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Vol. 17, Issue 2, 990-1005, February 2006

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Golgi Inheritance in Mammalian Cells Is Mediated through Endoplasmic Reticulum Export Activities

Nihal Altan-Bonnet ^* , Rachid Sougrat ^*, Wei Liu ^*, Erik L. Snapp ^*, Theresa Ward , and Jennifer Lippincott-Schwartz ^*

^* Cell Biology and Metabolism Branch, National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, MD 20892; The London School of Tropical Medicine and Hygiene, London WC1E 7HT, United Kingdom

Submitted February 24, 2005; Revised November 7, 2005; Accepted November 15, 2005
Monitoring Editor: Benjamin Glick

Golgi inheritance during mammalian cell division occurs through the disassembly, partitioning, and reassembly of Golgi membranes. The mechanisms responsible for these processes are poorly understood. To address these mechanisms, we have examined the identity and dynamics of Golgi proteins within mitotic membranes using live cell imaging and electron microscopy techniques. Mitotic Golgi fragments, seen in prometaphase and telophase, were found to localize adjacent to endoplasmic reticulum (ER) export domains, and resident Golgi transmembrane proteins cycled rapidly into and out of these fragments. Golgi proteins within mitotic Golgi haze—seen during metaphase—were found to redistribute with ER markers into fragments when the ER was fragmented by ionomycin treatment. The temperature-sensitive misfolding mutant ts045VSVG protein, when localized to the Golgi at the start of mitosis, became trapped in the ER at the end of mitosis in cells shifted to 40°C. Finally, reporters for Arf1 and Sar1 activity revealed that Arf1 and Sar1 undergo sequential inactivation during mitotic Golgi breakdown and sequential reactivation upon Golgi reassembly at the end of mitosis. Together, these findings support a model of mitotic Golgi inheritance that involves inhibition and subsequent reactivation of cellular activities controlling the cycling of Golgi components into and out of the ER.

The online version of this article contains supplemental material at MBC Online (http://www.molbiolcell.org).

Present address: Department of Biological Sciences, Rutgers University, Newark, NJ 07102.

Address correspondence to: Jennifer Lippincott-Schwartz (jlippin{at}helix.nih.gov).

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