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Vol. 17, Issue 4, 1495-1502, April 2006
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Essay
* Department of Molecular Biology, Princeton University, Princeton, NJ 08544;
Department of Zoology, Program in Cellular and Molecular Biology, University of Wisconsin, Madison, Madison, WI 53706
Submitted October 3, 2005;
Revised December 20, 2005;
Accepted January 18, 2006
Monitoring Editor: Benjamin Glick
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ABSTRACT |
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INTRODUCTION |
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; McNeil and Steinhardt, 2003).
Two forms of regulated exocytosis have been described, based on the fate of the secretory vesicle membrane after fusion with the PM—"full fusion" and "kiss-and-run" (Fesce et al., 1994; Artalejo et al., 1998; Schneider, 2001; Valtorta et al., 2001; Wightman and Haynes, 2004). During full fusion, the fusion pore opens and dilates until the membrane of the secretory vesicle is completely collapsed into the PM. The excess membrane is subsequently retrieved by clathrin-dependent or -independent mechanisms (Figure 1; Table 1). During kiss-and-run, the fusion pore opens but does not dilate, maintaining a diameter of 1–5 nm (Lollike et al., 1995; Staal et al., 2004; Table 1), and a fraction of the vesicle contents are released. The fusion pore is then rapidly resealed, thereby retrieving the secretory vesicle membrane more or less intact (Figure 1). In both cases, the exocytotic event itself is quite rapid, typically occurring in a less than a second (Table 1).
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KISS-AND-COAT EXOCYTOSIS |
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; Gandhi and Stevens, 2003; Allersma et al., 2004). Indeed, the relative fraction of exocytotic events that correspond to full fusion or kiss-and-run can be modulated within a given cell type by specific molecular interventions (Burgoyne and Barclay, 2002; Wang et al., 2003). However, it is also becoming apparent that several diverse cell types undergo regulated exocytosis in a far more sedate manner that does not conform to either full fusion or kiss-and-run (Table 1). Specifically, after fusion with the PM, cortical granules in eggs of sea urchins (Whalley et al., 1995), fish (Becker and Hart, 1999), and amphibians (Bement et al., 2000) are apparent as distinct compartments beneath the PM for 
5–60 s or more (Table 1). Similarly, pancreatic acinar cell secretory zymogen granules can remain in a fused state with the PM from 30 s up to 15 min (Nemoto et al., 2001, 2004; Thorn et al., 2004; Thorn and Parker, 2005). Even more protracted is exocytosis in alveolar type II cells, where the fused lamellar body granules may persist as morphologically distinct compartments for 30 min or more (Haller et al., 1998, 2001). And, in all of the above-mentioned cases, the fused vesicles have fusion pores 2–3 orders of magnitude larger than the 1- to 5-nm pores calculated for kiss-and-run exocytosis (Table 1). The ultimate fate of the secretory vesicle membrane remnants in these cell types is not as well understood as during full fusion or kiss-and-run, but at least some of it is apparently retrieved without collapsing into the PM (see below). The observation that the emptied secretory vesicle persists as a morphologically distinct compartment beneath the PM for many seconds to many minutes differentiates this type of exocytosis from full fusion, whereas the dilation and maintenance of the fusion pore also render it distinct from kiss-and-run. Thus, a third type of exo/endocytosis exists, used by otherwise diverse cell types that undergo regulated secretion. Because this type of exocytosis is associated with assembly of actin coats around the exocytosing secretory vesicles (see below), we suggest the name "kiss-and-coat" to distinguish this mode of exo/endocytosis from full fusion and kiss-and-run.
