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In Vitro Fusion Catalyzed By The Sporulation‐Specific T‐SNARE Light‐Chain Spo20p Is Stimulated By Phosphatidic Acid

Song Liu, K. A. Wilson, Travis Rice-Stitt, A. Neiman, J. McNew
Published 2007 · Biology, Medicine

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Sec9p and Spo20p are two SNAP25 family SNARE proteins specialized for different developmental stages in yeast. Sec9p interacts with Sso1/2p and Snc1/2p to mediate intracellular trafficking between post‐Golgi vesicles and the plasma membrane during vegetative growth. Spo20p replaces Sec9p in the generation of prospore membranes during sporulation. The function of Spo20p requires enzymatically active Spo14p, which is a phosphatidylcholine (PC)‐specific phospholipase D that hydrolyzes PC to generate phosphatidic acid (PA). Phosphatidic acid is required to localize Spo20p properly during sporulation; however, it seems to have additional roles that are not fully understood. Here we compared the fusion mediated by all combinations of the Sec9p or Spo20p C‐terminal domains with Sso1p/Sso2p and Snc1p/Snc2p. Our results show that Spo20p forms a less efficient SNARE complex than Sec9p. The combination of Sso2p/Spo20c is the least fusogenic t‐SNARE complex. Incorporation of PA in the lipid bilayer stimulates SNARE‐mediated membrane fusion by all t‐SNARE complexes, likely by decreasing the energetic barrier during membrane merger. This effect may allow the weak SNARE complex containing Spo20p to function during sporulation. In addition, PA can directly interact with the juxtamembrane region of Sso1p, which contributes to the stimulatory effects of PA on membrane fusion. Our results suggest that the fusion strength of SNAREs, the composition of organelle lipids and lipid–SNARE interactions may be coordinately regulated to control the rate and specificity of membrane fusion.
This paper references
10.1128/JB.173.6.2026-2034.1991
Phospholipid synthesis and lipid composition of subcellular membranes in the unicellular eukaryote Saccharomyces cerevisiae.
E. Zinser (1991)
10.1007/978-3-642-16483-5_4540
[Phospholipase D].
T. Taki (1986)
10.1126/SCIENCE.1129450
A Clamping Mechanism Involved in SNARE-Dependent Exocytosis
C. Giraudo (2006)
10.1083/JCB.140.1.29
Prospore Membrane Formation Defines a Developmentally Regulated Branch of the Secretory Pathway in Yeast
A. Neiman (1998)
10.1002/j.1460-2075.1993.tb06093.x
Yeast syntaxins Sso1p and Sso2p belong to a family of related membrane proteins that function in vesicular transport.
M. Aalto (1993)
Determination and analysis of urea and guanidine hydrochloride denaturation curves. Methods Enzymol 1986;131:266–280
CN Pace (1986)
10.1385/1-59259-175-2:61
Lipids in viral fusion.
A. Puri (2002)
10.1023/A:1010402819509
Mechanisms of Initiation of Membrane Fusion: Role of Lipids
P. Kinnunen (2000)
10.1126/SCIENCE.1066015
Phosphatidic Acid-Mediated Mitogenic Activation of mTOR Signaling
Y. Fang (2001)
10.1083/jcb.200507138
An intramolecular t-SNARE complex functions in vivo without the syntaxin NH2-terminal regulatory domain
Jeffrey S. Van Komen (2006)
10.1073/PNAS.96.22.12565
Rapid and efficient fusion of phospholipid vesicles by the alpha-helical core of a SNARE complex in the absence of an N-terminal regulatory domain.
F. Parlati (1999)
10.1074/jbc.M601778200
Lipidic Antagonists to SNARE-mediated Fusion*
T. J. Melia (2006)
10.1038/nsmb1124
Hemifusion arrest by complexin is relieved by Ca2+–synaptotagmin I
Johanna R. Schaub (2006)
10.1126/stke.2002.129.pl6
Protein Lipid Overlay Assay
S. Dowler (2002)
10.1016/0092-8674(80)90128-2
Identification of 23 complementation groups required for post-translational events in the yeast secretory pathway
P. Novick (1980)
10.1073/PNAS.0400271101
The specificity of SNARE-dependent fusion is encoded in the SNARE motif.
