Characterization of Arabidopsis thaliana Stellacyanin: A Comparison with Umecyanin

Proteins: Structure, Function and Genetics

Volumn 55, Issue 2, 2004, Pages 426-435

  Harrison, Mark D ^a   Dennison, Christopher ^a  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

Author keywords

Alkaline transition; Copper proteins; Cupredoxin; Paramagnetic NMR; Phytocyanin

Indexed keywords

COPPER; COPPER PROTEIN; CUPREDOXIN; PHYTOCYANIN; STELLACYANINE; UMECYANIN; UNCLASSIFIED DRUG; VEGETABLE PROTEIN;

ARABIDOPSIS; ARTICLE; BINDING SITE; CELL INCLUSION; ELECTRON SPIN RESONANCE; HORSERADISH; IN VITRO STUDY; OXIDATION REDUCTION REACTION; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN PURIFICATION; PROTON NUCLEAR MAGNETIC RESONANCE; SPECTROSCOPY; ULTRAVIOLET SPECTROSCOPY;

AMINO ACID SEQUENCE; ARABIDOPSIS; BINDING SITES; COPPER; ELECTROCHEMISTRY; ELECTRON SPIN RESONANCE SPECTROSCOPY; GENE EXPRESSION; MAGNETIC RESONANCE SPECTROSCOPY; METALLOPROTEINS; MOLECULAR SEQUENCE DATA; PLANT PROTEINS; PROTEIN FOLDING; PROTEIN RENATURATION;

ARABIDOPSIS; ARABIDOPSIS THALIANA; ARMORACIA RUSTICANA; TRACHEOPHYTA;

EID: 1842584506     PISSN: 08873585     EISSN: None     Source Type: Journal    
DOI: 10.1002/prot.20017     Document Type: Article

References (73)

