Skip to main content
SpringerLink
Log in

The tyrosine hydroxylase gene is expressed in endoderm and pancreas of early quail embryos

  • Original Articles
  • Published:
Anatomy and Embryology Aims and scope Submit manuscript

Abstract

The initial expression of the gene encoding tyrosine hydroxylase (TH) was studied in the trunk of quail embryos by in situ hybridization. We detected the presence of quail TH mRNA on embryonic day 3.5 (E3.5) in the sympathetic ganglia and aortic plexus, both neural crest derived structures. In contrast, the TH gene was expressed much earlier in the endodermal layer of E2 embryos, i. e. from the 8-somite stage onwards. TH mRNA was found also in the pancreatic bud, an endoderm-derived structure. The TH protein and catecholamines were subsequently looked for in these structures. TH immunoreactivity was found in cells of E2 explanted endoderm, but no catecholamine histofluorescence was observed before or after a few days in culture. TH-positive cells were also detected in cultures of pancreatic rudiments, explanted from E3 to E6 quail embryos. We suggest that the TH-positive cells of the endoderm are the progenitors of the catecholaminergic cells of the pancreas and of the enterochromaffin cells of the gut. The hypothesis that the TH-positive cells of the endoderm are involved in the expression of the catecholaminergic phenotype by neural crest cells is discussed.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Abo T, Balch CM (1981) A differentiation antigen of human NK and K cells identified by a monoclonal antibody (HNK1). J Immunol 127:1024–1029

    Google Scholar 

  • Allan IJ, Newgreen DF (1977) Catecholamine accumulation in neural crest cells and the primary sympathetic chain. Am J Anat 149:413–421

    Google Scholar 

  • Alpert S, Hanahan D, Teitelman G (1988) Hybrid insulin genes reveal a developmental lineage for pancreatic endocrine cells and imply a relationship with neurons. Cell 53:295–308

    Google Scholar 

  • Andrew A (1974) Further evidence that enterochromaffin cells are not derived from the neural crest. J Embryol Exp Morphol 31:589–598

    Google Scholar 

  • Carnahan JF, Anderson D, Patterson PH (1991) Evidence that enteric neurons may derive from the sympathoadrenal lineage. Dev Biol 148:552–561

    Google Scholar 

  • Cochard P (1984) Adrenergic differentiation in the autonomous nervous system. In: Duprat AM, Kato AC, Weber M (eds) The role of cell interactions in early neurogenesis. Plenum Press, New York, pp 109–121

    Google Scholar 

  • Cochard P, Goldstein M, Black IB (1978) Ontogenetic appearance and disappearance of tyrosine hydroxylase and catecholamines in the rat embryo. Proc Natl Acad Sci USA 75:2986–2990

    Google Scholar 

  • Cochard P, Goldstein M, Black IB (1979) Initial development of the noradrenergic phenotype in autonomic neuroblasts of the rat embryo in vivo. Dev Biol 71:100–114

    Google Scholar 

  • Cox KH, De Leon DL, Angerer LM, Angerer RC (1984) Detection of mRNA in the sea urchin embryos by in situ hybridization using asymmetric RNA probes. Dev Biol 101:485–502

    Google Scholar 

  • Dieterlen-Liévre F (1965) Etude morphologique et expérimentale de la différenciation du pancréas chez l'embryon de poulet. Bull Biol Fr Belg 99:1–116

    Google Scholar 

  • Drews U, Kussäther E, Usadel KH (1967) Histochemischer Nachweis der Cholinesterase in der Frühentwicklung der Hühnerkeimscheibe. Histochemie 8:65–89

    Google Scholar 

  • Dupin E, Maus M, Fauquet M (1993) Regulation of the quail tyrosine hydroxylase gene in neural crest cells by cAMP and β- adrenergic ligands. Dev Biol 159:75–86

    Google Scholar 

  • Eisenbarth GS, Shimizu K, Bowring MA, Wells S (1982). Expression of receptors for tetanus toxin and monoclonal antibody A2B5 by pancreatic islet cells. Proc Natl Acad Sci USA 79:5066–5070

    Google Scholar 

  • Enemar A, Falck B, Hakanson R (1965) Observations on the appearance of norepinephrine in the sympathetic nervous system of the chick embryo. Dev Biol 11:268–283

    Google Scholar 

  • Escurat M, Djabali K, Huc C, Landon F, Bécourt C, Boitard C, Gros F, Portier M M (1991) Origin of the beta cells of the islets of Langerhans is further questioned by the expression of neuronal intermediate filament proteins, peripherin and NF-L, in the rat insulinoma RIN5F cell line. Dev Neurosci 13:424–432

    Google Scholar 

  • Falck B, Hillarp NA, Thieme G, Torp A (1962) Fluorescence of catecholamines and related compounds condensed with formaldehyde. J Histochem Cytochem 10:348–354

    CAS  Google Scholar 

  • Fauquet M, Boni C (1993) The quail tyrosine hydroxylase gene promoter contains an active cAMP responsive element. J Neurochem 60:274–281

