Structure of the vacuolar adenosine triphosphatases

Cell Biochemistry and Biophysics

Volumn 34, Issue 2, 2001, Pages 191-208

  Wilkens, Stephan ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Electron microscopy; Protein structure; Vacuolar ATPase

Indexed keywords

EUKARYOTA;

ADENOSINE TRIPHOSPHATE; PROTON; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATASE;

ANIMAL; BIOLOGICAL MODEL; BRAIN; CATTLE; CHEMISTRY; ELECTRON MICROSCOPY; HYDROLYSIS; METABOLISM; PH; PHYSIOLOGY; PROTEIN CONFORMATION; PROTEIN TERTIARY STRUCTURE; REVIEW; ULTRASTRUCTURE;

ADENOSINE TRIPHOSPHATE; ANIMALS; BRAIN; CATTLE; HYDROGEN-ION CONCENTRATION; HYDROLYSIS; MICROSCOPY, ELECTRON; MODELS, BIOLOGICAL; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; PROTON-TRANSLOCATING ATPASES; PROTONS;

EID: 0035753543     PISSN: 10859195     EISSN: None     Source Type: Journal    
DOI: 10.1385/CBB:34:2:191     Document Type: Review

References (121)

1. Stevens, T. H. and Forgac, M. (1997) Structure, function and regulation of the vacuolar (H+)-ATPase. Annu. Rev. Cell Dev. Biol. 13, 779-808.
2. Finbow, M. E. and Harrison, M. A. (1997) The vacuolar H+-ATPase: a universal proton pump of eukaryotes. Biochem. J. 324, 697-712.
3. Nelson, N. and Harvey, W. R. (1999) Vacuolar and plasma membrane V-ATPases. Physiol. Rev. 79, 361-385.
4. +-translocating ATPase in Enterococcus hirae. J. Bioenerg. Biomembr. 32, 7-14.
5. 1 type ATPsynthase from the acidothermophilic archaebacterium, Sulfolobus acidocaldarius. J. Biol. Chem. 263, 17,251-17,254.
6. Boyer, P. D. (1997) The ATP synthase - a splendid molecular machine. Ann. Rev. Biochem. 66, 717-749.
7. Senior, A. E. (1988) ATP synthesis by oxidative phosphorylation. Physiol Rev. 68, 177-231.
8. Hirata, T., Nakamura, N., Omote, H., Wada, Y., and Futai, M. (2000) Regulation and reversibility of vacuolar H+-ATPase. J. Biol. Chem. 275, 386-389.
9. Xie, X.-S. and Stone, D. K. (1986) Isolation and reconstitution of the clathrin-coated vesicle proton translocating complex. J. Biol. Chem. 261, 2492-2495.
10. Arai, H., Berne, M., Terres, G., Terres, H., Puopolo, K., and Forgac, M. (1987) Subunit composition and ATP site labeling of the coated vesicle proton-translocating adenosinetriphosphatatse. Biochemistry 26, 6632-6638.
11. +-ATPase complex. J. Exp. Biol. 203, 61-70.
12. Arai, H., Terres, G., Pink, S., and Forgac, M. (1988) Topography and subunit stoichiometry of the coated vesicle proton pump. J. Biol. Chem. 263, 8796-8802.
13. +)-ATPase complex. J. Biol. Chem. 274, 28,909-28,915.
14. 1-ATPases. J. Biol. Chem. 263, 9102-9112.
15. Bowman, E. J., Tenney, K., and Bowman, B. J. (1988) Isolation of genes encoding the Neurospora vacuolar ATPase. Analysis of vma-1 encoding the 67-kDa subunit reveals homology to other ATPases. J. Biol. Chem. 263, 13,994-14,001.
16. + translocating adenosine triphosphatase from vacuolar membranes of Saccharomyces cerevisiae. J. Biol. Chem. 265, 6726-6733.
17. Puopolo, K., Kumamoto, C, Adachi, I., Magner, R., and Forgac, M. (1992) Differential expression of the "B" subunit of the vacuolar H(+)-ATPase in bovine tissues. J. Biol. Chem. 267, 3696-3706.
18. 32P]ATP. J. Biol. Chem. 270, 15,494-15,500.
