An Ordered Inheritance Strategy for the Golgi Apparatus: Visualization of Mitotic Disassembly Reveals a Role for the Mitotic Spindle

doi:10.1083/jcb.141.4.955

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© The Rockefeller University Press, 0021-9525/1998//955 $5.00
The Journal of Cell Biology, Volume 141, Number 4, , 1998 955-966

Articles

An Ordered Inheritance Strategy for the Golgi Apparatus: Visualization of Mitotic Disassembly Reveals a Role for the Mitotic Spindle

David T. Shima^*, Noemí Cabrera-Poch^*, Rainer Pepperkok, and Graham Warren^*

^* Cell Biology Laboratory, and Light Microscopy Laboratory, Imperial Cancer Research Fund, London WC2A 3PX, United Kingdom

During mitosis, the ribbon of the Golgi apparatus is transformedinto dispersed tubulo-vesicular membranes, proposed to facilitatestochastic inheritance of this low copy number organelle atcytokinesis. Here, we have analyzed the mitotic disassemblyof the Golgi apparatus in living cells and provide evidence that inheritance is accomplished through an ordered partitioningmechanism. Using a Sar1p dominant inhibitor of cargo exit fromthe endoplasmic reticulum (ER), we found that the disassemblyof the Golgi observed during mitosis or microtubule disruptiondid not appear to involve retrograde transport of Golgi residentsto the ER and subsequent reorganization of Golgi membrane fragments at ER exit sites, as has been suggested. Instead,direct visualization of a green fluorescent protein (GFP)-taggedGolgi resident through mitosis showed that the Golgi ribbonslowly reorganized into 1–3-µm fragments duringG2/early prophase. A second stage of fragmentation occurredcoincident with nuclear envelope breakdown and was accompaniedby the bulk of mitotic Golgi redistribution. By metaphase,mitotic Golgi dynamics appeared to cease. Surprisingly, the disassembly of mitotic Golgi fragments was not a random event,but involved the reorganization of mitotic Golgi by microtubules,suggesting that analogous to chromosomes, the Golgi apparatususes the mitotic spindle to ensure more accurate partitioningduring cytokinesis.

Abbreviations used in this paper: BFA, brefeldin A; COP, coat protein; ERGIC, endoplasmic reticulum–Golgi intermediate compartment; GFP, green fluorescent protein; NAGFP, glycosyltransferase NAGTI; TAC, tip attachment complex.

D.T. Shima is a Hitchings-Elion fellow supported by the Burroughs Wellcome Fund and N. Cabrera-Poch is a recipient of a PostdoctoralFellowship from the Spanish Ministry of Education and Culture.

Drs. Shima and Cabrera-Poch contributed equally to this work.

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