Skip to main content
PMC home page
Biochemical Journal logoLink to Biochemical Journal
. 1989 Sep 1;262(2):605–610. doi: 10.1042/bj2620605

A multicompartmental model of fluid-phase endocytosis in rabbit liver parenchymal cells.

R Blomhoff 1, M S Nenseter 1, M H Green 1, T Berg 1
PMCID: PMC1133311  PMID: 2803270

Abstract

Fluid-phase endocytosis was studied in isolated rabbit liver parenchymal cells by using 125I-poly(vinylpyrrolidone) (PVP) as a marker. First, uptake of 125I-PVP by cells was determined. Also, cells were loaded with 125I-PVP for 20, 60 and 120 min, and release of marker was monitored for 120-220 min. Then we used the Simulation, Analysis and Modeling (SAAM) computer program and the technique of model-based compartmental analysis to develop a mechanistic model for fluid-phase endocytosis in these cells. To fit all data simultaneously, a model with three cellular compartments and one extracellular compartment was required. The three kinetically distinct cellular compartments are interpreted to represent (1) early endosomes, (2) a prelysosomal compartment equivalent to the compartment for uncoupling of receptor and ligand (CURL) and/or multivesicular bodies (MVB), and (3) lysosomes. The model predicts that approx. 80% of the internalized 125I-PVP was recycled to the medium from the early-endosome compartment. The apparent first-order rate constant for this recycling was 0.094 min-1, thus indicating that an average 125I-PVP molecule is recycled in 11 min. The model also predicts that recycling to the medium occurs from all three intracellular compartments. From the prelysosomal compartment, 40% of the 125I-PVP molecules are predicted to recycle to the medium and 60% are transferred to the lysosomal compartment. The average time for recycling from the prelysosomal compartment to the medium was estimated to be 66 min. For 125I-PVP in the lysosomal compartment, 0.3%/min was transferred back to the medium. These results, and the model developed to interpret the data, predict that there is extensive recycling of material endocytosed by fluid-phase endocytosis to the extracellular environment in rabbit liver parenchymal cells.

