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. 1979 Dec;33:9–16. doi: 10.1289/ehp.79339

Biochemistry of intestinal development.

S J Henning
PMCID: PMC1638120  PMID: 575507

Abstract

In biochemical terms, the rat small intestine is relatively immature at birth and for the first two postnatal weeks. Then during the third week a dramatic array of enzymic changes begins, and by the end of the fourth week the intestine has the digestive and absorptive properties of the adult. Selective examples of these changes are discussed with emphasis on their implications for toxicological studies. The review also includes a detailed consideration of the roles of the dietary change of weaning and of glucocorticoid and thyroid hormones in the regulation of intestinal development.

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Selected References

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  1. Allen C., Kendall J. W. Maturation of the circadian rhythm of plasma corticosterone in the rat. Endocrinology. 1967 May;80(5):926–930. doi: 10.1210/endo-80-5-926. [DOI] [PubMed] [Google Scholar]
  2. BLAIR D. G., YAKIMETS W., TUBA J. Rat intestinal sucrase. II. The effects of rat age and sex and of diet on sucrase activity. Can J Biochem Physiol. 1963 Apr;41:917–929. [PubMed] [Google Scholar]
  3. Bartová A. Functioning of the hypothalamo-pituitary-adrenal system during postnatal development in rats. Gen Comp Endocrinol. 1968 Apr;10(2):235–239. doi: 10.1016/0016-6480(68)90030-0. [DOI] [PubMed] [Google Scholar]
  4. Beam H. E., Henning S. J. Development of the circadian rhythm of jejunal sucrase activity in the weanling rat. Am J Physiol. 1978 Oct;235(4):E437–E442. doi: 10.1152/ajpendo.1978.235.4.E437. [DOI] [PubMed] [Google Scholar]
  5. Brambell F. W. The transmission of immunity from mother to young and the catabolism of immunoglobulins. Lancet. 1966 Nov 19;2(7473):1087–1093. doi: 10.1016/s0140-6736(66)92190-8. [DOI] [PubMed] [Google Scholar]
  6. Burholt D. R., Schultze B., Maurer W. Mode of growth of the jejunal crypt cells of the rat: an autoradiographic study using double labelling with 3H- and 14C-thymidine in lower and upper parts of crypts. Cell Tissue Kinet. 1976 Mar;9(2):107–117. doi: 10.1111/j.1365-2184.1976.tb01259.x. [DOI] [PubMed] [Google Scholar]
  7. CLARK S. L., Jr The ingestion of proteins and colloidal materials by columnar absorptive cells of the small intestine in suckling rats and mice. J Biophys Biochem Cytol. 1959 Jan 25;5(1):41–50. doi: 10.1083/jcb.5.1.41. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. CLARK S. L., Jr The localization of alkaline phosphatase in tissues of mice, using the electron microscope. Am J Anat. 1961 Jul;109:57–83. doi: 10.1002/aja.1001090106. [DOI] [PubMed] [Google Scholar]
  9. Cheng H., Leblond C. P. Origin, differentiation and renewal of the four main epithelial cell types in the mouse small intestine. I. Columnar cell. Am J Anat. 1974 Dec;141(4):461–479. doi: 10.1002/aja.1001410403. [DOI] [PubMed] [Google Scholar]
  10. Clark S. L., Jr The effects of cortisol and BUDR on cellular differentiation in the small intestine in suckling rats. Am J Anat. 1971 Nov;132(3):319–337. doi: 10.1002/aja.1001320304. [DOI] [PubMed] [Google Scholar]
  11. Clos J., Crépel F., Legrand C., Legrand J., Rabié A., Vigouroux E. Thyroid physiology during the postnatal period in the rat: a study of the development of thyroid function and of the morphogenetic effects of thyroxine with special reference to cerebellar maturation. Gen Comp Endocrinol. 1974 Jun;23(2):178–192. doi: 10.1016/0016-6480(74)90127-0. [DOI] [PubMed] [Google Scholar]
  12. DOELL R. G., KRETCHMER N. INTESTINAL INVERTASE: PRECOCIOUS DEVELOPMENT OF ACTIVITY AFTER INJECTION OF HYDROCORTISONE. Science. 1964 Jan 3;143(3601):42–44. doi: 10.1126/science.143.3601.42. [DOI] [PubMed] [Google Scholar]
  13. DOELL R. G., KRETCHMER N. Studies of small intestine during development. I. Distribution and activity of beta-galactosidase. Biochim Biophys Acta. 1962 Aug 13;62:353–362. doi: 10.1016/0006-3002(62)90097-5. [DOI] [PubMed] [Google Scholar]
