Abstract
The postnatal development of intestine is associated with a decline in brush border lactase activity in rodents. This is similar to adulthood hypolactasia, a phenomenon prevalent in humans worldwide. In the present study, the effect of luminal proteases from adult rat intestine was studied in vitro on intestinal lactase activity in saline control, thyroxine, insulin and cortisone treated rat pups. Lactase levels were determined by enzyme analysis and Western blotting. mRNA levels encoding lactase were determined by Northern blotting. Administration of thyroxine for 4 days reduced (P < 0.05) lactase activity, but insulin treatment had no effect in 8-day-old rat intestine. However, cortisone administration augmented (P < 0.01) lactase activity, under these conditions. Western blot analysis showed decreased lactase signal corresponding to 220-kDa protein band in thyroxine treated animals. However, the intensity of lactase signal was high in cortisone treated animals compared to controls. mRNA levels encoding lactase showed a 6.8-kb mRNA transcript in saline and hormone treated rats. mRNA levels encoding lactase were increased in cortisone treated animals but were reduced in thyroxine injected pups compared to controls. Microvillus membranes from saline (P < 0.01) and thyroxine (P < 0.05) or insulin (P < 0.01) treated rats upon incubation with luminal wash from adult rat intestine showed a significant decline in lactase activity. These findings suggest that thyroxine, insulin or cortisone induced changes in lactase expression in suckling rat intestine make it susceptible to luminal proteases, which may in part be responsible for observed maturational decline in lactase activity in adult rat intestine.
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De Vrese MD, Stegelmann A, Richter B, Fenselau S, Laue C, Schrezenmeir J (2001) Probiotics-compensation for lactase insufficiency. Am J Clin Nutr 73:421S–429S
Kuokkanen M, Enattah NS, Oksanen A, Savilahti E, Orpana A, Jarvela I (2003) Transcriptional regulation of the lactase-phlorizin hydrolase gene by polymorphisms associated with adult-type hypolactasia. Gut 52:647–652
Buller HA, Rings EH, Pajkrt D, Montgomery RK, Grand RJ (1990) Glycosylation of lactasephlorizin hydrolase in rat small intestine during development. Gastroenterology 98:667–675
Dai D, Nanthakumar NN, Savidge TC, Newburg DS, Walker WA (2002) Region-specific ontogeny of alpha-2, 6-sialyltransferase during normal and cortisone-induced maturation in mouse intestine. Am J Physiol Gastrointest Liver Physiol 282: G480–G490
Nsi-Emvo E, Launay JF, Raul F (1987) Is adult-type hypolactasia in the intestine of mammals related to changes in the intracellular processing of lactase? Cell Mol Biol 33:335–344
Britton JR, Koldovsky O (1988) Development of luminal protein digestion in suckling and weanling rats. Biol Neonate 53:39–46
Kaur K, Mahmood S, Mahmood A (2006) The susceptibility of lactase to luminal proteases in developing rat intestine. Indian J Gastroenterol 25:179–181
Kessler M, Acuto O, Storelli C, Murer M, Semenza G (1978) A modified procedure for the rapid preparation of efficiently transporting vesicle from small intestinal brush border membrane: their use in investigating some properties of d-glucose and choline transport systems. Biochim Biophys Acta 506:136–154
Kaur J, Jaswal VMS, Nagpaul J, Mahmood A (1993) Effect of chronic ethanol administration on the absorptive functions of rat small intestine. Alcohol 10:299–302
Dahlqvist A (1964) Method for assay of intestinal disaccharidases. Anal Biochem 7:8–25
Lowry OH, Rosenbrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the folin-phenol reagent. J Biol Chem 193:265–275
Lammeli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685
Mahmood A, Mahmood S, Desehryver-KecsKimeti K, Alpers DH (1993) Characterization of proteins in rat and human intestinal surfactant particles. Arch Biochem Biophys 300:280–286
Chomenzynski P, Sacchi N (1987) Single step method of RNA isolation by acid guanidium thiocyanate phenol chloroform extraction. Anal Biochem 162:156–159
Kaur J, Kaur K, Mahmood A, Mahmood S (2005) In vitro translation of mRNA to lactase during postnatal development of rat intestine. J Biosci 30:101–107
