Characterization of vacuolar-ATPase and selective inhibition of vacuolar-H(+)-ATPase in osteoclasts

Biochemical and Biophysical Research Communications

Volumn 357, Issue 4, 2007, Pages 821-827

  Yao, GuanFeng ^a   Feng, HaoTian ^b   Cai, YanLing ^a   Qi, WeiLi ^a   Kong, KangMei ^a  

^a SHANTOU UNIVERSITY MEDICAL COLLEGE   (China)

^b UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

Bone resorption; Osteoclast; V ATPase; V ATPase inhibitors

Indexed keywords

5 (5,6 DICHLOROINDOLYL) 2 METHOXY N (1,2,2,6,6 PENTAMETHYLPIPERIDIN 4 YL) 2,4 PENTADIENAMIDE; AC45 PROTEIN; ADENOSINE TRIPHOSPHATASE; AMIDE; BAFILOMYCIN A1; COMPLEMENTARY DNA; CONCANAMYCIN A; FRUCTOSE BISPHOSPHATE ALDOLASE; M8 PROTEIN; M9 PROTEIN; MEMBRANE PROTEIN; OSTEOCLAST DIFFERENTIATION FACTOR; PROTEIN; SB 242784; UNCLASSIFIED DRUG; VACUOLAR ADENOSINE TRIPHOSPHATASE;

ALPHA CHAIN; BINDING SITE; BONE CANCER; CELL VACUOLE; GENE; GENE DELETION; GENETIC ANALYSIS; HUMAN; NONHUMAN; NUCLEOTIDE SEQUENCE; OSTEOCLAST; OSTEOLYSIS; OSTEOPOROSIS; PAGET BONE DISEASE; PRIORITY JOURNAL; PROTON TRANSPORT; SHORT SURVEY; SIGNAL TRANSDUCTION; UNSPECIFIED SIDE EFFECT; YEAST;

ADENOSINE TRIPHOSPHATASES; ADENOSINE TRIPHOSPHATE; ANIMALS; ENZYME ACTIVATION; HUMANS; OSTEOCLASTS; SIGNAL TRANSDUCTION; VACUOLES;

EUKARYOTA;

EID: 34247872795     PISSN: 0006291X     EISSN: 10902104     Source Type: Journal    
DOI: 10.1016/j.bbrc.2007.04.082     Document Type: Short Survey

References (73)

