Dense core lysosomes can fuse with late endosomes and are re-formed from the resultant hybrid organelles

Journal of Cell Science

Volumn 110, Issue 17, 1997, Pages 2027-2040

  Bright, Nicholas A ^a   Reaves, Barbara J ^a   Mullock, Barbara M ^a   Luzio, J Paul ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Electron microscopy; Endocytosis; Lysosome biogenesis

Indexed keywords

BETA FRUCTOFURANOSIDASE; BOVINE SERUM ALBUMIN; SOMATOMEDIN B RECEPTOR; WORTMANNIN;

ARTICLE; CELL ORGANELLE; ELECTRON MICROSCOPY; ENDOCYTOSIS; ENDOSOME; LYSOSOME; PRIORITY JOURNAL;

ANDROSTADIENES; ANIMALS; ANTIGENS, CD; BETA-FRUCTOFURANOSIDASE; CATHEPSINS; CELLS, CULTURED; CYSTEINE ENDOPEPTIDASES; ENDOCYTOSIS; ENDOPEPTIDASES; ENDOSOMES; ENZYME INHIBITORS; ENZYME PRECURSORS; FIBROBLASTS; GLYCOSIDE HYDROLASES; GOLD; HYDROLASES; KIDNEY; LYSOSOME-ASSOCIATED MEMBRANE GLYCOPROTEINS; LYSOSOMES; MEMBRANE GLYCOPROTEINS; MICROSCOPY, IMMUNOELECTRON; RATS; RECEPTOR, IGF TYPE 2; SERUM ALBUMIN, BOVINE; SUCROSE;

BOVINAE;

EID: 0030783009     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (65)

