Role of p97 and Syntaxin 5 in the Assembly of Transitional Endoplasmic Reticulum

Roy, Line; Bergeron, John J.M.; Lavoie, Christine; Hendriks, Rob; Gushue, Jennifer N.; Fazel, Ali; Pelletier, Amélie; Morré, D. James; Subramaniam, V. Nathan; Hong, Wanjin; Paiement, Jacques

doi:10.1091/mbc.11.8.2529

Cited by 99 publications

(100 citation statements)

References 61 publications

(108 reference statements)

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“…p97 participates in reassembly of ilimaquinone dispersed Golgi membranes into Golgi stacks (Acharya et al, 1995), reformation of unfenestrated Golgi cisternae from mitotic Golgi fragments (Rabouille et al, 1995(Rabouille et al, , 1998, fusion of yeast ER membranes (Latterich et al, 1995;Lin et al, 2001), formation but not maintenance of tubulated ER from low-density microsomes Roy et al, 2000), and formation and growth of the nuclear envelope and associated ER network (Hetzer et al, 2001). These in vitro assays all reconstitute complex processes related to organelle assembly.…”

Section: P97 and Membrane Fusionmentioning

confidence: 86%

“…To test the possibility that p97 might be more specifically involved in trafficking between ER and Golgi (Zhang et al, 1994;Roy et al, 2000), we monitored the delivery of GFPtagged VSV-G ts045 protein from the ER to the cell surface in individual cells (Presley et al, 1997). Regardless of whether p97(E578Q) was expressed or not, transferring the cells from nonpermissive to permissive temperature allowed movement of VSV-G ts045 from ER to Golgi and then to the cell surface ( Figure 8C), except in cells in which the ER was fully vacuolated and thereby occupying most of the cell's volume.…”

Section: Effects Of Inhibiting Nsf and P97 On Secretory Pathway Functionmentioning

confidence: 99%

“…However, because p97 has most clearly been implicated in organelle assembly reactions reconstituted in vitro (Acharya et al, 1995;Latterich et al, 1995;Rabouille et al, 1995;Roy et al, 2000;Hetzer et al, 2001), we specifically asked whether p97(E578Q) expression affects de novo organelle assembly in vivo. Both p97 and NSF are needed to form Golgi stacks from mitotic Golgi fragments in vitro (Rabouille et al, 1995).…”

Section: Effects Of P97(e578q) On Golgi Reassembly In Vivomentioning

confidence: 99%

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Distinct Roles for the AAA ATPases NSF and p97 in the Secretory Pathway

Dalal

Rosser

Cyr

et al. 2004

MBoC

166

176

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NSF and p97 are related AAA proteins implicated in membrane trafficking and organelle biogenesis. p97 is also involved in pathways that lead to ubiquitin-dependent proteolysis, including ER-associated degradation (ERAD). In this study, we have used dominant interfering ATP-hydrolysis deficient mutants (NSF(E329Q) and p97(E578Q)) to compare the function of these AAA proteins in the secretory pathway of mammalian cells. Expressing NSF(E329Q) promotes disassembly of Golgi stacks into dispersed vesicular structures. It also rapidly inhibits glycosaminoglycan sulfation, reflecting disruption of intra-Golgi transport. In contrast, expressing p97(E578Q) does not affect Golgi structure or function; glycosaminoglycans are normally sulfated and secreted, as is the VSV-G ts045 protein. Instead, expression of p97(E578Q) causes ubiquitinated proteins to accumulate on ER membranes and slows degradation of the ERAD substrate cystic-fibrosis transmembrane-conductance regulator. In addition, expression of p97(E578Q) eventually causes the ER to swell. More specific assessment of effects of p97(E578Q) on organelle assembly shows that the Golgi apparatus disperses and reassembles normally after treatment with brefeldin A and during mitosis. These findings demonstrate that ATPhydrolysis-dependent activities of NSF and p97 in the cell are not equivalent and suggest that only NSF is directly involved in regulating membrane fusion. INTRODUCTIONMembrane fusion is an essential step in all forms of vesicle trafficking and organelle assembly. Fusion is driven by a series of regulated protein-protein interactions. Many participating proteins have been identified, and their specific roles are gradually coming to light (reviewed in Jahn et al., 2003). Among these proteins are a number of ATPases.N-ethyl maleimide sensitive factor (NSF) was one of the first proteins specifically linked to membrane fusion (Wilson et al., 1989). It belongs to a family of chaperone-like ATPases known as AAA (ATPases associated with a variety of cellular activities) proteins (Neuwald et al., 1999). NSF together with ␣-SNAP (soluble NSF attachment protein) dissociates the SNARE (SNAP receptor) complexes that promote association and fusion of cellular membranes. More recently, NSF has also been implicated in other cellular processes on the basis of its ability to bind the AMPA receptor GluR2, ␤-arrestin 1, and GATE-16 (reviewed in Whiteheart et al., 2001). However, its role in SNARE disassembly and membrane fusion remains its best understood function.Not all ATP-requiring steps that lead to membrane fusion can be attributed to NSF (Goda and Pfeffer, 1991;Latterich and Schekman, 1994;Rodriguez et al., 1994;Wilson, 1995).Other ATPases must therefore be involved. One AAA protein thought to be an alternate to NSF is known as p97 (also referred to as valosin-containing protein, VCP). p97 is an abundant and highly conserved protein (Peters et al., 1990) whose cellular function has been the subject of much debate. A break in the mystery of p97's function came when it turn...

