial cell plasticity. Science 307(5715):1603–1609. doi:10.1126/science.1105718, pii: 307/5715/1603

    Article  CAS  PubMed  Google Scholar 

  • Polyak K, Weinberg RA (2009) Transitions between epithelial and mesenchymal states: acquisition of malignant and stem cell traits. Nat Rev Cancer 9(4):265–273. doi:10.1038/nrc2620, pii: nrc2620

    Article  CAS  PubMed  Google Scholar 

  • Rohde LA, Heisenberg CP (2007) Zebrafish gastrulation: cell movements, signals, and mechanisms. Int Rev Cytol 261:159–192. doi:10.1016/S0074-7696(07)61004-3, pii: S0074-7696(07)61004-3

    Article  CAS  PubMed  Google Scholar 

  • Schoenenberger CA, Matlin KS (1991) Cell polarity and epithelial oncogenesis. Trends Cell Biol 1(4):87–92, pii: 0962892491900358

    Article  CAS  PubMed  Google Scholar 

  • Shook D, Keller R (2003) Mechanisms, mechanics and function of epithelial–mesenchymal transitions in early development. Mech Dev 120(11):1351–1383, pii: S0925477303002090

    Article  CAS  PubMed  Google Scholar 

  • Solnica-Krezel L, Sepich DS (2012) Gastrulation: making and shaping germ layers. Annu Rev Cell Dev Biol 28:687–717. doi:10.1146/annurev-cellbio-092910-154043

    Article  CAS  PubMed  Google Scholar 

  • Solursh M, Revel JP (1978) A scanning electron microscope study of cell shape and cell appendages in the primitive streak region of the rat and chick embryo. Differentiation 11(3):185–190

    Article  CAS  PubMed  Google Scholar 

  • Takahashi Y, Sato Y, Suetsugu R, Nakaya Y (2005) Mesenchymal-to-epithelial transition during somitic segmentation: a novel approach to studying the roles of Rho family GTPases in morphogenesis. Cells Tissues Organs 179(1–2):36–42. doi:10.1159/000084507, pii: 84507

    Article  CAS  PubMed  Google Scholar 

  • Thiery JP, Acloque H, Huang RY, Nieto MA (2009) Epithelial–mesenchymal transitions in development and disease. Cell 139(5):871–890. doi:10.1016/j.cell.2009.11.007, pii: S0092-8674(09)01419-6

    Article  CAS  PubMed  Google Scholar 

  • Van Aelst L, Symons M (2002) Role of Rho family GTPases in epithelial morphogenesis. Genes Dev 16(9):1032–1054. doi:10.1101/gad.978802

    Article  PubMed  Google Scholar 

  • Wakely J, England MA (1977) Scanning electron microscopy (SEM) of the chick embryo primitive streak. Differentiation 7(3):181–186

    Article  CAS  PubMed  Google Scholar 

  • Yeaman C, Grindstaff KK, Nelson WJ (1999) New perspectives on mechanisms involved in generating epithelial cell polarity. Physiol Rev 79(1):73–98

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This study was carried out in the laboratory of Dr. Guojun Sheng at RIKEN CDB. I thank Ms. Erike W. Sukowati for supporting most of the experiments and also thank Ms. Hazuki Hiraga and Dr. Guojun Sheng for corrections and critical comments on the manuscript.

Author information

Authors and Affiliations

  1. Lab for Early Embryogenesis, RIKEN Center for Developmental Biology, Kobe, Japan

    Yukiko Nakaya

Authors
  1. Yukiko Nakaya
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yukiko Nakaya .

Editor information

Editors and Affiliations

  1. Graduate School of Frontier Biosciences, Osaka University, Osaka, Japan

    Hisato Kondoh

  2. Graduate School Science, Nagoya University, Nagoya, Japan

    Atsushi Kuroiwa

Rights and permissions

Reprints and permissions

Copyright information

© 2014 Springer Japan

About this chapter

Cite this chapter

Nakaya, Y. (2014). Interaction of Epithelial Cells and Basement Membrane in the Regulation of EMT Exemplified in Chicken Embryo Gastrulation. In: Kondoh, H., Kuroiwa, A. (eds) New Principles in Developmental Processes. Springer, Tokyo. https://doi.org/10.1007/978-4-431-54634-4_9

Download citation

Publish with us

Policies and ethics

Search

Navigation