Mechanism of Constitutive Export from the Golgi: Bulk Flow via the Formation, Protrusion, and En Bloc Cleavage of large trans-Golgi Network Tubular Domains

Molecular Biology of the Cell

Volumn 14, Issue 11, 2003, Pages 4470-4485

  Polishchuk, Elena V ^a   Di Pentima, Alessio ^a   Luini, Alberto ^a   Polishchuk, Roman S ^a  

^a Ist Ric Farmacologiche Mario Negri ^*  (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CARRIER PROTEIN; COAT PROTEIN; KINESIN;

ANIMAL CELL; ARTICLE; CELL MEMBRANE; CELL VACUOLE; CONTROLLED STUDY; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; MEMBRANE FUSION; MICROTUBULE; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; PROTEIN TRANSPORT; REGULATORY MECHANISM; TRANS GOLGI NETWORK;

ANIMALS; BIOLOGICAL TRANSPORT; CELL MEMBRANE; CELLS, CULTURED; CERCOPITHECUS AETHIOPS; CLATHRIN; COS CELLS; CRICETINAE; ENDOPLASMIC RETICULUM; GOLGI APPARATUS; HELA CELLS; HUMANS; MEMBRANE FUSION; MEMBRANE GLYCOPROTEINS; MICROINJECTIONS; MICROSCOPY, CONFOCAL; MICROSCOPY, IMMUNOELECTRON; MICROTUBULES; MODELS, MOLECULAR; TRANS-GOLGI NETWORK; VIRAL ENVELOPE PROTEINS;

ANIMALIA;

EID: 0345687308     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E03-01-0033     Document Type: Article

References (46)

