Endosome Processing: Structural, Functional and Kinetic Interrelations

  • Lutz Thilo

Abstract

Clostridial neurotoxins exert their effect from within the cytoplasm of nerve cells. Rather than gaining direct access through the cell-surface membrane, the toxin exploits the process of endocytosis to gain entry into cells. As this would still leave the toxin on the exoplasmic side of the endocytic membrane, a translocation step through the membrane into the cytoplasm must follow at some stage along the endocytic pathway. An awareness of the steps which are involved in endosome processing can be helpful to assess the mechanism by which the toxin can reach its site of action in the cell.

Keywords

Leukemia Cysteine Fractionation Polypeptide Hydrochloride 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Courtoy PJ. Dissection of endosomes. In Steer C, Hanover J, eds. Intracellular trafficking of proteins. Cambridge University Press, 1991: 103.Google Scholar
  2. 2.
    Burgess TL, Kelly RB. Constitutive and regulated secretion of proteins. Ann Rev Cell Biol 1987; 3: 243.PubMedCrossRefGoogle Scholar
  3. 3.
    Goldstein IL, Brown MS, Anderson RGW, Russell DW, Schneider, WJ. Receptor-mediated endocytosis: Concepts emerging from the LDL receptor system. Ann Rev Cell Biol 1985; 1: 1.PubMedCrossRefGoogle Scholar
  4. 4.
    Raub TJ, Koroly MJ, Roberts RM. Rapid endocytosis and recycling of wheat germ agglutinin binding sites on CHO cells: Evidence for two compartments in a nondegradative pathway. J Cell Physiol 1990; 144: 52.PubMedCrossRefGoogle Scholar
  5. 5.
    Sandvig K, Olsnes S, Brown JE, Petersen OW, van Deurs B. Endocytosis from coated pits of Shiga toxin: a glycolipid-binding protein from Shigella dysenteriae 1. J Cell Biol 1989; 108: 1331.PubMedCrossRefGoogle Scholar
  6. 6.
    Marsh M. The entry of enveloped viruses into cells by endocytosis. Biochem. J. 1984; 218: 1.PubMedGoogle Scholar
  7. 7.
    Green SA, Kelly RB. Endocytic membrane traffic to the Golgi apparatus in a regulated secretory cell line. J. Biol. Chem. 1990; 265: 2 1269.Google Scholar
  8. 8.
    Brodsky FM, Hill BL, Acton SL, Näthke I, Wong DH, Ponnambalam S, Parham P. Clathrin light chains: arrays of protein motifs that regulate coated-vesicle dynamics. Trends Biochem Sci 1991; 16: 208.PubMedCrossRefGoogle Scholar
  9. 9.
    Hansen SH, Sandvig K, van Deurs B. The pre-endosomal compartment comprises distinct coated and noncoated endocytic vesicle populations. J Cell Biol 1991; 113: 731.PubMedCrossRefGoogle Scholar
  10. 10.
    Tran D, Carpentier J-L, Sawano F, Gordon P, Orci L. Ligands internalized through coated and noncoated invaginations follow a common intracellular pathway. Proc Natl Acad Sci USA 1987; 84: 7957.PubMedCrossRefGoogle Scholar
  11. 11.
    Montesano R, Roth J, Robert A, Orci L. Non-coated membrane invaginations are involved in binding and internalization of cholera and tetanus toxins. Nature 1982; 296: 651.PubMedCrossRefGoogle Scholar
  12. 12.
    Keen JH. Clathrin and associated assembly and disassembly proteins. Ann Rev Biochem 1990; 59: 415.PubMedCrossRefGoogle Scholar
  13. 13.
    Ahle S, Ungewickell E. Auxilin, a newly identified clathrin-associated protein in coated vesicles from bovine brain. J Cell Biol 1990; 111: 19.PubMedCrossRefGoogle Scholar
  14. 14.
    McCloskey M, Poo M-M. Protein diffusion in cell membranes: Some biological implications. Int Rev Cytol 1984; 87: 19.PubMedCrossRefGoogle Scholar
  15. 15.
    Hopkins CR. Selective membrane protein trafficking: vectorial flow and filter. Trends Biochem Sci 1992; 17: 27.PubMedCrossRefGoogle Scholar
  16. 16.
    Dunn WA, Hubbard AL. Receptor-mediated endocytosis of epidermal growth factor by hepatocytes in the perfused rat liver: ligand and receptor dynamics. J Cell Biol 1984; 98: 2148.Google Scholar
  17. 17.
    Anderson RGW, Brown MS, Goldstein IL. Role of the coated endocytic vesicle in the uptake of receptor bound low density lipoprotein in human fibroblasts. Cell 1977; 10: 351.PubMedCrossRefGoogle Scholar
