Cryo-electron Microscopy of the Vacuolar ATPase Motor Reveals its Mechanical and Regulatory Complexity

Journal of Molecular Biology

Volumn 386, Issue 4, 2009, Pages 989-999

  Muench, Stephen P ^a   Huss, Markus ^b   Song, Chun Feng ^a   Phillips, Clair ^a   Wieczorek, Helmut ^b   Trinick, John ^a   Harrison, Michael A ^a  

^a UNIVERSITY OF LEEDS   (United Kingdom)

^b UNIVERSITY OF OSNABRÜCK   (Germany)

Author keywords

3D reconstruction; cryo electron microscopy; H+ ATPase; vacuolar membrane

Indexed keywords

ADENOSINE TRIPHOSPHATASE; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE;

ARTICLE; CRYOELECTRON MICROSCOPY; CRYSTAL STRUCTURE; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME ASSAY; ENZYME REGULATION; ENZYME STRUCTURE; ENZYME SUBUNIT; MANDUCA SEXTA; MOLECULAR MODEL; NONHUMAN; NUCLEOTIDE SEQUENCE; OPTICAL RESOLUTION; PRIORITY JOURNAL; PROTEIN DOMAIN; THREE DIMENSIONAL IMAGING;

EUKARYOTA; MANDUCA SEXTA;

EID: 60149087436     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2009.01.014     Document Type: Article

References (64)

