Secretory traffic triggers the formation of tubular continuities across Golgi sub-compartments

Nature Cell Biology

Volumn 6, Issue 11, 2004, Pages 1071-1081

  Trucco, Alvar ^a   Polischuck, Roman S ^a   Martella, Oliviano ^a   Di Pentima, Alessio ^a   Fusella, Aurora ^a   Di Giandomenico, Daniele ^a   San Pietro, Enrica ^a   Beznoussenko, Galina V ^a   Polischuk, Elena V ^a   Baldassarre, Massimiliano ^a   Buccione, Roberto ^a   Geerts, Willie J C ^b   Koster, Abraham J ^b   Burger, Koert N J ^b   Mironov, Alexander A ^a   Luini, Alberto ^a  

^a Consorzio Mario Negri Sud ^*  (Italy)

^b UTRECHT UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ARTICLE; CELL COMPARTMENTALIZATION; CELL STRUCTURE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; GOLGI COMPLEX; INTRACELLULAR TRANSPORT; MEMBRANE TRANSPORT; NONHUMAN; PRIORITY JOURNAL; RAT; SECRETORY CELL; SIGNAL TRANSDUCTION; TOMOGRAPHY;

BIOLOGICAL TRANSPORT; CELL COMPARTMENTATION; CELL LINE; ENDOPLASMIC RETICULUM; GOLGI APPARATUS; MICROSCOPY, ELECTRON;

ANIMALIA;

EID: 7944220328     PISSN: 14657392     EISSN: None     Source Type: Journal    
DOI: 10.1038/ncb1180     Document Type: Article

References (49)

