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The 3.5-Å CryoEM Structure of Nanodisc-Reconstituted Yeast Vacuolar ATPase Vo Proton Channel.

Roh SH, Stam NJ, Hryc CF, Couoh-Cardel S, Pintilie G, Chiu W, Wilkens S
Mol Cell 69 993-1004.e3 (2018)
Cited: 57 times
EuropePMC logo PMID: 29526695

Abstract

The molecular mechanism of transmembrane proton translocation in rotary motor ATPases is not fully understood. Here, we report the 3.5-Å resolution cryoEM structure of the lipid nanodisc-reconstituted Vo proton channel of the yeast vacuolar H+-ATPase, captured in a physiologically relevant, autoinhibited state. The resulting atomic model provides structural detail for the amino acids that constitute the proton pathway at the interface of the proteolipid ring and subunit a. Based on the structure and previous mutagenesis studies, we propose the chemical basis of transmembrane proton transport. Moreover, we discovered that the C terminus of the assembly factor Voa1 is an integral component of mature Vo. Voa1's C-terminal transmembrane α helix is bound inside the proteolipid ring, where it contributes to the stability of the complex. Our structure rationalizes possible mechanisms by which mutations in human Vo can result in disease phenotypes and may thus provide new avenues for therapeutic interventions.

Reviews - 6c6l mentioned but not cited (1)

  1. Exploring the Therapeutic Potential of Membrane Transport Proteins: Focus on Cancer and Chemoresistance. Almasi S, El Hiani Y. Cancers (Basel) 12 E1624 (2020)

Articles - 6c6l mentioned but not cited (7)

  1. The 3.5-Å CryoEM Structure of Nanodisc-Reconstituted Yeast Vacuolar ATPase Vo Proton Channel. Roh SH, Stam NJ, Hryc CF, Couoh-Cardel S, Pintilie G, Chiu W, Wilkens S. Mol Cell 69 993-1004.e3 (2018)
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  5. research-article Human V-ATPase a-subunit isoforms bind specifically to distinct phosphoinositide phospholipids. Mitra C, Kane PM. bioRxiv 2023.04.24.538068 (2023)
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  7. Six states of Enterococcus hirae V-type ATPase reveals non-uniform rotor rotation during turnover. Burton-Smith RN, Song C, Ueno H, Murata T, Iino R, Murata K. Commun Biol 6 755 (2023)


Reviews citing this publication (15)

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  8. The V-ATPases in cancer and cell death. Chen F, Kang R, Liu J, Tang D. Cancer Gene Ther 29 1529-1541 (2022)
  9. Essay on Biomembrane Structure. Gerle C. J Membr Biol 252 115-130 (2019)
  10. The Plant V-ATPase. Seidel T. Front Plant Sci 13 931777 (2022)
  11. Cryo-EM studies of the rotary H+-ATPase/synthase from Thermus thermophilus. Nakanishi A, Kishikawa JI, Mitsuoka K, Yokoyama K. Biophys Physicobiol 16 140-146 (2019)
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Articles citing this publication (34)

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  7. Cryo-EM and MD infer water-mediated proton transport and autoinhibition mechanisms of Vo complex. Roh SH, Shekhar M, Pintilie G, Chipot C, Wilkens S, Singharoy A, Chiu W. Sci Adv 6 eabb9605 (2020)
  8. Cryo-EM sample preparation method for extremely low concentration liposomes. Tonggu L, Wang L. Ultramicroscopy 208 112849 (2020)
  9. Interaction of the late endo-lysosomal lipid PI(3,5)P2 with the Vph1 isoform of yeast V-ATPase increases its activity and cellular stress tolerance. Banerjee S, Clapp K, Tarsio M, Kane PM. J Biol Chem 294 9161-9171 (2019)
  10. Cryo-EM structures of undocked innexin-6 hemichannels in phospholipids. Burendei B, Shinozaki R, Watanabe M, Terada T, Tani K, Fujiyoshi Y, Oshima A. Sci Adv 6 eaax3157 (2020)
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  12. Atp6ap2 deletion causes extensive vacuolation that consumes the insulin content of pancreatic β cells. Binger KJ, Neukam M, Tattikota SG, Qadri F, Puchkov D, Willmes DM, Wurmsee S, Geisberger S, Dechend R, Raile K, Kurth T, Nguyen G, Poy MN, Solimena M, Muller DN, Birkenfeld AL. Proc Natl Acad Sci U S A 116 19983-19988 (2019)
  13. Functional reconstitution of vacuolar H+-ATPase from Vo proton channel and mutant V1-ATPase provides insight into the mechanism of reversible disassembly. Sharma S, Oot RA, Khan MM, Wilkens S. J Biol Chem 294 6439-6449 (2019)
  14. Unusual features of the c-ring of F1FO ATP synthases. Vlasov AV, Kovalev KV, Marx SH, Round ES, Gushchin IY, Polovinkin VA, Tsoy NM, Okhrimenko IS, Borshchevskiy VI, Büldt GD, Ryzhykau YL, Rogachev AV, Chupin VV, Kuklin AI, Dencher NA, Gordeliy VI. Sci Rep 9 18547 (2019)
  15. Defining steps in RAVE-catalyzed V-ATPase assembly using purified RAVE and V-ATPase subcomplexes. Jaskolka MC, Tarsio M, Smardon AM, Khan MM, Kane PM. J Biol Chem 296 100703 (2021)
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  19. Structure of the Human BK Ion Channel in Lipid Environment. Tonggu L, Wang L. Membranes (Basel) 12 758 (2022)
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  21. Assembly of Spinach Chloroplast ATP Synthase Rotor Ring Protein-Lipid Complex. Novitskaia O, Buslaev P, Gushchin I. Front Mol Biosci 6 135 (2019)
  22. Variants in ATP6V0A1 cause progressive myoclonus epilepsy and developmental and epileptic encephalopathy. Bott LC, Forouhan M, Lieto M, Sala AJ, Ellerington R, Johnson JO, Speciale AA, Criscuolo C, Filla A, Chitayat D, Alkhunaizi E, Shannon P, Nemeth AH, Italian Undiagnosed Diseases Network , Angelucci F, Lim WF, Striano P, Zara F, Helbig I, Muona M, Courage C, Lehesjoki AE, Berkovic SF, ATPase Consortium , Fischbeck KH, Brancati F, Morimoto RI, Wood MJA, Rinaldi C, Rinaldi C. Brain Commun 3 fcab245 (2021)
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  28. A Role for the V0 Sector of the V-ATPase in Neuroexocytosis: Exogenous V0d Blocks Complexin and SNARE Interactions with V0c. Lévêque C, Maulet Y, Wang Q, Rame M, Rodriguez L, Mochida S, Sangiardi M, Youssouf F, Iborra C, Seagar M, Vitale N, El Far O. Cells 12 750 (2023)
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