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Cell adhesion properties of neural stem cells in the chick embryo

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Abstract

The nervous system of vertebrates is derived from an early embryonic region referred to as the neural plate. In the chick embryo, the neural plate is populated by neural stem cells specified from the epiblast shortly after the onset of gastrulation. Accompanying the formation of the plate, chondroitin sulfate glycosaminoglycans are expressed in the basal extracellular matrix. We describe in vitro experiments measuring cell adhesion of epiblast cells during the formation of the neural plate. Our findings may suggest that neural stem cells are set apart from non-neural epiblast by changes in relative cell-cell and cell-substrate adhesion. Specifically, changes in cell adhesion separating neural stem cells from the non-neural epiblast may be augmented by the presence of exogenous chondroitin-6-sulfate in the epiblast basal lamina at the time neural progenitors are specified in the epiblast.

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References

  • Baranski M, Berdougo E, Sandler JS, Darnell DK, Burrus LW (2000) The dynamic expression pattern of frzb-1 suggests multiple roles in chick development. Dev Biol 217:25–41

    Article  CAS  PubMed  Google Scholar 

  • Beningo KA, Dembo M, Kaverina I, Small JV, Wang YL (2001) Nascent focal adhesions are responsible for the generation of strong propulsive forces in migrating fibroblasts. J Cell Biol 153:881–888

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Brittis PA, Canning DR, Silver J (1992) Chondroitin sulfate as a regulator of neuronal patterning in the retina. Science 255:733–736

    Article  CAS  PubMed  Google Scholar 

  • Brown AJ, Sanders EJ (1991) Interactions between mesoderm cells and the extracellular matrix following gastrulation in the chick embryo. J Cell Sci 99(Pt 2):431–441

    PubMed  Google Scholar 

  • Butterfield KC, Conovaloff A, Caplan M, Panitch A (2010) Chondroitin sulfate-binding peptides block chondroitin 6-sulfate inhibition of cortical neurite growth. Neurosci Lett 478:82–87

    Article  CAS  PubMed  Google Scholar 

  • Canning DR, Hoke A, Malemud CJ, Silver J (1996) A potent inhibitor of neurite outgrowth that predominates in the extracellular matrix of reactive astrocytes. Int J Dev Neurosci 14:153–175

    Article  CAS  PubMed  Google Scholar 

  • Canning DR, Amin T, Richard E (2000) Regulation of epiblast cell movements by chondroitin sulfate during gastrulation in the chick. Dev Dyn 219:545–559

    Article  CAS  PubMed  Google Scholar 

  • Chapman SC, Brown R, Lees L, Schoenwolf GC, Lumsden A (2004) Expression analysis of chick Wnt and frizzled genes and selected inhibitors in early chick patterning. Dev Dyn 229:668–676

    Article  CAS  PubMed  Google Scholar 

  • Eisenmann KM, McCarthy JB, Simpson MA, Keely PJ, Guan JL, Tachibana K, Lim L, Manser E, Furcht LT, Iida J (1999) Melanoma chondroitin sulphate proteoglycan regulates cell spreading through Cdc42, Ack-1 and p130cas. Nat Cell Biol 1:507–513

    Article  CAS  PubMed  Google Scholar 

  • Fernandez-Garre P, Rodriguez-Gallardo L, Gallego-Diaz V, Alvarez IS, Puelles L (2002) Fate map of the chicken neural plate at stage 4. Development 129:2807–2822

    CAS  PubMed  Google Scholar 

  • Friedlander DR, Milev P, Karthikeyan L, Margolis RK, Margolis RU, Grumet M (1994) The neuronal chondroitin sulfate proteoglycan neurocan binds to the neural cell adhesion molecules Ng-CAM/L1/NILE and N-CAM, and inhibits neuronal adhesion and neurite outgrowth. J Cell Biol 125:669–680

    Article  CAS  PubMed  Google Scholar 

  • Gilbert RJ, McKeon RJ, Darr A, Calabro A, Hascall VC, Bellamkonda RV (2005) CS-4,6 is differentially upregulated in glial scar and is a potent inhibitor of neurite extension. Mol Cell Neurosci 29:545–558

