Chromophore attachment in phycocyanin: Functional amino acids of phycocyanobilin - α-phycocyanin lyase and evidence for chromophore binding

FEBS Journal

Volumn 273, Issue 6, 2006, Pages 1262-1274

  Zhao, Kai Hong ^a   Wu, Dong ^a   Zhang, Ling ^a   Zhou, Ming ^a   Böhm, Stephan ^b   Bubenzer, Claudia ^b   Scheer, Hugo ^b  

^a HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^b UNIVERSITY OF MUNICH   (Germany)

Author keywords

Biliproteins; Biosynthesis; Cyanobacteria; Photosynthesis; Post translational modification

Indexed keywords

ALPHA PHYCOCYANIN LYASE; AMINO ACID; ARGININE; HETERODIMER; ISOPROTEIN; LYASE; NICKEL; PHYCOCYANIN; PHYCOCYANIN C; PHYCOCYANOBILIN; TRYPTOPHAN; UNCLASSIFIED DRUG; ZINC;

AFFINITY CHROMATOGRAPHY; ALPHA CHAIN; AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; BINDING AFFINITY; CARBOXY TERMINAL SEQUENCE; CATALYSIS; CATALYST; CHEMICAL MODIFICATION; CHROMATOPHORE; CONTROLLED STUDY; CORRELATION ANALYSIS; COVALENT BOND; CYANOBACTERIUM; ENZYME ACTIVITY; ENZYME MECHANISM; FLUORESCENCE; MASTIGOCLADUS LAMINOSUS; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN MOTIF;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; AMINO ACIDS; ANIMALS; CYANOBACTERIA; LYASES; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; MUTATION; PHYCOBILINS; PHYCOBILISOMES; PHYCOCYANIN; PIGMENTS, BIOLOGICAL; PROTEIN BINDING; PROTEIN PROCESSING, POST-TRANSLATIONAL; TETRAPYRROLES;

CYANOBACTERIA; MASTIGOCLADUS LAMINOSUS;

EID: 33644755865     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2006.05149.x     Document Type: Article

References (51)