1. Forgac M. Vacuolar ATPases: rotary proton pumps in physiology and pathophysiology. Nature Rev. Mol. Cell Biol. 8 (2007) 917-929
2. + ATPase: molecular structure and function, physiological roles and regulation. J. Exp. Biol. 209 (2006) 577-589
3. 1-ATPase. Proc. Natl Acad. Sci. USA 100 (2003) 2312-2315
4. Noji H., Yasuda R., Yoshida M., and Kinosita K. Direct observation of the rotation of F-1-ATPase. Nature 386 (1997) 299-302
5. Wilkens S., Vasilyeva E., and Forgac M. Structure of the vacuolar ATPase by electron microscopy. J. Biol. Chem. 274 (1999) 31804-31810
6. 1-ATPase determined by mass spectrometry. J. Biol. Chem. 283 (2008) 3329-3337
7. +-ATPase from Enterococcus hirae. Science 308 (2005) 654-659
8. Nelson N. Evolution of organellar proton-ATPases. Biochim. Biophys. Acta 1100 (1992) 109-124
9. +-ATPase from Enterococcus hirae and its V-0 moiety. J. Biochem. 125 (1999) 414-421
10. Hirata T., Iwamoto-Kihara A., Sun-Wada G.H., Okajima T., Wada Y., and Futai M. Subunit rotation of vacuolar-type proton pumping ATPase: relative rotation of the G and c subunits. J. Biol. Chem. 278 (2003) 23714-23719
11. Rubinstein J.L., Walker J.E., and Henderson R. Structure of the mitochondrial ATP synthase by electron cryomicroscopy. EMBO J. 22 (2003) 6182-6192
12. Lau W.C.Y., Baker L.A., and Rubinstein J.L. Cryo-EM structure of the yeast ATP synthase. J. Mol. Biol. 382 (2008) 1256-1264
13. Gregorini M., Wang J., Xie X.S., Milligan R.A., and Engel A. Three-dimensional reconstruction of bovine brain V-ATPase by cryo-electron microscopy and single particle analysis. J. Struct. Biol. 158 (2007) 445-454
14. Venzke D., Domgall I., Kocher T., Féthière J., Fischer S., and Böttcher B. Elucidation of the stator organization in the V-ATPase of Neurospora crassa. J. Mol. Biol. 349 (2005) 659-669
15. Wilkens S., Inoue T., and Forgac M. Three-dimensional structure of the vacuolar ATPase: localization of subunit H by difference imaging and chemical cross-linking. J. Biol. Chem. 279 (2004) 41942-41949
16. Zhang Z., Zheng Y., Mazon H., Milgrom E., Kitagawa N., Kish-Trier E., et al. Structure of the yeast vacuolar ATPase. J. Biol. Chem. 283 (2008) 35983-35995
17. Sumner J.P., Dow J.A., Earley F.G., Klein U., Jager D., and Wieczorek H. Regulation of plasma membrane V-ATPase activity by dissociation of peripheral subunits. J. Biol. Chem. 270 (1995) 5649-5653
18. Kane P.M. Disassembly and reassembly of the yeast vacuolar H(+)-ATPase in vivo. J. Biol. Chem. 270 (1995) 17025-17032
19. Graf R., Harvey W.R., and Wieczorek H. Purification and properties of a cytosolic V-1 ATPase. J. Biol. Chem. 271 (1996) 20908-20913
20. +-ATPase by protein kinase A. J. Biol. Chem. 282 (2007) 33735-33742
21. Hong-Hermesdorf A., Brux A., Grüber A., Grüber G., and Schumacher K. A WNK kinase binds and phosphorylates V-ATPase subunit C. FEBS Lett. 580 (2006) 932-939
22. 1 complexes. J. Biol. Chem. 275 (2000) 21761-21767
23. Domgall I., Venzke D., Luttge U., Ratajczak R., and Böttcher B. Three-dimensional map of a plant V-ATPase based on electron microscopy. J. Biol. Chem. 277 (2002) 13115-13121
24. Zhang Z., Inoue T., Forgac M., and Wilkens S. Localization of subunit C (Vma5p) in the yeast vacuolar ATPase by immuno electron microscopy. FEBS Lett. 580 (2006) 2006-2010
25. Schweikl H., Klein U., Schindlbeck M., and Wieczorek H. A vacuolar-type ATPase, partially purified from potassium transporting plasma membranes of tobacco hornworm midgut. J. Biol. Chem. 264 (1989) 11136-11142
26. Wieczorek H., Cioffi M., Klein U., Harvey W.R., Schweikl H., and Wolfersberger M.G. Isolation of goblet cell apical membrane from tobacco hornworm midgut and purification of its vacuolar-type ATPase. In: Fleischer S., and Fleischer B. (Eds). Methods in Enzymology (Part W): Biomembranes: Cellular and Subcellular Transport (1990), Academic Press, San Diego and London 608-616
27. 0 complexes. FEBS Lett. 581 (2007) 5566-5572
28. Ludtke S.J., Baldwin P.R., and Chiu W. EMAN: semiautomated software for high-resolution single particle reconstructions. J. Struct. Biol. 128 (1999) 82-97
29. van Heel M., Smith A.E., Smith A.E., Smith A.E., Smith A.E., and Smith A.E. A new generation of the IMAGIC image processing system. J. Struct. Biol. 116 (1996) 17-24
30. Diepholz M., Borsch M., and Böttcher B. Structural organization of the V-ATPase and its implications for regulatory assembly and disassembly. Biochem. Soc. Trans. 36 (2008) 1027-1031
31. Kawasaki-Nishi S., Nishi T., and Forgac M. 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
