The Golgi complex: 120 years and it doesn't show

Maria Antonietta De Matteis, Daniela Corda, Alberto Luini

One hundred and twenty years after its discovery, the Golgi complex still attracts the interest of cell biologists, and many yet open questions address both ‘old’ and ‘new’ aspects of its function. Over this long period, the field has shifted focus several times, giving rise to distinct eras of Golgi research. The initial descriptive era lay the basis for our present knowledge of the Golgi organization and transport function, whereas the subsequent reductionist era involved the identification of basic molecular machineries that execute fundamental and elementary trafficking steps. During the genomic era, we have observed a notable increase in the repertoire of molecular components known to contribute to the organization and function of the Golgi, as well as to the integration of Golgi functions with the global cell response. Presently, in the postgenomic era, we are faced with the challenge of incorporating available information into a coherent model of the morphological and functional organization of the Golgi that encompasses the diverse roles of this organelle in cargo transport, sorting and processing; in lipid metabolism; and as a relay or generator of signaling cascades.

The diverse roles of the Golgi are the focus of the review articles collected in this FEBS Letters Special Issue on the Golgi complex. This Special Issue has been inspired by a FEBS special meeting held last October in Sorrento, namely the 2018 Golgi meeting: membrane trafficking in cell organization and homeostasis (Fig. 1).

The structure and content of this Special Issue hopefully crystallizes the interesting scientific exchanges that took place at the 2018 Golgi meeting, which spanned across four general themes: (a) autoregulation and homeostasis of the transport apparatus; (b) interorganellar signaling and coordination with complex cellular responses; (c) lipid biosynthesis and trafficking; and (d) cargo processing in the Golgi.

Autoregulation and homeostasis of the transport apparatus

The first session of the 2018 Golgi meeting addressed the mechanisms by which the membrane traffic system maintains its homeostasis and performs its enormous tasks in a safe, efficient, and robust way in the face of the perturbations it is exposed to, using specialized sensing and signaling systems. A central question in this field is how the transport stations communicate across each other and with other cell modules through signaling pathways. This question was addressed both at the meeting and in this special issue, through the perspective of signaling events occurring at the ER‐Golgi interface [1] and at the Golgi [2-4].

Interorganellar signaling and coordination with complex cellular responses

The second part of the 2018 Golgi meeting and this special issue maintain the above focus on the role of signalling in endomembranes function, but also emphasize more on the cross‐regulation concept. Such examples of cross‐regulation include: the lysosome‐based signaling and its impact on nuclear functions [5]; the endomembrane‐based signaling and various types of stress, either oxidative or nutritional [6]; the regulation of ion homeostasis by the Golgi, with a talk dedicated to a disease (the Wilson syndrome) due to a defect in copper metabolism [7]; and the role of calcium in the apical secretion of GPI‐linked proteins [8]. Another exciting theme in the 2018 Golgi meeting session on interorganellar signaling and coordination with complex cellular responses was the signaling mechanisms linking the Golgi fragmentation process to mitotic entry.

Lipid biosynthesis and trafficking

The next, rich part of the 2018 Golgi meeting and this special issue focuses on lipid transport and metabolism, and is dominated by two interrelated topics: the contact sites between cellular organelles; and the lipid transfer proteins operating between organelles, and particularly between the ER and the Golgi. Key talks of the 2018 Golgi meeting were dedicated to the basic molecular mechanisms underlying the contact structures, and to the rapidly emerging variety of lipid exchanges across interorganelle contacts [9]. Following a logical sequence, the focus next shifted to themes of lipid transport and metabolism, and in particular of metabolism of the glycosphigolipids [10], with in depth discussions on the role of these lipids in disease and cell fate determination.

Cargo processing in the Golgi

The final theme of cargo transport and processing is dedicated to what is probably the core function of the Golgi complex, the assembly of glycans on cargo protein and lipid scaffold, for which the Golgi is often defined the glycosylation factory of the cell [11]. The main topics here are glycosylation and signaling in health and disease, the fundamental, yet still relatively unexplored mechanisms of glycan assembly during intra‐Golgi transport by the plethora of glycoenzymes continuously recycling through the Golgi stack, and the regulation of glycosylation by posttranslational modifications.