1. Grandin N., and Charbonneau M. The increase in intracellular pH associated with Xenopus egg activation is a Ca(2+)-dependent wave. J. Cell Sci. 101 Pt 1 (1992) 55-67
2. Morel N., Dunant Y., and Israel M. Neurotransmitter release through the V0 sector of V-ATPase. J. Neurochem. 79 3 (2001) 485-488
3. Nishi T., and Forgac M. The vacuolar (H+)-ATPases-nature's most versatile proton pumps. Nat. Rev. Mol. Cell Biol. 3 2 (2002) 94-103
4. Nelson N., and Harvey W.R. Vacuolar and plasma membrane proton-adenosinetriphosphatases. Physiol. Rev. 79 2 (1999) 361-385
5. Teitelbaum S.L. Bone resorption by osteoclasts. Science 289 5484 (2000) 1504-1508
6. Forgac M. Structure and properties of the vacuolar (H+)-ATPases. J. Biol. Chem. 274 19 (1999) 12951-12954
7. Nelson H., Mandiyan S., and Nelson N. A conserved gene encoding the 57 kDa subunit of the yeast vacuolar H+-ATPase. J. Biol. Chem. 264 3 (1989) 1775-1778
8. Hirata R., Ohsumk Y., Nakano A., Kawasaki H., Suzuki K., and Anraku Y. Molecular structure of a gene, VMA1, encoding the catalytic subunit of H(+)-translocating adenosine triphosphatase from vacuolar membranes of Saccharomyces cerevisiae. J. Biol. Chem. 265 12 (1990) 6726-6733
9. Kane P.M., Yamashiro C.T., Wolczyk D.F., Neff N., Goebl M., and Stevens T.H. Protein splicing converts the yeast TFP1 gene product to the 69-kD subunit of the vacuolar H(+)-adenosine triphosphatase. Science 250 4981 (1990) 651-657
10. 32P]ATP. J. Biol. Chem. 270 26 (1995) 15494-15500
11. Graham L.A., Powell B., and Stevens T.H. Composition and assembly of the yeast vacuolar H(+)-ATPase complex. J. Exp. Biol. 203 Pt 1 (2000) 61-70
12. 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 18 (1997) 11750-11756
13. 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 1 (1998) 150-156
14. Nelson H., Mandiyan S., Noumi T., Moriyama Y., Miedel M.C., and Nelson N. Molecular cloning of cDNA encoding the C subunit of H(+)-ATPase from bovine chromaffin granules. J. Biol. Chem. 265 33 (1990) 20390-20393
15. Beltran C., Kopecky J., Pan Y.C., Nelson H., and Nelson N. Cloning and mutational analysis of the gene encoding subunit C of yeast vacuolar H(+)-ATPase. J. Biol. Chem. 267 2 (1992) 774-779
16. Ho M.N., Hill K.J., Lindorfer M.A., and Stevens T.H. Isolation of vacuolar membrane H(+)-ATPase-deficient yeast mutants; the VMA5 and VMA4 genes are essential for assembly and activity of the vacuolar H(+)-ATPase. J. Biol. Chem. 268 1 (1993) 221-227
17. Graham L.A., Hill K.J., and Stevens T.H. VMA8 encodes a 32 kDa V1 subunit of the Saccharomyces cerevisiae vacuolar H(+)-ATPase required for function and assembly of the enzyme complex. J. Biol. Chem. 270 25 (1995) 15037-15044
18. Nelson H., Mandiyan S., and Nelson N. A bovine cDNA and a yeast gene (VMA8) encoding the subunit D of the vacuolar H(+)-ATPase. Proc. Natl. Acad. Sci. USA 92 2 (1995) 497-501
19. 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 29 (2000) 22075-22081
20. Hirsch S., Strauss A., Masood K., Lee S., Sukhatme V., and Gluck S. Isolation and sequence of a cDNA clone encoding the 31 kDa subunit of bovine kidney vacuolar H+-ATPase. Proc. Natl. Acad. Sci. USA 85 9 (1988) 3004-3008
21. Imai-Senga Y., Sun-Wada G.H., Wada Y., and Futai M. A human gene, ATP6E1, encoding a testis-specific isoform of H(+)-ATPase subunit E. Gene 289 1-2 (2002) 7-12
22. Lu M., Holliday L.S., Zhang L., Dunn Jr. W.A., and Gluck S.L. Interaction between aldolase and vacuolar H+-ATPase: evidence for direct coupling of glycolysis to the ATP-hydrolyzing proton pump. J. Biol. Chem. 276 32 (2001) 30407-30413