32. Maegawa Y., Morita H., Iyaguchi D., Yao M., Watanabe N., and Tanaka I. Structure of the catalytic nucleotide-binding subunit A of A-type ATP synthase from Pyrococcus horikoshii reveals a novel domain related to the peripheral stalk. Acta Crystallogr. D 62 (2006) 483-488
33. 0 subunits A and B. J. Mol. Biol. 358 (2006) 725-740
34. 0 Domain. J. Biol. Chem. 280 (2005) 27896-27903
35. Jones R.P.O., Durose L.J., Findlay J.B.C., and Harrison M.A. Defined sites of interaction between subunits E (Vma4p), C (Vma5p), and G (Vma10p) within the stator structure of the vacuolar H+-ATPase. Biochemistry 44 (2005) 3933-3941
36. 1 sector. J. Biol. Chem. 275 (2000) 15449-15457
37. Drory O., Frolow F., and Nelson N. Crystal structure of yeast V-ATPase subunit C reveals its stator function. EMBO Rep. 5 (2004) 1148-1152
38. Sagermann M., Stevens T.H., and Matthews B.W. Crystal structure of the regulatory subunit H of the V-type ATPase of Saccharomyces cerevisiae. Proc. Natl Acad. Sci. USA 98 (2001) 7134-7139
39. Bauerle C., Ho M.N., Lindorfer M.A., and Stevens T.H. The Saccharomyces cerevisiae VMA6 gene encodes the 36-kDa subunit of the vacuolar H(+)-ATPase membrane sector. J. Biol. Chem. 268 (1993) 12749-12757
40. Iwata M., Imamura H., Stambouli E., Ikeda C., Tamakoshi M., Nagata K., et al. Crystal structure of a central stalk subunit C and reversible association/dissociation of vacuole-type ATPase. Proc. Natl Acad. Sci. USA 101 (2004) 59-64
41. Makiyio H., Iino R., Ikeda C., Imamura H., Tamakoshi M., Iwata M., et al. Structure of a central stalk subunit F of prokaryotic V-type ATPase/synthase from Thermus thermophilus. EMBO J. 24 (2005) 3974-3983
42. Féthière J., Venzke D., Diepholz M., Seybert A., Geerlof A., Gentzel M., et al. Building the stator of the yeast vacuolar-ATPase: specific interaction between subunits E and G. J. Biol. Chem. 279 (2004) 40670-40676
43. +-ATPase. J. Mol. Biol. 366 (2007) 933-944
44. 1-ATPase from bovine heart mitochondria. Nature 370 (1994) 621-628
45. Nelson N. Organellar proton-ATPases. Curr. Opin. Cell Biol. 4 (1992) 654-660
46. 1 complex. J. Biol. Chem. 281 (2006) 22752-22760
47. Féthière J., Venzke D., Madden D.R., and Böttcher B. Peripheral stator of the yeast V-ATPase: stoichiometry and specificity of interaction between the EG complex and subunits C and H. Biochemistry 44 (2005) 15906-15914
48. Xu T., Vasilyeva E., and Forgac M. Subunit interactions in the clathrin-coated vesicle vacuolar (H+)-ATPase complex. J. Biol. Chem. 274 (1999) 28909-28915
49. +-ATPase are linked by an interaction between the G and a subunits. J. Biol. Chem. 282 (2007) 14421-14427
50. +-ATPase (V-ATPase) interacts with the H subunit and is required for V-ATPase function. J. Biol. Chem. 277 (2002) 38409-38415
51. +-ATPase. J. Biol. Chem. 277 (2002) 3357-3363
52. 0 domain subunits and efficient osteoclastic bone resorption. J. Biol. Chem. 283 (2008) 13194-13204
53. Kane Dickson V., Silvester J.A., Fearnley I.M., Leslie A.G., and Walker J.E. On the structure of the stator of the mitochondrial ATP synthase. EMBO J. 25 (2006) 2911-2918
54. Dunn S.D., McLachlin D.T., and Revington M. The second stalk of Escherichia coli ATP synthase. Biochim. Biophys. Acta 1458 (2000) 356-363
55. 0 parts of the Escherichia coli ATP synthase. Biochim. Biophys. Acta 1365 (1998) 93-97
56. Stock D., Leslie A.G.W., and Walker J.E. Molecular architecture of the rotary motor in ATP synthase. Science 286 (1999) 1700-1705
57. 1-ATPase rotates in the correct direction. Science 319 (2008) 955-958
58. Ho M.N., Hirata R., Umemoto N., Ohya Y., Takatsuki A., Stevens T.H., and Anraku Y. VMA13 encodes a 54-kDa vacuolar H(+)-ATPase subunit required for activity but not assembly of the enzyme complex in Saccharomyces cerevisiae. J. Biol. Chem. 268 (1993) 18286-18292
59. 1 domain by interaction with the rotary subunit F. J. Biol. Chem. 283 (2008) 4512-4519
60. Beltran C., and Nelson N. The membrane sector of vacuolar H(+)-ATPase by itself is impermeable to protons. Acta Physiol. Scand. 607 (1992) 41-47
61. 0 subunit d that is critical for coupling of the yeast vacuolar proton-translocating ATPase. J. Biol. Chem. 281 (2006) 30001-30014
62. White H.D., Thirumurugan K., Walker M.L., and Trinick J. A second generation apparatus for time resolved electron cryo-microscopy using stepper motors and electrospray. J. Struct. Biol. 144 (2003) 246-252
63. Mindella J.A., and Grigorieff N. Accurate determination of local defocus and specimen tilt in electron microscopy. J. Struct. Biol. 142 (2003) 334-337
64. Frank J., Smith A.E., Smith A.E., Smith A.E., Smith A.E., Smith A.E., and Smith A.E. SPIDER and WEB: processing and visualization of images in 3D electron microscopy and related fields. J. Struct. Biol. 116 (1996) 190-199