19. Vasilyeva, E. and Forgac, M. (1996) 3′-O-(4-Benzoyl)benzoyladenosine 5′-triphosphate inhibits activity of the vacuolar (H+)-ATPase from bovine brain clathrin-coated vesicles by modification of a rapidly exchangeable, non-catalytic nucleotide binding site on the B subunit. J. Biol. Chem. 271, 12,775-12,782.
20. Forgac, M. (1999) Structure and properties of the clathrin-cocited vesicle and yeast vacuolar V-ATPases. J. Bioenerg. Biomembr. 31, 57-65.
21. +-ATPases. J. Exp. Biol. 203, 71-80.
22. 1-ATPase. Biochem. Biophys Acta 1319, 19-58.
23. 1-ATPase from bovine heart mitochondria. Nature 370, 621-628.
24. Liu, Q., Leng, X.-H., Newman, P. R., Vasilyeva, E., Kane, P. M., and Forgac, M. (1997) Site-directed mutagenesis of the yeast V-ATPase A subunit. J. Biol. Chem. 272, 11,750-11,756.
25. Liu, Q., Kane, P. M., Newman, P. R., and Forgac, M. (1996) Site-directed mutagenesis of the yeast V-ATPase B subunit (Vma2p). J. Biol. Chem. 269, 31,592-31,597.
26. MacLeod, K. J., Vasilyeva, E., Baleja, J. D., and Forgac, M. (1998) Mutational analysis of the nucleotide binding sites of the yeast V-ATPase. J. Biol. Chem. 273, 150-156.
27. Feng, Y. and Forgac, M. (1994) Inhibition of vacuolar H(+)-ATPase by disulfide bond formation between cysteine 254 and cysteine 532 in subunit A. J. Biol. Chem. 269, 13,224-13,230.
28. 1-ATPase B subunit. J. Struct. Biol. 127, 79-82.
29. +-ATPase. J. Biol. Chem. 268, 221-227.
30. Doherty, R. D., and Kane, P. M. (1993) Partial assembly of the yeast vacuolar H(+)-ATPase in mutants lacking one subunit of the enzyme. J. Biol. Chem. 268, 16,845-16,851.
31. Puopolo, K., Sczekan, M., Magner, R., and Forgac, M. (1992) The 40-kDa subunit enhances but is not required for activity of the coated vesicle proton pump. J. Biol. Chem. 267, 5171-5176.
32. +-ATPase. J. Exp. Biol. 203, 81-87.
33. 1 complexes. J. Biol. Chem. 275, 21,761-21,767.
34. 1-ATPase. J. Biol. Chem. 271, 20,908-20,913.
35. +)-ATPase. Proc. Natl. Acad. Sci. USA 92, 497-501.
36. Bowman, E. J., Steinhardt, A., and Bowman, B. J. (1995) Isolation of the vma-4 gene encoding the 26 kDa subunit of the Neurospora crassa vacuolar ATPase. Biochim. Biophys. Acta 1237, 95-98.
37. +)-ATPase required for function and assembly of the enzyme complex. J. Biol. Chem. 270, 15,037-15,044.
38. Nelson, H., Mandiyan, S., and Nelson, N. (1994) The Saccharomyces cerevisiae VMA7 gene encodes a 14-kDa subunit of the vacuolar H(+)-ATPase catalytic sector. J. Biol. Chem. 269, 24,150-24,155.
39. +)-ATPase complex. J. Biol. Chem. 269, 25,974-25,977.
40. +)-ATPase. J. Biol. Chem. 270, 13,726-13,732.
41. +)-ATPase related to the b subunit of F-ATPases. J. Exp. Biol. 199, 1147-1156.
42. 1-situated stalk subunits of the yeast vacuolar proton-translocating ATPase. J. Biol. Chem. 272, 26,787-26,793.
43. +-V-ATPase. J. Exp. Biol. 203, 127-135.
44. +)-ATPase subunit required for activity but not assembly of the enzyme complex in Saccharomyces cerevisiae. J. Biol. Chem. 268, 18,286-18,292.
45. Xie, X. S., Crider, B. P., Ma, Y. M., and Stone, D. K. (1994) Role of a 50-57-kDa polypeptide heterodimer in the function of the clathrin-coated vesicle proton pump. J. Biol. Chem. 269, 25,809-25,815.
46. Xie, X. S. (1996) Reconstitution of ATPase activity from individual subunits of the clathrin-coated vesicle proton pump. J. Biol. Chem. 271, 30,980-30,985.
47. +)-ATPase requires the 50 kDa subunit of the clathrin assembly complex AP-2. J. Biol. Chem. 269, 32,592-31,597.
