Skip to main content
Log in

Can a non-gut mesenchyme support differentiation of gut endocrine cells?

  • Published:
Anatomy and Embryology Aims and scope Submit manuscript

Summary

This experiment was designed to find out if endoderm lacks an intrinsic ability to give rise to gut endocrine cells, and, if not, whether differentiation of endocrine cells can be supported by mesenchyme from a source outside the digestive tract. Heterospecific combinations of proventricular endoderm and flank mesenchyme from chick and quail embryos at 3.25–4 days of incubation were grown as chorio-allantoic grafts to a final incubation age of 21 days. Re-associated proventricular endoderm and mesenchyme served as controls. The proventricular endoderm induced some smooth muscle in the flank mesenchyme but the latter did not support as advanced glandular morphogenesis as did proventricular mesenchyme. Nevertheless, endocrine cells differentiated in experimental as in control grafts and at similar frequencies. The various types were distinguished immunocytochemically by their contained peptides; the range of types found was specific for the proventriculus. Hence it is concluded not only that the particular non-gut mesenchyme used does support differentiation of gut endocrine cells, but also that the determination of the progenitors of endocrine cells, and the selection of the range of types destined to differentiate in a particular part of the digestive tract under normal circumstances, occurs early in development — before 3.25 days of incubation in the case of the proventriculus.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Alison BC (1989) The distribution and ontogeny of gastrin/CCK-, somatostatin- and neurotensin-immunoreactive cells in the gastrointestinal tract of the chicken. Histol Histopathol 4:55–62

    Google Scholar 

  • Alison BC (1990) Distribution and ontogeny of glucagon- and pancreatic polypeptide-immunoreactive cells in the gastro-intestinal tract of the chicken. Anat Embryol 182:605–610

    Google Scholar 

  • Andrew A, Rawdon BB (1990) Intestinal mesenchyme provokes differentiation of intestinal endocrine cells in gizzard endoderm. Differentiation 43:165–174

    Google Scholar 

  • Cowap J (1985) The first appearance of endocrine cells in the splenic lobe of the embryonic chick pancreas. Gen Comp Endocrinol 60:131–137

    Google Scholar 

  • Haffen K, Lacroix B, Kedinger M, Simon-Assmann P, Grenier JF (1982) Inductive properties displayed by mesenchymal cells of the rat intestinal mucosa on epithelial differentiation. Gastroenterology 82:1077

    Google Scholar 

  • Haffen K, Lacroix B, Kedinger M, Simon-Assmann PM (1983) Inductive properties of fibroblastic cultures derived from rat intestinal mucosa on epithelial differentiation. Differentiation 23:226–233

    Google Scholar 

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

    Google Scholar 

  • Ishizuya-Oka A (1983) Electron microscopical study of self-differentiation potency in the chick embryonic endoderm cultured in vitro. Roux' Arch Dev Biol 192:171–178

    Google Scholar 

  • Kedinger M, Simon-Assmann P, Haffen K (1986) Differentiation pattern of rat intestinal endodermal cells cultured on mesenchymal cell monolayers: comparison with in vivo development of cell-cell associations. Eur J Cell Biol [Suppl 42]:15

  • Kedinger M, Simon-Assmann P, Bouziges F, Arnold C, Alexandre E, Haffen K (1990) Smooth muscle actin expression during rat gut development and induction in fetal skin fibroblastic cells associated with intestinal embryonic epithelium. Differentiation 43:87–97

    Google Scholar 

  • Kirkland SC (1986) Endocrine differentiation by a human rectal adenocarcinoma cell line (HRA-19). Differentiation 33:148–155

    Google Scholar 

  • Kramer B, Andrew A, Rawdon BB, Becker P (1987) The effect of pancreatic mesenchyme on the differentiation of endocrine cells from gastric endoderm. Development 100:661–671

    Google Scholar 

  • Le Douarin N, Bussonnet C (1966) Détermination précoce et rôle inducteur de l'endoderm pharyngien chez l'embryon de poulet. CR Acad Sci (Paris) 263:1241–1243

    Google Scholar 

  • Le Douarin N, Bussonnet C, Chaumont F (1968) Etude des capacités de differenciation et du rôle morphogène de l'endoderme pharyngien chez l'embryon d'oiseau. Ann Embryol Morphol Exp 1:29–40

    Google Scholar 

  • McLoughlin CB (1961) Importance of mesenchymal factors in the differentiation of chick epidermis. II. Modification of epidermal differentiation by contact with different types of mesenchyme. J Embryol Exp Morphol 9:385–409

    Google Scholar 

  • Mizuno T (1975) Une hypothèse sur l'organogenese du tractus digestif. CR Soc Biol (Paris) 169:1096–1098

    Google Scholar 

  • Mizuno T, Yasugi S (1990) Susceptibility of epithelia to directive influences of mésenchymes during organogenesis: uncoupling of morphogenesis and cytodifferentiation. Cell Differ Dev 31:151–159

