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MBC in Press, published online ahead of print July 25, 2007
Mol. Biol. Cell 10.1091/mbc.E07-03-0205

A more recent version of this article appeared on October 1, 2007
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Submitted on March 5, 2007
Revised on July 9, 2007
Accepted on July 16, 2007

Role of the V-ATPase in Regulation of the Vacuolar Fission-Fusion Equilibrium

Tonie L. Baars,* Sebastian Petri,{dagger}{ddagger} Christopher Peters,* and Andreas Mayer*

*Département de Biochimie, Université de Lausanne, 1066 Epalinges, Switzerland; {dagger}Friedrich-Miescher-Laboratorium der Max-Planck-Gesellschaft, 72076 Tübingen, Germany

Monitoring Editor: Akihiko Nakano

Like numerous other eukaryotic organelles the vacuole of the yeast S. cerevisiae undergoes coordinated cycles of membrane fission and fusion in the course of the cell cycle and in adaptation to environmental conditions. Organelle fission and fusion processes must be balanced to ensure organelle integrity. Coordination of vacuole fission and fusion depends on the interactions of vacuolar SNARE proteins and the dynamin-like GTPase Vps1p. Here, we identify a novel factor that impinges on the fusion/fission equilibrium: The vacuolar H+-ATPase (V-ATPase) performs two distinct roles in vacuole fission and fusion. Fusion requires the physical presence of the V0 sector of the V-ATPase, but not its pump activity. Vacuole fission, on the other hand, depends on proton translocation by the V-ATPase. Eliminating proton pumping by the V-ATPase either pharmacologically or by conditional or constitutive V-ATPase mutations blocked salt-induced vacuole fragmentation in vivo. In living cells fisson defects are epistatic to fusion defects. Therefore, mutants lacking the V-ATPase display large single vacuoles instead of multiple smaller vacuoles, the phenotype that is generally seen in mutants having defects only in vacuolar fusion. Its dual involvement in vacuole fission and fusion suggests the V-ATPase as a potential regulator of vacuolar morphology and membrane dynamics.

{ddagger}Present address: Zentrum für Molekulare Biologie der Universität Heidelberg, Im Neuenheimer Feld 282, 69120 Heidelberg, Germany.

Address correspondence to: Andreas Mayer (Andreas.Mayer{at}unil.ch)




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