Role for dynamin in late endosome dynamics and trafficking of the cation-independent mannose 6-phosphate receptor

Molecular Biology of the Cell

Volumn 11, Issue 2, 2000, Pages 481-495

  Nicoziani, Paolo ^a,d   Vilhardt, Frederik ^a   Llorente, Alicia ^b   Hilout, Leila ^c   Courtoy, Pierre J ^c   Sandvig, Kirsten ^b   Van Deurs, Bo ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b OSLO UNIVERSITY HOSPITAL   (Norway)

^c DE DUVE INSTITUTE   (Belgium)

^d Consorzio Mario Negri Sud ^*  (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CLATHRIN; DYNAMIN; SOMATOMEDIN B RECEPTOR;

ARTICLE; CELL MEMBRANE TRANSPORT; CONTROLLED STUDY; ELECTRON MICROSCOPY; ENDOCYTOSIS; ENDOSOME; GOLGI COMPLEX; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RECEPTOR BINDING;

EID: 0033995518     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.11.2.481     Document Type: Article

References (68)

1. Altschuler, Y., Barbas, S.M., Terlecky, L.J., Tang, K., Hardy, S., Mostov, K.E., and Schmid, S.L. (1998). Redundant and distinct functions for dynamin-1 and dynamin-2 isoforms. J. Cell Biol. 143, 1871-1881.
2. Boleti, H., Benmerah, A., Ojcius, D.M., Cerf-Bensussan, N., and Dautry-Varsat, A. (1999). Chlamydia infection of epithelial cells expressing dynamin and Eps15 mutants: clathrin-independent entry into cells and dynamin-dependent productive growth. J. Cell Sci. 112, 1487-1496.
3. Bright, N.A., Reaves, B.J., Mullock, B.M., and Luzio, P.J. (1997). Dense core lysosomes can fuse with late endosomes and are reformed from the resultant hybrid organelles. J. Cell Sci. 110, 2027-2040.
4. Bucci, C., Thomsen, P., Nicoziani, P., McCarthy, J., and van Deurs, B. (2000). Rab7: a key to lysosome biogenesis. Mol. Biol. Cell (in press).
5. Cao, H., Garcia, F., and McNiven, M.A. (1998). Differential distribution of dynamin isoforms in mammalian cells. Mol. Biol. Cell 9, 2595-2609.
6. Chao, H.H., Waheed, A., Pohlmann, R., Hille, A., and von Figura, K. (1990). Mannose 6-phosphate receptor dependent secretion of lysosomal enzymes. EMBO J. 9, 3507-3513.
7. Chege, N.W., and Pfeffer, S.R. (1990). Compartmentation of the Golgi complex: brefeldin-A distinguishes trans-Golgi cisternae from trans-Golgi network. J. Cell Biol. 111, 893-899.
8. Cornillie, F., Brosens, I., Belsey, E.M., Marbaix, E., Baudhuin, P., and Courtoy, P.J. (1991). Lysosomal enzymes in the human endometrium: a biochemical study in untreated and levonorgestrel-treated women. Contraception 43, 387-400.
9. Courtoy, P.J. (1993). Analytical subcellular fractionation of endosomal compartments in rat hepatocytes. In: Subcellular Biochemistry, vol. 19, ed. J.J.M. Bergeron and J.R. Harris, New York: Plenum Press, 29-68.
10. Damke, H., Baba, T., van der Bliek, A, and Schmid, S.L. (1995a). Clathrin-independent pinocytosis is induced in cells overexpressing a temperature-sensitive mutant of dynamin. J. Cell Biol. 131, 69-80.
11. Damke, H., Baba, T., Warnock, D.E., and Schmid, S.L. (1994). Induction of mutant dynamin specifically blocks endocytic coated vesicles formation. J. Cell Biol. 127, 915-934.
12. Damke, H., Gossen, M., Freundlieb, S., Bujard, H., and Schmid, S.L. (1995b). Tightly regulated and inducible expression of dominant interfering dynamin mutant in stably transformed HeLa cells. Methods Enzymol. 257, 209-220.
13. Diaz, E., and Pfeffer, S.R. (1998). TIP47: a cargo selection device for mannose 6-phosphate receptor trafficking. Cell 93, 433-443.
14. Diaz, E., Schimmoeller, F., and Pfeffer, S.R. (1997). A novel rab9 effector required for endosome-to-TGN transport. J. Cell Biol. 138, 283-290.
15. Donaldson, J.G., Kahn, R.A., Lippincott-Schwartz, J., and Klausner, R.D. (1991). Binding of ARF and β-COP to Golgi membranes: possible regulation by a trimeric G protein. Science 254, 1197-1199.
16. Draper, R.K., Goda, Y., Brodsky, F.M., and Pfeffer, S.R. (1990). Antibodies to clathrin inhibit endocytosis but not recycling to the trans-Golgi network in vitro. Science 248, 1539-1541.
17. Duncan, J.R., and Kornfeld, S. (1988). Intracellular movement of two mannose 6-phosphate receptors: return to the Golgi apparatus. J. Cell Biol. 106, 617-628.
18. 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.
