Structure and regulation of the vacuolar ATPases

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1777, Issue 7-8, 2008, Pages 599-604

  Cipriano, Daniel J ^a   Wang, Yanru ^a   Bond, Sarah ^a   Hinton, Ayana ^a   Jefferies, Kevin C ^a   Qi, Jie ^a   Forgac, Michael ^a  

^a TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

ATP dependent proton transport; Function of intracellular and plasma membrane V ATPases; Regulation of V ATPase activity; V ATPase structure; Vacuolar ATPases

Indexed keywords

PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE;

ACIDIFICATION; AMINO TERMINAL SEQUENCE; CARBOXY TERMINAL SEQUENCE; CELL MEMBRANE; CELL TYPE; CONDUCTANCE; ENZYME ACTIVITY; HYDROLYSIS; PH MEASUREMENT; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN STRUCTURE; PROTON TRANSPORT; REVIEW; STRUCTURE ANALYSIS;

ANIMALS; CELL MEMBRANE; ENDOCYTOSIS; ENDOSOMES; KINETICS; LYSOSOMES; MODELS, MOLECULAR; VACUOLAR PROTON-TRANSLOCATING ATPASES;

BACTERIA (MICROORGANISMS);

EID: 46349090602     PISSN: 00052728     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbabio.2008.03.013     Document Type: Review

References (76)

