Summary
The morphological and cytochemical modifications taking place during the first days of neonatal life have been studied at the ultrastructural level in the duodenum of mice. In the first week, the supranuclear part of the absorbing cells is formed by a network of smooth tubules and vacuoles connected with each other. Most of these formations show alkaline phosphatase activity. Below this zone, a cluster of dense tubules and dense bodies, already described in the last days of foetal life, (Hugon and Borgers, 1969) is situated above the Golgi apparatus and the nucleus. Alkaline and acid phosphatase activities are present in this cluster but the Golgi cisternae and vesicles are negative for both enzymes.
During the second week, the supranuclear zone of the absorbing cells presents striking modifications with formations of autophagic vacuoles and disappearance of the network of smooth profiles. However, the phosphatase activities are still present on the remaining dense tubules and dense bodies. On the sixteenth day, the morphological structure of the absorptive cells is rather similar to that observed in the full-grown gut. Alkaline phosphatase appears in the Golgi cisternae and acid phosphatase in the Golgi vesicles. These findings are briefly discussed in relation to the absorption of proteins by the neonatal gut and to the concept of the vacuolar apparatus.
Similar content being viewed by others
References
Anderson, J., Leissring, J.: The transfer of serum proteins from mother to young in the guinea-pig. 11 — Histochemistry of tissues involved in prenatal transfer. Amer. J. Anat. 109, 157–173 (1961).
Batt, E. R.: Sulfate accumulation by mouse intestine: influence of age and other factors. Amer. J. Physiol. 217, 1101–1104 (1961).
—, Schachter, D.: Developmental pattern of some intestinal transport mechanisms in newborn rats and mice. Amer. J. Physiol. 216, 1064–1068 (1969).
Bjorkman, N., Sibalin, M.: Acid phosphatase activity in cytoplasmic bodies of the absorbing intestinal cells from suckling pigs. Experientia (Basel) 23, 339 (1967).
Brambell, F. W.: The transmission of immunity from mother to young and the catabolism of immunoglobulins. Lancet 1966 II, 1084–1092.
Clarke, R., Hardy, R.: An analysis of the mechanism of cessation of uptake of macro-molecular substances by the intestine of the young rat. J. Physiol. (Lond.) 204, 127–136 (1969).
Cornell, R., Padykula, H. A.: A cytological study of intestinal absorption in the suckling rat. sAmer. J. Anat. 125, 291–316 (1969).
Danovitch, S. H., Laster, L.: The development of arylsulphatase in the small intestine of the rat. Biochem. J. 114, 343–350 (1969).
De Duve, Ch.: The lysosome in retrospect. In: Lysosomes in biology and pathology, edit. by Dingle, J., and Fell, H., vol. 3, p. 42. Amsterdam: North-Holland Publisher. 1969.
—, Wattiaux, R.: Functions of lysosomes. Ann Rev. Physiol. 28, 435–492 (1966).
Dunn, F. S.: The fine structure of the absorptive epithelial cells of the developing small intestine of the rat. J. Anat. (Lond.) 101, 57–68 (1967).
El-Aaser, A. A., Reid, E.: Phosphatase activities in rat liver before and after birth. Histochem. J. 1, 439–458 (1969).
Etzler, M. E.: An immunological investigation of alkaline phosphatases in the developing mouse intestine. Ann Arbor, Michigan, U.S.A.: A. Xerox & Company 1969.
Etzler, M. E., Moog, F.: Biochemical identification and characterization of the multiple forms of alkaline phosphatase in the developing duodenum of the mouse. Develop. Biol. 18, 515–535 (1969).
Gallacher, N. D.: Mechanism and site of vitamin B12 absorption in suckling rats. Nature (Lond.) 222, 877–878 (1969).
Graney, D. O.: The uptake of ferritin by ileal absorptive cells in suckling rats. An electron microscope study. Amer. J. Anat. 123, 227–253 (1968).
Grey, R. D.: Epithelial cell migration in the intestine of the young mouse. Develop. Biol. 18, 501–514 (1968).
Halliday, R.: The effect of steroid hormones on the absorption of antibody by the young rat. J. Endocr. 18, 64 (1959).
Hardy, R.: The influence of specific chemical factor in the solvent on the absorption of macromolecular substances from the small intestine of the new-born calf. J. Physiol. (Lond.) 204, 607–632 (1969).
—: The absorption of polyvinyl pyrrolidone by the new-born pig intestine. J. Physiol. (Lond.) 204, 633–651 (1969).
Hayward, A. F.: Changes in fine structure of developing intestinal epithelium associated with pinocytosis. J. Anat. (Lond.) 102, 57–70 (1967).
Hill, R. B., Prosper, J., Hirschfield, J. S., Kern, F.: Protein starvation and the small intestine. 1. The growth and morphology of the small intestine in weanling rats. Exp. molec. Path. 8, 66–74 (1968).
Holman, J.: Fine structure and dimensions of intestinal microvilli during the early post-incubation period in chickens. Z. mikr.-anat. Forsch. 79, 14–26 (1968).
Hugon, J. S., Borgers, M.: Ultrastructural differentiation and enzymatic localization of phosphatases in the developing duodenal epithelium of the mouse. I. The foetal mouse. Histochemie 19, 13–30 (1969).
Jordan, S. M., Morgan, E. H.: The development of selectivity of protein absorption from the intestine during suckling in the rat. Aust. J. exp. Biol. med. Sci. 46, 465–472 (1968).
Kenworthy, R., Stubbs, J. M., Syme, G.: Ultrastructure of small-intestinal epithelium in weaned and unweaned pigs and pigs with post-weaning diarrhoea. J. Path. Bact. 93, 493–498 (1967).