1. Acharya, U., Jacobs, R., Peters, J.M., Watson, N., Farquhar, M.G., and Malhotra, V. (1995). The formation of Golgi stacks from vesiculated Golgi membranes requires two distinct fusion events. Cell 82, 895-904.
2. Band, A.M., Maatta, J., Kaariainen, L., and Kuismanen, E. (2001). Inhibition of the membrane fusion machinery prevents exit from the TGN and proteolytic processing by furin. FEBS Lett. 505, 118-124.
3. Bannykh, S.I., and Balch, W.E. (1997). Membrane dynamics at the endoplasmic reticulum-Golgi interface. J. Cell Biol. 138, 1-4.
4. Banting, G., and Ponnambalam, S. (1997). TGN38 and its orthologues: roles in post-TGN vesicle formation and maintenance of TGN morphology. Biochim. Biophys. Acta 1355, 209-217.
5. Brown, W.J., Chambers, K., and Doody, A. (2003). Phospholipase A2 (PLA2) enzymes in membrane trafficking: mediators of membrane shape and function. Traffic 4, 214-221.
6. Burger, K.N. (2000). Greasing membrane fusion and fission machineries. Traffic 1, 605-613.
7. Cao, H., Thompson, H.M., Krueger, E.W., and McNiven, M.A. (2000). Disruption of Golgi structure and function in mammalian cells expressing a mutant dynamin. J. Cell Sci. 113, 1993-2002.
8. Clermont, Y., Rambourg, A., and Hermo, L. (1995). Trans-Golgi network (TGN) of different cell types: three-dimensional structural characteristics and variability. Anat. Rec. 242, 289-301.
9. Corda, D., Hidalgo Carcedo, C., Bonazzi, M., Luini, A., and Spanò, S. (2002). Molecular aspects of membrane fission in the secretory pathway. Cell. Mol. Life Sci. 59, 1819-1832.
10. Dell'Angelica, E.C., Shotelersuk, V., Aguilar, R.C., Gahl, W.A., and Bonifacino, J.S. (1999). Altered trafficking of lysosomal proteins in Hermansky-Pudlak syndrome due to mutations in the beta 3A subunit of the AP-3 adaptor. Mol. Cell 3, 11-21.
11. Dittie, A.S., Klumperman, J., and Tooze, S.A. (1999). Differential distribution of mannose-6-phosphate receptors and furin in immature secretory granules. J. Cell Sci. 112, 3955-3966.
12. Doray, B., Ghosh, P., Griffith, J., Geuze, H.J., and Kornfeld, S. (2002). Cooperation of GGAs and AP-1 in packaging MPRs at the trans-Golgi network. Science 297, 1700-1703.
13. Farsad, K., Ringstad, N., Takei, K., Floyd, S.R., Rose, K., and De Camilli, P. (2001). Generation of high curvature membranes mediated by direct endophilin bilayer interactions. J. Cell Biol. 155, 193-200.
14. Fisher, L.W., Stubbs, J.T. 3rd, and Young, M.F. (1995). Antisera and cDNA probes to human and certain animal model bone matrix noncollagenous proteins. Acta Orthop. Scand. Suppl. 266, 61-65.
15. Folsch, H., Pypaert, M., Schu, P., and Mellman, I. (2001). Distribution and function of AP-1 clathrin adaptor complexes in polarized epithelial cells. J. Cell Biol. 152, 595-606.
16. Fukunaga, T., Furuno, A., Hatsuzawa, K., Tani, K., Yamamoto, A., and Tagaya, M. (1998). NSF is required for the brefeldin A-promoted disassembly of the Golgi apparatus. FEBS Lett. 435, 237-240.
17. Griffiths, G., and Hoppeler, H. (1986). Quantitation in immunocytochemistry: correlation of immunogold labeling to absolute number of membrane antigens. J. Histochem. Cytochem. 34, 1389-1398.
18. Griffiths, G., Pfeiffer, S., Simons, K., and Matlin, K. (1985). Exit of newly synthesized membrane proteins from the trans cisterna of the Golgi complex to the plasma membrane. J. Cell Biol. 101, 949-964.
19. Griffiths, G., and Simons, K. (1986). The trans Golgi network: sorting at the exit site of the Golgi complex. Science 234, 438-443.
20. Hirschberg, K., Miller, C.M., Ellenberg, J., Presley, J.F., Siggia, E.D., Phair, R.D., and Lippincott-Schwartz, J. (1998). Kinetic analysis of secretory protein traffic and characterization of Golgi to plasma membrane transport intermediates in living cells. J. Cell Biol. 143, 1485-1503.
21. Hirst, J., Lui, W.W., Bright, N.A., Totty, N., Seaman, M.N., and Robinson, M.S. (2000). A family of proteins with gamma-adaptin and VHS domains that facilitate trafficking between the trans-Golgi network and the vacuole/lysosome. J. Cell Biol. 149, 67-80.
22. Honing, S., Griffith, J., Geuze, H.J., and Hunziker, W. (1996). The tyrosine-based lysosomal targeting signal in lamp-1 mediates sorting into Golgi-derived clathrin-coated vesicles. EMBO J. 15, 5230-5239.
23. Keller, P., and Simons, K. (1997). Post-Golgi biosynthetic trafficking. J. Cell Sci. 110, 3001-3009.
24. Keller, P., Toomre, D., Diaz, E., White, J., and Simons, K. (2001). Multicolour imaging of post-Golgi sorting and trafficking in live cells. Nat. Cell Biol. 3, 140-149.
