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Porosome in Cell Secretion DISC OVERIES 2014, Jul -Sep, 2(3): e29 DOI: 10.15190/d.2014.21 Porosome in cell secretion REVIEW Article Porosome: a membrane microdomain acting as the universal secretory portal in exocytosis Mircea Leabu*, Cristina Mariana Niculite University of Medicine and Pharmacy “Carol Davila”, and “Victor Babes” National Institute of Pathology, Bucharest, Romania *Corresponding author : Mircea Leabu, PhD, “Victor Babes” National Institute of Pathology, 99-101, Splaiul Independentei, 050096, Bucharest, Romania; E-mail: [email protected] Submitted: Sept. 10, 2014; Revised: Sept. 22, 2014; Accepted: Sept. 22, 2014; Published: Sept. 23, 2014; Citation : Leabu M, Niculite CM. Porosome: a membrane microdomain acting as the universal secretory portal in exocytosis. Discoveries 2014, Jul-Sep; 2(3): e29. DOI: 10.15190/d.2014.21 ABSTRACT Keywords : porosome, membrane fusion, cell secretion, exocytosis, membrane traffic Most, if not all, cells in the organism, at least in some period of their lifetime, secrete materials that are produced within the cell. Cell secretion is a Abbreviations: Soluble N-ethyl-maleimide-sensitive factor attachment protein receptor (SNARE); N-ethyl- phenomenon requiring membrane fusion at a maleimide sensitive factor (NSF); plasma membrane specialized plasma membrane structure called the (PM); Atomic Force Microscopy (AFM); electron ‘porosome,’ which allows the material stored within microscopy (EM); chloride channels (ClC); 4,4'- secretory vesicles to be delivered to the cell’s Diisothiocyanato-2,2'-stilbenedisulfonic acid disodium exterior environment. This is achieved when the salt (DIDS) secretory vesicles fuse at the base of the porosome complex, establishing a fusion pore or fluid SUMMARY continuity between the vesicle interior and the cell’s 1. Introduction exterior. Besides cell secretion, membrane fusion is 2. Corner stones in the history of cell secretion and necessary for intracellular membrane traffic and membrane fusion vesicular transport from one endomembrane bound 3. Ultrastructure of the porosome structure to another. In addition to cell secretion, 4. Molecular organization of the porosome membrane fusion is necessary for intracellular 5. Porosome or fusion pore, or porosome and membrane trafficking and vesicle transport from fusion pore one intracellular membrane to another. We suggest 6. Porosome: a membrane microdomain that the debate about whether to use the term 7. Concluding remarks ‘porosome’ or ‘fusion pore’ to describe this process is unnecessary, since both of these terms are useful in describing aspects of the last event of cell 1. Introduction secretion, namely exocytosis. In this review, we Membrane fusion is a ubiquitous biological event in will summarize the information related to the the life of a cell. It is required for movement of discovery of the porosome, a universal secretory materials from outside to inside cells and its portal for exocytosis, and discuss porosome converse, as well as for trafficking of membranes molecular organization and function. Finally, we and soluble materials within cells. Indeed, will develop the notion that the porosome is a membrane fusion is considered a “ sine qua non ” specialized plasma membrane microdomain. phenomenon in secretory pathways. Therefore, www.discoveriesjournals.org 1 Porosome in cell secretion ♦ The POROSOME is a membrane microdomain with a complex supramolecular organization deciphering the mechanism of membrane fusion distributed on specific membrane microdomains became a challenging task for cell biologists. The with a cholesterol-enriched composition 4. However, first review on this topic appeared in 1973 1. Post other proteins contribute to the precision in time and Allison 1 pointed out the significance of and space of membrane fusion 5. Here we will membrane fusion in exocytosis, for both digestion discuss an important membrane nanostructure that and transport, although the term transcytosis had is organized as a membrane microdomain called a not yet been introduced. They also stressed the porosome. The porosomes are important in importance of turnover and redistribution of secretory vesicle docking and fusion at the target intracellular membranes and exocytosis. They membrane where exocytosis occurs. related that “the major significance of the storage of secretory products within vesicles lies not so much 2. Corner stones in the history of cell secretion in the storage process, […] but in the process by and membrane fusion which these products are released [in exquisite Secretion is a cellular function that is essential for precision, we can add] from the cell by exocytosis”. tissue and organ biogenesis and homeostasis as well They also mentioned that “exocytosis offers a as for social interactions