Mechanism of Constitutive Export from the Golgi: Bulk Flow Via the Formation, Protrusion, and En Bloc Cleavage of Large Trans-golgi Network Tubular Domains

Overview

Journal Mol Biol Cell

Specialties Cell Biology
Molecular Biology

Date 2003 Aug 26

PMID 12937271

Citations 72

Authors

Elena V Polishchuk

Alessio Di Pentima

Alberto Luini

Roman S Polishchuk

Affiliations

Soon will be listed here.

Abstract

Transport of constitutive cargo proteins from the Golgi complex to the plasma membrane (PM) is known to be mediated by large tubular-saccular carriers moving along microtubules. However, the process by which these large structures emerge from the trans-Golgi network (TGN) remains unclear. Here, we address the question of the formation of Golgi-to-PM carriers (GPCs) by using a suitable cluster of morphological techniques, providing an integrated view of their dynamics and three-dimensional structure. Our results indicate that exit from the TGN of a constitutive traffic marker, the VSVG protein, occurs by bulk flow and is a three-step process. First, the formation of a tubular-reticular TGN domain (GPC precursor) that includes PM-directed proteins and excludes other cargo and Golgi-resident proteins. Notably, this step does not require membrane fusion. Second, the docking of this preformed domain on microtubules and its kinesin-mediated extrusion. Finally, the detachment of the extruded domain by membrane fission. The formation of GPCs does not involve cargo concentration and is not associated with the presence of known coat proteins on GPC precursors. In summary, export from the Golgi occurs via the formation, protrusion and en bloc cleavage of specialized TGN tubular-saccular domains.

Citing Articles

ER exit in physiology and disease.

Robinson C, Duggan A, Forrester A Front Mol Biosci. 2024; 11:1352970.

PMID: 38314136 PMC: 10835805. DOI: 10.3389/fmolb.2024.1352970.

The exocyst complex is an essential component of the mammalian constitutive secretory pathway.

Pereira C, Stalder D, Anderson G, Shun-Shion A, Houghton J, Antrobus R J Cell Biol. 2023; 222(5).

PMID: 36920342 PMC: 10041652. DOI: 10.1083/jcb.202205137.

Golgin Subfamily A Member 5 Is Essential for Production of Extracellular Matrix Proteins during TGF-1-Induced Periodontal Ligament-Fibroblastic Differentiation.

Kim H, Kim S, Choi M, Jang Y Stem Cells Int. 2022; 2022:3273779.

PMID: 35879965 PMC: 9308542. DOI: 10.1155/2022/3273779.

Microtubules in Pancreatic β Cells: Convoluted Roadways Toward Precision.

Bracey K, Gu G, Kaverina I Front Cell Dev Biol. 2022; 10:915206.

PMID: 35874834 PMC: 9305484. DOI: 10.3389/fcell.2022.915206.

The Golgi complex: An organelle that determines urothelial cell biology in health and disease.

Kreft M, Mironov A, Hudoklin S Histochem Cell Biol. 2022; 158(3):229-240.

PMID: 35773494 PMC: 9399047. DOI: 10.1007/s00418-022-02121-0.

References

Rabouille C, Kondo H, Newman R, Hui N, Freemont P, Warren G . Syntaxin 5 is a common component of the NSF- and p97-mediated reassembly pathways of Golgi cisternae from mitotic Golgi fragments in vitro. Cell. 1998; 92(5):603-10. DOI: 10.1016/s0092-8674(00)81128-9. View

Keller P, Simons K . Post-Golgi biosynthetic trafficking. J Cell Sci. 1998; 110 ( Pt 24):3001-9. DOI: 10.1242/jcs.110.24.3001. View

Rehling P, Darsow T, Katzmann D, Emr S . Formation of AP-3 transport intermediates requires Vps41 function. Nat Cell Biol. 1999; 1(6):346-53. DOI: 10.1038/14037. View

Polishchuk R, Polishchuk E, Marra P, Alberti S, Buccione R, Luini A . Correlative light-electron microscopy reveals the tubular-saccular ultrastructure of carriers operating between Golgi apparatus and plasma membrane. J Cell Biol. 2000; 148(1):45-58. PMC: 2156208. DOI: 10.1083/jcb.148.1.45. View

