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This is due to the protein kinase C-dependent phosphorylation of its basic C-terminal region, which results in its acidification and thus in its shedding from the negatively charged plasma membrane bilayer. Subsequent dephosphorylation by calcineurin allows TMEM24 to return to contact sites, where it may participate in replenishing PI 4,5 P 2 pools via its PI transport properties. In yeast, Nvj2 was reported to relocalize from the nuclear—vacuolar junction to ER—Golgi contacts in response to ER stress, thus pointing to regulation also for this SMP domain-containing tether, although the underlying mechanisms remain unclear [ 48 ].

If so, it would have to involve disassembly of the complex, as two of its components are integral membrane proteins of the ER and of the mitochondria, respectively. Much remains to be understood about SMP domain-containing proteins and their tethering and lipid transport functions. Their number is likely to expand, as the structural characterization of proteomes advances. Key open questions are the mechanisms through which these proteins extract and then deliver lipids from and to bilayers and the regulation of these reactions.

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As SMP-dependent transport between bilayers does not require energy and flows down the concentration gradient of the lipids, there must be mechanisms to control their lipid transport activities in order to preserve the heterogeneous lipid composition of participating bilayers. The field of membrane contact sites is rapidly advancing and opening new vistas about inter-organelle communication in cellular function.

A hallmark of eukaryotic cells is their organization into membrane-bound compartments. This allows for the spatial and temporal separation of incompatible biochemical processes. Nevertheless, cellular organelles including endoplasmic reticulum ER , mitochondria, Golgi, lysosome, and peroxisome must co-ordinate their activities to allow the cell to function properly as a biological system. An emerging theme is that communication between compartments often occurs at sites of close apposition between organelle membranes, called membrane contact sites MCSs.

These MCSs play important roles in metabolic channeling, allowing molecules such as lipids and calcium to be transferred directly from one organelle to another [ 60 ].

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Identifying the proteins that mediate organelle contacts is an active area of research [ 61 ] and contacts between many different organelle types are being newly discovered. Recently, a variety of new imaging techniques have been applied to elucidate the structure, function, and dynamics of MCSs. MCSs have long been observed by electron microscopy EM —see the contribution by Tim Levine in this forum for a discussion of the history of organelle contacts. Modern electron microscopy techniques, including cryo-electron microscopy and tomography, have revealed a number of structural features of MCSs.

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Cryo-electron tomography revealed structural differences between different types of ER—plasma membrane contact sites. Electron microscopy techniques allow visualization of MCSs with exquisite resolution; however, these techniques are not well suited to answer questions about organelle and MCS dynamics, because cells must be fixed prior to imaging. The advent of genetically encoded fluorescent labels, such as green fluorescent protein GFP and its spectral variants, has revolutionized the study of cell biology and allows imaging of the dynamic processes in living cells, including MCSs.

The use of fluorescent proteins targeted to the ER and other organelles facilitated further insights into the functions of MCSs—that of organelle remodeling. Work from the laboratory of Gia Voeltz demonstrated that fission of both mitochondria and endosomes occurs at sites of contact with the ER [ 64 , 65 ]. How general a phenomenon this is remains to be demonstrated.

Other fluorescence-based approaches have been used to obtain complementary information about MCSs. Bimolecular fluorescence involves the use of a split Venus fluorescent protein construct. One half of the Venus protein is conjugated to a membrane protein in one organelle, and the other half to a known and specific membrane protein in another organelle. Although the technique may bias the frequency and duration of MCSs by artificially stabilizing them, Schuldiner and colleagues have used this technique for its extraordinary power to discover MCSs between organelles not previously observed [ 61 ].

Bimolecular fluorescence complementation has also been used to investigate the interaction between specific proteins on different organelles, for example, between lipid droplets LDs and mitochondria or peroxisomes [ 67 ]. Live cell fluorescence imaging is a powerful technique to answer systems-level questions about the frequency, duration, and overall dynamics of MCSs. However, the inability to distinguish fluorophores with highly overlapping emission spectra has limited its use to the labeling of a few different organelles in live cells.

Our laboratory has recently developed a cell labeling, imaging, and computational analysis method to identify the systems-level dynamic organization of organelle interactions in cells [ 68 ]. We targeted fluorescent fusion proteins to ER, mitochondria, Golgi, lysosomes, and peroxisomes and used a vital dye to label LDs.

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We then used confocal and lattice lightsheet spectral imaging approaches to image these six organelles simultaneously, in live fibroblast cells Fig. This approach provides a powerful tool to identify potential MCSs and to generate hypotheses regarding their dynamics. We demonstrated that all six labeled organelles made contacts with each and every other labeled organelle. These contacts often had elaborate morphologies, involving multiple different organelles in close proximity Fig.

