Atp6v1c1 is an essential component of the osteoclast proton pump and in F-actin ring formation in osteoclasts

Biochemical Journal

Volumn 417, Issue 1, 2009, Pages 195-203

  Feng, Shengmei ^a,b   Deng, Lianfu ^c   Chen, Wei ^b,d   Shao, Jianzhong ^a   Xu, Guoliang ^e   Li, Yi Ping ^a,b,c,d,f  

^a ZHEJIANG UNIVERSITY   (China)

^b FORSYTH INSTITUTE   (United States)

^c Shanghai Institute of Traumatology and Orthopaedics   (China)

^d HARVARD SCHOOL OF DENTAL MEDICINE   (United States)

^e INSTITUTE OF BIOCHEMISTRY AND CELL BIOLOGY   (China)

^f Zhejiang Cell Biomedical Research College   (China)

Author keywords

Acidification; Atp6v1c1 (C1); Bone resorption; Filamentous actin (F actin) ring; Osteoclast; Vacuolar type proton translocating ATPase (V ATPase)

Indexed keywords

ACIDIFICATION; ATP6V1C1 (C1); BONE RESORPTION; FILAMENTOUS ACTIN (F-ACTIN) RING; OSTEOCLAST; VACUOLAR-TYPE PROTON-TRANSLOCATING ATPASE (V-ATPASE);

BONE; CHEMICAL ACTIVATION; CYTOLOGY; NUCLEIC ACIDS; PLASMAS; PROTONS; PUMPS; RNA;

CELL MEMBRANES;

ADENOSINE TRIPHOSPHATASE; F ACTIN; OSTEOCLAST DIFFERENTIATION FACTOR; PROTON PUMP; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE C1; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE C2A; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE C2B; UNCLASSIFIED DRUG; ACTIN; ATP6V1C1 PROTEIN, MOUSE; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; SMALL INTERFERING RNA;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL ACTIVATION; CELL DIFFERENTIATION; CELL MEMBRANE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; GENE SILENCING; HUMAN; HUMAN CELL; MICROTUBULE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OSTEOCLAST; OSTEOLYSIS; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RNA INTERFERENCE; ANIMAL; C57BL MOUSE; CELL CULTURE; CYTOLOGY; DNA MICROARRAY; FLUORESCENT ANTIBODY TECHNIQUE; GENETICS; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; LENTIVIRINAE; METABOLISM; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

LENTIVIRUS;

ACTINS; ANIMALS; BLOTTING, WESTERN; CELL DIFFERENTIATION; CELLS, CULTURED; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; LENTIVIRUS; MICE; MICE, INBRED C57BL; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; OSTEOCLASTS; PROTON PUMPS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, SMALL INTERFERING; VACUOLAR PROTON-TRANSLOCATING ATPASES;

EID: 58249089414     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20081073     Document Type: Article

References (42)

