Mapping of a copper-binding site on the small CP12 chloroplastic protein of Chlamydomonas reinhardtii using top-down mass spectrometry and site-directed mutagenesis

Biochemical Journal

Volumn 419, Issue 1, 2009, Pages 75-82

  Erales, Jenny ^a   Gontero, Brigitte ^a   Whitelegge, Julian ^b   Halgand, Frédéric ^b,c  

^a AIX MARSEILLE UNIVERSITÉ   (France)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c CNRS   (France)

Author keywords

Calvin cycle; Chlamydomonas reinhardtii chloroplastic protein CP12; Copper binding site; Redox transition; Sitedirected mutagenesis; Top down mass spectrometry (top down MS)

Indexed keywords

CALVIN CYCLE; CHLAMYDOMONAS REINHARDTII CHLOROPLASTIC PROTEIN CP12; COPPER-BINDING SITE; REDOX TRANSITION; SITEDIRECTED MUTAGENESIS; TOP-DOWN MASS SPECTROMETRY (TOP-DOWN MS);

BINDING ENERGY; COPPER; COPPER COMPOUNDS; ELECTROSPRAY IONIZATION; EXPERIMENTS; MASS SPECTROMETERS; MASS SPECTROMETRY; METAL IONS; MUTAGENESIS; SPECTRUM ANALYSIS;

BINDING SITES;

ASPARAGINE; ASPARTIC ACID; CELL PROTEIN; COPPER ION; GLUTAMIC ACID; GLUTAMINE; LYSINE; METAL ION; MUTANT PROTEIN; PROTEIN CP12; UNCLASSIFIED DRUG; COPPER; CP12 PROTEIN, PLANT; VEGETABLE PROTEIN;

ARTICLE; BINDING SITE; CHLAMYDOMONAS REINHARDTII; CHLOROPLAST; COMPLEX FORMATION; CONTROLLED STUDY; ELECTROSPRAY MASS SPECTROMETRY; EXPERIMENTAL DESIGN; GENE MAPPING; IMMOBILIZED METAL AFFINITY CHROMATOGRAPHY; MUTATIONAL ANALYSIS; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; SITE DIRECTED MUTAGENESIS; TANDEM MASS SPECTROMETRY; WILD TYPE; ANIMAL; CHEMISTRY; CIRCULAR DICHROISM; GENETICS; IMMUNOBLOTTING; MASS SPECTROMETRY; METABOLISM; MUTATION; PHOTOSYNTHESIS; PHYSIOLOGY; PROTEIN SECONDARY STRUCTURE;

CHLAMYDOMONAS REINHARDTII;

ANIMALS; BINDING SITES; CHLAMYDOMONAS REINHARDTII; CHLOROPLASTS; CIRCULAR DICHROISM; COPPER; IMMUNOBLOTTING; MASS SPECTROMETRY; MUTAGENESIS, SITE-DIRECTED; MUTATION; PHOTOSYNTHESIS; PLANT PROTEINS; PROTEIN STRUCTURE, SECONDARY; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION; TANDEM MASS SPECTROMETRY;

EID: 62749115182     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20082004     Document Type: Article

References (50)

