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The effect of RA on the chick Ebf1-3 genes expression in somites and pharyngeal arches

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Abstract

Expression of chick early B cell factor 1-3 (cEbf1-3) genes in regions of high retinoic acid (RA) activity, such as somites and pharyngeal arches (PAs), and regulation of other EBF members by RA raise the possibility that the internal cue RA may regulate cEbf1-3 expression in these tissues. To check this possibility, RA gain and loss of function experiments were conducted. Ectopic expression of RA led to up-regulation of cEbf2, 3 but did not change cEbf1 expression in somites. Expectedly, inhibition of RA by disulfiram resulted in downregulation of cEbf2, 3, but did not change cEbf1 expression in somites. The same RA gain and loss of function experiments did not change cEbf1-3 expression in PAs. However, ectopic expression of RA in the cranial neural tube before migration of neural crest cells downregulated cEbf1, 3 and up-regulated cEbf2 expression in the PAs. The same experiment, but with application of disulfiram, resulted in downregulation of cEbf2, but did not alter the expression of the other two genes. We conclude that the three cEbf genes act differently in response to RA signals in somitic mesoderm. cEbf1 may be not RA dependant in somites; however, the other two cEbf genes positively respond to RA signalling in somites. Additionally, only the migratory cEbf-expressing cells into the PAs are affected by RA signals.

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References

  • Alles AJ, Sulik KK (1992) Pathogenesis of retinoid-induced hindbrain malformations in an experimental model. Clin Dysmorphol 1:187–200

    Article  CAS  PubMed  Google Scholar 

  • Amirthalingam GS, Howard S, Alvarez S, de Lera AR, Itasaki N (2009) Regulation of Hoxb4 induction after neurulation by somite signal and neural competence. BMC Dev Biol 9:17

    Article  PubMed Central  PubMed  Google Scholar 

  • Bally-Cuif L, Dubois L, Vincent A (1998) Molecular cloning of Zcoe2, the zebrafish homolog of Xenopus Xcoe2 and mouse EBF-2, and its expression during primary neurogenesis. Mech Dev 77:85–90

    Article  CAS  PubMed  Google Scholar 

  • Bronner-Fraser M, Stern C (1991) Effects of mesodermal tissues on avian neural crest cell migration. Dev Biol 143:213–217

    Article  CAS  PubMed  Google Scholar 

  • Chen X, Esplin BL, Garrett KP, Welner RS, Webb CF, Kincade PW (2008) Retinoids accelerate B lineage lymphoid differentiation. J Immunol 180:138–145

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Christ B, Wilting J (1992) From somites to vertebral column. Ann Anat 174:23–32

    Article  CAS  PubMed  Google Scholar 

  • Corradi A et al (2003) Hypogonadotropic hypogonadism and peripheral neuropathy in Ebf2-null mice. Dev (Camb, Engl) 130:401–410

    Article  CAS  Google Scholar 

  • Crozatier M, Valle D, Dubois L, Ibnsouda S, Vincent A (1996) Collier, a novel regulator of Drosophila head development, is expressed in a single mitotic domain. Curr Biol 6:707–718

    Article  CAS  PubMed  Google Scholar 

  • Daburon V, Mella S, Plouhinec JL, Mazan S, Crozatier M, Vincent A (2008) The metazoan history of the COE transcription factors. Selection of a variant HLH motif by mandatory inclusion of a duplicated exon in vertebrates. BMC Evol Biol 8:131

    Article  PubMed Central  PubMed  Google Scholar 

  • Davis JA, Reed RR (1996) Role of Olf-1 and Pax-6 transcription factors in neurodevelopment. J Neurosci 16:5082–5094

    CAS  PubMed  Google Scholar 

  • Dietrich S, Schubert FR, Lumsden A (1997) Control of dorsoventral pattern in the chick paraxial mesoderm. Dev (Camb, Engl) 124:3895–3908

    CAS  Google Scholar 

  • Dubois L, Vincent A (2001) The COE–Collier/Olf1/EBF–transcription factors: structural conservation and diversity of developmental functions. Mech Dev 108:3–12

    Article  CAS  PubMed  Google Scholar 

  • El-Magd MA (2011) The function and regulation of chick Ebf genes in somite development Saarbrücken, Germany: LAP Lambert Academic Publishing ISBN-10: 3846590886, ISBN-13: 978-3846590881