1. Nersissian AM, Shipp EL. Blue copper-binding domains. Adv Prot Chem 2002;60:271-340.
2. Colman PM, Freeman HC, Guss JM, Murata M, Norris VA, Ramshaw JAM, Venkatappa MP. X-ray crystal structure analysis of plastocyanin at 2.7 Å resolution. Nature 1978;272:319-324.
3. Guss JM, Freeman HC. Structure of oxidized poplar plastocyanin at 1.6 Å resolution. J Mol Biol 1983;169:521-563.
4. Petratos K, Banner DW, Beppu T, Wilson KS, Tsernoglou D. The crystal structure of pseudoazurin from Alcaligenes faecalis S-6 determined at 2.9 Å resolution. FEBS Lett 1987;218:209-214.
5. Baker EN. Structure of azurin from Alcaligenes denitrificans refinement at 1.8 Å resolution and comparison of the 2 crystallographically independent molecules. J Mol Biol 1988;203:1071-1095.
6. Romero A, Nar H, Huber R, Messerschmidt A, Kalverda AP, Canters GW, Durley R, Mathews FS. Crystal-structure analysis and refinement at 2.15 angstrom resolution of amicyanin, a type-I blue copper protein, from Thiobacillus versutus. J Mol Biol 1994;236:1196-1211.
7. Hart PJ, Nersissian AM, Herrmann RG, Nalbandyan RM, Valentine JS, Eisenberg D. A missing link in cupredoxins: crystal structure of cucumber stellacyanin at 1.6 Å resolution. Protein Sci 1996;5:2175-2183.
8. Guss JM, Merritt EA, Phizackerley RP, Freeman HC. The structure of a phytocyanin, the basic blue protein from cucumber, refined at 1.8 Å resolution. J Mol Biol 1996;262:686-705.
9. Walter RL, Ealick SE, Friedman AM, Blake RC, Proctor P, Shoham M. Multiple wavelength anomalous diffraction (MAD) crystal structure of rusticyanin: a highly oxidizing cupredoxin with extreme acid stability. J Mol Biol 1996;263:730-751.
10. Bond CS, Blankenship RE, Freeman HC, Guss JM, Maher MJ, Selvaraj FM, Wilce MCJ, Willingham KM. Crystal structure of auracyanin, a "blue" copper protein from the green thermophilic photosynthetic bacterium Chloroflexus aurantiacus. J Mol Biol 2001;306:47-67.
11. Malmström BG. Rack-induced bonding in blue-copper proteins. Eur J Biochem 1994;223:711-718.
12. Williams RJP. Energized (entatic) states of groups and of secondary structures in proteins and metalloproteins. Eur J Biochem 1995;234:363-381.
13. Solomon EI, Penfield KW, Gewirth AA, Lowery MD, Shadle SE, Guckert JA, LaCroix LB. Electronic structure of the oxidized and reduced blue copper sites: contributions to the electron transfer pathway, reduction potential, and geometry. Inorg Chim Acta 1996;243:67-78.
14. Andrew CR, Yeo MH, Valentine JS, Karlsson BG, Bonander N, Van Pouderoyen G, Canters GW, Loehr TM, Sanders-Loehr J. Raman spectroscopy as an indicator of Cu-S bond-length in type-1 and type-2 copper cysteinate proteins. J Am Chem Soc 1994; 116: 11489-11498.
15. LaCroix LB, Shadle SE, Wang Y, Averill BA, Hedman B, Hodgson KO, Solomon EI. Electronic structure of the perturbed blue copper site in nitrite reductase: spectroscopic properties, bonding, and implications for the entatic/rack state. J Am Chem Soc 1996;118: 7755-7768.
16. Nersissian AM, Immoos C, Hill MG, Hart PJ, Williams G, Herrmann RG, Valentine JS. Uclacyanins, stellacyanins, and plantacyanins are distinct subfamilies of phytocyanins: plant-specific mononuclear blue copper proteins. Protein Sci 1998;7:1915-1929.
17. Dennison C, Harrison MD, Lawler AT. Alkaline transition of phytocyanins: a comparison of stellacyanin and umecyanin. Biochem J 2003;371:377-383.
18. Van Gysel A, Van Montagu M, Inzé D. A negatively light-regulated gene from Arabidopsis thaliana encodes a protein showing high similarity to blue copper-binding proteins. Gene 1993;136:79-85.
19. Borner GHH, Sherrier DJ, Stevens TJ, Arkin IT, Dupree P. Prediction of glycosylphosphatidylinositol-anchored proteins in Arabidopsis: a genomic analysis. Plant Physiol 2002;129:486-499.
20. Paul KG, Stigbrand T. Umecyanin, a novel intensely blue copper protein from horseradish root. Biochim Biophys Acta 1970;221: 255-263.
21. Stigbrand T, Malmström BG, Vänngård T. On the state of copper in the blue protein umecyanin. FEBS Lett 1971;12:260-262.
22. Dennison C, Lawler AT. Investigations of the alkaline and acid transitions of umecyanin, a stellacyanin from horseradish roots. Biochemistry 2001;40:3158-3166.
23. Thompson JD, Higgins DG, Gibson TJ. Clustal-W - improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 1994;22:4673-4680.
24. Van Driessche G, Dennison C, Sykes AG, Van Beeumen J. Heterogeneity of the covalent structure of the blue copper protein umecyanin from horseradish roots. Protein Sci 1995;4:209-227.
