Tyrosine Phosphorylation Inhibits the Interaction of 14-3-3 Proteins with the Plant Plasma Membrane H⁺-ATPase

Abstract

Interaction of 14-3-3 proteins with their targets depends not only on the phosphorylation status of the target but also on that of 14-3-3 ([Fu et al., 2000]). In this work we demonstrated that the maize 14-3-3 isoform GF14-6 is a substrate of the tyrosine kinase insulin growth factor receptor 1. By means of site-directed mutants of GF14-6, we identified Tyr-137 as the specific tyrosine residue phosphorylated by the insulin growth factor receptor 1. Phosphorylation of GF14-6 on Tyr-137 lowered its affinity for a peptide mimicking the 14-3-3 binding site of the plant plasma membrane H⁺-ATPase. Moreover, phosphorylation in planta of 14-3-3 tyrosine residues, resulting from incubation with the tyrosine phosphatase inhibitor, phenylarsine oxide, decreased their association to the H⁺-ATPase.

14-3-3 proteins - plasma membrane H⁺-ATPase - tyrosine phosphorylation - signal transduction

References

• 1 Aducci P., Camoni L., Marra M., Visconti S.. From cytosol to organelles: 14-3-3 proteins as multifunctional regulators of plant cell.  IUBMB life. (2002);  53 49-55
• 2 Aitken A.. Functional specificity in 14-3-3 isoform interactions through dimer formation and phosphorylation. Chromosome location of mammalian isoforms and variants.  Plant Mol. Biol.. (2002);  50 993-1010
• 3 Ballio A., Carilli A., Santurbano B., Tuttobello L.. Produzione di fusicoccina in scala pilota.  Ann. Ist. Super. Sanità. (1968);  4 317-332
• 4 Baunsgaard L., Fuglsang A. T., Jahn T., Korthout H. A. A. J., de Boer A. H., Palmgren M. G.. The 14-3-3s associate with the plasma membrane H⁺-ATPase to generate a fusicoccin binding complex and a fusicoccin responsive system.  Plant J.. (1998);  13 661-671
• 5 Baur M., Meyer A. J., Heumann H. G., Lützelschwab M., Michalke W.. Distribution of plasma membrane H⁺-ATPase and polar current patterns in leaves and stems of Elodea canadensis. .  Botanica Acta. (1996);  109 382-387
• 6 Bradford M. M.. A rapid and sensitive method for the quantification of microgram quantities of protein using the principle of protein dye binding.  Anal. Biochem.. (1976);  72 248-254
• 7 Camoni L., Iori V., Marra M., Aducci P.. Phosphorylation-dependent interaction between plant plasma membrane H⁺-ATPase and 14-3-3 proteins.  J. Biol. Chem.. (2000);  275 9919-9923
• 8 Camoni L., Visconti S., Marra M., Aducci P.. Adenosine 5′-monophosphate inhibits the association of 14-3-3 proteins with the plant plasma membrane H(⁺)-ATPase.  J. Biol. Chem.. (2001);  276 31709-31712
• 9 Cooper J. A., Esch F. S., Taylor S. S., Hunter T.. Phosphorylation sites in enolase and lactate dehydrogenase utilized by tyrosine protein kinase in vivo and in vitro. .  J. Biol. Chem.. (1984);  259 7835-7841
• 10 Curti G., Massardi F., Lado P.. Synergistic activation of plasma membrane H⁺-ATPase in Arabidopsis thaliana cells by turgor decrease and by fusicoccin.  Physiol. Plant.. (1993);  87 592-600
• 11 Finnie C., Borch J., Collinge D. B.. 14-3-3s: eukaryotic regulatory proteins with many functions.  Plant Mol. Biol.. (1999);  40 545-554
• 12 Frangioni J. V., Neel B. G.. Solubilization and purification of enzymatically active glutathione S-transferase (pGEX) fusion proteins.  Anal. Biochem.. (1993);  210 179-187
