Reversible disassembly of the yeast V-ATPase revisited under in vivo conditions

Biochemical Journal

Volumn 462, Issue 1, 2014, Pages 185-197

  Tabke, Katharina ^a   Albertmelcher, Andrea ^a   Vitavska, Olga ^a   Huss, Markus ^a   Schmitz, Hans Peter ^a   Wieczorek, Helmut ^a  

^a UNIVERSITY OF OSNABRÜCK   (Germany)

Author keywords

Microtubule; Reversible disassembly; Saccharomyces cerevisiae; Vacuolar ATPase (V ATPase)

Indexed keywords

CYAN FLUORESCENT PROTEIN; GALACTOSE; GLUCOSE; GREEN FLUORESCENT PROTEIN; PROTON PUMP; UNCLASSIFIED DRUG; VACUOLAR ADENOSINE TRIPHOSPHATASE; VACUOLAR ADENOSINE TRIPHOSPHATASE A; VMA1 PROTEIN; VMA10 PROTEIN; VMA13 PROTEIN; VMA4 PROTEIN; VMA5 PROTEIN; VMA7 PROTEIN; VMA8 PROTEIN; VPH1 PROTEIN; YELLOW FLUORESCENT PROTEIN;

ARTICLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOSKELETON; CYTOSOL; ENZYME ACTIVITY; FLUORESCENCE MICROSCOPY; FLUORESCENCE RESONANCE ENERGY TRANSFER; MANDUCA SEXTA; MICROTUBULE; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; SACCHAROMYCES CEREVISIAE; WESTERN BLOTTING;

CYTOSOL; PROTEIN SUBUNITS; PROTON-TRANSLOCATING ATPASES; SACCHAROMYCES CEREVISIAE; VACUOLAR PROTON-TRANSLOCATING ATPASES;

EID: 84904622964     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20131293     Document Type: Article

References (49)

