Direct pathway from early/recycling endosomes to the Golgi apparatus revealed through the study of Shiga toxin B-fragment transport

Journal of Cell Biology

Volumn 143, Issue 4, 1998, Pages 973-990

  Mallard, Frédéric ^a   Antony, Claude ^a   Tenza, Danièle ^a   Salamero, Jean ^a   Goud, Bruno ^a   Johannes, Ludger ^a  

^a CNRS   (France)

Author keywords

Clathrin; Endosomes; Golgi; Intracellular transport; Shiga toxin

Indexed keywords

ADAPTOR PROTEIN; ADAPTOR PROTEIN 1; CELL PROTEIN; CLATHRIN; SHIGA TOXIN; UNCLASSIFIED DRUG;

ARTICLE; CELL SELECTION; CELL ULTRASTRUCTURE; CONFOCAL MICROSCOPY; ENDOCYTOSIS; ENDOSOME; GOLGI COMPLEX; HUMAN; HUMAN CELL; HYPOTHESIS; PRIORITY JOURNAL; PROTEIN LOCALIZATION; SHIGELLA DYSENTERIAE; SULFATION;

ADAPTOR PROTEIN COMPLEX GAMMA SUBUNITS; BACTERIAL TOXINS; BIOLOGICAL TRANSPORT; BREFELDIN A; CELL FRACTIONATION; CELL MEMBRANE; CLATHRIN; ENDOSOMES; EXOTOXINS; GOLGI APPARATUS; HELA CELLS; HUMANS; KINETICS; MEMBRANE PROTEINS; MICROSCOPY, IMMUNOELECTRON; OLIGOPEPTIDES; PEPTIDE FRAGMENTS; PROTEIN SORTING SIGNALS; PROTEIN SYNTHESIS INHIBITORS; SHIGA TOXINS; TEMPERATURE;

NEGIBACTERIA; SHIGELLA DYSENTERIAE;

EID: 0032538927     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.143.4.973     Document Type: Article

References (79)

