Organelle-specific isoenzymes of plant V-ATPase as revealed by in vivo-FRET analysis

Seidel T, Schnitzer D, Golldack D, Sauer M, Dietz K-J (2008)
BMC Cell Biology 9(1): 28.

Zeitschriftenaufsatz | Veröffentlicht | Englisch
Abstract / Bemerkung
BACKGROUND: The V-ATPase (VHA) is a protein complex of 13 different VHA-subunits. It functions as an ATP driven rotary-motor that electrogenically translocates H+ into endomembrane compartments. In Arabidopsis thaliana V-ATPase is encoded by 23 genes posing the question of specific versus redundant function of multigene encoded isoforms. RESULTS: The transmembrane topology and stoichiometry of the proteolipid VHA-c" as well as the stoichiometry of the membrane integral subunit VHA-e within the V-ATPase complex were investigated by in vivo fluorescence resonance energy transfer (FRET). VHA-c", VHA-e1 and VHA-e2, VHA-a, VHA-c3, truncated variants of VHA-c3 and a chimeric VHA-c/VHA-c" hybrid were fused to cyan (CFP) and yellow fluorescent protein (YFP), respectively. The constructs were employed for transfection experiments with Arabidopsis thaliana mesophyll protoplasts. Subcellular localization and FRET analysis by confocal laser scanning microscopy (CLSM) demonstrated that (i.) the N- and C-termini of VHA-c" are localised in the vacuolar lumen, (ii.) one copy of VHA-c" is present within the VHA-complex, and (iii.) VHA-c" is localised at the ER and associated Golgi bodies. (iv.) A similar localisation was observed for VHA-e2, whereas (v.) the subcellular localisation of VHA-e1 indicated the trans Golgi network (TGN)-specifity of this subunit. CONCLUSION: The plant proteolipid ring is a highly flexible protein subcomplex, tolerating the incorporation of truncated and hybrid proteolipid subunits, respectively. Whereas the membrane integral subunit VHA-e is present in two copies within the complex, the proteolipid subunit VHA-c" takes part in complex formation with only one copy. However, neither VHA-c" isoform 1 nor any of the two VHA-e isoforms were identified at the tonoplast. This suggest a function in endomembrane specific VHA-assembly or targeting rather than proton transport.
BMC Cell Biology
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Seidel T, Schnitzer D, Golldack D, Sauer M, Dietz K-J. Organelle-specific isoenzymes of plant V-ATPase as revealed by in vivo-FRET analysis. BMC Cell Biology. 2008;9(1): 28.
Seidel, T., Schnitzer, D., Golldack, D., Sauer, M., & Dietz, K. - J. (2008). Organelle-specific isoenzymes of plant V-ATPase as revealed by in vivo-FRET analysis. BMC Cell Biology, 9(1), 28.
Seidel, T., Schnitzer, D., Golldack, D., Sauer, M., and Dietz, K. - J. (2008). Organelle-specific isoenzymes of plant V-ATPase as revealed by in vivo-FRET analysis. BMC Cell Biology 9:28.
Seidel, T., et al., 2008. Organelle-specific isoenzymes of plant V-ATPase as revealed by in vivo-FRET analysis. BMC Cell Biology, 9(1): 28.
T. Seidel, et al., “Organelle-specific isoenzymes of plant V-ATPase as revealed by in vivo-FRET analysis”, BMC Cell Biology, vol. 9, 2008, : 28.
Seidel, T., Schnitzer, D., Golldack, D., Sauer, M., Dietz, K.-J.: Organelle-specific isoenzymes of plant V-ATPase as revealed by in vivo-FRET analysis. BMC Cell Biology. 9, : 28 (2008).
Seidel, Thorsten, Schnitzer, Daniel, Golldack, Dortje, Sauer, Markus, and Dietz, Karl-Josef. “Organelle-specific isoenzymes of plant V-ATPase as revealed by in vivo-FRET analysis”. BMC Cell Biology 9.1 (2008): 28.
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PMID: 27717369
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PMID: 23718549
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PMID: 24014545
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PMID: 22212511
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PMID: 21278126
Multiple redox and non-redox interactions define 2-Cys peroxiredoxin as a regulatory hub in the chloroplast.
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PMID: 19995730
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50 References

Daten bereitgestellt von Europe PubMed Central.