23. Miura K., Miyazawa S., Furuta S., Mitsushita J., Kamijo K., Ishida H., Miki T., Suzukawa K., Resau J., Copeland T.D., et al. The Sos1-Rac1 signaling. Possible involvement of a vacuolar H(+)-ATPase E subunit. J. Biol. Chem. 276 49 (2001) 46276-46283
24. Graf R., Lepier A., Harvey W.R., and Wieczorek H. A novel 14 kDa V-ATPase subunit in the tobacco hornworm midgut. J. Biol. Chem. 269 5 (1994) 3767-3774
25. Nelson H., Mandiyan S., and Nelson N. The Saccharomyces cerevisiae VMA7 gene encodes a 14 kDa subunit of the vacuolar H(+)-ATPase catalytic sector. J. Biol. Chem. 269 39 (1994) 24150-24155
26. Graham L.A., Hill K.J., and Stevens T.H. VMA7 encodes a novel 14 kDa subunit of the Saccharomyces cerevisiae vacuolar H(+)-ATPase complex. J. Biol. Chem. 269 42 (1994) 25974-25977
27. Supekova L., Supek F., and Nelson N. The Saccharomyces cerevisiae VMA10 is an intron-containing gene encoding a novel 13 kDa subunit of vacuolar H(+)-ATPase. J. Biol. Chem. 270 23 (1995) 13726-13732
28. Supekova L., Sbia M., Supek F., Ma Y., and Nelson N. A novel subunit of vacuolar H(+)-ATPase related to the b subunit of F-ATPases. J. Exp. Biol. 199 Pt 5 (1996) 1147-1156
29. Ohya Y., Umemoto N., Tanida I., Ohta A., Iida H., and Anraku Y. Calcium-sensitive cls mutants of Saccharomyces cerevisiae showing a Pet- phenotype are ascribable to defects of vacuolar membrane H(+)-ATPase activity. J. Biol. Chem. 266 21 (1991) 13971-13977
30. Anraku Y., Hirata R., Wada Y., and Ohya Y. Molecular genetics of the yeast vacuolar H(+)-ATPase. J. Exp. Biol. 172 (1992) 67-81
31. Geyer M., Fackler O.T., and Peterlin B.M. Subunit H of the V-ATPase involved in endocytosis shows homology to beta-adaptins. Mol. Biol. Cell 13 6 (2002) 2045-2056
32. Geyer M., Yu H., Mandic R., Linnemann T., Zheng Y.H., Fackler O.T., and Peterlin B.M. Subunit H of the V-ATPase binds to the medium chain of adaptor protein complex 2 and connects Nef to the endocytic machinery. J. Biol. Chem. 277 32 (2002) 28521-28529
33. Perin M.S., Fried V.A., Stone D.K., Xie X.S., and Sudhof T.C. Structure of the 116 kDa polypeptide of the clathrin-coated vesicle/synaptic vesicle proton pump. J. Biol. Chem. 266 6 (1991) 3877-3881
34. Li Y.P., Chen W., and Stashenko P. Molecular cloning and characterization of a putative novel human osteoclast-specific 116 kDa vacuolar proton pump subunit. Biochem. Biophys. Res. Commun. 218 3 (1996) 813-821
35. Manolson M.F., Rea P.A., and Poole R.J. Identification of 3-O-(4-benzoyl)benzoyladenosine 5′-triphosphate- and N,N′-dicyclohexylcarbodiimide-binding subunits of a higher plant H+-translocating tonoplast ATPase. J. Biol. Chem. 260 22 (1985) 12273-12279
36. Toyomura T., Murata Y., Yamamoto A., Oka T., Sun-Wada G.H., Wada Y., and Futai M. From lysosomes to the plasma membrane: localization of vacuolar-type H+ -ATPase with the a3 isoform during osteoclast differentiation. J. Biol. Chem. 278 24 (2003) 22023-22030
37. Li Y.P., Chen W., Liang Y., Li E., and Stashenko P. Atp6i-deficient mice exhibit severe osteopetrosis due to loss of osteoclast-mediated extracellular acidification. Nat. Genet. 23 4 (1999) 447-451
38. Anraku Y., Umemoto N., Hirata R., and Wada Y. Structure and function of the yeast vacuolar membrane proton ATPase. J. Bioenerg. Biomembr. 21 5 (1989) 589-603
39. 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 8 (1997) 4795-4803