1. Aniento, F., Emans, N., Griffiths, G. and Gruenberg, J. (1993). Cytoplasmic dynein-dependent vesicular transport from early to late endosomes. J. Cell Biol. 123, 1373-1388.
2. Aniento, F., Gu, F., Parton, R. G. and Gruenberg, J. (1996). An endosomal β-COP is involved in the pH-dependent formation of transport vesicles destined for late endosomes. J. Cell Biol. 133, 29-41.
3. Berg, T., Gjoen, T. and Bakke, O. (1995). Physiological functions of endosomal proteolysis. Biochem. J. 307, 313-326.
4. Cohn, Z. A. and Ehrenreich, B. A. (1969). The uptake, storage and intracellular hydrolysis of carbohydrates by macrophages. J. Exp. Med. 129, 201-225.
5. DeCourcy, K. and Storrie, B. (1991). Osmotic swelling of endocytic compartments induced by internalised sucrose is restricted to mature lysosomes in cultured mammalian cells. Exp. Cell Res. 192, 52-60.
6. De Duve, C. (1963). General properties of lysosomes: the lysosome concept. In Lysosomes. Ciba Foundation Symposium (ed. A. V. S. De Reuck and M. P. Cameron). pp. 1-31. Churchill Livingstone, London.
7. De Duve, C. and Wattiaux, R. (1966). Functions of lysosomes. Annu. Rev. Physiol. 28, 435-492.
8. De Duve, C. (1983). Lysosomes revisited. Eur. J. Biochem. 137, 391-397.
9. De Mey, J. (1986). The preparation and use of gold probes. In Practical Applications in Pathology and Biology (ed. J. M. Polak and S. Van Noorden). pp. 115-145, Wright, Bristol, UK.
10. Deng, Y. and Storrie, B. (1988). Animal cell lysosomes rapidly exchange membrane proteins. Proc. Nat. Acad. Sci. USA 85, 3860-3864.
11. Deng, Y., Griffiths, G. and Storrie, B. (1991). Comparative behaviour of lysosomes and the prelysosomal compartment (PLC) in in vivo cell fusion experiments. J. Cell Sci. 99, 571-582.
12. 125I-asialofetuin by the perfused rat liver. J. Biol. Chem. 255, 5971-5978.
13. Felder, S., Miller, K., Moehren, G., Ullrich, A., Schlessinger, J. and Hopkins, C. R. (1990). Kinase activity controls the sorting of the epidermal growth factor receptor within the multivesicular body. Cell 61, 623-634.
14. Futter, C. E., Pearse, A., Hewlett, L. J. and Hopkins, C. R. (1996). Multivesicular endosomes containing internalised HGF-EGF receptor complexes mature and then fuse directly with lysosomes. J. Cell Biol. 132, 1011-1023
15. Geuze, H. J., Stoorvogel, W., Strous, G. J., Slot, J. W., Bleekemolen, J. E. and Mellman, I. (1988). Sorting of mannose-6-phosphate receptors and lysosomal membrane proteins in endocytic vesicles. J. Cell Biol. 107, 2491-2501.
16. Griffiths, G., Hoflack, B., Simons, K., Mellman, I. and Kornfeld, S. (1988). The mannose-6-phosphate receptor and the biogenesis of lysosomes. Cell 52, 329-341.
17. Griffiths, G., Matteoni, R., Bach, R. and Hoflack, B. (1990). Characterization of the cation-independent mannose-6-phosphate receptor-enriched prelysosomal compartment in NRK cells. J. Cell Sci. 95, 441-461.
18. Griffiths, G. and Gruenberg, J. (1991). The arguments for pre-existing early and late endosomes. Trends Cell Biol. 1, 5-9.
19. Griffiths, G. (1993). Fine structure immunocytochemistry. pp. 1-459, Springer-Verlag, Berlin.
20. Griffiths, G. (1996). On vesicles and membrane compartments. Protoplasma 195, 37-58.
21. Griffiths, G. M. (1996). Secretory lysosomes: a special mechanism of regulated secretion in haemopoietic cells. Trends Cell Biol. 6, 329-332.
22. Gruenberg, J. and Maxfield, F. R. (1995). Membrane transport in the endocytic pathway. Curr. Opin. Cell Biol. 7, 552-563.
23. Gruenberg, J., Griffiths, G. and Howell, K. E. (1989). Characterisation of the early endosome and putative endocytic carrier vesicles in vivo and with an assay of vesicle fusion in vitro. J. Cell Biol. 108, 1301-1316.
24. Hales, C. N. (1978). Proteolysis and the evolutionary origin of polypeptide hormones. FEBS Lett. 94, 10-16.
25. Holtzman, E. (1989). Lysosomes. Plenum Press, New York.
26. Honing, S., Griffith, J., Geuze, H. J. and Hunziker, W. (1996). The tyrosine-based lysosomal targeting signal in lamp-1 mediates sorting into Golgiderived clathrin-coated vesicles. EMBO J. 15, 5230-5239.
27. Hopkins, C. R., Gibson, A., Shipman, M. and Miller, K. (1990). Movement of internalised receptor-ligand complexes along a continuous endosomal reticulum. Nature 346, 335-339.
28. Hunziker, W. and Geuze, H. J. (1996). Intracellular trafficking of lysosomal membrane proteins. BioEssays 18, 379-389.
29. Jahraus, A., Storrie, B., Griffiths, G. and Desjardins, M. (1994). Evidence for retrograde traffic between terminal lysosomes and the prelysosomal/late endosome compartment. J. Cell Sci. 107, 145-157
30. Kornfeld, S. (1986). Trafficking of lysosomal enzymes in normal and disease states. J. Clin. Invest. 77, 1-6.
31. Kornfeld, S. and Mellman, I. (1989). The biogenesis of lysosomes. Annu. Rev. Cell Biol. 5, 483-525.
32. Lawrence, B. P. and Brown, W. J. (1992). Autophagic vacuoles rapidly fuse with pre-existing lysosomes in cultured hepatoeytes. J. Cell Sci. 102, 515-526.
33. Ludwig, T., Griffiths, G. and Hoflack, B. (1991). Distribution of newly synthesised lysosomal enzymes in the endocytic pathway of normal rat kidney cells. J. Cell Biol. 115, 1561-1572.
34. Luzio, J. P. (1994). Lysosomes. In The Encyclopaedia of Molecular Biology (ed. J. Kendrew), pp. 597-600. Blackwell Science, Oxford.
35. Marsh, M., Bolzau, E. and Helenius, A. (1983). Penetration of Semliki Forest virus from acidic prelysosomal vacuoles. Cell 32, 931-940.