48. Zhou, Z., Peng, S.-B., Crider, B. P., Andersen, P., Xie, X.-S., and Stone, D. K. (1999) Recombinant SFD isoforms activate vacuolar proton pumps. J. Biol. Chem. 274, 15,913-15,919.
49. +-ATPase of Saccharomyces cerevisiae. Acta Cryst. 56, 475-477.
50. +-ATPase. J. Biol. Chem. 271, 22,487-22,493.
51. +-ATPase. J. Biol. Chem. 267, 14,294-14,303.
52. Manolson, M. F., Wu, B., Proteau, D., Taillon, B. E., Roberts, B. T., Hoyt, M. A., and Jones, E. W. (1994) STV1 gene encodes functional homologue of 95-kDa yeast vacuolar H(+)-ATPase subunit Vph1p. J. Biol. Chem. 269, 14,064-14,074.
53. Leng, X. H., Nishi, T., and Forgac, M. (1999) Transmembrane topography of the 100 kDa a subunit (Vph1p) of the yeast vacuolar protontranslocating ATPase. J. Biol. Chem. 274, 14,655-14,661.
54. +-ATPases. Proc. Natl. Acad. Sci. USA 85, 5521-5524.
55. Arai, H., Berne, M., and Forgac, M. (1987) Inhibition of the coated vesicle proton pump and labeling of a 17000 Dalton polypeptide by DCCD. J. Biol. Chem. 262, 11,006-11,011.
56. +)-ATPase activity. J. Biol. Chem. 266, 24,526-24,532.
57. +-ATPase. J. Biol. Chem. 272, 4795-4803.
58. Oka, T., Yamamoto, R., and Futai, M. (1998) Multiple genes for vacuolar-type ATPase proteolipids in Caenorhabditis elegans. A new gene, vha-3, has a distinct cell-specific distribution. J. Biol. Chem. 273, 22,570-22,576.
59. +)-ATPase from Arabidopsis thaliana. Plant Mol. Biol. 29, 227-244.
60. Nishigori, H., Yamada, S., Tomura, H., Fernald, A. A., Beau, M. M. L., Takeuchi, T., and Takeda, J. (1998) Identification and characterization of the gene encoding a second proteolipid subunit of human vacuolar H+-ATPase (ATP6F). Genomics 50, 222-228.
61. Bäuerle, C., Ho, M. N., Lindorfer, M. A., and Stevens, T. H. (1993) The Saccharomyces cerevisiae VMA6 gene encodes the 36-kDa subunit of the vacuolar H(+)-ATPase membrane sector. J. Biol. Chem. 268, 12,749-12,757.
62. Supek, F., Supekova, L., Mandiyan, S., Pan, Y.-C., Nelson, H., and Nelson, N. (1994) A novel accessory subunit for vacuolar H-ATPase from chromaffin granules. J. Biol. Chem. 269, 24,102-24,106.
63. Ludwig, J., Kerscher, S., Brandt, U., Pfeiffer, K., Getlawi, F., Apps, D. K., and Schägger, H. (1998) Identification and characterization of a novel 9.2-kDa membrane sector-associated protein of vacuolar proton ATPase from chromaffin granules. J. Biol. Chem. 273, 10,939-10,947.
64. Merzendorfer, H., Huss, M., Schmid, R., Harvey, W. R., and Wieczorek, H. (1999) A novel insect V-ATPase subunit M9.7 is glycosylated extensively. J. Biol. Chem. 274, 17,372-17,378.
65. + ATPase. J. Cell. Biol. 105, 1637-1648.
66. 1-like structure. J. Biol. Chem. 264, 15,606-15,612.
67. Klink, R. and Lüttge, U. (1991) Electron microscopic demonstration of a "head and stalk" structure of the leaf vacuolar ATPase in Mesembryanthemum crystallinum L. Bot. Acta 104, 122-131.
68. +-ATPases of Daucus carota. Bot. Acta 104, 117-121.
69. Dschida, W. J. and Bowman, B. J. (1992) Structure of the vacuolar ATPase from Neurospora crassa as determined by electron microscopy. J. Biol. Chem. 267, 18,783-18,789.
70. Bowman, B. J., V'azquez-Laslop, N., and Bowman, E. J. (1992) The vacuolar ATPase of Neurospora crassa. J. Bioenerg. Biomembr. 24, 361-370.