Buller HA, Kothe MJ, Goldman DA, Grubman SA, Sasak WV, Matsudaira PT Montgomery RK, Grand RJ (1990) Coordinate expression of lactase-phlorizin hydrolase mRNA and enzyme levels in rat intestine during development. J Biol Chem 265:6978–6983
Motohashi Y, Fukushima A, Kondo T, Sakuma K (1997) Lactase decline in weaning rats is regulated at the transcriptional level and not caused by termination of milk ingestion. J Nutr 127:1737–1743
Freund JN, Duluc I, Foltzer-Jourdainne C, Gosse F, Raul F (1990) Specific expression of lactase in the jejunum and colon during postnatal development and hormone treatments in the rat. Biochem J 268:99–103
Villa M, Menard D, Semenza G, Mantei N (1992) The expression of lactase enzymatic activity and mRNA in human fetal jejunum. Effect of organ culture and of treatment with hydrocortisone. FEBS Lett 301:202–206
Nanthakumar NN, Young C, Ko JS, Meng D, Chen J, Buie T, Walker WA (2005) Glucocorticoid responsiveness in developing human intestine: possible role in prevention of necrotizing enterocolitis. Am J Physiol Gastrointest Liver Physiol 288:G85–G92
Foltzer-Jourdainne C, Kedinger M, Raul F (1989) Perinatal expression of brush-border hydrolases in rat colon: hormonal and tissue regulations. Am J Physiol 257:G496–G503
Yeh KY, Yeh M, Holt PR (1991) Thyroxine and cortisone cooperate to modulate postnatal intestinal enzyme differentiation in the rat. Am J Physiol 260:G371–G378
Raul F, Noriega R, Nsi-Emvo E, Doffoel M, Grenier JF (1983) Lactase activity is under hormonal control in the intestine of adult rat. Gut 24:648–652
Malo C, Menard D (1983) Synergistic effects of insulin and thyroxine on the differentiation and proliferation of epithelial cells of suckling mouse small intestine. Biol Neonate 44:177–184
Black BL (1978) Morphological development of the epithelium of the embryonic chick intestine in culture: influence of thyroxine and hydrocortisone. Am J Anat 153:573–599
Herbst JJ, Koldovsky O (1974) Cell migration and cortisone induction of sucrase activity in jejunum and ileum. Biochem J 126:471–476
Hollox EJ, Poulter M, Zvarik M, Ferak V, Krause A, Jenkins T, Saha N, Kozlov AI, Swallow DM (2001) Lactase haplotype diversity in the Old World. Am J Hum Genet 68:160–172
Wang Y, Harvey CB, Hollox EJ, Phillips AD, Poulter M, Clay P, Walker-Smith JA, Swallow DM (1998) The genetically programmed down-regulation of lactase in children. Gastroenterology 114:1230–1236
Freund JN, Domon-Dell C, Kedinger M, Duluc I (1998) The Cdx-1 and Cdx-2 homeobox genes in the intestine. Biochem Cell Biol 76:957–969
Lloyd M, Mevissen G, Fischer M, Olsen W, Goodspeed D, Genini M, Boll W, Semenza G, Mantei N (1992) Regulation of intestinal lactase in adult hypolactasia. J Clin Invest 89:524–529
Tsuboi KK, Kwong LK, Neu J, Sunshine P (1981) A proposed mechanism of normal intestinal lactase decline in the postweaned mammal. Biochem Biophys Res Commun 101:645–652
Rings EH, de Boer PA, Moorman AF, Van Beers EH, Dekker J, Montgomery RK, Grand RJ, Buller H (1992) Lactase gene expression during early development of rat small intestine. Gastroenterology 103:1154–1161
Biol-N’garagba MC, Louisot P (2003) Regulation of the intestinal glycoprotein glycosylation during postnatal development: role of hormonal and nutritional factors. Biochimie 85:331–352
Vaeth GF, Henning SJ (1982) Postnatal development of peptidase enzymes in rat small intestine. J Pediatr Gastroenterol Nutr 1:111–117
Ekstrom GM, Westrom BR (1991) Cathepsin B and D activities in intestinal mucosa during postnatal development in pigs. Relation to intestinal uptake and transmission of macromolecules. Biol Neonate 59:314–321
Mahmood A, Torres-Pinedo R (1985) Effect of hormone administration on the sialylation and fucosylation of intestinal microvillus membranes of suckling rats. Pediatr Res 19:899–902
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Senior Research Fellowship, from Indian Council of Medical Research, New Delhi, supported Ms. Kamaljit Kaur Chaudhry.
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Chaudhry, K.K., Mahmood, S. & Mahmood, A. Hormone induced expression of brush border lactase in suckling rat intestine. Mol Cell Biochem 312, 11–16 (2008). https://doi.org/10.1007/s11010-008-9715-7
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DOI: https://doi.org/10.1007/s11010-008-9715-7