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Role of FGF signalling in neural crest cell migration during early chick embryo development

Published online by Cambridge University Press:  06 December 2018

Xiao-tan Zhang ,
Guang Wang ,
Yan Li ,
Manli Chuai ,
Kenneth Ka Ho Lee  and
Xuesong Yang Open the ORCID record for Xuesong Yang [Opens in a new window]
Xiao-tan Zhang
Affiliation:
Department of Histology and Embryology, International Joint Laboratory for Embryonic Development & Prenatal Medicine, Medical College, Jinan University, Guangzhou 510632, China Key Laboratory for Regenerative Medicine of the Ministry of Education, Jinan University, Guangzhou, China
Guang Wang
Affiliation:
Department of Histology and Embryology, International Joint Laboratory for Embryonic Development & Prenatal Medicine, Medical College, Jinan University, Guangzhou 510632, China Key Laboratory for Regenerative Medicine of the Ministry of Education, Jinan University, Guangzhou, China
Yan Li
Affiliation:
Department of Histology and Embryology, International Joint Laboratory for Embryonic Development & Prenatal Medicine, Medical College, Jinan University, Guangzhou 510632, China
Manli Chuai
Affiliation:
Division of Cell and Developmental Biology, University of Dundee, Dundee, DD1 5EH, UK
Kenneth Ka Ho Lee
Affiliation:
Joint CUHK-UoS Laboratory for Stem Cell and Regenerative Medicine, School of Biomedical Sciences, Chinese University of Hong Kong, Shatin, Hong Kong
Xuesong Yang*
Affiliation:
Department of Histology and Embryology, International Joint Laboratory for Embryonic Development & Prenatal Medicine, Medical College, Jinan University, Guangzhou 510632, China
*
Address for correspondence: Xuesong Yang. Department of Histology and Embryology, International Joint Laboratory for Embryonic Development & Prenatal Medicine, Medical College, Jinan University, Guangzhou 510632, China Fax: +20 85221343. E-mail: [email protected]
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Summary

Fibroblast growth factor (FGF) signalling acts as one of modulators that control neural crest cell (NCC) migration, but how this is achieved is still unclear. In this study, we investigated the effects of FGF signalling on NCC migration by blocking this process. Constructs that were capable of inducing Sprouty2 (Spry2) or dominant-negative FGFR1 (Dn-FGFR1) expression were transfected into the cells making up the neural tubes. Our results revealed that blocking FGF signalling at stage HH10 (neurulation stage) could enhance NCC migration at both the cranial and trunk levels in the developing embryos. It was established that FGF-mediated NCC migration was not due to altering the expression of N-cadherin in the neural tube. Instead, we determined that cyclin D1 was overexpressed in the cranial and trunk levels when Sprouty2 was upregulated in the dorsal neural tube. These results imply that the cell cycle was a target of FGF signalling through which it regulates NCC migration at the neurulation stage.

Keywords

Cell cycleEMTFGF signallingNeural crest cellsSprouty2
Type
Research Article
Information
Zygote , Volume 26 , Issue 6 , December 2018 , pp. 457 - 464
Copyright
© Cambridge University Press 2018 

