Function and specificity of 14-3-3 proteins in the regulation of carbohydrate and nitrogen metabolism.

Protein phosphorylation is key to the regulation of many proteins. Altered protein activity often requires the interaction of the phosphorylated protein with a class of "adapters" known as 14-3-3 proteins. This review will cover aspects of 14-3-3 interaction with key proteins of carbon and nitrogen metabolism such as nitrate reductase, glutamine synthetase and sucrose-phosphate synthase. It will also address 14-3-3 involvement in signal transduction pathways with emphasis on the regulation of plant metabolism. To date, 14-3-3 proteins have been identified and studied in many diverse systems, yielding a plethora of data, requiring careful analysis and interpretation. Problems such as these are not uncommon when dealing with multigene families. The number of isoforms makes the question of redundancy versus specificity of 14-3-3 proteins a crucial one. This issue is discussed in relation to structure, function and expression of 14-3-3 proteins.

[1]  C. Rommel,et al.  Activated Ras displaces 14-3-3 protein from the amino terminus of c-Raf-1. , 1996, Oncogene.

[2]  S. Huber,et al.  Identification of the major regulatory phosphorylation site in sucrose-phosphate synthase. , 1993, Archives of biochemistry and biophysics.

[3]  Steven C. Huber,et al.  ROLE AND REGULATION OF SUCROSE-PHOSPHATE SYNTHASE IN HIGHER PLANTS. , 1996, Annual review of plant physiology and plant molecular biology.

[4]  C. Larsson,et al.  A phosphothreonine residue at the C-terminal end of the plasma membrane H+-ATPase is protected by fusicoccin-induced 14-3-3 binding. , 1998, Plant physiology.

[5]  J. Kijne,et al.  Subcellular differences in post‐translational modification of barley 14‐3‐3 proteins , 2000, FEBS letters.

[6]  M. Yaffe,et al.  The Structural Basis for 14-3-3:Phosphopeptide Binding Specificity , 1997, Cell.

[7]  A. Shaw,et al.  The 14-3-3 proteins , 2000, Current Biology.

[8]  S. Huber,et al.  Control of plant enzyme activity by reversible protein phosphorylation , 1994 .

[9]  R. Burgoyne,et al.  Interaction between protein kinase C and Exo1 (14-3-3 protein) and its relevance to exocytosis in permeabilized adrenal chromaffin cells. , 1992, The Biochemical journal.

[10]  F. Madueño,et al.  Dimerization of Arabidopsis 14‐3‐3 proteins: structural requirements within the N‐terminal domain and effect of calcium , 1999, FEBS letters.

[11]  E Ruoslahti,et al.  Isolation of high-affinity peptide antagonists of 14-3-3 proteins by phage display. , 1999, Biochemistry.

[12]  R. Ferl,et al.  14‐3‐3 proteins associate with the regulatory phosphorylation site of spinach leaf nitrate reductase in an isoform‐specific manner and reduce dephosphorylation of Ser‐543 by endogenous protein phosphatases , 1996, FEBS letters.

[13]  H. Goodman,et al.  Cloning and expression of an Arabidopsis gene encoding a putative peroxisomal ascorbate peroxidase , 1997, Plant Molecular Biology.

[14]  A. Aitken,et al.  Phosphorylated nitrate reductase from spinach leaves is inhibited by 14-3-3 proteins and activated by fusicoccin , 1996, Current Biology.

[15]  C. MacKintosh,et al.  14‐3‐3s regulate global cleavage of their diverse binding partners in sugar‐starved Arabidopsis cells , 2000, The EMBO journal.

[16]  Bert de Boer,et al.  Fusicoccin — a key to multiple 14-3-3 locks? , 1997 .

[17]  C. Larsson,et al.  Data mining the Arabidopsis genome reveals fifteen 14-3-3 genes. Expression is demonstrated for two out of five novel genes. , 2001, Plant physiology.

[18]  A. Prescha,et al.  Increase in lipid content in potato tubers modified by 14-3-3 gene overexpression. , 2001, Journal of agricultural and food chemistry.

[19]  Masahiko Watanabe,et al.  Molecular cloning of cDNA to rat 14-3-3 η chain polypeptide and the neuronal expression of the mRNA in the central nervous system , 1991 .

[20]  W. Kaiser,et al.  5‐Aminoimidazole‐4‐carboxamide riboside activates nitrate reductase in darkened spinach and pea leaves , 1996 .

