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First published online 29 August 2006
doi: 10.1242/jcs.03172

Journal of Cell Science 119, 3888-3900 (2006)
Published by The Company of Biologists 2006
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Research Article

Starvation and ULK1-dependent cycling of mammalian Atg9 between the TGN and endosomes

Andrew R. J. Young1, Edmond Y. W. Chan1, Xiao Wen Hu1, Robert Köchl1, Samuel G. Crawshaw2, Stephen High2, Dale W. Hailey3, Jennifer Lippincott-Schwartz3 and Sharon A. Tooze1,*

1 Cancer Research UK London Research Institute, 44 Lincoln's Inn Fields, London, WC2A 3PX, UK
2 Faculty of Life Sciences, University of Manchester, Smith Building, Oxford Road, Manchester, M13 9PT, UK
3 NIH / NICHD / CBMB, Bldg 18T Room 101, 9000 Rockville Pike, Bethesda, MD, 20892, USA

* Author for correspondence (e-mail: Sharon.tooze{at}cancer.org.uk)

Accepted 11 July 2006

Autophagy, fundamentally a lysosomal degradation pathway, functions in cells during normal growth and certain pathological conditions, including starvation, to maintain homeostasis. Autophagosomes are formed through a mechanism that is not well understood, despite the identification of many genes required for autophagy. We have studied the mammalian homologue of Atg9p, a multi-spanning transmembrane protein essential in yeast for autophagy, to gain a better understanding of the function of this ubiquitious protein. We show that both the N- and C-termini of mammalian Atg9 (mAtg9) are cytosolic, and predict that mAtg9 spans the membrane six times. We find that mAtg9 is located in the trans-Golgi network and late endosomes and colocalizes with TGN46, the cation-independent mannose-6-phosphate receptor, Rab7 and Rab9. Amino acid starvation or rapamycin treatment, which upregulates autophagy, causes a redistribution of mAtg9 from the TGN to peripheral, endosomal membranes, which are positive for the autophagosomal marker GFP-LC3. siRNA-mediated depletion of the putative mammalian homologue of Atg1p, ULK1, inhibits this starvation-induced redistribution. The redistribution of mAtg9 also requires PI 3-kinase activity, and is reversed after restoration of amino acids. We speculate that starvation-induced autophagy, which requires mAtg9, may rely on an alteration of the steady-state trafficking of mAtg9, in a Atg1-dependent manner.

Key words: Autophagy, Golgi, Rab proteins, Intracellular transport, Transmembrane protein


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