1. Forgac M. Vacuolar ATPases: rotary proton pumps in physiology and pathophysiology. Nat. Rev. Mol. Cell Biol. 8 (2007) 917-929
2. Nishi T., and Forgac M. The vacuolar (H+)-ATPases-nature's most versatile proton pumps. Nat. Rev. Mol. Cell Biol. 3 (2002) 94-103
3. Ghosh P., Dahms N.M., and Kornfeld S. Mannose 6-phosphate receptors: new twists in the tale. Nat. Rev. 4 (2003) 202-212
4. Gu F., and Gruenberg J. ARF1 regulates pH-dependent COP functions in the early endocytic pathway. J. Biol. Chem. 275 (2000) 8154-8160
5. Abrami L., Lindsay M., Parton R.G., Leppla S.H., and van der Goot F.G. Membrane insertion of anthrax protective antigen and cytoplasmic delivery of lethal factor occur at different stages of the endocytic pathway. J. Cell. Biol. 166 (2004) 645-651
6. Sun-Wada G.H., Toyomura T., Murata Y., Yamamoto A., Futai M., and Wada Y. The a3 isoform of V-ATPase regulates insulin secretion from pancreatic beta-cells. J. Cell. Sci. 119 (2006) 4531-4540
7. Wagner C.A., Finberg K.E., Breton S., Marshansky V., Brown D., and Geibel J.P. Renal vacuolar H+-ATPase. Physiol. Rev. 84 (2004) 1263-1314
8. Karet F.E., Finberg K.E., Nelson R.D., Nayir A., Mocan H., Sanjad S.A., Rodriguez-Soriano J., Santos F., Cremers C.W., Di Pietro A., Hoffbrand B.I., Winiarski J., Bakkaloglu A., Ozen S., Dusunsel R., Goodyer P., Hulton S.A., Wu D.K., Skvorak A.B., Morton C.C., Cunningham M.J., Jha V., and Lifton R.P. Mutations in the gene encoding B1 subunit of H+-ATPase cause renal tubular acidosis with sensorineural deafness. Nat. Genet. 21 (1999) 84-90
9. Frattini A., Orchard P.J., Sobacchi C., Giliani S., Abinun M., Mattsson J.P., Keeling D.J., Andersson A.K., Wallbrandt P., Zecca L., Notarangelo L.D., Vezzoni P., and Villa A. Defects in TCIRG1 subunit of the vacuolar proton pump are responsible for a subset of human autosomal recessive osteopetrosis. Nat. Genet. 25 (2000) 343-346
10. Nanda A., Brumell J.H., Nordstrom T., Kjeldsen L., Sengelov H., Borregaard N., Rotstein O.D., and Grinstein S. Activation of proton pumping in human neutrophils occurs by exocytosis of vesicles bearing vacuolar-type H+-ATPases. J. Biol. Chem. 271 (1996) 15963-15970
11. Pietrement C., Sun-Wada G.H., Silva N.D., McKee M., Marshansky V., Brown D., Futai M., and Breton S. Distinct expression patterns of different subunit isoforms of the V-ATPase in the rat epididymis. Biol. Reprod. 74 (2006) 185-194
12. Rojas J.D., Sennoune S.R., Martinez G.M., Bakunts K., Meininger C.J., Wu G., Wesson D.E., Seftor E.A., Hendrix M.J., and Martinez-Zaguilan R. Plasmalemmal vacuolar H+-ATPase is decreased in microvascular endothelial cells from a diabetic model. J. Cell. Physiol. 201 (2004) 190-200
13. Sennoune S.R., Bakunts K., Martinez G.M., Chua-Tuan J.L., Kebir Y., Attaya M.N., and Martinez-Zaguilan R. Vacuolar H+-ATPase in human breast cancer cells with distinct metastatic potential: distribution and functional activity. Am. J. Physiol. Cell. Physiol. 286 (2004) C1443-C1452
14. Arai H., Terres G., Pink S., and Forgac M. Topography and subunit stoichiometry of the coated vesicle proton pump. J. Biol. Chem. 263 (1988) 8796-8802
15. 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
16. Ohira M., Smardon A.M., Charsky C.M., Liu J., Tarsio M., and Kane P.M. The E and G subunits of the yeast V-ATPase interact tightly and are both present at more than one copy per V1 complex. J. Biol. Chem. 281 (2006) 22752-22760
17. Liu Q., Kane P.M., Newman P.R., and Forgac M. Site-directed mutagenesis of the yeast V-ATPase B subunit (Vma2p). J. Biol. Chem. 271 (1996) 2018-2022
18. Liu Q., Leng X.H., Newman P.R., Vasilyeva E., Kane P.M., and Forgac M. Site-directed mutagenesis of the yeast V-ATPase A subunit. J. Biol. Chem. 272 (1997) 11750-11756
19. MacLeod K.J., Vasilyeva E., Baleja J.D., and Forgac M. Mutational analysis of the nucleotide binding sites of the yeast vacuolar proton-translocating ATPase. J. Biol. Chem. 273 (1998) 150-156
20. MacLeod K.J., Vasilyeva E., Merdek K., Vogel P.D., and Forgac M. Photoaffinity labeling of wild-type and mutant forms of the yeast V-ATPase A subunit by 2-azido-[(32)P]ADP. J. Biol. Chem. 274 (1999) 32869-32874
21. Vasilyeva E., and Forgac M. 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 noncatalytic nucleotide binding site on the B subunit. J. Biol. Chem. 271 (1996) 12775-12782
22. Vasilyeva E., Liu Q., MacLeod K.J., Baleja J.D., and Forgac M. Cysteine scanning mutagenesis of the noncatalytic nucleotide binding site of the yeast V-ATPase. J. Biol. Chem. 275 (2000) 255-260
23. Arata Y., Baleja J.D., and Forgac M. Localization of subunits D, E, and G in the yeast V-ATPase complex using cysteine-mediated cross-linking to subunit B. Biochemistry 41 (2002) 11301-11307
