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J. Biol. Chem., Vol. 283, Issue 37, 25735-25751, September 12, 2008

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A Block in Endoplasmic Reticulum-to-Golgi Trafficking Inhibits Phospholipid Synthesis and Induces Neutral Lipid Accumulation^*

Maria L. Gaspar, Stephen A. Jesch, Raghuvir Viswanatha, Amy L. Antosh, William J. Brown, Sepp D. Kohlwein, and Susan A. Henry¹

From the Department of Molecular Biology and Genetics, Cornell University, Ithaca, New York 14853 and Institute of Molecular Biosciences, University of Graz, A8010 Graz, Austria

Seeking to better understand how membrane trafficking is coordinated with phospholipid synthesis in yeast, we investigated lipid synthesis in several Sec^- temperature-sensitive mutants, including sec13-1. Upon shift of sec13-1 cells to the restrictive temperature of 37 °C, phospholipid synthesis decreased dramatically relative to the wild type control, whereas synthesis of neutral lipids, especially triacylglycerol (TAG), increased. When examined by fluorescence microscopy, the number of lipid droplets appeared to increase and formed aggregates in sec13-1 cells shifted to 37 °C. Electron microscopy confirmed the increase in lipid droplet number and revealed that many were associated with the vacuole. Analysis of lipid metabolism in strains lacking TAG synthase genes demonstrated that the activities of the products of these genes contribute to accumulation of TAG in sec13-1 cells after the shift to 37 °C. Furthermore, the permissive temperature for growth of the sec13-1 strain lacking TAG synthase genes was 3 °C lower than sec13-1 on several different growth media, indicating that the synthesis of TAG has physiological significance under conditions of secretory stress. Together these results suggest that following a block in membrane trafficking, yeast cells channel lipid metabolism from phospholipid synthesis into synthesis of TAG and other neutral lipids to form lipid droplets. We conclude that this metabolic switch provides a degree of protection to cells during secretory stress.

Received for publication, April 7, 2008 , and in revised form, June 27, 2008.

^* This work was supported, in whole or in part, by National Institutes of Health Grants GM019629 (to S. A. H.) and DK51596 (to W. J. B.) from the NIGMS and NIDDK, respectively. This work was also supported by SFB Lipotox P3005 of the Austrian Science Fund (to S. D. K.). The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

¹ To whom correspondence should be addressed: 260 Roberts Hall, Cornell University, Ithaca, NY 14853. Fax: 607-255-3803; E-mail: sah42{at}cornell.edu.

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