1. Alami, M., M.-P. Taupiac, H. Reggio, A. Bienvenüe, and B. Beaumelle. 1998. Involvement of ATP-dependent Pseudomonas exotoxin translocation from a late recycling compartment in lymphocyte intoxication procedure. Mol. Biol. Cell. 9:387-402.
2. Aniento, F., F. Gu, R.G. Parlon, and J. Gruenberg. 1996. An endosomal beta COP is involved in the pH-dependent formation of transport vesicles destined for late endosomes. J. Cell Biol. 133:29-41.
3. Benaroch, P., M. Yilla, G. Raposo, K. Ito, K. Miwa, H.J. Geuze, and H.L. Ploegh. 1995. How MHC class II molecules reach the endocytic pathway. EMBO (Eur. Mol. Biol. Organ.) J. 14:37-49.
4. Brown, W.J., D.B. DeWald, S.D. Emr, H. Plutner, and W.E. Balch. 1995. Role for phosphatidylinositol 3-kinase in the sorting and transport of newly synthesized lysosomal enzymes in mammalian cells. J. Cell Biol. 130:781-796.
5. Chapman, R.E., and S. Munro. 1994. Retrieval of TGN proteins from the cell surface requires endosomal acidification. EMBO (Eur. Mol. Biol. Organ.) J. 13:2305-2312.
6. Clague, M.J., S. Urbe, F. Aniento, and J. Gruenberg. 1994. Vacuolar ATPase activity is required for endosomal carrier vesicle formation. J. Biol. Chem. 269:21-24.
7. Daro, E., D. Sheff, M. Gomez, T. Kreis, and I. Mellman. 1997. Inhibition of endosome function in CHO cells bearing a temperature-sensitive defect in the coatomer (COPI) component epsilon-COP. J. Cell Biol. 139:1747-1759.
8. De Camilli, P., K. Takei, and P.S. McPherson. 1995. The function of dynamin in endocytosis. Curr. Opin. Neurobiol. 5:559-565.
9. Donaldson, J.G., D. Finazzi, and R.D. Klausner. 1992. Brefeldin A inhibits Golgi membrane-catalysed exchange of guanine nucleotide onto ARF protein. Nature. 360:350-352.
10. Durrbach, A., D. Louvard, and E. Coudrier. 1996. Actin filaments facilitate two steps of endocytosis. J. Cell Sci. 109:457-465.
11. Fishman, J.B., and R.E. Fine. 1987. A trans Golgi-derived exocytic coated vesicle can contain both newly synthesized cholinesterase and internalized transferrin. Cell. 48:157-164.
12. Futter, C.E., A. Gibson, E.H. Allchin, S. Maxwell, L.J. Ruddock, G. Odorizzi, D. Domingo, I.S. Trowbridge, and C.R. Hopkins. 1998. In polarized MDCK cells basolateral vesicles arise from clathrin-gamma-adaptin-coated domains on endosomal tubules. J. Cell Biol. 141:611-623.
13. Geuze, H.J., J.W. Slot, G.J. Strous, H.F. Lodish, and A.L. Schwartz. 1983. Intracellular site of asialoglycoprotein receptor-ligand uncoupling: double-label immunoelectron microscopy during receptor-mediated endocytosis. Cell. 32: 277-287.
14. Geuze, H.J., J.W. Slot, and A.L. Schwartz. 1987. Membranes of sorting organelles display lateral heterogeneity in receptor distribution. J. Cell Biol. 104:1715-1723.
15. Goud, B., C. Jouanne, and J.-C. Antoine. 1984. Reversible pinocytosis of horse-radish peroxidase in lymphoid cells. Exp. Cell Res. 153:218-235.
16. Gruenberg, J., and F.R. Maxfield. 1995. Membrane transport in the endocytic pathway. Curr. Opin. Cell Biol. 7:552-563.
17. Gu, F., F. Aniento, R.G. Parton, and J. Gruenberg. 1997. Functional dissection of COP-I subunits in the biogenesis of multivesicular endosomes. J. Cell Biol. 139:1183-1195.
18. Hansen, S.H., K. Sandvig, and B. van Deurs. 1992. Internalization efficiency of the transferrin receptor. Exp. Cell Res. 199:19-28.
19. Helms, J.B., and J.E. Rothman. 1992. Inhibition by brefeldin A of a Golgi membrane enzyme that catalyses exchange of guanine nucleotide bound to ARF. Nature. 360:352-354.