[21]  I. Dahse,et al.  Over‐expression of plant 14‐3‐3 proteins in tobacco: enhancement of the plasmalemma K+ conductance of mesophyll cells 1 2 , 1997, FEBS letters.

[22]  C. MacKintosh Regulation of spinach-leaf nitrate reductase by reversible phosphorylation. , 1992, Biochimica et biophysica acta.

[23]  D. Toroser,et al.  Site‐specific regulatory interaction between spinach leaf sucrose‐phosphate synthase and 14‐3‐3 proteins , 1998, FEBS letters.

[24]  X. F. Zhang,et al.  Identification of the 14.3.3 ζ Domains Important for Self-association and Raf Binding (*) , 1995, The Journal of Biological Chemistry.

[25]  R. Tischner,et al.  The chloroplastic glutamine synthetase (GS-2) of tobacco is phosphorylated and associated with 14-3-3 proteins inside the chloroplast , 2001, Planta.

[26]  F. D. Carlson Physiological and Biochemical Aspects of Nervous Integration , 1968 .

[27]  V. Dixit,et al.  14-3-3 Proteins Associate with A20 in an Isoform-specific Manner and Function Both as Chaperone and Adapter Molecules* , 1996, The Journal of Biological Chemistry.

[28]  S. Huber,et al.  Post-translational regulation of nitrate reductase activity: a role for Ca2+ and 14-3-3 proteins , 1996 .

[29]  J. Kijne,et al.  Differences in spatial expression between 14-3-3 isoforms in germinating barley embryos. , 1999, Plant physiology.

[30]  M. Piotrowski,et al.  Five new 14-3-3 isoforms from Nicotiana tabacum L.: implications for the phylogeny of plant 14-3-3 proteins , 1997, Planta.

[31]  N. Crawford,et al.  Identification in vitro of a post-translational regulatory site in the hinge 1 region of Arabidopsis nitrate reductase. , 1996, The Plant cell.

[32]  J. Schjoerring,et al.  Post-translational regulation of cytosolic glutamine synthetase by reversible phosphorylation and 14-3-3 protein interaction. , 2000, The Plant journal : for cell and molecular biology.

[33]  R. Ferl,et al.  Brain proteins in plants: an Arabidopsis homolog to neurotransmitter pathway activators is part of a DNA binding complex. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[34]  S. W. Wang,et al.  Localization of 14-3-3 proteins in the nuclei of arabidopsis and maize. , 1997, The Plant journal : for cell and molecular biology.

[35]  R. Ferl,et al.  Molecular organization and tissue-specific expression of an Arabidopsis 14-3-3 gene. , 1996, The Plant cell.

[36]  Robert J. Ferl,et al.  14-3-3 PROTEINS AND SIGNAL TRANSDUCTION. , 1996, Annual review of plant physiology and plant molecular biology.

[37]  H. Korthout,et al.  A fusicoccin binding protein belongs to the family of 14-3-3 brain protein homologs. , 1994, The Plant cell.

[38]  The expression of 14-3-3 isoforms in potato is developmentaly regulated , 1998 .

[39]  R. Ferl,et al.  Regulation of starch accumulation by granule-associated plant 14-3-3 proteins. , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[40]  C. Lillo Light/dark regulation of higher plant nitrate reductase related to hysteresis and calcium/magnesium inhibition , 1994 .

[41]  C. Oecking,et al.  Association of 14-3-3 proteins with the C-terminal autoinhibitory domain of the plant plasma-membrane H+-ATPase generates a fusicoccin-binding complex , 1999, Planta.

[42]  A. Cashmore,et al.  Photoregulated gene expression may involve ubiquitous DNA binding proteins. , 1990, The EMBO journal.

[43]  S. Kawabata,et al.  cDNA cloning and characterization of mitochondrial import stimulation factor (MSF) purified from rat liver cytosol. , 1994, Journal of biochemistry.

[44]  Julio Salinas,et al.  Two related low-temperature-inducible genes of Arabidopsis encode proteins showing high homology to 14-3-3 proteins, a family of putative kinase regulators , 1994, Plant Molecular Biology.

[45]  W. Campbell,et al.  Nitrate Reductase Biochemistry Comes of Age , 1996, Plant physiology.

[46]  Robert J. Ferl,et al.  A single Arabidopsis GF14 isoform possesses biochemical characteristics of diverse 14-3-3 homologues , 1994, Plant Molecular Biology.

[47]  E. Lagendijk,et al.  Characterization of the yeast BMH1 gene encoding a putative protein homologous to mammalian protein kinase II activators and protein kinase C inhibitors , 1992, FEBS letters.

