Metabolic enzymes as targets for 14-3-3 proteins

Plant Molecular Biology

Volumn 50, Issue 6, 2002, Pages 1053-1063

  Huber, Steven C ^a   MacKintosh, Carol ^b   Kaiser, Werner M ^c  

^a NORTH CAROLINA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF DUNDEE   (United Kingdom)

^c UNIVERSITY OF WÜRZBURG   (Germany)

Author keywords

14 3 3 affinity chromatography; Divalent cations; Glutamine synthetase; NADH:nitrate reductase; Polyamines; Proteolytic degradation; Sucrose phosphate synthase

Indexed keywords

BIODEGRADATION; BIOSYNTHESIS; CARBON; ENZYMES; METABOLISM; NITROGEN;

PHOSPHORYLATION;

PLANTS (BOTANY);

14-3-3 PROTEINS; ADENOSINE MONOPHOSPHATE; AMINO ACID OXIDOREDUCTASES; ENZYMES; GLUCOSYLTRANSFERASES; GLUTAMATE-AMMONIA LIGASE; GLYCERALDEHYDE-3-PHOSPHATE DEHYDROGENASES; GLYCINE DEHYDROGENASE (DECARBOXYLATING); GLYCOSIDES; MAGNESIUM; NITRATE REDUCTASE (NADH); NITRATE REDUCTASES; PHOSPHORYLATION; PLANTS; PROTEIN BINDING; RIBONUCLEOSIDES; TYROSINE 3-MONOOXYGENASE;

EID: 0036914587     PISSN: 01674412     EISSN: None     Source Type: Journal    
DOI: 10.1023/A:1021284002779     Document Type: Review

References (73)

