In vitro study of the intestinal brush border enzyme activities in developing anuran amphibian: Effects of thyroxine, cortisol, and insulin
J. C. Pouyet
Department of Vertebrate Biology, Orsay Center, Paris South University, 91405 Orsay, France
Search for more papers by this authorJ. Hourdry
Department of Vertebrate Biology, Orsay Center, Paris South University, 91405 Orsay, France
Search for more papers by this authorJ. C. Pouyet
Department of Vertebrate Biology, Orsay Center, Paris South University, 91405 Orsay, France
Search for more papers by this authorJ. Hourdry
Department of Vertebrate Biology, Orsay Center, Paris South University, 91405 Orsay, France
Search for more papers by this authorAbstract
The effects of several hormones on intestinal brush border membrane enzymatic activities have been investigated in intestinal explants taken from the amphibian midwife toad at different developmental stages. Explants were treated for at least 2 days with thyroxine (0.1 μg/ml of culture medium) or for 2 days with cortisol (25 μg/ml) or insulin (6 mU/ml). The hydrolases examined were maltase, trehalase, glucoamylase, and alkaline phosphatase. In the explants from tadpoles in prometamorphosis, thyroxine had no effect on hydrolase activities; cortisol increased the activity of only glucoamylase, and insulin increased activity of maltase, glucoamylase, and alkaline phosphatase. When the explants were taken from tadpoles at the beginning of climax, cortisol and insulin generally stimulated the enzyme activities studied. When taken from tadpoles at the end of climax, at the moment when the embryonic cells under the degenerating epithelium divide, cortisol and insulin had little effect on these activities. When the animals terminate their metamorphosis, the intestinal epithelium of the explants is totally newly formed (secondary epithelium). At this time, cortisol stimulated the activities of maltase, glucoamylase, and alkaline phosphatase, while insulin decreased the activities of maltase and glucoamylase.
Literature Cited
- Black, B. L., and F. Moog, (1978) Alkaline phosphatase and maltase activity in the embryonic chick intestine in culture. Influence of thyroxine and hydrocortisone. Dev. Biol., 66: 232–249.
- Broyles, R. H. (1981) Changes in the blood during amphibian metamorphosis. In: Metamorphosis, a Problem in Developmental Biology. L. I. Gilbert and E. Frieden eds. Plenum Press, New York, pp. 461–490.
- Cheng-Kaung, H. L. (1983) Changes in pancreatic beta cell population during larval development of Rana pipiens. Gen. Comp. Endocrinol., 49: 50–56.
- Chieffi, G., and M. Carfagna (1960) The alkaline phosphatase of the intestinal epithelium of Bufo vulgaris tadpoles during metamorphosis. The influence of hydrocortisone in the epithelial phosphatase in vitro. Acta Embryol. Morphol. Exp., 3: 213–220.
- Dahlqvist, A. (1964) Method for assay of intestinal disaccharidases. Anal. Biochem., 7: 18–25.
- Dauça, M., J., Hourdry, J. S. Hugon, and D. Menard (1980) Amphibian intestinal brush border enzymes during thyroxine induced metamorphosis. A biochemical and cytochemical study. Histochemistry, 70: 32–42.
-
Dodd, M. H. I., and
J. M. Dodd
(1976)
The biology of metamorphosis. In:
Physiology of Amphibia.
B. Lofts, ed.
Acad. Press,
New York,
Vol. 3,
pp. 467–599.
10.1016/B978-0-12-455403-0.50015-3 Google Scholar
- Eichholz, A. (1967) Structural and functional organization of the brush border of the intestinal epithelial cells. III. Enzymic activities and chemical composition of various fractions of trisrupted brush borders. Biochim. Biophys. Acta, 735: 475–482.
- El Maraghi-Ater, H., J. Mesnard and J. Hourdry (1986) Hormonal control of the intestinal brush border enzyme activities in developing anuran amphibians. I. Effects of hydrocortisone and insulin during spontaneous metamorphosis. Gen. Comp. Endocrinol., 61: 53–63.
- Frye, B. E. (1964) Metamorphic changes in the blood sugar and the pancreatic islets of the frog, Rana clamitans. J. Exp. Zool., 755: 215–224.
- Grassi-Milano, E., P., Cianfoni, and F. Accordi (1979) The stibling cells of the adrenal gland of Rana esculenta complex during embryonal development and metamorphosis. Riv. Biol., 72: 309–328.
-
Hanke, W., and
U. Neuman
(1972)
Carbohydrate metabolism in amphibia.
Gen. Comp. Endocrinol. [Suppl.]
3:
198–208.
10.1016/0016-6480(72)90149-9 Google Scholar
- Hourdry, J., and A. Beaumont (1985) Les Métamorphoses des Amphibiens. Singer-Polignac, Masson, Paris.
- Hourdry, J., J. G. Chabot, D. Ménard, and J. S. Hugon (1979) Intestinal brush border enzyme activities in developing amphibian Rana catesbeiana. Comp. Biochem. Physiol [A], 63A: 121–125
- Hsu, S. Y., N. W., Yu, and S. J. Chen (1980) Development of Δ 5-3β-hydroxysteroid dehydrogenase activity in the interrenal gland of Rana catesbeiana. Gen. Comp. Endocrinol., 42: 167–170.
- Hulsebus, J., and E. S. Farrar (1985) Insulin-like immunoreactivity in serum and pancreas of metamorphosing tadpoles. Gen. Comp. Endocrinol., 58: 114–119.