24. Arata Y., Baleja J.D., and Forgac M. Cysteine-directed cross-linking to subunit B suggests that subunit E forms part of the peripheral stalk of the vacuolar H+-ATPase. J. Biol. Chem. 277 (2002) 3357-3363
25. Inoue T., and Forgac M. Cysteine-mediated cross-linking indicates that subunit C of the V-ATPase is in close proximity to subunits E and G of the V1 domain and subunit a of the V0 domain. J. Biol. Chem. 280 (2005) 27896-27903
26. 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
27. 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
28. Jefferies K.C., and Forgac M. Subunit H of the V-ATPase inhibits ATP hydrolysis by the free V1 domain by interaction with the rotary subunit F. J. Biol. Chem. 283 (2008) 4512-4519
29. 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. U. S. A. 98 (2001) 7134-7139
30. 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
31. Abrahams J.P., Leslie A.G., Lutter R., and Walker J.E. Structure at 2.8 A resolution of F1-ATPase from bovine heart mitochondria. Nature 370 (1994) 621-628
32. Tomashek J.J., Graham L.A., Hutchins M.U., Stevens T.H., and Klionsky D.J. V1-situated stalk subunits of the yeast vacuolar proton-translocating ATPase. J. Biol. Chem. 272 (1997) 26787-26793
33. Powell B., Graham L.A., and Stevens T.H. Molecular characterization of the yeast vacuolar H+-ATPase proton pore. J. Biol. Chem. 275 (2000) 23654-23660
34. Mandel M., Moriyama Y., Hulmes J.D., Pan Y.C., Nelson H., and Nelson N. cDNA sequence encoding the 16-kDa proteolipid of chromaffin granules implies gene duplication in the evolution of H+-ATPases. Proc. Natl. Acad. Sci. U.S.A. 85 (1988) 5521-5524
35. Hirata R., Graham L.A., Takatsuki A., Stevens T.H., and Anraku Y. VMA11 and VMA16 encode second and third proteolipid subunits of the Saccharomyces cerevisiae vacuolar membrane H+-ATPase. J. Biol. Chem. 272 (1997) 4795-4803
36. von Ballmoos C., and Dimroth P. Two distinct proton binding sites in the ATP synthase family. Biochemistry 46 (2007) 11800-11809
37. Iwata M., Imamura H., Stambouli E., Ikeda C., Tamakoshi M., Nagata K., Makyio H., Hankamer B., Barber J., Yoshida M., Yokoyama K., and Iwata S. Crystal structure of a central stalk subunit C and reversible association/dissociation of vacuole-type ATPase. Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 59-64
38. Leng X.H., Nishi T., and Forgac M. Transmembrane topography of the 100-kDa a subunit (Vph1p) of the yeast vacuolar proton-translocating ATPase. J. Biol. Chem. 274 (1999) 14655-14661
39. Kawasaki-Nishi S., Nishi T., and Forgac M. Arg-735 of the 100-kDa subunit a of the yeast V-ATPase is essential for proton translocation. Proc. Natl. Acad. Sci. U. S. A. 98 (2001) 12397-12402
40. Imamura H., Nakano M., Noji H., Muneyuki E., Ohkuma S., Yoshida M., and Yokoyama K. Evidence for rotation of V1-ATPase. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 2312-2315
41. 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
42. Vik S.B., Long J.C., Wada T., and Zhang D. A model for the structure of subunit a of the Escherichia coli ATP synthase and its role in proton translocation. Biochim. Biophys. Acta 1458 (2000) 457-466
43. 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
44. Wang Y., Inoue T., and Forgac M. TM2 but not TM4 of subunit c'' interacts with TM7 of subunit a of the yeast V-ATPase as defined by disulfide-mediated cross-linking. J. Biol. Chem. 279 (2004) 44628-44638
45. Bowman B.J., McCall M.E., Baertsch R., and Bowman E.J. A model for the proteolipid ring and bafilomycin/concanamycin-binding site in the vacuolar ATPase of Neurospora crassa. J. Biol. Chem. 281 (2006) 31885-31893
46. Wang Y., Inoue T., and Forgac M. Subunit a of the yeast V-ATPase participates in binding of bafilomycin. J. Biol. Chem. 280 (2005) 40481-40488
47. Wang Y., Cipriano D.J., and Forgac M. Arrangement of subunits in the proteolipid ring of the V-ATPase. J. Biol. Chem. 282 (2007) 34058-34065
48. Malkus P., Graham L.A., Stevens T.H., and Schekman R. Role of Vma21p in assembly and transport of the yeast vacuolar ATPase. Mol. Biol. Cell 15 (2004) 5075-5091
49. Tycko B., and Maxfield F.R. Rapid acidification of endocytic vesicles containing alpha 2-macroglobulin. Cell 28 (1982) 643-651
50. Kim J.H., Lingwood C.A., Williams D.B., Furuya W., Manolson M.F., and Grinstein S. Dynamic measurement of the pH of the Golgi complex in living cells using retrograde transport of the verotoxin receptor. J. Cell Biol. 134 (1996) 1387-1399
51. Feng Y., and Forgac M. A novel mechanism for regulation of vacuolar acidification. J. Biol. Chem. 267 (1992) 19769-19772