71. Wilkens, S., Vasilyeva, E., and Forgac, M. (1999) Structure of the vacuolar ATPase by electron microscopy. J. Biol. Chem. 274, 31,804-31,810.
72. 0) of Escherichia coli from cryoelectron microscopy. Biochemistry 29, 5339-5343.
73. 1. J. Mol. Biol. 295, 387-391.
74. Boekema, E. J., Ubbink-Kok, T., Lolkema, J. S., Brisson, A., and Konings, W. N. (1997) Visualization of a peripheral stalk in V-type ATPase: evidence for the stator structure essential to rotational catalysis. Proc. Acad. Natl. Sci. USA 94, 14,291-14,293.
75. Boekema, E. J., Ubbink-Kok, T., Lolkema, J. S., Brisson, A., and Konings, W. N. (1998) Structure of V-type ATPase from Clostridium fervidus by electron microscopy. Photosynth. Res. 57, 267-273.
76. +-ATPase of the thermophilic bacterium Caloramator fervidus. J. Mol. Biol. 296, 311-321.
77. 0 in the ATPsynthase from Escherichia coli. Biochem. Biophys. Acta 1365, 93-97.
78. Wilkens, S. and Capaldi, R. A. (1998) ATPsynthases second stalk comes into focus. Nature 393, 29.
79. 1. J. Mol. Biol. 281, 757-762.
80. Karrasch, S. and Walker, J. E. (1999) Novel features in the structure of bovine ATPsynthase. J. Mol. Biol. 290, 379-384.
81. 1 ATPase: significance of structural homologies and diversities. Biochemistry 37, 17,659-17,663.
82. 1 ATPase visualized by electron microscopy. FEBS Lett. 453, 383-386.
83. 1-ATPase studied by electron microscopy and image processing. Biochim. Biophys. Acta 851, 353-360.
84. 1 adenosinetriphosphatase. Biochemistry 28, 4709-4716.
85. 1-ATPase of Escherichia coli. J. Mol. Biol. 173, 131-136.
86. 1 adenosinetriphosphatase decorated with monoclonal antibodies to individual subunits of the complex. Biochemistry 28, 4717-4724.
87. 0 domain of the coated vesicle proton-ATPase. J. Biol. Chem. 267, 9773-9778.
88. +-V-ATPase from tobacco hornworm midgut. J. Bioenerg. Biomembr. 31, 67-74.
89. 0 sector. J. Biol. Chem. 258, 604-609.
90. 0). EMBO J. 4, 515-518.
91. 0 complex of the Escherichia coli ATP synthase. Investigation by electron spectroscopic imaging and immuno electron microscopy. Eur. J. Biochem. 230, 58-67.
92. 0 ATP synthase in aqueous buffer. FEBS Lett. 397, 30-34.
93. +-transporting ATPases. Curr. Opin. Struct. Biol. 6, 491-498.
94. Margolles-Clark, E., Tenney, K., Bowman, E. J., and Bowman, B. J. (1999) The structure of the vacuolar ATPase in Neurospora crassa. J. Bioenerg. Biomembr. 31, 29-37.
95. Páli, T., Finbow, M. E., Holzenburg, A., Findlay, J. B., and Marsh, D. (1995) Lipid-protein interactions and assembly of the 16-kDa channel polypeptide from Nephrops norvegicus. Studies with spin-label electron spin resonance spectroscopy and electron microscopy. Biochemistry 34, 9211-9218.
96. John, S. A., Saner, D., Pitts, J. D., Holzenburg, A., Finbow, M. E., and Lal, R. (1997) Atomic force microscopy of arthropod gap junctions. J. Struct. Biol. 120, 22-31.
97. Stock, D., Leslie, A. G. W., and Walker, J. E. (1999) Molecular architecture of the rotary motor in ATP synthase. Science 286, 1700-1705.
98. Seelert, H., Poetsch, A., Dencher, N. A., Engel, A., Stahlberg, H., and Muller, D. J. (2000) Structural biology: proton-powered turbine of a plant motor. Nature 405, 418-119.
99. +-transporting ATPsynthase: functional dimers and trimers and determination of stoichiometry by cross-linking analysis. J. Biol. Chem. 273, 29,701-29,705.
