Electron cryomicroscopy observation of rotational states in a eukaryotic V-ATPase

Nature

Volumn 521, Issue 7551, 2015, Pages 241-245

  Zhao, Jianhua ^a,b   Benlekbir, Samir ^a   Rubinstein, John L ^a,b  

^a HOSPITAL FOR SICK CHILDREN RESEARCH INSTITUTE   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; MEMBRANE PROTEIN; PROTEOLIPID; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; ADENOSINE TRIPHOSPHATE; LIPID BILAYER; PROTEIN SUBUNIT; PROTON;

BACTERIUM; CATALYSIS; ELECTRON MICROSCOPY; ENZYME ACTIVITY; EUKARYOTE; EXPERIMENTAL STUDY; MEMBRANE; OBSERVATIONAL METHOD; PH; SOLUBILIZATION; YEAST;

ARTICLE; CONFORMATIONAL TRANSITION; CRYOELECTRON MICROSCOPY; CRYSTAL STRUCTURE; CRYSTALLIZATION; ENZYME ACTIVE SITE; ENZYME CONFORMATION; HYDROLYSIS; NONHUMAN; NUCLEOTIDE BINDING SITE; PRIORITY JOURNAL; PROTON TRANSPORT; ROTATION; SACCHAROMYCES CEREVISIAE; STOICHIOMETRY; YEAST; BIOCATALYSIS; CELL MEMBRANE; CHEMICAL STRUCTURE; CHEMISTRY; ENZYMOLOGY; LIPID BILAYER; METABOLISM; PLIABILITY; PROTEIN CONFORMATION; PROTEIN SUBUNIT; SOLUBILITY; ULTRASTRUCTURE;

EUKARYOTA; SACCHAROMYCES CEREVISIAE;

ADENOSINE TRIPHOSPHATE; BIOCATALYSIS; CELL MEMBRANE; CRYOELECTRON MICROSCOPY; LIPID BILAYERS; MODELS, MOLECULAR; PLIABILITY; PROTEIN CONFORMATION; PROTEIN SUBUNITS; PROTONS; ROTATION; SACCHAROMYCES CEREVISIAE; SOLUBILITY; VACUOLAR PROTON-TRANSLOCATING ATPASES;

EID: 84929335211     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature14365     Document Type: Article

References (51)