1. Grossman AR Schaefer MR Chiang GG Collier JL 1993 The phycobilisome, a light-harvesting complex responsive to environmental conditions Microbiol Rev 57 725 749
2. Glazer AN 1994 Adaptive variations in phycobilisome structure Adv Mol Cell Biol 10 119 149
3. Sidler WA 1994 Phycobilisome and phycobiliprotein structures. In The Molecular Biology of Cyanobacteria Bryant DA, ed.), pp. 139 216 Kluwer Dordrecht
4. Glazer AN 1985 Light harvesting by phycobilisomes Ann Rev Biophys Biophys Chem 14 47 77
5. Frank G Sidler W Widmer H Zuber H 1978 The complete amino-acid sequence of both subunits of C-phycocyanin from the cyanobacterium Mastigocladus laminosus Hoppe-Seyler's Z Physiol Chem 359 1491 1507
6. Schirmer T Bode W Huber R Sidler W Zuber H 1985 X-Ray crystallographic structure of the light-harvesting biliprotein C-phycocyanin from the thermophilic cyanobacterium Mastigocladus laminosus and its resemblance to globin structures J Mol Biol 184 257 277
7. Beale SI 1994 Biosynthesis of cyanobacterial tetrapyrrole pigments: Hemes, chlorophylls and phycobilins. In The Molecular Biology of Cyanobacteria Bryant DA, ed.), pp. 519 558 Kluwer Dordrecht
8. Schluchter WM Glazer AN 1999 Biosynthesis of Phycobiliproteins in Cyanobacteria. In The Phototrophic Prokaryotes Peschek GA Löffelhardt W Schmetterer G, eds), pp. 83 95 Kluwer/Plenum Press New York
9. Zhao K-H Deng M-G Zheng M Zhou M Parbel A Storf M Meyer M Strohmann B Scheer H 2000 Novel activity of a phycobiliprotein lyase: both the attachment of phycocyanobilin and the isomerization to phycoviolobilin are catalyzed by PecE and PecF FEBS Lett 469 9 13
10. Shen G Saunee NA Gallo E Begovic Z Schluchter WM Bryant DA 2004 Identification of novel phycobiliprotein lyases in cyanobacteria. In PS 2004 light-Harvesting Systems Workshop, book of abstracts. p. 14
11. Wu S-H Lagarias JC 2000 Defining the bilin lyase domain: lessons from the extended phytochrome superfamily Biochemistry 39 13487 13495
12. Hughes J Lamparter T Mittmann F Hartmann E 1997 A prokaryotic phytochrome Nature 386 663
13. Zhao K-H Ran Y Li M Sun Y-N Zhou M Storf M Kupka M Böhm S Bubenzer C Scheer H 2004 Photochromic biliproteins from the cyanobacterium Anabaena sp. PCC 7120: lyase activities, chromophore exchange and photochromism in phytochrome and phycoerythrocyanin Biochemistry 43 11576 11588
14. cm, by autocatalytic chromophore binding to ApcE Biochim Biophys Acta 1706 81 87
15. Robben U Lindner I Gärtner W Schaffner K 2001 Analyse der Topologie der Chromophor-Bindungstasche von Phytochrom durch Variation des Chlromophor-Substitutionsmuster Angew Chemie 113 1080 1082
16. Arciero DM Bryant DA Glazer AN 1988 In vitro attachment of bilins to apophycocyanin. 1. Specific covalent adduct formation at cysteinyl residues involved in phycocyanobilin binding in C-phycocyanin J Biol Chem 263 18343 18349
17. Zhao KH Zhu JP Song B Zhou M Storf M Böhm S Bubenzer C Scheer H 2004 Non-enzymatic chromophore attachment in biliproteins: Conformational control by the detergent Triton X-100 Biochim Biophys Acta 1657 131 145
18. 1-Cys-α84-phycoviolobilin chromophore of phycoerythrocyanin Biochemistry 40 12444 12456
19. Swanson RV Zhou J Leary JA Williams T de Lorimier R Bryant DA Glazer AN 1992 Characterization of phycocyanin produced by cpcE and cpcF mutants and identification of an intergenic suppressor of the defect in bilin attachment J Biol Chem 267 16146 16154
20. Zhou J Gasparich GE Stirewalt VL de Lorimier R Bryant DA 1992 The cpcE and cpcF genes of Synechococcus sp. PCC 7002. Construction and phenotypic characterization of interposon mutants J Biol Chem 267 16138 16145
21. Kahn K Mazel D Houmard J Tandeau de Marsac N Schaefer MR 1997 A role for cpeYZ in cyanobacterial phycoerythrin biosynthesis J Bacteriol 179 998 1006
22. Six C Thomas J-C Thion L Lemoine Y Zal F Partensky F 2005 Characterization of two novel phycoerythrin-associated linker proteins in the marine cyanobacterium Synechococcus sp. WH8102 J Bacteriol 187 1685 1694
23. Fairchild CD Zhao J Zhou J Colson SE Bryant DA Glazer AN 1992 Phycocyanin α-subunit phycocyanobilin lyase Proc Natl Acad Sci USA 89 7017 7021
24. Tooley AJ Cai YA Glazer AN 2001 Biosynthesis of a fluorescent cyanobacterial C-phycocyanin holo-alpha. subunit in a heterologous host Proc Natl Acad Sci USA 98 10560 10565
25. Bhalerao RP Gustafsson P 1994 Factors Influencing the Phycobilisome Rod Composition of the Cyanobacterium Synechococcus sp. PCC7942 - effects of reduced phycocyanin content, lack of rod-linkers, and over-expression of the rod-terminating linker Physiol Plant 90 187 197
