Predicting redox-sensitive cysteines in plant enzymes by homology modeling

Comptes Rendus de l'Academie des Sciences - Serie III

Volumn 320, Issue 10, 1997, Pages 767-781

  Anderson, Louise E ^a   Li, Dong ^a   Muslin, Elizabeth H ^a   Stevens, Fred J ^b   Schiffer, Marianne ^b  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^b ARGONNE NATIONAL LABORATORY   (United States)

Author keywords

Domain locking disulfides; Light activation; Light inactivation; Oxidative inactivation; Redox sensitive cysteines; Reductive activation

Indexed keywords

CYSTEINE; DISULFIDE; ENZYME; FRUCTOSE BISPHOSPHATASE; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; MALATE DEHYDROGENASE; PHOSPHATASE; THIOREDOXIN; VEGETABLE PROTEIN;

ALLOSTERISM; BINDING SITE; BIOTECHNOLOGY; CHLOROPLAST; ENZYME ACTIVATION; ENZYME ACTIVE SITE; ENZYME CONFORMATION; ENZYME MECHANISM; GERMINATION; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATION REDUCTION REACTION; PHOTOACTIVATION; PROTEIN DOMAIN; REVIEW; SEQUENCE HOMOLOGY; SITE DIRECTED MUTAGENESIS;

VIRIDIPLANTAE;

EID: 0031259562     PISSN: 07644469     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0764-4469(97)85012-3     Document Type: Article

References (82)

