Logo of jcellbiolHomeThe Rockefeller University PressEditorsContactInstructions for AuthorsThis issue
J Cell Biol. Jul 1, 1994; 126(1): 211–221.
PMCID: PMC2120088

Fetal endoderm primarily holds the temporal and positional information required for mammalian intestinal development

Abstract

In rodents, the intestinal tract progressively acquires a functional regionalization during postnatal development. Using lactase-phlorizin hydrolase as a marker, we have analyzed in a xenograft model the ontogenic potencies of fetal rat intestinal segments taken prior to endoderm cytodifferentiation. Segments from the presumptive proximal jejunum and distal ileum grafted in nude mice developed correct spatial and temporal patterns of lactase protein and mRNA expression, which reproduced the normal pre- and post-weaning conditions. Segments from the fetal colon showed a faint lactase immunostaining 8-10 d after transplantation in chick embryos but not in mice; it is consistent with the transient expression of this enzyme in the colon of rat neonates. Heterotopic cross-associations comprising endoderm and mesenchyme from the presumptive proximal jejunum and distal ileum developed as xenografts in nude mice, and they exhibited lactase mRNA and protein expression patterns that were typical of the origin of the endodermal moiety. Endoderm from the distal ileum also expressed a normal lactase pattern when it was associated to fetal skin fibroblasts, while the fibroblasts differentiated into muscle layers containing alpha-smooth- muscle actin. Noteworthy, associations comprising colon endoderm and small intestinal mesenchyme showed a typical small intestinal morphology and expressed the digestive enzyme sucrase-isomaltase normally absent in the colon. However, in heterologous associations comprising lung or stomach endoderm and small intestinal mesenchyme, the epithelial compartment expressed markers in accordance to their tissue of origin but neither intestinal lactase nor sucrase-isomaltase. A thick intestinal muscle coat in which cells expressed alpha-smooth- muscle actin surrounded the grafts. The results demonstrate that: (a) the temporal and positional information needed for intestinal ontogeny up to the post-weaning stage results from an intrinsic program that is fixed in mammalian fetuses prior to endoderm cytodifferentiation; (b) this temporal and positional information is primarily carried by the endodermal moiety which is also able to change the fate of heterologous mesodermal cells to form intestinal mesenchyme; and (c) the small intestinal mesenchyme in turn may deliver instructive information as shown in association with colonic endoderm; yet this effect is not obvious with nonintestinal endoderms.