25. Mann K, Schäfer W, Thoenes U, Messerschmidt A, Mehrabian Z, Nalbandyan R. The amino-acid sequence of a type-I copper protein with an unusual serine-rich and hydroxyproline-rich C-terminal domain isolated from cucumber peelings. FEBS Lett 1992;314:220-223.
26. Bergman C, Gandvik E-A, Nyman PO, Strid L. The amino acid sequence of stellacyanin from the lacquer tree. Biochem Biophys Res Comm 1977;77:1052-1059.
27. Schininà ME, Maritano S, Barra D, Mondovi B, Marchesini A. Mavicyanin, a stellacyanin-like protein from zucchini peelings: primary structure and comparison with other cupredoxins. Biochim Biophys Acta 1996;1297:28-32.
28. Peisach J, Levine WG, Blumberg WE. Structural properties of stellacyanin, a copper mucoprotein from Rhus vernicifera, the Japanese lac tree. J Biol Chem 1967;242:2847-2858.
29. Marchesini A, Minelli M, Merkle H, Kroneck PM. Mavicyanin, a blue copper protein from Cucurbita pepo medullosa: purification and characterization. Eur J Biochem 1979;101:77-84.
30. Nersissian AM, Mehrabian ZB, Nalbandyan RM, Hart PJ, Fraczkiewicz G, Czernuszewicz RS, Bender CJ, Peisach J, Herrmann RG, Valentine JS. Cloning, expression, and spectroscopic characterization of Cucumis sativus stellacyanin in its nonglycosylated form. Protein Sci 1996;5:2184-2192.
31. Borner GHH, Lilley KS, Stevens TJ, Dupree P. Identification of glycosylphosphatidylinositol-anchored proteins in Arabidopsis: a proteomic and genomic analysis. Plant Physiol 2003;132:568-577
32. Kakutami T, Watanabe H, Arima K, Beppu T. A blue protein as an inactivating factor for nitrite reductase from Alcaligenes faecalis strain S-6. J Biochem 1981;89:463-472.
33. Liu MY, Liu MC, Payne WJ, Legall J. Properties and electron-transfer specificity of copper proteins from the denitrifier Achromobacter cycloclastes. J Bacteriol 1986;166:604-608.
34. 1-type nitrite reductase from, and the absence of a copper-type nitrite reductase from, the aerobic denitrifier Thiosphaera pantotropha - the role of pseudoazurin as an electron-donor. Eur J Biochem 1993;212:377-385.
35. Van Spanning RJM, Wansell CW, Reijnders WNM, Oltmann LF, Stouthamer AH. Mutagenesis of the gene encoding amicyanin of Paracoccus denitrificans and the resultant effect on methylamine oxidation. FEBS Lett 1990;275:217-220.
36. Barber J. Photosynthetic electron-transport in relation to thylakoid membrane-composition and organization. Plant Cell Environ 1983;6:311-322.
37. Haehnel W. Photosynthetic electron-transport in higher-plants. Annu Rev Plant Physiol 1984;35:659-693.
38. Messerschmidt A. Blue copper oxidases. Adv Inorg Chem 1993;40: 121-185.
39. Solomon EI, Sundaram UM, Machonkin TE. Multicopper oxidases and oxygenases. Chem Rev 1996;96:2563-2605.
40. Casimiro DR, Toy-Palmer A, Blake RC, Dyson HJ. Gene synthesis, high-level expression and mutagenesis of Thiobacillus ferrooxidans rusticyanin: His 85 is a ligand to the blue copper center. Biochemistry 1995;34:6640-6648.
41. Wada KN, Aota SI, Tsuchiya R, Ishibashi F, Gojobori T, Ikemura T. Codon usage tabulated from the GenBank genetic sequence data. Nucl Acids Res 1990;18:2367-2411.
42. Inubushi T, Becker ED. Efficient detection of paramagnetically shifted NMR resonances by optimizing the WEFT pulse sequence. J Magn Reson 1983;51:128-133.
43. Bertini I, Ciurli S, Dikiy A, Gasanov R, Luchinat C, Martini G, Safarov N. High-field NMR studies of oxidized blue copper proteins: the case of spinach plastocyanin. J Am Chem Soc 1999;121: 2037-2046.
44. De Kerpel JOA, Pierloot K, Ryde U, Roos BO. Theoretical study of the structural and spectroscopic properties of stellacyanin. J Phys Chem B 1998;102:4638-4647.
45. LaCroix LB, Randall DW, Nersissian AM, Hoitink CWG, Canters GW, Valentine JS, Solomon EI. Spectroscopic and geometric variations in perturbed blue copper centers: electronic structures of stellacyanin and cucumber basic protein. J Am Chem Soc 1998;120:9621-9631.
46. 1H NMR spectroscopy. Biochemistry 1996;35:3085-3092.
47. Dennison C, Oda K, Kohzuma T. Paramagnetic NMR studies of copper-containing nitrite reductases. Chem Commun 2000;9:751-752.
48. Sato K, Dennison C. Effect of histidine 6 protonation on the active site structure and electron-transfer capabilities of pseudoazurin from Achromobacter cycloclastes. Biochemistry 2002;41:120-130.
49. Sato K, Kohzuma T, Dennison C. Active-site structure and electron-transfer reactivity of plastocyanins. J Am Chem Soc 2003;125:2101-2112.
50. Bertini I, Fernandez CO, Karlsson BG, Leckner J, Luchinat C, Malmström BG, Nersissian AM, Pierattelli R, Shipp E, Valentine JS, Vila AJ. Structural information through NMR hyperfine shifts in blue copper proteins. J Am Chem Soc 2000;122:3701-3707.