Kreitzer G, Marmorstein A, Okamoto P, Vallee R, Rodriguez-Boulan E . Kinesin and dynamin are required for post-Golgi transport of a plasma-membrane protein. Nat Cell Biol. 2000; 2(2):125-7. DOI: 10.1038/35000081. View

Hirst J, Lui W, Bright N, Totty N, Seaman M, Robinson M . 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. 2000; 149(1):67-80. PMC: 2175106. DOI: 10.1083/jcb.149.1.67. View

Cao H, Thompson H, Krueger E, McNiven M . Disruption of Golgi structure and function in mammalian cells expressing a mutant dynamin. J Cell Sci. 2000; 113 ( Pt 11):1993-2002. DOI: 10.1242/jcs.113.11.1993. View

Mostov K, Verges M, Altschuler Y . Membrane traffic in polarized epithelial cells. Curr Opin Cell Biol. 2000; 12(4):483-90. DOI: 10.1016/s0955-0674(00)00120-4. View

Mironov A, Polishchuk R, Luini A . Visualizing membrane traffic in vivo by combined video fluorescence and 3D electron microscopy. Trends Cell Biol. 2000; 10(8):349-53. DOI: 10.1016/s0962-8924(00)01787-6. View

10.

Lippincott-Schwartz J, Roberts T, Hirschberg K . Secretory protein trafficking and organelle dynamics in living cells. Annu Rev Cell Dev Biol. 2000; 16:557-89. PMC: 4781643. DOI: 10.1146/annurev.cellbio.16.1.557. View

11.

Folsch H, Pypaert M, Schu P, Mellman I . Distribution and function of AP-1 clathrin adaptor complexes in polarized epithelial cells. J Cell Biol. 2001; 152(3):595-606. PMC: 2195989. DOI: 10.1083/jcb.152.3.595. View

12.

Nichols B, Kenworthy A, Polishchuk R, Lodge R, Roberts T, Hirschberg K . Rapid cycling of lipid raft markers between the cell surface and Golgi complex. J Cell Biol. 2001; 153(3):529-41. PMC: 2190578. DOI: 10.1083/jcb.153.3.529. View

13.

Sprong H, van der Sluijs P, van Meer G . How proteins move lipids and lipids move proteins. Nat Rev Mol Cell Biol. 2001; 2(7):504-13. DOI: 10.1038/35080071. View

14.

BAND A, Maatta J, Kaariainen L, Kuismanen E . Inhibition of the membrane fusion machinery prevents exit from the TGN and proteolytic processing by furin. FEBS Lett. 2001; 505(1):118-24. DOI: 10.1016/s0014-5793(01)02798-3. View

15.

Farsad K, Ringstad N, Takei K, Floyd S, Rose K, De Camilli P . Generation of high curvature membranes mediated by direct endophilin bilayer interactions. J Cell Biol. 2001; 155(2):193-200. PMC: 2198845. DOI: 10.1083/jcb.200107075. View

16.

Mironov A, Beznoussenko G, Nicoziani P, Martella O, Trucco A, Kweon H . Small cargo proteins and large aggregates can traverse the Golgi by a common mechanism without leaving the lumen of cisternae. J Cell Biol. 2002; 155(7):1225-38. PMC: 2199327. DOI: 10.1083/jcb.200108073. View

17.

Roux A, Cappello G, Cartaud J, Prost J, Goud B, Bassereau P . A minimal system allowing tubulation with molecular motors pulling on giant liposomes. Proc Natl Acad Sci U S A. 2002; 99(8):5394-9. PMC: 122780. DOI: 10.1073/pnas.082107299. View

18.

Nishimura N, Plutner H, Hahn K, Balch W . 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 U S A. 2002; 99(10):6755-60. PMC: 124475. DOI: 10.1073/pnas.092150699. View

19.

Ladinsky M, Wu C, McIntosh S, McIntosh J, Howell K . Structure of the Golgi and distribution of reporter molecules at 20 degrees C reveals the complexity of the exit compartments. Mol Biol Cell. 2002; 13(8):2810-25. PMC: 117944. DOI: 10.1091/mbc.01-12-0593. View

20.

Fukunaga T, Furuno A, Hatsuzawa K, Tani K, Yamamoto A, Tagaya M . NSF is required for the brefeldin A-promoted disassembly of the Golgi apparatus. FEBS Lett. 1998; 435(2-3):237-40. DOI: 10.1016/s0014-5793(98)01081-3. View