Full Text

The Full Text of this article is available as a PDF (3.4M).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Auffray C, Rougeon F. Purification of mouse immunoglobulin heavy-chain messenger RNAs from total myeloma tumor RNA. Eur J Biochem. 1980 Jun;107(2):303–314. [PubMed]
  • Büller HA, Rings EH, Montgomery RK, Sybicki MA, Grand RJ. Suckling rat colon synthesizes and processes active lactase-phlorizin hydrolase immunologically identical to that from jejunum. Pediatr Res. 1989 Sep;26(3):232–236. [PubMed]
  • Dauça M, Bouziges F, Colin S, Kedinger M, Keller MK, Schilt J, Simon-Assmann P, Haffen K. Development of the vertebrate small intestine and mechanisms of cell differentiation. Int J Dev Biol. 1990 Mar;34(1):205–218. [PubMed]
  • Duluc I, Jost B, Freund JN. Multiple levels of control of the stage- and region-specific expression of rat intestinal lactase. J Cell Biol. 1993 Dec;123(6 Pt 1):1577–1586. [PMC free article] [PubMed]
  • Duluc I, Boukamel R, Mantei N, Semenza G, Raul F, Freund JN. Sequence of the precursor of intestinal lactase-phlorizin hydrolase from fetal rat. Gene. 1991 Jul 22;103(2):275–276. [PubMed]
  • Duluc I, Galluser M, Raul F, Freund JN. Dietary control of the lactase mRNA distribution along the rat small intestine. Am J Physiol. 1992 Jun;262(6 Pt 1):G954–G961. [PubMed]
  • Duprey P, Chowdhury K, Dressler GR, Balling R, Simon D, Guenet JL, Gruss P. A mouse gene homologous to the Drosophila gene caudal is expressed in epithelial cells from the embryonic intestine. Genes Dev. 1988 Dec;2(12A):1647–1654. [PubMed]
  • Ferguson A, Gerskowitch VP, Russell RI. Pre- and postweaning disaccharidase patterns in isografts of fetal mouse intestine. Gastroenterology. 1973 Feb;64(2):292–297. [PubMed]
  • Foltzer-Jourdainne C, Kedinger M, Raul F. Perinatal expression of brush-border hydrolases in rat colon: hormonal and tissue regulations. Am J Physiol. 1989 Oct;257(4 Pt 1):G496–G503. [PubMed]
  • Freund JN, Duluc I, Raul F. Discrepancy between the intestinal lactase enzymatic activity and mRNA accumulation in sucklings and adults. Effect of starvation and thyroxine treatment. FEBS Lett. 1989 May 8;248(1-2):39–42. [PubMed]
  • Freund JN, Duluc I, Foltzer-Jourdainne C, Gosse F, Raul F. Specific expression of lactase in the jejunum and colon during postnatal development and hormone treatments in the rat. Biochem J. 1990 May 15;268(1):99–103. [PMC free article] [PubMed]
  • Freund JN, Duluc I, Raul F. Lactase expression is controlled differently in the jejunum and ileum during development in rats. Gastroenterology. 1991 Feb;100(2):388–394. [PubMed]
  • Freund JN, Foltzer-Jourdainne C, Duluc I, Galluser M, Gosse F, Raul F. Rat lactase activity and mRNA expression in relation to the thyroid and corticoid status. Cell Mol Biol. 1991;37(4):463–466. [PubMed]
  • Freund JN, Boukamel R, Benazzouz A. Gradient expression of Cdx along the rat intestine throughout postnatal development. FEBS Lett. 1992 Dec 14;314(2):163–166. [PubMed]
  • Gordon JI. Understanding gastrointestinal epithelial cell biology: lessons from mice with help from worms and flies. Gastroenterology. 1993 Aug;105(2):315–324. [PubMed]
  • Gumpel-Pinot M, Yasugi S, Mizuno T. Différenciation d'épithéliums endodermiques associés au mésoderme splanchnique. C R Acad Sci Hebd Seances Acad Sci D. 1978 Jan;286(1):117–120. [PubMed]
  • Haffen K, Kedinger M, Simon-Assmann PM, Lacroix B. Mesenchyme-dependent differentiation of intestinal brush-border enzymes in the gizzard endoderm of the chick embryo. Prog Clin Biol Res. 1982;85(Pt B):261–270. [PubMed]
  • Hauri HP, Quaroni A, Isselbacher KJ. Monoclonal antibodies to sucrase/isomaltase: probes for the study of postnatal development and biogenesis of the intestinal microvillus membrane. Proc Natl Acad Sci U S A. 1980 Nov;77(11):6629–6633. [PMC free article] [PubMed]