20. Humphrey, J.S., P.J. Peters, L.C. Yuan, and J.S. Bonifacino. 1993. Localization of TGN38 to the trans-Golgi network: Involvement of a cytoplasmic tyrosine-containing sequence. J. Cell Biol. 120:1123-1135.
21. Hunziker, W., J.A. Whitney, and I. Mellman. 1991. Selective inhibition of transcytosis by brefeldin A in MDCK cells. Cell. 67:617-627.
22. Hunziker, W., J.A. Whitney, and I. Mellman. 1992. Brefeldin A and the endocytic pathway. Possible implications for membrane traffic and sorting. FEBS (Fed. Eur. Biochem. Soc.) Lett. 307:93-96.
23. Iacopetta, B.J., and E.H. Morgan. 1983. The kinetics of transferrin endocytosis and iron uptake from transferrin in rabbit reticulocytes. J. Biol. Chem. 258: 9108-9115.
24. Jin, M., G. Sahagian, and M.D. Snider. 1989. Transport of surface mannose 6-phosphate receptor to the Golgi complex in cultured human cells. J. Biol. Chem. 264:7675-7680.
25. Johannes, L., and B. Goud. 1998. Surfing on a retrograde wave: how does Shiga toxin reach the endoplasmic reticulum? Trends Cell Biol. 8:158-162.
26. Johannes, L., D. Tenza, C. Antony, and B. Goud. 1997. Retrograde transport of KDEL-bearing B-fragment of Shiga toxin. J. Biol. Chem. 272:19554-19561.
27. Kim, J.H., L. Johannes, B. Goud, C. Antony, C.A. Lingwood, R. Daneman, and S. Grinstein. 1998. Nonivasive measurement of the pH of the endoplasmic reticulum at rest and during calcium release. Proc. Natl. Acad. Sci. USA. 95: 2997-3002.
28. Klausner, R.D., J.G. Donaldson, and J. Lippincott-Schwartz. 1992. Brefeldin A: Insights into the control of membrane traffic and organelle structure. J. Cell Biol. 116:1071-1080.
29. Le Borgne, R., and B. Hoflack. 1997. Mannose 6-phosphate receptors regulate the formation of clathrin-coated vesicles in the TGN. J. Cell Biol. 137:335-345.
30. Le Borgne, R., G. Griffiths, and B. Hoflack. 1996. Mannose 6-phosphate receptors and ADP-ribosylation factors cooperate for high affinity interaction of the AP-1 Golgi assembly proteins with membranes. J. Biol. Chem. 271:2162-2170.
31. Lingwood, C.A. 1993. Verotoxins and their glycolipid receptors. Adv. Lipid Res. 25:189-211.
32. Lingwood, C.A. 1996. Role of verotoxin receptors in pathogenesis. Trends Microbiol. 4:147-153.
33. Lippincott-Schwartz, J., J.G. Donaldson, A. Schweizer, E.G. Berger, H.P. Hauri, L.C. Yuan, and R.D. Klausner. 1990. Microtubule-dependent retrograde transport of proteins into the ER in the presence of brefeldin A suggests an ER recycling pathway. Cell. 60:821-836.
34. Lippincott-Schwartz, J., L. Yuan, C. Tipper, M. Amherdt, L. Orci, and R.D. Klausner. 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., A. Rapak, S.L. Schmid, B. van Deurs, and K. Sandvig. 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., T. Soldati, M.A. Riederer, Y. Goda, M. Zerial, and S.R. Pfeffer. 1993. Rab9 functions in transport between late endosomes and the trans Golgi network. EMBO (Eur. Mol. Biol. Organ.) J. 12:677-682.
37. Louvard, D., C. Morris, G. Warren, K. Stanley, F. Winkler, and H. Reggio. 1983. A monoclonal antibody to the heavy chain of clathrin. EMBO (Eur. Mol. Biol. Organ.) J. 2:1655-1664.
38. Matlin, K.S., and K. Simons. 1983. Reduced temperature prevents transfer of a membrane glycoprotein to the cell surface but does not prevent terminal glycosylation. Cell. 34:233-243.
39. Maxfield, F.R., and S. Mayor. 1997. Cell surface dynamics of GPI-anchored proteins. Adv. Exp. Med. Biol. 419:355-364.
40. Mellman, I. 1996. Endocytosis and molecular sorting. Annu. Rev. Cell. Dev. Biol. 12:575-625.