Proton translocation driven by ATP hydrolysis in V-ATPases.
Kawasaki-Nishi S, Nishi T, Forgac M., FEBS Lett. 545(1), 2003
PMID: 12788495
Structure, function and regulation of the plant vacuolar H(+)-translocating ATPase.
Ratajczak R., Biochim. Biophys. Acta 1465(1-2), 2000
PMID: 10748245
The Arabidopsis det3 mutant reveals a central role for the vacuolar H(+)-ATPase in plant growth and development.
Schumacher K, Vafeados D, McCarthy M, Sze H, Wilkins T, Chory J., Genes Dev. 13(24), 1999
PMID: 10617574
Essential role of the V-ATPase in male gametophyte development.
Dettmer J, Schubert D, Calvo-Weimar O, Stierhof YD, Schmidt R, Schumacher K., Plant J. 41(1), 2005
PMID: 15610354
Arabidopsis vacuolar H-ATPase subunit E isoform 1 is required for Golgi organization and vacuole function in embryogenesis.
Strompen G, Dettmer J, Stierhof YD, Schumacher K, Jurgens G, Mayer U., Plant J. 41(1), 2005
PMID: 15610355
Trans-complex formation by proteolipid channels in the terminal phase of membrane fusion.
Peters C, Bayer MJ, Buhler S, Andersen JS, Mann M, Mayer A., Nature 409(6820), 2001
PMID: 11214310
Structure and function of the vacuolar H+-ATPase: moving from low-resolution models to high-resolution structures.
Harrison M, Durose L, Song CF, Barratt E, Trinick J, Jones R, Findlay JB., J. Bioenerg. Biomembr. 35(4), 2003
PMID: 14635779
The mechanochemistry of V-ATPase proton pumps.
Grabe M, Wang H, Oster G., Biophys. J. 78(6), 2000
PMID: 10827963
Subunit rotation of vacuolar-type proton pumping ATPase: relative rotation of the G and C subunits.
Hirata T, Iwamoto-Kihara A, Sun-Wada GH, Okajima T, Wada Y, Futai M., J. Biol. Chem. 278(26), 2003
PMID: 12670943
A simple nomenclature for a complex proton pump: VHA genes encode the vacuolar H(+)-ATPase.
Sze H, Schumacher K, Muller ML, Padmanaban S, Taiz L., Trends Plant Sci. 7(4), 2002
PMID: 11950611
Subcellular distribution of the V-ATPase complex in plant cells, and in vivo localisation of the 100 kDa subunit VHA-a within the complex.
Kluge C, Seidel T, Bolte S, Sharma SS, Hanitzsch M, Satiat-Jeunemaitre B, Ross J, Sauer M, Golldack D, Dietz KJ., BMC Cell Biol. 5(), 2004
PMID: 15310389
Structure-function relationships of A-, F- and V-ATPases.
Gruber G, Wieczorek H, Harvey WR, Muller V., J. Exp. Biol. 204(Pt 15), 2001
PMID: 11533110
The rotor in the membrane of the ATP synthase and relatives.
Arechaga I, Jones PC., FEBS Lett. 494(1-2), 2001
PMID: 11297723
VMA11 and VMA16 encode second and third proteolipid subunits of the Saccharomyces cerevisiae vacuolar membrane H+-ATPase.
Hirata R, Graham LA, Takatsuki A, Stevens TH, Anraku Y., J. Biol. Chem. 272(8), 1997
PMID: 9030535
Evidence that there are two copies of subunit c" in V0 complexes in the vacuolar H+-ATPase.
Gibson LC, Cadwallader G, Finbow ME., Biochem. J. 366(Pt 3), 2002
PMID: 12038966
Expression and localization of the mouse homologue of the yeast V-ATPase 21-kDa Subunit c" (Vma16p).
Nishi T, Kawasaki-Nishi S, Forgac M., J. Biol. Chem. 276(36), 2001
PMID: 11441017
Structure and assembly of the yeast V-ATPase.
Graham LA, Flannery AR, Stevens TH., J. Bioenerg. Biomembr. 35(4), 2003
PMID: 14635776
Identification and characterization of a novel 9.2-kDa membrane sector-associated protein of vacuolar proton-ATPase from chromaffin granules.
Ludwig J, Kerscher S, Brandt U, Pfeiffer K, Getlawi F, Apps DK, Schagger H., J. Biol. Chem. 273(18), 1998
