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• W2025033557 abstract "Calcium cations play a critical role in regulating vesicular transport between different intracellular membrane-bound compartments. The role of calcium in transport between the Golgi cisternae, however, remains unclear. Using a well characterized cell-free intra-Golgi transport assay, we now show that changes in free Ca2+ concentration in the physiological range regulate this transport process. The calcium-chelating agent 1,2-bis(2-aminophenoxy)ethane-N,N,N′,N′-tetraacetic acid blocked transport with an IC50 of approximately 0.8 mm. The effect of 1,2-bis(2-aminophenoxy)ethane-N,N,N′,N′-tetraacetic acid was reversible by addition of fresh cytosol and was irreversible when performed in the presence of a Ca2+ ionophore that depletes calcium from lumenal stores. We demonstrate here that intra-Golgi transport is stimulated by low Ca2+concentrations (20–100 nm) but is inhibited by higher concentrations (above 100 nm). Further, we show that calmodulin antagonists specifically block intra-Golgi transport, implying a role for calmodulin in mediating the effect of calcium. Our results suggest that Ca2+ efflux from intracellular pools may play an essential role in regulating intra-Golgi transport. Calcium cations play a critical role in regulating vesicular transport between different intracellular membrane-bound compartments. The role of calcium in transport between the Golgi cisternae, however, remains unclear. Using a well characterized cell-free intra-Golgi transport assay, we now show that changes in free Ca2+ concentration in the physiological range regulate this transport process. The calcium-chelating agent 1,2-bis(2-aminophenoxy)ethane-N,N,N′,N′-tetraacetic acid blocked transport with an IC50 of approximately 0.8 mm. The effect of 1,2-bis(2-aminophenoxy)ethane-N,N,N′,N′-tetraacetic acid was reversible by addition of fresh cytosol and was irreversible when performed in the presence of a Ca2+ ionophore that depletes calcium from lumenal stores. We demonstrate here that intra-Golgi transport is stimulated by low Ca2+concentrations (20–100 nm) but is inhibited by higher concentrations (above 100 nm). Further, we show that calmodulin antagonists specifically block intra-Golgi transport, implying a role for calmodulin in mediating the effect of calcium. Our results suggest that Ca2+ efflux from intracellular pools may play an essential role in regulating intra-Golgi transport. endoplasmic reticulum calmodulin vesicular stomatitis virus 1,2-bis(2-aminophenoxy)ethane-N,N,N′,N′-tetraacetic acid guanosine 5′-O-(thiotriphosphate) soluble NSF attachment protein Although Ca2+ is the most abundant cation in vertebrates, eukaryotic cells sequester Ca2+ efficiently, mainly by uptake into intracellular stores, and thus display low cytosolic concentrations of about 100 nm (for reviews see Refs. 1Clapham D.E. Cell. 1995; 80: 259-268Abstract Full Text PDF PubMed Scopus (2261) Google Scholar and 2Pozzan T. Rizzuto R. Volpe P. Meldolesi J. Physiol. Rev. 1994; 74: 595-636Crossref PubMed Scopus (30) Google Scholar). Fast and short (transient) increases in the cytosolic Ca2+ concentration play a pivotal role in many physiological processes, and the dynamic characteristics of these pools are regulated in a well defined manner. Calcium sequestration into the ER1 lumen depends on Ca2+-ATPases, known as sarco/endoplasmic reticulum ATPases (for reviews see Ref. 2Pozzan T. Rizzuto R. Volpe P. Meldolesi J. Physiol. Rev. 1994; 74: 595-636Crossref PubMed Scopus (30) Google Scholar), all of which share the common property of being selectively inhibited by thapsigargin, a tumor-promoting sesquiterpene lactone (3Lytton J. Westlin M. Hanley M.R. J. Biol. Chem. 1991; 266: 17067-17071Abstract Full Text PDF PubMed Google Scholar). Calcium handling by the ER is also controlled by inositol 1,4,5-triphosphate and ryanodine receptors (4Berridge M.J. Nature. 1993; 361: 315-325Crossref PubMed Scopus (6157) Google Scholar, 5Ferris C.D. Snyder S.H. J. Neurosci. 