Identification of kiss-and-coat as a distinct mechanism in regulated exocytosis is important for at least four reasons. First, it is likely that kiss-and-coat exocytosis is uniquely adapted to promote discharge of secretory material under conditions where it cannot be released rapidly. That is, in the cell types most clearly shown to undergo kiss-and-coat exocytosis (Table 1), the secretory vesicles are much larger than those in many neurons and neuroendocrine cell types (500–15,000 versus 20–50 nm in diameter; Table 1), whereas the vesicle contents are often much less soluble. For example, egg cortical granules contain virtually crystalline arrays of lectins (Wessel et al., 2001), and lamellar bodies, the major secretory compartment in alveolar type II cells, contain tightly packed surfactant, which is comprised of a protein–phospholipid mixture (Dietl and Haller, 2005). So insoluble is surfactant, it frequently remains associated in a clot extending outside the cell from the fusion pore for many minutes after the onset of exocytosis (Haller et al., 2001). Extended fusion and dilated fusion pores would ensure complete release of such large macromolecules from large vesicles by maximizing the size and duration of the interface between the vesicle contents and the extracellular medium. Second, kiss-and-coat permits sequential exocytosis (Nemoto et al., 2001; Thorn and Parker, 2005). That is, by maintaining a relatively large, stable portal between the primary vesicle (i.e., the vesicle that first fuses with the PM), subsequent homotypic fusion events of secondary and tertiary vesicles are ensured of free movement of vesicle contents to the extracellular medium (Figure 1). Third, given the wealth of cell types with large secretory vesicles and the apparent frequency of sequential exocytosis, it is likely that kiss-and-coat is at least as common as either full fusion or kiss-and-run. Fourth, prolonged union of secretory vesicles with the PM without collapse of the vesicle membrane into the PM has critical mechanistic implications for the events that follow fusion. These implications are discussed next.
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ACTIN COATING AS A SECRETORY VESICLE STABILIZER |
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) has revealed that cortical granules become surrounded with F-actin after fusion with the PM (Figure 2). Such actin coats are not restricted to Xenopus eggs: F-actin was previously shown to associate with "crypts" thought to represent sites of granule release in zebrafish eggs (Becker and Hart, 1999). Furthermore, studies of fixed pancreatic acinar cells, using probes for both F-actin and exocytosing zymogen granules, have shown clearly that the remnant secretory granule membranes in these cells are likewise associated with F-actin, whereas those granules that have not undergone exocytosis are not (Nemoto et al., 2004; Turvey and Thorn, 2004). These studies were presaged by previous work on fixed samples of acinar cells showing that a subset of secretory vesicles were associated with F-actin, although it was not clear whether F-actin coating preceded or followed exocytosis (Valentijn et al., 2000). Similarly, a recent study of fixed alveolar cells has revealed that a subset of secretory vesicles are associated with F-actin (van Weeren et al., 2004), suggesting that F-actin coating is a conserved feature of exocytosis in this cell type as well. The importance of F-actin coats for the stability of the vesicle remnants is revealed by the fact that disruption of F-actin results in collapse (full fusion) of cortical granule membranes into the PM after exocytosis in Xenopus eggs (Sokac et al., 2003) and abnormal expansion of fused zymogen granules into structures that mimic those seen in pancreatitis in pancreatic acinar cells (Valentijn et al., 1999; Nemoto et al., 2004; but see also Bi and Williams, 2005).
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; Nemoto et al., 2004). In Xenopus eggs, actin assembly starts at the fusion pore and then spreads along the entire granule surface, to actually compress the exocytosing cortical granule (Figure 2; Sokac et al., 2003). In pancreatic acini, assembling actin does not immediately compress the compartments but instead progressively encloses zymogen granules undergoing sequential exocytosis (Nemoto et al., 2004). Thus, depending on the requirements of the cell type in question, actin assembly is subjected to extraordinarily tight spatial and temporal control.
The coating of exocytosing vesicles with F-actin not only stabilizes the secretory compartment during prolonged union with the PM but also may be responsible for eventual compensatory endocytosis. In Xenopus eggs, the actin coat compresses the cortical granule membrane, at least some of which seems to be retrieved directly (Sokac et al., 2003), whereas zymogen granule membranes undergo similar compression in acinar cells after exocytosis and seem to be retrieved at least in part without collapse into the PM (Nemoto et al., 2004; Thorn et al., 2004). Furthermore, that actin coats in Xenopus eggs actually compress exocytosing granules (Sokac et al., 2003) raises the possibility that coating could also promote expulsion of secretory granule contents into the extracellular medium. These findings reveal a new and important function for F-actin in membrane trafficking in addition to its previously demonstrated roles in receptor-mediated endocytosis (Engqvist-Goldstein and Drubin, 2003; Merrifield, 2004) and modulation of membrane fusion (Vitale et al., 2001, Ehre et al., 2005).
