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A Phosphorylation in the C-terminal Auto-inhibitory Domain of the Plant Plasma Membrane H+-ATPase Activates the Enzyme with No Requirement for Regulatory 14-3-3 Proteins.

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Piette, Anne-Sophie [UCL] Derua, Rita [] Waelkens, Etienne [] Boutry, Marc [UCL] Duby, Geoffrey [UCL]

The plant plasma membrane H(+)-ATPase is regulated by an auto-inhibitory C-terminal domain that can be displaced by phosphorylation of the penultimate residue, a Thr, and the subsequent binding of 14-3-3 proteins. By mass spectrometric analysis of plasma membrane H(+)-ATPase isoform 2 (PMA2) isolated from Nicotiana tabacum plants and suspension cells, we identified a new phosphorylation site, Thr-889, in a region of the C-terminal domain upstream of the 14-3-3 protein binding site. This residue was mutated into aspartate or alanine, and the mutated H(+)-ATPases expressed in the yeast Saccharomyces cerevisiae. Unlike wild-type PMA2, which could replace the yeast H(+)-ATPases, the PMA2-Thr889Ala mutant did not allow yeast growth, whereas the PMA2-Thr889Asp mutant resulted in improved growth and increased H(+)-ATPase activity despite reduced phosphorylation of the PMA2 penultimate residue and reduced 14-3-3 protein binding. To determine whether the regulation taking place at Thr-889 was independent of phosphorylation of the penultimate residue and 14-3-3 protein binding, we examined the effect of combining the PMA2-Thr889Asp mutation with mutations of other residues that impair phosphorylation of the penultimate residue and/or binding of 14-3-3 proteins. The results showed that in yeast, PMA2 Thr-889 phosphorylation could activate H(+)-ATPase if PMA2 was also phosphorylated at its penultimate residue. However, binding of 14-3-3 proteins was not required, although 14-3-3 binding resulted in further activation. These results were confirmed in N. tabacum suspension cells. These data define a new H(+)-ATPase activation mechanism that can take place without 14-3-3 proteins.

Document type Article de périodique (Journal article) – Article de recherche – Journal Article, Research Support, Non-U.S. Gov't
Access type Accès restreint
Publication date 2011
Language Anglais
Journal information "Journal of Biological Chemistry" - Vol. 286, no. 21, p. 18474-82 (2011)
Peer reviewed yes
Publisher American Society for Biochemistry and Molecular Biology, Inc. ((United States) Baltimore)
issn 0021-9258
Publication status Publié
Affiliations UCL - SST/ISV - Institut des sciences de la vie
UCL - SST/LIBST - Louvain Institute of Biomolecular Science and Technology
MESH Subject Tobacco - enzymology - genetics ; Saccharomyces cerevisiae - genetics - metabolism ; Recombinant Proteins - genetics - metabolism ; Proton-Translocating ATPases - genetics - metabolism ; Protein Structure, Tertiary ; Plant Proteins - genetics - metabolism ; Phosphorylation ; Mutation, Missense ; Enzyme Activation - physiology ; Cell Membrane - enzymology - genetics ; Amino Acid Substitution ; 14-3-3 Proteins - genetics - metabolism
Keywords 3100
Links
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Bibliographic reference Piette, Anne-Sophie ; Derua, Rita ; Waelkens, Etienne ; Boutry, Marc ; Duby, Geoffrey. A Phosphorylation in the C-terminal Auto-inhibitory Domain of the Plant Plasma Membrane H+-ATPase Activates the Enzyme with No Requirement for Regulatory 14-3-3 Proteins.. In: Journal of Biological Chemistry, Vol. 286, no. 21, p. 18474-82 (2011)
Permanent URL http://hdl.handle.net/2078.1/75938