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References

Abu-Issa, R, Smyth, G, Smoak, I, Yamamura, K and Meyers, EN (2002) Fgf8 is required for pharyngeal arch and cardiovascular development in the mouse. Development 129, 4613–4625.Google Scholar
Aranda, S, Alvarez, M, Turro, S, Laguna, A and de la Luna, S (2008) Sprouty2-mediated inhibition of fibroblast growth factor signaling is modulated by the protein kinase DYRK1A. Mol Cell Biol 28, 5899–5911.Google Scholar
Barembaum, M and Bronner-Fraser, M (2005) Early steps in neural crest specification. Semin Cell Dev Biol 16, 642–646.Google Scholar
Barriga, EH and Mayor, R (2015) Embryonic cell–cell adhesion: a key player in collective neural crest migration. Curr Top Dev Biol 112, 301–323.Google Scholar
Beenken, A and Mohammadi, M (2009) The FGF family: biology, pathophysiology and therapy. Nat Rev Drug Discov 8, 235–253.Google Scholar
Berg, T, Rountree, CB, Lee, L, Estrada, J, Sala, FG, Choe, A, Veltmaat, JM, De Langhe, S, Lee, R, Tsukamoto, H, Crooks, GM, Bellusci, S, and Wang, KS (2007) Fibroblast growth factor 10 is critical for liver growth during embryogenesis and controls hepatoblast survival via beta-catenin activation. Hepatology 46, 1187–1197.Google Scholar
Brewer, JR, Mazot, P and Soriano, P (2016) Genetic insights into the mechanisms of Fgf signaling. Genes Dev 30, 751–771.Google Scholar
Bryant, DM, Wylie, FG and Stow, JL (2005) Regulation of endocytosis, nuclear translocation, and signaling of fibroblast growth factor receptor 1 by E-cadherin. Mol Biol Cell 16, 14–23.Google Scholar
Clay, MR and Halloran, MC (2014) Cadherin 6 promotes neural crest cell detachment via F-actin regulation and influences active Rho distribution during epithelial-to-mesenchymal transition. Development 141, 2506–2515.Google Scholar
Debiais, F, Lemonnier, J, Hay, E, Delannoy, P, Caverzasio, J and Marie, PJ (2001) Fibroblast growth factor-2 (FGF-2) increases N-cadherin expression through protein kinase C and Src-kinase pathways in human calvaria osteoblasts. J Cell Biochem 81, 68–81.Google Scholar
Hall, BK (2008) The neural crest and neural crest cells: discovery and significance for theories of embryonic organization. J Biosci 33, 781–793.Google Scholar
Hamburger, V and Hamilton, HL (1951) A series of normal stages in the development of the chick embryo. J Morphol 88, 49–92.Google Scholar
Henrique, D, Adam, J, Myat, A, Chitnis, A, Lewis, J and Ish-Horowicz, D (1995) Expression of a Delta homologue in prospective neurons in the chick. Nature 375, 787–790.Google Scholar
Itoh, N, Ohta, H, Nakayama, Y and Konishi, M (2016) Roles of FGF signals in heart development, health, and disease. Front Cell Dev Biol 4, 110.Google Scholar
Li, S, Quarto, N and Longaker, MT (2010) Activation of FGF signaling mediates proliferative and osteogenic differences between neural crest derived frontal and mesoderm parietal derived bone. PLoS One 5, e14033.Google Scholar
Martinez-Morales, PL, Diez del Corral, R, Olivera-Martinez, I, Quiroga, AC, Das, RM, Barbas, JA, Storey, KG, and Morales, AV (2011) FGF and retinoic acid activity gradients control the timing of neural crest cell emigration in the trunk. J Cell Biol 194, 489–503.Google Scholar
Mayor, R, Morgan, R and Sargent, MG (1995) Induction of the prospective neural crest of Xenopus . Development 121, 767–777.Google Scholar
McKinney, MC, McLennan, R and Kulesa, PM (2016) Angiopoietin 2 signaling plays a critical role in neural crest cell migration. BMC Biol 14, 111.Google Scholar
Nichols, DH (1987) Ultrastructure of neural crest formation in the midbrain/rostral hindbrain and preotic hindbrain regions of the mouse embryo. Am J Anat 179, 143–154.Google Scholar
Perrais, M, Chen, X, Perez-Moreno, M and Gumbiner, BM (2007) E-cadherin homophilic ligation inhibits cell growth and epidermal growth factor receptor signaling independently of other cell interactions. Mol Biol Cell 18, 2013–2025.Google Scholar
Pla, P, Moore, R, Morali, OG, Grille, S, Martinozzi, S, Delmas, V, and Larue, L (2001) Cadherins in neural crest cell development and transformation. J Cell Physiol 189, 121–132.Google Scholar