  18. 18.
    Griffiths G, Back R, Marsh M. A quantitative analysis of the endocytic pathway in Baby Hamster Kidney cells. J Cell Biol 1989; 109: 2703.Google Scholar
  19. 19.
    Thilo L. Quantification of endocytosis-derived membrane traffic. Biochim Biophys Acta 1985; 822: 243.PubMedCrossRefGoogle Scholar
  20. 20.
    Mellman IS, Steinman RM, Unkeless JC, Cohn ZA. Selective iodination and polypeptide composition of pinocytic vesicles. J Cell Biol 1980; 86: 712.PubMedCrossRefGoogle Scholar
  21. 21.
    Koval M, Pagano RE. Lipid recycling between the plasma membrane and intracellular compartments: Transport and metabolism of fluorescent sphingomyelin analogues in cultured fibroblasts. J Cell Biol 1989; 108: 2169.Google Scholar
  22. 22.
    Bretscher MS, Lutter R. A new method for detecting endocytosed proteins. EMBO J 1988; 7: 4087.PubMedGoogle Scholar
  23. 23.
    Phillips JH, Burridge K, Wilson SP, Kirshner N. Visualization of the exocytosis/endocytosis secretory cycle in cultured adrenal chromaffin cells. J Cell Biol 1983; 97: 1906.PubMedCrossRefGoogle Scholar
  24. 24.
    Patzak A, Böck G, Fischer-Colbrie R, Schauenstein K, Schmidt W, Lingg G, Winkler H. Exocytic exposure and retrieval of membrane antigens of chromaffin granules: Quantitative evaluation of immunofluorescence on the surface of chromaffin cells. J Cell Biol 1984; 98: 1817.PubMedCrossRefGoogle Scholar
  25. 25.
    van Grafenstein H, Roberts CS, Baker PF. Kinetic analysis of the triggered exocytosis/endocytosis secretory cycle in cultured bovine adrenal medullary cells. J Cell Biol 1986; 103: 2343.Google Scholar
  26. 26.
    Bonifacino JS, Perez P, Klausner RD, Sandoval IV. Study of the transit of an integral membrane protein from secretory granules through the plasma membrane of secreting rat basophilic leukemia cells using a specific monoclonal antibody. J Cell Biol 1986; 102: 516.PubMedCrossRefGoogle Scholar
  27. 27.
    Patzak A, Winkler H. Exocytotic exposure and recycling of membrane antigens of chromaffin granules: Ultrastructural evaluation after immunolabeling. J Cell Biol 1986; 102: 510.PubMedCrossRefGoogle Scholar
  28. 28.
    Torri-Tarelli F, Villa A, Valtorta F, De Camilli P, Greengard P, Ceccarelli B. Redistribution of synaptophysin and synapsin I during oe-lactrotoxin-induced release of neurotransmitter at the neuromuscular junction. J Cell Biol 1990; 110: 449.PubMedCrossRefGoogle Scholar
  29. 29.
    Thilo L. Selective internalization of granule membrane after secretion in mast cells. Proc Natl Acad Sci USA 1985; 82: 1711.PubMedCrossRefGoogle Scholar
  30. 30.
    Black JD, Dolly JO. Interaction of 125I-labeled Botulinum neurotoxins with nerve terminals. II. Autoradiographic evidence for its uptake into motor nerves by acceptor-mediated endocytosis. J Cell Biol 1986; 103: 535.PubMedCrossRefGoogle Scholar
  31. 31.
    Hopkins CR, Gibson A, Shipman M, Miller K. Movement of internalized ligand-receptor complexes along a continuous endosomal reticulum. Nature 1990; 346: 335.PubMedCrossRefGoogle Scholar
  32. 32.
    Griffiths G, Hoflack B, Simons K, Mellman I, Kornfeld S. The mannose 6-phosphate receptor and the biogenesis of lysosomes. Cell 1988; 52: 329.PubMedCrossRefGoogle Scholar
  33. 33.
    Tooze J, Hollinshead M. Tubular early endosomal networks in AtT20 and other cells. J Cell Biol 1991; 115: 635.PubMedCrossRefGoogle Scholar
  34. 34.
    Knapp PE, Swanson JA. Plasticity of the tubular lysosomal compartment in macrophages. J Cell Sci 1990; 95: 433.PubMedGoogle Scholar
  35. 35.
    Mellman I, Fuchs R, Helenius A. Acidification of the endocytic and exocytic pathways. Ann Rev Biochem 1986; 55: 663.PubMedCrossRefGoogle Scholar
  36. 36.
    Yamashiro DJ, Maxfield FR. Acidification of morphologically distinct endosomes in mutant and wild-type Chinese Hamster Ovary cells. J Cell Biol 1987; 105: 2723.Google Scholar
  37. 37.
    Cain CC, Sipe DM, Murphy RM. Regulation of endocytic pH by Na+,K+-ATPase in living cells. Proc Natl Acad Sci USA 1989; 86: 544.PubMedCrossRefGoogle Scholar