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COMPARTMENT MIXING AS A STIMULUS FOR LOCAL ACTIN ASSEMBLY |
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). Similarly, actin coats in pancreatic acini are likewise restricted to zymogen granules that have exocytosed (Nemoto et al., 2004; Turvey and Thorn, 2004). Second, comparison of the timing of calcium elevation in Xenopus eggs versus exocytosis and actin coat assembly reveals that actin coat assembly is tightly correlated with exocytosis itself but not directly correlated with calcium elevation (Figure 3). Third, in pancreatic acini, actin assembly during sequential exocytosis is likewise directly correlated with fusion of adjacent zymogen granules, and not directly correlated with the stimulus for exocytosis itself, except insofar as the stimulus is required to initiate exocytosis (Nemoto et al., 2004).
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Thus, there is a tight spatial and temporal correlation between actin assembly on exocytosing secretory vesicles and the fusion event itself, and only an indirect correlation with the stimulus for secretion, implying that fusion itself is the trigger. The two major changes that result from secretory vesicle–PM fusion are exposure of the interior of the secretory compartments to the extracellular medium and mixing of components of the PM with the components of the secretory vesicle membrane. However, actin coats form around exocytosing cortical granules in Xenopus eggs regardless of the makeup of the external medium (our unpublished data). We therefore propose that compartment mixing acts as the proximal trigger for actin assembly on exocytosing secretory vesicles, such that the union of previously separated components of the PM and secretory vesicle membranes results in rapid actin filament nucleation (Figure 4).
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A compartment mixing-dependent mechanism for actin assembly has at least one obvious advantage over a mechanism triggered by calcium elevation per se. That is, F-actin is well known to suppress exocytosis by acting as a barrier to secretory vesicle–PM fusion (Ehre et al., 2005). Thus, if actin assembly were triggered as a result of calcium elevation, any secretory vesicles that failed to immediately fuse with the PM in response to calcium would nonetheless become coated with F-actin and likely be inhibited from fusing later. Given that in eggs (Terasaki, 1995; Bement et al., 2000), pancreatic acini (Nemoto et al., 2001), and aveolar type II cells (Haller et al., 1998) not all secretory vesicles fire immediately upon calcium elevation, an actin assembly mechanism directly entrained to calcium elevation would be expected to significantly reduce the number, extent, or both of functional exocytotic events.
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MECHANISMS OF COMPARTMENT MIXING-DEPENDENT ACTIN ASSEMBLY |
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 TOPABSTRACTINTRODUCTIONKISS-AND-COAT EXOCYTOSISACTIN COATING AS A...COMPARTMENT MIXING AS A... MECHANISMS OF COMPARTMENT MIXING... COMPARTMENT MIXING-DEPENDENT...FUTURE DIRECTIONSACKNOWLEDGMENTSREFERENCES |
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If these mechanisms are to work as a signal for local actin assembly, the diffusional mobility of proteins, lipids, or both into or out of the membrane remnants of the secretory vesicle would have to be somewhat, but not completely, limited. Otherwise, any necessary gradients of membrane components would either be rapidly equalized upon fusion (Allersma et al., 2004) or would never develop in the first place. Although this point has not been investigated thoroughly in the examples of kiss-and-coat exocytosis cited above, analysis of fixed samples has shown that, after exocytosis, syntaxin-2, a PM SNARE, localizes to zymogen granule membrane remnants in pancreatic acinar cells (Pickett et al., 2005). Surprisingly, it has also been shown that diffusion of a lipid marker from fused secretory granule membranes into the PM is relatively minimal in the same system (Thorn et al., 2004). As suggested by the authors, this might reflect either differential mobility of particular players or differences in experimental conditions between the two studies. In Xenopus eggs, phosphatidylinositol 4,5-bisphosphate (PIP2) from the PM incorporates into exocytosing cortical granule membranes (Figure 5), as do biotinylated cell surface proteins (our unpublished data), at levels that are reduced relative to those found in the PM, consistent with the generation of local gradients within the plane of the secretory vesicle membrane.
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) and has been suggested as a general mediator of actin assembly during exocytosis (Cremona and De Camilli, 2001). As described above, PIP2 incorporates into exocytosing Xenopus egg cortical granule membranes. Additionally, the DAG mimic phorbol 12-myristate 13-acetate promotes actin assembly on vesicles in Xenopus eggs and egg extracts in a manner that may be N-WASP and Cdc42 dependent (Taunton et al., 2000). Because actin coat assembly in Xenopus is associated with both local Cdc42 activation and N-WASP recruitment (Sokac et al., 2003), either or both of these lipids could promote local actin assembly after incorporation into cortical granule membranes.