[48]  P. Liao,et al.  The inhibitor protein of phosphorylated nitrate reductase from spinach (Spinacia oleracea) leaves is a 14‐3‐3 protein , 1996, FEBS letters.

[49]  A. Prescha,et al.  Repression of the 14-3-3 gene affects the amino acid and mineral composition of potato tubers. , 2002, Journal of agricultural and food chemistry.

[50]  W. Kaiser,et al.  Partial Purification and Characterization of a Calcium-Dependent Protein Kinase and an Inhibitor Protein Required for Inactivation of Spinach Leaf Nitrate Reductase , 1995, Plant physiology.

[51]  J. Rostas,et al.  Subcellular Localisation of 14‐3‐3 Isoforms in Rat Brain Using Specific Antibodies , 1994, Journal of Neurochemistry.

[52]  D. Bowles,et al.  Fusicoccin, 14-3-3 proteins, and defense responses in tomato plants. , 1999, Plant physiology.

[53]  Christine Finnie,et al.  14-3-3 proteins: eukaryotic regulatory proteins with many functions , 1999, Plant Molecular Biology.

[54]  R. Epand,et al.  Protein Kinase C , 1993, British Journal of Cancer.

[55]  T. Isobe,et al.  The 14‐3‐3 protein binds its target proteins with a common site located towards the C‐terminus , 1997, FEBS letters.

[56]  J. Soll,et al.  14-3-3 Proteins Form a Guidance Complex with Chloroplast Precursor Proteins in Plants , 2000, Plant Cell.

[57]  I. Graham,et al.  Arabidopsis Seedling Growth, Storage Lipid Mobilization, and Photosynthetic Gene Expression Are Regulated by Carbon:Nitrogen Availability1 , 2002, Plant Physiology.

[58]  H. Thordal-Christensen,et al.  A pathogen-induced gene of barley encodes a protein showing high similarity to a protein kinase regulator. , 1992, The Plant journal : for cell and molecular biology.

[59]  S. Masters,et al.  14-3-3 proteins: structure, function, and regulation. , 2000, Annual review of pharmacology and toxicology.

[60]  S. Huber,et al.  Biological significance of divalent metal ion binding to 14-3-3 proteins in relationship to nitrate reductase inactivation. , 1998, Plant & cell physiology.

[61]  T. Isobe,et al.  Brain 14‐3‐3 protein is an activator protein that activates tryptophan 5‐monooxygenase and tyrosine 3‐monooxygenase in the presence of Ca2+,calmodulin‐dependent protein kinase II , 1987, FEBS letters.

[62]  M. Stitt,et al.  Nitrate regulation of metabolism and growth. , 1999, Current opinion in plant biology.

[63]  R. Ferl,et al.  Functional elements of the Arabidopsis Adh promoter include the G-box , 1992, Plant Molecular Biology.

[64]  T. Kinoshita,et al.  Specific binding of vf14-3-3a isoform to the plasma membrane H+-ATPase in response to blue light and fusicoccin in guard cells of broad bean. , 2001, Plant physiology.

[65]  A. Kandlbinder,et al.  Modulation of nitrate reductase: some new insights, an unusual case and a potentially important side reaction. , 2002, Journal of experimental botany.

[66]  S. Howell,et al.  Expression and characterization of maize ZBP14, a member of a new family of zinc-binding proteins. , 1995, Biochemical Journal.

[67]  M. Gibbs,et al.  RESPIRATION DURING PHOTOSYNTHESIS. , 1964, Record of chemical progress.

[68]  C. Testerink,et al.  14‐3‐3 proteins interact with a 13‐lipoxygenase, but not with a 9‐lipoxygenase , 2000, FEBS letters.

[69]  R. Ferl,et al.  Characterization of the Arabidopsis Adh G-box binding factor. , 1990, The Plant cell.

[70]  R. Ferl,et al.  The arabidopsis 14-3-3 family of signaling regulators. , 2001, Plant physiology.

[71]  P. Allen,et al.  Interaction of 14-3-3 with Signaling Proteins Is Mediated by the Recognition of Phosphoserine , 1996, Cell.

[72]  R S Quatrano,et al.  14-3-3 Proteins Are Part of an Abscisic Acid–VIVIPAROUS1 (VP1) Response Complex in the Em Promoter and Interact with VP1 and EmBP1 , 1998, Plant Cell.

[73]  G M Coruzzi,et al.  Carbon and nitrogen sensing and signaling in plants: emerging 'matrix effects'. , 2001, Current opinion in plant biology.

