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Structure of the rotor ring modified with N,N'-dicyclohexylcarbodiimide of the Na+-transporting vacuolar ATPase.

Mizutani K, Yamamoto M, Suzuki K, Yamato I, Kakinuma Y, Shirouzu M, Walker JE, Yokoyama S, Iwata S, Murata T
Proc Natl Acad Sci U S A 108 13474-9 (2011)
Cited: 34 times
EuropePMC logo PMID: 21813759

Abstract

The prokaryotic V-ATPase of Enterococcus hirae, closely related to the eukaryotic enzymes, provides a unique opportunity to study the ion-translocation mechanism because it transports Na(+), which can be detected by radioisotope (22Na(+)) experiments and X-ray crystallography. In this study, we demonstrated that the binding affinity of the rotor ring (K ring) for 22Na(+) decreased approximately 30-fold by reaction with N,N(')-dicyclohexylcarbodiimide (DCCD), and determined the crystal structures of Na(+)-bound and Na(+)-unbound K rings modified with DCCD at 2.4- and 3.1-Å resolutions, respectively. Overall these structures were similar, indicating that there is no global conformational change associated with release of Na(+) from the DCCD-K ring. A conserved glutamate residue (E139) within all 10 ion-binding pockets of the K ring was neutralized by modification with DCCD, and formed an "open" conformation by losing hydrogen bonds with the Y68 and T64 side chains, resulting in low affinity for Na(+). This open conformation is likely to be comparable to that of neutralized E139 forming a salt bridge with the conserved arginine of the stator during the ion-translocation process. Based on these findings, we proposed the ion-translocation model that the binding affinity for Na(+) decreases due to the neutralization of E139, thus releasing bound Na(+), and that the structures of Na(+)-bound and Na(+)-unbound DCCD-K rings are corresponding to intermediate states before and after release of Na(+) during rotational catalysis of V-ATPase, respectively.

Articles - 2db4 mentioned but not cited (6)

  1. Crystal structure of the Mg·ADP-inhibited state of the yeast F1c10-ATP synthase. Dautant A, Velours J, Giraud MF. J Biol Chem 285 29502-29510 (2010)
  2. Structure of the rotor ring modified with N,N'-dicyclohexylcarbodiimide of the Na+-transporting vacuolar ATPase. Mizutani K, Yamamoto M, Suzuki K, Yamato I, Kakinuma Y, Shirouzu M, Walker JE, Yokoyama S, Iwata S, Murata T. Proc Natl Acad Sci U S A 108 13474-13479 (2011)
  3. Archazolid A binds to the equatorial region of the c-ring of the vacuolar H+-ATPase. Bockelmann S, Menche D, Rudolph S, Bender T, Grond S, von Zezschwitz P, Muench SP, Wieczorek H, Huss M. J Biol Chem 285 38304-38314 (2010)
  4. A1Ao-ATP synthase of Methanobrevibacter ruminantium couples sodium ions for ATP synthesis under physiological conditions. McMillan DG, Ferguson SA, Dey D, Schröder K, Aung HL, Carbone V, Attwood GT, Ronimus RS, Meier T, Janssen PH, Cook GM. J Biol Chem 286 39882-39892 (2011)
  5. PA1b inhibitor binding to subunits c and e of the vacuolar ATPase reveals its insecticidal mechanism. Muench SP, Rawson S, Eyraud V, Delmas AF, Da Silva P, Phillips C, Trinick J, Harrison MA, Gressent F, Huss M. J Biol Chem 289 16399-16408 (2014)
  6. Application of Homology Modeling by Enhanced Profile-Profile Alignment and Flexible-Fitting Simulation to Cryo-EM Based Structure Determination. Yamamori Y, Tomii K. Int J Mol Sci 23 1977 (2022)


Reviews citing this publication (4)