    Google Scholar 

  • Fauquet M, Ziller C (1989) A monoclonal antibody directed against quail tyrosine hydroxylase: description and use in immunocytochemical studies on differentiating neural crest cells. J Histochem Cytochem 37:1197–1205

    Google Scholar 

  • Fauquet M, Smith J, Ziller C, Le Douarin NM (1981) Differentiation of autonomic neuron precursors in vitro: cholinergic and adrenergic traits in cultured neural crest cells. J Neurosci 1:478–92

    Google Scholar 

  • Fauquet M, Grima B, Lamouroux A, Mallet J (1988) Cloning of quail tyrosine hydroxylase: amino acid homology with other hydroxylases discloses functional domains. J Neurochem 50:142–148

    Google Scholar 

  • Fontaine J, Le Douarin NM (1977) Analysis of endoderm formation in the avian blastoderm by the use of quail-chick chimaeras. The problem of the neurectodermal origin of the cells of the APUD series. J Embryol Exp Morphol 41:209–222

    Google Scholar 

  • Fontaine J, Le Lièvre C, Le Douarin NM (1977) What is the developmental fate of neural crest cells which migrate into the pancreas in the avian embryo? Gen Comp Endocrinol 33:394–404

    Google Scholar 

  • Furness JB, Costa M, Wilson A J (1977) Water-stable fluorophores, produced by reaction with aldehyde solutions, for the histochemical localization of catechol- and indolethylamines. Histochemistry 52:159–170

    Google Scholar 

  • Ignarro LJ, Shideman FE (1968) Appearance and concentration of catecholamines and their biosynthesis in the embryonic and developing chick. J Pharmacol Exp Ther 159:38–48

    Google Scholar 

  • Kirby ML, Gilmore SA (1972). A fluorescence study on the ability of the notochord to synthesize and store catecholamines in early chick embryos. Anat Rec 173:469–478

    Google Scholar 

  • Kirby ML, Gilmore SA (1976) A correlative histofluorescence and light microscopic study of the formation of the sympathetic trunks in chick embryos. Anat Rec 186:437–450

    Google Scholar 

  • König R (1979) Consecutive demonstration of catecholamines and dopamine-β-hydroxylase within the same specimen. Histochemistry 61:301–305

    Google Scholar 

  • Lawrence IE, Burden HW (1973) Catecholamines and morphogenesis of the chick embryo neural tube and notochord. Am J Anat 137:199–208

    Google Scholar 

  • Le Douarin NM (1964) Etude expérimentale de l'organogenèse du tube digestif et du foie chez l'embryon de poulet. Bull Biol Fr Belg 98:544–676

    Google Scholar 

  • Le Douarin NM (1982) The neural crest. Cambridge University Press, Cambridge

    Google Scholar 

  • Le Douarin NM (1988) On the origin of pancreatic endocrine cells. Cell 53:169–171

    PubMed  Google Scholar 

  • Le Douarin NM, Teillet MA (1973) The migration of neural crest cells to the wall of the digestive tract in avian embryo. J Embryol Exp Morphol 30:31–48

    Google Scholar 

  • Levitt M, Spectror S, Sjoerdsma A, Udenfriends S (1965) Elucidation of the rate-limiting step in norepinephrine biosynthesis in the perfused guinea pig heart. J Pharmacol Exp Ther 148:1–8

    Google Scholar 

  • Mackey HM, Payette RF, Gershon MD (1988) Tissue effects on the expression of serotonin, tyrosine hydroxylase and GABA in cultures of neurogenic cells from the neuraxis and branchial arches. Development 104:205–217

    Google Scholar 

  • Nataf V, Monier S (1992) Effect of insulin and insulin-like growth factor 1 on the expression of the catecholaminergic phenotype by neural crest cells. Dev Brain Res 69:59–66

    Google Scholar 

  • Newgreen DF, Allan IJ, Young HM, Southwell BR (1981) Accumulation of exogenous catecholamines in the neural tube and non neural tissues of the early fowl embryo. Wilhelm Roux's Arch Entwicklungsmech Org 190:320–330

    Google Scholar 

  • Newgreen DF, Powel NE, Moser B (1990) Spatiotemporal changes in HNK1/L2 glycoconjugates on avian embryo somite and neural crest cells. Dev Biol 139:100–120

    Google Scholar 

  • Pearse AGE (1966) Common cytochemical properties of cells producing polypeptide hormones, with particular reference to calcitonin and the thyroid C cells. Vet Rec 79:587–590

    Google Scholar 

  • Pearse AGE (1968) Common cytochemical and ultrastructural characteristics of cells producing polypeptide hormones (the APUD series) and their relevance to thyroid and ultimobranchial C cells and calcitonin. Proc Roy Soc Lond[Biol]170:71–80

    Google Scholar 

  • Pictet RL, Rall LB, Phelps P, Rutter WJ (1976) The neural crest and the origin of the insulin-producing and other gastrointestinal hormone-producing cells. Science 191:191–192

