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Secretory traffic triggers the formation of tubular continuities across Golgi sub-compartments

Nature Cell Biology volume 6, pages 1071–1081 (2004)Cite this article

Abstract

The organization of secretory traffic remains unclear, mainly because of the complex structure and dynamics of the secretory pathway. We have thus studied a simplified system, a single synchronized traffic wave crossing an individual Golgi stack, using electron tomography. Endoplasmic-reticulum-to-Golgi carriers join the stack by fusing with cis cisternae and induce the formation of intercisternal tubules, through which they redistribute their contents throughout the stack. These tubules seem to be pervious to Golgi enzymes, whereas Golgi vesicles are depleted of both enzymes and cargo. Cargo then traverses the stack without leaving the cisternal lumen. When cargo exits the stack, intercisternal connections disappear. These findings provide a new view of secretory traffic that includes dynamic intercompartment continuities as key players.

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Figure 1: The nocodazole-induced secretory system during the 15 °C block.
Figure 2: Morphometric analysis of the structural changes in nocodazole-induced stacks during the passage of a cargo wave.
Figure 3: Tubular connections between successive cisternae during the passage of a cargo wave through nocodazole-induced stacks.
Figure 4: Progression of cargo through nocodazole-induced stacks.
Figure 5: Tubular connections between successive cisternae of Golgi stacks during traffic in non-perturbed cells.
Figure 6: Schematic model of the passage of a synchronized traffic wave through a single Golgi stack.

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Acknowledgements

A. Mironov and A. Luini are principal investigators and have contributed equally to this project. We would like to thank all those who provided us with antibodies and cDNAs, P. Lupetti for assistance with fast-freezing experiments, C. P. Berrie for critical reading of the manuscript and E. Fontana for artwork preparation. We acknowledge financial support from the AIRC, Telethon Italy and a European Research Training Network (A.L. and K.N.J.B.). A.J.K. is supported by the Royal Netherlands Academy of Arts and Sciences (KNAW), and W.J.C.G. and K.N.J.B. by FEI.

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  1. Alvar Trucco and Roman S. Polishchuk: These authors contributed equally to this work.

Authors and Affiliations

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

    Alvar Trucco, Roman S. Polishchuk, Oliviano Martella, Alessio Di Pentima, Aurora Fusella, Daniele Di Giandomenico, Enrica San Pietro, Galina V. Beznoussenko, Elena V. Polishchuk, Massimiliano Baldassarre, Roberto Buccione, Alexander A. Mironov & Alberto Luini

  2. Department of Molecular Cell Biology, Institute of Biomembranes, Utrecht University, Utrecht, 3584 CH, The Netherlands

    Willie J. C. Geerts, Abraham J. Koster & Koert N. J. Burger

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Trucco, A., Polishchuk, R., Martella, O. et al. Secretory traffic triggers the formation of tubular continuities across Golgi sub-compartments. Nat Cell Biol 6, 1071–1081 (2004). https://doi.org/10.1038/ncb1180

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