25. Klumperman, J., Hille, A., Veenendaal, T., Oorschot, V., Stoorvogel, W., von Figura, K., and Geuze, H.J. (1993). Differences in the endosomal distributions of the two mannose 6-phosphate receptors. J. Cell Biol. 121, 997-1010.
26. Kreitzer, G., Marmorstein, A., Okamoto, P., Vallee, R., and Rodriguez-Boulan, E. (2000). Kinesin and dynamin are required for post-Golgi transport of a plasma-membrane protein. Nat. Cell Biol. 2, 125-127.
27. Ladinsky, M.S., Wu, C.C., McIntosh, S., McIntosh, J.R., and Howell, K.E. (2002). Structure of the Golgi and distribution of reporter molecules at 20 degrees C reveals the complexity of the exit compartments. Mol. Biol. Cell 13, 2810-2825.
28. Liljedahl, M., Maeda, Y., Colanzi, A., Ayala, I., Van Lint, J., and Malhotra, V. (2001). Protein kinase D regulates the fission of cell surface destined transport carriers from the trans-Golgi network. Cell 10, 409-420.
29. Lippincott-Schwartz, J., Roberts, T.H., and Hirschberg, K. (2000). Secretory protein trafficking and organelle dynamics in living cells. Annu. Rev. Cell Dev. Biol. 16, 557-589.
30. Mironov, A.A., et al. (2001). Small cargo proteins and large aggregates can traverse the Golgi by a common mechanism without leaving the lumen of cisternae. J. Cell Biol. 155, 1225-1238.
31. Mironov, A.A., Polishchuk, R.S., and Luini, A. (2000). Visualizing membrane traffic in vivo by combined video fluorescence and 3-D electron microscopy. Trends Cell Biol. 10, 349-353.
32. Mostov, K.E., Verges, M., and Altschuler, Y. (2000). Membrane traffic in polarized epithelial cells. Curr. Opin. Cell Biol. 12, 483-490.
33. Nichols, B.J., Kenworthy, A.K., Polishchuk, R.S., Lodge, R., Roberts, T.H., Hirschberg, K., Phair, R.D., and Lippincott-Schwartz, J. (2001). Rapid cycling of lipid raft markers between the cell surface and Golgi complex. J. Cell Biol. 153, 529-541.
34. Nishimura, N., Plutner, H., Hahn, K., and Balch, W.E. (2002). The delta subunit of AP-3 is required for efficient transport of VSV-G from the trans-Golgi network to the cell surface. Proc. Natl. Acad. Sci. USA 99, 6755-6760.
35. Ohno, H., Tomemori, T., Nakatsu, F., Okazaki, Y., Aguilar, R.C., Foelsch, H., Mellman, I., Saito, T., Shirasawa, T., and Bonifacino, J.S. (1999). MulB, a novel adaptor medium chain expressed in polarized epithelial cells. FEBS Lett. 449, 215-220.
36. Polishchuk, R.S., and Mironov, A.A. (2001). Correlative video/light electron microscopy. In: Current Protocols in Cell Biology, ed. J.S. Bonifacino, M. Dasso, J.B. Harford, J. Lippincott-Schwartz, and K.M. Yamada, John Wiley & Sons, New York, 4.8.1-4.8.9.
37. Polishchuk, R.S., Polishchuk, E.V., Marra, P., Buccione, R., Alberti, S., Luini, A., and Mironov, A.A. (2000). GFP-based correlative light-electron microscopy reveals the saccular-tubular ultrastructure of carriers in transit from the Golgi apparatus to the plasma membrane. J. Cell Biol. 148, 45-58.
38. Rabouille, C., Kondo, H., Newman, R., Hui, N., Freemont, P., and Warren, G. (1998). Syntaxin 5 is a common component of the NSF- and p97-mediated reassembly pathways of Golgi cistemae from mitotic Golgi fragments in vitro. Cell 92, 603-610.
39. Rambourg, A., and Clermont, Y. (1990). Three-dimensional electron microscopy: structure of the Golgi apparatus. Eur. J. Cell Biol. 51, 189-200.
40. Rehling, P., Darsow, T., Katzmann, D.J., and Emr, S.D. (1999). Formation of AP-3 transport intermediates requires Vps41 function. Nat. Cell Biol. 1, 346-353.
41. Rothman, J.E., and Wieland, F.T. (1996). Protein sorting by transport vesicles. Science 272, 227-234.
42. Roux, A., Cappello, G., Cartaud, J., Prost, J., Goud, B., and Bassereau, P. (2002). A minimal system allowing tubulation with molecular motors pulling on giant liposomes. Proc. Natl. Acad. Sci. USA 99, 5394-5399.
43. Sariola, M., Saraste, J., and Kuismanen, E. (1995). Communication of post-Golgi elements with early endocytic pathway: regulation of endoproteolytic cleavage of Semliki Forest virus p62 precursor. J. Cell Sci. 108, 2465-2475.
44. Sprong, H., van der Sluijs, P., and van Meer, G. (2001). How proteins move lipids and lipids move proteins. Nat. Rev. Mol. Cell. Biol. 2, 504-513.
45. Toomre, D., Keller, P., White, J., Olivo, J.C., and Simons, K. (1999). Dual-color visualization of trans-Golgi network to plasma membrane traffic along microtubules in living cells. J. Cell Sci. 112, 21-33.
46. White, J., Keller, P., and Stelzer, E.H. (2001). Spatial partitioning of secretory cargo from Golgi resident proteins in live cells. BMC Cell Biol. 2, 19.