This paper represents my view of the development of the concept of cisternal progression-maturation over the last few decades, to date. It is not meant to be particularly technical or exhaustive, and it is not addressed only to the specialist. For more detailed information, readers are referred to the key references.
The goal is mainly to stimulate discussion, for which the cisternal maturation model appears to be a very apt subject. Indeed, perhaps more than other models in biology, cisternal maturation has been accompanied from the beginning by a number of controversies. The reason for this is not completely clear to me. It might be because the model addresses issues at the historic core of Cisternal maturation model cell biology; or because it challenges long-established views; or perhaps it is because its relevance actually goes beyond Cisternal maturation model field of intra-Golgi trafficking, as it might also apply to other trafficking steps for instance, from early to late Cisternal maturation model 12 and it gives rise to the concept of dynamic compartment identity, 3 which is of broad relevance in cell biology.
And last, but not least, the debate has suffered from uncertainties that are due to technical reasons: The cisternal progression-maturation concept has a relatively old precursor, called the progression model, according to which the transport of cargo proteins through the Golgi complex occurs by the progression of cisternae from the cis face to the trans face of the Golgi stack. The membrane flow begins with the exit from the endoplasmic reticulum of membranous carriers containing cargo proteins, and it continues with the movement of these membranes to the cis face of the Golgi complex, where they coalesce into a new cis cisterna.
This process repeats itself, and at the same time, the trans-most Golgi cisternae disassemble into transport carriers that are directed towards the plasma membrane. As a result, each cisterna changes its position in the stack—repeatedly—until it reaches the trans face. Thus, the cisternae themselves act as carriers in this intra-Golgi trafficking segment.
This model is simple and elegant, and it accommodated many morphological observations from the early decades of electron microscopy EM. Transport by cisternal progression. Cargo proteins leave the ER within dissociative carriers that reach the cis face of the Golgi stack, where these carriers coalesce to form a new cis-Golgi cisterna.
At the same time, the trans-most Golgi cisterna in this case, identifiable with the TGN disassembles into transport carriers that are directed towards the plasma membrane.
As we know, this simple state of affairs was destined to change. The main culprit, among several other Cisternal maturation model, was a series of observations documenting the presence of specific compositional differences between adjacent cisternae within a given stack reviewed in ref. This showed that the Golgi cisternae are not similar to each other, as would be expected if the cisternae were simply progressing from cis to trans.
For instance, it is now known that each cisterna has its own characteristic complement of glycosylating enzymes that differ from those of the other cisternae, and that those are arranged from cis to trans in the same order in which they are used in the sequence of glycosylation reactions that take place in the Golgi complex. This suggested a Cisternal maturation model different organization of intra-Golgi transport.
The cisternae must be stable compartments through which the cargo proteins Cisternal maturation model transported forward sequentially, by some dissociative carrier. Since the Golgi is surrounded by a number of spherical vesicles of regular size 60—70 nm in diameterit was logical to propose that it is these vesicles that are the carriers that mediate trafficking from the proximal to the distal cisternae across the Golgi stack.
For instance, the large procollagen aggregates might not actually be transported; they might just be stationary bodies where a Cisternal maturation model procollagen molecules are occasionally trapped, while productive transport takes place in other Cisternal maturation model of the cisternae see ref. Thus, despite these discrepancies, the anterograde vesicular model gained broad acceptance. And during the molecular era of trafficking, the Golgi vesicles were isolated and their components were identified COP-I subunits, Arf, etc.
In the mids, however, the transport models were re-examined critically in a few different laboratories. On the one hand, there was a feeling that the complexity of the morphological observations in different cell types could not be explained by the simple vesicular model, and that other carriers e.
To this end, it was necessary to introduce the idea of cisternal maturation. This idea was discussed initially through personal exchanges between interested members of the scientific community, and then in a brief space of time, several groups published review articles in visible mainstream journals proposing the cisternal maturation idea.
Transport by cisternal progression-maturation. Cargo proteins leave the ER within dissociative carriers that reach the cis face of the Cisternal maturation model stack, where these carriers coalesce and receive cis-Golgi enzymes that recycle from the cis cisterna, forming a new cis cisterna in the process.
Subsequently, this cis cisterna receives medial-Golgi components from the medial cisterna and loses its cis components to a new forming cis cisterna. This changes its composition and it matures into a medial cisterna, and it also progresses to a medial position in the Golgi stack.
This maturation process repeats itself until the original cis cisterna, now matured into a trans-Golgi network element and located at the trans-Golgi face, recycles its resident enzymes back to the underlying trans cisterna and breaks down into cargo-laden carriers, which move to the plasma membrane. The first study explicitly designed to test the cisternal progression-maturation model vis-a-vis the vesicular model was published in These observations could not be dismissed as incomplete or ascribed to an exceptional transport formula see above and, coupled with Cisternal maturation model constancy of Cisternal maturation model enzymatic compositions of cisternae, could only be interpreted as being due to the progression-maturation mechanism, although the maturation compositional change of the cisternae was not visualized in these experiments see below.
They therefore represented a turning point in the field, and initiated a period of Cisternal maturation model of the transport mechanisms. Moreover, they carried important implications, quickly grasped by a few investigators, that impinged on the question as to whether cellular compartments may have dynamic rather than stable identities. Together with this, two reports came out: However, the most critical test came a few years later, with the direct demonstration by two independent laboratories one of which had been among the early proponents of the model; see ref.