with other cells. The term further advantage over other methods of secretion cell secretion was apparently first used (according in that the stimulus for the release of the secretory to a Pub Med search) in 1949 6. However, searching product can act directly on the plasma membrane on Google Academic, we find a paper, using “cell which is also the site of fusion and release. This secretion”, in 1911 7, which reports an abnormal enables the secretion of material by exocytosis to be mucous secretion. As a matter of fact, it is possible restricted to specific regions of the plasma to be surprised regarding the first use of the term membrane by means of differences in the ability of after a search in a well documented library, but it is various areas of the plasma membrane to respond to not our goal here to make a rigorous historical the release stimulus and by differences in the investigation. A significant moment in the transition capacity of regions of the plasma membrane to fuse from intuition to proof was made in 1964 by a paper with the secretory granule membrane” 1. Moreover, published by Lucien Caro and George Palade 8. Post and Alison intuitively suggested that These authors reported for the first time the “exocytotic activity involving fusion of secretory pathway of cell secretion in pancreatic acinar cells 8. granules with the plasma membrane would be A nice portrayal of this first great step in our expected to produce a significant increase in the knowledge of cell secretion can be found in surface area of the plasma membrane unless Palade’s Nobel lecture 9. Almost 50 years have mechanisms were available to compensate for this passed before cell biologists could decipher at the increase” 1. molecular level the pathway followed by a secreted At the present time, we know that the protein from its biosynthesis to its release to the diversity of exocytotic mechanisms is related to the outside of the cell. destiny of vesicle membranes, whether they At the time that Caro and Palade were undergo events such as “full fusion”, “kiss-and-run” undertaking their ultrastructural observations there or “kiss-and-coat” processes 2,3 . In addition, any was no detailed information at the molecular level dispute about membrane fusion as an event on the mechanisms involved in this complex governed by the membrane lipids or controlled by cellular event, except that it involved several membrane proteins is over. We know that many organelles (ribosomes, endoplasmic reticulum, types of membrane components, both lipid and Golgi apparatus), as well as other cellular protein, are important in the act of membrane ultrastructures such as secretory vesicles and cell fusion. For example, the best described proteins membrane. that act during membrane fusion are SNAREs In time, a new concept appeared that was (Soluble N-ethyl-maleimide-sensitive factor necessary to describe the mechanism of cell attachment protein receptor), and they are secretion, namely membrane fusion. Nothing www.discoveriesjournals.org 2 Porosome in cell secretion contained in a vesicle inside the cell can be exocytotic membrane vesicle with the plasma exocytosed without fusion of the secretory vesicle membrane. membrane with the cell membrane. The first The concept of specific membrane docking apparent use of the term “membrane fusion” dates before fusion and the presence of a cell membrane to 1962 and is related to fertilization in plants and structure that facilitates docking was discussed by animals 10 , whereas use of the term fusion in Bhanu Jena 16,17 . He coined the term “porosome” to relationship to cell secretion was first mentioned in describe this structure, which was inferred from 1973 11 . This occurred in spite of a theory on ultrastructural studies. The porosome was described membrane fusion that was advanced in 1971 12 . This as “a cup-shaped lipoprotein-containing basket-like phenomenon was presented as an important event in structure at the plasma membrane where secretory cell biology, even though only two cellular vesicles dock and then fuse to release vesicular processes were pointed out to support the idea: contents 16,17 . The structure of this element has been endocytosis needed for directing engulfed material described as a circular array of t- and v-SNARE to digestion in lysosomes, and exocytosis for proteins ( target- and secretory vesicle SNAREs) transporting materials from inside the cell to the that must dock at the inner plasma membrane extracellular space. According to this theory, surface before fusion of the vesicle and plasma “membrane fusion reaction is considered in four membranes can occur 16,17 . stages: membrane contact; induction; fusion; and stabilization” 12 . This contribution was based on the 3. Ultrastructure of the porosome fact
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