    Google Scholar 

  • Mizuno T, Ishizuya A (1982a) Etude au microscope électronique de la différenciation in vitro de l'endoderme d'intestin grêle de jeune embryon d'oiseau, associé ou non à son mesenchyme. CR Seances Soc Franco-Jap Biol 176:580–584

    Google Scholar 

  • Mizuno T, Ishizuya A (1982b) Etude ultrastructurale de l'endoderme du tube digestif de l'embryon de poulet après autodifférenciation in vitro. CR Soc Biol (Paris) 176:889–894

    Google Scholar 

  • Pearse AGE, Polak JM (1975) Bifunctional reagents as vapour and liquid phase fixatives for immunohistochemistry. Histochem J 7:179–186

    Google Scholar 

  • Rawdon BB (1978) Preventing evaporation of antiserum during indirect immunocytochemical staining. Stain Technol 53:289–290

    Google Scholar 

  • Rawdon BB (1979) Immunostaining of ɛ-cells in the rostral pars distalis and PAS-positive cells in the pars intermedia of a teleost (Sarotherodon mossambicus) by antisera to the mammalian prolactins. Gen Comp Endocrinol 37:374–382

    Google Scholar 

  • Rawdon BB, Andrew A (1979) An immunocytochemical study of the distribution of pancreatic endocrine cells in chicks, with special reference to the relationship between pancreatic polypeptide- and somatostatin-immunoreactive cells. Histochemistry 59:189–197

    Google Scholar 

  • Rawdon BB, Andrew A (1981) An immunocytochemical survey of endocrine cells in the gastrointestinal tract of chicks at hatching. Cell Tissue Res 220:279–292

    Google Scholar 

  • Rawdon BB, Andrew A (1988) Can proventricular mesenchyme promote differentiation of endocrine cells in gizzard endoderm? Cell Differ Dev 25:135–144

    Google Scholar 

  • Rawdon BB, Kramer B, Andrew A (1984) The distribution of endocrine cell progenitors in gut of chick embryos. J Embryol Exp Morphol 82:131–145

    Google Scholar 

  • Skalli O, Ropraz P, Trzeciak A, Benzonana G, Gillessen D, Gabbiani G (1986) A monoclonal antibody against α-smooth muscle actin: a new probe for smooth muscle differentiation. J Cell Biol 103:2787–2796

    Google Scholar 

  • Stein BA, Andrew A (1989) Differentiation of endocrine cells in chick allantoic epithelium combined with pancreatic mesenchyme. Cell Differ Dev 26:173–180

    Google Scholar 

  • Sumiya M (1976a) Localization of autodifferentiation potencies in the early endoderm of the chick embryo. J Fac Sci Univ Tokyo Sect IV, 13:363–381

    Google Scholar 

  • Sumiya M (1976b) Differentiation of the digestive tract epithelium of the chick embryo cultured in vitro enveloped in a fragment of the vitelline membrane, in the absence of mesenchyme. Wilhelm Roux' Arch Entwicklungsmech Org 179:1–17

    Google Scholar 

  • Sumiya MM, Mizuno T (1974) Différenciation de l'endoderme de tractus digestif de l'embryon de poulet cultivé in vitro dans une membrane vitelline en l'absence du mésenchyme. CR Acad Sci (Paris) 278:1529–1532

    Google Scholar 

  • Sumiya MM, Mizuno T (1976) Development of the autodifferentiation potencies in the endoderm of the chick embryo. Proc Jap Acad 52:587–590

    Google Scholar 

  • Vaillant C, Dockray G, Walsh JH (1979) The avian proventriculus is an abundant source of endocrine cells with bombesin-like immunoreactivity. Histochemistry 64:307–314

    Google Scholar 

  • Wiertz-Hoessels EL, Hara K, Hekking JW, van Straaten HW, Thors F, Drukker (1987) Differentiation of gut endoderm in dependence of the notochord. Anat Embryol 176:337–343

    Google Scholar 

  • Wolff E (1961) Utilisation de la membrane vitelline de l'oeuf de poule en culture organotypique — techniques et possibilités. Dev Biol 3:767–786

    Google Scholar 

  • Yanaihara N, Yanaihara C, Nagai K, Sato H, Shimizu F, Yamaguchi K, Abe K (1980) Motilin immunoreactivity in porcine, canine, human and rat tissues. Biomed Res 1:76–83

    Google Scholar 

  • Yasugi S, Kedinger M, Simon-Assmann P, Bouziges F, Haffen K (1989) Differentiation of proventricular epithelium in xenoplastic associations with mesenchymal or fibroblastic cells. Roux' Arch Dev Biol 198:114–117

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Andrew, A., Rawdon, B.B. Can a non-gut mesenchyme support differentiation of gut endocrine cells?. Anat Embryol 185, 509–516 (1992). https://doi.org/10.1007/BF00174088

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00174088

Key words

Navigation