1992; 12: 1567-1574Crossref PubMed Google Scholar, 6Fill M. Coronado R. Trends Neurosci. 1988; 11: 453-457Abstract Full Text PDF PubMed Scopus (91) Google Scholar, 7McPherson P.S. Campbell K.P. J. Biol. Chem. 1993; 268: 13765-13768Abstract Full Text PDF PubMed Google Scholar). Although much is known about the ER as an intracellular Ca2+ storage pool, far less is known about calcium sequestration by the Golgi apparatus. Recent studies documented the presence of a sarco/endoplasmic reticulum adenosine triphosphatase isoform and inositol 1,4,5-triphosphate receptors on the Golgi and showed that they dynamically regulate calcium homeostasis of this organelle (8Pinton P. Pozzan T. Rizzuto R. EMBO J. 1998; 17: 5298-5308Crossref PubMed Scopus (379) Google Scholar). Increasing evidence indicates the involvement of Ca2+ cations in different intracellular transport steps. For example, Ca2+ requirement was demonstrated for ER to Golgi transport and for the assembly of the nuclear envelope (9Schwaninger R. Beckers C.J. Balch W.E. J. Biol. Chem. 1991; 266: 13055-13063Abstract Full Text PDF PubMed Google Scholar, 10Sullivan K.M. Busa W.B. Wilson K.L. Cell. 1993; 73: 1411-1422Abstract Full Text PDF PubMed Scopus (121) Google Scholar). Moreover, recent studies showed that both homotypic vacuolar fusion and fusion between early endosomes depend on Ca2+ and calmodulin (CaM), the ubiquitous calcium effector (11Peters C. Mayer A. Nature. 1998; 396: 575-580Crossref PubMed Scopus (324) Google Scholar, 12Colombo M.I. Beron W. Stahl P.D. J. Biol. Chem. 1997; 272: 7707-7712Abstract Full Text Full Text PDF PubMed Scopus (115) Google Scholar, 13Holroyd C. Kistner U. Annaert W. Jahn R. Mol. Biol. Cell. 1999; 10: 3035-3044Crossref PubMed Scopus (71) Google Scholar). However, the role played by Ca2+ in intra-Golgi transport remains unclear. The cell-free intra-Golgi transport assay was reported to be insensitive to the Ca2+ chelator EGTA (14Fries E. Rothman J.E. Proc. Natl. Acad. Sci. U. S. A. 1980; 77: 3870-3874Crossref PubMed Scopus (118) Google Scholar), suggesting that Ca2+ is not required for intra-Golgi transport, whereas based on evidence from semi-intact cells, Schwaninger et al.(9Schwaninger R. Beckers C.J. Balch W.E. J. Biol. Chem. 1991; 266: 13055-13063Abstract Full Text PDF PubMed Google Scholar) suggested that this cation is required at a late stage of transport within the Golgi. In this study we have characterized the requirement for calcium in transport within the Golgi. We present evidence that intra-Golgi transport require low free Ca2+ concentrations within the physiological range and that above a critical level (100 nm) Ca2+ has the reverse effect and inhibit transport. We thus show that free Ca2+ is required in a very narrow concentration range for this process and suggest a dual role for Ca2+ in intra-Golgi transport. In addition, we provide evidence that links CaM to the stimulatory effect of Ca2+ on transport. Rat brain cytosol was prepared essentially as described previously for bovine brain cytosol (15Porat A. Sagiv Y. Elazar Z. J. Biol. Chem. 2000; 275: 14457-14465Abstract Full Text Full Text PDF PubMed Scopus (100) Google Scholar). The standard intra-Golgi transport was performed as described previously (16Balch W.E. Dunphy W.G. Braell W.A. Rothman J.E. Cell. 1984; 39: 405-416Abstract Full Text PDF PubMed Scopus (479) Google Scholar). A standard intra-Golgi transport assay (25 μl) contained 2.5 mmHepes buffer, pH 7.0, 15 mm KCl, 2.5 mmmagnesium acetate, 0.4 μCi of UDP-[3H]N-acetylglucosamine, 5 μl of a 1:1 mixture of donor and acceptor Golgi membranes (2–3 μg of protein), 0.25 μl (30 ng) of His6αSNAP, 10 μm palmitoyl-coenzyme A, and ATP and UTP regenerating systems. Transport activity was dependent upon addition of cytosol, and in this study 27.5 μg of rat brain cytosol was added to achieve optimum conditions for the transport activity. The transport reactions were incubated at 30 °C for 2 h. [3H]N-Acetylglucosamine incorporated into VSV-G protein was determined as described previously (17Legesse-Miller A. Sagiv Y. Porat A. Elazar