1. Athwal, G.S. and Huber, S.C. 2002. Divalent cations and polyamines bind to loop 8 of 14-3-3 proteins, modulating their interaction with phosphorylated nitrate reductase. Plant J. 29: 1-14.
2. Athwal, G.S., Huber, J.L. and Huber, S.C. 1998a. Phosphorylated nitrate reductase and 14-3-3 proteins: The site of interaction, effects of ions, and evidence for an AMP binding site on 14-3-3 proteins. Plant Physiol. 118: 1041-1048.
3. Athwal, G.S., Huber, J.L. and Huber, S.C. 1998b. Biological significance of divalent cation binding to 14-3-3 proteins in relationship to nitrate reductase inactivation. Plant Cell Physiol. 39: 1065-1072.
4. Athwal, G.S., Lombardo, C.R., Huber, J.L., Masters, S.C., Fu, H. and Huber, S.C. 2000. Modulation of 14-3-3 protein interactions with target polypeptides by physical and metabolic effectors. Plant Cell Physiol. 41: 523-533.
5. Bachmann, M., Huber, J.L., Liao, P.-C., Gage, D.A., Huber, S.C. 1996a. The inhibitor protein of phosphorylated nitrate reductase from spinach (Spinacia oleracea L.) leaves is a 14-3-3 protein. FEBS Lett. 387: 127-131.
6. Bachmann, M., Huber, J.L., Athwal, G.S., Wu K., Ferl, R.J. and Huber, S.C. 1996b. 14-3-3 Proteins associate with the regulatory phosphorylation site of spinach leaf nitrate reductase in an isoform-specific manner and reduce dephosphorylation by endogenous protein phosphatases. FEBS Lett. 398: 26-30.
7. Bachmann, M., Shiraishi, N., Campbell, W.H., Yoo, B.-C., Harmon, A. and Huber, S.C. 1996c. Identification of Ser-543 as the major regulatory phosphorylation site in spinach leaf nitrate reductase. Plant Cell 8: 505-517.
8. Bauwe, H., and Kopriva, S. 1995. The gdcsPA gene from Flaveria pringlei (Asteraceae). Plant Physiol. 107: 655-662.
9. Bihn, E.A., Paul, A.L., Wang, S.W., Erdos, G.W. and Ferl, R.J. 1997. Localization of 14-3-3 proteins in the nuclei of Arabidopsis and maize. Plant J. 12: 1439-1445.
10. Braselmann S., and McCormick, F. 1995. Ber and Raf form a complex in vivo via 14-3-3 proteins. EMBO J. 14: 4839-4848.
11. Bunney, T.D., van Walraven, H.S. and de Boer, A.H. 2001. 14-3-3 Protein is a regulator of the mitochondrial and chloroplast ATP synthase. Proc Natl. Acad. Sci. USA 98: 4249-4254.
12. Camoni, L., Harper, J.F. and Palmgren, M.G. 1998. 14-3-3 Proteins activate a plant calcium-dependent protein kinase (CDPK). FEBS Lett. 430: 381-384.
13. +-ATPase. J. Biol. Chem. 276: 31709-31712.
14. Chung, H.-J., Sehnke, P.C. and Ferl, R.J. 1999. The 14-3-3 proteins: Cellular regulators of plant metabolism. Trends Plant Sci. 4: 367-371.
15. Cotelle, V., Meek, S.E.M., Provan, F., Milne, F.C., Morrice, N. and MacKintosh, C. 2000. 14-3-3s regulate global cleavage of their diverse binding partners in sugar-starved Arabidopsis cells. EMBO J. 19: 2869-2876.
16. Douglas, P., Pigaglio, E., Ferrer, A., Halford, N.G. and MacKintosh, C. 1996. Three spinach leaf nitrate reductase/3-hydroxy-3-methylglutaryl-CoA reductase kinases that are regulated by reversible phosphorylation and/or calcium ions. Biochem. J. 325: 101-109.
17. Douglas, P., Moorhead, G., Hong, Y., Morrice N. and MacKintosh, C. 1998. Purification of a nitrate reductase kinase from Spinacea oleracea leaves, and its identification as a calmodulin-domain protein kinase. Planta 206: 435-442.
18. Finnemann, J. and Schjoerring, J.K. 2000. Post-translational regulation of cytosolic glutamine synthetase by reversible phosphorylation and 14-3-3 protein interaction. Plant J. 24: 171-181.
19. Fu, H., Subramanian R.R., and Masters, S.C. 2000. 14-3-3 Proteins: Structure, function, and regulation. Annu. Rev. Pharmacol. Toxicol. 40: 617-647.
20. +-ATPase. J. Biol. Chem. 273: 7698-7702.
21. Holtman, W.L., Roberts, M.R. and Wang, M. 2000a. 14-3-3 Proteins and a 13-lipoxygenase form associations in a phosphorylation-dependent manner. Biochem. Soc. Trans. 28: 834-836.
22. Holtman, W.L., Roberts, M.R., Oppedijk, B.J., Testerink, C., van Zeijl, M.J. and Wang, M. 2000b. 14-3-3 Proteins interact with a 13-lipoxygenase, but not with a 9-lipoxygenase. FEBS Lett. 474: 48-52.
23. Huber, S.C., and Kaiser, W.M. 1996. 5-Aminoimidazole-4-carboxamide riboside activates nitrate reductase in darkened spinach and pea leaves. Physiol. Plant. 98: 833-837.
24. Huber, J.L., Huber, S.C., Campbell, W.H. and Redinbaugh, M.G. 1992. Reversible light/dark modulation of spinach leaf nitrate reductase activity involves protein phosphorylation. Arch. Biochem. Biophys. 296: 58-65.
25. 2+ and 14-3-3 proteins. Trends Plant Sci. 1: 432-438.