1. Wedel, N., Soll, J. and Paap, B. K. (1997) CP12 provides a new mode of light regulation of Calvin cycle activity in higher plants. Proc. Natl. Acad. Sci. U.S.A. 94, 10479-10484
2. Wedel, N. and Soll, J. (1998) Evolutionary conserved light regulation of Calvin cycle activity by NADPH-mediated reversible phosphoribulokinase/ CP12/glyceraldehyde3- phosphate dehydrogenase complex dissociation. Proc. Natl. Acad. Sci. U.S.A. 95, 9699-9704
3. Oesterhelt, C., Klocke, S., Holtgrefe, S., Linke, V., Weber, A. P. and Scheibe, R. (2007) Redox regulation of chloroplast enzymes in Galdieria sulphuraria in view of eukaryotic evolution. Plant Cell. Physiol. 48, 1359-1373
4. Boggetto, N., Gontero, B. and Maberly, S. C. (2007) Regulation of phosphoribulokinase and glyceraldehyde 3-phosphate dehydrogenase in a freshwater diatom, Asterionella formosa (Bacillariophyceae). J. Phycol. 43, 1227-1234
5. Erales, J., Maberly, S and Gontero, B. (2008) Specificity and function of glyceraldehyde 3-phosphate dehydrogenase in a freshwater diatom, Asterionella formosa (Bacillariophyceae). J. Phycol. 44, 1455-1464
6. Pohlmeyer, K., Paap, B. K., Soll, J. and Wedel, N. (1996) CP12: a small nuclear-encoded chloroplast protein provides novel insights into higher-plant GAPDH evolution. Plant Mol. Biol. 32, 969-978
7. Tamoi, M., Miyazaki, T., Fukamizo, T. and Shigeoka, S. (2005) The Calvin cycle in cyanobacteria is regulated by CP12 via the NAD(H)/NADP(H) ratio under light/dark conditions. Plant J. 42, 504-513
8. Lebreton, S., Andreescu, S., Graciet, E. and Gontero, B. (2006) Mapping of the interaction site of CP12 with glyceraldehyde-3-phosphate dehydrogenase from Chlamydomonas reinhardtii. Functional consequences for glyceraldehyde-3-phosphate dehydrogenase. FEBS J. 273, 3358-3369
9. 2 assimilation. Eur. J. Biochem. 271, 4737-4744
10. Graciet, E., Lebreton, S. and Gontero, B. (2004) Emergence of new regulatory mechanisms in the Benson-Calvin pathway via protein-protein interactions: a glyceraldehyde-3-phosphate dehydrogenase/CP12/ phosphoribulokinase complex. J. Exp. Bot. 55, 1245-1254
11. Graciet, E., Gans, P., Wedel, N., Lebreton, S., Camadro, J. M. and Gontero, B. (2003) The small protein CP12: a protein linker for supramolecular assembly. Biochemistry 42, 8163-8170
12. Graciet, E., Lebreton, S., Camadro, J. M. and Gontero, B. (2003) Characterization of native and recombinant A4 glyceraldehyde 3-phosphate dehydrogenase. Kinetic evidence for confromation changes upon association with the small protein CP12. Eur. J. Biochem. 270, 129-136
13. Marri, L., Trost, P., Pupillo, P. and Sparla, F. (2005) Reconstitution and properties of the recombinant glyceraldehyde-3-phosphate dehydrogenase/CP12/phosphoribulokinase supramolecular complex of Arabidopsis. Plant Physiol. 139, 1433-1443
14. Marri, L., Trost, P., Trivelli, X., Gonnelli, L., Pupillo, P. and Sparla, F. (2008) Spontaneous assembly of photosynthetic supramolecular complexes as mediated by the intrinsically unstructured protein CP12. J. Biol. Chem. 283, 1831-1838
15. Uversky, V. N. and Fink, A. L. (2004) Conformational constraints for amyloid fibrillation: the importance of being unfolded. Biochim. Biophys. Acta 1698, 131-153
16. Erales, J., Avilan, L., Lebreton, S. and Gontero, B. (2008) Exploring CP12 binding proteins revealed aldolase as a new partner for the phosphoribulokinase/glyceraldehyde 3-phosphate dehydrogenase/CP12 complex - purification and kinetic characterization of this enzyme from Chlamydomonas reinhardtii. FEBS J. 275, 1248-1259