  1. Rotary ATPases--dynamic molecular machines. Stewart AG, Laming EM, Sobti M, Stock D. Curr Opin Struct Biol 25 40-48 (2014)
  2. Operating principles of rotary molecular motors: differences between F1 and V1 motors. Yamato I, Kakinuma Y, Murata T. Biophys Physicobiol 13 37-44 (2016)
  3. Rotational Mechanism Model of the Bacterial V1 Motor Based on Structural and Computational Analyses. Singharoy A, Chipot C, Ekimoto T, Suzuki K, Ikeguchi M, Yamato I, Murata T. Front Physiol 10 46 (2019)
  4. Infrared spectroscopic studies on the V-ATPase. Kandori H, Furutani Y, Murata T. Biochim Biophys Acta 1847 134-141 (2015)

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  1. Structure of a Complete ATP Synthase Dimer Reveals the Molecular Basis of Inner Mitochondrial Membrane Morphology. Hahn A, Parey K, Bublitz M, Mills DJ, Zickermann V, Vonck J, Kühlbrandt W, Meier T. Mol Cell 63 445-456 (2016)
  2. Rotation mechanism of Enterococcus hirae V1-ATPase based on asymmetric crystal structures. Arai S, Saijo S, Suzuki K, Mizutani K, Kakinuma Y, Ishizuka-Katsura Y, Ohsawa N, Terada T, Shirouzu M, Yokoyama S, Iwata S, Yamato I, Murata T. Nature 493 703-707 (2013)
  3. Structure of the c(10) ring of the yeast mitochondrial ATP synthase in the open conformation. Symersky J, Pagadala V, Osowski D, Krah A, Meier T, Faraldo-Gómez JD, Mueller DM. Nat Struct Mol Biol 19 485-91, S1 (2012)
  4. Crystal structures of the PsbS protein essential for photoprotection in plants. Fan M, Li M, Liu Z, Cao P, Pan X, Zhang H, Zhao X, Zhang J, Chang W. Nat Struct Mol Biol 22 729-735 (2015)
  5. A new type of Na(+)-driven ATP synthase membrane rotor with a two-carboxylate ion-coupling motif. Schulz S, Iglesias-Cans M, Krah A, Yildiz O, Leone V, Matthies D, Cook GM, Faraldo-Gómez JD, Meier T. PLoS Biol 11 e1001596 (2013)
  6. Crystal structures of the ATP-binding and ADP-release dwells of the V1 rotary motor. Suzuki K, Mizutani K, Maruyama S, Shimono K, Imai FL, Muneyuki E, Kakinuma Y, Ishizuka-Katsura Y, Shirouzu M, Yokoyama S, Yamato I, Murata T. Nat Commun 7 13235 (2016)
  7. Enhancement of ginsenoside biosynthesis in cell cultures of Panax ginseng by N,N'-dicyclohexylcarbodiimide elicitation. Huang C, Qian ZG, Zhong JJ. J Biotechnol 165 30-36 (2013)
  8. Torque generation of Enterococcus hirae V-ATPase. Ueno H, Minagawa Y, Hara M, Rahman S, Yamato I, Muneyuki E, Noji H, Murata T, Iino R. J Biol Chem 289 31212-31223 (2014)
  9. Structural study on the architecture of the bacterial ATP synthase Fo motor. Hakulinen JK, Klyszejko AL, Hoffmann J, Eckhardt-Strelau L, Brutschy B, Vonck J, Meier T. Proc Natl Acad Sci U S A 109 E2050-6 (2012)
  10. The c-ring ion binding site of the ATP synthase from Bacillus pseudofirmus OF4 is adapted to alkaliphilic lifestyle. Preiss L, Langer JD, Hicks DB, Liu J, Yildiz O, Krulwich TA, Meier T. Mol Microbiol 92 973-984 (2014)
  11. Roles of AtpI and two YidC-type proteins from alkaliphilic Bacillus pseudofirmus OF4 in ATP synthase assembly and nonfermentative growth. Liu J, Hicks DB, Krulwich TA. J Bacteriol 195 220-230 (2013)