    Google Scholar 

  • Polak JM, Bloom SR, Marangos PJ (1984). Neuron-specific enolase, a marker for neuroendocrine cells. In: Falkmer S, Hakanson R, Sanders F (eds) Evolution and tumor pathology of the neuroendocrine system. Elsevier, Amsterdam, pp 433–542

    Google Scholar 

  • Polak M, Scharfmann R, Seilheimer B, Eisenbarth G, Dressler D, Verma IM, Potter H (1993) Nerve growth factor induces neuronlike differentiation of an insulin-secreting pancreatic beta cell line. Proc Natl Acad Sci USA 90:5781–5785

    Google Scholar 

  • Quéva C, Ness SA, Grasser FA, Graf T, Vandenbunder B, Stehelin D (1992) Expression patterns of c-myb and of v-myb induced myeloid-1 (mim-1) gene during the development of the chick embryo. Development 114:125–133

    Google Scholar 

  • Rothman T, Le Douarin NM, Fontaine-Pérus J, Gershon MD (1990) Developmental potential of neural crest-derived cells migrating from segments of developing quail bowel grafted into younger chick host embryos. Development 109:411–423

    Google Scholar 

  • Rothman TP, Gershon MD, Holtzer H (1978) The relationship of cell division to the acquisition of adrenergic characteristics by developing sympathetic ganglion cell precursors. Dev Biol 65:322–341

    Google Scholar 

  • Strudel G, Recasens M, Mandel P (1977) Identification de cat'echolamines et de sérotonine dans les chordes d'embryons de poulet. CR Acad Sci (D) 284:967–969

    Google Scholar 

  • Teitelman G (1990) Insulin cells of pancreas extend neurites but do not arise from the neuroectoderm. Dev Biol 142:368–379

    Google Scholar 

  • Teitelman G, Lee JK (1987) Cell lineage analysis of pancreatic islet cell development: glucagon and insulin cells arise from catecholaminergic precursors present in the pancreatic duct. Dev Biol 121:454–466

    Google Scholar 

  • Teitelman G, Baker H, Joh TH, Reis DJ (1979) Appearance of catecholamine-synthesizing enzymes during development of rat sympathetic nervous system: possible role of tissue environment. Proc Natl Acad Sci USA 76:509–513

    Google Scholar 

  • Thompson EM, Fleming KA, Evans DJ, Fundele R, Surani MA, Wright NA (1990) Gastric endocrine cells share a clonal origin with other gut cell lineages. Development 110:477–481

    Google Scholar 

  • Tucker GC, Aoyama H, Lipinski M, Tursz T, Thiery JP (1984) Identical reactivity of monoclonal antibodies HNK-1 and NC-1: conservation in vertebrates on cells derived from the neural primordium and on some leukocytes. Cell Differ 14:223–230

    Google Scholar 

  • Tyner AL, Godbout R, Compton RS, Tilghman SM (1990) The ontogeny of α-fetoprotein gene expression in the mouse gastrointestinal tract. J Cell Biol 110:915–927

    Google Scholar 

  • Vogel KS, Weston J (1990) The sympathoadrenal lineage in avian embryos. I. Adrenal chromaffin cells lose neuronal traits during embryogenesis. Dev Biol 139:1–12

    Google Scholar 

  • Watanabe T, Chikazawa H, Yamada H (1984) Catecholamine-containing pancreatic islet cells of the domestic fowl. Cell Tissue Res 237:239–244

    Google Scholar 

  • Wiedenmann B, Franke WW, Kuhn C, Moll R, Gould VE (1986) Synaptophysin: a marker protein for neuroendocrine cells and neoplasms. Proc Natl Acad Sci USA 83:3500–3504

    Google Scholar 

  • Xue ZG, Xue XJ, Fauquet M, Smith J, Le Douarin N (1992) Expression of the gene encoding tyrosine hydroxylase in a subpopulation of quail dorsal root ganglion cells cultured in the presence of insulin or chick embryo extract. Dev Brain Res 69:23–30

    Google Scholar 

  • Zhang J, Sieber-Blum M (1992) Characterization of the norepinephrine uptake system and the role of norepinephrine in the expression of the adrenergic phenotype by quail neural crest cells in clonal culture. Brain Res 570:251–258

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institut d'Embryologie Cellulaire et Moléculaire du CNRS et du Collége de France, 49 bis Avenue de la Belle Gabrielle, F-94130, Nogent sur Marne, France

    Catherine Ziller

  2. CNRS URA 1160, Institut Pasteur, 1 Rue Calmette, F-59019, Lille, France

    Marie Anne Mirabel & Bernard Vandenbunder

  3. CNRS URA 1414, Ecole Normale Supérieure, 46 Rue d'Ulm, 05, Paris Cedex, France

    Mireille Fauquet

Authors
  1. Catherine Ziller
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Marie Anne Mirabel
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Bernard Vandenbunder
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Mireille Fauquet
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ziller, C., Mirabel, M.A., Vandenbunder, B. et al. The tyrosine hydroxylase gene is expressed in endoderm and pancreas of early quail embryos. Anat Embryol 189, 307–315 (1994). https://doi.org/10.1007/BF00190587

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00190587

Key words

Search

Navigation