17. Delobel, A., Graciet, E., Andreescu, S., Gontero, B., Halgand, F. and Laprevote, O. (2005) Mass spectrometric analysis of the interactions between CP12, a chloroplast protein, and metal ions: a possible regulatory role within a PRK/GAPDH/CP12 complex. Rapid Commun. Mass Spectrom. 19, 3379-3388
18. Himelblau, E., Mira, H., Lin, S. J., Culotta, V. C., Penarrubia, L. and Amasino, R. M. (1998) Identification of a functional homolog of the yeast copper homeostasis gene ATX1 from Arabidopsis. Plant Physiol. 117, 1227-1234
19. Mira, H., Martinez-Garcia, F. and Penarrubia, L. (2001) Evidence for the plant-specific intercellular transport of the Arabidopsis copper chaperone CCH. Plant J. 25, 521-528
20. Mira, H., Vilar, M., Perez-Paya, E. and Penarrubia, L. (2001) Functional and conformational properties of the exclusive C-domain from the Arabidopsis copper chaperone (CCH). Biochem. J. 357, 545-549
21. Kelleher, N. L., Lin, H. Y., Valaskovic, G. A., Aaserud, D. J., Fridriksson, E. K. and McLafferty, F. W. (1999) Top down versus bottom up protein characterization by tandem high-resolution MS. J. Am. Chem. Soc. 121, 806-807
22. Forbes, A. J., Patrie, S. M., Taylor, G. K., Kim, Y. B., Jiang, L. and Kelleher, N. L. (2004) Targeted analysis and discovery of posttranslational modifications in proteins from methanogenic archaea by top-down MS. Proc. Natl. Acad. Sci. U.S.A. 101, 2678-2683
23. Deterding, L. J., Bhattacharjee, S., Ramirez, D. C., Mason, R. P. and Tomer, K. B. (2007) Top-down and bottom-up mass spectrometric characterization of human myoglobin-centered free radicals induced by oxidative damage. Anal. Chem. 79, 6236-6248
24. Patrie, S. M., Ferguson, J. T., Robinson, D. E., Whipple, D., Rother, M., Metcalf, W. W. and Kelleher, N. L. (2006) Top down MS of <60-kDa proteins from Methanosarcina acetivorans using quadrupole FRMS with automated octopole collisionally activated dissociation. Mol. Cell. Proteomics 5, 14-25
25. Pesavento, J. J., Garcia, B. A., Streeky, J. A., Kelleher, N. L. and Mizzen, C. A. (2007) Mild performic acid oxidation enhances chromatographic and top down mass spectrometric analyses of histones. Mol. Cell. Proteomics 6, 1510-1526
26. Pisitkun, T., Johnstone, R. and Knepper, M. A. (2006) Discovery of urinary biomarkers. Mol. Cell. Proteomics 5, 1760-1771
27. Whitelegge, J. P., Laganowsky, A., Nishio, J., Souda, P., Zhang, H. and Cramer, W. A. (2006) Sequencing covalent modifications of membrane proteins. J. Exp. Bot. 57, 1515-1522
28. Whitelegge, J., Halgand, F., Souda, P. and Zabrouskov, V. (2006) Top-down MS of integral membrane proteins. Expert. Rev. Proteomics 3, 585-596
29. Zabrouskov, V. and Whitelegge, J. P. (2007) Increased coverage in the transmembrane domain with activated-ion electron capture dissociation for top-down Fourier-transform MS of integral membrane proteins. J. Proteome Res. 6, 2205-2210
30. Geels, R. B., van der Vies, S. M., Heck, A. J. and Heeren, R. M. (2006) Electron capture dissociation as structural probe for noncovalent gas-phase protein assemblies. Anal. Chem. 78, 7191-7196
31. Xie, Y., Zhang, J., Yin, S. and Loo, J. A. (2006) Top-down ESI-ECD-FT-ICR MS localizes noncovalent protein-ligand binding sites. J. Am. Chem. Soc. 128, 14432-14433