1. +)-ATPases: nature's most versatile proton pumps. Nat. Rev. Mol. Cell Biol. 3, 94-103 CrossRef PubMed
2. Wieczorek, H., Brown, D., Grinstein, S., Ehrenfeld, J. and Harvey, W. R. (1999) Animal plasma membrane energization by proton-motive V-ATPases. BioEssays 21, 637-648 CrossRef PubMed (Pubitemid 29384445)
3. 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 CrossRef PubMed
4. +-ATPase in vivo. J. Biol. Chem. 270, 17025-17032 PubMed
5. Kane, P. M. (2012) Targeting reversible disassembly as a mechanism of controlling V-ATPase activity. Curr. Protein Pept. Sci. 13, 117-123 CrossRef PubMed
6. Reineke, S., Wieczorek, H. and Merzendorfer, H. (2002) Expression of Manduca sexta V-ATPase genes mvB, mvG and mvd is regulated by ecdysteroids. J. Exp. Biol. 205, 1059-1067 PubMed (Pubitemid 34853770)
7. +-V-ATPase to the actin cytoskeleton. J. Biol. Chem. 278, 18499-18505 CrossRef PubMed
8. Huh, W. K., Falvo, J. V., Gerke, L. C., Carroll, A. S., Howson, R. W., Weissman, J. S. and O'Shea, E. K. (2003) Global analysis of protein localization in budding yeast. Nature 425, 686-691 CrossRef PubMed (Pubitemid 37314307)
9. Kirchrath, L., Lorberg, A., Schmitz, H. P., Gengenbacher, U. and Heinisch, J. J. (2000) Comparative genetic and physiological studies of the MAP kinase Mpk1p from Kluyveromyces lactis and Saccharomyces cerevisiae. J. Mol. Biol. 300, 743-758 CrossRef PubMed
10. Ito, H., Fukuda, Y., Murata, K. and Kimura, A. (1983) Transformation of intact yeast cells treated with alkali cations. J. Bacteriol. 153, 163-168 PubMed (Pubitemid 13119852)
11. Schiestl, R. H. and Gietz, R. D. (1989) High efficiency transformation of intact yeast cells using single stranded nucleic acids as a carrier. Curr. Genet. 16, 339-346 CrossRef PubMed (Pubitemid 20034019)
12. Gietz, D., St Jean, A., Woods, R. A. and Schiestl, R. H. (1992) Improved method for high efficiency transformation of intact yeast cells. Nucleic Acids Res. 20, 1425 CrossRef PubMed
13. Kanemaki, M., Sanchez-Diaz, A., Gambus, A. and Labib, K. (2003) Functional proteomic identification of DNA replication proteins by induced proteolysis in vivo. Nature 423, 720-724 CrossRef PubMed (Pubitemid 36735689)
14. Wach, A., Brachat, A., Pohlmann, R. and Philippsen, P. (1994) New heterologous modules for classical or PCR-based gene disruptions in Saccharomyces cerevisiae. Yeast 10, 1793-1808 CrossRef PubMed
15. Wach, A., Brachat, A., Alberti-Segui, C., Rebischung, C. and Philippsen, P. (1997) Heterologous HIS3 marker and GFP reporter modules for PCR-targeting in Saccharomyces cerevisiae. Yeast 13, 1065-1075 CrossRef PubMed (Pubitemid 27368517)
16. Sheff, M. A. and Thorn, K. S. (2004) Optimized cassettes for fluorescent protein tagging in Saccharomyces cerevisiae. Yeast 21, 661-670 CrossRef PubMed (Pubitemid 38868184)
17. Mumberg, D., Muller, R. and Funk, M. (1994) Regulatable promoters of Saccharomyces cerevisiae: comparison of transcriptional activity and their use for heterologous expression. Nucleic Acids Res. 22, 5767-5768 CrossRef PubMed
18. Van Haecht, J. L., Bolipombo, M. and Rouxhet, P. G. (1985) Immobilization of Saccharomyces cerevisiae by adhesion: treatment of the cells by Al ions. Biotechnol. Bioeng. 27, 217-224 CrossRef PubMed (Pubitemid 15143327)
19. Muller, E. G., Snydsman, B. E., Novik, I., Hailey, D. W., Gestaut, D. R., Niemann, C. A., O'Toole, E. T., Giddings, Jr, T. H., Sundin, B. A. and Davis, T. N. (2005) The organization of the core proteins of the yeast spindle pole body. Mol. Biol. Cell 16, 3341-3352 CrossRef PubMed (Pubitemid 40962603)
20. Seidel, T., Golldack, D. and Dietz, K. J. (2005) Mapping of C-termini of V-ATPase subunits by in vivo-FRET measurements. FEBS Lett. 579, 4374-4382 CrossRef PubMed (Pubitemid 41116368)
21. Hu, C. D., Chinenov, Y. and Kerppola, T. K. (2002) Visualization of interactions among bZIP and Rel family proteins in living cells using bimolecular fluorescence complementation. Mol. Cell 9, 789-798 CrossRef PubMed (Pubitemid 34454889)
22. Hu, C. D. and Kerppola, T. K. (2003) Simultaneous visualization of multiple protein interactions in living cells using multicolor fluorescence complementation analysis. Nat. Biotechnol. 21, 539-545 CrossRef PubMed
23. Wieczorek, H., Cioffi, M., Klein, U., Harvey, W. R., Schweikl, H. and Wolfersberger, M. G. (1990) Isolation of goblet cell apical membrane from tobacco hornworm midgut and purification of its vacuolar-type ATPase. Methods Enzymol. 192, 608-616 CrossRef PubMed
