Phospholipase D activity is required for suppression of yeast phosphatidylinositol transfer protein defects

Xie, Zhigang; Fang, Min; Rivas, Marcos; Faulkner, Alexander J.; Sternweis, Paul C.; Engebrecht, JoAnne; Bankaitis, Vytas A.

doi:10.1073/pnas.95.21.12346

Cited by 154 publications

(174 citation statements)

References 36 publications

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“…Consistent with this suggestion, increased expression of Shf2p and Shf4p, yeast PITPs that display PtdIns-but not PtdCho-transfer activity in vitro, can rescue the growth and secretory defects of sec14 mutants and requires the function of Spo14p to do so (Li et al, 2000). However, Sec14p itself exhibits both PtdCho and PtdIns transfer activity in vitro (Bankaitis et al, 1990), and the results of genetic analyses have not supported a model in which the essential vegetative function of Sec14p is to provide for activation of Spo14p (Sreenivas et al, 1998;Xie et al, 1998), because unlike sec14⌬ mutants, spo14⌬ mutants are viable (Honigberg et al, 1992;Rose et al, 1995). Moreover, homozygous sfh2⌬ and sfh4⌬ diploids sporulate at wild-type frequencies (Rabitsch et al, 2001).…”

Section: Introductionmentioning

confidence: 77%

“…This phenomenon is referred to as "Sec14 bypass" (Cleves et al, 1991); under these circumstances, Spo14p is essential (Sreenivas et al, 1998;Xie et al, 1998;Li et al, 2002). To determine whether the requirement for Sec14p in sporulation could also be relieved by such mutations, we constructed the appropriate double mutants.…”

Section: The Requirement For Sec14p In Meiosis Can Be Bypassedmentioning

confidence: 99%

“…Yeast strains used in this study are listed in Table 1. CTY159 (sec14-1 ts ) (obtained from Vytas Bankaitis, University of North Carolina, Chapel Hill; Xie et al, 1998), YES47 (pik1-11) and YES102 (pik1-83) (Hendricks et al, 1999), and SD102 (mss4-2) (obtained from Michael Hall, University of Basel; Desrivieres et al, 1998) were backcrossed six times against the SK-1 strain background (Fast, 1973). Pairs of haploid segregants of opposite mating type from the final backcrosses were mated to generate homozygous sec14-1 (Y3242), pik1-11 (Y3637), pik1-83 (Y3732), and mss4-2 (Y4350) diploids.…”

Section: Yeast Strains and Mediamentioning

confidence: 99%

“…Spo14p action is essential for the formation of the prospore membrane (Rudge et al, 1998b) and for increased PtdOH synthesis during sporulation (Rudge et al, 2001). In contrast, under normal physiological conditions, Spo14p is dispensable for secretion and hence is not essential for vegetative growth (Sreenivas et al, 1998;Xie et al, 1998). Thus, Spo14p plays a pivotal role in distinguishing between constitutive and developmentally regulated membrane trafficking events (Rudge et al, 2001;Rudge et al, 2002).…”

Section: Introductionmentioning

confidence: 99%

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Roles of Phosphoinositides and of Spo14p (phospholipase D)-generated Phosphatidic Acid during Yeast Sporulation

Rudge

Sciorra

Iwamoto

et al. 2004

MBoC

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During yeast sporulation, internal membrane synthesis ensures that each haploid nucleus is packaged into a spore. Prospore membrane formation requires Spo14p, a phosphatidylinositol 4,5-bisphosphate [PtdIns(4,5)P 2 ]-stimulated phospholipase D (PLD), which hydrolyzes phosphatidylcholine (PtdCho) to phosphatidic acid (PtdOH) and choline. We found that both meiosis and spore formation also require the phosphatidylinositol (PtdIns)/PtdCho transport protein Sec14p. Specific ablation of the PtdIns transport activity of Sec14p was sufficient to impair spore formation but not meiosis. Overexpression of Pik1p, a PtdIns 4-kinase, suppressed the sec14-1 meiosis and spore formation defects; conversely, pik1-ts diploids failed to undergo meiosis and spore formation. The PtdIns(4)P 5-kinase, Mss4p, also is essential for spore formation. Use of phosphoinositide-specific GFP-PH domain reporters confirmed that PtdIns(4,5)P 2 is enriched in prospore membranes. sec14, pik1, and mss4 mutants displayed decreased Spo14p PLD activity, whereas absence of Spo14p did not affect phosphoinositide levels in vivo, suggesting that formation of PtdIns(4,5)P 2 is important for Spo14p activity. Spo14p-generated PtdOH appears to have an essential role in sporulation, because treatment of cells with 1-butanol, which supports Spo14p-catalyzed PtdCho breakdown but leads to production of Cho and Ptd-butanol, blocks spore formation at concentrations where the inert isomer, 2-butanol, has little effect. Thus, rather than a role for PtdOH in stimulating PtdIns(4,5)P 2 formation, our findings indicate that during sporulation, Spo14p-mediated PtdOH production functions downstream of Sec14p-, Pik1p-, and Mss4p-dependent PtdIns(4,5)P 2 synthesis.

