The Yeast Pma1 Proton Pump: a Model for Understanding the Biogenesis of Plasma Membrane Proteins

Ferreira, Thierry; Mason, Anne B.; Slayman, Carolyn W.

doi:10.1074/jbc.r100022200

Cited by 63 publications

(54 citation statements)

References 42 publications

(41 reference statements)

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“…Numerous mutants that affect its catalytic activity, quality control in the ER and/or trafficking to the cell surface have been generated and characterized [11,12].…”

Section: Biogenesis and Transport Of The Proton Pumping H D -Atpasementioning

confidence: 99%

Lipid-dependent surface transport of the proton pumping ATPase: A model to study plasma membrane biogenesis in yeast

Toulmay

Schneiter

2007

Biochimie

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The proton pumping H þ -ATPase, Pma1, is one of the most abundant integral membrane proteins of the yeast plasma membrane. Pma1 activity controls the intracellular pH and maintains the electrochemical gradient across the plasma membrane, two essential cellular functions. The maintenance of the proton gradient, on the other hand, also requires a specialized lipid composition of this membrane. The plasma membrane of eukaryotic cells is typically rich in sphingolipids and sterols. These two lipids condense to form less fluid membrane microdomains or lipid rafts. The yeast sphingolipid is peculiar in that it invariably contains a saturated very long-chain fatty acid with 26 carbon atoms. During cell growth and plasma membrane expansion, both C26-containing sphingolipids and Pma1 are first synthesized in the endoplasmatic reticulum from where they are transported by the secretory pathway to the cell surface. Remarkably, shortening the C26 fatty acid to a C22 fatty acid by mutations in the fatty acid elongation complex impairs raft association of newly synthesized Pma1 and induces rapid degradation of the ATPase by rerouting the enzyme from the plasma membrane to the vacuole, the fungal equivalent of the lysosome. Here, we review the role of lipids in mediating raft association and stable surface transport of the newly synthesized ATPase, and discuss a model, in which the newly synthesized ATPase assembles into a membrane environment that is enriched in C26-containing lipids already in the endoplasmatic reticulum. The resulting proteinelipid complex is then transported and sorted as an entity to the plasma membrane. Failure to successfully assemble this lipideprotein complex results in mistargeting of the protein to the vacuole.

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“…Numerous mutants that affect its catalytic activity, quality control in the ER and/or trafficking to the cell surface have been generated and characterized [11,12].…”

Section: Biogenesis and Transport Of The Proton Pumping H D -Atpasementioning

confidence: 99%

Lipid-dependent surface transport of the proton pumping ATPase: A model to study plasma membrane biogenesis in yeast

Toulmay

Schneiter

2007

Biochimie

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“…4C), further confirming the presence of Bem3 on secretory vesicles. Because sec10-2 cells show a defect in secretory vesicle fusion with the plasma membrane at the restrictive temperature (Roth et al, 1998) only a minor fraction of Bem3 co-fractionated with the plasma membrane marker, Pma1 (Ferreira et al, 2001;Luo and Chang, 2000) ( Fig. 4C).…”

Section: The Bem3 Compartment Contains Both Endocytic and Secretory Mmentioning

confidence: 99%

Bem3, a Cdc42 GTPase-Activating Protein, traffics to an intracellular compartment and recruits the secretory Rab GTPase Sec4 to endomembranes

Mukherjee

Sen

Boettner

et al. 2013

Journal of Cell Science

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SummaryCell polarity is essential for many cellular functions including division and cell-fate determination. Although RhoGTPase signaling and vesicle trafficking are both required for the establishment of cell polarity, the mechanisms by which they are coordinated are unclear. Here, we demonstrate that the yeast RhoGAP (GTPase activating protein), Bem3, is targeted to sites of polarized growth by the endocytic and recycling pathways. Specifically, deletion of SLA2 or RCY1 led to mislocalization of Bem3 to depolarized puncta and accumulation in intracellular compartments, respectively. Bem3 partitioned between the plasma membrane and an intracellular membrane-bound compartment. These Bem3-positive structures were polarized towards sites of bud emergence and were mostly observed during the pre-mitotic phase of apical growth. Cell biological and biochemical approaches demonstrated that this intracellular Bem3 compartment contained markers for both the endocytic and secretory pathways, which were reminiscent of the Spitzenkörper present in the hyphal tips of growing fungi. Importantly, Bem3 was not a passive cargo, but recruited the secretory Rab protein, Sec4, to the Bem3-containing compartments. Moreover, Bem3 deletion resulted in less efficient localization of Sec4 to bud tips during early stages of bud emergence. Surprisingly, these effects of Bem3 on Sec4 were independent of its GAP activity, but depended on its ability to efficiently bind endomembranes. This work unveils unsuspected and important details of the relationship between vesicle traffic and elements of the cell polarity machinery: (1) Bem3, a cell polarity and peripherally associated membrane protein, relies on vesicle trafficking to maintain its proper localization; and (2) in turn, Bem3 influences secretory vesicle trafficking.