Z. J. Biol. Chem. 1998; 273: 3105-3109Abstract Full Text Full Text PDF PubMed Scopus (55) Google Scholar). Each of the transport assay experiments shown in this study represent at least three independent assays performed in duplicate. (Where standard errors are absent the results represent 3 independent experiments with duplicates. Standard errors did not exceed 5%.) For the glycosylation assay, “wild type donor” membranes were prepared as described by Taylor et al. (18Taylor T.C. Kanstein M. Weidman P. Melancon P. Mol. Biol. Cell. 1994; 5: 237-252Crossref PubMed Scopus (44) Google Scholar). Briefly Golgi membranes were isolated from wild type Chinese hampster ovary cells infected with VSV, after which the isolated “wild type donor” membranes were treated withN-ethylmaleimide (1 mm) for 15 min on ice, at which time dithiothreitol (2 mm) was added to quench any remaining N-ethylmaleimide. The glycosylation assay was performed under identical conditions as those described for the standard transport assay. The free cation concentrations were determined using the Bound and Determined (BAD) software (33Brooks S.P. Storey K.B. Anal. Biochem. 1992; 201: 119-126Crossref PubMed Scopus (324) Google Scholar). To address the role of Ca2+ in intra-Golgi transport we tested the effects of EGTA and BAPTA, two Ca2+chelators, on the well characterized cell-free intra-Golgi transport assay (16Balch W.E. Dunphy W.G. Braell W.A. Rothman J.E. Cell. 1984; 39: 405-416Abstract Full Text PDF PubMed Scopus (479) Google Scholar). Addition of increasing amounts of BAPTA inhibited transport with an IC50 of approximately 0.8 mm, whereas EGTA showed only a minimal effect (Fig.1 A). The inhibition of transport observed in the presence of BAPTA is not due to chelation of Mg2+ because a similar pattern was observed when BAPTA was added in the presence of 3 mm MgCl2. When BAPTA was added to the cell-free transport assay in the presence of an equivalent molar concentration of Ca2+, no inhibition was observed (Fig. 1 B). The different effects of these chelators on intra-Golgi transport cannot be explained by a different cation preference, because BAPTA and EGTA bind Ca2+ with a similar affinity at neutral pH. However, BAPTA has >100-fold higher ion association and dissociation rates than EGTA (19Tsien R.Y. Biochemistry. 1980; 19: 2396-2404Crossref PubMed Scopus (1689) Google Scholar). Thus, processes that are dependent on fast and local changes in Ca2+concentration will be sensitive to BAPTA but not to EGTA (20Hochner B. Parnas H. Parnas I. Neurosci. Lett. 1991; 125: 215-218Crossref PubMed Scopus (42) Google Scholar, 21Wang S.S. Thompson S.H. Biophys. J. 1995; 69: 1683-1697Abstract Full Text PDF PubMed Scopus (41) Google Scholar). The effect of BAPTA on intra-Golgi transport was fully reversible when the Golgi membranes were reisolated and incubated with fresh untreated cytosol (Fig. 1 C). However, when the membranes were incubated with BAPTA in the presence of 100 μm ionomycin, a Ca2+ ionophore that causes release of Ca2+from lumenal stores, fresh cytosol failed to restore transport. These results are consistent with the notion that low and transient Ca2+ effluxes, possibly from the Golgi membrane, are essential for intra-Golgi transport. To exclude the possibility that the inhibition of the assay signal by BAPTA resulted from decreased glycosylation activity of GlcNAc transferase rather than from inhibition of transport, we used a glycosylation assay that determines GlcNAc activity when membrane transport is inactivated (for details see “Experimental Procedures”). As shown in Fig. 1 D, neither BAPTA nor EGTA affected the glycosylation of VSV-G protein, indicating that BAPTA indeed exerts its effect on the process of intra-Golgi transport. To examine at which stage BAPTA acts in inhibiting intra-Golgi transport, we examined the effect of BAPTA when combined with two other inhibitors of transport (15Porat A. Sagiv Y. Elazar Z. J. Biol. Chem. 2000; 275: 14457-14465Abstract Full Text Full Text PDF PubMed Scopus (100) Google Scholar, 22Melancon P. Glick