41. Miettinen, H.M., K. Matter, W. Hunziker, J.K. Rose, and I. Mellman. 1992. Fc receptor endocytosis is controlled by a cytoplasmic domain determinant that actively prevents coated pit localization. J. Cell Biol. 116:875-888.
42. Molloy, S.S., L. Thomas, J.K. VanSlyke, P.E. Stenberg, and G. Thomas. 1994. Intracellular trafficking and activation of the furin proprotein convertase: localization to the TGN and recycling from the cell surface. EMBO (Eur. Mol. Biol. Organ.) J. 13:18-33.
43. Mukherjee, S., R.N. Ghosh, and F.R. Maxfield. 1997. Endocytosis. Physiol. Rev. 77:759-803.
44. Munier-Lehmann, H., F. Mauxion, and B. Hoflack. 1996. Function of the two mannose 6-phosphate receptors in lysosomal enzyme transport. Biochem. Soc. Trans. 24:133-136.
45. Nambiar, M.P., and H.C. Wu. 1995. Ilimaquinone inhibits the cytotoxicities of ricin, diphtheria toxin, and other protein toxins in Vero cells. Exp. Cell Res. 219:671-678.
46. O'Brien, A.D., V.L. Tesh, A. Donohue-Rolfe, M.P. Jackson, S. Olsnes, K. Sandvig, A.A. Lindberg, and G.T. Keusch. 1992. Shiga toxin: biochemistry, genetics, mode of action, and role in pathogenesis. Curr. Top. Microbiol. Immunol. 180:65-94.
47. Ohno, H., J. Stewart, M.C. Fournier, H. Bosshart, I. Rhee, S. Miyatake, T. Saito, A. Gallusser, T. Kirchhausen, and J.S. Bonifacino. 1995. Interaction of tyrosine-based sorting signals with clathrin-associated proteins. Science. 269: 1872-1875.
48. Pelham, H.R., L.M. Roberts, and J.M. Lord. 1992. Toxin entry: how reversible is the secretory pathway? Trends Cell Biol. 2:183-185.
49. Ponnambalam, S., C. Rabouille, J.P. Luzio, T. Nilsson, and G. Warren. 1994. The TGN38 glycoprotein contains two non-overlapping signals that mediate localization to the trans-Golgi network. J. Cell Biol. 125:253-268.
50. Reaves, B., and G. Banling. 1994a. Vacuolar ATPase inactivation blocks recycling to the trans-Golgi network from the plasma membrane. FEBS Lett. 345:61-66.
51. Reaves, B., and G. Banting. 1994b. Overexpression of TGN38/41 leads to mislocalisation of gamma-adaptin. FEBS (Fed. Eur. Biochem. Soc.) Lett. 351: 448-456.
52. Reaves, B., M. Horn, and G. Banting. 1993. TGN38/41 recycles between the cell surface and the TGN: brefeldin A affects its rate of return to the TGN. Mol. Biol. Cell. 4:93-105.
53. Riederer, M.A., T. Soldati, A.D. Shapiro, J. Lin, and S.R. Pfeffer. 1994. Lysosome biogenesis requires Rab9 function and receptor recycling from endosomes to the trans-Golgi network. J. Cell Biol. 125:573-582.
54. Robinson, M.S., and T.E. Kreis. 1992. Recruitment of coat proteins onto Golgi membranes in intact and permeabilized cells: effects of brefeldin A and G protein activators. Cell. 69:129-138.
55. Rothman, J.E., and F.T. Wieland. 1996. Protein sorting by transport vesicles. Science. 272:227-234.
56. Salamero, J., R. Le Borgne, C. Saudrais, B. Goud, and B. Hoflack. 1996. Expression of major histocompatibility complex class II molecules in HeLa cells promotes the recruitment of AP-1 Golgi-specific assembly proteins on Golgi membranes. J. Biol. Chem. 271:30318-30321.
57. Sandvig, K., and S. Olsnes. 1979. Effect of temperature on the uptake, excretion and degradation of abrin and ricin by HeLa cells. Exp. Cell Res. 121:15-25.
58. Sandvig, K., and B. van Deurs. 1996. Endocytosis, intracellular transport, and cytotoxic action of Shiga toxin and ricin. Physiol. Rev. 76:949-966.
59. Sandvig, K., S. Olsnes, J.E. Brown, O.W. Petersen, and B. van Deurs. 1989. Endocytosis from coated pits of Shiga toxin: A glycolipid-binding protein from Shigella dysenteriae 1. J Cell Biol. 108:1331-1343.