26. Igamerdiev, A.U. and Kleczkowski, L.A. 2001. Implications of adenylate kinase-governed equilibrium of adenylates on contents of free magnesium in plant cells and compartments. Biochem. J. 360: 225-231.
27. Ikeda, Y., Koizumi, N., Kusano, T. and Sano, H. 2000. Specific binding of a 14-3-3 protein to autophosphorylated WPK4, an SNF1-related wheat protein kinase, and to WPK4-phosphorylated nitrate reductase. J. Biol. Chem. 275: 31695-31700.
28. Kaiser, W.M. and Huber, S.C. 1997. Correlation between apparent phosphorylation state of nitrate reductase (NR), NR hysteresis and degradation of NR protein. J. Exp. Bot. 48: 1367-1374.
29. Kaiser, W.M. and Huber, S.C. 2001. Regulation of nitrate reductase: Mechanism, physiological relevance and environmental triggers. J. Exp. Bot. 52: 1981-1989.
30. Kaiser, W.M. and Spill, D. 1991. Rapid modulation of spinach leaf nitrate reductase by photosynthesis. II. In vitro modulation by ATP and AMP. Plant Physiol. 96: 368-375.
31. Kaiser, W.M., Weiner, H. and Huber, S.C. 1999. Nitrate reductase in higher plants: A case study for transduction of environmental stimuli into control of catalytic activity. Physiol. Plant. 105: 385-390.
32. Kanamaru, K., Wang, R., Su, W., and Crawford, N.M. 1999. Ser-534 in the hinge 1 region of Arabidopsis nitrate reductase is conditionally required for binding of 14-3-3 proteins and in vitro inhibition. J. Biol. Chem. 274: 4160-4165.
33. Koyama, H. and Tsuji, M. 1983. Biochem. Pharmacol. 32: 3547-3553.
34. Liu, Y.-C., Elly, C., Yoshida, H., Bonnefoy-Berard, N. and Altman, A. 1996. Activation-modulated association of 14-3-3 proteins with Cb1 in T cells. J. Biol. Chem. 271: 14591-14595.
35. Lu, G., DeLisle, A.J., de Vetten, N.C. and Ferl, R.J. 1992. Brain proteins in plants: An Arabidopsis homolog to neurotransmitter pathway activators in part of a DNA binding complex. Proc. Natl. Acad. Sci. USA 89: 11490-11494.
36. Luo, Z.-j., Zhang, X.-f., Rapp, U. and Avruch, J. 1995. Identification of the 14.3.3 z domains important for self-association and Raf binding. J. Biol. Chem. 270: 23681-23687.
37. MacKintosh, C. 1992. Regulation of spinach-leaf nitrate reductase by reversible phosphorylation. Biochim. Biophys. Acta 1137: 121-126.
38. MacKintosh, C. and Meek, S.E.M. 2001. Regulation of plant NR activity by reversible phosphorylation, 14-3-3 proteins and proteolysis. Cell. Mol. Life Sci. 58: 205-214.
39. Man, H.-M., and Kaiser, W.M. 2001. Increased glutamine synthethase activity and changes in amino acid pools in leaves treated with 5-aminoimidazole-4-carboxyamide ribonucleoside (AICAR). Physiol. Plant. 111: 291-296.
40. May, T. and Soll, J. 2000. 14-3-3 Proteins form a guidance complex with chloroplast precursor proteins in plants. Plant Cell 12: 53-64.
41. Markiewicz, E., Wilczynski, G., Rzepecki, R., Kulma, A. and Szopa, J. 1996. The 14-3-3 protein binds to the nuclear matrix endonuclease and has a possible function in the control of plant senescence. Cell. Mol. Biol. Lett. 1: 391-415.
42. McMichael, R.W. Jr., Bachmann, M. and Huber, S.C. (1995). Spinach leaf sucrose-phosphate synthase and nitrate reductase are phosphorylated/inactivated by multiple protein kinases in vitro. Plant Physiol. 108: 1077-1082.
43. Moorhead, G., Douglas, P., Morrice, N., Scarabel, M., Aitken, A. and MacKintosh, C. 1996. Phosphorylated nitrate reductase from spinach leaves is inhibited by 14-3-3 proteins and activated by fusicoccin. Curr. Biol. 6: 1104-1113.
44. Moorehead, G., Douglas, P., Cotelle, V., Harthill, J., Morrice, N., Meek, S., Deiting, U., Scrarabel, M., Aitken, A. and MacKintosh, C. 1999. Phosphorylation-dependent interactions between enzymes of plant metabolism and 14-3-3-proteins. Plant J. 18: 1-12.
45. Muslin, A.J., Tanner, J.W., Allen, P.M. and Shaw, A.S. 1996. Interaction of 14-3-3 with signaling proteins is mediated by the recognition of phosphoserine. Cell 84: 889-897.
46. Pan, S., Sehnke, P.C., Ferl, R.J. and Gurley, W.B. 1999. Specific interactions with TBP and TFIIB in vitro suggest 14-3-3 proteins may participate in transcriptional regulation when part of a DNA binding complex. Plant Cell 11: 1591-1602.
47. Pozuela, M., MacKintosh, C., Galván, A. and Fernández, E. 2001. Cytosolic glutamine synthetase and not nitrate reductase from the green alga Chlamydomonas reinhardtii is phosphorylated and binds 14-3-3 proteins. Planta 212: 264-269.
48. Prescha, A., Swiedrych, A., Biernat, J. and Szopa, J. 2001. The increase in lipid content in potato tubers modified by 14-3-3 gene overexpression. J. 49: 3638-3643.
49. Rockel, P., Strube, F., Rockel, A., Wildt, J. and Kaiser, W.M. 2002. Regulation of nitric oxide (NO) production by plant nitrate reductase in vivo and in vitro. J. Exp. Bot. 53: 103-110.