19. Gieselmann, V., Pohlmann, R., Hasilik, A., and von Figura, K. (1983). Biosynthesis and transport of cathepsin D in cultured human fibroblast. J. Cell Biol. 97, 1-5.
20. Goda, Y., and Pfeffer, S.R. (1988). Selective recycling of the mannose 6-phosphate/IGF-II receptor to the trans-Gołgi network in vitro. Cell 55, 309-320.
21. Goda, Y., and Pfeffer, S.R. (1991). Identification of a novel, N-ethylmaleimide-sensitive cytosolic factor required for vesicular transport from endosomes to the trans-Golgi network. J. Cell Biol. 112, 823-831.
22. 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.
23. Griffiths, G., Patron, R.G., Lucocq, J., van Deurs, B., Brown, D., Slot, J.W., and Geuze, H.J. (1993). The immuno-fluorescent era of membrane traffic trends. Cell Biol. 3, 214-219.
24. Henley, J.R., and McNiven, M.A. (1996). Association of a dynamin-like protein with the Golgi apparatus in mammalian cells. J. Cell Biol. 133, 761-775.
25. Hille-Rehfeld, A. (1995). Mannose 6-phosphate receptor in sorting and transport of lysosomal enzymes. Biochim. Biophys. Acta 1241, 177-194.
26. Hunziker, W., Whitney, J.A., and Mellman, I. (1991). Selective inhibition of transcytosis by brefeldin A in MDCK cells. Cell 67, 617-627.
27. Itin, C., Rancano, C., Nakajima, Y., and Pfeffer, S.R. (1997). A novel assay reveals a role for soluble N-ethylmaleimide-sensitive fusion attachment protein in mannose 6-phosphate receptor transport from endosomes to the trans Golgi network. J. Biol. Chem. 272, 27737-27744.
28. Jones, S.M., Howell, K.E., Henley, J.R., Cao, H., and McNiven, M.A. (1998). Role of dynamin in the formation of transport vesicles from the trans-Golgi network. Science 279, 573-577.
29. Kasai, K., Shin, H., Shinotsuka, C., Murakami, K., and Nakayama, K. (1999). Dynamin II is involved in endocytosis but not in the formation of transport vesicles from the trans-Golgi network. J. Biochem. 125, 780-789.
30. Kelly, R.B. (1999). New twist for dynamin. Nat. Cell Biol. 1, E8-E9.
31. Kirchhausen, T. (1999). Cell biology: boa constrictor or rattle-snake? Nature 398, 470-471.
32. Kobayashi, T., Beuchat, M.H., Lindsay, M., Frias, S., Palmiter, R.D., Sakuraba, H., Parton, R.G., and Gruenberg, J. (1999). Late endosomal membranes rich in lysobisphosphatidic acid regulate cholesterol transport. Nat. Cell Biol. 1, 113-118.
33. Laemmli, U.K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
34. Lippincott-Schwartz, J., Yuan, L., Tipper, C., Amherdt, M., Orci, L., and Klausner, R.D. (1991). Brefeldin A's effects on endosomes, lysosomes, and the TGN suggest a general mechanism for regulating organelle structure and membrane traffic. Cell 67, 601-616.
35. Llorente, A., Rapak, A., Schmid, S.L., van Deurs, B., and Sandvig, K. (1998). Expression of mutant dynamin inhibits toxicity and transport of endocytosed ricin to the Golgi apparatus. J. Cell Biol. 140, 553-563.
36. Lombardi, D., Soldati, T., Riederer, M.A., Goda, Y., Zerial, M., and Pfeffer, S.R. (1993). Rab9 functions in transport between late endosomes and the trans Golgi network. EMBO J. 12, 677-682.
37. Maier, O., Knoblich, M., and Westermann, P. (1996). Dynamin II binds to the trans-Golgi network. Biochem. Biophys. Res. Commun. 223, 229-233.
38. Mallard, F., Antony, C., Tenza, D., Salamero, J., Goud, B., and Johannes, L. (1998). Direct pathway from early/recycling endosomes to the Golgi apparatus revealed through the study of Shiga toxin B-fragment transport. J. Cell Biol. 143, 973-990.
39. Mayor, S., Sabharanjak, S., and Maxfield, F.R. (1998). Cholesterol-dependent retention of GPI-anchored proteins in endosomes. EMBO J. 17, 4626-4638.
40. McNiven, M.A. (1998). Dynamin: a molecular motor with pinchase action. Cell 94, 151-154.
41. Mukherjee, S., and Maxfield, F.R. (1999). Cholesterol: stuck in traffic. Nat. Cell Biol. 1, E37-E38.
42. Mullock, B.M., Bright, N.A., Fearon, C.W., Gray, S.R., and Luzio, J.P. (1998). Fusion of lysosomes with late endosomes produces a hybrid organelle of intermediate density and is NSF dependent. J. Cell Biol. 140, 591-601.
43. Orci, L., Palmer, D.J., Amherdt, M., and Rothman, J.E. (1993). Coated vesicles assembly in the Golgi requires only coatomer and ARF protein from the cytosol. Nature 364, 732-734.
44. Press, B., Feng, Y., Hoflack, B., and Wandinger-Ness, A. (1998). Mutant rab7 causes the accumulation of cathepsin D and cation-independent mannose 6-phosphate receptor in an early endocytic compartment. J. Cell Biol. 140, 1075-1089.