    Article  CAS  PubMed  Google Scholar 

  • Grumet M, Flaccus A, Margolis RU (1993) Functional characterization of chondroitin sulfate proteoglycans of brain: interactions with neurons and neural cell adhesion molecules. J Cell Biol 120:815–824

    Article  CAS  PubMed  Google Scholar 

  • Gu WL, Fu SL, Wang YX, Li Y, Lu HZ, Xu XM, Lu PH (2009) Chondroitin sulfate proteoglycans regulate the growth, differentiation and migration of multipotent neural precursor cells through the integrin signaling pathway. BMC Neurosci 10:128

    Article  PubMed Central  PubMed  Google Scholar 

  • Hamburger V, Hamilton HL (1992) A series of normal stages in the development of the chick embryo. 1951. Dev Dyn 195:231–272

    Article  CAS  PubMed  Google Scholar 

  • Hatta K, Takeichi M (1986) Expression of N-cadherin adhesion molecules associated with early morphogenetic events in chick development. Nature 320:447–449

    Article  CAS  PubMed  Google Scholar 

  • Hatta K, Takagi S, Fujisawa H, Takeichi M (1987) Spatial and temporal expression pattern of N-cadherin cell adhesion molecules correlated with morphogenetic processes of chicken embryos. Dev Biol 120:215–227

    Article  CAS  PubMed  Google Scholar 

  • Hayes MJ, Rescher U, Gerke V, Moss SE (2004) Annexin-actin interactions. Traffic 5:571–576

    Article  CAS  PubMed  Google Scholar 

  • Ida M, Shuo T, Hirano K, Tokita Y, Nakanishi K, Matsui F, Aono S, Fujita H, Fujiwara Y, Kaji T, Oohi-ra A (2006) Identification and functions of chondroitin sulfate in the milieu of neural stem cells. J Biol Chem 281:5982–5991

    Article  CAS  PubMed  Google Scholar 

  • Izumikawa T, Sato B, Kitagawa H (2014) Chondroitin sulfate is indispensable for pluripotency and differentiation of mouse embryonic stem cells. Sci Rep 4:3701

    Article  PubMed Central  PubMed  Google Scholar 

  • Joyner AL, Liu A, Millet S (2000) Otx2, Gbx2 and Fgf8 interact to position and maintain a mid-hindbrain organizer. Curr Opin Cell Biol 12:736–741

    Article  CAS  PubMed  Google Scholar 

  • Keane RW, Mehta PP, Rose B, Honig LS, Loewenstein WR, Rutishauser U (1988) Neural differentiation, NCAM-mediated adhesion, and gap junctional communication in neuroectoderm. A study in vitro. J Cell Biol 106:1307–1319

    Article  CAS  PubMed  Google Scholar 

  • Ketschek AR, Haas C, Gallo G, Fischer I (2012) The roles of neuronal and glial precursors in overcoming chondroitin sulfate proteoglycan inhibition. Exp Neurol 235:627–637

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kobayashi D, Kobayashi M, Matsumoto K, Ogura T, Nakafuku M, Shimamura K (2002) Early subdivisions in the neural plate define distinct competence for inductive signals. Development 129:83–93

    CAS  PubMed  Google Scholar 

  • Li H, Leung TC, Hoffman S, Balsamo J, Lilien J (2000) Coordinate regulation of cadherin and integrin function by the chondroitin sulfate proteoglycan neurocan. J Cell Biol 149:1275–1288

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Maeda N, Ishii M, Nishimura K, Kamimura K (2011) Functions of chondroitin sulfate and heparan sulfate in the developing brain. Neurochem Res 36:1228–1240

    Article  CAS  PubMed  Google Scholar 

  • Moss SE, Morgan RO (2004) The annexins. Genome Biol 5:219

    Article  PubMed Central  PubMed  Google Scholar 

  • Nishimura K, Ishii M, Kuraoka M, Kamimura K, Maeda N (2010) Opposing functions of chondroitin sulfate and heparan sulfate during early neuronal polarization. Neuroscience 169:1535–1547

    Article  CAS  PubMed  Google Scholar 

  • Puelles L, Fernandez-Garre P, Sanchez-Arrones L, Garcia-Calero E, Rodriguez-Gallardo L (2005) Correlation of a chicken stage 4 neural plate fate map with early gene expression patterns. Brain Res Brain Res Rev 49:167–178

