Structure of the vacuolar H+-ATPase rotary motor reveals new mechanistic insights

Structure

Volumn 23, Issue 3, 2015, Pages 461-471

  Rawson, Shaun ^a   Phillips, Clair ^a   Huss, Markus ^b   Tiburcy, Felix ^b   Wieczorek, Helmut ^b   Trinick, John ^a   Harrison, Michael A ^a   Muench, Stephen P ^a  

^a UNIVERSITY OF LEEDS   (United Kingdom)

^b UNIVERSITY OF OSNABRÜCK   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; PROTON PUMP; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; INSECT PROTEIN;

ANIMAL CELL; ARTICLE; CATALYSIS; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME ACTIVE SITE; ION TRANSPORT; MOLECULAR MECHANICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN STRUCTURE; PROTON TRANSPORT; STOICHIOMETRY; THEORETICAL MODEL; AMINO ACID SEQUENCE; ANIMAL; CHEMICAL STRUCTURE; CHEMISTRY; CRYOELECTRON MICROSCOPY; ENZYMOLOGY; FOURIER ANALYSIS; MANDUCA; NUCLEOTIDE SEQUENCE; PROTEIN QUATERNARY STRUCTURE; PROTEIN SECONDARY STRUCTURE;

EUKARYOTA;

AMINO ACID SEQUENCE; ANIMALS; CATALYTIC DOMAIN; CONSERVED SEQUENCE; CRYOELECTRON MICROSCOPY; FOURIER ANALYSIS; INSECT PROTEINS; MANDUCA; MODELS, MOLECULAR; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, SECONDARY; VACUOLAR PROTON-TRANSLOCATING ATPASES;

EID: 84923923054     PISSN: 09692126     EISSN: 18784186     Source Type: Journal    
DOI: 10.1016/j.str.2014.12.016     Document Type: Article

References (65)

