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Vol. 18, Issue 5, 1595-1608, May 2007

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The Biogenesis of the Golgi Ribbon: The Roles of Membrane Input from the ER and of GM130

Pierfrancesco Marra^*, Lorena Salvatore, Alexander Mironov, Jr, Antonella Di Campli, Giuseppe Di Tullio, Alvar Trucco, Galina Beznoussenko, Alexander Mironov, and Maria Antonietta De Matteis

Department of Cell Biology and Oncology, Consorzio Mario Negri Sud, 66030 Santa Maria Imbaro, Chieti, Italy

Submitted October 3, 2006; Revised November 29, 2006; Accepted February 6, 2007
Monitoring Editor: Benjamin Glick

The Golgi complex in mammalian cells forms a continuous ribbon of interconnected stacks of flat cisternae. We show here that this distinctive architecture reflects and requires the continuous input of membranes from the endoplasmic reticulum (ER), in the form of pleiomorphic ER-to-Golgi carriers (EGCs). An important step in the biogenesis of the Golgi ribbon is the complete incorporation of the EGCs into the stacks. This requires the Golgi-matrix protein GM130, which continuously cycles between the cis-Golgi compartments and the EGCs. On acquiring GM130, the EGCs undergo homotypic tethering and fusion, maturing into larger and more homogeneous membrane units that appear primed for incorporation into the Golgi stacks. In the absence of GM130, this process is impaired and the EGCs remain as distinct entities. This induces the accumulation of tubulovesicular membranes, the shortening of the cisternae, and the breakdown of the Golgi ribbon. Under these conditions, however, secretory cargo can still be delivered to the Golgi complex, although this occurs less efficiently, and apparently through transient and/or limited continuities between the EGCs and the Golgi cisternae.

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

Present addresses: * Section of Cell and Molecular Biology, Institute of Cancer Research, Chester Beatty Laboratories, 237 Fulham Road, London SW3 6JB, United Kingdom;

Electron Microscopy Unit, Faculty of Life Sciences, Stopford Building, University of Manchester, Oxford Road, Manchester, M139PT, United Kingdom.

Address correspondence to: Maria Antonietta De Matteis (dematteis{at}negrisud.it) or Alexander Mironov (mironov{at}negrisud.it)

Abbreviations used: CHX, cycloheximide; EGCs, ER-to-Golgi carriers; GC, Golgi complex; KDELR, KDEL receptor; N309, an antibody directed against the N309 aa of GM130.