52. Feng Y., and Forgac M. Cysteine 254 of the 73-kDa A subunit is responsible for inhibition of the coated vesicle (H+)-ATPase upon modification by sulfhydryl reagents. J. Biol. Chem. 267 (1992) 5817-5822
53. Feng Y., and Forgac M. Inhibition of vacuolar H(+)-ATPase by disulfide bond formation between cysteine 254 and cysteine 532 in subunit A. J. Biol. Chem. 269 (1994) 13224-13230
54. Forgac M. The vacuolar H+-ATPase of clathrin-coated vesicles is reversibly inhibited by S-nitrosoglutathione. J. Biol. Chem. 274 (1999) 1301-1305
55. Kane P.M. The where, when, and how of organelle acidification by the yeast vacuolar H+-ATPase. Microbiol. Mol. Biol. Rev. 70 (2006) 177-191
56. Beyenbach K.W., and Wieczorek H. The V-type H+ ATPase: molecular structure and function, physiological roles and regulation,. J. Exp. Biol. 209 (2006) 577-589
57. Sautin Y.Y., Lu M., Gaugler A., Zhang L., and Gluck S.L. Phosphatidylinositol 3-kinase-mediated effects of glucose on vacuolar H+-ATPase assembly, translocation and acidification of intracellular compartments in renal epithelial cells. Mol. Cell Biol. 25 (2005) 575-589
58. Trombetta E.S., Ebersold M., Garrett W., Pypaert M., and Mellman I. Activation of lysosomal function during dendritic cell maturation. Science 299 (2003) 1400-1403
59. Kane P.M. Disassembly and reassembly of the yeast vacuolar H(+)-ATPase in vivo. J. Biol. Chem. 270 (1995) 17025-17032
60. Parra K.J., and Kane P.M. Reversible association between the V1 and V0 domains of yeast vacuolar H+-ATPase is an unconventional glucose-induced effect. Mol. Cell Biol. 18 (1998) 7064-7074
61. Qi J., and Forgac M. Cellular environment is important in controlling V-ATPase dissociation and its dependence on activity. J. Biol. Chem. 282 (2007) 24743-24751
62. Xu T., and Forgac M. Microtubules are involved in glucose-dependent dissociation of the yeast vacuolar [H+]-ATPase in vivo. J. Biol. Chem. 276 (2001) 24855-24861
63. Seol J.H., Shevchenko A., Shevchenko A., and Deshaies R.J. Skp1 forms multiple protein complexes, including RAVE, a regulator of V-ATPase assembly. Nat. Cell Biol. 3 (2001) 384-391
64. Smardon A.M., Tarsio M., and Kane P.M. The RAVE complex is essential for stable assembly of the yeast V-ATPase. J. Biol. Chem. 277 (2002) 13831-13839
65. Kawasaki-Nishi S., Nishi T., and Forgac M. Yeast V-ATPase complexes containing different isoforms of the 100-kDa a-subunit differ in coupling efficiency and in vivo dissociation. J. Biol. Chem. 276 (2001) 17941-17948
66. Manolson M.F., Wu B., Proteau D., Taillon B.E., Roberts B.T., Hoyt M.A., and Jones E.W. STV1 gene encodes functional homologue of 95-kDa yeast vacuolar H(+)-ATPase subunit Vph1p. J. Biol. Chem. 269 (1994) 14064-14074
67. Shao E., and Forgac M. Involvement of the nonhomologous region of subunit A of the yeast V-ATPase in coupling and in vivo dissociation. J. Biol. Chem. 279 (2004) 48663-48670
68. Shao E., Nishi T., Kawasaki-Nishi S., and Forgac M. Mutational analysis of the non-homologous region of subunit A of the yeast V-ATPase. J. Biol. Chem. 278 (2003) 12985-12991
69. Parra K.J., Keenan K.L., and Kane P.M. The H subunit (Vma13p) of the yeast V-ATPase inhibits the ATPase activity of cytosolic V1 complexes. J. Biol. Chem. 275 (2000) 21761-21767
70. Adachi I., Arai H., Pimental R., and Forgac M. Proteolysis and orientation on reconstitution of the coated vesicle proton pump. J. Biol. Chem. 265 (1990) 960-966
71. Arai H., Pink S., and Forgac M. Interaction of anions and ATP with the coated vesicle proton pump. Biochemistry 28 (1989) 3075-3082
72. Xu T., and Forgac M. Subunit D (Vma8p) of the yeast vacuolar H+-ATPase plays a role in coupling of proton transport and ATP hydrolysis. J. Biol. Chem. 275 (2000) 22075-22081
73. Kawasaki-Nishi S., Bowers K., Nishi T., Forgac M., and Stevens T.H., The amino-terminal domain of the vacuolar proton-translocating ATPase a subunit controls targeting and in vivo dissociation, and the carboxyl-terminal domain affects coupling of proton transport and ATP hydrolysis. J. Biol. Chem. 276 (2001) 47411-47420
74. Mulberg A.E., Tulk B.M., and Forgac M. Modulation of coated vesicle chloride channel activity and acidification by reversible protein kinase A-dependent phosphorylation. J. Biol. Chem. 266 (1991) 20590-20593
75. Brett C.L., Tukaye D.N., Mukherjee S., and Rao R. The yeast endosomal Na+K+/H+ exchanger Nhx1 regulates cellular pH to control vesicle trafficking. Mol. Biol. Cell 16 (2005) 1396-1405
76. Boyer P.D. The binding change mechanism for ATP synthase-some probabilities and possibilities. Biochim. Biophys. Acta 1140 (1993) 215-250