We further demonstrated that these contacts were dependent upon an intact microtubule cytoskeleton, as treatment with nocodazole, which disrupts microtubule polymerization, reduced the number of organelle interactions, especially those involving LDs. This pattern shifted in response to changes in the availability of nutrients for example, starvation or excess fatty acids , but the ER always remained the central node in the interactome network, making the most contacts with other organelles.

Functional reconstitution of membranes and biogenesis, Membrane fusion

Spectral imaging reveals organelle interactions. Images were acquired on a confocal microscope with a spectral detector, and subjected to linear unmixing and spatial deconvolution. Right : enlargement of the region outlined in the left panel. The ER transparent yellow is shown in the right panels only. We used this spectral imaging approach to track individual organelles, and map their contacts over time.

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We focused on LDs, which are thought to exchange lipids including phospholipids, fatty acids, and cholesterol with various other compartments in response to cell signaling events [ 69 ]. Tracking LDs, we found that most made near continuous contact with the ER, which is a major site of lipid synthesis. Contacts between LDs and other organelles were shorter, and occurred in various different combinations. Some LDs made contact with only one or two other organelles over the course of five minutes, while some LDs touched every other labeled organelle in rapid succession.

We also visualized contacts between mitochondria and other organelles, and found that mitochondria make the most contact with ER, followed by Golgi and LDs. In the future, this method could be combined with probes that detect metabolites such as lipids or calcium, in order to measure their transfer between organelles at MCSs directly. Multispectral and other imaging methods will be useful for investigating the effect of various perturbations on organelle contacts and dynamics.

Lipid Sorting and Multivesicular Endosome Biogenesis

We envision using this approach to investigate organelle organization in response to various environmental and developmental cues, including changes in the availability of nutrients, exposure to drugs, and infection with pathogens. Organelle contacts are also likely to change over the course of the cell cycle, and may show unique signatures in different regions of polarized or migrating cells.

Faster imaging will reveal even more information about the dynamics of different types of organelle interactions. For example, LDs may interact with different compartments as they are born emerging from the ER , grow, deliver lipids to other compartments, and turn over via lipolysis or lipophagy. Spectral imaging will also be a useful tool for identifying proteins that mediate or regulate MCSs, and for visualizing protein complexes and cytoskeletal elements at the interface between organelles. MCSs are a fascinating frontier in cell biology, mediating a variety of important metabolic functions.

We are confident that the continued development of better fluorescent probes, as well as ever gentler, faster and higher-resolution imaging methods, will allow for exciting new discoveries in this emerging field.

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  • Here I will review some of the year history of this field, to identify four of the landmark discoveries and also point out some intellectual near misses along the way. First Contact. Even though there is no accepted definition for a contact site, the closer and more extended a proximity is, the more it suggests some function. This has meant that the contact sites with the narrowest gaps tend to have been studied most.

    The first contacts were described in Fig. Working on muscle cells these authors reported similar contacts in [ 71 ].

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    • Timeline of early contact site discoveries. For references in the timeline please see [ 70 , 71 , 75 , 81 , 82 , 83 , 72 , 74 — 76 , 80 — 84 ]. A refashioned GERL. Ultrastructural analysis by electron microscopy progressed to the point where Alex Novikoff identified regions of specialised ER associated with Golgi membranes, particularly on the trans face of the Golgi near lysosomes. Novikoff proposed wrongly that lysosomes develop directly from the Golgi-associated ER [ 72 , 73 ].

      Because of this error in proposed function, the significance and accuracy of the morphological concept of contact between ER and trans-Golgi was easily dismissed [ 74 ]. Subsequently, ER—Golgi contact sites have been ascribed roles in lipid traffic [ 14 ] and see contribution by Guillaume Drin.

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      Furthermore, interactions between organelles in this region of the cell are now known to be even more complex than Novikoff envisaged see contribution by Sarah Cohen et al. Giving the idea some muscle. It is no accident that some of the easiest contacts to see are in muscle cells, as their highly enlarged ER called the sarcoplasmic reticulum SR forms extended contacts. The plasma membrane is also unusual, invaginating to form long transverse tubules. Each transverse tubule is sandwiched between a pair of parallel SR tubules, together forming a triad, as named by Porter and Palade [ 71 ].

      Along the length of each triad, the SR forms multiple close contacts with the transverse tubule. In Clara Franzini-Armstrong identified proteins inside the contact zones Fig. Over the following three decades these proteins were shown to consist of coupled calcium channels that convert the plasma membrane depolarisation spike to a rapid widespread release of SR calcium.

      No to interfacial purity. A major approach in the early days of membrane cell biology was cell fractionation. Membrane fractions, for example from density gradients, were specifically enriched in individual organelles and de-enriched in all others.