Regarding the molecular players likely to couple signals generated by compartment mixing to actin assembly, we are on firmer ground. The rho class GTPases, which promote actin filament assembly via various effectors, have been implicated in secretion in several systems (Bader et al., 2004) and at least two of these are required for actin coat assembly during kiss-and-coat exocytosis—Cdc42 and Rho. In Xenopus eggs, active Cdc42 localizes to exocytosing cortical granules as does N-WASP (Sokac et al., 2003), a Cdc42 target that promotes actin assembly. Furthermore, perturbing Cdc42 function prevents actin coat assembly and mimics the phenotype produced by actin disruption. In pancreatic acinar cells, disruption of Rho function likewise prevents actin coating of zymogen granules and mimics pharmacological inhibition of actin assembly (Nemoto et al., 2004), and induction of exocytosis is associated with activation of both Rho and Rac (Bi and Williams, 2005).
Dynamin represents another potential downstream target of compartment mixing-generated signals, based on several previous observations. Specifically, dynamin has been implicated in retrieval of exocytotic vesicles after kiss-and-run exocytosis (Graham et al., 2002; Holroyd et al., 2002; Tsuboi et al., 2004) and is known to promote vesicle-associated actin assembly (Lee and De Camilli, 2002; Merrifield et al., 2002; Orth et al., 2002; Schafer et al., 2002). Although the secretory compartment remnants associated with kiss-and-coat exocytosis are far larger than those typically associated with dynamin-dependent retrieval, it could potentially function by helping carve out small portions of the remnant membrane, similar to the late stages of phagocytosis (Aggeler and Werb, 1982).
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COMPARTMENT MIXING-DEPENDENT ACTIN ASSEMBLY IN OTHER CONTEXTS |
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). Analogous to the results from Xenopus eggs and pancreatic acini, recent studies show that rho class GTPases are progressively recruited to forming phagosomes (Hoppe and Swanson, 2004). The means by which the GTPases are activated has yet to be determined, but it has been shown that phagosome formation is accompanied by focal exocytosis (Bajno et al., 2000). Cell locomotion is accompanied by activation of rho GTPases at the leading edge of crawling cells (Kraynov et al., 2000) and membrane inserts in the same region (Schmoranzer et al., 2003). Similarly, PM damage is accompanied by both local exocytosis (Bi et al., 1995), and activation of rho class GTPases (Benink and Bement, 2005). Newly forming, E-cadherin-mediated cell–cell adhesion sites recruit exocyst components from the cytoplasm to direct local exocytosis (Grindstaff et al., 1998), and cadherin engagement activates Rho-family GTPases (Braga and Yap, 2005). Last, during cytokinesis, the furrow region has long been known as a site of local membrane insertion (Danilchik et al., 2003), and has recently been shown to be a site of local RhoA activation (Bement et al., 2005).
Although the notion that compartment mixing directs local rho GTPase activation and actin remodeling in situations beyond kiss-and-coat exocytosis has yet to be tested, this idea is particularly attractive for at least two reasons. First, in all of the above-mentioned examples, actin assembly is confined in a very precise manner at or near the PM, with immediate proximity to the site of exocytosis. Second, microtubules are required for many of the above-mentioned processes, and one of the major functions of microtubules is to direct membrane insertion (Goodson et al., 1997).
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FUTURE DIRECTIONS |
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ACKNOWLEDGMENTS |
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Footnotes |
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Address correspondence to: William M. Bement (wmbement{at}wisc.edu).
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) were fixed at times before and after calcium elevation and then stained for F-actin with fluorescent phalloidin. In Z-sections, PIP2 (green) is found at the PM before elevation of calcium (PRIOR) but is not evident in cortical granules. Shortly after calcium elevation (EARLY), PIP2 spreads part way into the exocytosing cortical granule membrane (arrowhead) before any sign of F-actin coating (red). At later stages (LATE), the PIP2 is distributed throughout the cortical granule membrane and is surrounded by an F-actin coat (arrows). (For imaging methods, see Sokac et al., 2003