  • El-Magd MA, Allen S, McGonnell I, Otto A, Patel K (2013a) Bmp4 regulates chick Ebf2 and Ebf3 gene expression in somite development. Develop Growth Differ 55:710–722. doi:10.1111/dgd.12077

    CAS  Google Scholar 

  • EL-Magd MA, Sayed-Ahmed A, Awad A, Shukry M (2013b) Regulation of chick early B-cell factor-1 gene expression in feather development. Acta Histochem. doi:10.1016/j.acthis.2013.11.010

    PubMed  Google Scholar 

  • El-Magd MA, Abo-Al-Ela HG, El-Nahas A, Saleh AA, Mansour AA (2014) Effects of a novel SNP of IGF2R gene on growth traits and expression rate of IGF2R and IGF2 genes in gluteus medius muscle of Egyptian buffalo. Gene 540:133–139. doi:10.1016/j.gene.2014.02.059

    Article  CAS  PubMed  Google Scholar 

  • Fields S, Ternyak K, Gao H, Ostraat R, Akerlund J, Hagman J (2008) The ‘zinc knuckle’ motif of Early B cell Factor is required for transcriptional activation of B cell-specific genes. Mol Immunol 45:3786–3796

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Garcia-Dominguez M, Poquet C, Garel S, Charnay P (2003) Ebf gene function is required for coupling neuronal differentiation and cell cycle exit. Dev (Camb, Engl) 130:6013–6025

    Article  CAS  Google Scholar 

  • Garel S, Marin F, Mattei MG, Vesque C, Vincent A, Charnay P (1997) Family of Ebf/Olf-1-related genes potentially involved in neuronal differentiation and regional specification in the central nervous system. Dev Dyn 210:191–205

    Article  CAS  PubMed  Google Scholar 

  • Garel S, Marin F, Grosschedl R, Charnay P (1999) Ebf1 controls early cell differentiation in the embryonic striatum. Dev (Camb, Engl) 126:5285–5294

    CAS  Google Scholar 

  • Garel S, Yun K, Grosschedl R, Rubenstein JL (2002) The early topography of thalamocortical projections is shifted in Ebf1 and Dlx1/2 mutant mice. Dev (Camb, Engl) 129:5621–5634

    Article  CAS  Google Scholar 

  • Gisler R, Jacobsen SE, Sigvardsson M (2000) Cloning of human early B-cell factor and identification of target genes suggest a conserved role in B-cell development in man and mouse. Blood 96:1457–1464

    CAS  PubMed  Google Scholar 

  • Green YS, Vetter ML (2011) EBF proteins participate in transcriptional regulation of Xenopus muscle development. Dev Biol 358:240–250. doi:10.1016/j.ydbio.2011.07.034

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Grifone R, Jarry T, Dandonneau M, Grenier J, Duprez D, Kelly RG (2008) Properties of branchiomeric and somite-derived muscle development in Tbx1 mutant embryos. Dev Dyn 237:3071–3078. doi:10.1002/dvdy.21718

    Article  PubMed  Google Scholar 

  • Guo C et al (2011) A Tbx1-Six1/Eya1-Fgf8 genetic pathway controls mammalian cardiovascular and craniofacial morphogenesis. J Clin Invest 121:1585–1595. doi:10.1172/JCI44630

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hagman J, Travis A, Grosschedl R (1991) A novel lineage-specific nuclear factor regulates mb-1 gene transcription at the early stages of B cell differentiation. EMBO J 10:3409–3417

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hagman J, Belanger C, Travis A, Turck CW, Grosschedl R (1993) Cloning and functional characterization of early B-cell factor, a regulator of lymphocyte-specific gene expression. Genes Dev 7:760–773

    Article  CAS  PubMed  Google Scholar 

  • Hamburger V, Hamilton HL (1951) A series of normal stages in the development of the chick embryo. J Morphology 88:49–92

    Article  CAS  Google Scholar 

  • Hesslein DG et al (2009) Ebf1-dependent control of the osteoblast and adipocyte lineages. Bone 44:537–546. doi:10.1016/j.bone.2008.11.021

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Horigome N, Myojin M, Ueki T, Hirano S, Aizawa S, Kuratani S (1999) Development of cephalic neural crest cells in embryos of Lampetra japonica, with special reference to the evolution of the jaw. Dev Biol 207:287–308