  • Helander HF. Morphological studies on the development of the rat colonic mucosa. Acta Anat (Basel) 1973;85(2):155–176. [PubMed]
  • Izpisúa-Belmonte JC, Falkenstein H, Dollé P, Renucci A, Duboule D. Murine genes related to the Drosophila AbdB homeotic genes are sequentially expressed during development of the posterior part of the body. EMBO J. 1991 Aug;10(8):2279–2289. [PMC free article] [PubMed]
  • James R, Kazenwadel J. Homeobox gene expression in the intestinal epithelium of adult mice. J Biol Chem. 1991 Feb 15;266(5):3246–3251. [PubMed]
  • Jones FS, Holst BD, Minowa O, De Robertis EM, Edelman GM. Binding and transcriptional activation of the promoter for the neural cell adhesion molecule by HoxC6 (Hox-3.3). Proc Natl Acad Sci U S A. 1993 Jul 15;90(14):6557–6561. [PMC free article] [PubMed]
  • Kedinger M, Simon PM, Grenier JF, Haffen K. Role of epithelial--mesenchymal interactions in the ontogenesis of intestinal brush-border enzymes. Dev Biol. 1981 Sep;86(2):339–347. [PubMed]
  • Kedinger M, Simon-Assmann PM, Lacroix B, Haffen K. Role of glucocorticoids on the maturation of brush border enzymes in fetal rat gut endoderm. Experientia. 1983 Oct 15;39(10):1150–1152. [PubMed]
  • Kedinger M, Simon-Assmann PM, Lacroix B, Marxer A, Hauri HP, Haffen K. Fetal gut mesenchyme induces differentiation of cultured intestinal endodermal and crypt cells. Dev Biol. 1986 Feb;113(2):474–483. [PubMed]
  • Kedinger M, Simon-Assmann P, Bouziges F, Arnold C, Alexandre E, Haffen K. Smooth muscle actin expression during rat gut development and induction in fetal skin fibroblastic cells associated with intestinal embryonic epithelium. Differentiation. 1990 Apr;43(2):87–97. [PubMed]
  • Kendall K, Jumawan J, Koldovsky O, Krulich L. Effect of the host hormonal status on development of sucrase and acid beta-galactosidase in isografts of rat small intestine. J Endocrinol. 1977 Jul;74(1):145–146. [PubMed]
  • Kendall K, Jumawan J, Koldovský O. Development of jejunoileal differences of activity of lactase, sucrase and acid beta-galactosidase in isografts of fetal rat intestine. Biol Neonate. 1979;36(3-4):206–214. [PubMed]
  • Kubota S, Tashiro K, Yamada Y. Signaling site of laminin with mitogenic activity. J Biol Chem. 1992 Mar 5;267(7):4285–4288. [PubMed]
  • Lacroix B, Kedinger M, Simon-Assmann P, Rousset M, Zweibaum A, Haffen K. Developmental pattern of brush border enzymes in the human fetal colon. Correlation with some morphogenetic events. Early Hum Dev. 1984 Feb;9(2):95–103. [PubMed]
  • Le Douarin N, Bussonnet C. Détermination précoce et rôle inducteur de l'endoderme pharyngien chez l'embryon de poulet. C R Acad Sci Hebd Seances Acad Sci D. 1966 Oct 24;263(17):1241–1243. [PubMed]
  • Lefebvre O, Wolf C, Kédinger M, Chenard MP, Tomasetto C, Chambon P, Rio MC. The mouse one P-domain (pS2) and two P-domain (mSP) genes exhibit distinct patterns of expression. J Cell Biol. 1993 Jul;122(1):191–198. [PMC free article] [PubMed]
  • Martin GR, Henning SJ. Enzymic development of the small intestine: are glucocorticoids necessary? Am J Physiol. 1984 Jun;246(6 Pt 1):G695–G699. [PubMed]
  • Montgomery RK, Sybicki MA, Grand RJ. Autonomous biochemical and morphological differentiation in fetal rat intestine transplanted at 17 and 20 days of gestation. Dev Biol. 1981 Oct 15;87(1):76–84. [PubMed]
  • Nsi-Emvo E, Foltzer-Jourdainne C, Raul F, Gosse F, Duluc I, Koch B, Freund JN. Precocious and reversible expression of sucrase-isomaltase unrelated to intestinal cell turnover. Am J Physiol. 1994 Apr;266(4 Pt 1):G568–G575. [PubMed]
  • Paul T, Flatz G. Temporary depression of lactase activity by thyroxine in suckling rats. Enzyme. 1983;30(1):54–58. [PubMed]
  • Probstmeier R, Martini R, Tacke R, Schachner M. Expression of the adhesion molecules L1, N-CAM and J1/tenascin during development of the murine small intestine. Differentiation. 1990 Jul;44(1):42–55. [PubMed]
