Skip to main content
PMC home page
Biochemical Journal logoLink to Biochemical Journal
. 1980 Jun 15;188(3):609–618. doi: 10.1042/bj1880609

Changes in the synthesis of ribosomal ribonucleic acid and of poly(A)-containing ribonucleic acid during the differentiation of intestinal epithelial cells in the rat and in the chick.

A Morrison, J W Porteous
PMCID: PMC1161941  PMID: 6162451

Abstract

Epithelial cells were isolated from rat and chick small intestine by techniques which separated subpopulations of differentiating villus and upper crypt cells from each other and from populations of mitotically dividing lower crypt cells. Incorporation of precursors into epithelial-cell DNA, cytoplasmic rRNA and cytoplasmic poly(A)-containing RNA occurred in the lower crypt cells in vivo when precursor was supplied from the vascular system of the intestine. Incorporation of precursor into 28S and 18S rRNA continued in the upper crypt cells, but occurred to only a very slight extent (if at all) in villus cells, whereas incorporation into poly(A)-containing RNA continued (at a diminishing rate) as the differentiating cells migrated along the villi. When precursor was supplied from the intestinal lumen, its incorporation into DNA and into rRNA of crypt cells was not very different from that observed with the other mode of precursor administration, but incorporation into villus-cell poly(A)-containing RNA then occurred at essentially the same rate in all intestinal epithelial cells in vivo. Cytoplasmic poly(A)-containing RNA appeared to turn over in rat crypt cells with a half-life not exceeding 24 h; crypt-cell rRNA showed no turnover and no evidence could be found for the presence of 'metabolic DNA'.