1. Xu, J., Cheng, T., Feng, H. T., Pavlos, N. J. and Zheng, M. H. (2007) Structure and function of V-ATPases in osteoclasts: potential therapeutic targets for the treatment of osteolysis. Histol. Histopathol. 22, 443-454
2. Forgac, M. (2007) Vacuolar ATPases: rotary proton pumps in physiology and pathophysiology. Nat. Rev. Mol. Cell Biol. 8, 917-929
3. +-ATPases. J. Biol. Chem. 274, 12951-12954
4. +-ATPase complex. J. Biol. Chem. 274, 28909-28915
5. +-ATPase. Annu. Rev. Cell Dev. Biol. 13, 779-808
6. Nishi, T., Kawasaki-Nishi, S. and Forgac, M. (2003) Expression and function of the mouse V-ATPase d subunit isoforms. J. Biol. Chem. 278, 46396-46402
7. +-ATPase in proton-secreting cells of the kidney and epididymis. Am. J. Physiol. Cell Physiol. 287, C149-C162
8. Pietrement, C., Sun-Wada, G. H., Silva, N. D., McKee, M., Marshansky, V., Brown, D., Futai, M. and Breton, S. (2006) Distinct expression patterns of different subunit isoforms of the V-ATPase in the rat epididymis. Biol. Reprod. 74, 185-194
9. +-ATPase C, G and d subunits, and their evaluation in autosomal recessive distal renal tubular acidosis. Gene 297, 169-177
10. Sun-Wada, G. H., Yoshimizu, T., Imai-Senga, Y., Wada, Y. and Futai, M. (2003) Diversity of mouse proton-translocating ATPase: presence of multiple isoforms of the C, d and G subunits. Gene 302, 147-153
11. + pump with G subunit isoforms (G1 and G2) in mouse neurons. J. Biol. Chem. 277, 36296-36303
12. Lee, B. S., Holliday, L. S., Ojikutu, B., Krits, I. and Gluck, S. L. (1996) Osteoclasts express the B2 isoform of vacuolar H+-ATPase intracellularly and on their plasma membranes. Am. J. Physiol. 270, C382-C388
13. Li, Y. P., Chen, W., Liang, Y., Li, E. and Stashenko, P. (1999) Atp6i-deficient mice exhibit severe osteopetrosis due to loss of osteoclast-mediated extracellular acidification. Nat. Genet. 23, 447-451
14. Kornak, U., Kasper, D., Bosl, M. R., Kaiser, E., Schweizer, M., Schulz, A., Friedrich, W., Delling, G. and Jentsch, T. J. (2001) Loss of the CLC-7 chloride channel leads to osteopetrosis in mice and man. Cell 104, 205-215
15. +-ATPase with the a3 isoform during osteoclast differentiation. J. Biol. Chem. 278, 22023-22030
16. Sun-Wada, G. H., Murata, Y., Namba, M., Yamamoto, A., Wada, Y. and Futai, M. (2003) Mouse proton pump ATPase C subunit isoforms (C2-a and C2-b) specifically expressed in kidney and lung. J. Biol. Chem. 278, 44843-44851
17. Faccio, R., Grano, M., Colucci, S., Villa, A., Giannelli, G., Quaranta, V. and Zallone, A. (2002) Localization and possible role of two different αVß3 integrin conformations in resting and resorbing osteoclasts. J. Cell Sci. 115, 2919-2929
18. Saltel, F., Destaing, O., Bard, F., Eichert, D. and Jurdic, P. (2004) Apatite-mediated actin dynamics in resorbing osteoclasts. Mol. Biol. Cell 15, 5231-5241
19. Pfaff, M. and Jurdic, P. (2001) Podosomes in osteoclast-like cells: structural analysis and cooperative roles of paxillin, proline-rich tyrosine kinase 2 (Pyk2) and integrin αVß3. J. Cell Sci. 114, 2775-2786
20. Lee, S. H., Rho, J., Jeong, D., Sul, J. Y., Kim, T., Kim, N., Kang, J. S., Miyamoto, T., Suda, T., Lee, S. K. et al. (2006) v-ATPase V0 subunit d2-deficient mice exhibit impaired osteoclast fusion and increased bone formation. Nat. Med. 12, 1403-1409
21. Hu, Y., Nyman, J., Muhonen, P., Vaananen, H. K. and Laitala-Leinonen, T. (2005) Inhibition of the osteoclast V-ATPase by small interfering RNAs. FEBS Lett. 579, 4937-4942