1. Li D., Stevens F.J., Schiffer M., Anderson L.E. Mechanism of light modulation: Identification of potential redox-sensitive cysteines distal to catalytic site in light-activated chloroplast enzymes. Biophys. J. 67:1994;29-35.
2. Villeret V., Huang S.H., Zhang Y.P., Xue Y.F., Lipscomb W.N. Crystal structure of spinach chloroplast fructose-1,6-bisphosphatase at 2.8 Å resolution. Biochemistry. 34:1995;4299-4306.
3. Jacquot J.-P., Lopez-Jaramillo J., Chueca A., Cherfils J., Lemaire S., Chedozeau B., Miginiac-Maslow M., Decottignies P., Wolosiuk R., Lopez-Gorge J. High-level expression of recombinant pea chloroplast fructose-1,6-bisphosphatase and mutagenesis of its regulatory site. Eur. J. Biochem. 229:1995;675-681.
4. Jacquot J.-P., Lopez-Jaramillo J., Miginiac-Maslow M., Lemaire S., Cherfils J., Chueca A., Lopez-Gorge J. Cysteine-153 is required for redox regulation of pea chloroplast fructose-1,6-bisphosphatase. FEBS Lett. 401:1997;143-147.
5. Rodriguez-Suarez R.J., Mora-García S., Wolosiuk R.A. Characterization of cysteine residues involved in the reductive activation and the structural stability of rapeseed (Brassica napus) chloroplast fructose-1,6-bisphosphatase. Biochem. Biophys. Res. Commun. 232:1997;388-393.
6. Muslin E.H., Li D., Stevens F.J., Donnelly M., Schiffer M., Anderson L.E. Engineering a domain-locking disulfide into a bacterial malate dehydrogenase produces a redox-sensitive enzyme. Biophys. J. 68:1995;2218-2223.
7. Muslin E.H. An investigation into the redox-sensitivity of two plant dehydrogenases. Thesis. 1997;University of Illinois, Chicago.
8. Hilbert M., Böhm G., Jaenicke R. Structural relationships of homologous proteins as a fundamental principle of homology modeling. Proteins. 17:1993;138-151.
9. May A.C.W., Johnson M.S., Rufino S.D., Ako H., Zhu Z.Y., Sowdhamini R., Srinivasan N., Rodionov M.A., Blundell T.L. The recognition of protein structure and function from sequence: adding value to genome data. Phil. Trans. Royal Soc. London, Ser. B. 344:1994;373-381.
10. Johnson M.S., Srinivasan N., Sowdhamini R., Blundell T.L. Knowledge-based protein modeling. Critical Rev. Biochem. Mol. Biol. 29:1994;1-68.
11. Taylor W.L. Remotely related sequences and structures: analysis and predictive modelling. Trends Biotechnol. 12:1994;154-158.
12. Šali A. Modelling mutations and homologous proteins. Curr. Opin. Biotech. 6:1995;437-451.
13. Eisenhaber F., Persson B., Argos P. Protein structure prediction: recognition of primary, secondary, and tertiary structural features from amino acid sequence. Crit. Rev. Biochem. Mol. Biol. 30:1995;1-94.
14. Moult J. The current state of the art in protein structure prediction. Curr. Opin. Biotechnol. 7:1996;422-427.
15. Jones D.T. Progress in protein structure prediction. Curr. Opin. Struc. Biol. 7:1997;377-387.
16. Ziegler H., Ziegler I. Der Einfluss der Belichtung auf die NADP+-abhängige Glyceraldehyd-3-Phosphat-Dehydrogenase. Planta. 65:1965;369-380.
17. Buchanan B.B. Role of light in the regulation of chloroplast enzymes. Ann. Rev. Plant Physiol. 288:1980;1-9.
18. Anderson L.E. Light/dark modulation of enzyme activity in plants. Callow J.A. Advances in Botanical Research. 12:1986;1-46 Academic Press, New York.
19. 2 assimilation in oxygenic photosynthesis. Arch. Biochem. Biophys. 288:1991;1-9.
20. Schelbe R. Redox-modulation of chloroplast enzymes. A common principle for individual control. Plant Physiol. 96:1991;1-3.
21. Salamon Z., Tollin G., Hirasawa H., Gardet-Salvi L., Stritt-Etter A.L., Knaff D.B., Schürmann P. The oxidation-reduction properties of spinach thioredoxins f and m and of ferredoxin:thioredoxin reductase. Biochim. Biophys. Acta. 1230:1995;114-118.
22. Chow L.-P., Iwadate H., Yano K., Kamo M., Tsugita A., Gardet-Salvi L., Stritt-Etter A.-L., Schrürmann P. Amino acid sequence of spinach ferredoxin:thioredoxin reductase catalytic subunit and identification of thiol groups constituting a redox-active disulfide and a (4Fe-4S) cluster. Eur. J. Biochem. 231:1995;149-156.
23. Brandes H.K., Larimer F.W., Geck M.K., Stringer C.D., Schümann P. Direct identification of the primary nucleophile of thioredoxin f. J. Biol. Chem. 268:1993;18411-18414.
