Crossref journal-article
Rockefeller University Press
The Journal of Cell Biology (291)
Abstract

The Golgi complex is a dynamic organelle engaged in both secretory and retrograde membrane traffic. Here, we use green fluorescent protein–Golgi protein chimeras to study Golgi morphology in vivo. In untreated cells, membrane tubules were a ubiquitous, prominent feature of the Golgi complex, serving both to interconnect adjacent Golgi elements and to carry membrane outward along microtubules after detaching from stable Golgi structures. Brefeldin A treatment, which reversibly disassembles the Golgi complex, accentuated tubule formation without tubule detachment. A tubule network extending throughout the cytoplasm was quickly generated and persisted for 5–10 min until rapidly emptying Golgi contents into the ER within 15–30 s. Both lipid and protein emptied from the Golgi at similar rapid rates, leaving no Golgi structure behind, indicating that Golgi membranes do not simply mix but are absorbed into the ER in BFA-treated cells. The directionality of redistribution implied Golgi membranes are at a higher free energy state than ER membranes. Analysis of its kinetics suggested a mechanism that is analogous to wetting or adsorptive phenomena in which a tension-driven membrane flow supplements diffusive transfer of Golgi membrane into the ER. Such nonselective, flow-assisted transport of Golgi membranes into ER suggests that mechanisms that regulate retrograde tubule formation and detachment from the Golgi complex are integral to the existence and maintenance of this organelle.

Bibliography

Sciaky, N., Presley, J., Smith, C., Zaal, K. J. M., Cole, N., Moreira, J. E., Terasaki, M., Siggia, E., & Lippincott-Schwartz, J. (1997). Golgi Tubule Traffic and the Effects of Brefeldin A Visualized in Living Cells. The Journal of Cell Biology, 139(5), 1137–1155.

Authors 9
  1. Noah Sciaky (first)
  2. John Presley (additional)
  3. Carolyn Smith (additional)
  4. Kristien J.M. Zaal (additional)
  5. Nelson Cole (additional)
  6. Jorge E. Moreira (additional)
  7. Mark Terasaki (additional)
  8. Eric Siggia (additional)
  9. Jennifer Lippincott-Schwartz (additional)
References 78 Referenced 414
  1. 10.1242/jcs.103.3.785 / J Cell Sci / The small GTP-binding protein rab6p is distributed from medial Golgi to the trans-Golgi network as determined by a confocal microscopic approach by Antony (1992)
  2. 10.1242/jcs.107.7.1885 / J Cell Sci / Movement of membrane tubules along microtubules in vitro: evidence for specialized sites of motor attachment by Allan (1994)
  3. 10.1016/0092-8674(94)90359-X / Cell / Vesicular stomatitis virus glycoprotein is sorted and concentrated during export from the endoplasmic reticulum by Balch (1994)
  4. 10.1021/bi00041a012 / Biochemistry / Characterization of a cytosolic activity that induces the formation of Golgi membrane tubules in a cell-free reconstitution system by Banta (1995)
  5. {'key': '2023072207285217300_B5'}
  6. 10.1016/0014-4827(87)90352-1 / Exp Cell Res / Galactosyltransferase and sialyltransferase are located in different subcellular compartments in HeLa cells by Berger (1987)
  7. 10.1017/S0033583500003735 / Quart Rev Biophysics / Physical properties of the fluid lipid-bilayer component of cell membranes: a perspective by Bloom (1991)
  8. 10.1016/0092-8674(93)90323-I / Cell / ADP-ribosylation factor, a small GTP-dependent regulatory protein, stimulates phospholipase D activity by Brown (1993)
  9. 10.1016/S0006-3495(97)78848-9 / Biophysics J / Electrostatics of bilayer bending by Chou (1997)
  10. 10.1002/ar.1092420302 / Anat Rec / Trans-Golgi network (TGN) of different cell types: three-dimensional structural characteristics and variability by Clermont (1995)
  11. 10.1083/jcb.120.1.15 / J Cell Biol / Tubulation of Golgi membranes in vivo and in vitro in the absence of brefeldin A by Cluett (1993)
  12. 10.1126/science.8290961 / Science / Phospholipase D: a downstream effector effector of ARF in granulocytes by Cockcroft (1994)