B.S. Malhotra V. Weidman P.J. Serafini T. Gleason M.L. Orci L. Rothman J.E. Cell. 1987; 51: 1053-1062Abstract Full Text PDF PubMed Scopus (299) Google Scholar). In the experiment described in Fig.2, the transport assay was either terminated at different time points by placing the reaction on ice, or at these time points the inhibitors BAPTA, anti-SBP56 antibodies, or GTPγS were added as indicated, and the reaction was allowed to proceed for 2 h. Control samples treated with buffer only were incubated likewise at 30° C until the end of the 2-h incubation period and served to represent 100% of transport activity. All three inhibitors, when added at the onset of the reaction, produced 90% inhibition of transport. The reaction became resistant to BAPTA after the inhibition by GTPγS and anti-SBP56 antibodies, indicating that Ca2+ is required late in the transport process, possibly at the fusion stage. It has been demonstrated that different organelles, including the Golgi apparatus, accumulate Ca2+ in their lumen (8Pinton P. Pozzan T. Rizzuto R. EMBO J. 1998; 17: 5298-5308Crossref PubMed Scopus (379) Google Scholar). To test the role of the lumenal Ca2+ pool in intra-Golgi transport, Golgi membranes were incubated in the presence of increasing concentrations of either ionomycin (a Ca2+ ionophore) or thapsigargin (a tumor-promoting sesquiterpene lactone that binds with high affinity and irreversibly inhibits all sarco/endoplasmic reticulum adenosine triphosphatase pumps). These two compounds are known to reduce lumenal Ca2+ levels selectively from intracellular organelles. As shown in Fig. 3, both ionomycin and thapsigargin inhibited intra-Golgi transport with IC50 values of 35 and 50 μm, respectively, with no effect on glycosylation by GlcNAc transferase. These results clearly indicated that lumenal Ca2+ was essential for this process. Having demonstrated that release of Ca2+ from intracellular stores may play a role in regulating transport, we examined the concentration of free Ca2+ required for intra-Golgi transport. For that purpose we added increasing CaCl2concentrations to the cell-free transport assay in the presence of 5 mm BAPTA or EGTA (Fig. 4,A and B). Interestingly addition of 100 nm free Ca2+ caused the assay signal to return to almost maximal levels (88% of the control determined in the absence of any Ca2+ chelator), but addition of higher free Ca2+ concentrations significantly inhibited the cell-free transport assay. When tested, neither Mn2+ nor Cu2+ was able to substitute Ca2+ (Fig.4 A). We then tested the inhibitory effect of Ca2+ using EGTA as cation chelator. Under these conditions the stimulatory effect of Ca2+ could not be observed. However, as found in the presence of BAPTA, free Ca2+concentrations above 100 nm inhibited transport, reaching a maximum effect at about 200 nm free Ca2+ (Fig. 4 B). These results clearly demonstrated that within the physiological range, Ca2+plays a dual role in regulating intra-Golgi transport. Furthermore, the ability of BAPTA but not EGTA to inhibit transport by chelating Ca2+ suggests that the effect of Ca2+ in regulating membrane fusion is localized to the vicinity of the membrane. A number of studies using endosomal fusion (12Colombo M.I. Beron W. Stahl P.D. J. Biol. Chem. 1997; 272: 7707-7712Abstract Full Text Full Text PDF PubMed Scopus (115) Google Scholar) or yeast vacuole homotypic fusion (11Peters C. Mayer A. Nature. 1998; 396: 575-580Crossref PubMed Scopus (324) Google Scholar) have demonstrated a requirement for the cytosolic Ca2+ effector, CaM. We therefore examined the involvement of CaM in intra-Golgi transport. For that purpose, increasing concentrations of two specific CaM inhibitors, W7 or trifluoperazine dimaleate, were added to the cell-free transport assay. As shown in Fig. 5 A, 25 μm either W7 or trifluoperazine dimaleate inhibited up to 90% of the total transport activity with an IC50 of about 10 μm. Addition of W5, a much weaker CaM antagonist, however, only partially inhibited transport (IC50 > 250 μm) thus indicating that the inhibition observed