24. Geck M.K., Larimer F.W., Hartman F.C. Identification of residues of spinach thioredoxin f that influence interactions with target enzymes. J. Biol. Chem. 217:1996;24736-24740.
25. Scheibe R., Anderson L.E. Dark moduation of NADP-dependent malate dehydrogenase and glucose-6-phosphate dehydrogenase in the chloroplast. Biochim. Biophys. Acta. 636:1981;58-64.
26. m in pea chloroplasts: Concentration and redox state under light and dark conditions. FEBS Lett. 133:1981;301-304.
27. Soulié J.-M., Buc J., Meunier J.-C., Pradel J., Ricard J. Molecular properties of chloroplastic thioredoxin f and the photoregulation of the activity of fructose 1,6-bisphosphatase. Eur. J. Biochem. 119:1981;497-502.
28. Meunier J.C., Gontero B., Ferte N., Buc J. Some aspects of activation and inactivation of several chloroplastic enzymes (fructose-1,6-bisphosphatase), sedoheptulose-1,7-bisphosphatase, NADP-malate dehydrogenase) in relation with their molecular properties. Scheibe R. Light-Dark Modulation of Plant Enzyme Activity. 1983;60-68 University of Bayreuth, Bayreuth.
29. Schürmann P. The ferreodixin-thioredoxin system in activation and deactivation of chloroplast enzymes. Scheibe R. Light-Dark Modulation of Plant Enzyme Activity. 1983;11-18 University of Bayreuth, Bayreuth.
30. Schürmann P., Kobayashi Y. Regulation of chloroplast fructose 1,6-bisphosphatase activity by the ferredoxin-thioredoxin system. Sybesma C. Advances in Photosynthesis Research. 3:1984;629-632 Martinus Nijhoff/Dr. W. Junk, The Hague.
31. Gontero B., Meunier J.-C., Buc J. Efficient purification of spinach chloroplastic sedoheptulose 1,7-bisphosphatase (SBPase). Kinetic comparison with fructuose 1,6-bisphosphatase (FBPase). Sybesma C. Advances in Photosynthesis Research. 1984;505-508 Martinus Nijhoff/Dr. W. Junk, The Hague.
32. Li A.D., Stevens F.J., Huppe H.C., Kersanach R., Anderson L.E. Chlamydomonas reinhardtii NADP-linked glyceraldehyde-3-phosphate dehydrogenase contains the same Cys residues identified as potentially domain-locking in the higher plant enzyme and is light activated. Photosyn. Res. 51:1997;167-177.
33. Anderson L.E., Huppe H.C., Li D., Stevens F.J. Identification of a potential redox-sensitive inter-domain disulfide in the sedoheptulose bisphosphatase of Chlamydomonas reinhardtii. Plant J. 10:1996;553-560.
34. Anderson L.E., Gover S., Rowland P., Adams M.J. Mechanism of dark modulation: Activation of cyanobacterial glucose-6-phosphate dehydrogenase by disulfide bond formation. 21st Midwest Photosynthesis Conference, Turkey Run IN. 1995;9. (abstract).
35. Janin J., Wodak S.J. Structural domains in proteins and their role in the dynamics of protein function. Prog. Biophys. Mol. Biol. 42:1983;21-78.
36. Skarzynski T., Wonacott A.J. Coenzyme-induced conformational changes in glyceraldehyde-3-phosphate dehydrogenase from Bacillus stearothermophilus. J. Mol. Biol. 203:1988;1097-1118.
37. Pacold M.E., Anderson L.E., Li D., Stevens F.J. Redox-sensitivity and light modulation of enzyme activity in the rhodophytes Gracilaria tikvahiae and Chondrus crispus. J. Phycol. 31:1995;297-301.
38. Pacold M.E., Stevens F.J., Li D., Anderson L.E. The NADP-linked glyceraldehyde-3-phosphate dehydrogenase of Anabaena variabilis and Synechocystis PCC 6803 which lack one of the cysteines found in the higher plant enzyme are not reductively activated. Photosyn. Res. 43:1995;125-130.
39. Tamol M., Ishikawa T., Takeda T., Shigeoka S. Enzymic and molecular characterization of NADP-dependent glyceraldehyde-phosphate-3 dehydrogenase from Synechococcus PCC 7942: resistance of the enzyme to hydrogen peroxide. Biochem. J. 316:1996;685-690.
40. Li D., Anderson L.E. Expression and characterization of pea chloroplastic glyceraldehyde-3-phosphate dehydrogenase composed of only subunit B. Plant Physiol. 1997;. (in press).
41. Birktoft J.J., Rhodes G., Banaszak L.J. Refined crystal structure of cytoplasmic malate dehydrogenase at 2.5 Å resolution. Biochemistry. 28:1989;6065-6081.
42. a values in proteins of the thioredoxin family. J. Mol. Biol. 253:1995;799-812.
43. Sowdhamini R., Srinivasan N., Shoichet B., Santi D.V., Ramakrishnan C., Balaram P. Stereochemical modeling of disulfide bridges. Criteria for introduction into proteins by site-directed mutagenesis. Protein Eng. 3:1989;95-103.
