Hormonal Regulation of the Rat Small Intestine: Responsiveness of Villus and Crypt Cells to Insulin during the Suckling Period and Unresponsiveness after Weaning

Buts, Jean-Paul; Dekeyser, Nadine; Kolanowski, Jaroslaw; Hoof, F. Van

doi:10.1203/00006450-199002000-00015

Cited by 40 publications

(30 citation statements)

References 13 publications

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“…Blunting and shortening of villi were recorded after 4 weeks of soya feeding [30]. But [28]; tri-iodo-thyronine [34]; insulin [2]), growth factors (EGF, IGF, TGF [27]) and polyamines [13].…”

Section: Histomorphometrymentioning

confidence: 99%

Morphology and enzyme activities of the small intestine are modulated by dietary protein source in the preruminant calf

Montagné¹,

Toullec²,

Savidge³

et al. 1999

Reprod. Nutr. Dev.

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-A study was undertaken to assess the impact of the protein nature and soya antigenicity on the morphology and some enzyme activities of the jejunum in preruminant calves. Twenty Holstein calves fitted with a duodenal cannula were fed a liquid diet based on skimmed milk powder (SMP) for 2 weeks. They were then switched onto diets containing a mixture of SMP and either antigenic heated soybean flour (HSF; n = 12) or hypo-antigenic soya protein concentrate (SPC; n = 8) for 8 weeks, after which they were reverted back to the SMP diet for 2 weeks. The diets contained similar amounts of digestible nitrogen and energy, and were fed at a rate of 55 g DM/kg o . 75/d. Proximal jejunal biopsies were collected just before (week 0), during (weeks 2 and 8) and after (week 10) feeding of the soya-based diets, and were used for morphology measurements and the determination of total alkaline phosphatase, lactase, amino-peptidases A and N, and dipeptidyl peptidase IV activities. Feed intake and growth were similar between the HSF and SPC groups during the experimental period. The effects of antigenicity and the antigenicity x time interaction were never significant (P > 0.05). Villus height decreased (P < 0.01) between weeks 0 and 2, and increased (P < 0.05) between weeks 8 and 10. Villus width increased between weeks 2 and 8 (P < 0.001 Crypt depth also increased between weeks 0 and 2 (P < 0.001 Specific activities of alkaline phosphatase (P < 0.01) and amino-peptidase N (P < 0.05) decreased between weeks 0 and 2. Conversely, those of alkaline phosphatase (P < 0.0001 ), lactase (P < 0.01) and dipeptidyl-peptidase IV (P < 0.0001) increased between weeks 8 and 10. Specific activities for lactase and amino-peptidase N decreased (P < 0.01) between weeks 2 and 8.

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Section: Histomorphometrymentioning

confidence: 99%

Morphology and enzyme activities of the small intestine are modulated by dietary protein source in the preruminant calf

Montagné¹,

Toullec²,

Savidge³

et al. 1999

Reprod. Nutr. Dev.

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“…At this time, plasma insulin levels rise markedly (2), whereas milk-borne insulin is still active (3), allowing optimal interaction of the hormone with intestinal IR, which are located on both endoluminal and basolateral membranes of the cell (4). After weaning, the 2-fold decrease in IR concentration is associated with a reduction in responsiveness of mature enterocytes to the hormone (1,5). Our recent studies (6,7) suggest that the premature induction of SI is triggered by the binding of the hormone to the extracellular ␣-receptor subunit, allowing autophosphorylation of the tyrosine-kinase intrinsic to the juxtamembrane and cytoplasmic domains of the ␤-receptor subunit.…”

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confidence: 99%

“…We conclude that the ontogenic expression of brush border membrane hydrolases and their premature stimulation by insulin are regulated at least in part by the activation of p44/p42 ERKs but not by p38 MAP kinase. The onset of weaning (d 14 -17) in the suckling rat is a critical period during which immature enterocytes exhibit elevated responsiveness to insulin (1). At this time, plasma insulin levels rise markedly (2), whereas milk-borne insulin is still active (3), allowing optimal interaction of the hormone with intestinal IR, which are located on both endoluminal and basolateral membranes of the cell (4).…”

mentioning

confidence: 99%

“…Several studies conducted in vivo and in vitro (1,(5)(6)(7)33) have demonstrated that exogenous insulin is able to induce prematurely (before weaning) sucrase activity, sucrase protein, and sucrase mRNA levels. Likewise, in suckling and weaning rats, exogenous insulin stimulates the ontogenic expression of lactase and maltase with enzyme responses proportional to the dose of insulin given (6).…”

mentioning

confidence: 99%

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Ontogeny of MAP Kinases in Rat Small Intestine: Premature Stimulation by Insulin of BBM Hydrolases Is Regulated by ERKs but not by p-38 MAP Kinase