Importantly, the use of yeast as the model organism was necessary because yeast cisternae are not arranged in stacks; rather, they move apparently freely in the cytosol, and can therefore be monitored individually in vivo by video-microscopy at the resolution that was currently available stacked cisterna could not be resolved by the technology of the day.
The use of yeast, however, also raised questions as to whether these conclusions that were drawn for yeast are actually applicable universally, to all eukaryotic cells.
Given the degree of conservation of the fundamental cellular mechanisms found across species, including yeast and mammals, this is indeed likely to be the case. Nevertheless, experimental confirmation needs to be obtained.
Another question left open by these experiments was due to the technical difficulty of visualizing fluorescent cargo proteins together with the cisternal markers. Because the cargo could not be visualized, an objection was that Cisternal maturation model maturing cisternae being analyzed might not be involved in cargo transport.
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Again, this appears very unlikely; however, experimental confirmation is Cisternal maturation model. In any case, and in spite of the difficulties, these direct observations of cisternal maturation provided essential and direct support for this model.
In fact, together with the results on procollagen transport in fibroblasts, these data represent the experimental Cisternal maturation model of the cisternal progression-maturation concept. At almost the same time, other researchers showed that the concept of compartment maturation is applicable also to other transport steps, and specifically to early-to-late endosomal trafficking in mammalian cells.
Cisternal maturation model, Zerial and colleagues showed that over time, early endosomes lose their characteristic marker Rab 5 and acquire instead Rab 7, the main late-endosome marker, i. The same study also proposed that the mechanism of Rab conversion is the central event in compartment maturation.
This was a key discovery in the context of the issue of compartment maturation. Moreover, an important extension of this work was published recently, whereby the molecular mechanisms of this Rab conversion were further unravelled in Caenorhabditis elegans.
However, here we need to go back to the specific case of intra-Golgi transport and examine the current status of the cisternal-maturation model, with a focus, of course, on its difficulties. A general problem is our lack of knowledge about several aspects of the Golgi-maturation process, and especially the molecular ones.
These uncertainties certainly do not strengthen the model.
However, at this stage, it is more important for us to ask whether there are major difficulties that might lead us to discard this model altogether, or to alter it radically. There are two main potential cases Cisternal maturation model this kind, in my view.
One is related to the kinetics of exit of cargo from the Golgi complex. While the progression-maturation scheme predicts a linear exit rate, the kinetics that have been experimentally observed turn out to be mono-exponential.
In my view, and in the view of others, the Cisternal maturation model hypothesis fails to explain major and well-established observations in the field. Indeed, a conceptually simple explanation that might reconcile the maturation scheme with the kinetic data can be envisaged: This is an important modification of the maturation model that needs to be experimentally tested. If confirmed, it would explain all of the observed data in a logical Cisternal maturation model.
Another potentially serious problem would arise if some cargoes were found to traverse the Golgi complex at different rates than those predicted by the progression-maturation mechanisms. It is therefore important to study the trafficking patterns of more, and indeed all, of the cargo classes.
Transport by a modified cisternal progression-maturation mechanism. This mechanism is identical to cisternal maturation-progression, except that the maturation ends at the trans-Golgi level, rather than at the trans-Golgi network TGN.
Then, the trans-Golgi element recycles its resident enzymes back to the underlying cisterna and breaks down into cargo-laden carriers, which move to and accumulate in, the TGN. This modification to the cisternal maturation-progression model accommodates data indicating a mono-exponential rate of export from the TGN.
One of the results of the introduction of the maturation model and of all of the interesting discussion that has followed has been to free the minds Cisternal maturation model those of us in the field, and to attract more speculation. In this context, it is interesting to look at the recently proposed cisternal-progenitor model.
This is motivated, I believe, simply by the difficulty of envisioning that cisternal stacking is reversible, as required by cisternal maturation. This model proposes that even large supramolecular cargo, like procollagen aggregates, can move across cisternae located at different levels in neighboring stacks through Cisternal maturation model transient continuities that are established by a Rab-conversion-related mechanism.
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Author information Article notes Copyright and License information Disclaimer. Received Dec 30; Accepted Dec This article has been cited by other articles in PMC.
Cisternal Progression The cisternal progression-maturation concept has a relatively old precursor, called the progression model, according to which the transport of cargo proteins through the Golgi complex occurs by the progression of cisternae from the cis face to the trans face of the Golgi stack. Open in a separate window.
Anterograde Vesicular Transport As we know, this simple state of affairs was destined to change. Cisternal Progression-Maturation In the mids, however, the transport models were re-examined critically in a few different laboratories.
Post-Golgi Compartment Maturation Models At almost the same time, other researchers showed that the concept of compartment maturation is applicable also to other transport steps, and specifically to early-to-late endosomal trafficking in mammalian cells. Modified Cisternal Progression-Maturation However, at Cisternal maturation model stage, it is more important for us Cisternal maturation model ask whether there are major difficulties that might lead us to discard this model altogether, or to alter it radically.
Perspectives One of the results of the introduction of the maturation model and of all of the interesting discussion that has followed has been to free the minds of those of us in the field, and to attract more speculation. Comment on this article: Rab conversion as a mechanism of progression from early to late endosomes. Identification of Cisternal maturation model switch in early-to-late endosome transition.
Behnia R, Munro S.
Organelle identity and the sign-posts for membrane traffic. CR Acad Sci Paris ; French [ PubMed ].