51. Cunsolo V, Foti S, LaRosa C, Saletti R, Canters GW, Verbeet MP. Free energy for blue copper protein unfolding determined by electrospray ionisation mass spectrometry. Rapid Commun Mass Spectrom 2001;15:1817-1825.
52. Malmström BG, Reinhammar B, Vänngård T. The state of copper in stellacyanin and laccase from the lacquer tree Rhus vernicifera. Biochim Biophys Acta 1970;205:48-57.
53. Romero A, Hoitink CWG, Nar H, Huber R, Messerschmidt A, Canters GW. X-ray analysis and spectroscopic characterization of M121Q azurin - a copper site model for stellacyanin. J Mol Biol 1993;229:1007-1021.
54. Diederix REM, Canters GW, Dennison C. The Met99Gln mutant of amicyanin from Paracoccus versutus. Biochemistry 2000;39: 9551-9560.
55. Gewirth AA, Cohen SL, Schugar HJ, Solomon EI. Spectroscopic and theoretical studies of the unusual EPR parameters of distorted tetrahedral cupric sites: correlations to X-ray spectral features of core levels. Inorg Chem 1987;26:1133-1146.
56. Dennison C, Harrison MD. The active site structure of umecyanin, the stellacyanin from horseradish roots. J Am Chem Soc. In press.
57. Battistuzzi G, Borsari M, Loschi L, Righi F, Sola M. Redox thermodynamics of blue copper proteins. J Am Chem Soc 1999;121: 501-506.
58. Olsson MHM, Ryde U. The influence of axial ligands on the reduction potential of blue copper proteins. J Biol Inorg Chem 1999;4:654-663.
59. Olsson MHM, Hong G, Warshel A. Frozen density functional free energy simulations of redox proteins: computational studies of the reduction potential of plastocyanin and rusticyanin. J Am Chem Soc 2003;125:5025-5039.
60. Chang S, Puryear JD, Dilip L, Dias MA, Funkhouser EA, Newton RJ, Cainrey J. Gene expression under water deficit in loblolly pine (Pinus taeda): isolation and characterization of cDNA clones. Physiol Plantarum 1996;97:139-148.
61. Yoshizaki M, Furumoto T, Hata S, Shinozaki M, Izui K. Characterization of a novel gene encoding a phytocyanin-related protein in morning glory (Pharbitis nil). Biochem Biophys Res Comm 2000; 268:466-470.
62. Zhang Y, Sederoff RR, Allona I. Differential expression of genes encoding cell wall proteins in vascular tissues from vertical and bent loblolly pine trees. Tree Physiol 2000;20:457-466.
63. Romo S, Labrador E, Dopico B. Water stress-regulated gene expression in Cicer arietinum seedlings and plants. Plant Physiol Biochem 2001;39:1017-1026.
64. Connors BJ, Miller M, Maynard CA, Powell WA. Cloning and characterization of promoters from American chestnut capable of directing reporter gene expression in transgenic Arabidopsis plants. Plant Sci 2002;163:771-781.
65. Fedorova M, Van de Mortel J, Matsumoto PA, Cho J, Town CD, Van den Bosch KA, Gantt JS, Vance CP. Genome-wide identification of nodule-specific transcripts in the model legume Medicago truncatula. Plant Physiol 2002;130:519-537.
66. Kong HY, Jung HW, Lee SC, Choi D, Hwang BK. A gene encoding stellacyanin is induced in Capsicum annuum by pathogens, methyl jasmonate, abscisic acid, wounding, drought and salt stress. Physiol Plantarum 2002;115:550-562.
67. Seki M, Narusaka M, Ishida J, Nanjo T, Fujita M, Oono Y, Kamiya A, Nakajima M, Enju A, Sakurai T, Satou M, Akiyama K, Taji T, Yamaguchi-Shinozaki K, Carnicini P, Kawai J, Hayashizaki Y, Shinozaki K. Monitoring the expression profiles of 7000 Arabidopsis genes under drought, cold and high-salinity stresses using a full-length cDNA microarray. Plant J 2002;31:279-292.
68. Richards KD, Schott EJ, Sharma YK, Davis KR, Gardner RC. Aluminum induces oxidative stress genes in Arabidopsis thaliana. Plant Physiol 1998;116:409-418.
69. Rossel JB, Wilson IW, Pogson BJ. Global changes in gene expression in response to high light in Arabidopsis. Plant Physiol 2002;130:1109-1120.
70. Yang KY, Im YJ, Chung GC, Cho BH. Activity of the Arabidopsis blue copper-binding protein gene promoter in transgenic tobacco plants upon wounding. Plant Cell Rep 2002;20:987-991.
71. Lohman KN, Gan SS, John MC, Amasino RM. Molecular analysis of natural leaf senescence in Arabidopsis thaliana. Physiol Plantarum 1994;92:322-328.
72. Weaver LM, Gan SS, Quirino B, Amasino RM. A comparison of the expression patterns of several senescence-associated genes in response to stress and hormone treatment. Plant Mol Biol 1998;37: 455-469.
73. Miller JD, Arteca RN, Pell EJ. Senescence-associated gene expression during ozone-induced leaf senescence in Arabidopsis. Plant Physiol 1999;120:1015-1023.