Full text

PDF
610

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Al-Dewachi H. S., Wright N. A., Appleton D. R., Watson A. J. The cell cycle time in the rat jejunal mucosa. Cell Tissue Kinet. 1974 Nov;7(6):587–594. doi: 10.1111/j.1365-2184.1974.tb00442.x. [DOI] [PubMed] [Google Scholar]
  2. Appleton T. C., Pelc S. R., Tarbit M. H. Formation and loss of DNA in intestinal epithelium. J Cell Sci. 1969 Jul;5(1):45–55. doi: 10.1242/jcs.5.1.45. [DOI] [PubMed] [Google Scholar]
  3. BURTON K. A study of the conditions and mechanism of the diphenylamine reaction for the colorimetric estimation of deoxyribonucleic acid. Biochem J. 1956 Feb;62(2):315–323. doi: 10.1042/bj0620315. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Burholt D. R., Schultze B., Maurer W. Autoradiographic confirmation of the mitotic division of every mouse jejunal crypt cell labelled with 3 H-thymidine. Evidence against the existence of cells synthesizing metabolic DNA. Cell Tissue Kinet. 1973 May;6(3):229–237. [PubMed] [Google Scholar]
  5. Cairnie A. B., Lamerton L. F., Steel G. G. Cell proliferation studies in the intestinal epithelium of the rat. I. Determination of the kinetic parameters. Exp Cell Res. 1965 Sep;39(2):528–538. doi: 10.1016/0014-4827(65)90055-8. [DOI] [PubMed] [Google Scholar]
  6. 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]
  7. Clausen T. Measurement of 32P activity in a liquid scintillation counter without the use of scintillator. Anal Biochem. 1968 Jan;22(1):70–73. doi: 10.1016/0003-2697(68)90260-1. [DOI] [PubMed] [Google Scholar]
  8. Craig R. K., Brown P. A., Harrison O. S., McIlreavy D., Campbell P. N. Guinea-pig milk-protein synthesis. Isolation and characterization of messenger ribonucleic acids from lactating mammary gland and identification of caseins and pre-alpha-lactalbumin as translation products in heterologous cell-free systems. Biochem J. 1976 Oct 15;160(1):57–74. doi: 10.1042/bj1600057. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Feldman E. J., Dowling R. H., McNaughton J., Peters T. J. Effects of oral versus intravenous nutrition on intestinal adaptation after small bowel resection in the dog. Gastroenterology. 1976 May;70(5 PT1):712–719. [PubMed] [Google Scholar]
  10. 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]
  11. Grey R. D., LeCount T. S. Distribution of leucyl naphthylamidase and alkaline phosphatase on the villi of the chick duodenum. J Histochem Cytochem. 1970 Jun;18(6):416–423. doi: 10.1177/18.6.416. [DOI] [PubMed] [Google Scholar]
  12. Groner B., Phillips S. L. Polyadenylate metabolism in the nuclei and cytoplasm of Saccharomyces cerevisiae. J Biol Chem. 1975 Jul 25;250(14):5640–5646. [PubMed] [Google Scholar]
  13. 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]
  14. Kerridge D. F. Estimation of the ratio (gamma) of poly(ADP-ribose) synthetase activity in non-lower-crypt cells to that in lower-crypt cells in vovo from an analysis of enzyme activities and thymidine incorporation in populations of sequentially isolated cells. Biochem J. 1979 Jun 15;180(3):462–463. doi: 10.1042/bj1800462. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. 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]
  16. Monahan J. J., Hall R. H. Fractionation of L-cell chromatin into DNA, RNA, and protein fractions on Cs2SO4 equilibruim density gradients. Anal Biochem. 1974 Nov;62(1):217–239. doi: 10.1016/0003-2697(74)90382-0. [DOI] [PubMed] [Google Scholar]
  17. Munro H. N. The determination of nucleic acids. Methods Biochem Anal. 1966;14:113–176. doi: 10.1002/9780470110324.ch5. [DOI] [PubMed] [Google Scholar]
  18. 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]
  19. Penman S., Vesco C., Penman M. Localization and kinetics of formation of nuclear heterodisperse RNA, cytoplasmic heterodisperse RNA and polyribosome-associated messenger RNA in HeLa cells. J Mol Biol. 1968 May 28;34(1):49–60. doi: 10.1016/0022-2836(68)90234-9. [DOI] [PubMed] [Google Scholar]
  20. Peterson A. M. Differentiation associated changes in thymidylate synthetase and thymidine kinase activities in intestinal cells. Cell Differ. 1976 Apr;5(1):37–43. doi: 10.1016/0045-6039(76)90013-0. [DOI] [PubMed] [Google Scholar]
  21. Porteous J. W., Furneaux H. M., Pearson C. K., Lake C. M., Morrison A. Poly(adenosine diphosphate ribose) synthetase activity in nuclei of dividing and of non-dividing but differentiating intestinal epithelial cells. Biochem J. 1979 Jun 15;180(3):455–461. doi: 10.1042/bj1800455. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Porteous J. W. Glucose as a fuel for small intestine. Biochem Soc Trans. 1978;6(3):534–539. doi: 10.1042/bst0060534. [DOI] [PubMed] [Google Scholar]
  23. QUASTLER H., SHERMAN F. G. Cell population kinetics in the intestinal epithelium of the mouse. Exp Cell Res. 1959 Jun;17(3):420–438. doi: 10.1016/0014-4827(59)90063-1. [DOI] [PubMed] [Google Scholar]
  24. SHORTER R. G., CREAMER B. Ribonucleic acid and protein metabolism in the gut. I. Observations in gastro-intestinal cells with rapid turnover. Gut. 1962 Jun;3:118–128. doi: 10.1136/gut.3.2.118. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Sassier P., Bergeron M. Cellular changes in the small intestine epithelium in the course of cell proliferation and maturation. Subcell Biochem. 1978;5:129–185. doi: 10.1007/978-1-4615-7942-7_3. [DOI] [PubMed] [Google Scholar]
  26. Schultze B., Haack V., Schmeer A. C., Maurer W. Autoradiographic investigation on the cell kinetics of crypt epithelia in the jejunum of the mouse. Confirmation of steady state growth with constant frequency distribution of cells throughout the cycle. Cell Tissue Kinet. 1972 Mar;5(2):131–145. doi: 10.1111/j.1365-2184.1972.tb01010.x. [DOI] [PubMed] [Google Scholar]
  27. Towler C. M., Pugh-Humphreys G. P., Porteous J. W. Characterization of columnar absorptive epithelial cells isolated from rat jejunum. J Cell Sci. 1978 Feb;29:53–75. doi: 10.1242/jcs.29.1.53. [DOI] [PubMed] [Google Scholar]
  28. Webster H. L., Harrison D. D. Enzymic activities during the transformation of crypt to columnar intestinal cells. Exp Cell Res. 1969 Aug;56(2):245–253. doi: 10.1016/0014-4827(69)90009-3. [DOI] [PubMed] [Google Scholar]
  29. Weiser M. M. Intestinal epithelial cell surface membrane glycoprotein synthesis. I. An indicator of cellular differentiation. J Biol Chem. 1973 Apr 10;248(7):2536–2541. [PubMed] [Google Scholar]
  30. Wiegers U., Kramer G., Klapproth K., Hilz H. Separate pyrimidine-nucleotide pools for messenger-RNA and ribosomal-RNA synthesis in HeLa S3 cells. Eur J Biochem. 1976 May 1;64(2):535–540. doi: 10.1111/j.1432-1033.1976.tb10333.x. [DOI] [PubMed] [Google Scholar]
  31. Zajicek G., Michaeli Y., Weinreb M. M. Kinetics of the inner enamel epithelium in the adult rat incisor during accelerated eruption. Cell Tissue Kinet. 1972 Jan;5(1):35–39. doi: 10.1111/j.1365-2184.1972.tb00353.x. [DOI] [PubMed] [Google Scholar]
  32. de Both N. J., van Dongen J. M., van Hofwegen B., Keulemann J., Visser W. J., Galjaard H. The influence of various cell kinetic conditions on functional differentiation in the small intestine of the rat. A study of enzymes bound to subcellular organelles. Dev Biol. 1974 May;38(1):119–137. doi: 10.1016/0012-1606(74)90263-2. [DOI] [PubMed] [Google Scholar]
  33. van Dongen J. M., Visser W. J., Daems W. T., Galjaard H. The relation between cell proliferation, differentiation and ultrastructural development in rat intestinal epithelium. Cell Tissue Res. 1976 Oct 29;174(2):183–199. doi: 10.1007/BF00222158. [DOI] [PubMed] [Google Scholar]

Articles from Biochemical Journal are provided here courtesy of The Biochemical Society

RESOURCES