  • Quaroni A, Isselbacher KJ. Study of intestinal cell differentiation with monoclonal antibodies to intestinal cell surface components. Dev Biol. 1985 Oct;111(2):267–279. [PubMed]
  • Rings EH, de Boer PA, Moorman AF, van Beers EH, Dekker J, Montgomery RK, Grand RJ, Büller HA. Lactase gene expression during early development of rat small intestine. Gastroenterology. 1992 Oct;103(4):1154–1161. [PubMed]
  • Rubin DC, Swietlicki E, Roth KA, Gordon JI. Use of fetal intestinal isografts from normal and transgenic mice to study the programming of positional information along the duodenal-to-colonic axis. J Biol Chem. 1992 Jul 25;267(21):15122–15133. [PubMed]
  • Ruiz i Altaba A, Melton DA. Interaction between peptide growth factors and homoeobox genes in the establishment of antero-posterior polarity in frog embryos. Nature. 1989 Sep 7;341(6237):33–38. [PubMed]
  • Sakai K, Kweon MN, Kohri T, Kishino Y. Effects of pulmonary surfactant and surfactant protein A on phagocytosis of fractionated alveolar macrophages: relationship to starvation. Cell Mol Biol. 1992 Apr;38(2):123–130. [PubMed]
  • Simo P, Simon-Assmann P, Arnold C, Kedinger M. Mesenchyme-mediated effect of dexamethasone on laminin in cocultures of embryonic gut epithelial cells and mesenchyme-derived cells. J Cell Sci. 1992 Jan;101(Pt 1):161–171. [PubMed]
  • Simon-Assmann P, Kedinger M. Heterotypic cellular cooperation in gut morphogenesis and differentiation. Semin Cell Biol. 1993 Jun;4(3):221–230. [PubMed]
  • Sweetser DA, Hauft SM, Hoppe PC, Birkenmeier EH, Gordon JI. Transgenic mice containing intestinal fatty acid-binding protein-human growth hormone fusion genes exhibit correct regional and cell-specific expression of the reporter gene in their small intestine. Proc Natl Acad Sci U S A. 1988 Dec;85(24):9611–9615. [PMC free article] [PubMed]
  • Takahashi Y, Bontoux M, Le Douarin NM. Epithelio--mesenchymal interactions are critical for Quox 7 expression and membrane bone differentiation in the neural crest derived mandibular mesenchyme. EMBO J. 1991 Sep;10(9):2387–2393. [PMC free article] [PubMed]
  • Tsuboi KK, Castillo RO. Development of jejunoileal differences in rat intestine. J Pediatr Gastroenterol Nutr. 1989 Aug;9(2):140–143. [PubMed]
  • Winter HS, Hendren RB, Fox CH, Russell GJ, Perez-Atayde A, Bhan AK, Folkman J. Human intestine matures as nude mouse xenograft. Gastroenterology. 1991 Jan;100(1):89–98. [PubMed]
  • WOLFF E, HAFFEN K. Sur une methode de culture d'organes embryonnaires "in vitro". Tex Rep Biol Med. 1952;10(2):463–472. [PubMed]
  • Wolgemuth DJ, Behringer RR, Mostoller MP, Brinster RL, Palmiter RD. Transgenic mice overexpressing the mouse homoeobox-containing gene Hox-1.4 exhibit abnormal gut development. Nature. 1989 Feb 2;337(6206):464–467. [PubMed]
  • Yeh KY, Holt PR. Ontogenic timing mechanism initiates the expression of rat intestinal sucrase activity. Gastroenterology. 1986 Mar;90(3):520–526. [PubMed]
  • Zweibaum A, Hauri HP, Sterchi E, Chantret I, Haffen K, Bamat J, Sordat B. Immunohistological evidence, obtained with monoclonal antibodies, of small intestinal brush border hydrolases in human colon cancers and foetal colons. Int J Cancer. 1984 Nov 15;34(5):591–598. [PubMed]

Articles from The Journal of Cell Biology are provided here courtesy of The Rockefeller University Press

Formats:

Related citations in PubMed

See reviews...See all...

Cited by other articles in PMC

See all...

Links

  • MedGen
    MedGen
    Related information in MedGen
  • PubMed
    PubMed
    PubMed citations for these articles
  • Substance
    Substance
    PubChem Substance links

Recent Activity

Your browsing activity is empty.

Activity recording is turned off.

Turn recording back on

See more...