Similarly to glycosylation, organelle dynamics, involving transport to and through the Golgi are also core elements of the Golgi. Several talks at the 2018 Golgi meeting and review articles in this special issue focused on the factors involved in membrane tethering, docking, fission and fusion [12-14]; the enzyme adaptors; and the small regulatory GTPases with functions in enzyme recycling through the Golgi [15]. Remarkably, the framework for the analysis of these mechanisms was the organization by cisternal progression maturation of intra‐Golgi traffic, which appeared to be generally accepted by the Golgi community, after years of uncertainties and debate.

The fascination of the topic blended with the beauty of the landscape, the soft warm air and the great local food sparked lively discussions among the participants. We hope that this Special Issue can distill the exceptional atmosphere of the 2018 Golgi meeting, which the Golgi community wishes to see regularly repeated in the Amalfi coast. Integration of membrane transport with other cell functions and the great puzzle of glycan assembly in the Golgi are predicted by many to continue to enjoy center stage at the next Golgi meeting.

The Golgi Special Issue

References:

1. Centonze FG and Farhan H (2019)  Crosstalk of endoplasmic reticulum exit sites and cellular signaling. FEBS Lett  593,  2280– 2288. Wiley Online Library
2. Di Martino R, Sticco L and Luini A (2019)  Regulation of cargo export and sorting at the trans‐golgi Network. FEBS Lett  593,  2306– 2318. Wiley Online Library
3. Kulkarni‐Gosavi P, Makhoul C and Gleeson PA (2019)  Form and function of the Golgi apparatus: scaffolds, cytoskeleton and signaling. FEBS Lett  593, 2289– 2305. Wiley Online Library
4. von Blume J and Hausser A (2019)  Lipid‐dependent coupling of secretory cargo sorting and trafficking at the trans‐Golgi network. FEBS Lett  593,  2412– 2427. Wiley Online Library
5. De Leonibus C, Cinque L and Settembre C (2019)  Emerging lysosomal pathways for quality control at the endoplasmic reticulum. FEBS Lett  593, 2319– 2329. Wiley Online Library
6. Sasaki K and Yoshida H (2019)  Golgi stress response and organelle zones. FEBS Lett  593,  2330– 2340. Wiley Online Library
7. Polishchuk RS and Polishchuk EV (2019)  From and to the Golgi – defining the Wilson disease protein road map. FEBS Lett  593,  2341– 2350. Wiley Online Library
8. Lebreton S, Paladino S and Zurzolo C (2019)  Clustering in the Golgi apparatus governs sorting and function of GPI‐APs in polarized epithelial cells. FEBS Lett  593,  2351– 2365. Wiley Online Library
9. Kumagai K and Hanada K (2019)  Structure, functions and regulation of CERT, a lipid‐transfer protein for the delivery of ceramide at the ER–Golgi membrane contact sites. FEBS Lett  593,  2366– 2377. Wiley Online Library
10. Jiménez‐Rojo N and Riezman H (2019)  On the road to unraveling the molecular functions of ether lipids. FEBS Lett  593,  2378– 2389. Wiley Online Library
11. Pothukuchi P, Agliarulo I, Russo D, Rizzo R, Russo F and Parashuraman S(2019)  Translation of genome to glycome: role of the Golgi apparatus  593, 2390– 2411.Google Scholar
12. Welch LG and Munro S (2019)  A tale of short tails, through thick and thin: investigating the sorting mechanisms of Golgi enzymes. FEBS Lett  593, 2452– 2465. Wiley Online Library
13. Blackburn JB, D'Souza Z and Lupashin VV (2019)  Maintaining order: COG complex controls Golgi trafficking, processing and sorting. FEBS Lett  593, 2466– 2487. Wiley Online Library
14. Zhukovsky MA, Filograna A, Luini A, Corda D and Valente C (2019) Phosphatidic acid in membrane rearrangements. FEBS Lett  593,  2428– 2451. Wiley Online Library
15. Lipatova Z and Segev N (2019)  Ypt/Rab GTPases and their TRAPP GEFs at the Golgi. FEBS Lett  593,  2488– 2500. Wiley Online Library