32. Savitski, M. M., Nielsen, M. L. and Zubarev, R. A. (2006) ModifiComb, a new proteomic tool for mapping substoichiometric post-translational modifications, finding novel types of modifications, and fingerprinting complex protein mixtures. Mol. Cell. Proteomics 5, 935-948
33. Roth, M. J., Forbes, A. J., Boyne, M. T., 2nd, Kim, Y. B., Robinson, D. E. and Kelleher, N. L. (2005) Precise and parallel characterization of coding polymorphisms, alternative splicing, and modifications in human proteins by MS. Mol. Cell. Proteomics 4, 1002-1008
34. Whitelegge, J. P., Zabrouskov, V., Halgand, F., Souda, P., Bassilian, S., Yan, W., Wolinsky, L., Loo, J. A., Wong, D. T. and Faull, K. F. (2007) Protein-sequence polymorphisms and post-translational modifications in proteins from human saliva using top-down fourier-transform ion cyclotron resonance MS. Int. J. Mass Spectrom. 268, 190-197
35. Graciet, E., Gans, P., Wedel, N., Lebreton, S., Camadro, J. M. and Gontero, B. (2003) The small protein CP12: a protein linker for supramolecular complex assembly. Biochemistry 42, 8163-8170
36. Chen, Y. H., Yang, J. T. and Chau, K. H. (1974) Determination of the helix and β form of proteins in aqueous solution by circular dichroism. Biochemistry 13, 3350-3359
37. Bradford, M. M. (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
38. Loo, J. A. (2000) Electrospray ionization MS: a technology for studying noncovalent macromolecular complexes. Int. J. Mass Spectrom. 200, 175-186
39. Kaltashov, I. A., Zhang, M., Eyles, S. J. and Abzalimov, R. R. (2006) Investigation of structure, dynamics and function of metalloproteins with electrospray ionization MS. Anal. Bioanal. Chem. 386, 472-481
40. 2+) in metalloproteins. J. Inorg. Biochem. 71, 115-127
41. Halgand, F. and Laprevote, O. (2001) Mean charge state and charge state distribution of proteins as structural probes. An electrospray ionisation MS study of lysozyme and ribonuclease A. Eur. J. Mass Spectrom. 7, 433-439
42. Armitage, P. (1971) Statistical Methods In Medical Research, p. 504, Blackwell Scientific Publications, Oxford and Edinburgh
43. Turecek, F. (2007) Copper-biomolecule complexes in the gas phase. The ternary way. Mass Spectrom. Rev. 26, 563-582
44. Gardebien, F., Thangudu, R. R., Gontero, B. and Offmann, B. (2006) Construction of a 3D model of CP12, a protein linker. J. Mol. Graph. Model 25, 186-195
45. Gabelica, V. and De Pauw, E. (2005) Internal energy and fragmentation of ions produced in electrospray sources. Mass Spectrom. Rev. 24, 566-587
46. Howard, T. P., Metodiev, M., Lloyd, J. C. and Raines, C. A. (2008) Thioredoxin-mediated reversible dissociation of a stromal multiprotein complex in response to changes in light availability. Proc. Natl. Acad. Sci. U.S.A. 105, 4056-4061
47. Millhauser, G. L. (2007) Copper and the prion protein: methods, structures, function, and disease. Annu. Rev. Phys. Chem. 58, 299-320
48. Zheng, R., Jenkins, T. M. and Craigie, R. (1996) Zinc folds the N-terminal domain of HIV-1 integrase, promotes multimerization, and enhances catalytic activity. Proc. Natl. Acad. Sci. U.S.A. 93, 13659-13664
49. Uversky, V. N., Li, J. and Fink, A. L. (2001) Metal-triggered structural transformations, aggregation, and fibrillation of human α-synuclein. A possible molecular link between Parkinson's disease and heavy metal exposure. J. Biol. Chem. 276, 44284-44296
50. Roepstorff, P. and Fohlman, J. (1984) Proposal for a common nomenclature for sequence ions in mass spectra of peptides. Biomed. Mass. Spectrom. 11, 601