F. Paumet (2004)
10.1073/pnas.082100899
Distinct SNARE complexes mediating membrane fusion in Golgi transport based on combinatorial specificity
F. Parlati (2002)
10.1074/jbc.M506862200
Membrane Fusion Induced by Neuronal SNAREs Transits through Hemifusion*[boxs]
Xiaobing Lu (2005)
10.1128/EC.4.12.2017-2028.2005
The Polybasic Juxtamembrane Region of Sso1p Is Required for SNARE Function In Vivo
Jeffrey S. Van Komen (2005)
10.1534/genetics.166.1.89
Genetic Evidence of a Role for Membrane Lipid Composition in the Regulation of Soluble NEM-Sensitive Factor Receptor Function in Saccharomyces cerevisiae
A. Coluccio (2004)
10.1016/0003-2697(73)90217-0
A rapid, sensitive, and specific method for the determination of protein in dilute solution.
W. Schaffner (1973)
10.1038/1834
Regulation of SNARE complex assembly by an N-terminal domain of the t-SNARE Sso1p
K. Nicholson (1998)
10.1016/0092-8674(94)90194-5
Sec9 is a SNAP-25-like component of a yeast SNARE complex that may be the effector of Sec4 function in exocytosis
P. Brennwald (1994)
10.1083/jcb.200501093
SNAREs can promote complete fusion and hemifusion as alternative outcomes
C. Giraudo (2005)
10.1034/j.1600-0854.2003.00086.x
Modulation of Membrane Curvature by Phosphatidic Acid and Lysophosphatidic Acid
E. E. Kooijman (2003)
10.1016/S0962-8924(98)01285-9
A model for structural similarity between different SNARE complexes based on sequence relationships.
T. Weimbs (1998)
10.1016/0896-6273(89)90193-1
A synaptic vesicle membrane protein is conserved from mammals to Drosophila
T. Südhof (1989)
10.1038/5803
Folding intermediates of SNARE complex assembly
K. Fiebig (1999)
10.1038/sj.embor.7400935
Mechanism of arachidonic acid action on syntaxin–Munc18
E. Connell (2007)
10.1016/0092-8674(93)90465-3
Homologs of the synaptobrevin/VAMP family of synaptic vesicle proteins function on the late secretory pathway in S. cerevisiae
V. Protopopov (1993)
10.1242/jcs.02841
Phospholipase D and the SNARE Sso1p are necessary for vesicle fusion during sporulation in yeast
H. Nakanishi (2006)
10.1038/35080071
How proteins move lipids and lipids move proteins
H. Sprong (2001)
10.1016/j.cell.2006.12.016
Selective Activation of Cognate SNAREpins by Sec1/Munc18 Proteins
J. Shen (2007)
10.1083/JCB.146.4.741
Electrospray Ionization Tandem Mass Spectrometry (Esi-Ms/Ms) Analysis of the Lipid Molecular Species Composition of Yeast Subcellular Membranes Reveals Acyl Chain-Based Sorting/Remodeling of Distinct Molecular Species En Route to the Plasma Membrane
R. Schneiter (1999)
10.1091/MBC.E05-03-0243
Molecular interactions position Mso1p, a novel PTB domain homologue, in the interface of the exocyst complex and the exocytic SNARE machinery in yeast.
M. Knop (2005)
10.1016/J.CHEMBIOL.2005.03.004
Arachidonic acid allows SNARE complex formation in the presence of Munc18.
C. Rickman (2005)
Characterization of temperature-sensitive mutations in the yeast syntaxin 1 homologues Sso1p and Sso2p, and evidence of a distinct function for Sso1p in sporulation.
J. Jaentti (2002)
10.1016/S0092-8674(00)81404-X
SNAREpins: Minimal Machinery for Membrane Fusion
T. Weber (1998)
MEASURING THE CONFORMATIONAL STABILITY OF PROTEINS
Sushma Yadav (1992)
10.1038/79659
Interactions within the yeast t-SNARE Sso1p that control SNARE complex assembly
M. Munson (2000)
10.1126/SCIENCE.1589771
Synaptotagmin: a calcium sensor on the synaptic vesicle surface.
N. Brose (1992)
10.1016/S0076-6879(03)72016-3
Liposome fusion assay to monitor intracellular membrane fusion machines.
B. L. Scott (2003)
10.1038/362318A0
SNAP receptors implicated in vesicle targeting and fusion
T. Söllner (1993)
10.1021/BI00421A014
Unfolding free energy changes determined by the linear extrapolation method. 1. Unfolding of phenylmethanesulfonyl alpha-chymotrypsin using different denaturants.
M. M. Santoro (1988)
10.1016/S0014-5793(02)03483-X
The role of phosphatidic acid in the regulation of the Ras/MEK/Erk signaling cascade
B. T. Andresen (2002)
10.1038/35025000
Compartmental specificity of cellular membrane fusion encoded in SNARE proteins
J. McNew (2000)
10.1126/SCIENCE.1321498
Syntaxin: a synaptic protein implicated in docking of synaptic vesicles at presynaptic active zones.
