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Published online February 25, 2008
doi:10.1083/jcb.200708109
The Journal of Cell Biology, Vol. 180, No. 4, 803-812
The Rockefeller University Press, 0021-9525 $30.00
© 2008 Blagoveshchenskaya et al.
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Article

 Integration of Golgi trafficking and growth factor signaling by the lipid phosphatase SAC1

Anastasia Blagoveshchenskaya1, Fei Ying Cheong1, Holger M. Rohde2, Greta Glover3, Andreas Knödler1, Teresa Nicolson3, Guido Boehmelt2, and Peter Mayinger1,4

1 Division of Nephrology and Hypertension and 4 Department of Cell and Developmental Biology, Oregon Health and Science University, Portland, OR 97239
2 Boehringer Ingelheim Austria GmbH, 1121 Vienna, Austria
3 Oregon Hearing Research Center and Howard Hughes Medical Institute, Portland, OR 97239

Correspondence to Peter Mayinger: mayinger{at}ohsu.edu

When a growing cell expands, lipids and proteins must be delivered to its periphery. Although this phenomenon has been observed for decades, it remains unknown how the secretory pathway responds to growth signaling. We demonstrate that control of Golgi phosphatidylinositol-4-phosphate (PI(4)P) is required for growth-dependent secretion. The phosphoinositide phosphatase SAC1 accumulates at the Golgi in quiescent cells and down-regulates anterograde trafficking by depleting Golgi PI(4)P. Golgi localization requires oligomerization of SAC1 and recruitment of the coat protein (COP) II complex. When quiescent cells are stimulated by mitogens, SAC1 rapidly shuttles back to the endoplasmic reticulum (ER), thus releasing the brake on Golgi secretion. The p38 mitogen-activated kinase (MAPK) pathway induces dissociation of SAC1 oligomers after mitogen stimulation, which triggers COP-I–mediated retrieval of SAC1 to the ER. Inhibition of p38 MAPK abolishes growth factor–induced Golgi-to-ER shuttling of SAC1 and slows secretion. These results suggest direct roles for p38 MAPK and SAC1 in transmitting growth signals to the secretory machinery.

Abbreviations used in this paper: COP, coat protein; ERK, extracellular signal-regulated kinase; LZ, leucine zipper; MEK, MAPK/ERK kinase; PDI, protein disulfide isomerase; PI, phosphoinositide; PI(4)P, phosphatidylinositol-4-phosphate.


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