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.
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1 December 1997
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December 01 1997
Golgi Tubule Traffic and the Effects of Brefeldin A Visualized in Living Cells
In Special Collection:
JCB65: Trafficking and Organelles
Noah Sciaky,
Noah Sciaky
*Cell Biology and Metabolism Branch, National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, Maryland 20892; ‡National Institute of Neurological Disorders and Stroke, NIH, Bethesda, Maryland 20892; §Department of Physiology, University of Connecticut Health Center, Farmington, Connecticut 06032; and ‖Department of Physics, Cornell University, Ithaca, New York 14853
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John Presley,
John Presley
*Cell Biology and Metabolism Branch, National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, Maryland 20892; ‡National Institute of Neurological Disorders and Stroke, NIH, Bethesda, Maryland 20892; §Department of Physiology, University of Connecticut Health Center, Farmington, Connecticut 06032; and ‖Department of Physics, Cornell University, Ithaca, New York 14853
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Carolyn Smith,
Carolyn Smith
*Cell Biology and Metabolism Branch, National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, Maryland 20892; ‡National Institute of Neurological Disorders and Stroke, NIH, Bethesda, Maryland 20892; §Department of Physiology, University of Connecticut Health Center, Farmington, Connecticut 06032; and ‖Department of Physics, Cornell University, Ithaca, New York 14853
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Kristien J.M. Zaal,
Kristien J.M. Zaal
*Cell Biology and Metabolism Branch, National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, Maryland 20892; ‡National Institute of Neurological Disorders and Stroke, NIH, Bethesda, Maryland 20892; §Department of Physiology, University of Connecticut Health Center, Farmington, Connecticut 06032; and ‖Department of Physics, Cornell University, Ithaca, New York 14853
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Nelson Cole,
Nelson Cole
*Cell Biology and Metabolism Branch, National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, Maryland 20892; ‡National Institute of Neurological Disorders and Stroke, NIH, Bethesda, Maryland 20892; §Department of Physiology, University of Connecticut Health Center, Farmington, Connecticut 06032; and ‖Department of Physics, Cornell University, Ithaca, New York 14853
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Jorge E. Moreira,
Jorge E. Moreira
*Cell Biology and Metabolism Branch, National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, Maryland 20892; ‡National Institute of Neurological Disorders and Stroke, NIH, Bethesda, Maryland 20892; §Department of Physiology, University of Connecticut Health Center, Farmington, Connecticut 06032; and ‖Department of Physics, Cornell University, Ithaca, New York 14853
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Mark Terasaki,
Mark Terasaki
*Cell Biology and Metabolism Branch, National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, Maryland 20892; ‡National Institute of Neurological Disorders and Stroke, NIH, Bethesda, Maryland 20892; §Department of Physiology, University of Connecticut Health Center, Farmington, Connecticut 06032; and ‖Department of Physics, Cornell University, Ithaca, New York 14853
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Eric Siggia,
Eric Siggia
*Cell Biology and Metabolism Branch, National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, Maryland 20892; ‡National Institute of Neurological Disorders and Stroke, NIH, Bethesda, Maryland 20892; §Department of Physiology, University of Connecticut Health Center, Farmington, Connecticut 06032; and ‖Department of Physics, Cornell University, Ithaca, New York 14853
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Jennifer Lippincott-Schwartz
Jennifer Lippincott-Schwartz
*Cell Biology and Metabolism Branch, National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, Maryland 20892; ‡National Institute of Neurological Disorders and Stroke, NIH, Bethesda, Maryland 20892; §Department of Physiology, University of Connecticut Health Center, Farmington, Connecticut 06032; and ‖Department of Physics, Cornell University, Ithaca, New York 14853
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Noah Sciaky
