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. 1974 Apr 1;61(1):1–13. doi: 10.1083/jcb.61.1.1

DYNAMICS OF CYTOPLASMIC MEMBRANES IN GUINEA PIG PANCREATIC ACINAR CELLS

I. Synthesis and Turnover of Membrane Proteins

J Meldolesi 1
PMCID: PMC2109262  PMID: 4819305

Abstract

The rate of synthesis and the turnover of cytoplasmic membrane proteins were determined in the acinar cells of guinea pig pancreas with the aim of investigating the mechanisms by which the intracellular transport of secretion products occurs. These cells are highly specialized toward protein secretion. By means of in vitro pulse-chase experiments and in vivo double-labeling experiments, using radioactive L-leucine as the tracer, it was found that the turnover of secretory proteins is much faster than that of all membranes involved in their transport (rough and smooth microsome and zymogen granule membranes). Sodium dodecyl sulfate-polyacrylamide disk gel electrophoresis of membrane proteins revealed that in each of these membranes there is a marked heterogeneity of turnover; generally the high molecular weight polypeptides have a shorter half-life than the low molecular weight polypeptides. These data indicate that the membranes participating in the intracellular transport of secretory proteins are not synthesized concomitantly with the latter. Rather, they are probably reutilized in several successive secretory cycles. The possible relevance of these findings to other secretory systems is discussed.

