Purification of a plant nucleotide pyrophosphatase as a protein that interferes with nitrate reductase and glutamine synthetase assays

European Journal of Biochemistry

Volumn 270, Issue 6, 2003, Pages 1356-1362

  Moorhead, Greg B G ^a,b   Meek, Sarah E M ^a   Douglas, Pauline ^a,b   Bridges, Dave ^a,b   Smith, Catherine S ^a,b   Morrice, Nick ^a   MacKintosh, Carol ^a  

^a UNIVERSITY OF DUNDEE   (United Kingdom)

^b UNIVERSITY OF CALGARY   (Canada)

Author keywords

AMP; Glutamine synthetase; Nitrate reductase; Nucleotide pyrophosphatase (nucleotide pyrophosphohydrolase); Nudix hydrolase

Indexed keywords

ADENOSINE PHOSPHATE; ADENOSINE TRIPHOSPHATE; COPPER ION; FLAVINE ADENINE NUCLEOTIDE; FLUORIDE; GLUTAMATE AMMONIA LIGASE; NICKEL; NITRATE REDUCTASE; NUCLEOTIDE PYROPHOSPHATASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; ZINC ION;

ARTICLE; BRASSICA; ENZYME ASSAY; ENZYME PURIFICATION; ENZYME SUBSTRATE; ESCHERICHIA COLI; HYDROLYSIS; NONHUMAN; PLANT; PRIORITY JOURNAL;

ADENOSINE MONOPHOSPHATE; ADENOSINE TRIPHOSPHATE; AMINO ACID SEQUENCE; BIOLOGICAL ASSAY; BRASSICA; ENZYME INHIBITORS; FLAVIN-ADENINE DINUCLEOTIDE; GLUTAMATE-AMMONIA LIGASE; MOLECULAR SEQUENCE DATA; NAD; NITRATE REDUCTASE; NITRATE REDUCTASES; PLANT PROTEINS; PYROPHOSPHATASES; SEQUENCE ALIGNMENT;

BOTRYTIS; BRASSICA; BRASSICA OLERACEA; BRASSICA OLERACEA VAR. BOTRYTIS; ESCHERICHIA COLI; SPINACIA OLERACEA;

EID: 0037353090     PISSN: 00142956     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1432-1033.2003.03509.x     Document Type: Article

References (36)