Full text

PDF
605

Selected References

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

  1. Berg T., Kindberg G. M., Ford T., Blomhoff R. Intracellular transport of asialoglycoproteins in rat hepatocytes. Evidence for two subpopulations of lysosomes. Exp Cell Res. 1985 Dec;161(2):285–296. doi: 10.1016/0014-4827(85)90086-2. [DOI] [PubMed] [Google Scholar]
  2. Besterman J. M., Airhart J. A., Woodworth R. C., Low R. B. Exocytosis of pinocytosed fluid in cultured cells: kinetic evidence for rapid turnover and compartmentation. J Cell Biol. 1981 Dec;91(3 Pt 1):716–727. doi: 10.1083/jcb.91.3.716. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Buktenica S., Olenick S. J., Salgia R., Frankfater A. Degradation and regurgitation of extracellular proteins by cultured mouse peritoneal macrophages and baby hamster kidney fibroblasts. Kinetic evidence that the transfer of proteins to lysosomes is not irreversible. J Biol Chem. 1987 Jul 15;262(20):9469–9476. [PubMed] [Google Scholar]
  4. England I. G., Naess L., Blomhoff R., Berg T. Uptake, intracellular transport and release of 125I-poly(vinylpyrrolidone) and [14C]-sucrose-asialofetuin in rat liver parenchymal cells. Effects of ammonia on the intracellular transport. Biochem Pharmacol. 1986 Jan 15;35(2):201–208. doi: 10.1016/0006-2952(86)90514-9. [DOI] [PubMed] [Google Scholar]
  5. Foster D. M., Aamodt R. L., Henkin R. I., Berman M. Zinc metabolism in humans: a kinetic model. Am J Physiol. 1979 Nov;237(5):R340–R349. doi: 10.1152/ajpregu.1979.237.5.R340. [DOI] [PubMed] [Google Scholar]
  6. Geuze H. J., Slot J. W., Strous G. J., Peppard J., von Figura K., Hasilik A., Schwartz A. L. Intracellular receptor sorting during endocytosis: comparative immunoelectron microscopy of multiple receptors in rat liver. Cell. 1984 May;37(1):195–204. doi: 10.1016/0092-8674(84)90315-5. [DOI] [PubMed] [Google Scholar]
  7. Goldstein J. L., Brown M. S., Anderson R. G., Russell D. W., Schneider W. J. Receptor-mediated endocytosis: concepts emerging from the LDL receptor system. Annu Rev Cell Biol. 1985;1:1–39. doi: 10.1146/annurev.cb.01.110185.000245. [DOI] [PubMed] [Google Scholar]
  8. Goud B., Jouanne C., Antoine J. C. Reversible pinocytosis of horseradish peroxidase in lymphoid cells. Exp Cell Res. 1984 Jul;153(1):218–235. doi: 10.1016/0014-4827(84)90463-4. [DOI] [PubMed] [Google Scholar]
  9. Green M. H., Uhl L., Green J. B. A multicompartmental model of vitamin A kinetics in rats with marginal liver vitamin A stores. J Lipid Res. 1985 Jul;26(7):806–818. [PubMed] [Google Scholar]
  10. Hornick C. A., Hamilton R. L., Spaziani E., Enders G. H., Havel R. J. Isolation and characterization of multivesicular bodies from rat hepatocytes: an organelle distinct from secretory vesicles of the Golgi apparatus. J Cell Biol. 1985 May;100(5):1558–1569. doi: 10.1083/jcb.100.5.1558. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Jones R. H., Reeve E. B., Swanson G. D. Statistical identification of compartmental models with application to plasma protein kinetics. Comput Biomed Res. 1984 Jun;17(3):277–288. doi: 10.1016/s0010-4809(84)80019-1. [DOI] [PubMed] [Google Scholar]
  12. Kooistra T., Pratten M. K., Lloyd J. B. Serum-dependence of fluid-phase pinocytosis and specificity in adsorptive pinocytosis of simple proteins in rat peritoneal macrophages. Biosci Rep. 1981 Jul;1(7):587–594. doi: 10.1007/BF01116309. [DOI] [PubMed] [Google Scholar]
  13. Malmendier C. L., Delcroix C., Berman M. Interrelations in the oxidative metabolism of free fatty acids, glucose, and glycerol in normal and hyperlipemic patients. A compartmental model. J Clin Invest. 1974 Aug;54(2):461–476. doi: 10.1172/JCI107782. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Morrill G. A., Kostellow A. B., Weinstein S. P. Endocytosis in the amphibian oocyte. Effect of insulin and progesterone on membrane and fluid internalization during the meiotic divisions. Biochim Biophys Acta. 1984 Feb 17;803(1-2):71–77. doi: 10.1016/0167-4889(84)90056-9. [DOI] [PubMed] [Google Scholar]
  15. Munniksma J., Noteborn M., Kooistra T., Stienstra S., Bouma J. M., Gruber M., Brouwer A., Praaning-van Dalen Dalen D., Knook D. L. Fluid endocytosis by rat liver and spleen. Experiments with 125I-labelled poly(vinylpyrrolidone) in vivo. Biochem J. 1980 Nov 15;192(2):613–621. doi: 10.1042/bj1920613. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Nenseter M. S., Blomhoff R., Drevon C. A., Kindberg G. M., Norum K. R., Berg T. Uptake of LDL in parenchymal and non-parenchymal rabbit liver cells in vivo. LDL uptake is increased in endothelial cells in cholesterol-fed rabbits. Biochem J. 1988 Sep 1;254(2):443–448. doi: 10.1042/bj2540443. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Scharschmidt B. F., Lake J. R., Renner E. L., Licko V., Van Dyke R. W. Fluid phase endocytosis by cultured rat hepatocytes and perfused rat liver: implications for plasma membrane turnover and vesicular trafficking of fluid phase markers. Proc Natl Acad Sci U S A. 1986 Dec;83(24):9488–9492. doi: 10.1073/pnas.83.24.9488. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Seglen P. O. Preparation of isolated rat liver cells. Methods Cell Biol. 1976;13:29–83. doi: 10.1016/s0091-679x(08)61797-5. [DOI] [PubMed] [Google Scholar]
  19. Steinman R. M., Mellman I. S., Muller W. A., Cohn Z. A. Endocytosis and the recycling of plasma membrane. J Cell Biol. 1983 Jan;96(1):1–27. doi: 10.1083/jcb.96.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Tolleshaug H., Berg T., Nilsson M., Norum K. R. Uptake and degradation of 125I-labelled asialo-fetuin by isolated rat hepatocytes. Biochim Biophys Acta. 1977 Aug 25;499(1):73–84. doi: 10.1016/0304-4165(77)90230-6. [DOI] [PubMed] [Google Scholar]
  21. Wang E., Michl J., Pfeffer L. M., Silverstein S. C., Tamm I. Interferon suppresses pinocytosis but stimulates phagocytosis in mouse peritoneal macrophages: related changes in cytoskeletal organization. J Cell Biol. 1984 Apr;98(4):1328–1341. doi: 10.1083/jcb.98.4.1328. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Wastney M. E., Hall S. E., Berman M. Ketone body kinetics in humans: a mathematical model. J Lipid Res. 1984 Feb;25(2):160–174. [PubMed] [Google Scholar]
  23. Wileman T., Harding C., Stahl P. Receptor-mediated endocytosis. Biochem J. 1985 Nov 15;232(1):1–14. doi: 10.1042/bj2320001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. van Deurs B., Röpke C., Thorball N. Kinetics of pinocytosis studied by flow cytometry. Eur J Cell Biol. 1984 May;34(1):96–102. [PubMed] [Google Scholar]

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

RESOURCES