1. Sumner, J. P. et al. Regulation of plasma membrane V-ATPase activity by dissociation of peripheral subunits. J. Biol. Chem. 270, 5649-5653 (1995).
2. Kane, P. M. Disassembly and reassembly of the yeast vacuolar H+-ATPase in vivo. J. Biol. Chem. 270, 17025-17032 (1995).
3. Pänke, O., Cherepanov, D. A., Gumbiowski, K., Engelbrecht, S. & Junge, W. Viscoelastic dynamics of actin filaments coupled to rotary F-ATPase: angular torque profile of the enzyme. Biophys. J. 81, 1220-1233 (2001).
4. Stewart, A. G., Lee, L. K., Donohoe, M., Chaston, J. J. & Stock, D. The dynamic stator stalk of rotary ATPases. Nature Commun. 3, 687 (2012).
5. Zhou, M. et al. Ion mobility-mass spectrometry of a rotary ATPase reveals ATP-induced reduction in conformational flexibility. Nature Chem. 6, 208-215 (2014).
6. Walker, J. E. ATP synthesis by rotary catalysis (Nobel Lecture). Angew. Chem. Int. Edn 37, 2309-2319 (1998).
7. Walker, J. E. Keilin Memorial Lecture. The ATP synthase: the understood, the uncertain and the unknown. Biochem. Soc. Trans. 41, 1-16 (2013).
8. Arai, S. et al. Rotation mechanism of Enterococcus hirae V1-ATPase based on asymmetric crystal structures. Nature 493, 703-707 (2013).
9. Benlekbir, S., Bueler, S. A. & Rubinstein, J. L. Structure of the vacuolar-type ATPase from Saccharomyces cerevisiae at 11-Å resolution. Nature Struct. Mol. Biol. 19, 1356-1362 (2012).
10. Rawson, S. et al. Structure of the vacuolar H+-ATPase rotary motor reveals new mechanistic insights. Structure 23, 461-471 (2015).
11. Amunts, A. et al. Structure of the yeast mitochondrial large ribosomal subunit. Science 343, 1485-1489 (2014).
12. Trabuco, L. G., Villa, E., Mitra, K., Frank, J. & Schulten, K. Flexible fitting of atomic structures into electron microscopy maps using molecular dynamics. Structure 16, 673-683 (2008).
13. Hirata, R., Graham, L. A., Takatsuki, A., Stevens, T. H. & Anraku, Y. VMA11 and VMA16 encode second and third proteolipid subunits of the Saccharomyces cerevisiae vacuolar membrane H+-ATPase. J. Biol. Chem. 272, 4795-4803 (1997).
14. Nishi, T., Kawasaki-Nishi, S. & Forgac, M. The first putative transmembrane segment of subunit c″ (Vma16p) of the yeast V-ATPase is not necessary for function. J. Biol. Chem. 278, 5821-5827 (2003).
15. Matthies, D. et al. High-resolution structure and mechanism of an F/V-hybrid rotor ring in a Na+-coupled ATP synthase. Nature Commun. 5, 5286 (2014).
16. Nishi, T., Kawasaki-Nishi, S. & Forgac, M. Expression and localization of the mouse homologue of the yeast V-ATPase 21-kDa subunit c″ (Vma16p). J. Biol. Chem. 276, 34122-34130 (2001).
17. Powell, B., Graham, L. A. & Stevens, T. H. Molecular characterization of the yeast vacuolar H+-ATPase proton pore. J. Biol. Chem. 275, 23654-23660 (2000).
18. Finnigan, G. C., Hanson-Smith, V., Stevens, T. H. & Thornton, J. W. Evolution of increased complexity in a molecular machine. Nature 481, 360-364 (2012).
19. Stock, D., Leslie, A. G. & Walker, J. E. Molecular architecture of the rotary motor in ATP synthase. Science 286, 1700-1705 (1999).
20. Nicholls, D. G. & Ferguson, S. J. Bioenergetics 3rd edn, Ch. 3 (Academic, 2002).
21. Bueler, S. A. & Rubinstein, J. L. Vma9p need not be associated with the yeast V-ATPase for fully-coupled proton pumping activity in vitro. Biochemistry 54, 853-858 (2015).
22. Toei, M., Toei, S. & Forgac, M. Definition ofmembranetopology and identification of residues important for transport in subunit a of the vacuolar ATPase. J. Biol. Chem. 286, 35176-35186 (2011).
23. Junge, W. & Nelson, N. Structural biology. Nature's rotary electromotors. Science 308, 642-644 (2005).
24. Lau, W. C. Y. & Rubinstein, J. L. Subnanometre-resolution structure of the intact Thermus thermophilus H+-driven ATP synthase. Nature 481, 214-218 (2012).
25. Abrahams, J. P., Leslie, A. G., Lutter, R. & Walker, J. E. Structure at 2.8 Å resolution of F1-ATPase from bovine heart mitochondria. Nature 370, 621-628 (1994).
26. Cingolani, G. & Duncan, T. M. Structure of the ATP synthase catalytic complex (F(1)) from Escherichia coli in an autoinhibited conformation. Nature Struct. Mol. Biol. 18, 701-707 (2011).
27. Numoto, N., Hasegawa, Y., Takeda, K. & Miki, K. Inter-subunit interaction and quaternary rearrangement defined by the central stalk of prokaryotic V1-ATPase. EMBO Rep. 10, 1228-1234 (2009).
