Skip to main content
NCBI home page
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1996 Mar 5;93(5):1786–1791. doi: 10.1073/pnas.93.5.1786

The nucleation of receptor-mediated endocytosis.

D A Edwards 1, K J Gooch 1, I Zhang 1, G H McKinley 1, R Langer 1
PMCID: PMC39859  PMID: 8700836

Abstract

A theory of the mechanical origins of receptor-mediated endocytosis shows that a spontaneous membrane complex formation can provide the stimulus for a local membrane motion toward the cytosol. This motion is identified with a nucleation stage of receptor-mediated endocytosis. When membrane complexes cluster, membrane deformation is predicted to be most rapid. The rate of growth of membrane depressions depends upon the relative rates of approach of aqueous cytosolic and extracellular fluids toward the cell membrane. With cytosolic and extracellular media characterized by apparent viscosities, the rate of growth of membrane depressions is predicted to increase as the extracellular viscosity nears the apparent viscosity of the cytosol and then to decrease when the extracellular viscosity exceeds that of the cytosol. To determine whether these trends would be apparent in the overall endocytosis rate constant, an experimental study of transferrin-mediated endocytosis in two different cell lines was conducted. The experimental results reveal the same dependence of internalization rate on extracellular viscosity as predicted by the theory. These and other comparisons with experimental data suggest that the nucleation stage of receptor-mediated endocytosis is important in the overall endocytosis process.