1. Douglas, P., Morrice, N. & MacKintosh, C. (1995) Identification of a regulatory phosphorylation site in the hinge 1 region of nitrate reductase from spinach (Spinacea oleracea) leaves. FEBS Lett. 377, 113-117.
2. Weiner, H. & Kaiser, W.M. (2000) Binding to 14-3-3 proteins is not sufficient to inhibit nitrate reductase in spinach leaves. FEBS Lett. 480, 217-220.
3. Glaab, J. & Kaiser, W.M. (1995) Inactivation of nitrate reductase involves NR-proteins phosphorylation and subsequent binding of an inhibitor protein. Planta 195, 514-518.
4. MacKintosh, C., Douglas, P. & Lillo, C. (1995) Identification of a protein that inhibits the phosphorylated form of nitrate reductase from spinach (Spinacea oleracea) leaves. Plant Physiol. 101, 451-457.
5. Bachmann, M., Huber, J.L., Athwal, G.S., Wu, K., Fed, R.J. & Huber, S.C. (1996) 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. FEBS Lett. 398, 26-30.
6. Moorhead, G., Douglas, P., Morrice, N., Scarabel, M., Aitken, A. & 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.
7. Kaiser, W.M. & 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.
8. Sasaki, A., Okuo, K., Yosimura, T., Sekino, N., Sato, T., Ogura, N. & Nakagawa, H. (1995) More of action of inactivator protein from spinach leaves of nitrate reductase. Physiol. Mol. Biol. Plants 1, 121-128.
9. Yamagishi, K., Sato, T., Ogura, N. & Nakagawa, H. (1988) Isolation and some properties of a 115-kilodalton nitrate reductase-inactivator protein from Spinacea oleracea. Plant Cell Physiol. 29, 371-376.
10. Yoshimura, T., Sekino, N., Okuo, K., Sato, T., Ogura, N. & Nakagawa, H. (1992) A nitrate reductase inactivator protein from spinach. Purification, molecular weight and subunit composition. Plant Cell Physiol. 33, 363-369.
11. Sonoda, M., Ide, H., Nakayama, S., Sato, T. & Nakagawa, H. (2000) Cloning and expression analysis of nitrate reductase inactivator (NRI) gene from spinach. Plant Cell Physiol. 41, s160.
12. Kaiser, W.M., Weiner, H., Kandlbinder, A., Tsai, C.B., Rockel, P., Sonoda, M. & Planchet, E. (2002) Modulation of nitrate reductase: some new insights, an unusual case and a potentially important side reaction. J. Exp Bot. 370, 875-882.
13. Moorhead, G., Douglas, P., Cotelle, V., Harthill, J., Morrice, N., Meek, S., Deiting, U., Stitt, M., Scarabel, M., Aitken, A. & MacKintosh, C. (1999) Phosphorylation-dependent interactions between enzymes of plant metabolism and 14-3-3 proteins. Plant J. 18, 1-12.
14. Pozuelo Rubio, M., MacKintosh, C., Galván, A. & Fernández, E. (2001) Cytosolic glutamine synthetase and not nitrate reductase from the green alga Chlamydomonas reinhartii is phosphorylated and binds 14-3-3 protein. Planta 212, 264-269.
15. Finnemann, J. & Schjoerring, J.K. (2000) Post-translational regulation of cytosolic glutamine synthetase by reversible phosphorylation and 14-3-3 protein interaction. Plant J. 24, 171-178.
16. Riedel, J., Tischner, R. & Mack, G. (2001) The chloroplastic glutamine synthetase (GS-2) of tobacco is phosphorylated and associated with 14-3-3 proteins inside the chloroplast. Planta 213, 396-401.
17. Stasiewicz, S. & Dunham, V.L. (1979) Isolation and characterization of two forms of glutamine synthetsae from soybean hypocotyl. Biochem. Biophys. Res. Commun. 87, 627-634.
18. Lea, P.J., Blackwell, R.D., Chen, F.L. & Hecht, U. (1990) Enzymes of ammonium assimilation. In Methods in Plant Biochemistry (Dey, P.M. & Harborne, J.B., eds), pp. 257-276. Academic Press, London, UK.
19. Frick, D.N. & Bessman, M.J. (1995) Cloning, purification, and properties of a novel NADH pyrophosphatase. Evidence for a nucleotide pyrophosphatase catalytic domain in MutT-like enzymes. J. Biol. Chem. 270, 1529-1534.
20. Medda, R., Padiglia, A., Lorrai, A., Murgia, B., Agro, A.F., Castagnola, M. & Floris, G. (2000) Purification and properties of a nucleotide pyrophosphatase from lentil seedlings. J. Protein. Chem. 19, 209-214.
21. Bessman, M.J., Frick, D.N. & O'Handley, S.F. (1996) The MutT proteins or 'Nudix' hydrolases, a family of versatile, widely distributed, 'housecleaning' enzymes. J. Biol. Chem. 271, 25059-25062.
22. Conyers, G.B. & Bessman, M.J. (1999) The gene, ialA, associated with the invasion of human erythrocytes by Bartonella bacilliformis, designates a nudix hydrolase active on dinucleoside 5'-polyphosphates. J. Biol. Chem. 274, 1203-1206.
23. McLennan, A.G. (1999) The MutT motif family of nucleotide phosphohydrolases in man and human pathogens. Int. J. Mol Med. 4, 79-89.
24. Safrany, S.T., Ingram, S.W., Cartwright, J.L., Falck, J.R., McLennan, A.G., Barnes, L.D. & Shears, S.B. (1999) The diadenosine hexaphosphate hydrolases from Schizosaccharomyces pombe and Saccharomyces cerevisiae are homologues of the human diphosphoinositol polyphosphate phosphohydrolase. Overlapping substrate specificities in a MutT-type protein. J. Biol. Chem. 274, 21735-21740.
25. Gijsbers, R., Ceulemans, H., Stalmans, W. & Bollen, M. (2001) Structural and catalytic similarities between nucleotide pyrophosphatases/phosphodiesterases and alkaline phosphatases. J. Biol. Chem. 276, 1361-1368.
26. Seethalakshmi, S. & Rao, N.A. (1979) Regulation of the activity of mung bean (Phaseolus aureus) glutamine synthetase by amino acids and nucleotides. Arch. Biochem. Biophys. 196, 588-597.
27. Stefan, C., Wera, S., Stalmans, W. & Bollen, M. (1996) The inhibition of the insulin receptor by the receptor protein PC-1 is not specific and results from the hydrolysis of ATP. Diabetes 45, 980-983.
28. Yamaya, T. & Ohira, K. (1977) Purification and properties of a nitrate reductase inactivating factor from rice cells in suspension culture. Plant Cell Physiol. 18, 915-925.
29. Sorger, G.J. Premakumar, R. & Gooden, D. (1978) Demonstration in vitro of two intracellular inactivators of nitrate reductase from Neurospora. Biochim. Biophys. Acta 540, 33-47.
30. Leong, C.C. & Shen, T.C. (1980) Nitrate reductase inhibitor of rice plants. Biochim. Biophys. Acta 612, 245-252.
31. Gallardo, F. & Canovas, F.M. (1992) A macromolecular inhibitor of glutamine-synthetase activity in tomato root extracts. Phytochem. 31, 2267-2271.
32. Athwal, G.S., Huber, J.L. & Huber, S.C. (1998) 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. Plant Physiol. 118, 1041-1048.
33. Huber, S.C. & Huber, J.L. (1995) Metabolic effects of spinach leaf nitrate reductase: effects on enzymatic activity and dephosphorylation by endogenous phosphatases. Planta 196, 180-189.
34. Gasmi, L., Cartwright, J.L. & McLennan, A.G. (1999) Cloning, expression and characterization of YSA1H, a human adenosine 5′-diphosphosugar pyrophosphatase possessing a MutT motif. Bioehem. J. 344, 331-337.
35. Douglas, P., Pigaglio, E., Ferrer, A., Halfords, N.G. & MacKintosh, C. (1997) Three spinach leaf nitrate reductase-3-hydroxy-3-methylglutaryl-CoA reductase kinases that are required by reversible phosphorylation and/or Ca2+ ions. Biochem. J. 325, 101-109.
36. Lillo, C., Kazazaic, S., Ruoff, P. & Meyer, C. (1997) Characterization of nitrate reductase from light- and dark-exposed leaves (comparison of different species and effects of 14-3-3 inhibitor proteins). Plant Physiol. 114, 1377-1383.