M. Bennett (1992)
10.1016/0076-6879(86)31045-0
Determination and analysis of urea and guanidine hydrochloride denaturation curves.
C. Pace (1986)
Identification of domains required for developmentally regulated SNARE function in Saccharomyces cerevisiae.
A. Neiman (2000)
10.1091/MBC.E03-04-0245
Roles of phosphoinositides and of Spo14p (phospholipase D)-generated phosphatidic acid during yeast sporulation.
S. Rudge (2004)
10.1038/26412
Crystal structure of a SNARE complex involved in synaptic exocytosis at 2.4 Å resolution
R B Sutton (1998)
10.1083/jcb.200112081
Regulation of membrane fusion by the membrane-proximal coil of the t-SNARE during zippering of SNAREpins
T. J. Melia (2002)
10.1007/s00294-003-0462-8
Mapping of sporulation-specific functions in the yeast syntaxin gene SSO1
Mattias Öyen (2003)
10.1091/MBC.E03-11-0798
Positive and negative regulation of a SNARE protein by control of intracellular localization.
H. Nakanishi (2004)
10.1016/0005-2736(91)90295-J
Small-volume extrusion apparatus for preparation of large, unilamellar vesicles.
R. Macdonald (1991)
10.1091/MBC.12.6.1611
SPO21 is required for meiosis-specific modification of the spindle pole body in yeast.
B. K. Bajgier (2001)
10.1128/EC.2.3.431-445.2003
Ady4p and Spo74p Are Components of the Meiotic Spindle Pole Body That Promote Growth of the Prospore Membrane in Saccharomyces cerevisiae
M. Nickas (2003)
10.1093/emboj/17.21.6200
Genetic and morphological analyses reveal a critical interaction between the C‐termini of two SNARE proteins and a parallel four helical arrangement for the exocytic SNARE complex
L. Katz (1998)
10.1083/JCB.150.1.105
Close is not enough: SNARE-dependent membrane fusion requires an active mechanism that transduces force to membrane anchors.
J. McNew (2000)
10.1083/JCB.109.6.3039
The identification of a novel synaptosomal-associated protein, SNAP-25, differentially expressed by neuronal subpopulations
G. Oyler (1989)
10.1083/JCB.140.1.81
Relocalization of Phospholipase D Activity Mediates Membrane Formation During Meiosis
S. Rudge (1998)
10.1091/MBC.E04-12-1124
Insulin-stimulated plasma membrane fusion of Glut4 glucose transporter-containing vesicles is regulated by phospholipase D1.
P. Huang (2005)
10.1093/emboj/19.14.3657
Role of the spindle pole body of yeast in mediating assembly of the prospore membrane during meiosis
M. Knop (2000)
10.1074/JBC.M403012200
Phospholipase D1 Regulates Secretagogue-stimulated Insulin Release in Pancreatic β-Cells*
W. E. Hughes (2004)
Measuring the conformational stability of a protein. In: Creighton TE, editor. Protein Structure: A Practical Approach
CN Pace (1990)
10.1101/87969139.11A.211
Meiosis and Ascospore Development
R. E. Esposito (1981)
10.1016/S0968-0004(97)01097-9
PKB/Akt: connecting phosphoinositide 3-kinase to cell survival and beyond.
B. M. Marte (1997)
10.1128/MMBR.69.4.565-584.2005
Ascospore Formation in the Yeast Saccharomyces cerevisiae
A. Neiman (2005)
10.1016/S1097-2765(00)80343-3
The length of the flexible SNAREpin juxtamembrane region is a critical determinant of SNARE-dependent fusion.
J. McNew (1999)
10.1021/BI025934+
The membrane-dipped neuronal SNARE complex: a site-directed spin labeling electron paramagnetic resonance study.
Dae-Hyuk Kweon (2002)



This paper is referenced by
10.1146/annurev-cellbio-100109-104131
Membrane fusion: five lipids, four SNAREs, three chaperones, two nucleotides, and a Rab, all dancing in a ring on yeast vacuoles.
W. Wickner (2010)
10.1111/tra.12423
Phosphatidic Acid Sequesters Sec18p from cis‐SNARE Complexes to Inhibit Priming
Matthew L. Starr (2016)
10.1016/j.bbalip.2009.01.013
Phospholipase D function in Saccharomyces cerevisiae.
R. Mendonsa (2009)
10.1073/pnas.0908694106
Phosphoinositides and SNARE chaperones synergistically assemble and remodel SNARE complexes for membrane fusion
J. Mima (2009)
10.1128/EC.00076-09
Phosphatidylinositol-4,5-Bisphosphate and Phospholipase D-Generated Phosphatidic Acid Specify SNARE-Mediated Vesicle Fusion for Prospore Membrane Formation
R. Mendonsa (2009)
10.1007/978-3-211-76310-0_16
Functional cross talk between membrane trafficking and cell signalling
M. Sallese (2008)
Regulation of membrane fusion by Tlg2p & Vps45p through the endosomal system of Saccharomyces cerevisiae
C. MacDonald (2009)
10.1271/bbb.80265
Manipulation of Major Membrane Lipid Synthesis and Its Effects on Sporulation in Saccharomyces cerevisiae
L. Deng (2008)
10.1016/j.bbalip.2009.03.013
Emerging findings from studies of phospholipase D in model organisms (and a short update on phosphatidic acid effectors).
P. Raghu (2009)
10.1074/jbc.M111.307439
Distinct Contributions of Vacuolar Qabc- and R-SNARE Proteins to Membrane Fusion Specificity*
R. Izawa (2011)
10.1111/j.1469-8137.2009.02880.x
Exocytosis and cell polarity in plants - exocyst and recycling domains.
V. Žárský (2009)
10.3389/fcell.2019.00083
Regulation of Membrane Turnover by Phosphatidic Acid: Cellular Functions and Disease Implications
R. Thakur (2019)
10.1042/EBC20190089
Phosphatidic acid: an emerging versatile class of cellular mediators.
Sang-Chul Kim (2020)
Copyright 2014 Colin Stoy THE ROLE OF THE DGK1 AND PAH1 IN LIPID INTERCONVERSION ON SACCHAROMYCES CEREVISIAE VACUOLE PHYSIOLOGY, HOMEOSTASIS, PROTEIN SORTING AND FUSION BY
Colin Stoy (2014)
10.1101/2020.05.04.074880
Direct PA-binding by Chm7 is required for nuclear envelope surveillance at herniations
David J. Thaller (2020)
Rôle de l'estérification des acides gras dans la régulation de la sécrétion d'insuline et le stress métabolique induits par le glucose
A. Barbeau (2012)
10.3389/fpls.2018.00371
Gene Expression Pattern and Protein Localization of Arabidopsis Phospholipase D Alpha 1 Revealed by Advanced Light-Sheet and Super-Resolution Microscopy
D. Novak (2018)
10.1534/genetics.111.127126
Sporulation in the Budding Yeast Saccharomyces cerevisiae
A. Neiman (2011)
10.3390/ijms21186794
New Era of Diacylglycerol Kinase, Phosphatidic Acid and Phosphatidic Acid-Binding Protein
F. Sakane (2020)
10.1101/365775
Phosphatidic acid inhibits SNARE priming by inducing conformational changes in Sec18 protomers
Matthew L. Starr (2018)
10.3389/fcell.2020.00700
Tubular ER Associates With Diacylglycerol-Rich Structures During Lipid Droplet Consumption
Suriakarthiga Ganesan (2020)
10.1007/978-94-007-3015-1_4
Role of PI(4,5)P(2) in vesicle exocytosis and membrane fusion.
T. Martin (2012)
10.1091/mbc.E08-05-0538
Munc18a scaffolds SNARE assembly to promote membrane fusion.
Travis L. Rodkey (2008)
10.1074/jbc.M111.317420
Yeast Lipin 1 Orthologue Pah1p Regulates Vacuole Homeostasis and Membrane Fusion*
Terry L Sasser (2011)
10.1111/tra.12632
Metabolic control of cytosolic‐facing pools of diacylglycerol in budding yeast
Suriakarthiga Ganesan (2019)
10.1016/j.celrep.2020.02.102
Phospholipase D1 Ablation Disrupts Mouse Longitudinal Hippocampal Axis Organization and Functioning.
Luísa Santa-Marinha (2020)
10.4137/LPI.S31781
Tracking Diacylglycerol and Phosphatidic Acid Pools in Budding Yeast
Suriakarthiga Ganesan (2015)
10.1074/jbc.M109.010223
Complex Lipid Requirements for SNARE- and SNARE Chaperone-dependent Membrane Fusion*
J. Mima (2009)
10.1111/tra.12064
The Lipid Composition and Physical Properties of the Yeast Vacuole Affect the Hemifusion–Fusion Transition
Surya Karunakaran (2013)
10.1083/jcb.201011118
α-Synuclein and ALPS motifs are membrane curvature sensors whose contrasting chemistry mediates selective vesicle binding
I. Pranke (2011)
10.1111/j.1600-0854.2008.00742.x
Molecular Mechanisms of PLD Function in Membrane Traffic
M. Roth (2008)
10.1074/jbc.RA118.006552
Phosphatidic acid induces conformational changes in Sec18 protomers that prevent SNARE priming
Matthew L. Starr (2019)
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