in the presence of the different antagonists is CaM-mediated. Notably, W7 or trifluoperazine dimaleate failed to significantly inhibit the glycosylation of VSV-G protein as determined by the glycosylation assay (data not shown). To further verify the involvement of CaM in this process, we performed a two-stage transport assay in which Golgi membranes were first treated with or without W7 (30 min on ice) in transport assay conditions. The membranes were then reisolated, washed, and tested for transport activity in the presence of fresh cytosol (Fig. 5 B). Addition of fresh cytosol to the control membranes recovered most of their transport activity, whereas W7-treated membranes could restore up to 90% of transport only when purified CaM was added together with the fresh cytosol. Hence, CaM appears to be involved in intra-Golgi transport. These results also indicate that the low levels of CaM in the cytosol are insufficient to reactivate the Golgi membranes after treatment with W7. CaM-dependent transport was strongly inhibited by BAPTA (Fig. 5 B) indicating that Ca2+ is required for the CaM activation of transport. It has been well demonstrated that Ca2+ regulates vesicular transport between a number of different intracellular organelles, but its involvement in intra-Golgi transport remains poorly understood. Here, we have investigated the role Ca2+ plays in this process by using the well established intra-Golgi transport assay. We found that low cytosolic Ca2+ concentrations (approximately 100 nm) are optimal for intra-Golgi transport whereas higher Ca2+ concentrations inhibit this process. Moreover, it appears that Ca2+ efflux from intracellular stores (possibly from the Golgi complex itself) is essential for intra-Golgi transport. Our results indicated that Ca2+ played a role in late stages of transport, possibly in the fusion of vesicles with their target membrane. Finally we demonstrate that CaM is involved in intra-Golgi transport. Several studies have documented that Ca2+ plays an important role in regulated exocytosis of secretory granules and synaptic vesicles (reviewed in Refs. 23Sudhof T.C. Nature. 1995; 375: 645-653Crossref PubMed Scopus (1761) Google Scholar and 24Scheller R.H. Neuron. 1995; 14: 893-897Abstract Full Text PDF PubMed Scopus (196) Google Scholar). More recently it was reported that Ca2+ participates in other intracellular transport events, including ER to Golgi transport (25Beckers C.J. Plutner H. Davidson H.W. Balch W.E. J. Biol. Chem. 1990; 265: 18298-18310Abstract Full Text PDF PubMed Google Scholar), assembly of nuclear membrane (10Sullivan K.M. Busa W.B. Wilson K.L. Cell. 1993; 73: 1411-1422Abstract Full Text PDF PubMed Scopus (121) Google Scholar), transcytotic vesicle fusion (26Barroso M.R. Bernd K.K. DeWitt N.D. Chang A. Mills K. Sztul E.S. J. Biol. Chem. 1996; 271: 10183-10187Abstract Full Text Full Text PDF PubMed Scopus (72) Google Scholar), vacuolar membrane fusion (11Peters C. Mayer A. Nature. 1998; 396: 575-580Crossref PubMed Scopus (324) Google Scholar), and fusion between endosomes (12Colombo M.I. Beron W. Stahl P.D. J. Biol. Chem. 1997; 272: 7707-7712Abstract Full Text Full Text PDF PubMed Scopus (115) Google Scholar, 13Holroyd C. Kistner U. Annaert W. Jahn R. Mol. Biol. Cell. 1999; 10: 3035-3044Crossref PubMed Scopus (71) Google Scholar). The requirement for Ca2+ in intra-Golgi transport has remained unclear, however, because early reports using a cell-free intra-Golgi transport assay demonstrated no effect of EGTA (14Fries E. Rothman J.E. Proc. Natl. Acad. Sci. U. S. A. 1980; 77: 3870-3874Crossref PubMed Scopus (118) Google Scholar), whereas in semi-intact cells, EGTA was able to inhibit this transport process (9Schwaninger R. Beckers C.J. Balch W.E. J. Biol. Chem. 1991; 266: 13055-13063Abstract Full Text PDF PubMed Google Scholar). In agreement with the early reports, we now show that intra-Golgi transport is indeed resistant to EGTA. However, this transport step is highly sensitive to the fast acting Ca2+ chelator, BAPTA. This phenomenon of sensitivity to BAPTA but resistance to EGTA has been observed for other systems of membrane fusion, including homotypic vacuolar fusion (11Peters C. Mayer A. Nature. 