    Article  CAS  PubMed  Google Scholar 

  • Purushothaman A, Sugahara K, Faissner A (2012) Chondroitin sulfate “wobble motifs” modulate maintenance and differentiation of neural stem cells and their progeny. J Biol Chem 287:2935–2942

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Rex M, Orme A, Uwanogho D, Tointon K, Wigmore PM, Sharpe PT, Scotting PJ (1997) Dynamic expression of chicken Sox2 and Sox3 genes in ectoderm induced to form neural tissue. Dev Dyn 209:323–332

    Article  CAS  PubMed  Google Scholar 

  • Schoenwolf GC, Alvarez IS (1989) Roles of neuroepithelial cell rearrangement and division in shaping of the avian neural plate. Development 106:427–439

    CAS  PubMed  Google Scholar 

  • Sirko S, von Holst A, Wizenmann A, Gotz M, Faissner A (2007) Chondroitin sulfate glycosaminoglycans control proliferation, radial glia cell differentiation and neurogenesis in neural stem/progenitor cells. Development 134:2727–2738

    Article  CAS  PubMed  Google Scholar 

  • Sirko S, Akita K, Von Holst A, Faissner A (2008) Structural and functional analysis of chondroitin sulfate proteoglycans in the neural stem cell niche. Methods Enzymol 479:37–71

    Article  Google Scholar 

  • Sirko S, von Holst A, Weber A, Wizenmann A, Theocharidis U, Gotz M, Faissner A (2010) Chondroitin sulfates are required for fibroblast growth factor-2-dependent proliferation and maintenance in neural stem cells and for epidermal growth factor-dependent migration of their progeny. Stem Cells 28:775–787

    Article  CAS  PubMed  Google Scholar 

  • Snow DM, Watanabe M, Letourneau PC, Silver J (1991) A chondroitin sulfate proteoglycan may influence the direction of retinal ganglion cell outgrowth. Development 113:1473–1485

    CAS  PubMed  Google Scholar 

  • Stacey M, Chang GW, Davies JQ, Kwakkenbos MJ, Sanderson RD, Hamann J, Gordon S, Lin HH (2003) The epidermal growth factor-like domains of the human EMR2 receptor mediate cell attachment through chondroitin sulfate glycosaminoglycans. Blood 102:2916–2924

    Article  CAS  PubMed  Google Scholar 

  • Stern CD (2005) Neural induction: old problem, new findings, yet more questions. Development 132:2007–2021

    Article  CAS  PubMed  Google Scholar 

  • Storey KG, Goriely A, Sargent CM, Brown JM, Burns HD, Abud HM, Heath JK (1998) Early posterior neural tissue is induced by FGF in the chick embryo. Development 125:473–484

    CAS  PubMed  Google Scholar 

  • Takagi H, Asano Y, Yamakawa N, Matsumoto I, Kimata K (2002) Annexin 6 is a putative cell surface receptor for chondroitin sulfate chains. J Cell Sci 115:3309–3318

    CAS  PubMed  Google Scholar 

  • Webb DJ, Parsons JT, Horwitz AF (2002) Adhesion assembly, disassembly and turnover in migrating cells—over and over and over again. Nat Cell Biol 4:E97–E100

    Article  CAS  PubMed  Google Scholar 

  • Zagris N, Chung AE, Stavridis V (2000) Differential expression of laminin genes in early chick embryo. Int J Dev Biol 44:815–818

    CAS  PubMed  Google Scholar 

  • Zagris N, Christopoulos M, Giakoumaki A (2004) Developmentally regulated expression and functional role of alpha 7 integrin in the chick embryo. Develop Growth Differ 46:299–307

    Article  CAS  Google Scholar 

Download references

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Correspondence to David R. Canning.

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Editor: T. Okamoto

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Canning, D.R., Cunningham, R.L. Cell adhesion properties of neural stem cells in the chick embryo. In Vitro Cell.Dev.Biol.-Animal 51, 507–514 (2015). https://doi.org/10.1007/s11626-014-9851-1

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  • DOI: https://doi.org/10.1007/s11626-014-9851-1

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