  14. Daniels V. G., Hardy R. N., Malinowska K. W., Nathanielsz P. W. The influence of exogenous steroids on macromolecule uptake by the small intestine of the new-born rat. J Physiol. 1973 Mar;229(3):681–695. doi: 10.1113/jphysiol.1973.sp010160. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Daniels V. G., Hardy R. N., Malinowska K. W. The effect of adrenalectomy or pharmacological inhibition of adrenocortical function on macromolecule uptake by the new-born rat intestine. J Physiol. 1973 Mar;229(3):697–707. doi: 10.1113/jphysiol.1973.sp010161. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Deren J. J., Broitman S. A., Zamcheck N. Effect of diet upon intestinal disaccharidases and disaccharide absorption. J Clin Invest. 1967 Feb;46(2):186–195. doi: 10.1172/JCI105521. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Dickson J. J., Messer M. Intestinal neuraminidase activity of suckling rats and other mammals. Relationship to the sialic acid content of milk. Biochem J. 1978 Feb 15;170(2):407–413. doi: 10.1042/bj1700407. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Doell R. G., Rosen G., Kretchmer N. Immunochemical studies of intestinal disaccharidases during normal and precocious development. Proc Natl Acad Sci U S A. 1965 Oct;54(4):1268–1273. doi: 10.1073/pnas.54.4.1268. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Dunn J. S. The fine structure of the absorptive epithelial cells of the developing small intestine of the rat. J Anat. 1967 Jan;101(Pt 1):57–68. [PMC free article] [PubMed] [Google Scholar]
  20. Dussault J. H., Labrie F. Development of the hypothalamic-pituitary-thyroid axis in the neonatal rat. Endocrinology. 1975 Nov;97(5):1321–1324. doi: 10.1210/endo-97-5-1321. [DOI] [PubMed] [Google Scholar]
  21. Etzler M. E., Birkenmeier H., Moog F. Localization of alkaline phosphatase isozymes in mouse duodenum by immunofluorescence microscopy. Histochemie. 1969;20(2):99–104. doi: 10.1007/BF00268702. [DOI] [PubMed] [Google Scholar]
  22. Fortin-Magana R., Hurwitz R., Herbst J. J., Kretchmer N. Intestinal enzymes: indicators of proliferation and differentiation in the jejunum. Science. 1970 Mar 20;167(3925):1627–1628. doi: 10.1126/science.167.3925.1627. [DOI] [PubMed] [Google Scholar]
  23. Furihata C., Kawachi T., Sugimura T. Premature induction of pepsinogen in developing rat gastric mucosa by hormones. Biochem Biophys Res Commun. 1972 May 26;47(4):705–711. doi: 10.1016/0006-291x(72)90549-9. [DOI] [PubMed] [Google Scholar]
  24. Galand G., Forstner G. G. Isolation of microvillus plasma membranes from suckling-rat intestine. The influence of premature induction of digestive enzymes by injection of cortisol acetate. Biochem J. 1974 Nov;144(2):293–302. doi: 10.1042/bj1440293. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Goldstein R., Klein T., Freier S., Menczel J. Alkaline phosphatase and disaccharidase activities in the rat intestine from birth to weaning. I. Effect of diet on enzyme development. Am J Clin Nutr. 1971 Oct;24(10):1224–1231. doi: 10.1093/ajcn/24.10.1224. [DOI] [PubMed] [Google Scholar]
  26. HALLIDAY R. Prenatal and postnatal transmission of passive immunity to young rats. Proc R Soc Lond B Biol Sci. 1955 Nov 29;144(916):427–430. doi: 10.1098/rspb.1955.0068. [DOI] [PubMed] [Google Scholar]
  27. HALLIDAY R. The absorption of antibodies from immune sera by the gut of the young rat. Proc R Soc Lond B Biol Sci. 1955 Mar 15;143(912):408–413. doi: 10.1098/rspb.1955.0020. [DOI] [PubMed] [Google Scholar]
  28. HALLIDAY R. The effect of steroid hormones on the absorption of antibody by the young rat. J Endocrinol. 1959 Jan;18(1):56–66. doi: 10.1677/joe.0.0180056. [DOI] [PubMed] [Google Scholar]
  29. Haltmeyer G. C., Denenberg V. H., Thatcher J., Zarrow M. X. Response of the adrenal cortex of the neonatal rat after subjection to stress. Nature. 1966 Dec 17;212(5068):1371–1373. doi: 10.1038/2121371a0. [DOI] [PubMed] [Google Scholar]
  30. Hayward A. F. Changes in fine structure of developing intestinal epithelium associated with pinocytosis. J Anat. 1967 Nov;102(Pt 1):57–70. [PMC free article] [PubMed] [Google Scholar]