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Section: P97 and Membrane Fusionmentioning

confidence: 86%

Section: Effects Of Inhibiting Nsf and P97 On Secretory Pathway Functionmentioning

confidence: 99%

Section: Effects Of P97(e578q) On Golgi Reassembly In Vivomentioning

confidence: 99%

See 1 more Smart Citation

Distinct Roles for the AAA ATPases NSF and p97 in the Secretory Pathway

Dalal

Rosser

Cyr

et al. 2004

MBoC

166

176

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“…SNAREs are not only involved in the heterotypic fusion of secretory vesicles with their appropriate acceptor compartment but also function in the homotypic fusion of like-like membranes such as vacuoles (Nichols et al, 1997) and ER-membranes (Patel et al, 1998;Roy et al, 2000). In contrast to Sec18p/NSFdependent homotypic yeast (Saccharomyces cerevisiae) vacuolar fusion, homotypic yeast ER, and animal transitional-ER (t-ER) fusion is dependent on Cdc48p/ p97 and its interaction with the t-SNAREs Ufe1p and Sed5p/syntaxin 5, respectively (Latterich et al, 1995;Roy et al, 2000).…”

mentioning

confidence: 99%

“…In contrast to Sec18p/NSFdependent homotypic yeast (Saccharomyces cerevisiae) vacuolar fusion, homotypic yeast ER, and animal transitional-ER (t-ER) fusion is dependent on Cdc48p/ p97 and its interaction with the t-SNAREs Ufe1p and Sed5p/syntaxin 5, respectively (Latterich et al, 1995;Roy et al, 2000). Interestingly, Ufe1p and Sed5p/ syntaxin 5 have dual roles: (a) ER-ER homotypic fusion required for ER biogenesis and maintenance, and (b) heterotypic fusion of early secretory compartment (i.e.…”

mentioning

confidence: 99%

Characterization of AtCDC48. Evidence for Multiple Membrane Fusion Mechanisms at the Plane of Cell Division in Plants