1. Bannykh, S. I. & Balch, W. E. Membrane dynamics at the endoplasmic reticulum-Golgi interface. J. Cell Biol. 138, 1-4 (1997).
2. Mironov, A. A., Weidman, P. & Luini, A. Variations on the intracellular transport theme: maturing cisternae and trafficking tubules. J. Cell Biol. 138, 481-484 (1997).
3. Bonfanti, L. et al. Procollagen traverses the Golgi stack without leaving the lumen of cisternae: evidence for cisternal maturation. Cell 95, 993-1003 (1998).
4. Glick, B. S. & Malhotra, V. The curious status of the Golgi apparatus. Cell 95, 883-889 (1998).
5. Pelham, H. R. Traffic through the Golgi apparatus. J. Cell Biol. 155, 1099-1101 (2001).
6. Weiss, M. & Nilsson, T. Protein sorting in the Golgi apparatus: a consequence of maturation and triggered sorting. FEBS Lett. 486, 2-9 (2000).
7. Martinez-Menarguez, J. A. et al. Peri-Golgi vesicles contain retrograde but not anterograde proteins consistent with the cisternal progression model of intra-Golgi transport. J. Cell Biol. 155, 1213-1224 (2001).
8. Lanoix, J. et al. GTP hydrolysis by arf-1 mediates sorting and concentration of Golgi resident enzymes into functional COP I vesicles. EMBO J. 18, 4935-4948 (1999).
9. Cosson, P., Amherdt, M., Rothman, J. E. & Orci, L. A resident Golgi protein is excluded from peri-Golgi vesicles in NRK cells. Proc. Natl Acad. Sci. USA 99, 12831-12834 (2002).
10. Kweon, H. S. et al. Golgi enzymes are enriched in perforated zones of Golgi cisternae but excluded from peri-Golgi vesicles. Mol. Biol. Cell (in the press).
11. Pelham, H. R. EJCB-Lecture. SNAREs and the organization of the secretory pathway. Eur. J. Cell Biol. 74, 311-314 (1997).
12. Klumperman, J. Transport between ER and Golgi. Curr. Opin. Cell Biol. 12, 445-449 (2000).
13. Hauri, H. P., Kappeler, F., Andersson, H. & Appenzeller, C. ERGIC-53 and traffic in the secretory pathway. J. Cell Sci. 113, 587-596 (2000).
14. Ladinsky, M. S., Mastronarde, D. N., McIntosh, J. R., Howell, K. E. & Staehelin, L. A. Golgi structure in three dimensions: functional insights from the normal rat kidney cell. J. Cell Biol. 144, 1135-1149 (1999).
15. Polishchuk, R. S. et al. Correlative light-electron microscopy reveals the tubular-saccular ultrastructure of carriers operating between Golgi apparatus and plasma membrane. J. Cell Biol. 148, 45-58 (2000).
16. Mironov, A. A. et al. 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 (2001 ).
17. Rambourg, A. & Clermont, Y. Three-dimensional electron microscopy: structure of the Golgi apparatus. Eur. J. Cell Biol. 51, 189-200 (1990).
18. Cole, N. B., Sciaky, N., Marotta, A., Song, J. & Lippincott-Schwartz, J. Golgi dispersal during microtubule disruption: regeneration of Golgi stacks at peripheral endoplasmic reticulum exit sites. Mol. Biol. Cell 7, 631-650 (1996).
19. Neumann, U., Brandizzi, F. & Hawes, C. Protein transport in plant cells: in and out of the Golgi. Ann. Bot. (Lond.) 92, 167-180 (2003).
20. Rabouille, C. et al. The Drosophila GMII gene encodes a Golgi alpha-mannosidase II. J. Cell Sci. 112, 3319-3330 (1999).
21. Thyberg, J. & Moskalewski, S. Role of microtubules in the organization of the Golgi complex. Exp. Cell Res. 246, 263-279 (1999).
22. Kuismanen, E. & Saraste, J. Low temperature-induced transport blocks as tools to manipulate membrane traffic. Methods Cell Biol. 32, 257-274 (1989).
23. Marsh, B. J., Mastronarde, D. N., Buttle, K. F., Howell, K. E. & McIntosh, J. R. Organellar relationships in the Golgi region of the pancreatic beta cell line, HIT-T15, visualized by high resolution electron tomography. Proc. Natl Acad. Sci. USA 98, 2399-2406 (2001).
24. Bergmann, J. E. Using temperature-sensitive mutants of VSV to study membrane protein biogenesis. Methods Cell Biol. 32, 85-110 (1989).
25. Aridor, M., Bannykh, S. I., Rowe, T. & Balch, W. E. Cargo can modulate COPII vesicle formation from the endoplasmic reticulum. J. Biol. Chem. 274, 4389-4399 (1999).
26. Aridor, M. et al. The Sar1 GTPase coordinates biosynthetic cargo selection with endoplasmic reticulum export site assembly. J. Cell Biol. 152, 213-229 (2001).
27. Keller, P., Toomre, D., Diaz, E., White, J. & Simons, K. Multicolour imaging of post-Golgi sorting and trafficking in live cells. Nat. Cell Biol. 3, 140-149 (2001).
28. Pelham, H. R. Recycling of proteins between the endoplasmic reticulum and Golgi complex. Curr. Opin. Cell Biol. 3, 585-591 (1991).
29. Orci, L., Schekman, R. & Perrelet, A. Interleaflet clear space is reduced in the membrane of COP I and COP II-coated buds/vesicles. Proc. Natl Acad. Sci. USA 93, 8968-8970 (1996).
30. Polishchuk, E. V., Di Pentima, A., Luini, A. & Polishchuk, R. S. Mechanism of constitutive export from the golgi: bulk flow via the formation, protrusion, and en bloc cleavage of large trans-golgi network tubular domains. Mol. Biol. Cell 14, 4470-4485 (2003).
31. Pelham, H. R. & Rothman, J. E. The debate about transport in the Golgi - two sides of the same coin? Cell 102, 713-719 (2000).
32. Volchuk, A. et al. Countercurrent distribution of two distinct SNARE complexes mediating transport within the Golgi stack. Mol. Biol. Cell 15, 1506-1518 (2004).
33. Pelham, H. Getting stuck in the Golgi. Traffic 1, 191-192 (2000).
34. Bretscher, M. S. & Munro, S. Cholesterol and the Golgi apparatus. Science 261, 1280-1281 (1993).
35. Munro, S. An investigation of the role of transmembrame domains in Golgi protein retention. EMBO J. 14, 4695-4704 (1995).
36. Cluett, E. B., Kuismanen, E. & Machamer, C. E. Heterogeneous distribution of the unusual phospholipid semilysobisphosphatidic acid through the Golgi complex. Mol. Biol. Cell 8, 2233-2240 (1997).
37. Holthuis, J. C., Pomorski, T., Raggers, R. J., Sprong, H. & Van Meer, G. The organizing potential of sphingolipids in intracellular membrane transport. Physiol. Rev. 81, 1689-1723 (2001).
38. Maxfield, F. R. & Wustner, D. Intracellular cholesterol transport. J. Clin. Invest. 110, 891-898 (2002).
39. Mitra, K., Ubarretxena-Belandia, I., Taguchi, T., Warren, G. & Engelman, D. M. Modulation of the bilayer thickness of exocytic pathway membranes by membrane proteins rather than cholesterol. Proc. Natl Acad. Sci. USA 101, 4083-4088 (2004).
40. Marra, P. et al. The GM130 and GRASP65 Golgi proteins cycle through and define a subdomain of the intermediate compartment. Nat. Cell Biol. 3, 1101-1113 (2001).
41. Seemann, J., Jokitalo, E., Pypaert, M. & Warren, G. Matrix proteins can generate the higher order architecture of the Golgi apparatus. Nature 407, 1022-1026 (2000).
42. Mironov, A. Jr, Luini, A. & Mironov, A. A synthetic model of intra-Golgi traffic. Faseb J. 12, 249-252 (1998).
43. Hirschberg, K., Phair, R. D. & Lippincott-Schwartz, J. Kinetic analysis of intracellular trafficking in single living cells with vesicular stomatitis virus protein G-green fluorescent protein hybrids. Methods Enzymol. 327, 69-89 (2000).
44. Weidman, P. J. Anterograde transport through the Golgi complex: do Golgi tubules hold the key? Trends Cell Biol. 5, 302-305 (1995).
45. Beznoussenko, G. V. & Mironov, A. A. Models of intracellular transport and evolution of the Golgi complex. Anat. Rec. 268, 226-238 (2002).
46. Horton, A. C. & Ehlers, M. D. Dual modes of endoplasmic reticulum-to-Golgi transport in dendrites revealed by live-cell imaging. J. Neurosci. 23, 6188-6199 (2003).
47. Marsh, B. J., Volkmann, N., McIntosh, J. R. & Howell, K. E. Direct continuities between cisternae at different levels of the Golgi complex in glucose-stimulated mouse islet beta cells. Proc. Natl Acad. Sci. USA 101, 5565-5570 (2004).
48. Nicolas, M. T., Bassot, J. M. & Nicolas, G. Immunogold labeling of luciferase in the luminous bacterium Vibrio harveyi after fast-freeze fixation and different freeze-substitution and embedding procedures. J. Histochem. Cytochem. 37, 663-674 (1989).
49. Koster, A. J. et al. Perspectives of molecular and cellular electron tomography. J. Struct. Biol. 120, 276-308 (1997).