- Jaffe, R. C. (1981) Plasma concentration of corticosterone during Rana catesbeiana tadpole metamorphosis. Gen. Comp. Endocrinol., 44: 314–318.
- Jolivet-Jaudet, G., and J. Leloup-Hatey (1984) Variations in aldosterone and corticosterone plasma levels during metamorphosis in Xenopus laevis tadpoles. Gen. Comp. Endocrinol., 56: 59–65.
- Kedinger, M., P. M., Simon, F. Raul, J. F. Grenier, and K. Haffen (1980) The effect of dexamethasone on the development of rat intestinal brush border enzymes in organ culture. Dev. Biol., 74: 9–21.
- Kedinger, M., P. M., Simon-Assmann, B. Lacroix, and K. Haffen (1983) Role of glucocorticoids on the maturation of brush border enzymes in fetal rat gut endoderm. Experientia, 39: 1150–1152.
- Krug, E. C., K. V., Honn, J. Battista and C. S. Nicoll (1983) Corticosteroids in serum of Rana catesbeiana during development and metamorphosis. Gen Comp. Endocrinol., 52: 232–241.
- Leibovitz, A. (1963) The growth and maintenance of tissue-cell culture in free gaz exchange with atmosphere. Am. J. Hyg., 78: 173–180.
- Lloyd, J. B., and W. J. Whelan (1969) An improved method for enzymic determination of glucose in the presence of maltose. Anal. Biochem., 30: 467–470.
-
Lowry, O. H.,
N. J., Posebrough,
A. L. Farr, and
R. J. Randall
(1951)
Protein measurement with the Folin phenol reagent.
J. Biol. Chem.,
793:
265–275.
10.1016/S0021-9258(19)52451-6 Google Scholar
- Martin, G. R., and S. J. Henning (1982) Relative importance of corticosterone and thyroxine in the postnatal development of sucrase and maltase in rat small intestine. Endocrinology, 3: 912–918.
- Ménard, D., and C. Malo (1979) Insulin-evoked precocious appearance of intestinal sucrase activity in suckling mice. Dev. Biol., 69: 661–665.
- Ménard, D., C., Malo and R. Calvert (1981) Insulin accelerates the development of intestinal brush border hydrolytic activities of suckling mice. Dev. Biol., 85: 150–155.
- Monnickendam, M. A., J. L., Millar, and M. Balls (1970) Cell proliferation in vivo and in vitro in visceral organs of the adult newt Triturus cristatus carnifex. J. Morphol., 132: 453–460.
- Monnickendam, M. A. and M., Balls (1973) Amphibian organ culture. Experientia, 29: 1–17.
- Pouyet, J. C. (1979) La Métamorphose in vitro des Amphibiens Anoures. Etude en Cultures Organotypiques, de la Queue, du Pancréas, de l'Intestin et de l'Estomac d'Alytes obstetricans L. et Discoglossus pictus O., en Présence de Thyroxine. Thése de Doctorat d'Etat, Orsay, France.
- Pouyet, J. C., and A. Beaumont (1975) Ultrastructure du pancréas larvaire d'un Amphibien Anoure, Alytes obstetricans L., en culture organotypique. C.R. Soc. Biol. (Paris) 169: 546–550.
- Pouyet, J. C., and J. Hourdry (1977) Effet de la thyroxine sur la structure des épithéliocytes intestinaux en culture organotypique, chez la larve de Discoglossus pictus Otth (Amphibien Anoure). Biol. Cell., 29: 123–134.
- Pouyet, J. C., and J. Hourdry (1980) Effet de la thyroxine sur la proliferation des épithéliocytes intestinaux en culture organotypique, chez la larve du crapaud-accoucheur (Alytes obstetricans Laurenti). Biol. Cell., 38: 237–242.
- Rapola, J. (1963) The adrenal cortex and metamorphosis of Xenopus laevis Daudin. Gen. Comp. Endocrinol., 3: 412–421.
- Robertson, D. R. (1975) The in vitro transport of calcium by the frog intestine and the effect of vitamin D3. Comp. Biochem. Physiol. [A], 51: 705–710.
- Schlegel-Haueter, S., P., Hore, K. R. Kerry and G. Semenza (1972) The preparation of lactase and glucoamylase of rat small intestine. Biochim. Biophys. Acta, 258: 506–519.
- Simon-Assmann, P. M., M., Kedinger, J. F. Grenier, and K. Haffen (1982a) Control of brush border enzymes by dexamethasone in the fetal rat intestine cultures in vitro. J. Pediatr. Gastroenterol. Nutr., 7: 257–265.
- Simon-Assman, P. M., M., Kedinger, F. Raul, J. F. Grenier and K. Haffen (1982b) Organ culture of suckling rat intestine: Comparative study of various hormones on brush border enzymes. In Vitro 18: 339–346.
- Taylor, A. C., and J. J. Kollros (1946) Stages in the normal development of Rana pipiens larvae. Anat. Rec., 94: 7–23.
- Wolf, K., and M. C. Quimby (1964) Amphibian cell culture: Permanent cell line from the bullfrog (Rana catesbeiana). Science, 144: 1578–1580.
- Yoshizawa, S., S., Moriuchi and N. Hosoya (1977) Induction of chick embryonic intestinal disaccharidases by hydrocortisone and sucrose in the organ culture system. J. Nutr. Sci. Vitaminol. (Tokyo), 23: 227–235.