44. Lemaire M., Issakidis E., Ruelland E., Decottignies P., Miginiac-Maslow M. An active-site cysteine of sorghum leaf NADP-malate dehydrogenase studied by site-directed mutagensis. FEBS Lett. 382:1996;137-140.
45. Hatch M.D., Agostino A. Bilevel disulfide group reduction in the activation of C4 leaf nicotinamide adenine dinucleotide phosphate-malate dehydrogenase. Plant Physiol. 100:1992;360-366.
46. Decottignies P., Schmitter J.M., Miginiac-Maslow M., Le Maréchal P., Jacquot J.-P., Gadal P. Primary structure of the light-dependent regulatory site of corn NADP-malate dehydrogenase. J. Biol. Chem. 263:1988;11780-11785.
47. Issakidis E., Miginiac-Maslow M., Decottignies P., Jacquot J.-P., Crétin C., Gadal P. Site-directed mutagenesis reveals the involvement of an additional thioredoxin-dependent regulatory site in the activation of recombinant sorghum leaf NADP-malate dehydrogenase. J. Biol. Chem. 267:1992;21577-21583.
48. Issakidis E., Decottignies P., Miginiac-Maslow M. A thioredoxin-independent fully active NADP-malate dehydrogenase obtained by site-directed mutagenesis. FEBS Lett. 321:1993;55-58.
49. Issakidis E., Saarinien M., Decottignies P., Jacquot J.-P., Crétin C., Gadal P., Miginiac-Maslow M. Identification and characterization of the second regulatory disulfide bridge of recombinant sorghum leaf NADP-malate dehydrogenase. J. Biol. Chem. 269:1994;3511-3517.
50. Reng W., Riessland R., Scheibe R., Jaenicke R. Cloning, site-specific mutagensis, expression and characterization of full-length chloroplast NADP-malate dehydrogenase from Pisum sativum. Eur. J. Biochem. 217:1993;189-197.
51. Scheibe R., Kampfenkel K., Wessels R., Tripier D. Primary structure and analysis of the location of the regulatory disulfide bond of pea chloroplast NADP-malate dehydrogenase. Biochim. Biophys. Acta. 1076:1991;1-8.
52. Ke H., Thorpe C.M., Seaton B.A., Lipscomb W.N., Marcus F. Structure refinement of fructose-1,6-bisphosphatase and its fructose 2,6-bisphosphate complex at 2.8 Å resolution. J. Mol. Biol. 212:1989;513-539.
53. Zhang Y., Liang J.-Y., Huang S., Ke H., Lipscomb W.N. Crystallographic studies of the catalytic mechanism of the neutral form of fructose-1,6-bisphosphatase. Biochemistry. 32:1993;1844-1857.
54. Ke H., Liang J.Y., Zhang Y., Lipscomb W.N. Conformational transition of fructose-1,6-bisphosphatase - structure comparison between the AMP complex (T-form) and the fructose-1,6-phoshate complex (R-form). Biochemistry. 30:1991;4412-4420.
55. Zhang Y., Liang J.-Y., Huang S., Lipscomb W.N. Toward a mechanism for the allosteric transition of pig kidney fructose-1,6-bisphosphatase. J. Mol. Biol. 244:1994;609-624.
56. Raines C.A., Lloyd J.C., Willingham N.M., Potts S., Dyer T.A. cDNA and gene sequences of wheat chloroplast sedoheptulose-1,7-bisphosphatase reveal homology with fructose-1,6-bisphosphatases. Eur. J. Biochem. 205:1992;1053-1059.
57. Martin W., Mustafa A.-Z., Henze K., Schnarrenberger C. Higher-plant chloroplast and cytosolic fructose-1,6-bisphosphatase isozymes: origins via duplication rather than prokaryote-eukaryote divergence. Plant Mol. Biol. 32:1996;485-491.
58. Willingham N.M., Lloyd J.C., Raines C.A. Molecular cloning of the Arabidopsis thaliana sedoheptulose-1,7-bisphosphatase gene and expression studies in wheat and Arabidopsis thaliana. Plant Mol. Biol. 26:1994;1191-1200.
59. Hahn D., Kueck U. Nucleotide sequence of a cDNA encoding the chloroplast sedoheptulose-1,7-bisphosphatase from Chlamydomonas reinhardtii. Plant Physiol. 104:1994;1101-1102.
60. Rowland P., Basak A.K., Gover S., Levy H.R., Adams M.J. The three-dimensional structure of glucose-6-phosphate dehydrogenase from Leuconostoc mesenteroides refined at 2.0 Å resolution. Structure. 2:1994;1073-1087.
61. Scanlan D.J., Sundaram S., Newman J., Mann N.H., Carr N.G. Characterization of a zwf mutant of Synechococcus sp. strain PCC 7942. J. Bacteriol. 177:1995;2550-2553.
62. Summers M.L., Wallis J.G., Campbell E.L., Meeks J.C. Genetic evidence of a major role for glucose-6-phosphate dehydrogenase in nitrogen fixation and dark growth of the cyanobacterium Nostoc sp. strain ATCC 29133. J. Bacteriol. 177:1995;6184-6194.