  31. Henning S. J., Ballard P. L., Kretchmer N. A study of the cytoplasmic receptors for glucocorticoids in intestine of pre- and postweanling rats. J Biol Chem. 1975 Mar 25;250(6):2073–2079. [PubMed] [Google Scholar]
  32. Henning S. J., Helman T. A., Kretchmer N. Studies on normal and precocious appearance of jejunal sucrase in suckling rats. Biol Neonate. 1975;26(3-4):249–262. doi: 10.1159/000240736. [DOI] [PubMed] [Google Scholar]
  33. Henning S. J., Kretchmer N. Development of intestinal function in mammals. Enzyme. 1973;15(1):3–23. [PubMed] [Google Scholar]
  34. Henning S. J. Permissive role of thyroxine in the ontogeny of jejunal sucrase. Endocrinology. 1978 Jan;102(1):9–15. doi: 10.1210/endo-102-1-9. [DOI] [PubMed] [Google Scholar]
  35. Henning S. J. Plasma concentrations of total and free corticosterone during development in the rat. Am J Physiol. 1978 Nov;235(5):E451–E456. doi: 10.1152/ajpendo.1978.235.5.E451. [DOI] [PubMed] [Google Scholar]
  36. Henning S. J., Sims J. M. Delineation of the glucocorticoid-sensitive period of intestinal development in the rat. Endocrinology. 1979 Apr;104(4):1158–1163. doi: 10.1210/endo-104-4-1158. [DOI] [PubMed] [Google Scholar]
  37. Herbst J. J., Fortin-Magana R., Sunshine P. Relationship of pyrimidine biosynthetic enzymes to cellular proliferation in rat intestine during development. Gastroenterology. 1970 Aug;59(2):240–246. [PubMed] [Google Scholar]
  38. Herbst J. J., Koldovský O. Cell migration and cortisone induction of sucrase activity in jejunum and ileum. Biochem J. 1972 Feb;126(3):471–476. doi: 10.1042/bj1260471. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Herbst J. J., Sunshine P. Postnatal development of the small intestine of the rat. Changes in mucosal morphology at weaning. Pediatr Res. 1969 Jan;3(1):27–33. doi: 10.1203/00006450-196901000-00004. [DOI] [PubMed] [Google Scholar]
  40. Imondi A. R., Balis M. E., Lipkin M. Changes in enzyme levels accompanying differentiation of intestinal epithelial cells. Exp Cell Res. 1969 Dec;58(2):323–330. doi: 10.1016/0014-4827(69)90512-6. [DOI] [PubMed] [Google Scholar]
  41. JENNESS R., REGEHR E. A., SLOAN R. E. COMPARATIVE BIOCHEMICAL STUDIES OF MILK. II. DIALYZABLE CARBOHYDRATES. Comp Biochem Physiol. 1964 Dec;13:339–352. doi: 10.1016/0010-406x(64)90028-3. [DOI] [PubMed] [Google Scholar]
  42. Jirsová V., Heringová A. Effect of aldosterone and corticosterone on beta-galactosidase and invertase activity in the small intestine of rats. Nature. 1965 Apr 17;206(981):300–301. doi: 10.1038/206300a0. [DOI] [PubMed] [Google Scholar]
  43. Jones R. E. Intestinal absorption and gastro-intestinal digestion of protein in the young rat during the normal and cortisone-induced post-closure period. Biochim Biophys Acta. 1972 Aug 9;274(2):412–419. doi: 10.1016/0005-2736(72)90187-3. [DOI] [PubMed] [Google Scholar]
  44. Kakihana R., Blum S., Kessler S. Developmental study of pituitary-adrenocortical response in mice: plasma and brain corticosterone determination after histamine stress. J Endocrinol. 1974 Feb;60(2):353–358. doi: 10.1677/joe.0.0600353. [DOI] [PubMed] [Google Scholar]
  45. Koldovsky O., Sunshine P., Kretchmer N. Cellular migration of intestinal epithelia in suckling and weaned rats. Nature. 1966 Dec 17;212(5068):1389–1390. doi: 10.1038/2121389a0. [DOI] [PubMed] [Google Scholar]
  46. Koldovský O., Palmieri M. Cortisone-evoked decrease of acid -galactosidase, -glucuronidase, N-acetyl- -glucosaminidase and arylsulphatase in the ileum of suckling rats. Biochem J. 1971 Dec;125(3):697–701. doi: 10.1042/bj1250697. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Kretchmer N. Lactose and lactase--a historical perspective. Gastroenterology. 1971 Dec;61(6):805–813. [PubMed] [Google Scholar]