50. Schultz, T.F., Medina, J., Hill, A. and Quatrano, R.S. 1998. 14-3-3 Proteins are part of an abscissic acid-VIVIPAROUS1 (VP1) response complex in the Em promoter and interact with VP1 and EmBP1. Plant Cell 10: 837-848.
51. Sehnke, P.C., Henry, R., Cline, K., and Ferl, R.J. 2000. Interaction of 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. Plant Physiol. 122: 235-241.
52. Sehnke, P.C., Chung, H.-J., Wu, K. and Ferl, R.J. 2001. Regulation of starch accumulation by granule-associated plant 14-3-3 proteins. Proc. Natl. Acad. Sci. USA 98: 765-770.
53. Sirover, M.A. 1999. New insights into an old protein: The functional diversity of mammalian glyceraldehydes-3-phosphate dehydrogenase. Biochim. Biophys. Acta 1432: 159-184.
54. Su, W., Huber, S.C. and Crawford, N. 1996. Identification in vitro of a post-translational regulatory site in the hinge 1 region of Arabidopsis nitrate reductase. Plant Cell 8: 519-527.
55. Sugden, C., Donaghy, P.G., Halford, N.G. and Hardie, D.G. 1999. Two SNF1-related protein kinases from spinach leaf phosphorylate and inactivate 3-hydroxy-3-methylglutaryl-coenzyme A reductase, nitrate reductase, and sucrose phosphate synthase in vitro. Plant Physiol. 120: 257-274.
56. Svennelid, F., Olsson, A., Piotrowski, M., Rosenquist, M., Ottman, C., Larsson, C., Oecking, C. and Sommarin, M. 1999. 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 11: 2379-2391.
57. Swiedrych, A., Prescha, A., Matysiak-Kata, I., Biernat, J. and Szopa, J. 2002. The repression of the 14-3-3 gene affects the amino acid and mineral composition of potato tubers. J. Agric. Food. Chem., in press.
58. Szopa, J., Wróbel, M., Matysiak-Kata, I. and Swiedrych, A. 2001. The metabolic profile of the 14-3-3 repressed transgenic potato tubers. Plant Sci. 161: 1075-1082.
59. Szopa, J., Swiedrych, A. and Matysiak-Kata, I. 2002. The repression of 14-3-3 resulting in the activation of nitrate reductase and sucrose phosphate synthase in leaves from transgenic potato plants. Physiol. Plant, in press.
60. Takahashi, S., Wakui, H., Gustafsson, J.A., Zilliacus, J. and Itoh, H. 2000. Functional interaction of the immunosuppressant mizoribine with the 14-3-3 protein. Biochem. Biophys. Res. Commun. 274: 87-92.
61. Thorson, J.A., Yu, L.W., Hsu, A.L., Shih, N.Y., Graves, P.R., Tanner, J.W., Allen, P.M., Piwnica-Worms, H. and Shaw, A.S. 1998. Mol. Cell. Biol. 18: 5229-5238.
62. Toroser, D., Athwal, G.S. and Huber, S.C. 1998. Evidence for a sequence specific regulatory interaction betweer sucrose-phosphate synthase and 14-3-3 proteins. FEBS Lett. 435: 110-114.
63. Tzivion, G., Luo, Z.-J. and Avruch, J. 1998. Nature 394: 88-92.
64. Tzivion, G., Luo, Z.-J. and Avruch, J. 2000. Calyculin A-induced vimentin phosphorylation sequensters 14-3-3 and displaces other 14-3-3 partners in vivo. J. Biol. Chem. 275: 29772-29778.
65. Vincent, M.F., Marangos, P.J., Gruber, H.E. and Van den Berghe, G. 1991. Inhibition by AICA riboside of gluconeogenesis in isolated rat hepatocytes. Diabetes 40: 1259-1266.
66. Vincenz, C. and Dixit, V.M. 1996. 14-3-3 Proteins associate with A20 in an isoform-specific manner and function both as chaperone and adapter molecules. J. Biol. Chem. 271: 20029-20034.
67. Waterman, M.J., Stavridi, E.S., Waterman, J.L. and Halazonetis, T.D. 1998. ATM-dependent activation of p53 involves dephosphorylation and association with 14-3-3 proteins. Nature Genet. 19: 175-178.
68. Weiner, H. and Kaiser, W.M. 1999. 14-3-3 Proteins control proteolysis of nitrate reductase in spinach leaves. FEBS Lett. 455: 75-78.
69. Weiner, H. and Kaiser, W.M. 2000. Binding to 14-3-3 proteins I is not sufficient to inhibit nitrate reductase in spinach leaves. FEBS Lett. 480: 217-220.
70. Wilczynski, G., Kulma, A., Sikorski, A.F. and Szopa, J. 1997. ADP-ribosylation factor (ARF) regulates camp synthesis in potato. J. Plant Physiol. 151: 689-698.
71. Wu, K., Lu, G., Sehnke, P. and Ferl, R.J. 1997. The heterologous interactions among plant 14-3-3 proteins and identification of regions that are important for dimerization. Arch. Biochem. Biophys. 339: 2-8.
72. Yaffe, M. B., Rittinger, K., Volinia, S., Caron, P.R., Aitken, A., Leffers, H., Gamblin, S.J., Smerdon, S.J. and Cantley, L.C. 1997. The structural basis for 14-3-3: Phosphopeptide binding specificity. Cell 91: 961-971.
73. Yamasaki, H. and Sakihama Y. 2000. Simultaneous production of nitric oxide and peroxynitrite by plant nitrate reductase: In vitro evidence for the NR-dependent formation of active nitrogen species. FEBS Lett. 468: 89-92.