  13. 10.1126/science.273.5276.797 / Science / Diffusional mobility of Golgi proteins in membranes of living cells by Cole (1996)
  14. 10.1091/mbc.7.4.631 / Mol Biol Cell / Golgi dispersal during microtubule disruption: regeneration of Golgi stacks of peripheral endoplasmic reticulum exit sites by Cole (1996)
  15. 10.1016/0092-8674(90)90221-Y / Cell / Tubulovesicular processes emerge from trans-Golgi cisternae, extend along microtubules and interlink adjacent trans-Golgi elements into a reticulum by Cooper (1990)
  16. 10.1016/0092-8674(88)90176-6 / Cell / The microtubule-dependent formation of a tubulovesicular network with characteristics of the ER from cell extracts by Dabora (1988)
  17. 10.1016/0092-8674(95)90182-5 / Cell / Axon membrane flows from the growth cone to the cell body by Dai (1995)
  18. 10.1091/mbc.6.7.871 / Mol Biol Cell / A role for calmodulin in organelle membrane tubulation by de Figueiredo (1995)
  19. 10.1103/RevModPhys.57.827 / Rev Modern Phys / Wetting: statics and dynamics by de Gennes (1985)
  20. 10.1083/jcb.109.1.61 / J Cell Biol / Brefeldin A redistributes resident and itinerant Golgi proteins to the endoplasmic reticulum by Doms (1989)
  21. 10.1016/0955-0674(94)90072-8 / Curr Opin Cell Biol / ARF: a key regulatory switch in membrane traffic and organelle structure by Donaldson (1994)
  22. 10.1126/science.1957170 / Science / Binding of ARF and β-COP to Golgi membranes: possible regulation by a trimeric G protein by Donaldson (1991)
  23. 10.1083/jcb.112.4.579 / J Cell Biol / Guanine nucleotides modulates the effects of brefeldin A in semipermeable cells: regulation of the association of 110-kD peripheral membrane proteins with the Golgi apparatus by Donaldson (1991)
  24. 10.1073/pnas.89.14.6408 / Proc Natl Acad Sci USA / ADP-ribosylation factor, a small GTP-binding protein, is required for binding of the coatomer protein βCOP to Golgi membranes by Donaldson (1992)
  25. 10.1038/360350a0 / Nature / Brefeldin A inhibits Golgi membrane-catalyzed exchange of guanine nucleotide onto ARF protein by Donaldson (1992)
  26. 10.1083/jcb.138.6.1193 / JCell Biol / Nuclear membrane dynamics and reassembly in living cells: targeting of an inner nuclear membrane protein in interphase and mitosis by Ellenberg (1997)
  27. {'key': '2023072207285217300_B27'}
  28. 10.1021/bi00018a024 / Biochemistry / Functional reconstitution of the human placental transferrin receptor into phospholipid bilayers leads to long tubular structures proceeding from the vesicle surface by Fuchs (1995)
  29. 10.1016/S0021-9258(19)81393-5 / J Biol Chem / Brefeldin A causes disassembly of the Golgi complex and accumulation of secretory proteins in the endoplasmic reticulum by Fujiwara (1988)
  30. 10.1083/jcb.108.2.277 / J Cell Biol / The dynamic nature of the Golgi complex by Griffiths (1989)
  31. 10.1038/373663b0 / Nature / Improved green fluorescence by Heim (1995)
  32. 10.1038/360352a0 / Nature / Inhibition by brefeldin A of a Golgi membrane enzyme that catalyses exchange of guanine nucleotide bound to ARF by Helms (1992)
  33. 10.1016/0092-8674(92)90226-3 / Cell / A brefeldin A-like phenotype is induced by the overexpression of a human ERD-2-like protein, ELP-1 by Hsu (1992)
  34. 10.1083/jcb.121.2.317 / J Cell Biol / Retrieval of transmembrane proteins to the endoplasmic reticulum by Jackson (1993)
  35. 10.1083/jcb.116.5.1071 / J Cell Biol / Brefeldin A: insights into the control of membrane traffic and organelle structure by Klausner (1992)
  36. 10.1083/jcb.134.2.295 / J Cell Biol / Evidence that phospholipase D mediates ADP ribosylation factor– dependent formation of Golgi coated vesicles by Ktistakis (1996)
  37. 10.1083/jcb.127.1.29 / J Cell Biol / HVEM tomography of the trans-Golgi network: structural insights and identification of a lace–like vesicle coat by Ladinsky (1994)
  38. 10.1016/0092-8674(92)90476-S / Cell / Ligand-induced redistribution of a human KDEL receptor from the Golgi complex to the endoplasmic reticulum by Lewis (1992)
