Intestinal development in the suckling rat: effect of insulin on the maturation of villus and crypt cell functions

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Abstract
The influence of insulin on the postnatal development of intestinal functions linked to villus cells (sucrase, lactase, maltase and aminopeptidase) and crypt cells (secretory component of immunoglobulins, SC) has been studied in suckling and weanling rats. At 9 days of age, the animals received a daily injection of insulin 12.5 mU g-1 body weight day-1 for 4 days. Compared with saline-treated controls, insulin had no effect on the development of the intestinal mucosal mass parameters determined in the jejunum, ileum and colon. A premature appearance of surcase was noted in isolated jejunal villus and crypt cells, the level of activity reached by the enzyme being dependent of the amount of insulin injected. By 6 and 12 h after a single injection of the hormone (12.5 mU g-1 body weight), sucrase activity was detected in all the cell fractions along the villus-crypt axis. In villus cells of insulin-treated rats, maltase, lactase and aminopeptidase activities were significantly (P < 0.001) increased (+201%, +50%, +207%, respectively, vs. controls), whereas the concentration of SC measured by a sensitive immunoradiometric assay was enhanced over the controls by 75% in villus cells, 83% in crypt cells and 172% in the liver. Weanling rats treated from day 10 to day 20 postpartum with 12.5 mU insulin also exhibited a higher intestinal production of SC (+ 93%, P < 0.01) than did saline controls. The administration of Actinomycin D to 9-day-old suckling rats 1 h after insulin injection completely inhibited the adaptative process to the hormone; the activities of sucrase, lactase, maltase and aminopeptidase measured in rats treated with Actinomycin D being equivalent to those recorded in saline controls. Our data demonstrate that: (i) a premature increase of the circulating level of insulin accelerates the maturation of intestinal functions linked to both villus and crypt cells; (ii) the response to the hormone occurs rapidly over the entire villus-crypt unit, whatever the degree of epithelial cellular differentiation; (iii) the stimulation of the synthesis of brushborder membrane enzymes by insulin appears to be regulated at the level of transcription.