26. Tandeau de Marsac N Mazel D Damerval T Guglielmi G Capuano V Houmard J 1988 Photoregulation of gene expression in the filamentous cyanobacterium Calothrix sp. PCC 7601: light-harvesting complexes and cell differentiation Photosynth Res 18 99 132
27. Fairchild CD Glazer AN 1994 Oligomeric structure, enzyme kinetics, and substrate specificity of the phycocyanin alpha subunit phycocyanobilin lyase J Biol Chem 269 8686 8694
28. Zhao KH Wu D Zhou M Zhang L Böhm S Bubenzer C Scheer H 2005 Amino acid residues associated with enzymatic activity of the isomerizing phycoviolobilin-lyase PecE/F Biochemistry 44 8126 8137
29. Scheer H 1982 Phycobiliproteinsq6 : Molecular aspects of photosynthetic antenna systems. In Light Reaction Path of Photosynthesis Fong FK, ed.), pp. 7 45 Springer Berlin
30. Braslavsky SE Holzwarth AR Schaffner K 1983 Solution conformations, photophysics, and photochemistry of bili-pigments - bilirubin and biliverdin dimethylesters and related linear tetrapyrroles Angew Chem Int Ed Engl 22 656 674
31. Berkelman T Lagarias JC 1986 Visualization of bilin-linked peptides and proteins in polyacrylamide gels Anal Biochem 156 194 201
32. Suckau D Mak M Przybylski M 1992 Protein surface topology-probing by selective chemical modification and mass spectrometric peptide mapping Proc Natl Acad Sci USA 89 5630 5634
33. Bazaes S Goldie H Cardemil E Jabalquinto AM 1995 Identification of reactive lysines in phosphoenolpyruvate carboxykinases from Escherichia coli and Saccharomyces cerevisiae FEBS Lett 360 207 210
34. Hoare DG Koshland JDE 1967 A method for the quantitative modification and estimation of carboxylic acid group in proteins J Biol Chem 242 2447 2453
35. Spande TF Witkop B 1967 Determination of the tryptophan content of proteins with N-bromosuccinimide Methods Enzymol 11 498 506
36. Tsou CL 1962 Relation between modification of functional groups of proteins and their biological activity. 1. A graphical method for the determination of the number and type of essential groups Sci Sin 11 1535 1558
37. Miles EW 1977 Modification of histidyl residues in proteins by diethylpyrocarbonate Methods Enzymol 47 431 442
38. Lundblad RL 1991 Chemical Reagents for Protein Modification 2nd edn CRC Press Boca Raton
39. Kaneko T Sato S Kotani H Tanaka A Asamizu E Nakamura Y Miyajima N Hirosawa M Sugiura M Sasamoto S et al. 1996 Sequence analysis of the genome of the unicellular cyanobacterium Synechocystis sp. strain PCC6803. II. Sequence determination of the entire genome and assignment of potential protein-coding regions DNA Res 3 109 136
40. Kaneko T Nakamura Y Wolk CP Kuritz T Sasamoto S Watanabe A Iriguchi M Ishikawa A Kawashima K Kimura T et al. 2001 Complete genomic sequence of the filamentous nitrogen-fixing cyanobacterium Anabaena sp. strain PCC 7120 DNA Res 8 205 213
41. Nakamura Y Kaneko T Sato S Ikeuchi M Katoh H Sasamoto S Watanabe A Iriguchi M Kawashima K Kimura T et al. 2002 Complete genome structure of the thermophilic cyanobacterium Thermosynechococcus elongatus BP-1 DNA Res 9 123 130
42. Schluchter WM Bryant DA 2002 Analysis and reconstitution of phycobiliproteins: methods for the characterization of bilin attachment reactions. In Heme, Chlorophyll, and Bilins Smith AG Witty M, eds), pp. 311 334 Humana Press Totowa, NJ, USA
43. Adir N Vainer R Lerner N 2002 Refined structure of c-phycocyanin from the cyanobacterium Synechococcus vulcanus at 1.6 A: insights into the role of solvent molecules in thermal stability and co-factor structure Biochim Biophys Acta 1556 168 174
44. Kneip C Parbel A Förstendorf H Scheer H Siebert F Hildebrandt P 1998 FT-NIR-resonance raman spectroscopic study of the α-subunit of phycoerythrocyanin and phycocyanin from the cyanobacterium Mastigocladus laminosus J Raman Spectr 29 939 944
45. Beuhler RJ Pierce RC Friedman L 1976 Reversible addition 3-äthyliden mit R-SH J Biol Chem 251 2405 2411
46. Sambrook J Fritsch EF Maniatis T 1989 Molecular Cloning: a Laboratory Manual 2nd edn Cold Spring. Harbour Laboratory Press New York
47. Zhao K-H Wu D Wang L Zhou M Storf M Bubenzer C Strohmann B Scheer H 2002 Characterization of phycoviolobilin phycoerythrocyanin-α84-cystein-lyase- (isomerizing) from Mastigocladus laminosus Eur J Biochem 269 4542 4550
48. Laemmli UK 1970 Cleavage of structural proteins during the assembly of the head of bacteriopharge T4 Nature 227 680 685
49. Bradford MM 1976 A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding Anal Biochem 72 248 254
50. Levy HM Leber PD Ryan EM 1963 Inactivation of myosin by 2,4-dinitrophenol and protection by adenosine triphosphatase and other phosphate compounds J Biol Chem 238 3654 3659
51. Horowitz P Criscimagna NL 1982 The specificity of active-site alkylation by iodoacetic acid in the enzyme thiosulfate sulfurtransferase Biochim Biophys Acta 702 173 177