1. J.P. Abrahams, A.G. Leslie, R. Lutter, and J.E. Walker Structure at 2.8 Å resolution of F1-ATPase from bovine heart mitochondria Nature 370 1994 621 628
2. C.M. Angevine, K.A.G. Herold, O.D. Vincent, and R.H. Fillingame Aqueous access pathways in ATP synthase subunit A - reactivity of cysteine substituted into transmembrane helices 1, 3, and 5 J. Biol. Chem. 282 2007 9001 9007
3. 1-ATPase based on asymmetric crystal structures Nature 493 2013 703 707
4. C. Beltran, and N. Nelson The membrane sector of vacuolar H(+)-ATPase by itself is impermeable to protons Acta Physiol. Scand. Suppl. 607 1992 41 47
5. S. Benlekbir, S.A. Bueler, and J.L. Rubinstein Structure of the vacuolar-type ATPase from Saccharomyces cerevisiae at 11Å resolution Nat. Struct. Mol. Biol. 19 2012 1356 1362
6. H.C. Blair, S.L. Teitelbaum, R. Ghiselli, and S. Gluck Osteoclastic bone resorption by a polarized vacuolar proton pump Science 245 1989 855 857
7. 1-ATPase from bovine heart mitochondria at 1.9Å resolution J. Biol. Chem. 282 2007 14238 14242
8. P.D. Boyer The ATP synthase - a splendid molecular machine Ann. Rev. Biochem. 66 1997 717 749
9. E. Cao, M. Liao, Y. Cheng, and D. Julius TRPV1 structures in distinct conformations reveal activation mechanisms Nature 504 2013 113 118
10. O. Drory, F. Frolow, and N. Nelson Crystal structure of yeast subunit C reveals its stator function EMBO Rep. 5 2004 1148 1152
11. M. Forgac Vacuolar ATPases: rotary proton pumps in physiology and pathophysiology Nat. Rev. Mol. Cell Biol. 8 2007 917 929
12. 1-c-ring complexes of F-ATP synthase J. Struct. Biol. 177 2012 490 497
13. O. Goldenberg, E. Erez, G. Nimrod, and N. Ben-Tal The ConSurf-DB: pre-calculated evolutionary conservation profiles of protein structures Nucleic Acids Res. 37 2009 323 327
14. M. Gräbe, H. Wang, and G. Oster The mechanochemistry of V-ATPase proton pumps Biophys. J. 78 2000 2798 2813
15. T. Hirata, A. Iwamoto-Kihara, G.H. Sun-Wada, T. Okajima, Y. Wada, and M. Futai Subunit rotation of vacuolar-type proton pumping ATPase: relative rotation of the G and C subunits J. Biol. Chem. 278 2003 23714 23719
16. M. Huss, G. Ingenhorst, S. König, M. Gassel, S. Dröse, A. Zeeck, K. Altendorf, and H. Wieczorek Concanamycin A, the specific inhibitor of V-ATPase, binds to the V(o) subunit c J. Biol. Chem. 277 2002 40544 40548
17. M. Huss, and H. Wieczorek Influence of ATP and ADP on dissociation of the V-ATPase into its V(1) and V(o) complexes FEBS Lett. 581 2007 5566 5572
18. 1-ATPase subunits Proc. Natl. Acad. Sci. USA 104 2007 485 490
19. 1-motor Proc. Natl. Acad. Sci. USA 102 2005 17929 17933
20. M. Iwata, H. Imamura, E. Stambouli, C. Ikeda, M. Tamakoshi, K. Nagata, H. Makyio, B. Hankamer, J. Barber, and M. Yoshida Crystal structure of a central stalk subunit C and reversible association/dissociation of vacuolar-type ATPase Proc. Natl. Acad. Sci. USA 101 2004 59 64
21. W. Junge, H. Lill, and S. Engelbrecht ATP synthase: and electrochemical transducer with rotary mechanics Trends Biochem. Sci. 22 1997 420 423
22. 1-ATPase Nature 459 2009 364 370
23. P.M. Kane Disassembly and reassembly of the yeast vacuolar H(+)-ATPase in vivo J. Biol. Chem. 270 1995 17025 17032
24. S. Kawasaki-Nishi, T. Nishi, and M. Forgac Interacting helical surfaces of the transmembrane segments of subunits a and c' of the yeast V-ATPase defined by disulfide-mediated cross-linking J. Biol. Chem. 278 2003 41908 41913
25. L.A. Kelley, and M.J.E. Sternberg Protein structure prediction on the web: a case study using the Phyre server Nat. Protocols 4 2009 363 371
26. +-ATPase subunit ATP6V0A2 Nat. Genet. 40 2008 32 34
27. 0 motor Proc. Natl. Acad. Sci. USA 107 2010 1367 1372
28. +-driven ATP synthase Nature 481 2011 214 218
29. P. Lu, X.C. Bai, D. Ma, T. Xie, C. Yan, L. Sun, G. Yang, Y. Zhao, R. Zhou, S.H. Scheres, and Y. Shi Three-dimensional structure of human γ-secretase Nature 512 2014 166 170
30. H. Makiyio, R. Iino, C. Ikeda, H. Imamura, M. Tamakoshi, M. Iwata, D. Stock, R.A. Bernal, E.P. Carpenter, and M. Yoshida Structure of a central stalk subunit F of prokaryotic V-type ATPase/synthase from Thermus thermophilus EMBO J. 24 2005 3974 3983
31. +-ATPase in vesicular trafficking: targeting, regulation and function Curr. Opin. Cell Biol. 20 2008 415 426
32. V. Marshansky, J.L. Rubinstein, and G. Grüber Eukaryotic V-ATPase: novel structural findings and functional insights Biochim. Biophys. Acta 1837 2014 857 879
33. +-ATPase from Ilyobacter tartaricus Science 308 2005 659 662
34. H. Merzendorfer, M. Huss, R. Schmid, W.R. Harvey, and H. Wieczorek A novel insect V-ATPase subunit M9.7 is glycosylated extensively J. Biol. Chem. 274 1999 17372 17378
35. J.A. Mindell, and N. Grigorieff Accurate determination of local defocus and specimen tilt in electron microscopy J. Mol. Biol. 142 2003 334 347