*Cell Biology and Metabolism Branch, National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, Maryland 20892; ‡National Institute of Neurological Disorders and Stroke, NIH, Bethesda, Maryland 20892; §Department of Physiology, University of Connecticut Health Center, Farmington, Connecticut 06032; and ‖Department of Physics, Cornell University, Ithaca, New York 14853
John Presley
*Cell Biology and Metabolism Branch, National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, Maryland 20892; ‡National Institute of Neurological Disorders and Stroke, NIH, Bethesda, Maryland 20892; §Department of Physiology, University of Connecticut Health Center, Farmington, Connecticut 06032; and ‖Department of Physics, Cornell University, Ithaca, New York 14853
Carolyn Smith
*Cell Biology and Metabolism Branch, National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, Maryland 20892; ‡National Institute of Neurological Disorders and Stroke, NIH, Bethesda, Maryland 20892; §Department of Physiology, University of Connecticut Health Center, Farmington, Connecticut 06032; and ‖Department of Physics, Cornell University, Ithaca, New York 14853
Kristien J.M. Zaal
*Cell Biology and Metabolism Branch, National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, Maryland 20892; ‡National Institute of Neurological Disorders and Stroke, NIH, Bethesda, Maryland 20892; §Department of Physiology, University of Connecticut Health Center, Farmington, Connecticut 06032; and ‖Department of Physics, Cornell University, Ithaca, New York 14853
Nelson Cole
*Cell Biology and Metabolism Branch, National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, Maryland 20892; ‡National Institute of Neurological Disorders and Stroke, NIH, Bethesda, Maryland 20892; §Department of Physiology, University of Connecticut Health Center, Farmington, Connecticut 06032; and ‖Department of Physics, Cornell University, Ithaca, New York 14853
Jorge E. Moreira
*Cell Biology and Metabolism Branch, National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, Maryland 20892; ‡National Institute of Neurological Disorders and Stroke, NIH, Bethesda, Maryland 20892; §Department of Physiology, University of Connecticut Health Center, Farmington, Connecticut 06032; and ‖Department of Physics, Cornell University, Ithaca, New York 14853
Mark Terasaki
*Cell Biology and Metabolism Branch, National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, Maryland 20892; ‡National Institute of Neurological Disorders and Stroke, NIH, Bethesda, Maryland 20892; §Department of Physiology, University of Connecticut Health Center, Farmington, Connecticut 06032; and ‖Department of Physics, Cornell University, Ithaca, New York 14853
Eric Siggia
*Cell Biology and Metabolism Branch, National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, Maryland 20892; ‡National Institute of Neurological Disorders and Stroke, NIH, Bethesda, Maryland 20892; §Department of Physiology, University of Connecticut Health Center, Farmington, Connecticut 06032; and ‖Department of Physics, Cornell University, Ithaca, New York 14853
Jennifer Lippincott-Schwartz
*Cell Biology and Metabolism Branch, National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, Maryland 20892; ‡National Institute of Neurological Disorders and Stroke, NIH, Bethesda, Maryland 20892; §Department of Physiology, University of Connecticut Health Center, Farmington, Connecticut 06032; and ‖Department of Physics, Cornell University, Ithaca, New York 14853
1. Abbreviations used in this paper: ARF, ADP-ribosylation factor; BFA, brefeldin A; FRAP, fluorescence recovery after photobleaching; GFP, green fluorescent protein; NEM, N-ethylmaleimide; ROI, region of interest.
Address all correspondence to Jennifer Lippincott-Schwartz, Cell Biology and Metabolism Branch, NICHD, NIH, Building 18T, Room 101, Bethesda, MD 20892. Tel.: (301) 496-6368. Fax: (301) 402-0078.
Noah Sciaky's current address is Department of Pediatrics, National Jewish Center, Denver, Colorado.
Received:
May 06 1997
Revision Received:
October 06 1997
Online ISSN: 1540-8140
Print ISSN: 0021-9525
1997
J Cell Biol (1997) 139 (5): 1137–1155.
Article history
Received:
May 06 1997
Revision Received:
October 06 1997
Citation
Noah Sciaky, John Presley, Carolyn Smith, Kristien J.M. Zaal, Nelson Cole, Jorge E. Moreira, Mark Terasaki, Eric Siggia, Jennifer Lippincott-Schwartz; Golgi Tubule Traffic and the Effects of Brefeldin A Visualized in Living Cells . J Cell Biol 1 December 1997; 139 (5): 1137–1155. doi: https://doi.org/10.1083/jcb.139.5.1137
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