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Abstract

The endoplasmic reticulum (ER) is the largest organelle in mammalian cells. More than 50 years ago, its morphology was already described as consisting of two major compartments: the rough ER and the smooth ER, which both fulfil precise and distinct functions to sustain the cellular metabolism. The rough ER localizes in the perinuclear region and is composed of packed membrane sheets with studded ribosomes. The smooth ER extends to the cell periphery as a continuous tubular membrane meshwork. Impairment of the ER structure is related to multiple diseases, in particular psycho-motor degenerations such as hereditary spastic paraplegia. The current model of the ER architecture suggests that specific ER proteins, called ER-shaping proteins, generate and maintain the ER morphology. Different families of ER-shaping proteins support either the curvature or the flatness of the membrane and the exact ER morphology depends on their local concentrations. Although the structural role of these proteins has been extensively characterized, the mechanism of their regulation by the cell is mostly unknown. Moreover, the process has to be very dynamic, as the ER membrane morphology is rapidly interconverted. Our work has discovered that several ER-shaping proteins are modified by a post-translational modification named S-palmitoylation. S-palmitoylation is the covalent but reversible attachment of a 16 carbons chain fatty acid to a cysteine residue of a protein. Interestingly, both ER-sheet and ER-tubule promoting proteins were modified. We observed that these palmitoylated ER-shaping proteins are all controlled by the same palmitoyl-acyltransferase: DHHC6. Thus, our results suggest that DHHC6 is a master regulator of the ER architecture. We also demonstrated that palmitoylation stabilizes the lifetime of one specific substrate: CLIMP-63, which induces ER-sheet proliferation. Transient expression of DHHC6 generated prominent ER-sheets, which were dependent on CLIMP-63's presence and palmitoylation. On the contrary, the absence of DHHC6 diminished the size of the rough ER. Finally, to study protein palmitoylation, we developed a novel assay which was able to quantify the fraction of palmitoylated protein at steady state. Taken together, our data highlight the first general mechanism that mediates the ER architecture. Our future work will focus on understanding how and when the cell uses palmitoylation of ER-shaping proteins and clarifying the effectors of this signalling pathway.

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