Dickey²,

et al. 2002

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The components of the cellular machinery that accomplish the various complex and dynamic membrane fusion events that occur at the division plane during plant cytokinesis, including assembly of the cell plate, are not fully understood. The most well-characterized component, KNOLLE, a cell plate-specific soluble N-ethylmaleimide-sensitive fusion protein (NSF)-attachment protein receptor (SNARE), is a membrane fusion machine component required for plant cytokinesis. Here, we show the plant ortholog of Cdc48p/p97, AtCDC48, colocalizes at the division plane in dividing Arabidopsis cells with KNOLLE and another SNARE, the plant ortholog of syntaxin 5, SYP31. In contrast to KNOLLE, SYP31 resides in defined punctate membrane structures during interphase and is targeted during cytokinesis to the division plane. In vitro-binding studies demonstrate that AtCDC48 specifically interacts in an ATP-dependent manner with SYP31 but not with KNOLLE. In contrast, we show that KNOLLE assembles in vitro into a large approximately 20S complex in an Sec18p/NSF-dependent manner. These results suggest that there are at least two distinct membrane fusion pathways involving Cdc48p/p97 and Sec18p/NSF that operate at the division plane to mediate plant cytokinesis. Models for the role of AtCDC48 and SYP31 at the division plane will be discussed.Plant cell division is completed by the highly dynamic process of de novo cell plate construction leading to the separation of two daughter cells. Formation of this unique cytokinetic organelle involves at least three key membrane fusion steps: (a) fusion of secretory vesicles across the division plane to form a membranous tubular-vesicular network, (b) consolidation of the tubular-vesicular network, and (c) fusion of the cell plate leading-edge with the original parental plasma membrane to complete division (Samuels et al., 1995). These distinct stages of cell plate biogenesis likely involve both heterotypic and homotypic membrane fusion events. In addition to the cell plate, the division plane contains an extensive endoplasmic reticulum (ER) network that has been suggested to function in the formation of the cell plate (Hepler, 1982). Assembly of cell plateassociated ER is likely to involve homotypic fusion of ER membrane within the division plane.Two homologous classes of ATPases associated with various cellular activities (AAA) proteins (Frö hlich, 2001), Sec18p N-ethylmaleimide-sensitive fusion protein (NSF) and Cdc48p/p97 (p97 is also known as VCP), regulate a variety of secretory membrane fusion processes (Acharya et al., 1995;Latterich et al., 1995;Rabouille et al., 1995). Monomers of Sec18p/NSF and Cdc48p/p97 consist of two Mg 2ϩ -dependent ATPase domains and an N-terminal substrate/adapter domain that assemble into biologically active ring-shaped oligohexamers (Peters et al., 1990; Hanson et al., 1997). Of these two AAA complexes, the biochemical function of Sec18p/NSF, which along with its cofactor, soluble NSF-attachment protein (␣-SNAP) regulates hetero-and homotypic membrane fusion, has...

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Proteomics of rat liver Golgi complex: Minor proteins are identified through sequential fractionation

Taylor

Hays

et al. 2000

Electrophoresis

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The discovery of novel proteins resident to the Golgi complex will fuel our future studies of Golgi structure/function and provide justification for proteomic analysis of this organelle. Our approach to Golgi proteomics was to first isolate and characterize the intact organelle free of proteins in transit by use of tissue pretreated with cycloheximide. Then the stacked Golgi fraction was fractionated into biochemically defined subfractions: Triton X-114 insoluble, aqueous, and detergent phases. The aqueous and detergent phases were further fractionated by anion-exchange column chromatography. In addition, radiolabeled cytosol was incubated with stacked Golgi fractions containing proteins in transit, and the proteins bound to the Golgi stacks in an energy-dependent manner were characterized. All fractions were analyzed by two-dimensional (2-D) gel electrophoresis and identification numbers were given to 588 unique 2-D spots. Tandem mass spectrometry was used to analyze 93 of the most abundant 2-D spots taken from preparative Triton X-114 insoluble, aqueous and detergent phase 2-D gels. Fifty-one known and 22 unknown proteins were identified. This study represents the first installment in the mammalian Golgi proteome database. Our data suggest that cell fractionation followed by biochemical dissection of specific classes of molecules provides a significant advantage for the identification of low abundance proteins in organelles.

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Role of p97 and Syntaxin 5 in the Assembly of Transitional Endoplasmic Reticulum

Cited by 99 publications

References 61 publications

Distinct Roles for the AAA ATPases NSF and p97 in the Secretory Pathway

Distinct Roles for the AAA ATPases NSF and p97 in the Secretory Pathway

Characterization of AtCDC48. Evidence for Multiple Membrane Fusion Mechanisms at the Plane of Cell Division in Plants

Proteomics of rat liver Golgi complex: Minor proteins are identified through sequential fractionation

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