  38. 38.
    Dean RT, Jessup W, Roberts CR. Effects of exogenous amines on mammalian cells, with particular reference to membrane flow. Biochem J 1984; 217: 27.PubMedGoogle Scholar
  39. 39.
    Simpson LL. Ammonium chloride and methylamine hydrochloride antagonise clostridial neurotoxins. J Pharmacol Exp Ther 1983; 225: 546.PubMedGoogle Scholar
  40. 40.
    Blum JS, Fiani ML, Stahl PD. Proteolytic cleavage of ricin A chain in endosomal vesicles. J Biol Chem 1991; 266: 2 2091.Google Scholar
  41. 41.
    Dunn KW, McGraw TE, Maxfield FR. Iterative fractionation of recycling receptors from lysosomally destined ligands in an early sorting endosome. J Cell Biol 1989; 109: 3303.PubMedCrossRefGoogle Scholar
  42. 42.
    Ward DM, Ajioka R, Kaplan J. Cohort movement of different ligands and receptors in the intracellular endocytic pathway of alveolar macrophages. J Biol Chem 1989; 264: 8164.PubMedGoogle Scholar
  43. 43.
    Stoorvogel W, Geuze HJ, Griffith JM, Schwartz AL, Strous GJ. Relations between the intracellular pathways of the receptors for transferrin, asialoglycoprotein, and mannose 6-phosphate in human hepatoma cells. J Cell Biol 1989; 108: 2137.Google Scholar
  44. 44.
    Linderman JJ, Lauffenburger DA. Analysis of intracellular receptor/ligand sorting in endosomes. J Theor Biol 1988; 132: 203.PubMedCrossRefGoogle Scholar
  45. 45.
    Haylett T, Thilo L. Limited and selective transfer of plasma membrane glycoproteins to membrane of secondary lysosomes. J Cell Biol 1986; 103: 1249.PubMedCrossRefGoogle Scholar
  46. 46.
    Woods JW, Doriaux M, Farquhar MG. Transferrin receptors recycle to cis and middle as well as trans Golgi cisternae in Ig-secreting myeloma cells. J Cell Biol 1986; 103: 277.PubMedCrossRefGoogle Scholar
  47. 47.
    Jin M, Sahagian GG, Snider MD. Transport of surface mannose 6-phosphate receptor to the Golgi complex in cultured human cells. J Biol Chem 1989; 263: 7675.Google Scholar
  48. 48.
    van Deurs B, Sandvig K, Petersen OW, Olsnes S, Simons K, Griffiths G. Estimation of the amount of internalized ricin that reaches the trans-Golgi network. J Cell Biol 1988; 106: 253.PubMedCrossRefGoogle Scholar
  49. 49.
    Farquhar MG. Progress in unraveling pathways of Golgi traffic. Ann Rev Cell Biol 1985; 1: 447.PubMedCrossRefGoogle Scholar
  50. 50.
    Griffiths G, Gruenberg J. The arguments for pre-existing early and late endosomes. Trends Cell Biol 1991; 1: 5.PubMedCrossRefGoogle Scholar
  51. 51.
    Stoorvogel W, Strous GJ, Geuze HJ, Oorschot V, Schwartz AL. Late endosomes derive from early endosomes by maturation. 1991; Cell 65: 417.PubMedCrossRefGoogle Scholar
  52. 52.
    Rothman JE, Orci L. Molecular dissection of the secretory pathway. Nature 1992; 355: 409.PubMedCrossRefGoogle Scholar
  53. 53.
    Roederer M, Barry JR, Wilson RB, Murphy RF. Endosomes can undergo an ATP-dependent density increase in the absence of dense lysosomes. Eur J Cell Biol 1990; 51: 229.PubMedGoogle Scholar
  54. 54.
    Mullock BM, Branch WJ, van Schaik M, Gilbert LK, Luzio JP. Reconstitution of an endosomelysosome interaction in a cell-free system. J Cell Biol 1989; 108: 2093.Google Scholar
  55. 55.
    Ward DM, Hackenyos DP, Kaplan J. Fusion of sequentially internalized vesicles in alveolar macrophages. J Cell Biol 1990; 110: 1013.PubMedCrossRefGoogle Scholar
  56. 56.
    Salzman NH, Maxfield FR. Fusion accessibility of endocytic compartments along the recycling and lysosomal endocytic pathways in intact cells. J Cell Biol 1989; 109: 2097.Google Scholar
  57. 57.
    Mayorga LS, Diaz R, Stahl PD. Plasma membrane-derived vesicles containing receptor-ligand complexes are fusogenic with early endosomes in a cell-free system. J Biol Chem 1988; 263: 17213.PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 1993

Authors and Affiliations

  • Lutz Thilo
    • 1
  1. 1.Dept. of Medical BiochemistryUniversity of Cape Town Medical SchoolObservatory, Cape TownSouth Africa

Personalised recommendations