28. Kabaleeswaran, V. et al. Asymmetric structure of the yeast F1 ATPase in the absence of bound nucleotides. J. Biol. Chem. 284, 10546-10551 (2009).
29. Wächter, A. et al. Two rotary motors in F-ATP synthase are elastically coupled by a flexible rotor and a stiff stator stalk. Proc. Natl Acad. Sci. USA 108, 3924-3929 (2011).
30. Marr, C. R., Benlekbir, S. & Rubinstein, J. L. Fabrication of carbon films with approximately 500 nm holes for cryo-EM with a direct detector device. J. Struct. Biol. 185, 42-47 (2014).
31. Rubinstein, J. L. & Brubaker, M. A. Alignment of cryo-EM movies of individual particles by optimization of image translations. ArXiv 1409, 1-11 (2014).
32. Mindell, J. A. & Grigorieff, N. Accurate determination of local defocus and specimen tilt in electron microscopy. J. Struct. Biol. 142, 334-347 (2003).
33. Zhao, J., Brubaker, M. A. & Rubinstein, J. L. TMaCS: a hybrid template matching and classification system for partially-automated particle selection. J. Struct. Biol. 181, 234-242 (2013).
34. Zhao, J., Brubaker, M. A., Benlekbir, S. & Rubinstein, J. L. Description and comparison of algorithms for correcting anisotropic magnification in cryo-EM images. ArXiv 1501, 1-10 (2015).
35. Scheres, S. H. RELION: implementation of a Bayesian approach to cryo-EM structure determination. J. Struct. Biol. 180, 519-530 (2012).
36. Scheres, S. H. W. et al. Disentangling conformational states of macromolecules in 3D-EM through likelihood optimization. Nature Methods 4, 27-29 (2007).
37. Kucukelbir, A., Sigworth, F. J. & Tagare, H. D. Quantifying the local resolution of cryo-EM density maps. Nature Methods 11, 63-65 (2014).
38. Loken, C. et al. SciNet: lessons learned from building a power-efficient top-20 system and data centre. J. Phys. Conf. Ser. 256, 012026 (2010).
39. Goddard, T. D., Huang, C. C. & Ferrin, T. E. Visualizing density maps with UCSF Chimera. J. Struct. Biol. 157, 281-287 (2007).
40. Pintilie, G. D., Zhang, J., Goddard, T. D., Chiu, W. & Gossard, D. C. Quantitative analysis of cryo-EM density map segmentation by watershed and scale-space filtering, and fitting of structures by alignment to regions. J. Struct Biol. 170, 427-438 (2010).
41. Kelley, L. A. & Sternberg, M. J. Protein structure prediction on the Web: a case study using the Phyre server. Nature Protocols 4, 363-371 (2009).
42. Söding, J., Biegert, A. & Lupas, A. N. The HHpred interactive server for protein homology detection and structure prediction. Nucleic Acids Res. 33, 244-248 (2005).
43. Sali, A. & Blundell, T. L. Comparative protein modelling by satisfaction of spatial restraints. J. Mol. Biol. 234, 779-815 (1993).
44. Drory, O., Frolow, F. & Nelson, N. Crystal structure of yeast V-ATPase subunit C reveals its stator function. EMBO Rep. 5, 1148-1152 (2004).
45. Sagermann, M., Stevens, T. H. & Matthews, B. W. Crystal structure of the regulatory subunit H of the V-type ATPase of Saccharomyces cerevisiae. Proc. Natl Acad. Sci. USA 98, 7134-7139 (2001).
46. Balakrishna, A. M., Basak, S., Manimekalai, M. S. S. & Gruber, G. Crystal structure of subunits D and F in complex give insight into energy transmission of the eukaryotic V-ATPase from Saccharomyces cerevisiae. J. Biol. Chem. 290, 3183-3196 (2015).
47. Oot, R. A., Huang, L. S., Berry, E. A. & Wilkens, S. Crystal structure of the yeast vacuolar ATPase heterotrimeric EGC(head) peripheral stalk complex. Structure 20, 1881-1892 (2012).
48. Iwata, M. et al. Crystal structure of a central stalk subunit C and reversible association/dissociation of vacuole-type ATPase. Proc. Natl Acad. Sci. USA 101, 59-64 (2004).
49. Srinivasan, S., Vyas, N. K., Baker, M. L. & Quiocho, F. A. Crystal structure of the cytoplasmic N-terminal domain of subunit I, a homolog of subunit a, of V-ATPase. J. Mol. Biol. 412, 14-21 (2011).
50. Murata, T., Yamato, I., Kakinuma, Y., Leslie, A. G. & Walker, J. E. Structure of the rotor of the V-Type Na+-ATPase from Enterococcus hirae. Science 308, 654-659 (2005).
51. Chen, S. et al. High-resolution noise substitution to measure overfitting and validate resolution in 3D structure determination by single particle electron cryomicroscopy. Ultramicroscopy 135, 24-35 (2013).