    Article  CAS  PubMed  Google Scholar 

  • Huang S et al (2009) ZNF423 is critically required for retinoic acid-induced differentiation and is a marker of neuroblastoma outcome. Cancer Cell 15:328–340

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Huang X, Hong CS, O'Donnell M, Saint-Jeannet JP (2005) The doublesex-related gene, XDmrt4, is required for neurogenesis in the olfactory system. Proc Natl Acad Sci U S A 102:11349–11354

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Jiang X, Choudhary B, Merki E, Chien KR, Maxson RE, Sucov HM (2002) Normal fate and altered function of the cardiac neural crest cell lineage in retinoic acid receptor mutant embryos. Mech Dev 117:115–122

    Article  CAS  PubMed  Google Scholar 

  • Kieslinger M et al (2005) EBF2 regulates osteoblast-dependent differentiation of osteoclasts. Dev Cell 9:757–767

    Article  CAS  PubMed  Google Scholar 

  • Liberg D, Sigvardsson M, Akerblad P (2002) The EBF/Olf/Collier family of transcription factors: regulators of differentiation in cells originating from all three embryonal germ layers. Mol Cell Biol 22:8389–8397

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lukin K, Fields S, Hartley J, Hagman J (2008) Early B cell factor: regulator of B lineage specification and commitment. Semin Immunol 20:221–227

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lumsden A, Sprawson N, Graham A (1991) Segmental origin and migration of neural crest cells in the hindbrain region of the chick embryo. Dev (Camb, Engl) 113:1281–1291

    CAS  Google Scholar 

  • Maden M (2002) Retinoid signalling in the development of the central nervous system. Nat Rev Neurosci 3:843–853. doi:10.1038/nrn963

    Article  CAS  PubMed  Google Scholar 

  • Maden M (2007) Retinoic acid in the development, regeneration and maintenance of the nervous system. Nat Rev Neurosci 8:755–765. doi:10.1038/nrn2212

    Article  CAS  PubMed  Google Scholar 

  • Mark M, Ghyselinck NB, Chambon P (2004) Retinoic acid signalling in the development of branchial arches. Curr Opin Genet Dev 14:591–598. doi:10.1016/j.gde.2004.07.012

    Article  CAS  PubMed  Google Scholar 

  • Matt N, Ghyselinck NB, Wendling O, Chambon P, Mark M (2003) Retinoic acid-induced developmental defects are mediated by RARbeta/RXR heterodimers in the pharyngeal endoderm. Dev (Camb, Engl) 130:2083–2093

    Article  CAS  Google Scholar 

  • Mazet F, Masood S, Luke GN, Holland ND, Shimeld SM (2004) Expression of AmphiCoe, an amphioxus COE/EBF gene, in the developing central nervous system and epidermal sensory neurons. Genesis 38:58–65

    Article  CAS  PubMed  Google Scholar 

  • Mella S, Soula C, Morello D, Crozatier M, Vincent A (2004) Expression patterns of the coe/ebf transcription factor genes during chicken and mouse limb development. Gene Expr Patterns 4:537–542

    Article  CAS  PubMed  Google Scholar 

  • Nieto MA, Patel K, Wilkinson DG (1996) In situ hybridization analysis of chick embryos in whole mount and tissue sections. Methods Cell Biol 51:219–235

    Article  CAS  PubMed  Google Scholar 

  • Noden DM, Trainor PA (2005) Relations and interactions between cranial mesoderm and neural crest populations. J Anat 207:575–601

    Article  PubMed Central  PubMed  Google Scholar 

  • Novitch BG, Wichterle H, Jessell TM, Sockanathan S (2003) A requirement for retinoic acid-mediated transcriptional activation in ventral neural patterning and motor neuron specification. Neuron 40:81–95

    Article  CAS  PubMed  Google Scholar 

  • Pang K, Matus DQ, Martindale MQ (2004) The ancestral role of COE genes may have been in chemoreception: evidence from the development of the sea anemone, Nematostella vectensis (Phylum Cnidaria; Class Anthozoa). Dev Genes Evol 214:134–138

    Article  CAS  PubMed  Google Scholar 

  • Pozzoli O, Bosetti A, Croci L, Consalez GG, Vetter ML (2001) Xebf3 is a regulator of neuronal differentiation during primary neurogenesis in Xenopus. Dev Biol 233:495–512