60. Sandvig, K., O. Garred, K. Prydz, J.V. Kozlov, S.H. Hansen, and B. van Deurs. 1992. Retrograde transport of endocytosed Shiga toxin to the endoplasmic reticulum. Nature. 358:510-512.
61. Sandvig, K., M. Ryd, O. Garred, E. Schweda, P.K. Holm, and B. van Deurs. 1994. Retrograde transport from the Golgi complex to the ER of both Shiga toxin and the nontoxic Shiga B-fragment is regulated by butyric acid and cAMP. J. Cell Biol. 126:53-64.
62. Schagger, H., and G. von Jagow. 1987. Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal. Biochem. 166:368-379.
63. Schapiro, F., C.A. Lingwood, W. Furuya, and S. Grinstein. 1998. pH-independent retrograde targeting of glycolipids to the Golgi complex. Am. J. Physiol. Cell Physiol. 43:319-332.
64. Schekman, R., and L. Orci. 1996. Coat proteins and vesicle budding. Science. 271:1526-1533.
65. Simpson, J.C., C. Dascher, L.M. Roberts, J.M. Lord, and W.E. Balch. 1995. Ricin cytotoxicity is sensitive to recycling between the endoplasmic reticulum and the Golgi complex. J. Biol. Chem. 270:20078-20083.
66. Slot, J.W., H.J. Geuze, S. Gigengack, G.E. Lienhard, and D.E. James. 1991. Immuno-localization of the insulin regulatable glucose transporter in brown adipose tissue of the rat. J. Cell Biol. 113:123-135.
67. Stamnes, M.A., and J.E. Rothman. 1993. The binding of AP-1 clathrin adaptor particles to Golgi membranes requires ADP-ribosylation factor, a small GTP-binding protein. Cell. 73:999-1005.
68. Stoorvogel, W., H.J. Geuze, J.M. Griffith, and G.J. Strous. 1988. The pathways of endocytosed transferrin and secretory protein are connected in the trans-Golgi reticulum. J. Cell Biol. 106:1821-1829.
69. Stoorvogel, W., V. Oorschot, and H.J. Geuze. 1996. A novel class of clathrin-coated vesicles budding from endosomes. J. Cell Biol. 132:21-33.
70. Strous, G.J., P. van Kerkhof, G. van Meer, S. Rijnboutt, and W. Stoorvogel. 1993. Differential effects of brefeldin A on transport of secretory and lysosomal proteins. J. Biol. Chem. 268:2341-2347.
71. Takei, K., P.S. McPherson, S.L. Schmid, and P. De Camilli. 1995. Tubular membrane invaginations coated by dynamin rings are induced by GTP-gamma S in nerve terminals. Nature. 374:186-190.
72. Traub, L.M., J.A. Ostrom, and S. Kornfeld. 1993. Biochemical dissection of AP-1 recruitment onto Golgi membranes. J. Cell Biol. 123:561-573.
73. van der Ende, A., A. du Maine, A.L. Schwartz, and G.J. Strous. 1989. Effect of ATP depletion and temperature on the transferrin-mediated uptake and release of iron by BeWo choriocarcinoma cells. Biochem. J. 259:685-692.
74. van Deurs, B., O.W. Petersen, S. Olsnes, and K. Sandvig. 1987. Delivery of internalized ricin from endosomes to cisternal Golgi elements is a discontinuous, temperature-sensitive process. Exp. Cell Res. 171:137-152.
75. van Weert, A.W., K.W. Dunn, H.J. Gueze, F.R. Maxfield, and W. Stoorvogel. 1995. Transport from late endosomes to lysosomes, but not sorting of integral membrane proteins in endosomes, depends on the vacuolar proton pump. J. Cell Biol. 130:821-834.
76. von Figura, K. 1991. Molecular recognition and targeting of lysosomal proteins. Curr. Opin. Cell Biol. 3:642-646.
77. Warnock, D.E., and S.L. Schmid. 1996. Dynamin GTPase, a force-generating molecular switch. Bioessays. 18:885-893.
78. Whitney, J.A., M. Gomez, D. Sheff, T.E. Kreis, and I. Mellman. 1995. Cytoplasmic coat proteins involved in endosome function. Cell. 83:703-713.
79. Wood, S.A., J.E. Park, and W.J. Brown. 1991. Brefeldin A causes a microtubule-mediated fusion of the trans-Golgi network and early endosomes. Cell. 67:591-600.