Marandi

2002

Pediatric Research

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Although mitogen-activating protein (MAP) kinases are crucial signal transduction molecules regulating cellular proliferation, differentiation, and morphology, their ontogenic changes in the small intestine have not been analyzed. Also, it remains unknown which pathway of activated MAP kinases regulates the expression of brush border membrane hydrolases during growth. Therefore, we have analyzed the mucosal distribution, ontogeny, and responses to insulin and to inhibitors of p44, p42, and p38 MAP kinases in immature and mature enterocytes using Western blot analysis and autoradiography after immunoprecipitation, immunohistochemistry, and in vitro phosphorylation assays. Between d 10 and 40 postpartum, diphosphorylated active p44/p42 extracellular regulated protein kinases (ERKs) increased in abundance compared with total immunoprecipitated ERKs, and were highly responsive to exogenous insulin. In concordance, ERK total activity increased by 4-fold during the same period of growth and was further enhanced 2-fold by exogenous insulin. In weaning rats, ERKs were mainly located in membranes of villus cells and with less intensity in crypt cells. By contrast, p38 MAP kinase was unresponsive to insulin and was confined to nuclei. Administration to sucklings of PD 098059, a specific inhibitor of ERKs, not only inhibited the premature stimulation of sucrase, lactase, and maltase total activities in response to exogenous insulin, but also depressed the natural expression of these brush border membrane enzymes in the absence of insulin stimulation.In concordance, administration of SB 203580, a specific inhibitor of p38 MAP kinase, failed to inhibit both the response of brush border membrane hydrolases to insulin and their natural expression in the absence of insulin stimulation. We conclude that the ontogenic expression of brush border membrane hydrolases and their premature stimulation by insulin are regulated at least in part by the activation of p44/p42 The onset of weaning (d 14 -17) in the suckling rat is a critical period during which immature enterocytes exhibit elevated responsiveness to insulin (1). At this time, plasma insulin levels rise markedly (2), whereas milk-borne insulin is still active (3), allowing optimal interaction of the hormone with intestinal IR, which are located on both endoluminal and basolateral membranes of the cell (4). After weaning, the 2-fold decrease in IR concentration is associated with a reduction in responsiveness of mature enterocytes to the hormone (1, 5). Our recent studies (6, 7) suggest that the premature induction of SI is triggered by the binding of the hormone to the extracellular ␣-receptor subunit, allowing autophosphorylation of the tyrosine-kinase intrinsic to the juxtamembrane and

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“…The development of the small intestine is regulated by, among other things, hormonal factors (12,(17)(18)(19)(20)(21)(22) and maturation factors such as polyamines (23)(24)(25)(26), which are found in milk and the postweaning diet, and are vital for the functioning and renewal of the gut epithelium. The role of polyamines in growth and differentiation is particularly important (27).…”

mentioning

confidence: 99%

Polyamine Participation in the Maturation of Glycoprotein Fucosylation, but not Sialylation, in Rat Small Intestine

Biol-N’garagba

2002

Pediatric Research

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The aim of this study was to determine the role of polyamines in the diet-related maturation of the intestinal glycoprotein glycosylation during postnatal development in the rat. The activity of ␣-2,6-sialyltransferase and the sialylated forms of glycoproteins in the intestinal brush-border membranes were found to decrease considerably after weaning, in parallel with the intestinal level of putrescine. By contrast, the activity of ␣-1,2-fucosyltransferases, the mRNA levels for two ␣-1,2-fucosyltransferase genes, FTA and FTB, and the fucosylated forms of glycoproteins all increased after weaning, in parallel with the levels of spermidine and spermine. These results suggest a possible role of polyamines in the evolution of glycosylation. The treatment of suckling rats with spermidine or spermine reproduced the high intestinal levels of these polyamines corresponding to those normally found after weaning. After these treatments, a rise in the activity of the ␣-1,2-fucosyltransferase was observed, associated with a fall in ␣-L-fucosidase activity. The ␣-1,2-fucosyltransferase FTB gene was found to be regulated at the transcriptional level, but not by its inhibitor, fuctinin. The result of these variations was the precocious appearance of several ␣-1,2-fucoproteins, which are normally found in brushborder membranes after weaning. The treatment of suckling rats with putrescine, which induced only a transitory rise in intestinal putrescine, had a similar but weaker effect on the fucosylation process than spermidine or spermine, and treatment with ornithine was ineffective. ␣-2,6-Sialylation was not affected by any of the treatments. Spermidine and spermine turned out to be more effective than putrescine for intestinal glycoprotein fucosylation, but did not affect their sialylation. Spermidine and spermine, whose intestinal levels where found to increase at weaning time, may have been partly responsible for the natural evolution of the intestinal glycoprotein fucosylation that occurred during this period. The rat small intestine is immature until the end of the third week of life, when the weaning period begins. Intestinal maturation is associated with morphologic changes, an increase in mucus production, immunologic adaptation to new microbial and nutritional antigenic contents (1), and digestive adaptation to new nutriments (2).Two types of glycoproteins play important functional roles in the small intestine. Mucins (secreted by the goblet cells) are different in composition between neonatal and mature rats, especially as regards their glycan chains (3). In the neonate, these changes may affect the permeability (4) and the barrier function of the intestine, and consequently may favor infections (5) and food allergies (6). At the apical enterocyte level, in the brush-border membranes, most of the digestive enzymes (lactase, sucrase, maltase, aminopeptidase, alkaline phosphatase) are glycoproteins whose activity changes a great deal at weaning time to enable the animal to cope with the adult solid diet (2). A shift from...

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Hormonal Regulation of the Rat Small Intestine: Responsiveness of Villus and Crypt Cells to Insulin during the Suckling Period and Unresponsiveness after Weaning

Cited by 40 publications

References 13 publications

Morphology and enzyme activities of the small intestine are modulated by dietary protein source in the preruminant calf

Morphology and enzyme activities of the small intestine are modulated by dietary protein source in the preruminant calf

Ontogeny of MAP Kinases in Rat Small Intestine: Premature Stimulation by Insulin of BBM Hydrolases Is Regulated by ERKs but not by p-38 MAP Kinase

Polyamine Participation in the Maturation of Glycoprotein Fucosylation, but not Sialylation, in Rat Small Intestine

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