  12. A c subunit with four transmembrane helices and one ion (Na+)-binding site in an archaeal ATP synthase: implications for c ring function and structure. Mayer F, Leone V, Langer JD, Faraldo-Gómez JD, Müller V. J Biol Chem 287 39327-39337 (2012)
  13. Kinetic properties of the mitochondrial F1FO-ATPase activity elicited by Ca2+ in replacement of Mg2. Nesci S, Trombetti F, Ventrella V, Pirini M, Pagliarani A. Biochimie 140 73-81 (2017)
  14. Mussel and mammalian ATP synthase share the same bioenergetic cost of ATP. Nesci S, Ventrella V, Trombetti F, Pirini M, Pagliarani A. J Bioenerg Biomembr 45 289-300 (2013)
  15. EPR Studies of V-ATPase with Spin-Labeled Inhibitors DCC and Archazolid: Interaction Dynamics with Proton Translocating Subunit c. Gölz JP, Bockelmann S, Mayer K, Steinhoff HJ, Wieczorek H, Huss M, Klare JP, Menche D. ChemMedChem 11 420-428 (2016)
  16. Rotation Mechanism of Molecular Motor V1-ATPase Studied by Multiscale Molecular Dynamics Simulation. Isaka Y, Ekimoto T, Kokabu Y, Yamato I, Murata T, Ikeguchi M. Biophys J 112 911-920 (2017)
  17. Active-site structure of the thermophilic Foc-subunit ring in membranes elucidated by solid-state NMR. Kang SJ, Todokoro Y, Yumen I, Shen B, Iwasaki I, Suzuki T, Miyagi A, Yoshida M, Fujiwara T, Akutsu H. Biophys J 106 390-398 (2014)
  18. Mutagenesis of the residues forming an ion binding pocket of the NtpK subunit of Enterococcus hirae V-ATPase. Kawano-Kawada M, Iwaki T, Hosaka T, Murata T, Yamato I, Homma M, Kakinuma Y. J Bacteriol 194 4546-4549 (2012)
  19. Loose binding of the DF axis with the A3B3 complex stimulates the initial activity of Enterococcus hirae V1-ATPase. Alam MJ, Arai S, Saijo S, Suzuki K, Mizutani K, Ishizuka-Katsura Y, Ohsawa N, Terada T, Shirouzu M, Yokoyama S, Iwata S, Kakinuma Y, Yamato I, Murata T. PLoS One 8 e74291 (2013)
  20. One-pot synthesis of anilides, herbicidal activity and molecular docking study. Sartori SK, Alvarenga ES, Franco CA, Ramos DS, Oliveira DF. Pest Manag Sci 74 1637-1645 (2018)
  21. Role of the N-terminal signal peptide in the membrane insertion of Aquifex aeolicus F1F0 ATP synthase c-subunit. Zhang C, Marcia M, Langer JD, Peng G, Michel H. FEBS J 280 3425-3435 (2013)
  22. Design, Synthesis, EPR-Studies and Conformational Bias of Novel Spin-Labeled DCC-Analogues for the Highly Regioselective Labeling of Aliphatic and Aromatic Carboxylic Acids. Gölz JP, NejatyJahromy Y, Bauer M, Muhammad A, Schnakenburg G, Grimme S, Schiemann O, Menche D. Chemistry 22 9591-9598 (2016)
  23. Adaptive responses of Bacillus cereus ATCC14579 cells upon exposure to acid conditions involve ATPase activity to maintain their internal pH. Senouci-Rezkallah K, Jobin MP, Schmitt P. Microbiologyopen 4 313-322 (2015)
  24. Mutant LV(476-7)AA of A-subunit of Enterococcus hirae V1-ATPase: High affinity of A3B3 complex to DF axis and low ATPase activity. Alam J, Yamato I, Arai S, Saijo S, Mizutani K, Ishizuka-Katsura Y, Ohsawa N, Terada T, Shirouzu M, Yokoyama S, Iwata S, Kakinuma Y, Murata T. Springerplus 2 689 (2013)


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