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Selected References

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  1. Abrahams S. J., Holtzman E. Secretion and endocytosis in insulin-stimulated rat adrenal medulla cells. J Cell Biol. 1973 Feb;56(2):540–558. doi: 10.1083/jcb.56.2.540. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Amsterdam A., Ohad I., Schramm M. Dynamic changes in the ultrastructure of the acinar cell of the rat parotid gland during the secretory cycle. J Cell Biol. 1969 Jun;41(3):753–773. doi: 10.1083/jcb.41.3.753. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Amsterdam A., Schramm M., Ohad I., Salomon Y., Selinger Z. Concomitant synthesis of membrane protein and exportable protein of the secretory granule in rat parotid gland. J Cell Biol. 1971 Jul;50(1):187–200. doi: 10.1083/jcb.50.1.187. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Arias I. M., Doyle D., Schimke R. T. Studies on the synthesis and degradation of proteins of the endoplasmic reticulum of rat liver. J Biol Chem. 1969 Jun 25;244(12):3303–3315. [PubMed] [Google Scholar]
  5. Barancik L. C., Lieberman I. The kinetics of incorporation of protein into the liver plasma membrane. Biochem Biophys Res Commun. 1971 Sep;44(5):1084–1088. doi: 10.1016/s0006-291x(71)80196-1. [DOI] [PubMed] [Google Scholar]
  6. Benedeczky I., Smith A. D. Ultrastructural studies on the adrenal medulla of golden hamster: origin and fate of secretory granules. Z Zellforsch Mikrosk Anat. 1972;124(3):367–386. doi: 10.1007/BF00355037. [DOI] [PubMed] [Google Scholar]
  7. Bock K. W., Siekevitz P., Palade G. E. Localization and turnover studies of membrane nicotinamide adenine dinucleotide glycohydrolase in rat liver. J Biol Chem. 1971 Jan 10;246(1):188–195. [PubMed] [Google Scholar]
  8. Bosmann H. B., Hagopian A., Eylar E. H. Cellular membranes: the biosynthesis of glycoprotein and glycolipid in hela cell membranes. Arch Biochem Biophys. 1969 Mar;130(1):573–583. doi: 10.1016/0003-9861(69)90073-3. [DOI] [PubMed] [Google Scholar]
  9. CARO L. G., PALADE G. E. PROTEIN SYNTHESIS, STORAGE, AND DISCHARGE IN THE PANCREATIC EXOCRINE CELL. AN AUTORADIOGRAPHIC STUDY. J Cell Biol. 1964 Mar;20:473–495. doi: 10.1083/jcb.20.3.473. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Castle J. D., Jamieson J. D., Palade G. E. Radioautographic analysis of the secretory process in the parotid acinar cell of the rabbit. J Cell Biol. 1972 May;53(2):290–311. doi: 10.1083/jcb.53.2.290. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Ceccarelli B., Hurlbut W. P., Mauro A. Depletion of vesicles from frog neuromuscular junctions by prolonged tetanic stimulation. J Cell Biol. 1972 Jul;54(1):30–38. doi: 10.1083/jcb.54.1.30. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Ceccarelli B., Hurlbut W. P., Mauro A. Turnover of transmitter and synaptic vesicles at the frog neuromuscular junction. J Cell Biol. 1973 May;57(2):499–524. doi: 10.1083/jcb.57.2.499. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Claude A. Growth and differentiation of cytoplasmic membranes in the course of lipoprotein granule synthesis in the hepatic cell. I. Elaboration of elements of the Golgi complex. J Cell Biol. 1970 Dec;47(3):745–766. doi: 10.1083/jcb.47.3.745. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Dévényi T., Hazai I., Ferenczi S., Báti J. Thin-layer ion-exchange chromatography on resin-coated chromatoplates. V. One-dimensional separation of amino acids. Acta Biochim Biophys Acad Sci Hung. 1971;6(4):385–388. [PubMed] [Google Scholar]
  15. Glass R. D., Doyle D. On the measurement of protein turnover in animal cells. J Biol Chem. 1972 Aug 25;247(16):5234–5242. [PubMed] [Google Scholar]
  16. Grynszpan-Winograd O. Morphological aspects of exocytosin in the adrenal medulla. Philos Trans R Soc Lond B Biol Sci. 1971 Jun 17;261(839):291–292. doi: 10.1098/rstb.1971.0058. [DOI] [PubMed] [Google Scholar]
  17. Hopkins C. R. The biosynthesis, intracellular transport, and packaging of melanocyte-stimulating peptides in the amphibian pars intermedia. J Cell Biol. 1972 Jun;53(3):642–653. doi: 10.1083/jcb.53.3.642. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Howell S. L., Kostianovsky M., Lacy P. E. Beta granule formation in isolated islets of langerhans: a study by electron microscopic radioautography. J Cell Biol. 1969 Sep;42(3):695–705. doi: 10.1083/jcb.42.3.695. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Howell S. L., Whitfield M. Synthesis and secretion of growth hormone in the rat anterior pituitary. I. The intracellular pathway, its time course and energy requirements. J Cell Sci. 1973 Jan;12(1):1–21. doi: 10.1242/jcs.12.1.1. [DOI] [PubMed] [Google Scholar]
  20. Iandolo J. J. Device for slicing polyacrylamide gels. Anal Biochem. 1970 Jul;36(1):6–10. doi: 10.1016/0003-2697(70)90325-8. [DOI] [PubMed] [Google Scholar]
  21. Jamieson J. D., Palade G. E. Intracellular transport of secretory proteins in the pancreatic exocrine cell. I. Role of the peripheral elements of the Golgi complex. J Cell Biol. 1967 Aug;34(2):577–596. doi: 10.1083/jcb.34.2.577. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Jamieson J. D., Palade G. E. Intracellular transport of secretory proteins in the pancreatic exocrine cell. II. Transport to condensing vacuoles and zymogen granules. J Cell Biol. 1967 Aug;34(2):597–615. doi: 10.1083/jcb.34.2.597. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Jamieson J. D., Palade G. E. Synthesis, intracellular transport, and discharge of secretory proteins in stimulated pancreatic exocrine cells. J Cell Biol. 1971 Jul;50(1):135–158. doi: 10.1083/jcb.50.1.135. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Kiehn E. D., Holland J. J. Membrane and nonmembrane proteins of mammalian cells. Synthesis, turnover, and size distribution. Biochemistry. 1970 Apr 14;9(8):1716–1728. doi: 10.1021/bi00810a010. [DOI] [PubMed] [Google Scholar]
  25. Kuriyama Y., Omura T., Siekevitz P., Palade G. E. Effects of phenobarbital on the synthesis and degradation of the protein components of rat liver microsomal membranes. J Biol Chem. 1969 Apr 25;244(8):2017–2026. [PubMed] [Google Scholar]
  26. LOWRY O. H., ROSEBROUGH N. J., FARR A. L., RANDALL R. J. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951 Nov;193(1):265–275. [PubMed] [Google Scholar]
  27. Meldolesi J., Cova D. Composition of cellular membranes in the pancreas of the guinea pig. IV. Polyacrylamide gel electrophoresis and amino acid composition of membrane proteins. J Cell Biol. 1972 Oct;55(1):1–18. doi: 10.1083/jcb.55.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Meldolesi J., Cova D. In vitro stimulation of enzyme secretion and the synthesis of microsomal membranes in the pancreas of the guinea pig. J Cell Biol. 1971 Nov;51(21):396–404. doi: 10.1083/jcb.51.2.396. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Meldolesi J., Cova D. Synthesis and interactions of cytoplasmic membranes in the pancreatic exocrine cells. Biochem Biophys Res Commun. 1971 Jul 2;44(1):139–143. doi: 10.1016/s0006-291x(71)80169-9. [DOI] [PubMed] [Google Scholar]
  30. Meldolesi J., Jamieson J. D., Palade G. E. Composition of cellular membranes in the pancreas of the guinea pig. 3. Enzymatic activities. J Cell Biol. 1971 Apr;49(1):150–158. doi: 10.1083/jcb.49.1.150. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Meldolesi J., Jamieson J. D., Palade G. E. Composition of cellular membranes in the pancreas of the guinea pig. I. Isolation of membrane fractions. J Cell Biol. 1971 Apr;49(1):109–129. doi: 10.1083/jcb.49.1.109. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Meldolesi J., Jamieson J. D., Palade G. E. Composition of cellular membranes in the pancreas of the guinea pig. II. Lipids. J Cell Biol. 1971 Apr;49(1):130–149. doi: 10.1083/jcb.49.1.130. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Morris S. J., Ralston H. J., 3rd, Shooter E. M. Studies on the turnover of mouse brain synaptosomal proteins. J Neurochem. 1971 Dec;18(12):2279–2290. doi: 10.1111/j.1471-4159.1971.tb00184.x. [DOI] [PubMed] [Google Scholar]
  34. Omura T., Siekevitz P., Palade G. E. Turnover of constituents of the endoplasmic reticulum membranes of rat hepatocytes. J Biol Chem. 1967 May 25;242(10):2389–2396. [PubMed] [Google Scholar]
  35. Siekevitz P. Biological membranes: the dynamics of their organization. Annu Rev Physiol. 1972;34:117–140. doi: 10.1146/annurev.ph.34.030172.001001. [DOI] [PubMed] [Google Scholar]
  36. Vandermeers A., Khayat M. H., Rathé J., Christophe J. Vies moyennes de cinq hydrolases dans le pancréas du rat normal ou en malnutrition protidique. Biochim Biophys Acta. 1968 Jun 24;158(3):448–455. [PubMed] [Google Scholar]
  37. Viveros O. H., Arqueros L., Kirshner N. Mechanism of secretion from the adrenal medulla. VII. Effect of insulin administration on the buoyant density, dopamine -hydroxylase, and catecholamine content of adrenal storage vesicles. Mol Pharmacol. 1971 Jul;7(4):444–454. [PubMed] [Google Scholar]

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