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Hormone induced expression of brush border lactase in suckling rat intestine

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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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References

  1. 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

    PubMed  Google Scholar 

  2. 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

    Article  PubMed  CAS  Google Scholar 

  3. 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

    PubMed  CAS  Google Scholar 

  4. 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

    PubMed  CAS  Google Scholar 

  5. 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

    PubMed  CAS  Google Scholar 

  6. Britton JR, Koldovsky O (1988) Development of luminal protein digestion in suckling and weanling rats. Biol Neonate 53:39–46

    PubMed  CAS  Google Scholar 

  7. Kaur K, Mahmood S, Mahmood A (2006) The susceptibility of lactase to luminal proteases in developing rat intestine. Indian J Gastroenterol 25:179–181

    PubMed  Google Scholar 

  8. 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

    Article  PubMed  CAS  Google Scholar 

  9. 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

    Article  PubMed  CAS  Google Scholar 

  10. Dahlqvist A (1964) Method for assay of intestinal disaccharidases. Anal Biochem 7:8–25

    Article  Google Scholar 

  11. Lowry OH, Rosenbrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the folin-phenol reagent. J Biol Chem 193:265–275

    PubMed  CAS  Google Scholar 

  12. Lammeli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685

    Article  Google Scholar 

  13. 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

    Article  PubMed  CAS  Google Scholar 

  14. Chomenzynski P, Sacchi N (1987) Single step method of RNA isolation by acid guanidium thiocyanate phenol chloroform extraction. Anal Biochem 162:156–159

    Google Scholar 

  15. 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

    Article  Google Scholar 

  16. 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

    PubMed  CAS  Google Scholar 

  17. 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

    PubMed  CAS  Google Scholar 

  18. 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

    PubMed  CAS  Google Scholar 

  19. 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

    Article  PubMed  CAS  Google Scholar 

  20. 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

    Article  PubMed  CAS  Google Scholar 

  21. 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

    PubMed  CAS  Google Scholar 

  22. 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

    PubMed  CAS  Google Scholar 

  23. 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

    Article  PubMed  CAS  Google Scholar 

  24. 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

    Article  PubMed  CAS  Google Scholar 

  25. 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

    Article  PubMed  CAS  Google Scholar 

  26. Herbst JJ, Koldovsky O (1974) Cell migration and cortisone induction of sucrase activity in jejunum and ileum. Biochem J 126:471–476

    Google Scholar 

  27. 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

    Article  PubMed  CAS  Google Scholar 

  28. 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

    Article  PubMed  CAS  Google Scholar 

  29. 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

    Article  PubMed  CAS  Google Scholar 

  30. 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

    Article  PubMed  CAS  Google Scholar 

  31. 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

    Article  PubMed  CAS  Google Scholar 

  32. 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

    PubMed  CAS  Google Scholar 

  33. 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

    Article  PubMed  CAS  Google Scholar 

  34. Vaeth GF, Henning SJ (1982) Postnatal development of peptidase enzymes in rat small intestine. J Pediatr Gastroenterol Nutr 1:111–117

    Article  PubMed  CAS  Google Scholar 

  35. 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

    Article  PubMed  CAS  Google Scholar 

  36. 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

    Article  PubMed  CAS  Google Scholar 

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Acknowledgement

Senior Research Fellowship, from Indian Council of Medical Research, New Delhi, supported Ms. Kamaljit Kaur Chaudhry.

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Correspondence to Akhtar Mahmood.

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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

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