45. Puri, V., Watanabe, R., Dominguez, M., Sun, X., Wheatley, C.L., Marks, D.L., and Pagano, R.E. (1999). Cholesterol modulates membrane traffic along the endocytic pathway in sphingolipid-storage diseases. Nat. Cell Biol. 1, 386-387.
46. Reaves, B.J., Bright, N.A., Mullock, B.M., and Luzio, J.P. (1996). The effect of wortmannin on the localization 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.
47. Riederer, M.A., Soldati, T., Shapiro, A.D., Lin, J., and Pfeffer, S.R. (1994). Lysosome biogenesis requires rab9 function and receptor recycling from endosomes to the trans-Golgi network. J. Cell Biol. 125, 573-582.
48. Rodal, S.K., Skretting, G., Garred, Ø., Vilhardt, F., van Deurs, B., and Sandvig, K. (1999). Extraction of cholesterol with methyl-β-cyclodextrin perturbs formation of clathrin-coated endocytic vesicles. Mol. Biol. Cell 10, 961-974.
49. Rohrer, J., Schweizer, A., Johnson, K.F., and Kornfeld, S. (1995). A determinant in the cytoplasmic tail of the cation-dependent mannose 6-phosphate receptor prevents trafficking to lysosomes. J. Cell Biol. 130, 1297-1306.
50. Rothman, J.E., and Wieland, F.T. (1996). Protein sorting by transport vesicles. Science 272, 227-234.
51. Schmid, S.L., McNiven, M.A., and De Camilli, P. (1998). Dynamin and its partners: a progress report. Curr. Opin. Cell Biol. 10, 504-512.
52. r mannose 6-phosphate receptor to the trans-Golgi network. J. Cell Biol. 122, 541-551.
53. 34 of the cytoplasmic tail of the cation-dependent mannose 6-phosphate receptor is reversibly palmitoylated and required for normal trafficking and lysosomal enzyme sorting. J. Cell Biol. 132, 577-584.
54. Schweizer, A., Kornfeld, S., and Rohrer, J. (1997). Proper sorting of the cation-dependent mannose 6-phosphate receptor in endosomes depends on a pair of aromatic amino acids in its cytoplasmic tail. Proc. Natl. Acad. Sci. USA 94, 14471-14476.
55. Serafini, T., Orci, L., Amherdt, M., Brunner, M., Kahn, R.A., and Rothman, J.E. (1991). ADP-ribosylation factor is a subunit of the coat of Golgi-derived COP-coated vesicles: a novel role for a GTP-binding protein. Cell 67, 239-253.
56. Sever, S., Muhlberg, A.B., and Schmid, S.L. (1999). Impairment of dynamin's GAP domain stimulates receptor-mediated endocytosis. Nature 398, 481-486.
57. Slot, J.W., and Geuze, H.J. (1984). Gold markers for single label and double immunolabeling of ultrathin cryosections. In: Immunogold Labeling for Electron Microscopy, ed. J.M. Polak and J.M. Varndell, Amsterdam: Elsevier, 129-142.
58. 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.
59. Stowell, M.H.B., Marks, B., Wigge, P., and McMahon, H.T. (1999). Nucleotide-dependent conformational changes in dynamin: evidence for a mechanochemical molecular spring. Nat. Cell Biol. 1, 27-32.
60. Sweitzer, S.M., and Hinshaw, J.E. (1998). Dynamin undergoes a GTP-dependent conformational change causing vesiculation. Cell 93, 1021-1029.
61. Takei, K., Haucke, V., Slepnev, V., Farsad, K., Salazar, M., Chen, H., and De Camilli, P. (1998). Generation of coated intermediates of clathrin-mediated endocytosis on protein-free liposomes. Cell 94, 131-141.
62. Takei, K., Slepnev, V.I., Haucke, V., and De Camilli, P. (1999). Functional partnership between amphiphysin and dynamin in clathrin mediated endocytosis. Nat. Cell Biol. 1, 33-39.
63. van der Bliek, A.M. (1999). Functional diversity in the dynamin family. Trends Cell Biol. 9, 96-102.
64. van Deurs, B., Holm, P.K., Kayser, L., and Sandvig, K. (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. 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.
66. +-ATPase with bafilomycin reduces delivery of internalized molecules from mature multivesicular endosomes to lysosomes in HEp-2 cells. Eur. J. Cell Biol. 69, 343-350.
67. Vickery, R.G., and von Zastrow, M. (1999). Distinct dynamin-dependent and -independent mechanisms target structurally homologous dopamine receptors to different endocytic membranes. J. Cell Biol. 144, 31-43.
68. Yoon, Y., Pitts, K.R., Dahan, S., and McNiven, M.A. (1998). A novel dynamin-like protein associates with cytoplasmic vesicles and tubules of the endoplasmic reticulum in mammalian cells. J. Cell Biol. 140, 779-793.