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Cited by 18ATP Synthase and ATPases ResearchCellular transport and secretionEnzyme Structure and Function

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Structural basis of V-ATPase V O region assembly by Vma12p, 21p, and 22p

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Wang, Hanlin, Bueler, Stephanie A., Rubinstein, John L.·2023·Proceedings of the National Academy of Sciences
DOI 10.1073/pnas.2217181120PMC PMC9963935

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Abstract

Vacuolar-type adenosine triphosphatases (V-ATPases) are rotary proton pumps that acidify specific intracellular compartments in almost all eukaryotic cells. These multi-subunit enzymes consist of a soluble catalytic V 1 region and a membrane-embedded proton-translocating V O region. V O is assembled in the endoplasmic reticulum (ER) membrane, and V 1 is assembled in the cytosol. However, V 1 binds V O only after V O is transported to the Golgi membrane, thereby preventing acidification of the ER. We isolated V O complexes and subcomplexes from Saccharomyces cerevisiae bound to V-ATPase assembly factors Vma12p, Vma21p, and Vma22p. Electron cryomicroscopy shows how the Vma12-22p complex recruits subunits a, e, and f to the rotor ring of V O while blocking premature binding of V 1 . Vma21p, which contains an ER-retrieval motif, binds the V O :Vma12-22p complex, “mature” V O , and a complex that appears to contain a ring of loosely packed rotor subunits and the proteins YAR027W and YAR028W. The structures suggest that Vma21p binds assembly intermediates that contain a rotor ring and that activation of proton pumping following assembly of V 1 with V O removes Vma21p, allowing V-ATPase to remain in the Golgi. Together, these structures show how Vma12-22p and Vma21p function in V-ATPase assembly and quality control, ensuring the enzyme acidifies only its intended cellular targets.

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Metadata

Authors
Wang, H., Bueler, S. A., & Rubinstein, J. L.
Affiliations
  • University of Toronto (CA)
  • Hospital for Sick Children (CA)
Corresponding author
Rubinstein, John L.
ORCID
Venue
Proceedings of the National Academy of Sciences
Publisher
National Academy of Sciences
Published
2023-02
Volume
120
Issue
6
Pages
e2217181120-e2217181120
ISSN
  • 0027-8424 (ISSN-L)
  • 1091-6490
DOI
10.1073/pnas.2217181120
PMC
PMC9963935
OpenAlex
W4318765538
Cited by
18
References
2
Citations by year
2026: 7 · 2025: 2 · 2024: 8 · 2023: 1
FWCI
1.60
Type
journal article
Language
en
Open access
Licence
Locations
  • Proceedings of the National Academy of Sciences (publishedVersion, cc-by-nc-nd)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion)
  • PubMed Central (publishedVersion, cc-by-nc-nd)
  • PubMed (publishedVersion)
Funders
  • Canada Research Chairs (CRC)
  • Gouvernement du Canada | Canadian Institutes of Health Research (PJT166152)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › ATP Synthase and ATPases Research
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Structural Biology › Enzyme Structure and Function
Keywords
V-ATPase, proton pump, Golgi membranes, Saccharomyces cerevisiae, quality control, cryo-electron microscopy
MeSH terms
Membrane Proteins, Protons, Saccharomyces cerevisiae, Vacuolar Proton-Translocating ATPases, Saccharomyces cerevisiae Proteins

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