22. Taranta, A., Migliaccio, S., Recchia, I., Caniglia, M., Luciani, M., De Rossi, G., Dionisi-Vici, C., Pinto, R. M., Francalanci, P., Boldrini, R. et al. (2003) Genotype-phenotype relationship in human ATP6i-dependent autosomal recessive osteopetrosis. Am. J. Pathol. 162, 57-68
23. Vitavska, O., Merzendorfer, H. and Wieczorek, H. (2005) The V-ATPase subunit C binds to polymeric F-actin as well as to monomeric G-actin and induces cross-linking of actin filaments. J. Biol. Chem. 280, 1070-1076
24. +-V-ATPase to the actin cytoskeleton. J. Biol. Chem. 278, 18499-18505
25. Yang, S. and Li, Y. P. (2007) RGS12 is essential for RANKL-evoked signaling for terminal differentiation of osteoclasts in vitro. J. Bone Miner. Res. 22, 45-54
26. Chen, W. and Li, Y. P. (1998) Generation of mouse osteoclastogenic cell lines immortalized with SV40 large T antigen. J. Bone Miner. Res. 13, 1112-1123
27. Kissler, S., Stern, P., Takahashi, K., Hunter, K., Peterson, L. B. and Wicker, L. S. (2006) In vivo RNA interference demonstrates a role for Nramp1 in modifying susceptibility to type 1 diabetes. Nat. Genet. 38, 479-483
28. Stewart, S. A., Dykxhoorn, D. M., Palliser, D., Mizuno, H., Yu, E. Y., An, D. S., Sabatini, D. M., Chen, I. S., Hahn, W. C., Sharp, P. A. et al. (2003) Lentivirus-delivered stable gene silencing by RNAi in primary cells. RNA 9, 493-501
29. Murrills, R. J. and Dempster, D. W. (1990) The effects of stimulators of intracellular cyclic AMP on rat and chick osteoclasts in vitro: validation of a simplified light microscope assay of bone resorption. Bone 11, 333-344
30. Yang, S., Chen, W., Stashenko, P. and Li, Y. P. (2007) Specificity of RGS10A as a key component in the RANKL signaling mechanism for osteoclast differentiation. J. Cell Sci. 120, 3362-3371
31. 2+]i oscillation regulation. Genes Dev. 21, 1803-1816
32. Baron, R., Neff, L., Louvard, D. and Courtoy, P. J. (1985) 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, 2210-2222
33. +-ATPase. Preferential expression of the a3 isoform during osteoclast differentiation. J. Biol. Chem. 275, 8760-8765
34. Blair, H. C., Teitelbaum, S. L., Ghiselli, R. and Gluck, S. (1989) Osteoclastic bone resorption by a polarized vacuolar proton pump. Science 245, 855-857
35. Tehrani, S., Faccio, R., Chandrasekar, I., Ross, F. P. and Cooper, J. A. (2006) Cortactin has an essential and specific role in osteoclast actin assembly. Mol. Biol. Cell 17, 2882-2895
36. Parra, K. J., Keenan, K. L. and Kane, P. M. (2000) The H subunit (Vma13p) of the yeast V-ATPase inhibits the ATPase activity of cytosolic V1 complexes. J. Biol. Chem. 275, 21761-21767
37. +-ATPase in vivo. J. Biol. Chem. 270, 17025-17032
38. Sumner, J. P., Dow, J. A., Earley, F. G., Klein, U., Jager, D. and Wieczorek, H. (1995) Regulation of plasma membrane V-ATPase activity by dissociation of peripheral subunits. J. Biol. Chem. 270, 5649-5653
39. Inoue, T. and Forgac, M. (2005) 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, 27896-27903
40. Abu-Amer, Y., Ross, F. P., Schlesinger, P., Tondravi, M. M. and Teitelbaum, S. L. (1997) Substrate recognition by osteoclast precursors induces C-src/microtubule association. J. Cell Biol. 137, 247-258
41. Henriksen, K., Sorensen, M. G., Nielsen, R. H., Gram, J., Schaller, S., Dziegiel, M. H., Everts, V., Bollerslev, J. and Karsdal, M. A. (2006) Degradation of the organic phase of bone by osteoclasts: a secondary role for lysosomal acidification. J. Bone Miner. Res. 21, 58-66
42. Kanehisa, J., Yamanaka, T., Doi, S., Turksen, K., Heersche, J. N., Aubin, J. E. and Takeuchi, H. (1990) A band of F-actin containing podosomes is involved in bone resorption by osteoclasts. Bone 11, 287-293