  48. Lebenthal E., Sunshine P., Kretchmer N. Effect of carbohydrate and corticosteroids on activity of -glucosidases in intestine of the infant rat. J Clin Invest. 1972 May;51(5):1244–1250. doi: 10.1172/JCI106919. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Lebenthal E., Sunshine P., Kretchmer N. Effect of prolonged nursing on the activity of intestinal lactase in rats. Gastroenterology. 1973 Jun;64(6):1136–1141. [PubMed] [Google Scholar]
  50. Lipkin M. Proliferation and differentiation of gastrointestinal cells. Physiol Rev. 1973 Oct;53(4):891–915. doi: 10.1152/physrev.1973.53.4.891. [DOI] [PubMed] [Google Scholar]
  51. MOSINGER B., PLACER Z., KOLDOVSKY O. Passage of insulin through the wall of the gastro-intestinal tract of the infant rat. Nature. 1959 Oct 17;184(Suppl 16):1245–1246. doi: 10.1038/1841245a0. [DOI] [PubMed] [Google Scholar]
  52. Moog F., Denes A. E., Powell P. M. Disaccharidases in the small intestine of the mouse: normal development and influence of cortisone, actinomycin D, and cycloheximide. Dev Biol. 1973 Nov;35(1):143–159. doi: 10.1016/0012-1606(73)90012-2. [DOI] [PubMed] [Google Scholar]
  53. Morris B., Morris R. The digestion and transmission of labelled immunoglobulin G by enterocytes of the proximal distal regions of the small intestine of young rats. J Physiol. 1977 Dec;273(2):427–442. doi: 10.1113/jphysiol.1977.sp012102. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Noack R., Koldovský O., Friedrich M., Heringová A., Jirsová V., Schenk G. Proteolytic and peptidase activities of the jejunum and ileum of the rat during postnatal development. Biochem J. 1966 Sep;100(3):775–778. doi: 10.1042/bj1000775. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Nordström C., Dahlqvist A., Josefsson L. Quantitative determination of enzymes in different parts of the villi and crypts of rat small intestine. Comparison of alkaline phosphatase, disaccharidases and dipepeptidases. J Histochem Cytochem. 1967 Dec;15(12):713–721. doi: 10.1177/15.12.713. [DOI] [PubMed] [Google Scholar]
  56. Orlic D., Lev R. Fetal rat intestinal absorption of horseradish peroxidase from swallowed amniotic fluid. J Cell Biol. 1973 Jan;56(1):106–119. doi: 10.1083/jcb.56.1.106. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. RUBINO A., ZIMBALATTI F., AURICCHIO S. INTESTINAL DISACCHARIDASE ACTIVITIES IN ADULT AND SUCKLING RATS. Biochim Biophys Acta. 1964 Nov 22;92:305–311. doi: 10.1016/0926-6569(64)90187-7. [DOI] [PubMed] [Google Scholar]
  58. Rao M. L., Rao G. S., Eckel J., Breuer H. Factors involved in the uptake of corticosterone by rat liver cells. Biochim Biophys Acta. 1977 Dec 22;500(2):322–332. doi: 10.1016/0304-4165(77)90024-1. [DOI] [PubMed] [Google Scholar]
  59. Reddy B. S., Wostmann B. S. Intestinal disaccharidase activities in the growing germfree and conventional rats. Arch Biochem Biophys. 1966 Mar;113(3):609–616. doi: 10.1016/0003-9861(66)90238-4. [DOI] [PubMed] [Google Scholar]
  60. Robberecht P., Deschodt-Lanckman M., Camus J., Bruylands J., Christophe J. Rat pancreatic hydrolases from birth to weaning and dietary adaptation after weaning. Am J Physiol. 1971 Jul;221(1):376–381. doi: 10.1152/ajplegacy.1971.221.1.376. [DOI] [PubMed] [Google Scholar]
  61. Rodewald R. Selective antibody transport in the proximal small intestine of the neonatal rat. J Cell Biol. 1970 Jun;45(3):635–640. doi: 10.1083/jcb.45.3.635. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. SLAUNWHITE W. R., LOCKIE G. N., BACK N., SANDBERG A. A. Inactivity in vivo of transcortin-bound cortisol. Science. 1962 Mar 23;135(3508):1062–1063. doi: 10.1126/science.135.3508.1062. [DOI] [PubMed] [Google Scholar]
  63. Samel M. Thyroid function during postnatal development in the rat. Gen Comp Endocrinol. 1968 Apr;10(2):229–234. doi: 10.1016/0016-6480(68)90029-4. [DOI] [PubMed] [Google Scholar]
  64. Williams R. M., Beck F. A histochemical study of gut maturation. J Anat. 1969 Nov;105(Pt 3):487–501. [PMC free article] [PubMed] [Google Scholar]
  65. Wysocki S. J., Segal W. Influence of thyroid hormones on enzyme activities of myelinating rat central-nervous tissues. Eur J Biochem. 1972 Jul 13;28(2):183–189. doi: 10.1111/j.1432-1033.1972.tb01901.x. [DOI] [PubMed] [Google Scholar]

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