[74]  R. Liddington,et al.  Crystal structure of the zeta isoform of the 14-3-3 protein , 1995, Nature.

[75]  A. Toker,et al.  Protein kinase C inhibitor proteins. Purification from sheep brain and sequence similarity to lipocortins and 14-3-3 protein. , 1990, European journal of biochemistry.

[76]  M. Sugiyama,et al.  Cloning and Characterization of Polyphenol Oxidase cDNAs of Phytolacca americana , 1995, Plant physiology.

[77]  S. Ishida,et al.  14-3-3 Proteins Regulate Intracellular Localization of the bZIP Transcriptional Activator RSG Article, publication date, and citation information can be found at www.aspb.org/cgi/doi/10.1105/tpc.010188. , 2001, The Plant Cell Online.

[78]  C. Meyer,et al.  Characterization of Nitrate Reductase from Light- and Dark-Exposed Leaves (Comparison of Different Species and Effects of 14-3-3 Inhibitor Proteins) , 1997, Plant physiology.

[79]  N. Crawford,et al.  Nitrate: nutrient and signal for plant growth. , 1995, The Plant cell.

[80]  Y. Inoue,et al.  Molecular cloning of rat cDNAs for the zeta and theta subtypes of 14-3-3 protein and differential distributions of their mRNAs in the brain. , 1994, Brain research. Molecular brain research.

[81]  W. Kaiser,et al.  14‐3‐3 proteins control proteolysis of nitrate reductase in spinach leaves , 1999, FEBS letters.

[82]  M. Redinbaugh,et al.  Reversible light/dark modulation of spinach leaf nitrate reductase activity involves protein phosphorylation. , 1992, Archives of biochemistry and biophysics.

[83]  S. Masters,et al.  Interaction of 14-3-3 with a nonphosphorylated protein ligand, exoenzyme S of Pseudomonas aeruginosa. , 1999, Biochemistry.

[84]  R. Ferl,et al.  Two Genes Encoding GF14 (14-3-3) Proteins in Zea mays (Structure, Expression, and Potential Regulation by the G-Box-Binding Complex) , 1994, Plant physiology.

[85]  Brian W. Bowen,et al.  Evolutionary implications of the family of 14-3-3 brain protein homologs in Arabidopsis thaliana , 2004, Genetica.

[86]  S. Kromer RESPIRATION DURING PHOTOSYNTHESIS , 1995 .

[87]  K. Koch CARBOHYDRATE-MODULATED GENE EXPRESSION IN PLANTS. , 1996, Annual review of plant physiology and plant molecular biology.

[88]  R. Ferl,et al.  Sequences of Three Arabidopsis General Regulatory Factor Genes Encoding GF14 (14-3-3) Proteins , 1995, Plant physiology.

[89]  R. Ferl,et al.  Specific Interactions with TBP and TFIIB in Vitro Suggest That 14-3-3 Proteins May Participate in the Regulation of Transcription When Part of a DNA Binding Complex , 1999, Plant Cell.

[90]  Robert J. Ferl,et al.  Evolution of the 14-3-3 Protein Family: Does the Large Number of Isoforms in Multicellular Organisms Reflect Functional Specificity? , 2000, Journal of Molecular Evolution.

[91]  R. Ferl,et al.  The Arabidopsis 14-3-3 Multigene Family , 1997, Plant physiology.

[92]  S. Huber,et al.  Divalent cations and polyamines bind to loop 8 of 14-3-3 proteins, modulating their interaction with phosphorylated nitrate reductase. , 2002, The Plant journal : for cell and molecular biology.

[93]  M. Palmgren,et al.  14‐3‐3 proteins activate a plant calcium‐dependent protein kinase (CDPK) , 1998, FEBS letters.

[94]  A. Carr,et al.  The 14-3-3 proteins encoded by the BMH1 and BMH2 genes are essential in the yeast Saccharomyces cerevisiae and can be replaced by a plant homologue. , 1995, European journal of biochemistry.

[95]  Booij,et al.  14-3-3 proteins double the number of outward-rectifying K+ channels available for activation in tomato cells , 1999, The Plant journal : for cell and molecular biology.

[96]  S. Huber,et al.  Phosphorylated nitrate reductase and 14-3-3 proteins. Site of interaction, effects of ions, and evidence for an amp-binding site on 14-3-3 proteins. , 1998, Plant physiology.

[97]  C. MacKintosh,et al.  Identification of a regulatory phosphorylation site in the hinge 1 region of nitrate reductase from spinach (Spinacea oleracea) leaves , 1995, FEBS letters.