Koldovsky, O., Heringova, A., Jirsova, V., Chytil, F., Hoskova, J.: Postnatal changes in galactosidase activity in the jejunum and ileum of mice rabbits, and guinea pigs. Canad. J. Biochem. 44, 523–527 (1966).
—, Sunshine, P., Kretchmer, N.: Cellular migration of intestinal epithelia in suckling and weaned rats. Nature (Lond.) 212, 1389–1390 (1966).
Kraehenbuhl, J. P., Campiche, M. A.: Early stages of intestinal absorption of specific antibodies in the newborn. An ultrastructural, cytochemical, and immunological study in the pig, rat, and rabbit. J. Cell Biol. 42, 345–365 (1969).
Lecce, J.: Absorption of macromolecule by neonatal intestines. Biol. Neonat. 9, 50–61 (1966).
Lipkin, M., Deschner, E.: Comparative analysis of cell renewal in the gastrointestinal tract of newborn hamster. Exp. Cell Res. 49, 1–12 (1968).
Maggi, V., Carbonnell, A. W.: Lysosomes and acid phosphatases during growth and differentiation in mice: a light and electron microscope study. Histochem. J. 1, 383–403 (1969).
Masnerova, M., Koldovsky, O., Kubat, K.: Postnatal changes in phosphatase and non-specific esterase activity in the large intestine of the rat. Experienta (Basel) 22, 518 (1966).
Merrill, T. G., Sprinz, H., Tousimis, A. J.: Changes of intestinal absorptive cells during maturation: an electron microscopic study of prenatal, postnatal, and adult guinea pig ileum. J. Ultrastruct. Res. 19, 304–326 (1967).
Millington, P. F., Brown, A. C.: Electron microscope studies of the distribution of phosphatases in rat intestinal epithelium from birth to ten days after weaning. Histochemie 8, 109–121 (1967).
Moog, F.: The regulation of alkaline phosphatase activity in the duodenum of the mouse from birth to maturity. J. exp. Zool. 181, 353–368 (1966).
—, Grey, R. D.: A system regulating alkaline phosphatase activity in the duodenum of the chick embryo and mouse. Biol. Neonat. 9, 10–23 (1965/66).
—: Alkaline phosphatase isozymes in the duodenum of the mouse: attainment of pattern of spatial distribution in normal development and under the influence of cortisone or actinomycin D. Develop. Biol. 18, 481–500 (1968).
—, Vire, H. R., Grey, R. D.: The multiple forms of alkaline phosphatase in the small intestine of the young mouse. Biochim. biophys. Acta (Amst.) 113, 336–349 (1966).
Nordstrom, C., Koldovsky, O., Dahlovist, A.: Localization of β-Galactosidases and acid phosphatase in the small intestinal wall comparison of adult and suckling rat. J. Histochem. Cytochem. 17, 341–347 (1969).
O'Connor, T. M.: Cell dynamics in the mouse from late fetal life to maturity. Amer. J. Anat. 118, 525–536 (1966).
Overton, J.: Fine structure of the free cell surface in developing mouse intestinal mucosa. J. exp. Zool. 159, 195–202 (1965).
—, Shoup, J.: Fine structure of cell surface specilizations in the maturing duodenal mucosa of the chick. J. Cell Biol. 21, 75–85 (1964).
Payne, F. C., Marsh, C. L.: Absorption of gamma globulin by the small intestine. Fed. Proc. 21, 909–912 (1962).
Penttila, A., Gripenberg, J.: Fine structure and enzyme histochemistry of developing duodenal epithelium of the chicken. Z. Anat. Entwickl.-Gesch. 129, 109–127 (1969).
Sibalin, M., Bjorkman, N.: On the fine structure and absorptive function of the porcine jejunal villi during the early suckling. Exp. Cell Res. 44, 165–174 (1966).
Staley, T. E., Jones, E. W., Marshall, A. E.: The jejunal absorptive cell of the newborn pig: an electron microscopic study. Anat. Rec. 161, 497–516 (1968).
Trasher, J. D., Greulich, R. C.: The duodenal progenitor population 11. Age related changes in size and distribution. J. exp. Zool. 159, 385–396 (1965).
Vodovar, N.: Intestin grêle du porc 11. Structure histologique des parois et plus particulièrement de la tunique muqueuse en fonction de l'age de l'animal. Ann. Biol. anim. 4, 113–139 (1964).
Vollrath, L.: Über die Bildung von Lysosomen im fetalen Dünndarm. Experienta (Basel) 24, 471 (1968).
—: Über die Entwicklung des Dünndarms der Ratte. Advanc. Anat. Embryol. and Cell Biol. 41, 2–70 (1969).
Williams, R. M., Beck, F.: A histochemical study of gut maturation. J. Anat. (Lond.) 105, 487–501 (1969).
Wissig, S. L., Graney, D. O.: Membrane modifications in the apical endocytic complex of ileal epithelial cells. J. Cell Biol. 39, 564–579 (1968).
Author information
Authors and Affiliations
Additional information
This work was supported by the grant no. N. D. G./27 from the Medical Research Council of Canada.
The author is greatly indebted to Dr. R. Côté, M. D. and Dr. N. Brière for their critical reading of the manuscript, and to Mr. M. Borgers and Mr. M. Couture for their skillful technical aid.
Rights and permissions
About this article
Cite this article
Hugon, J.S. Ultrastructural differentiation and enzymatic localization of phosphatases in the developing duodenal epithelium of the mouse. Histochemie 22, 109–124 (1970). https://doi.org/10.1007/BF00303622
Received:
Issue Date:
DOI: https://doi.org/10.1007/BF00303622