• 13 Fu H., Subramanian R. R., Masters S. C.. 14-3-3 proteins: structure, function and regulation.  Annu. Rev. Pharmacol. Toxicol.. (2000);  40 617-647
• 14 Fuglsang A. T., Visconti S., Drumm K., Jahn T., Stensballe A., Mattei B., Jensen O. N., Aducci P., Palmgren M. 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.  J. Biol. Chem.. (1999);  274 36774-36780
• 15 Fullone M. R., Visconti S., Marra M., Fogliano V., Aducci P.. Fusicoccin effect on the in vitro interaction between plant 14-3-3s and plasma membrane H⁺-ATPase.  J. Biol. Chem.. (1998);  273 7698-7702
• 16 Furlanetto R. W., Dey B. R., Lopaczynski W., Nissley S. P.. 14-3-3 proteins interact with the insulin-like growth factor receptor but not the insulin receptor.  Biochem. J.. (1997);  327 765-771
• 17 Hunter T.. Synthetic peptide substrates for a tyrosine protein kinase.  J. Biol. Chem.. (1982);  257 4843-4848
• 18 Laemmli U. K.. Cleavage of structural proteins during the assembly of the head of bacteriofage T4.  Nature. (1970);  227 680-685
• 19 Lu G., Sehnke P. C., Ferl R. J.. Phosphorylation and calcium binding properties of an Arabidopsis GF14 brain protein homolog.  Plant Cell. (1994);  6 501-510
• 20 Luan S., Ting J., Gupta R.. Protein tyrosine phosphatases in higher plants.  New Phytol.. (2001);  151 155-164
• 21 Markwell M. A. K., Haas S. M., Bieber L. L., Tolbert N. E.. A modification of the Lowry procedure to simplify protein determination in membrane and lipoprotein samples.  Anal. Biochem.. (1978);  87 206-210
• 22 Marra M., Fullone M. R., Fogliano V., Pen J., Mattei M., Masi S., Aducci P.. The 30-kilodalton protein present in purified fusicoccin receptor preparations is a 14-3-3-like protein.  Plant Physiol.. (1994);  106 1497-1501
• 23 Marra M., Fogliano V., Zambardi A., Fullone M. R., Nasta D., Aducci P.. The H⁺-ATPase purified from maize root plasma membranes retains fusicoccin in vivo activation.  FEBS Lett.. (1996);  382 293-296
• 24 Marra M., Olivari C., Visconti S., Albumi C., Aducci P., De Michelis M. I.. A phosphopeptide corresponding to the cytosolic stretch connecting transmembrane segments 8 and 9 of the plasma membrane H⁺-ATPase binds 14-3-3 proteins and inhibits fusicoccin-induced activation of the H⁺-ATPase.  Plant Biology. (2000);  2 1-6
• 25 Marré E., Bellando M., Beffagna N., Marré M. T., Romani G., Vergani P.. Synergisms, additive and non additive factors regulating proton extrusion and intracellular pH. Sharp, R., Novacky, A. J., and Randall, D. D., eds. Current Topics in Plant Biochemistry and Physiology, Vol. 11. Columbia, Missouri; The Interdisciplinary Plant Group (1993): 213-230
• 26 Moorhead G., Douglas P., Cotelle V., Harthill J., Morrice N., Meek S., Deiting U., Stitt M., Scarabel M., Aitken A., MacKintosh C.. Phosphorylation-dependent interactions between enzymes of plant metabolism and 14-3-3 proteins.  Plant J.. (1999);  18 1-12
• 27 Morandini P., Valera M., Albumi C., Bonza M. C., Giacometti S., Ravera G., Murgia I., Soave C., De Michelis M. I.. A novel interaction partner for the C-terminus of Arabidopsis thaliana plasma membrane H⁺-ATPase (AHA1 isoform): site and mechanism of action on H⁺-ATPase activity differ from those of 14-3-3 proteins.  Plant J.. (2002);  31 487-497
• 28 Muslin A. J., Tanner J. W., Allen P. M., Shaw A. S.. Interaction of 14-3-3 with signaling proteins is mediated by the recognition of phosphoserine.  Cell. (1996);  84 889-897