63. von Schaewen A., Langenkämper G., Graeve K., Wenderoth I., Scheibe R. Molecular characterization of the plastidic glucose-6-phosphate dehydrogenase from potato in comparison to its cytosolic counterpart. Plant Physiol. 109:1995;1327-1335.
64. Johnson T.C., Wada K., Buchanan B.B., Holmgren A. Reduction of purothionin by the wheat seed thioredoxin system and potential function as a secondary thiol messenger in redox control. Plant Physiol. 85:1987;446-451.
65. Kobrehel K., Yee B.C., Buchanan B.B. Role of the NADP/thioredoxin system in the reduction of a-amylase and trypsin inhibitor proteins. J. Biol. Chem. 266:1991;16135-16140.
66. Kobrehel K., Wong J.H., Balogh A., Kiss F., Yee B.C., Buchanan B.B. Specific reduction of wheat storage proteins by thioredoxin h. Plant Physiol. 99:1992;919-924.
67. Kiss F., Wu M.X., Wong J.H., Balogh A., Buchanan B.B. Redox active sulfhydryls are required for fructose 2,6-bisphosphatase activation of plant pyrophosphate fructose-6-phosphate 1-phosphotransferase. Arch. Biochem. Biophys. 287:1991;337-340.
68. Jiao J.-A., Yee B.C., Wong J.H., Kobrehel K., Buchanan B.B. Thioredoxin-linked changes in regulatory properties of barley alpha-amylase subtilisin inhibitor protein. Plant Physiol. Biochem. 31:1993;799-804.
69. Shin S.H., Wong J.H., Kobrehel K., Buchanan B.B. Reduction of castor-seed 2S albumin protein by thioredoxin. Planta. 189:1993;557-560.
70. Besse I., Wong J.H., Kobrehel K., Buchanan B.B. Thiocalsin: a thioredoxin-linked, substrate-specific protease dependent on calcium. Proc. Nat. Acad. Sci. (USA). 93:1996;3169-3175.
71. Florencio F.J., Gadal P., Buchanan B.B. Thioredoxin-linked activation of the chloroplast and cytosolic forms of Chlamydomonos reinhardtii glutamine synthetase. Plant Physiol. Biochem. 31:1993;649-655.
72. Umbach A.L., Siedow J.N. Covalent and noncovalent dimers of the cyanide-resistant alternative oxidase protein in higher plant mitochondria and their relationship to enzyme activity. Plant Physiol. 103:1993;845-854.
73. Anderson L.E., Li D., Prakash N., Stevens F.J. Identification of potential redox-sensitive cysteines in cytosolic forms of fructosebisphosphatase and glyceraldehyde-3-phosphate dehydrogenase. Planta. 196:1995;118-124.
74. Anderson L.E., Li A.D., Nehrlich S.C., Hill M.H., Stevens F.J. The cytosolic fructose bisphosphatase of Brassica napus contains a new potential regulatory disulfide and is redox-sensitive. Plant Sci. 128:1997;23-30.
75. Dale J. Cytosolic fructose-1,6-bisphosphatase: A key enzyme in the sucrose biosynthetic pathway. Photosynt Res. 38:1993;5-14.
76. Anderson L.E., Li A.D., Stevens F.J. The enolases of ice plant and Arabidopsis contain a potential disulfide and are redox-sensitive. Phytochemistry. 1997;. (in press).
77. Stevens F.J., Li A.D., Lateef S.S., Anderson L.E. Identification of potential inter-domain disulfides in three higher plant mitochondrial citrate synthases: paradoxical differences in redox-sensitivity as compared with the animal enzyme. Photosyn. Res. 1997;. (in press).
78. Qin J., Clore G.M., Kennedy W.P., Huth J.R., Gronenborn A.M. Solution structure of human thioredoxin in a mixed disulfide intermediate complex with its target peptide from the transcription factor NFκB. Structure. 3:1995;289-297.
79. Qin J., Clore G.M., Kennedy W.P., Kuszewski J., Gronenborn A.M. The solution structure of human thioredoxin complexed with its target from Ref-1 reveals peptide chain reversal. Structure. 4:1996;613-620.
80. Crétin C., Luchetta P., Joly C., Decottigenies P., Lepiniec L., Gadal P., Sallantin M., Huet J.-C., Pernollet J.C. Primary structure of sorghum malate dehydrogenase (NADP) deduced from cDNA sequence. Homology with malate dehydrogenase (NAD). Eur. J. Biochem. 192:1990;299-303.
81. Hall M.D., Levitt D.G., Banaszak L.J. Crystal structure of Escherichia coli malate dehydrogenase: a complex of the apoenzyme and citrate at 1.87 Å resolution. J. Mol. Biol. 226:1992;867-882.
82. Kossmann J., Müller-Röber B., Dyer T.A., Raines C.A. Cloning and expression analysis of the plastidic fructose-1,6-bisphosphatase coding sequence from potato: circumstantial evidence for the import of hexoses into chloroplasts. Planta. 188:1992;7-12.