100. 0 ATPase of Escherichia coli. J. Bacteriol. 180, 3205-3208.
101. Boekema, E. J., van Breemen, J. F. L., Brisson, A., Ubbink-Kok, T., Konings, W. N., and Lolkema, J. S. (1999) Connecting stalks in V-ATPase. Nature 401, 37-38.
102. Nelson, N., Perzov, N., Cohen, A., Hagai, K., Padler, V., and Nelson, H. (2000) Cellular biology of proton-motive force generation by V-ATPases. J. Exp. Biol. 203, 89-95.
103. Sumner, J. P, Dow, J. A., Earley, F. G., Klein, U., Jäger, D., and Wieczorek, H. (1995) Regulation of plasma membrane V-ATPase activity by dissociation of peripheral subunits. J. Biol. Chem. 270, 5649-5653.
104. +-ATPase in vivo. J. Biol. Chem. 270, 17,025-17,032.
105. Peng, S.-B., Li, X., Crider, B. P., Zhou, Z., Andersen, P., Tsai, S. J., Xie, X.-S., and Stone, D. K. (1999) Identification and reconstitution of an isofrom of the 116 kDa subunit of the vacuolar proton translocating ATPase. J. Biol. Chem. 275, 2549-2555.
106. +)-ATPase. Preferential expression of the a3 isoform during osteoclast differentiation. J. Biol. Chem. 275, 8760-8765.
107. Nishi, T. and Forgac, M. (2000) Molecular cloning and expression of three isoforms of the 100-kDa a subunit of the mouse vacuolar proton-translocating ATPase. J. Biol. Chem. 275, 6824-6830.
108. Crider, B. P., Andersen, P., White, A. E., Zhou, Z., Li, X., Mattsson, J. P., Lundberg, L., Keeling, D. J., Xie, X. S., Stone, D. K., and Peng, S. B. (1997) Subunit G of the vacuolar proton pump. Molecular characterization and functional expression. J. Biol. Chem. 272, 10,721-10,728.
109. Zhou, Z., Peng, S.-B., Crider, B. P., Slaughter, C., Xie, X.-S., and Stone, D. K. (1998) Molecular characterization of the 50- and 57-kDa subunits of the bovine vacuolar proton pump. J. Biol. Chem. 273, 5878-5884.
110. Legerton, T. L., Kanamori, K., Weiss, R. L., and Roberts, J. D. (1983) Measurements of cytoplasmic and vacuolar pH in Neurospora using nitrogen-15 nuclear magnetic resonance spectroscopy. Biochemistry 22, 899-903.
111. Futai, M., Oka, T., Sun-Wada, G.-H., Moriyama, Y., Kanazawa, H., and Wada, Y. (2000) Luminal acidification of diverse organelles by V-ATPase in animal cells. J. Exp. Biol. 203, 107-116.
112. + pump. J. Exp. Biol. 196, 361-373.
113. Muller, M., Irkens-Kiesecker, U., Rubinstein, B., and Taiz, L. (1996) On the mechanism of hyperacidification in lemon. Comparison of the vacuolar H(+)-ATPase activities of fruits and epicotyls. J. Biol. Chem. 271, 1916-1924.
114. 0-ATP synthases: glimpses of interacting parts in a dynamic molecular machine. J. Exp. Biol. 200, 217-224.
115. + transport to rotary catalysis in F-type ATPsynthases: structure and organization of the transmembrane rotary motor. J. Exp. Biol. 203, 9-17.
116. Junge, W., Lill, H., and Engelbrecht, S. (1997) ATP synthase: on electrochemical transducer with rotatory mechanics. TIBS 22, 420-423.
117. Boyer, P. (1993) The binding change mechanism for ATP synthase: some probabilities and possibilities. Biochim. Biophys. Acta 1140, 215-250.
118. Sabbert, D., Engelbrecht, S., and Junge, W. (1996) Intersubunit rotation in active F-ATPase. Nature 381, 623-626.
119. 1-ATP synthase during oxidative phosphorylation. Proc. Natl. Acad. Sci. USA 94, 10,583-10,587.
120. 1-ATPase. Nature 386, 299-302.
121. 3δ domain in the intact complex. J. Biol. Chem. 272, 19,621-19,624.