  39. 10.1007/BF02473201 / Histochem Cell Biol / Improving structural integrity of cryosections for immunogold labeling by Liou (1996)
  40. 10.1016/0962-8924(93)90078-F / Trends Cell Biol / Bidirectional membrane traffic between the endoplasmic reticulum and Golgi apparatus by Lippincott-Schwartz (1993)
  41. 10.1016/0092-8674(89)90685-5 / Cell / Rapid redistribution of Golgi proteins into the endoplasmic reticulum in cells treated with brefeldin A: evidence for membrane cycling from Golgi to ER by Lippincott-Schwartz (1989)
  42. 10.1016/0092-8674(90)90096-W / Cell / Microtubule-dependent retrograde transport of proteins into the ER in the presence of brefeldin A suggests an ER recycling pathway by Lippincott-Schwartz (1990)
  43. 10.1016/0092-8674(91)90534-6 / Cell / Brefeldin A's effects on endosomes, lysosomes and TGN suggest a general mechanism for regulating organelle structure and membrane traffic by Lippincott-Schwartz (1991)
  44. 10.1083/jcb.128.3.293 / J Cell Biol / Kinesin is the motor for microtubule-mediated Golgi-to-ER membrane traffic by Lippincott-Schwartz (1995)
  45. 10.1126/science.2581316 / Science (Wash DC) / A vital stain for the Golgi apparatus by Lipsky (1987)
  46. 10.1016/0092-8674(92)90027-A / Cell / The Golgi complex: in vitro veritas? by Mellman (1992)
  47. 10.1016/S0006-3495(95)79967-2 / Biophys J / Influence of transbilayer area asymmetry on the morphology of large unilamellar vesicles by Mui (1995)
  48. 10.1083/jcb.120.1.5 / J Cell Biol / Overlapping distribution of two glycosyltransferases in the Golgi apparatus of HeLa cells by Nilsson (1993)
  49. 10.1016/0092-8674(91)90273-2 / Cell / Brefeldin A, a drug that blocks secretion, prevents the assembly of non-clathrin coated buds on Golgi cisternae by Orci (1991)
  50. 10.1038/364732a0 / Nature / De novo assembly of coated vesicles from Golgi cisternae requires only coatomer and ARF proteins from the cytosol by Orci (1993)
  51. 10.1083/jcb.109.5.2067 / J Cell Biol / Molecular trapping of a fluorescent ceramide analogue at the Golgi apparatus of fixed cells: interaction with endogenous lipids provides a trans-Golgi marker for both light and electron microscopy by Pagano (1989)
  52. 10.1083/jcb.113.6.1267 / J Cell Biol / A novel fluorescent ceramide analogue for studying membrane traffic in animal cells: accumulation at the Golgi apparatus results in altered spectral properties of the sphingolipid precursor by Pagano (1991)
  53. 10.1016/S0021-9258(19)50311-8 / J Biol Chem / Binding of coatomer to Golgi membranes requires ADP-ribosylation factor by Palmer (1993)
  54. 10.1016/0955-0674(91)90027-V / Curr Opin Cell Biol / Recycling of proteins between the endoplasmic reticulum and Golgi complex by Pelham (1991)
  55. 10.1016/0092-8674(94)90002-7 / Cell / About turn for the COPs? by Pelham (1994)
  56. {'key': '2023072207285217300_B56'}
  57. {'key': '2023072207285217300_B57'}
  58. {'key': '2023072207285217300_B58', 'first-page': '189', 'article-title': 'Three-dimensional electron microscopy: structure of the Golgi apparatus', 'volume': '51', 'author': 'Rambourg', 'year': '1990', 'journal-title': 'Eur J Cell Biol'} / Eur J Cell Biol / Three-dimensional electron microscopy: structure of the Golgi apparatus by Rambourg (1990)
  59. 10.1002/aja.1001540402 / Am J Anat / Three-dimensional architecture of the Golgi apparatus in Sertoli cells of the rat by Rambourg (1979)
  60. 10.1016/S0960-9822(00)00051-8 / Curr Biol / Implications of the SNARE hypothesis for intracellular membrane topology and dynamics by Rothman (1994)
  61. 10.1126/science.272.5259.227 / Science / Protein sorting by transport vesicles by Rothman (1996)
  62. 10.1016/0014-5793(94)00484-6 / FEBS Lett / Membrane bending energy concept of vesicle- and cell-shapes and shape-transitions by Sackman (1994)
  63. 10.1016/1043-4682(92)90020-V / Semin Cell Biol / Pathways of protein sorting and membrane traffic between the rough endoplasmic reticulum and the Golgi complex by Saraste (1992)