40. Torigoe T., Izumi H., Ishiguchi H., Uramoto H., Murakami T., Ise T., Yoshida Y., Tanabe M., Nomoto M., Itoh H., et al. Enhanced expression of the human vacuolar H+-ATPase c subunit gene (ATP6L) in response to anticancer agents. J. Biol. Chem. 277 39 (2002) 36534-36543
41. Wang S.Y., Moriyama Y., Mandel M., Hulmes J.D., Pan Y.C., Danho W., Nelson H., and Nelson N. Cloning of cDNA encoding a 32 kDa protein. An accessory polypeptide of the H+-ATPase from chromaffin granules. J. Biol. Chem. 263 33 (1988) 17638-17642
42. 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 17 (1993) 12749-12757
43. Finbow M.E., and Harrison M.A. The vacuolar H+-ATPase: a universal proton pump of eukaryotes. Biochem. J. 324 Pt 3 (1997) 697-712
44. Ludwig J., Kerscher S., Brandt U., Pfeiffer K., Getlawi F., Apps D.K., and Schagger H. Identification and characterization of a novel 9.2 kDa membrane sector-associated protein of vacuolar proton-ATPase from chromaffin granules. J. Biol. Chem. 273 18 (1998) 10939-10947
45. Supek F., Supekova L., Mandiyan S., Pan Y.C., Nelson H., and Nelson N. A novel accessory subunit for vacuolar H(+)-ATPase from chromaffin granules. J. Biol. Chem. 269 39 (1994) 24102-24106
46. Jansen E.J., Holthuis J.C., McGrouther C., Burbach J.P., and Martens G.J. Intracellular trafficking of the vacuolar H+-ATPase accessory subunit Ac45. J. Cell Sci. 111 Pt 20 (1998) 2999-3006
47. Schoonderwoert V.T., and Martens G.J. Targeted disruption of the mouse gene encoding the V-ATPase accessory subunit Ac45. Mol. Membr. Biol. 19 1 (2002) 67-71
48. Demirci F.Y., White N.J., Rigatti B.W., Lewis K.F., and Gorin M.B. Identification, genomic structure, and screening of the vacuolar proton-ATPase membrane sector-associated protein M8-9 gene within the COD1 critical region (Xp11.4). Mol. Vis. 7 (2001) 234-239
49. Blair H.C., Teitelbaum S.L., Ghiselli R., and Gluck S. Osteoclastic bone resorption by a polarized vacuolar proton pump. Science 245 4920 (1989) 855-857
50. Baron R., Neff L., Louvard D., and Courtoy P.J. Cell-mediated extracellular acidification and bone resorption: evidence for a low pH in resorbing lacunae and localization of a 100-kD lysosomal membrane protein at the osteoclast ruffled border. J. Cell Biol. 101 6 (1985) 2210-2222
51. Baron R. Molecular mechanisms of bone resorption by the osteoclast. Anat. Rec. 224 2 (1989) 317-324
52. Vaananen H.K., Zhao H., Mulari M., and Halleen J.M. The cell biology of osteoclast function. J. Cell Sci. 113 Pt 3 (2000) 377-381
53. Laitala-Leinonen T., Lowik C., Papapoulos S., and Vaananen H.K. Inhibition of intravacuolar acidification by antisense RNA decreases osteoclast differentiation and bone resorption in vitro. J. Cell Sci. 112 Pt 21 (1999) 3657-3666
54. Lee B.S., Holliday L.S., Ojikutu B., Krits I., and Gluck S.L. Osteoclasts express the B2 isoform of vacuolar H(+)-ATPase intracellularly and on their plasma membranes. Am. J. Physiol. 270 1 Pt 1 (1996) C382-C388
55. Mattsson J.P., Skyman C., Palokangas H., Vaananen K.H., and Keeling D.J. Characterization and cellular distribution of the osteoclast ruffled membrane vacuolar H+-ATPase B-subunit using isoform-specific antibodies. J. Bone Miner. Res. 12 5 (1997) 753-760
56. Chen S.H., Bubb M.R., Yarmola E.G., Zuo J., Jiang J., Lee B.S., Lu M., Gluck S.L., Hurst I.R., and Holliday L.S. Vacuolar H+-ATPase binding to microfilaments: regulation in response to phosphatidylinositol 3-kinase activity and detailed characterization of the actin-binding site in subunit B. J. Biol. Chem. 279 9 (2004) 7988-7998