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Section: Introductionmentioning

confidence: 77%

Section: The Requirement For Sec14p In Meiosis Can Be Bypassedmentioning

confidence: 99%

Section: Yeast Strains and Mediamentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Roles of Phosphoinositides and of Spo14p (phospholipase D)-generated Phosphatidic Acid during Yeast Sporulation

Rudge

Sciorra

Iwamoto

et al. 2004

MBoC

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“…Lithium acetate yeast transformation and genetic techniques were performed, and yeast media were prepared as described previously (Kearns et al, 1997;Xie et al, 1998;Guo et al, 1999;Phillips et al, 1999). Yeast strains used in this study included: CTY182 , (Cleves et al, 1991;Phillips et al, 1999).…”

Section: Media and Genetic Techniquesmentioning

confidence: 99%

The Sac1 Phosphoinositide Phosphatase Regulates Golgi Membrane Morphology and Mitotic Spindle Organization in Mammals

Liu

Boukhelifa

Tribble

et al. 2008

MBoC

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Phosphoinositides (PIPs) are ubiquitous regulators of signal transduction events in eukaryotic cells. PIPs are degraded by various enzymes, including PIP phosphatases. The integral membrane Sac1 phosphatases represent a major class of such enzymes. The central role of lipid phosphatases in regulating PIP homeostasis notwithstanding, the biological functions of Sac1-phosphatases remain poorly characterized. Herein, we demonstrate that functional ablation of the single murine Sac1 results in preimplantation lethality in the mouse and that Sac1 insufficiencies result in disorganization of mammalian Golgi membranes and mitotic defects characterized by multiple mechanically active spindles. Complementation experiments demonstrate mutant mammalian Sac1 proteins individually defective in either phosphoinositide phosphatase activity, or in recycling of the enzyme from the Golgi system back to the endoplasmic reticulum, are nonfunctional proteins in vivo. The data indicate Sac1 executes an essential household function in mammals that involves organization of both Golgi membranes and mitotic spindles and that both enzymatic activity and endoplasmic reticulum localization are important Sac1 functional properties. INTRODUCTIONSpatial and temporal regulation of intracellular signaling in eukaryotic cells involves the compartmentalization of membrane surfaces into discrete, albeit often transient, functional units. There are several biochemical strategies by which cells generate such units or domains. One well-established strategy uses the chemical diversity offered by phosphoinositides (PIPs), i.e., phosphorylated forms of phosphatidylinositol (PtdIns) (Majerus, 1997;Fruman et al., 1998;Strahl and Thorner, 2007). The chemical heterogeneity of individual PIP species permits the construction of chemically unique platforms on membrane surfaces that, in turn, recruit unique cohorts of proteins that drive specific biological reactions. Spatial and temporal control of such reactions requires a finely coordinated balance between the activities of the lipid kinases that produce PIPs and the activities of enzymes that degrade them. PIP turnover is catalyzed by two general classes of enzymes: phospholipases and PIP phosphatases.Although experimental scrutiny of the phospholipases has historically been more intense, recent demonstrations of the significant biological functions played by PTEN, the myotubularins, and synaptojanins highlight the general importance of PIP phosphatases (Wishart et al., 2001;Wishart and Dixon, 2002;Wenk and De Camilli, 2004).The SAC domain derives from the yeast Sac1 protein (ySac1; Cleves et al., 1989), and it represents a signature for PIP phosphatase catalytic activity . PIP phosphatases such as phosphatase and tensin homolog (mutated in multiple advanced cancers 1) (PTEN) (Maehama et al., 2001), synaptojanins (Cremona et al., 1999), and synaptojanin-like proteins (Srinivasan et al., 1997;Stolz et al., 1998) all harbor SAC domains. The prototypical member of this family, ySac1, catalyzes the dephosphoryla...

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Brave little yeast, please guide us to Thebes: sphingolipid function in S. cerevisiae

Schneiter

1999

Bioessays

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Phospholipase D activity is required for suppression of yeast phosphatidylinositol transfer protein defects

Cited by 154 publications

References 36 publications

Roles of Phosphoinositides and of Spo14p (phospholipase D)-generated Phosphatidic Acid during Yeast Sporulation

Roles of Phosphoinositides and of Spo14p (phospholipase D)-generated Phosphatidic Acid during Yeast Sporulation

The Sac1 Phosphoinositide Phosphatase Regulates Golgi Membrane Morphology and Mitotic Spindle Organization in Mammals

Brave little yeast, please guide us to Thebes: sphingolipid function in S. cerevisiae

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