36. Miller, K., Beardmore, J., Kanety, H., Schlessinger, J. and Hopkins, C. R. (1986). Localisation of the epidermal growth factor (EGF) receptor within the endosome of EGF-stimulated epidermoid carcinoma (A431) cells. J. Cell Biol. 102, 500-509.
37. Montgomery, R. R., Webster, P. and Mellman, I. (1991). Accumulation of indigestible substances reduces fusion competence of macrophage lysosomes. J. Immunol. 147, 3087-3095.
38. Mullock, B. M., Branch, W. J., van Schaik, M., Gilbert, L. K. and Luzio, J. P. (1989). Reconstitution of an endosome-lysosome interaction in a cell-tree system. J. Cell Biol. 108, 2093-2099.
39. Mullock, B. M., Perez, J. H., Kuwana, T., Gray, S. R. and Luzio, J. P. (1994). Lysosomes can fuse with a late endosomal compartment in a cell-tree system from rat liver. J. Cell Biol. 126, 1173-1182.
40. Murphy, R. F. (1991). Maturation models for endosome and lysosome biogenesis. Trends Cell Biol. 1, 77-82.
41. Nakajima, Y. and Pfeffer, S. R. (1997). Phosphatidylinositol 3-kinase is not required for recycling of mannose 6-phosphate receptors from late endosomes to the trans-Golgi network. Mol. Biol. Cell 8, 577-582.
42. Parton, R. G., Prydz, K., Bomsel, M., Simons, K. and Griffiths, G. (1989). Meeting of the apical and basolateral endocytic pathways of the Madin Darby canine kidney cells in late endosomes. J. Cell Biol. 109, 3259-3272.
43. Pfeffer, S. R. (1987). The endosomal concentration of a mannose-6-phosphate receptor is unchanged in the absence of ligand synthesis. J. Cell Biol. 105, 229-234.
44. Punnonen, E.-L., Marjomaki, V. S. and Reunanen, H. (1994). 3 Methyladenine inhibits transport from late endosomes to lysosomes in cultured rat and mouse fibroblasts. Eur. J. Cell Biol. 65, 14-25.
45. Reaves, B. J., Bright, N. A., Mullock, B. M. and Luzio, J. P. (1996). The effect of wortmannin on the localisation of lysosomal type I integral membrane glycoproteins suggests a role for phosphoinositide 3-kinase activity in regulating membrane traffic late in the endocytic pathway. J. Cell Sci. 109, 749-762.
46. Reynolds, E. S. (1963). The use of lead citrate at high pH as an electron opaque stain in electron microscopy. J. Cell Biol. 17, 208-212.
47. Rohrer, J., Schweizer, A., Russell, D. and Kornfeld, S. (1996). The targeting of lamp I to lysosomes is dependent on the spacing of its cytoplasmic tail tyrosine sorting motif relative to the membrane. J. Cell Biol. 132, 565-576.
48. Rothman, J. E. (1994). Mechanisms of intracellular protein transport. Nature 372, 55-63.
49. Seaman, M. N. J., Ball, C. L. and Robinson, M. S. (1993). Targeting and mistargeting of plasma membrane adaptors in vitro. J. Cell Biol. 123, 1093-1105.
50. Shepherd, P. R., Reaves, B. J. and Davidson, H. W. (1996). Phosphoinositide 3-kinases and membrane traffic. Trends Cell Biol. 6, 92-97.
51. Slot, J. W. and Geuze, H. J. (1981). Sizing of Protein A-colloidal gold probes for immunoelcetron microscopy. J. Cell Biol. 90, 533-536.
52. Slot, J. W. and Geuze, H. J. (1983). The use of Protein A-colloidal gold (PAG) complexes as immunolabels in ultrathin frozen sections. In Immunohistochemistry (ed. A. C. Cuello), pp. 323-346. John Wiley & Sons, Chichester.
53. Slot, J. W. and Geuze, H. J. (1984). Gold markers for single and double immunolabelling of ultrathin cryosections. In Immunolabelling for electron microscopy (ed. J. M. Polak and I. M. Varndell), pp. 129-142. Elsevier Science, Amsterdam.
54. Slot, J. W. and Geuze, H. J. (1985). A new method of preparing gold probes for multiple-labelling cytochemistry. Eur. J. Cell Biol. 38, 87-93.
55. Stoorvogel, W., Strous, G. J., Geuze, H. J., Oorschot, V. and Schwartz, A. L. (1991). Late endosomes derive from early endosomes by maturation. Cell 65, 417-427
56. Stoorvogel, W., Oorschot, V. and Geuze, H. J. (1996). A novel class of clathrin-coated vesicles budding from endosomes. J. Cell Biol. 132, 21-33.
57. Storrie, B. and Desjardins, M. (1996). The biogenesis of lysosomes: is it a kiss and run, continuous fusion and fission process? BioEssays 18, 895-903.
58. Swanson, J., Yirinec, B., Burke, E., Bushnell, A. and Silverstein, S. C. (1986). Effect of alterations in size of the vacuolar compartment on pinocytosis in J774.2 macrophages. J. Cell physiol. 128, 145-201.
59. Tjelle, T. E., Brech, A., Juvet, L. K., Griffiths, G. and Berg, T. (1996). Isolation and characterization of early endosomes, late endosomes and terminal lysosomes: their role in protein degradation. J. Cell Sci. 109, 2905-2914.
60. Tokuyasu, K. T. (1978). A study of positive staining of ultrathin frozen sections. J. Ultrastruct. Res. 63, 287-307.
61. Traub, L. M., Bannykh, S. I., Rodel, J. E., Aridor, M., Balch, W. E. and Kornfeld, S. (1996). AP-2-containing clathrin coats assemble on mature lysosomes. J. Cell Biol. 135, 1801-1814.
62. Trowbridge, I. S., Collawn, J. F. and Hopkins, C. R. (1994). Signal-dependent membrane trafficking in the endocytic pathway. Annu Rev. Cell Biol. 9, 129-162.
63. van Deurs, B., Holm, P. K., Kayser, L., Sandvig, K.and Hansen, S. H. (1993). Multivesicular bodies in HEp-2 cells are maturing endosomes. Eur.J. Cell Biol. 61, 208-224.
64. van Deurs, B., Holm, P. K., Kayser, L. and Sandvig, K. D. (1995). Delivery to lysosomes in the human carcinoma cell line HEp-2 involves an actin filament-facilitated fusion between mature endosomes and preexisting lysosomes. Eur. J. Cell Biol. 66, 309-323.
65. Whitney, J. A., Gomez, M., Sheff, D., Kreis, T. E. and Mellman, I. (1995). Cytoplasmic coat proteins involved in endosome function. Cell 83, 703-713.