PMID: 9556572
Vma9p (subunit e) is an integral membrane V0 subunit of the yeast V-ATPase.
Compton MA, Graham LA, Stevens TH., J. Biol. Chem. 281(22), 2006
PMID: 16569636
The vegetative vacuole proteome of Arabidopsis thaliana reveals predicted and unexpected proteins.
Carter C, Pan S, Zouhar J, Avila EL, Girke T, Raikhel NV., Plant Cell 16(12), 2004
PMID: 15539469
Colocalization and FRET-analysis of subunits c and a of the vacuolar H+-ATPase in living plant cells.
Seidel T, Kluge C, Hanitzsch M, Ross J, Sauer M, Dietz KJ, Golldack D., J. Biotechnol. 112(1-2), 2004
PMID: 15288951
Vacuolar H+-ATPase activity is required for endocytic and secretory trafficking in Arabidopsis.
Dettmer J, Hong-Hermesdorf A, Stierhof YD, Schumacher K., Plant Cell 18(3), 2006
PMID: 16461582
Mapping of C-termini of V-ATPase subunits by in vivo-FRET measurements.
Seidel T, Golldack D, Dietz KJ., FEBS Lett. 579(20), 2005
PMID: 16061227
Three-dimensional map of a plant V-ATPase based on electron microscopy.
Domgall I, Venzke D, Luttge U, Ratajczak R, Bottcher B., J. Biol. Chem. 277(15), 2002
PMID: 11815621
Early steps in assembly of the yeast vacuolar H+-ATPase.
Kane PM, Tarsio M, Liu J., J. Biol. Chem. 274(24), 1999
PMID: 10358087
Role of Vma21p in assembly and transport of the yeast vacuolar ATPase.
Malkus P, Graham LA, Stevens TH, Schekman R., Mol. Biol. Cell 15(11), 2004
PMID: 15356264
Novel vacuolar H+-ATPase complexes resulting from overproduction of Vma5p and Vma13p.
Keenan Curtis K, Kane PM., J. Biol. Chem. 277(4), 2001
PMID: 11717306
Mutational analysis of subunit G (Vma10p) of the yeast vacuolar H+-ATPase.
Charsky CM, Schumann NJ, Kane PM., J. Biol. Chem. 275(47), 2000
PMID: 10969085
The SzA mutations of the B subunit of the Drosophila vacuolar H+ ATPase identify conserved residues essential for function in fly and yeast.
Du J, Kean L, Allan AK, Southall TD, Davies SA, McInerny CJ, Dow JA., J. Cell. Sci. 119(Pt 12), 2006
PMID: 16735441
Phenotypic subunit composition of the tobacco (Nicotiana tabacum L.) vacuolar-type H(+)-translocating ATPase.
Drobny M, Schnolzer M, Fiedler S, Luttge U, Fischer-Schliebs E, Christian AL, Ratajczak R., Biochim. Biophys. Acta 1564(1), 2002
PMID: 12101019
Isolation of intact vacuoles and proteomic analysis of tonoplast from suspension-cultured cells of Arabidopsis thaliana.
Shimaoka T, Ohnishi M, Sazuka T, Mitsuhashi N, Hara-Nishimura I, Shimazaki K, Maeshima M, Yokota A, Tomizawa K, Mimura T., Plant Cell Physiol. 45(6), 2004
PMID: 15215502
Stacks on tracks: the plant Golgi apparatus traffics on an actin/ER network.
Boevink P, Oparka K, Santa Cruz S, Martin B, Betteridge A, Hawes C., Plant J. 15(3), 1998
PMID: 9750355
Arrangement of subunits in the proteolipid ring of the V-ATPase.
Wang Y, Cipriano DJ, Forgac M., J. Biol. Chem. 282(47), 2007
PMID: 17897940
The H-pumping V-ATPase of higher plants: A versatile „eco-enzyme“ in response to environmental stress
Lüttge U, Fischer-Schliebs E, Ratajczak R., 2001
Molecular characterization of the yeast vacuolar H+-ATPase proton pore.
Powell B, Graham LA, Stevens TH., J. Biol. Chem. 275(31), 2000
PMID: 10825180
Dynamics of activity and structure of the tonoplast vacuolar-type H-ATPase in plants with differing CAM expression and in a C-3 plant under salt stress
Mariaux JB, Fischer-Schliebs E, Luttge U, Ratajczak R., 1997


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