• 29 Obsil T., Ghirlando R., Klein D. C., Ganguly S., Dyda F.. Crystal structure of the 14-3-3ζ : serotonin N-acetyltransferase complex: a role for scaffolding in enzyme regulation.  Cell. (2001);  105 257-267
• 30 Olivari C., Meanti C., De Michelis M. I., Rasi-Caldogno F.. Fusicoccin binding to its plasma membrane receptor and the activation of the plasma membrane H⁺-ATPase. IV. Fusicoccin induces the association between the plasma membrane H⁺-ATPase and the fusicoccin receptor.  Plant Physiol.. (1998);  116 529-537
• 31 Olivari C., Albumi C., Pugliarello M. C., De Michelis M. I.. Phenylarsine oxide inhibits the fusicoccin-induced activation of plasma membrane H⁺-ATPase.  Plant Physiol.. (2000);  122 463-470
• 32 Olsson A., Svennelid F., Ek B., Sommarin M., Larsson C.. A phosphothreonine residue at the C-terminal end of the plasma membrane H⁺-ATPase is protected by fusicoccin-induced 14-3-3 binding.  Plant Physiol.. (1998);  118 551-555
• 33 Palmgren M. G.. Plant plasma membrane H⁺-ATPases: powerhouses for nutrient uptake. Annu. Rev. Plant Physiol.  Plant Mol. Biol.. (2001);  52 817-845
• 34 Palmgren M. G., Fuglsang A. T., Jahn T.. Deciphering the role of 14-3-3 proteins.  Exp. Biol. Online. (1998);  3 4
• 35 Patschinsky T., Hunter T., Esch F. S., Cooper J. A., Sefton B. M.. Analysis of the sequence of amino acids surrounding site of tyrosine phosphorylation.  Proc. Natl. Acad. Sci. USA. (1982);  79 973-977
• 36 Rasi-Caldogno F., Pugliarello M. C., Olivari C., De Michelis M. I.. Controlled proteolysis mimics the effect of fusicoccin on the plasma membrane H⁺-ATPase.  Plant Physiol.. (1993);  103 391-398
• 37 Regenberg B., Villalba J. M., Lanfermeijer F. C., Palmgren M. G.. C-terminal deletion analysis of plant plasma membrane H⁺-ATPase: yeast as model system for solute transport across the plasma membrane.  Plant Cell. (1995);  7 1655-1666
• 38 Reuther G. W., Fu H., Cripe L. D., Collier R. J., Pendergast A. M.. Association of the protein kinases c-Bcr and Bcr-Abl with proteins of the 14-3-3 family.  Science. (1994);  266 129-133
• 39 Roberts M. R.. Regulatory 14-3-3 protein-protein interactions in plant cells.  Curr. Opin. Plant Biol.. (2000);  3 400-405
• 40 Svennelid F., Olsson A., Piotrowski M., Rosenquist M., Ottman C., Larsson C., Oecking C., Sommarin M.. 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.  Plant Cell. (1999);  11 2379-2391
• 41 Tzivion G., Avruch J.. 14-3-3 proteins: active cofactors in cellular regulation by serine/threonine phosphorylation.  J. Biol. Chem.. (2002);  277 3061-3064
• 42 van der Hoeven P. C. J., van del Wal J. C. M., Ruurs P., van Dijk M. C. M., van Blitterswijk W. J.. 14-3-3 isotypes facilitate coupling of protein kinase C-ζ to Raf-1: negative regulation by 14-3-3 phosphorylation.  Biochem. J.. (2000);  345 297-306
• 43 Würtele M., Jelich-Ottmann C., Wittinghofer A., Oecking C.. Structural view of a fungal toxin acting on a 14-3-3 regulatory complex.  EMBO J.. (2003);  22 987-994
• 44 Yaffe M. B., Rittinger K., Volinia S., Caron P. R., Aitken A., Leffers H., Gamblin S. J., Smerdon S. K., Cantley L. C.. The structural basis for 14-3-3 : phosphopeptide binding specificity.  Cell. (1997);  91 961-971

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