36. S.P. Muench, M. Huss, C. Phillips, C.F. Song, H. Wieczorek, J. Trinick, and M.A. Harrison Cryo-electron microscopy of the vacuolar ATPase motor reveals its mechanical and regulatory complexity J. Mol. Biol. 386 2009 989 999
37. S.P. Muench, J. Trinick, and M.A. Harrison Structural divergence of the rotary ATPases Q. Rev. Biophys. 44 2011 311 356
38. 1 motor of the Manduca sexta V-ATPase J. Mol. Biol. 426 2013 286 300
39. S.P. Muench, S. Rawson, V. Eyraud, A. Delmas, P. Da Silva, C. Phillips, J. Trinick, M.A. Harrison, F. Gressent, and M. Huss PA1b inhibitor binding to subunits c and e of the vacuolar ATPase reveals its insecticidal mechanism J. Biol. Chem. 289 2014 16399 16408
40. + ATPase from Enterococcus hirae Science 308 2005 654 659
41. T. Noumi, C. Beltran, H. Nelson, and N. Nelson Mutational analysis of yeast vacuolar H(+)-ATPase Proc. Natl. Acad. Sci. USA 88 1991 1938 1942
42. 1-ATPase EMBO Rep. 10 2009 1228 1234
43. R.A. Oot, L.S. Huang, E.A. Berry, and S. Wilkens Crystal structure of the yeast vacuolar ATPase heterotrimeric EGC(head) peripheral stalk complex Structure 20 2012 1881 1892
44. 1 complexes J. Biol. Chem. 275 2000 21761 21767
45. 0 symmetry mismatch is not obligatory EMBO J. 6 2005 1040 1044
46. R.A. Richardson, K. Papachristos, D.J. Read, O.G. Harlen, M.A. Harrison, E. Paci, S.P. Muench, and S.A. Harris Understanding the apparent stator-rotor connections in the rotary ATPase family using coarse-grained computer modelling Proteins 82 2014 3298 3311
47. P.B. Rosenthal, R.A. Crowther, and R. Henderson Optimal determination of particle orientation, absolute hand, and contrast loss in single-particle electron cryomicroscopy J. Mol. Biol. 333 2003 743 745
48. J.L. Rubinstein, J.E. Walker, and R. Henderson Structure of the mitochondrial ATP synthase by electron cryomicroscopy EMBO J. 22 2003 6182 6192
49. M. Sagermann, T.H. Stevens, and B.W. Matthews Crystal structure of the regulatory subunit H of the V-type ATPase of Saccharomyces cerevisiae Proc. Natl. Acad. Sci. USA 98 2001 7134 7139
50. S.H. Scheres RELION: implementation of a Bayesian approach to cryo-EM structure determination J. Struct. Biol. 180 2012 519 530
51. +-ATPase in human breast cancer cells with distinct metastatic potential: distribution and functional activity Am. J. Physiol. Cell Physiol. 286 2004 1443 1452
52. M.T. Smith, and J.L. Rubinstein Structural biology. Beyond blob-ology Science 345 2014 617 619
53. +-ATPase PLoS One 8 2013 e82207
54. S. Srinivasan, N.K. Vyas, M.L. Baker, and F.A. Quiocho Crystal structure of the cytoplasmic N-terminal domain of subunit I, a homolog of subunit a, of V-ATPase J. Mol. Biol. 412 2011 14 21
55. A.G. Stewart, L.K. Lee, M. Donohoe, J.J. Chaston, and D. Stock The dynamic stator stalk of rotary ATPases Nat. Commun. 3 2012 687
56. J.P. Sumner, J.A. Dow, F.G. Earley, U. Klein, D. Jäger, and H. Wieczorek Regulation of plasma membrane V-ATPase activity by dissociation of peripheral subunits J. Biol. Chem. 270 1995 5649 5653
57. K. Tabke, A. Albertmelcher, O. Vitavska, M. Huss, H.P. Schmitz, and H. Wieczorek Reversible disassembly of the yeast V-ATPase revisited under in vivo conditions Biochem. J. 462 2014 185 197
58. G. Tang, L. Peng, P.R. Baldwin, D.S. Mann, W. Jiang, I. Rees, and S.J. Ludtke EMAN2: an extensible image processing suite for electron microscopy J. Struct. Biol. 157 2007 38 46
59. M. Toei, S. Toei, and M. Forgac Definition of membrane topology and identification of residues important for transport in subunit A of the vacuolar ATPase J. Biol. Chem. 286 2011 35176 35186
60. L.G. Trabuco, E. Villa, K. Mitra, J. Frank, and K. Schulten Flexible fitting of atomic structures into electron microscopy maps using molecular dynamics Structure 16 2008 673 683
61. M. van Heel, G. Harauz, E.V. Orlova, R. Schmidt, and M. Schatz A new generation of the IMAGIC image processing system J. Struct. Biol. 116 1996 17 24
62. M. Vollmar, D. Schlieper, M. Winn, C. Buchner, and G. Groth Structure of the C(14) rotor ring of the proton translocating chloroplast ATP synthase J. Biol. Chem. 284 2009 18228 18235
63. Y. Wang, M. Toei, and M. Forgac Analysis of the membrane topology of transmembrane segments in the C-terminal hydrophobic domain of the yeast vacuolar ATPase subunit a (Vph1p) by chemical modification J. Biol. Chem. 283 2008 20696 20702
64. S. Wilkens, E. Vasilyeva, and M. Forgac Structure of the vacuolar ATPase by electron microscopy J. Biol. Chem. 274 1999 31804 31810
65. M. Zhou, N. Morgner, N.P. Barrera, A. Politis, S.C. Isaacson, D. Matak-Vinković, T. Murata, R.A. Bernal, D. Stock, and C.V. Robinson Mass spectrometry of intact V-type ATPases reveals bound lipids and the effects of nucleotide binding Science 334 2011 380 385