Full text

PDF
1786

Selected References

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

  1. Aaronson S. A. Growth factors and cancer. Science. 1991 Nov 22;254(5035):1146–1153. doi: 10.1126/science.1659742. [DOI] [PubMed] [Google Scholar]
  2. Brodsky F. M., Hill B. L., Acton S. L., Näthke I., Wong D. H., Ponnambalam S., Parham P. Clathrin light chains: arrays of protein motifs that regulate coated-vesicle dynamics. Trends Biochem Sci. 1991 Jun;16(6):208–213. doi: 10.1016/0968-0004(91)90087-c. [DOI] [PubMed] [Google Scholar]
  3. Carpentier J. L., Gorden P., Anderson R. G., Goldstein J. L., Brown M. S., Cohen S., Orci L. Co-localization of 125I-epidermal growth factor and ferritin-low density lipoprotein in coated pits: a quantitative electron microscopic study in normal and mutant human fibroblasts. J Cell Biol. 1982 Oct;95(1):73–77. doi: 10.1083/jcb.95.1.73. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Chien S., Sung K. L., Skalak R., Usami S., Tözeren A. Theoretical and experimental studies on viscoelastic properties of erythrocyte membrane. Biophys J. 1978 Nov;24(2):463–487. doi: 10.1016/S0006-3495(78)85395-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Ciechanover A., Schwartz A. L., Dautry-Varsat A., Lodish H. F. Kinetics of internalization and recycling of transferrin and the transferrin receptor in a human hepatoma cell line. Effect of lysosomotropic agents. J Biol Chem. 1983 Aug 25;258(16):9681–9689. [PubMed] [Google Scholar]
  6. Deeley J. O., Crum L. A., Coakley W. T. The influence of temperature and incubation time on deformability of human erythrocytes. Biochim Biophys Acta. 1979 Jun 13;554(1):90–101. doi: 10.1016/0005-2736(79)90009-9. [DOI] [PubMed] [Google Scholar]
  7. Evans E. A. Bending elastic modulus of red blood cell membrane derived from buckling instability in micropipet aspiration tests. Biophys J. 1983 Jul;43(1):27–30. doi: 10.1016/S0006-3495(83)84319-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Evans E., Yeung A. Apparent viscosity and cortical tension of blood granulocytes determined by micropipet aspiration. Biophys J. 1989 Jul;56(1):151–160. doi: 10.1016/S0006-3495(89)82660-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Gallez D., Coakley W. T. Interfacial instability at cell membranes. Prog Biophys Mol Biol. 1986;48(3):155–199. doi: 10.1016/0079-6107(86)90011-8. [DOI] [PubMed] [Google Scholar]
  10. 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]
  11. Ingber D. E., Dike L., Hansen L., Karp S., Liley H., Maniotis A., McNamee H., Mooney D., Plopper G., Sims J. Cellular tensegrity: exploring how mechanical changes in the cytoskeleton regulate cell growth, migration, and tissue pattern during morphogenesis. Int Rev Cytol. 1994;150:173–224. doi: 10.1016/s0074-7696(08)61542-9. [DOI] [PubMed] [Google Scholar]
  12. Jing S. Q., Spencer T., Miller K., Hopkins C., Trowbridge I. S. Role of the human transferrin receptor cytoplasmic domain in endocytosis: localization of a specific signal sequence for internalization. J Cell Biol. 1990 Feb;110(2):283–294. doi: 10.1083/jcb.110.2.283. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Leckband D. E., Israelachvili J. N., Schmitt F. J., Knoll W. Long-range attraction and molecular rearrangements in receptor-ligand interactions. Science. 1992 Mar 13;255(5050):1419–1421. doi: 10.1126/science.1542789. [DOI] [PubMed] [Google Scholar]
  14. Lisanti M. P., Caras I. W., Gilbert T., Hanzel D., Rodriguez-Boulan E. Vectorial apical delivery and slow endocytosis of a glycolipid-anchored fusion protein in transfected MDCK cells. Proc Natl Acad Sci U S A. 1990 Oct;87(19):7419–7423. doi: 10.1073/pnas.87.19.7419. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. McGraw T. E., Greenfield L., Maxfield F. R. Functional expression of the human transferrin receptor cDNA in Chinese hamster ovary cells deficient in endogenous transferrin receptor. J Cell Biol. 1987 Jul;105(1):207–214. doi: 10.1083/jcb.105.1.207. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Moy V. T., Florin E. L., Gaub H. E. Intermolecular forces and energies between ligands and receptors. Science. 1994 Oct 14;266(5183):257–259. doi: 10.1126/science.7939660. [DOI] [PubMed] [Google Scholar]
  17. Mulligan R. C. The basic science of gene therapy. Science. 1993 May 14;260(5110):926–932. doi: 10.1126/science.8493530. [DOI] [PubMed] [Google Scholar]
  18. Pagano R. E. Lipid traffic in eukaryotic cells: mechanisms for intracellular transport and organelle-specific enrichment of lipids. Curr Opin Cell Biol. 1990 Aug;2(4):652–663. doi: 10.1016/0955-0674(90)90107-p. [DOI] [PubMed] [Google Scholar]
  19. Pley U., Parham P. Clathrin: its role in receptor-mediated vesicular transport and specialized functions in neurons. Crit Rev Biochem Mol Biol. 1993;28(5):431–464. doi: 10.3109/10409239309078441. [DOI] [PubMed] [Google Scholar]
  20. Rodman J. S., Mercer R. W., Stahl P. D. Endocytosis and transcytosis. Curr Opin Cell Biol. 1990 Aug;2(4):664–672. doi: 10.1016/0955-0674(90)90108-q. [DOI] [PubMed] [Google Scholar]
  21. Rothberg K. G., Ying Y. S., Kolhouse J. F., Kamen B. A., Anderson R. G. The glycophospholipid-linked folate receptor internalizes folate without entering the clathrin-coated pit endocytic pathway. J Cell Biol. 1990 Mar;110(3):637–649. doi: 10.1083/jcb.110.3.637. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Sandvig K., van Deurs B. Endocytosis without clathrin (a minireview). Cell Biol Int Rep. 1991 Jan;15(1):3–8. doi: 10.1016/0309-1651(91)90077-v. [DOI] [PubMed] [Google Scholar]
  23. Schmid S. L. Biochemical requirements for the formation of clathrin- and COP-coated transport vesicles. Curr Opin Cell Biol. 1993 Aug;5(4):621–627. doi: 10.1016/0955-0674(93)90131-9. [DOI] [PubMed] [Google Scholar]
  24. Schonhorn J. E., Wessling-Resnick M. Brefeldin A down-regulates the transferrin receptor in K562 cells. Mol Cell Biochem. 1994 Jun 29;135(2):159–169. doi: 10.1007/BF00926519. [DOI] [PubMed] [Google Scholar]
  25. Smythe E., Carter L. L., Schmid S. L. Cytosol- and clathrin-dependent stimulation of endocytosis in vitro by purified adaptors. J Cell Biol. 1992 Dec;119(5):1163–1171. doi: 10.1083/jcb.119.5.1163. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Smythe E., Pypaert M., Lucocq J., Warren G. Formation of coated vesicles from coated pits in broken A431 cells. J Cell Biol. 1989 Mar;108(3):843–853. doi: 10.1083/jcb.108.3.843. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. 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]
  28. Trowbridge I. S. Endocytosis and signals for internalization. Curr Opin Cell Biol. 1991 Aug;3(4):634–641. doi: 10.1016/0955-0674(91)90034-v. [DOI] [PubMed] [Google Scholar]
  29. Wang N., Butler J. P., Ingber D. E. Mechanotransduction across the cell surface and through the cytoskeleton. Science. 1993 May 21;260(5111):1124–1127. doi: 10.1126/science.7684161. [DOI] [PubMed] [Google Scholar]
  30. Wang N., Ingber D. E. Control of cytoskeletal mechanics by extracellular matrix, cell shape, and mechanical tension. Biophys J. 1994 Jun;66(6):2181–2189. doi: 10.1016/S0006-3495(94)81014-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Wiley H. S., Herbst J. J., Walsh B. J., Lauffenburger D. A., Rosenfeld M. G., Gill G. N. The role of tyrosine kinase activity in endocytosis, compartmentation, and down-regulation of the epidermal growth factor receptor. J Biol Chem. 1991 Jun 15;266(17):11083–11094. [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES