Phospholipase D and the SNARE Sso1p are necessary for vesicle fusion during sporulation in yeast

Nakanishi, Hideki; Morishita, Masaki; Schwartz, Cindi L.; Coluccio, Alison; Engebrecht, JoAnne; Neiman, Aaron M.

doi:10.1242/jcs.02841

Cited by 110 publications

(152 citation statements)

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“…Since these proteins are involved in vesicle fusion during PSM formation (Riedel et al 2005;Nakanishi et al 2006), it is likely that Ssp2 also plays a role in vesicle fusion. As noted in the Introduction, Spo14 in both initiation and expansion of the PSM (Riedel et al 2005;Nakanishi et al 2006). Similarly, Ssp2 could act at both steps.…”

Section: Resultsmentioning

confidence: 99%

“…Spo14 is essential during sporulation, and it localizes to PSMs (Rose et al 1995). The phenotype of a spo14 null mutant is similar to that of the sso1 and sec9 spo20 mutants, indicating that Spo14 also participates in vesicle fusion (Riedel et al 2005;Nakanishi et al 2006). Studies of nonnull alleles of SPO14 and of mutations affecting the Spo14-interacting protein, Sma1, indicate that Spo14 acts at two discrete steps in PSM formation: the initial fusion of vesicles on the meiotic plaque and subsequent enlargement of the PSM to surround the adjoining nucleus (Riedel et al 2005;Nakanishi et al 2006).…”

mentioning

confidence: 93%

“…Sec9 is essential for secretion in vegetative cells, but it plays only a minor role during sporulation, where its function is largely replaced by the 1 sporulation-specific Sec9 homolog, Spo20 (Neiman 1998). In the sso1 mutant or in the sec9 spo20 double mutant, secretory vesicles accumulate near the meiotic plaque, but fail to coalesce to form a membrane sheet (Nakanishi et al 2006).…”

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confidence: 99%

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SSP2 and OSW1, Two Sporulation-Specific Genes Involved in Spore Morphogenesis in Saccharomyces cerevisiae

Agarwal

Roeder

2007

Genetics

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Spore formation in Saccharomyces cerevisiae requires the synthesis of prospore membranes (PSMs) followed by the assembly of spore walls (SWs). We have characterized extensively the phenotypes of mutants in the sporulation-specific genes, SSP2 and OSW1, which are required for spore formation. A striking feature of the osw1 phenotype is asynchrony of spore development, with some spores displaying defects in PSM formation and others spores in the same ascus blocked at various stages in SW development. The Osw1 protein localizes to spindle pole bodies (SPBs) during meiotic nuclear division and subsequently to PSMs/SWs. We propose that Osw1 performs a regulatory function required to coordinate the different stages of spore morphogenesis. In the ssp2 mutant, nuclei are surrounded by PSMs and SWs; however, PSMs and SWs often also encapsulate anucleate bodies both inside and outside of spores. In addition, the SW is not as thick as in wild type. The ssp2 mutant defect is partially suppressed by overproduction of either Spo14 or Sso1, both of which promote the fusion of vesicles at the outer plaque of the SPB early in PSM formation. We propose that Ssp2 plays a role in vesicle fusion during PSM formation.S PORULATION in the budding yeast, Saccharomyces cerevisiae, involves two overlapping processesmeiosis and spore morphogenesis. During meiosis, a diploid cell undergoes a single round of DNA replication, followed by two rounds of chromosome segregation, to generate four haploid nuclei. During spore morphogenesis, the four daughter nuclei are packaged into spores, which are contained within an ascus.Spore morphogenesis (reviewed by Neiman 2005) initiates with enlargement of the outer surface of the spindle pole body (SPB) to form the meiotic outer plaque. As cells undergo meiosis II, vesicles coalesce on the meiotic plaque to form a novel intracellular membrane called the prospore membrane (PSM). The doublelayered PSM extends outward from each SPB to surround the adjacent nucleus. When the leading edges of the PSM meet and become fused, the haploid nucleus is fully encapsulated to form a prospore. PSM closure triggers the final step of spore morphogenesis, spore wall (SW) formation. The SW is assembled between the two membranes of the PSM and consists of four layers. The two inner layers are composed of glucan and mannan, which are components of vegetative cell walls.

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Section: Resultsmentioning

confidence: 99%

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confidence: 93%

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confidence: 99%

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SSP2 and OSW1, Two Sporulation-Specific Genes Involved in Spore Morphogenesis in Saccharomyces cerevisiae

Agarwal

Roeder

2007

Genetics

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“…In yeast, PLD ortholog, Spo14, was shown to be necessary for membrane fusion during the formation of prospore membranes. 18 More recently, in yeast strain Pichia pastoris, Spo14 has been implicated in unconventional exocytosis of Acb1, and the process involves the fusion of APs with the plasma membrane. 19 PLD catalyzes the removal of choline from PC, generating PA, that could then serve as a precursor for the production of diacylglycerol (DAG).…”

Section: Discussionmentioning

confidence: 99%

Phospholipase D1 regulates autophagic flux and clearance of α-synuclein aggregates

et al. 2014

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Many neurodegenerative diseases, such as Alzheimer's disease and Parkinson's disease, are characterized by abnormal accumulations of aggregated proteins. Brains in these diseases also show accumulation of autophagic vesicles in the neuronal cytoplasm, suggesting impairment of the autophagic process. As autophagy involves de novo membrane production and vesicle fusion, extensive changes in lipid molecules are necessary. However, the involvement of signaling lipid-modifying enzymes in autophagy and their roles in neurodegenerative diseases are not clear. Using specific inhibitor, we show that loss of phospholipase D1 (PLD1) activity resulted in an accumulation of microtubule-associated protein light chain 3 (LC3), p62, and polyubiquitinated proteins, signs representing malfunction in autophagic flux. Fluorescence and electron microscopic analyses demonstrated impaired fusion of autophagosomes with lysosomes, resulting in accumulation of autophagosomes. Within the cells with impaired autophagic flux, a-synuclein aggregates accumulated in autophagosomes. Knockdown of PLD1 expression using small interfering RNA also resulted in impaired autophagic flux and accumulation of a-synuclein aggregates in autophagosomes. Neuronal toxicity caused by a-synuclein accumulation was rescued by overexpression of PLD1; however, expression of activity-deficient mutant, PLD1-KRM, showed reduced rescue effects. Finally, we demonstrated that both PLD activity and expression levels were reduced in brain tissues of dementia with Lewy bodies (DLB) patients, whereas the amounts of a-synuclein and p62 were increased in the same tissue samples. Collectively, these results suggest that insufficient PLD activity, and therefore, the changes in phospholipid compositions within membranes, might be an important contributor to impaired autophagic process and protein accumulation in Lewy body diseases.

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“…Mutations in a mitochondrial-specific phospholipase D fail to generate phosphatidic acid. Phospholipase D is also necessary for SNARE-based fusion reactions (Nakanishi et al, 2006;Vicogne et al, 2006). Importantly, the phospholipase acts Outside of the secretory pathway, organelle fusion is not mediated by the SNARE proteins.…”

Section: Non-snare-based Organelle Fusionmentioning

confidence: 99%

In VivoAnalysis of Membrane Fusion

Palfreyman¹,

Jørgensen²

2009

Encyclopedia of Life Sciences

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Membranes provide a barrier that allows chemical reactions to be isolated from the environment. The plasma membrane, for example, delineates self from nonself, and thus must have played an essential role in the evolution of life. Yet under numerous circumstances it is equally important that membranes be breached. Numerous forces oppose the spontaneous fusion of membranes; thus, specialized proteins have evolved to fuse membranes. The most well-understood fusion proteins are the viral fusion proteins and the SNARE proteins used in the secretory pathway. In addition, recent discoveries have lead to models for the fusion of organelles such as mitochondria and peroxisomes, as well as for cell-cell fusion. Despite the diverse structures of fusion proteins, it is possible that they function to drive membranes through a series of common lipid intermediates. Here we review the mechanisms of fusion for biological membranes, and highlight the similarities and differences in these processes.

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Phospholipase D and the SNARE Sso1p are necessary for vesicle fusion during sporulation in yeast

Cited by 110 publications

References 51 publications

SSP2 and OSW1, Two Sporulation-Specific Genes Involved in Spore Morphogenesis in Saccharomyces cerevisiae

SSP2 and OSW1, Two Sporulation-Specific Genes Involved in Spore Morphogenesis in Saccharomyces cerevisiae

Phospholipase D1 regulates autophagic flux and clearance of α-synuclein aggregates

In VivoAnalysis of Membrane Fusion

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