  64. 10.1242/jcs.100.3.415 / J Cell Sci / Distribution of the intermediate elements operating in ER to Golgi transport by Saraste (1991)
  65. {'key': '2023072207285217300_B65', 'first-page': '19', 'article-title': 'Morphological analysis of the Golgi apparatus in rat amelogenesis as revealed by the Ur-Pb-Cu block staining method and freeze fracture replication', 'volume': '33', 'author': 'Sasaki', 'year': '1984', 'journal-title': 'J Electron Microsc'} / J Electron Microsc / Morphological analysis of the Golgi apparatus in rat amelogenesis as revealed by the Ur-Pb-Cu block staining method and freeze fracture replication by Sasaki (1984)
  66. 10.1242/jcs.107.3.517 / J Cell Sci / A three-dimensional reconstruction study of the rough ER-Golgi interface in serial thin sections of the pancreatic acinar cell of the rat by Sesso (1994)
  67. 10.1126/science.271.5255.1526 / Science / Coat proteins and vesicle budding by Schekman (1996)
  68. 10.1016/0962-8924(96)80993-7 / Trends Cell Biol / Modulation of membrane dynamics and cell motility by membrane tension by Sheetz (1996)
  69. 10.1083/jcb.137.6.1211 / J Cell Biol / Partitioning of the Golgi apparatus during mitosis in living HeLa cells by Shima (1997)
  70. 10.1083/jcb.131.6.1387 / J Cell Biol / Anterograde and retrograde traffic between the rough endoplasmic reticulum and the Golgi complex by Stinchcombe (1995)
  71. {'key': '2023072207285217300_B71', 'first-page': '1', 'article-title': 'Three- dimensional architecture of the Golgi complex observed by high resolution scanning electron microscopy', 'volume': '18', 'author': 'Tanaka', 'year': '1986', 'journal-title': 'J Submicrosc Cytol'} / J Submicrosc Cytol / Three- dimensional architecture of the Golgi complex observed by high resolution scanning electron microscopy by Tanaka (1986)
  72. 10.1083/jcb.120.2.325 / J Cell Biol / Molecular cloning, characterization, subcellular localization, and dynamics of p23, the mammalian KDEL receptor by Tang (1993)
  73. 10.1083/jcb.103.4.1557 / J Cell Biol / Microtubules and the endoplasmic reticulum are highly interdependent structures by Terasaki (1986)
  74. 10.1083/jcb.107.6.2233 / J Cell Biol / Formation of membrane networks in vitro by kinesin-driven microtubule movement by Vale (1988)
  75. 10.1016/S0092-8674(85)80099-4 / Cell / Identification of a novel force-generating protein, kinesin, involved in microtubule-based motility by Vale (1985)
  76. 10.1146/annurev.bi.62.070193.001543 / Annu Rev Biochem / Membrane partitioning during cell division by Warren (1993)
  77. 10.1038/255684a0 / Nature / Cholesterol is selectively excluded from the phospholipid annulus surrounding an active calcium transport protein by Warren (1975)
  78. 10.1016/S0092-8674(05)80089-3 / Cell / Golgi membrane dynamics imaged by freeze-etch electron microscopy: views of different membrane coatings involved in tubulation versus vesiculation by Weidman (1993)
Dates
Type When
Created 23 years, 1 month ago (July 26, 2002, 12:47 p.m.)
Deposited 2 years, 1 month ago (July 22, 2023, 3:30 a.m.)
Indexed 5 days, 1 hour ago (Aug. 28, 2025, 8:38 a.m.)
Issued 27 years, 9 months ago (Dec. 1, 1997)
Published 27 years, 9 months ago (Dec. 1, 1997)
Published Online 27 years, 9 months ago (Dec. 1, 1997)
Published Print 27 years, 9 months ago (Dec. 1, 1997)
Funders 0

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@article{Sciaky_1997, title={Golgi Tubule Traffic and the Effects of Brefeldin A Visualized in Living Cells}, volume={139}, ISSN={1540-8140}, url={http://dx.doi.org/10.1083/jcb.139.5.1137}, DOI={10.1083/jcb.139.5.1137}, number={5}, journal={The Journal of Cell Biology}, publisher={Rockefeller University Press}, author={Sciaky, Noah and Presley, John and Smith, Carolyn and Zaal, Kristien J.M. and Cole, Nelson and Moreira, Jorge E. and Terasaki, Mark and Siggia, Eric and Lippincott-Schwartz, Jennifer}, year={1997}, month=dec, pages={1137–1155} }