1998; 396: 575-580Crossref PubMed Scopus (324) Google Scholar) and endosomal fusion (13Holroyd C. Kistner U. Annaert W. Jahn R. Mol. Biol. Cell. 1999; 10: 3035-3044Crossref PubMed Scopus (71) Google Scholar). This suggests that transient, probably local, changes in Ca2+concentration mediate the fusion process. Indeed, our results (Fig. 3) are consistent with the notion that intra-Golgi transport depends upon Ca2+ efflux from inner membrane stores. Several studies have indicated that the Golgi complex may function as a Ca2+ storage organelle (8Pinton P. Pozzan T. Rizzuto R. EMBO J. 1998; 17: 5298-5308Crossref PubMed Scopus (379) Google Scholar, 27Lin P. Le-Niculescu H. Hofmeister R. McCaffery J.M. Jin M. Hennemann H. McQuistan T. De Vries L. Farquhar M.G. J. Cell Biol. 1998; 141: 1515-1527Crossref PubMed Scopus (138) Google Scholar, 28Lin P. Yao Y. Hofmeister R. Tsien R.Y. Farquhar M.G. J. Cell Biol. 1999; 145: 279-289Crossref PubMed Scopus (119) Google Scholar, 29Lin P. Fischer T. Weiss T. Farquhar M.G. Proc. Natl. Acad. Sci. U. S. A. 2000; 97: 674-679Crossref PubMed Scopus (55) Google Scholar). Thus it is feasible that Ca2+ from the lumen of the Golgi directly participated in regulating intra-Golgi transport. In most cells the free Ca2+ concentration rests at approximately 100 nm, and following activation of cellular signaling pathways Ca2+ levels are elevated about 1000-fold (30Augustine G.J. Charlton M.P. Smith S.J. Annu. Rev. Neurosci. 1987; 10: 633-693Crossref PubMed Google Scholar, 31Llinas R. Sugimori M. Silver R.B. Neuropharmacology. 1995; 34: 1443-1451Crossref PubMed Scopus (110) Google Scholar). We have found that intra-Golgi transport is optimal in the presence of about 100 nm free Ca2+, but that higher Ca2+ concentrations strongly inhibit transport. This may imply that constitutive membrane transport is optimal when the cytosolic Ca2+ concentration remain at resting levels, but is inhibited upon elevation of cytosolic Ca2+. Because exocytosis depends critically on high Ca2+ levels, this may provide a mechanism for the cell to conserve the fusion machinery for the transient and more immediate requirement of exocytosis at the expense of constitutive transport. What are the downstream targets of Ca2+ in this system? It has recently been demonstrated that the Ca2+-binding protein CaM plays an important role in fusion between yeast vacuoles (11Peters C. Mayer A. Nature. 1998; 396: 575-580Crossref PubMed Scopus (324) Google Scholar). It was postulated that CaM acts in this system at a late step of the fusion reaction, probably after docking of the transport vesicle with its target membrane (11Peters C. Mayer A. Nature. 1998; 396: 575-580Crossref PubMed Scopus (324) Google Scholar). CaM antagonists were found to inhibit endosome fusion in vitro (12Colombo M.I. Beron W. Stahl P.D. J. Biol. Chem. 1997; 272: 7707-7712Abstract Full Text Full Text PDF PubMed Scopus (115) Google Scholar). The strong inhibition of intra-Golgi transport by the CaM antagonist reported here suggests that CaM may regulate various intracellular fusion processes in a Ca2+-dependent manner. Recently Mayer and co-workers (32Peters C. Andrews P.D. Stark M.J. Cesaro-Tadic S. Glatz A. Podtelejnikov A. Mann M. Mayer A. Science. 1999; 285: 1084-1087Crossref PubMed Scopus (138) Google Scholar) suggested that protein phosphatase 1 may be involved in late stages of vacuolar fusion, possibly in a CaM-dependent manner. Future studies will determine whether protein phosphatase 1 or another target represents the effector of Ca2+ in constitutive membrane transport and how this effector acts on the transport machinery. We thank Simone Fishburn for critical reading of the manuscript and for stimulating discussions." @default.
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• W2025033557 title "Regulation of Intra-Golgi Membrane Transport by Calcium" @default.
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