24. Brandt, R. and Lee, G. (1993) Functional organization of microtubule-associated protein tau: identification of regions which affect microtubule growth, nucleation, and bundle formation in vitro. J. Biol. Chem. 268, 3414-3419 PubMed (Pubitemid 23070977)
25. Merzendorfer, H., Reineke, S., Zhao, X. F., Jacobmeier, B., Harvey, W. R. and Wieczorek, H. (2000) The multigene family of the tobacco hornworm V-ATPase: novel subunits a, C, D, H, and putative isoforms. Biochim. Biophys. Acta 1467, 369-379 CrossRef PubMed (Pubitemid 30665590)
26. Huss, M., Ingenhorst, G., Konig, S., Gassel, M., Drose, S., Zeeck, A., Altendorf, K. and Wieczorek, H. (2002) Concanamycin A, the specific inhibitor of V-ATPases, binds to the Vo subunit c. J. Biol. Chem. 277, 40544-40548 CrossRef PubMed (Pubitemid 35215633)
27. + antiport in an animal plasma membrane. J. Biol. Chem. 266, 15340-15347 PubMed
28. +-ATPase. J. Biol. Chem. 285, 38304-38314 CrossRef PubMed
29. Pardee, J. D. and Spudich, J. A. (1982) Purification of muscle actin. Methods Enzymol. 85, 164-181 CrossRef PubMed
30. +-ATPase causes conditional lethality. Proc. Natl. Acad. Sci. U.S.A. 87, 3503-3507 CrossRef PubMed
31. Brachmann, C. B., Davies, A., Cost, G. J., Caputo, E., Li, J., Hieter, P. and Boeke, J. D. (1998) Designer deletion strains derived from Saccharomyces cerevisiae S288C: a useful set of strains and plasmids for PCR-mediated gene disruption and other applications. Yeast 14, 115-132 CrossRef PubMed (Pubitemid 28062863)
32. Seol, J. H., Shevchenko, A., Shevchenko, A. and Deshaies, R. J. (2001) Skp1 forms multiple protein complexes, including RAVE, a regulator of V-ATPase assembly. Nat. Cell Biol. 3, 384-391 CrossRef PubMed (Pubitemid 32288446)
33. Dechant, R., Binda, M., Lee, S. S., Pelet, S., Winderickx, J. and Peter, M. (2010) Cytosolic pH is a second messenger for glucose and regulates the PKA pathway through V-ATPase. EMBO J. 29, 2515-2526 CrossRef PubMed
34. Berchtold, D., Piccolis, M., Chiaruttini, N., Riezman, I., Riezman, H., Roux, A., Walther, T. C. and Loewith, R. (2012) Plasma membrane stress induces relocalization of Slm proteins and activation of TORC2 to promote sphingolipid synthesis. Nat. Cell Biol. 14, 542-547 CrossRef PubMed
35. Loewith, R. and Hall, M. N. (2011) Target of rapamycin (TOR) in nutrient signaling and growth control. Genetics 189, 1177-1201 CrossRef PubMed
36. +-ATPase. J. Biol. Chem. 268, 221-227 PubMed
37. Smardon, A. M. and Kane, P. M. (2007) RAVE is essential for the efficient assembly of the C subunit with the vacuolar H+-ATPase. J. Biol. Chem. 282, 26185-26194 CrossRef PubMed (Pubitemid 47443786)
38. +-ATPase is an unconventional glucose-induced effect. Mol. Cell. Biol. 18, 7064-7074 PubMed
39. 0 complexes. FEBS Lett. 581, 5566-5572 CrossRef PubMed
40. Osteresch, C., Bender, T., Grond, S., von Zezschwitz, P., Kunze, B., Jansen, R., Huss, M. and Wieczorek, H. (2012) The binding site of the V-ATPase inhibitor apicularen is in the vicinity of those for bafilomycin and archazolid. J. Biol. Chem. 287, 31866-31876 CrossRef PubMed
41. Muench, S. P., Huss, M., Song, C. F., Phillips, C., Wieczorek, H., Trinick, J. and Harrison, M. A. (2009) Cryo-electron microscopy of the vacuolar ATPase motor reveals its mechanical and regulatory complexity. J. Mol. Biol. 386, 989-999 CrossRef PubMed
42. 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 crosslinking of actin filaments. J. Biol. Chem. 280, 1070-1076 CrossRef PubMed
43. Boldogh, I., Vojtov, N., Karmon, S. and Pon, L. A. (1998) Interaction between mitochondria and the actin cytoskeleton in budding yeast requires two integral mitochondrial outer membrane proteins, Mmm1p and Mdm10p. J. Cell Biol. 141, 1371-1381 CrossRef PubMed (Pubitemid 28289912)
44. +]-ATPase in vivo. J. Biol. Chem. 276, 24855-24861 CrossRef PubMed
45. Davidse, L. C. and Flach, W. (1977) Differential binding of methyl benzimidazol-2-yl carbamate to fungal tubulin as a mechanism of resistance to this antimitotic agent in mutant strains of Aspergillus nidulans. J. Cell Biol. 72, 174-193 CrossRef PubMed (Pubitemid 8007657)
46. Thomas, J. H., Neff, N. F. and Botstein, D. (1985) Isolation and characterization of mutations in the β-tubulin gene of Saccharomyces cerevisiae. Genetics 111, 715-734 PubMed (Pubitemid 16192861)
47. Sweet, T. J., Boyer, B., Hu, W., Baker, K. E. and Coller, J. (2007) Microtubule disruption stimulates P-body formation. RNA 13, 493-502 CrossRef PubMed (Pubitemid 46506932)
48. +-ATPase and impairs vacuolar acidification. Plant Cell Physiol. 52, 946-956 CrossRef PubMed
49. Drory, O. and Nelson, N. (2006) The emerging structure of vacuolar ATPases. Physiology 21, 317-325 CrossRef PubMed (Pubitemid 44511759)