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Activation of the plant plasma membrane H+-ATPase by phosphorylation and binding of 14-3-3 proteins converts a dimer into a hexamer.

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Kanczewska, Justyna Marco, Sergio Vandermeeren, Caroline [UCL] Maudoux, Olivier Rigaud, Jean-Louis Boutry, Marc [UCL]

Plant plasma membrane H+-ATPases (PMAs) can be activated by phosphorylation of their penultimate residue (a Thr) and the subsequent binding of regulatory 14-3-3 proteins. Although 14-3-3 proteins usually exist as dimers and can bind two targets, the in vivo effects of their binding on the quaternary structure of H+-ATPases have never been examined. To address this question, we used a Nicotiana tabacum cell line expressing the Nicotiana plumbaginifolia PMA2 isoform with a 6-His tag. The purified PMA2 was mainly nonphosphorylated and 14-3-3-free, and it was shown by blue native gel electrophoresis and chemical cross-linking to exist as a dimer. Fusicoccin treatment of the cells resulted in a dramatic increase in Thr phosphorylation, 14-3-3 binding, and in vivo and in vitro ATPase activity, as well as in the conversion of the dimer into a larger, possibly hexameric, complex. PMA2 phosphorylation and 14-3-3 binding were observed also when cells in stationary growth phase were metabolically activated by transfer to fresh medium. When expressed in yeast, PMA2 was also phosphorylated and formed a complex with 14-3-3 proteins without requiring fusicoccin; no complex was observed when phosphorylation was prevented by mutagenesis. Single-particle analysis by cryoelectron microscopy showed that the PMA2-14-3-3 complex is a wheel-like structure with a 6-fold symmetry, suggesting that the activated complex consists of six H+-ATPase molecules and six 14-3-3 molecules.