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“…Although little is known about PM H þ -ATPase targeting information, the sorting and trafficking of Saccharomyces cerevisae PM H þ -ATPase1 (PMA1) have been studied to some extent (reviewed in Ferreira et al, 2001;Lefebvre et al, 2003). After translation and insertion into the ER membrane, PMA1 is packaged into COPII vesicles (Shimoni et al, 2000), then transported to the PM via the Golgi, because in various secretory mutants, it remains in the Golgi apparatus (sec7) or in the secretory vesicles trafficking between the Golgi and the PM (sec6 and sec1) (Holcomb et al, 1988;Chang and Slayman, 1991).…”

Section: Introductionmentioning

confidence: 99%

Targeting of a Nicotiana plumbaginifolia H⁺-ATPase to the Plasma Membrane Is Not by Default and Requires Cytosolic Structural Determinants

et al. 2004

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The structural determinants involved in the targeting of multitransmembrane-span proteins to the plasma membrane (PM) remain poorly understood. The plasma membrane H þ -ATPase (PMA) from Nicotiana plumbaginifolia, a well-characterized 10 transmembrane-span enzyme, was used as a model to identify structural elements essential for targeting to the PM. When PMA2 and PMA4, representatives of the two main PMA subfamilies, were fused to green fluorescent protein (GFP), the chimeras were shown to be still functional and to be correctly and rapidly targeted to the PM in transgenic tobacco. By contrast, chimeric proteins containing various combinations of PMA transmembrane spanning domains accumulated in the Golgi apparatus and not in the PM and displayed slow traffic properties through the secretory pathway. Individual deletion of three of the four cytosolic domains did not prevent PM targeting, but deletion of the large loop or of its nucleotide binding domain resulted in GFP fluorescence accumulating exclusively in the endoplasmic reticulum. The results show that, at least for this polytopic protein, the PM is not the default pathway and that, in contrast with single-pass membrane proteins, cytosolic structural determinants are required for correct targeting.

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The Yeast Pma1 Proton Pump: a Model for Understanding the Biogenesis of Plasma Membrane Proteins

Cited by 63 publications

References 42 publications

Lipid-dependent surface transport of the proton pumping ATPase: A model to study plasma membrane biogenesis in yeast

Lipid-dependent surface transport of the proton pumping ATPase: A model to study plasma membrane biogenesis in yeast

Bem3, a Cdc42 GTPase-Activating Protein, traffics to an intracellular compartment and recruits the secretory Rab GTPase Sec4 to endomembranes

Targeting of a Nicotiana plumbaginifolia H⁺-ATPase to the Plasma Membrane Is Not by Default and Requires Cytosolic Structural Determinants

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The Yeast Pma1 Proton Pump: a Model for Understanding the Biogenesis of Plasma Membrane Proteins

Cited by 63 publications

References 42 publications

Lipid-dependent surface transport of the proton pumping ATPase: A model to study plasma membrane biogenesis in yeast

Lipid-dependent surface transport of the proton pumping ATPase: A model to study plasma membrane biogenesis in yeast

Bem3, a Cdc42 GTPase-Activating Protein, traffics to an intracellular compartment and recruits the secretory Rab GTPase Sec4 to endomembranes

Targeting of a Nicotiana plumbaginifolia H+-ATPase to the Plasma Membrane Is Not by Default and Requires Cytosolic Structural Determinants

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Targeting of a Nicotiana plumbaginifolia H⁺-ATPase to the Plasma Membrane Is Not by Default and Requires Cytosolic Structural Determinants