    Article  CAS  PubMed  Google Scholar 

  • Razy-Krajka F, Lam K, Wang W, Stolfi A, Joly M, Bonneau R, Christiaen L (2014) Collier/OLF/EBF-dependent transcriptional dynamics control pharyngeal muscle specification from primed cardiopharyngeal progenitors. Dev Cell 29:263–276. doi:10.1016/j.devcel.2014.04.001

    Article  CAS  PubMed  Google Scholar 

  • Schilling TF, Kimmel CB (1994) Segment and cell type lineage restrictions during pharyngeal arch development in the zebrafish embryo. Dev (Camb, Engl) 120:483–494

    CAS  Google Scholar 

  • Simionato E et al (2007) Origin and diversification of the basic helix-loop-helix gene family in metazoans: insights from comparative genomics. BMC Evol Biol 7:33

    Article  PubMed Central  PubMed  Google Scholar 

  • Soprano DR, Qin P, Soprano KJ (2004) Retinoic acid receptors and cancers. Annu Rev Nutr 24:201–221. doi:10.1146/annurev.nutr.24.012003.132407

    Article  CAS  PubMed  Google Scholar 

  • Vermot J, Niederreither K, Garnier JM, Chambon P, Dolle P (2003) Decreased embryonic retinoic acid synthesis results in a DiGeorge syndrome phenotype in newborn mice. Proc Natl Acad Sci U S A 100:1763–1768. doi:10.1073/pnas.0437920100

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Vervoort M, Crozatier M, Valle D, Vincent A (1999) The COE transcription factor Collier is a mediator of short-range Hedgehog-induced patterning of the Drosophila wing. Curr Biol 9:632–639

    Article  CAS  PubMed  Google Scholar 

  • Wang SS, Betz AG, Reed RR (2002) Cloning of a novel Olf-1/EBF-like gene, O/E-4, by degenerate oligo-based direct selection. Mol Cell Neurosci 20:404–414

    Article  CAS  PubMed  Google Scholar 

  • Wang SS, Lewcock JW, Feinstein P, Mombaerts P, Reed RR (2004) Genetic disruptions of O/E2 and O/E3 genes reveal involvement in olfactory receptor neuron projection. Dev (Camb, Engl) 131:1377–1388

    Article  CAS  Google Scholar 

  • Wang W, Razy-Krajka F, Siu E, Ketcham A, Christiaen L (2013) NK4 antagonizes Tbx1/10 to promote cardiac versus pharyngeal muscle fate in the ascidian second heart field. PLoS Biol 11:e1001725. doi:10.1371/journal.pbio.1001725

    Article  PubMed Central  PubMed  Google Scholar 

  • Wilson L, Maden M (2005) The mechanisms of dorsoventral patterning in the vertebrate neural tube. Dev Biol 282:1–13. doi:10.1016/j.ydbio.2005.02.027

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

The authors would like to thank Prof. Ketan Patel (School of Biological Sciences, University of Reading, Reading, UK), Dr. Steve Allen and Dr. Imelda McGonnell (Department of Veterinary Basic Sciences, Royal Veterinary College, London, UK) for the revision of the manuscript and useful discussion.

Conflict of interest

The authors declare no conflict of interests.

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Authors and Affiliations

  1. Department of Anatomy and Embryology, Faculty of Veterinary Medicine, Kafrelsheikh University, El-Geish Street, Post Box 33516, Kafrelsheikh, Egypt

    Mohammed Abu El-Magd

  2. Department of Animal Wealth Development, Faculty of Veterinary Medicine, Zagazig University, Zagazig, Egypt

    Ayman A. Saleh

  3. Department of Physiology, Faculty of Veterinary Medicine, Zagazig University, Zagazig, Egypt

    Reda M. Abd El-Aziz

  4. Department of Biochemistry, Faculty of Veterinary Medicine, Mansoura University, Mansoura, Egypt

    Mohammed F. Salama

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  1. Mohammed Abu El-Magd
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  2. Ayman A. Saleh
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  3. Reda M. Abd El-Aziz
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  4. Mohammed F. Salama
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Correspondence to Mohammed Abu El-Magd.

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Communicated by Andreas Kispert

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Table 1 EBF proteins identified to date
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El-Magd, M.A., Saleh, A.A., El-Aziz, R.M.A. et al. The effect of RA on the chick Ebf1-3 genes expression in somites and pharyngeal arches. Dev Genes Evol 224, 245–253 (2014). https://doi.org/10.1007/s00427-014-0483-y

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