Document type Article de périodique (Journal article) – Article de recherche – Journal Article, Research Support, Non-U.S. Gov't
Access type Accès libre
Publication date 2005
Language Anglais
Journal information "Proceedings of the National Academy of Sciences of the United States of America" - Vol. 102, no. 33, p. 11675-80 (2005)
Peer reviewed yes
issn 0027-8424
Publication status Publié
Affiliation UCL - AGRO/CABI - Département de chimie appliquée et des bio-industries
MESH Subject 14-3-3 Proteins - chemistry - metabolism - ultrastructure ; Cell Line ; Cell Membrane - metabolism ; Culture Media - chemistry - pharmacology ; Dimerization ; Enzyme Activation - drug effects ; Glycosides - pharmacology ; Hydrogen-Ion Concentration ; Microscopy, Electron ; Phosphorylation - drug effects ; Phosphothreonine - metabolism ; Protein Binding - drug effects ; Protein Structure, Quaternary ; Proton-Translocating ATPases - chemistry - genetics - metabolism - ultrastructure ; Saccharomyces cerevisiae - genetics ; Tobacco - enzymology - genetics
Links
  1. Morsomme, Biochimica et Biophysica Acta. Protein Structure and Molecular Enzymology, 1465, 1 (2000)
  2. Palmgren Michael G, PLANTPLASMAMEMBRANEH+-ATPases: Powerhouses for Nutrient Uptake, 10.1146/annurev.arplant.52.1.817
  3. Briskin D. P., Basu S., Assmann S. M., Characterization of the Red Beet Plasma Membrane H+-ATPase Reconstituted in a Planar Bilayer System, 10.1104/pp.108.1.393
  4. Jahn Thomas, Dietrich Jens, Andersen Birgitte, Leidvik Brith, Otter Charlotta, Briving Carin, Kühlbrandt Werner, Palmgren Michael Gjedde, Large scale expression, purification and 2D crystallization of recombinant plant plasma membrane H+-ATPase, 10.1006/jmbi.2001.4688
  5. Morsomme Pierre, Chami Mohamed, Marco Sergio, Nader Joseph, Ketchum Karen A., Goffeau André, Rigaud Jean-Louis, Characterization of a Hyperthermophilic P-type ATPase fromMethanococcus jannaschiiExpressed in Yeast, 10.1074/jbc.m203871200
  6. Chadwick Christopher C., Goormaghtigh Erik, Scarborough Gene A., A hexameric form of the Neurospora crassa plasma membrane H+-ATPase, 10.1016/0003-9861(87)90041-5
  7. Kühlbrandt Werner, Auer Manfred, Scarborough Gene A., 10.1038/33967
  8. Rhee K.-H., Domain movements of plasma membrane H+-ATPase: 3D structures of two states by electron cryo-microscopy, 10.1093/emboj/cdf385
  9. Palmgren, Journal of Biological Chemistry, 266, 20470 (1991)
  10. Olsson Anne, Svennelid Fredrik, Ek Bo, Sommarin Marianne, Larsson Christer, A Phosphothreonine Residue at the C-Terminal End of the Plasma Membrane H+-ATPase Is Protected by Fusicoccin-Induced 14–3–3 Binding, 10.1104/pp.118.2.551
  11. Fuglsang Anja T., Visconti Sabina, Drumm Katrine, Jahn Thomas, Stensballe Allan, Mattei Benedetta, Jensen Ole N., Aducci Patrizia, Palmgren Michael G., Binding of 14-3-3 Protein to the Plasma Membrane H+-ATPase AHA2 Involves the Three C-terminal Residues Tyr946-Thr-Val and Requires Phosphorylation of Thr947, 10.1074/jbc.274.51.36774
  12. Camoni Lorenzo, Iori Valentina, Marra Mauro, Aducci Patrizia, Phosphorylation-dependent Interaction between Plant Plasma Membrane H+-ATPase and 14-3-3 Proteins, 10.1074/jbc.275.14.9919
  13. Maudoux Olivier, Batoko Henri, Oecking Claudia, Gevaert Kris, Vandekerckhove Joel, Boutry Marc, Morsomme Pierre, A Plant Plasma Membrane H+-ATPase Expressed in Yeast Is Activated by Phosphorylation at Its Penultimate Residue and Binding of 14-3-3 Regulatory Proteins in the Absence of Fusicoccin, 10.1074/jbc.m909690199
  14. Kinoshita T., Blue light activates the plasma membrane H+-ATPase by phosphorylation of the C-terminus in stomatal guard cells, 10.1093/emboj/18.20.5548
  15. Trends in plant science, 2, 60 (1997)
  16. Annals of the New York Academy of Sciences, 986, 198 (2002)
  17. Luo Hong, Morsomme Pierre, Boutry Marc, The Two Major Types of Plant Plasma Membrane H+-ATPases Show Different Enzymatic Properties and Confer Differential pH Sensitivity of Yeast Growth, 10.1104/pp.119.2.627
  18. Dambly Stéphanie, Boutry Marc, The Two Major Plant Plasma Membrane H+-ATPases Display Different Regulatory Properties, 10.1074/jbc.m007740200
  19. Morsomme, The EMBO Journal, 15, 5513 (1996)
  20. Svennelid F., Phosphorylation of Thr-948 at the C Terminus of the Plasma Membrane H+-ATPase Creates a Binding Site for the Regulatory 14-3-3 Protein, 10.1105/tpc.11.12.2379
  21. Schagger H., Cramer W.A., Vonjagow G., Analysis of Molecular Masses and Oligomeric States of Protein Complexes by Blue Native Electrophoresis and Isolation of Membrane Protein Complexes by Two-Dimensional Native Electrophoresis, 10.1006/abio.1994.1112
  22. Biophysical Journal Meeting Abstracts, 66, 1804 (1994)
  23. Van Heel Marin, Frank Joachim, Use of multivariate statistics in analysing the images of biological macromolecules, 10.1016/0304-3991(81)90059-0
  24. Marco Sergio, Chagoyen Mónica, de la Fraga Luis Gerardo, Carazo Jose María, Carrascosa Jose L, A variant to the “random approximation” of the reference-free alignment algorithm, 10.1016/s0304-3991(96)00083-6
  25. de la Fraga Luis Gerardo, Dopazo Joaqui´n, Carazo Jose´Mari´a, Confidence limits for resolution estimation in image averaging by random subsampling, 10.1016/0304-3991(95)00080-1
  26. Marabini R., Masegosa I.M., San Martı́n M.C., Marco S., Fernández J.J., de la Fraga L.G., Vaquerizo C., Carazo J.M., Xmipp: An Image Processing Package for Electron Microscopy, 10.1006/jsbi.1996.0036
  27. Würtele Martin, Jelich-Ottmann Christian, Wittinghofer Alfred, Oecking Claudia, Structural view of a fungal toxin acting on a 14-3-3 regulatory complex, 10.1093/emboj/cdg104
Bibliographic reference Kanczewska, Justyna ; Marco, Sergio ; Vandermeeren, Caroline ; Maudoux, Olivier ; Rigaud, Jean-Louis ; et. al. Activation of the plant plasma membrane H+-ATPase by phosphorylation and binding of 14-3-3 proteins converts a dimer into a hexamer.. In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 102, no. 33, p. 11675-80 (2005)
Permanent URL http://hdl.handle.net/2078.1/12801