57. Holliday L.S., Lu M., Lee B.S., Nelson R.D., Solivan S., Zhang L., and Gluck S.L. The amino-terminal domain of the B subunit of vacuolar H+-ATPase contains a filamentous actin binding site. J. Biol. Chem. 275 41 (2000) 32331-32337
58. Manolson M.F., Yu H., Chen W., Yao Y., Li K., Lees R.L., and Heersche J.N. The a3 isoform of the 100 kDa V-ATPase subunit is highly but differentially expressed in large (>or = 10 nuclei) and small (
59. Sobacchi C., Frattini A., Orchard P., Porras O., Tezcan I., Andolina M., Babul-Hirji R., Baric I., Canham N., Chitayat D., et al. The mutational spectrum of human malignant autosomal recessive osteopetrosis. Hum. Mol. Genet. 10 17 (2001) 1767-1773
60. Farina C., and Gagliardi S. Selective inhibitors of the osteoclast vacuolar proton ATPase as novel bone antiresorptive agents. Drug. Discov. Today 4 4 (1999) 163-172
61. Sundquist K., Lakkakorpi P., Wallmark B., and Vaananen K. Inhibition of osteoclast proton transport by bafilomycin A1 abolishes bone resorption. Biochem. Biophys. Res. Commun. 168 1 (1990) 309-313
62. Chatterjee D., Chakraborty M., Leit M., Neff L., Jamsa-Kellokumpu S., Fuchs R., and Baron R. Sensitivity to vanadate and isoforms of subunits A and B distinguish the osteoclast proton pump from other vacuolar H+ ATPases. Proc. Natl. Acad. Sci. USA 89 14 (1992) 6257-6261
63. Sundquist K.T., and Marks Jr. S.C. Bafilomycin A1 inhibits bone resorption and tooth eruption in vivo. J. Bone Miner. Res. 9 10 (1994) 1575-1582
64. Xu J., Feng H.T., Wang C., Yip K.H., Pavlos N., Papadimitriou J.M., Wood D., and Zheng M.H. Effects of Bafilomycin A1: an inhibitor of vacuolar H (+)-ATPases on endocytosis and apoptosis in RAW cells and RAW cell-derived osteoclasts. J. Cell Biochem. 88 6 (2003) 1256-1264
65. Kinashi H., Someno K., and Sakaguchi K. Isolation and characterization of concanamycins A, B and C. J. Antibiot. (Tokyo) 37 11 (1984) 1333-1343
66. Kinashi H., Sakaguchi K., Higashijima T., and Miyazawa T. Structures of concanamycins B and C. J. Antibiot. (Tokyo) 35 11 (1982) 1618-1620
67. Huss M., Ingenhorst G., Konig S., Gassel M., Drose S., Zeeck A., Altendorf K., and Wieczorek H. Concanamycin A, the specific inhibitor of V-ATPases, binds to the V(o) subunit c. J. Biol. Chem. 277 43 (2002) 40544-40548
68. Bowman E.J., Graham L.A., Stevens T.H., and Bowman B.J. The bafilomycin/concanamycin binding site in subunit c of the V-ATPases from Neurospora crassa and Saccharomyces cerevisiae. J. Biol. Chem. 279 32 (2004) 33131-33138
69. Zhang J., Feng Y., and Forgac M. Proton conduction and bafilomycin binding by the V0 domain of the coated vesicle V-ATPase. J. Biol. Chem. 269 38 (1994) 23518-23523
70. Wang Y., Inoue T., and Forgac M. Subunit a of the yeast V-ATPase participates in binding of bafilomycin. J. Biol. Chem. 280 49 (2005) 40481-40488
71. Bowman B.J., and Bowman E.J. Mutations in subunit C of the vacuolar ATPase confer resistance to bafilomycin and identify a conserved antibiotic binding site. J. Biol. Chem. 277 6 (2002) 3965-3972
72. Visentin L., Dodds R.A., Valente M., Misiano P., Bradbeer J.N., Oneta S., Liang X., Gowen M., and Farina C. A selective inhibitor of the osteoclastic V-H(+)-ATPase prevents bone loss in both thyroparathyroidectomized and ovariectomized rats. J. Clin. Invest. 106 2 (2000) 309-318
73. Gagliardi S., Nadler G., Consolandi E., Parini C., Morvan M., Legave M.N., Belfiore P., Zocchetti A., Clarke G.D., James I., et al. 5-(5,6-Dichloro-2-indolyl)-2-methoxy-2,4-pentadienamides: novel and selective inhibitors of the vacuolar H+-ATPase of osteoclasts with bone antiresorptive activity. J. Med. Chem. 41 10 (1998) 1568-1573