[98]  J Pohl,et al.  14-3-3ζ Binds a Phosphorylated Raf Peptide and an Unphosphorylated Peptide via Its Conserved Amphipathic Groove* , 1998, The Journal of Biological Chemistry.

[99]  E. Weiler,et al.  The fusicoccin receptor of plants is a member of the 14‐3‐3 superfamily of eukaryotic regulatory proteins , 1994, FEBS letters.

[100]  R. Bodnar,et al.  RGS3 interacts with 14-3-3 via the N-terminal region distinct from the RGS (regulator of G-protein signalling) domain. , 2002, The Biochemical journal.

[101]  A Aitken,et al.  Phosphorylation-dependent interactions between enzymes of plant metabolism and 14-3-3 proteins. , 1999, The Plant journal : for cell and molecular biology.

[102]  D. Toroser,et al.  Protein Phosphorylation as a Mechanism for Osmotic-Stress Activation of Sucrose-Phosphate Synthase in Spinach Leaves , 1997, Plant physiology.

[103]  W. Kaiser,et al.  Rapid Modulation of Spinach Leaf Nitrate Reductase by Photosynthesis : II. In Vitro Modulation by ATP and AMP. , 1991, Plant physiology.

[104]  H. Sano,et al.  Light and nutritional regulation of transcripts encoding a wheat protein kinase homolog is mediated by cytokinins. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[105]  Rongchen Wang,et al.  Ser-534 in the Hinge 1 Region of ArabidopsisNitrate Reductase Is Conditionally Required for Binding of 14-3-3 Proteins and in Vitro Inhibition* , 1999, The Journal of Biological Chemistry.

[106]  Michael B Yaffe,et al.  How do 14‐3‐3 proteins work? – Gatekeeper phosphorylation and the molecular anvil hypothesis , 2002, FEBS letters.

[107]  J. Sheen,et al.  Sugar sensing in higher plants , 1997 .

[108]  Tom D. Bunney,et al.  14-3-3 protein is a regulator of the mitochondrial and chloroplast ATP synthase , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[109]  Nitrate Acts as a Signal to Induce Organic Acid Metabolism and Repress Starch Metabolism in Tobacco. , 1997, The Plant cell.

[110]  R. Dixon,et al.  Functional dissection of a bean chalcone synthase gene promoter in transgenic tobacco plants reveals sequence motifs essential for floral expression , 1996, Plant Molecular Biology.

[111]  G. Moorhead,et al.  Purification of a nitrate reductase kinase from Spinacea oleracea leaves, and its identification as a calmodulin-domain protein kinase , 1998, Planta.

[112]  A. Aitken,et al.  A plant homologue to mammalian brain 14‐3‐3 protein and protein kinase C inhibitor , 1992, FEBS letters.

[113]  M. Palmgren,et al.  The 14-3-3 protein interacts directly with the C-terminal region of the plant plasma membrane H(+)-ATPase. , 1997, The Plant cell.

[114]  Masahiko Watanabe,et al.  Molecular cloning of rat cDNAs for β and γ subtypes of 14-3-3 protein and developmental changes in expression of their mRNAs in the nervous system , 1993 .

[115]  E. Pichersky,et al.  An evolutionarily conserved protein binding sequence upstream of a plant light-regulated gene. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[116]  Jonathan Cooper,et al.  A Novel Sphingosine-dependent Protein Kinase (SDK1) Specifically Phosphorylates Certain Isoforms of 14-3-3 Protein* , 1998, The Journal of Biological Chemistry.

[117]  A. Kato,et al.  Isolation and characterization of a rice cDNA similar to the bovine brain-specific 14-3-3 protein gene , 2004, Plant Molecular Biology.

[118]  N. de Vetten,et al.  A maize protein associated with the G-box binding complex has homology to brain regulatory proteins. , 1992, The Plant cell.

[119]  M. Palmgren,et al.  Energization of Plant Cell Membranes by H+-Pumping ATPases: Regulation and Biosynthesis , 1999, Plant Cell.

[120]  M. Piotrowski,et al.  Topology and target interaction of the fusicoccin‐binding 14‐3‐3 homologs of Commelina communis , 1997 .

[121]  R. Ferl,et al.  Interaction of a plant 14-3-3 protein with the signal peptide of a thylakoid-targeted chloroplast precursor protein and the presence of 14-3-3 isoforms in the chloroplast stroma. , 2000, Plant physiology.