Reichetzeder, C, Putra, SED, Li, J and Hocher, B (2016) Developmental origins of disease–crisis precipitates change. Cell Physiol Biochem 39, 919–938.Google Scholar
Sadaghiani, B and Thiebaud, CH (1987) Neural crest development in the Xenopus laevis embryo, studied by interspecific transplantation and scanning electron microscopy. Dev Biol 124, 91–110.Google Scholar
Sasaki, T, Ito, Y, Bringas, P Jr., Chou, S, Urata, MM, Slavkin, H, and Chai, Y (2006) TGFbeta-mediated FGF signaling is crucial for regulating cranial neural crest cell proliferation during frontal bone development. Development 133, 371–381.Google Scholar
Sato, A, Scholl, AM, Kuhn, EB, Stadt, HA, Decker, JR, Pegram, K, Hutson, MR and Kirby, ML (2011) FGF8 signaling is chemotactic for cardiac neural crest cells. Dev Biol 354, 18–30.Google Scholar
Shoval, I, Ludwig, A and Kalcheim, C (2007) Antagonistic roles of full-length N-cadherin and its soluble BMP cleavage product in neural crest delamination. Development 134, 491–501.Google Scholar
Smith, ER, Holt, SG, and Hewitson, TD (2017) FGF23 activates injury-primed renal fibroblasts via FGFR4-dependent signalling and enhancement of TGF-beta autoinduction. Int J Biochem Cell Biol 92, 63–78.Google Scholar
Steventon, B, Carmona-Fontaine, C and Mayor, R (2005) Genetic network during neural crest induction: from cell specification to cell survival. Semin Cell Dev Biol 16, 647–654.Google Scholar
Taneyhill, LA (2008) To adhere or not to adhere: the role of cadherins in neural crest development. Cell Adh Migr 2, 223–230.Google Scholar
Theveneau, E, Duband, JL and Altabef, M (2007) Ets-1 confers cranial features on neural crest delamination. PLoS One 2, e1142.Google Scholar
Theveneau, E and Mayor, R (2011) Collective cell migration of the cephalic neural crest: the art of integrating information. Genesis 49, 164–176.Google Scholar
Wang, G, Li, Y, Wang, X-Y, Han, Z, Chuai, M, Wang, L-J, Ho, KK, Lee, , Geng, J-G, and Yang, Y (2013) Slit/Robo1 signaling regulates neural tube development by balancing neuroepithelial cell proliferation and differentiation. Exp Cell Res 319, 1083–1093.Google Scholar
Wang, G, Li, Y, Wang, X-Y, Chuai, M, Chan, JY-H, Lei, J, Münsterberg, A, Lee, KKH, and Yang, X (2015) Misexpression of BRE gene in the developing chick neural tube affects neurulation and somitogenesis. Mol Biol Cell 26, 978–992.Google Scholar
Wang, G, Chen, E-N, Liang, C, Liang, J, Gao, L-R, Chuai, M, Münsterberg, A, Bao, Y, Cao, L, and Yang, X (2017) Atg7-mediated autophagy is involved in the neural crest cell generation in chick embryo. Mol Neurobiol 55, 3523–3536.Google Scholar
Yang, X, Dormann, D, Munsterberg, AE and Weijer, CJ (2002a) Cell movement patterns during gastrulation in the chick are controlled by positive and negative chemotaxis mediated by FGF4 and FGF8. Dev Cell 3, 425–437.Google Scholar
Yang, XS, Dormann, D, Munsterberg, AE and Weijer, CJ (2002b) Cell movement patterns during gastrulation in the chick are controlled by chemotaxis mediated by positive and negative FGF4 and FGF8. Dev Cell 3, 425–437.Google Scholar
Yang, XS, Chrisman, H and Weijer, CJ (2008) PDGF signalling controls the migration of mesoderm cells during chick gastrulation by regulating N-cadherin expression. Development 135, 3521–3530.Google Scholar
Yardley, N and Garcia-Castro, MI (2012) FGF signaling transforms non-neural ectoderm into neural crest. Dev Biol 372, 166–177.Google Scholar
Yue, Q, Wagstaff, L, Yang, X, Weijer, C and Munsterberg, A (2008) Wnt3a-mediated chemorepulsion controls movement patterns of cardiac progenitors and requires RhoA function. Development 135, 1029–1037.Google Scholar
Zhang, J, Chang, JY, Huang, Y, Lin, X, Luo, Y, Schwartz, RJ, Martin, JF, and Wang, F (2010) The FGF-BMP signaling axis regulates outflow tract valve primordium formation by promoting cushion neural crest cell differentiation. Circ Res 107, 1209–1219.Google Scholar
Zhang, P, Wang, G, Lin, ZL, Wu, Y, Zhang, J, Lee, KKH, Chuai, M, and Yang, X (2017) Alcohol exposure induces chick craniofacial bone defects by negatively affecting cranial neural crest development. Toxicol Lett 281, 53–64.Google Scholar
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