Conformational selection and folding-upon-binding of intrinsically disordered protein CP12 regulate photosynthetic enzymes assembly

Journal of Biological Chemistry

Volumn 287, Issue 25, 2012, Pages 21372-21383

  Fermani, Simona ^a   Trivelli, Xavier ^b,c   Sparla, Francesca ^a   Thumiger, Anton ^a   Calvaresi, Matteo ^a   Marri, Lucia ^a   Falini, Giuseppe ^a   Zerbetto, Francesco ^a   Trost, Paolo ^a  

^a UNIVERSITY OF BOLOGNA   (Italy)

^b UNIV LILLE   (France)

^c UNIVERSITÉ DES SCIENCES ET TECHNOLOGIES DE LILLE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVE SITE; BINARY COMPLEXES; C-TERMINAL TAIL; CARBON ASSIMILATION; CONFORMATIONAL SELECTION; DISORDERED PROTEINS; DISULFIDE BRIDGE; GLYCERALDEHYDE-3-PHOSPHATE DEHYDROGENASE; INTERACTION MECHANISMS; PHOSPHORIBULOKINASE; PHOTOSYNTHETIC ENZYMES; RE-OXIDATION; REDOX SWITCH; STRUCTURAL MOTIFS; SUPRAMOLECULAR COMPLEXES; TERNARY COMPLEX;

CARBON; COVALENT BONDS; HYDROGEN BONDS;

PROTEINS;

GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; PROTEIN CP12; REGULATOR PROTEIN; UNCLASSIFIED DRUG;

ALPHA HELIX; AMINO TERMINAL SEQUENCE; ARABIDOPSIS; ARTICLE; BETA TURN; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CRYSTAL STRUCTURE; CRYSTALLIZATION; ENZYME ACTIVE SITE; HYDROGEN BOND; MOLECULAR DYNAMICS; NONHUMAN; PHOTOSYNTHESIS; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN PROTEIN INTERACTION; PROTEIN SECONDARY STRUCTURE; SYNECHOCOCCUS;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CARRIER PROTEINS; DISULFIDES; ENZYME STABILITY; GLYCERALDEHYDE-3-PHOSPHATE DEHYDROGENASE (NADP+)(PHOSPHORYLATING); MULTIENZYME COMPLEXES; PHOSPHOTRANSFERASES (ALCOHOL GROUP ACCEPTOR); PHOTOSYNTHESIS; PROTEIN FOLDING;

EID: 84862274751     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.350355     Document Type: Article

References (55)

1. Buchanan, B. B., and Balmer, Y. (2005) Redox regulation. A broadening horizon. Annu. Rev. Plant Biol. 56, 187-220
2. Dai, S., Friemann, R., Glauser, D. A., Bourquin, F., Manieri, W., Schürmann, P., and Eklund, H. (2007) Structural snapshots along the reaction pathway of ferredoxin-thioredoxin reductase. Nature 448, 92-96 (Pubitemid 47037004)
3. Trost, P., Fermani, S., Marri, L., Zaffagnini, M., Falini, G., Scagliarini, S., Pupillo, P., and Sparla, F. (2006) Thioredoxin-dependent regulation of photosynthetic glyceraldehyde-3-phosphate dehydrogenase. Autonomous vs. CP12-dependent mechanisms. Photosynth. Res. 89, 263-275
4. Wedel, N., and Soll, J. (1998) Evolutionary conserved light regulation of Calvin cycle activity by NAPDH-mediated reversible phosphoribulokinase/CP12/ glyceraldehyde-3-phosphate-dehydrogenase complex dissociation. Proc. Natl. Acad. Sci. U.S.A. 95, 9699-9704
5. Scheibe, R., Wedel, N., Vetter, S., Emmerlich, V., and Sauermann, S. M. (2002) Co-existence of two regulatory NADP-glyceraldehyde 3-phosphate dehydrogenase complexes in higher plant chloroplasts. Eur. J. Biochem. 269, 5617-5624 (Pubitemid 35365550)
6. 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 (Pubitemid 36858977)
7. Tamoi, M., Miyazaki, T., Fukamizo, T., and Shigeoka, S. (2005) The Calvin cycle in cyanobacteria is regulated by CP12 via NAD(H)/NADP(H) ratio under light/dark conditions. Plant J. 42, 504-513 (Pubitemid 40722146)
8. Marri, L., Pesaresi, A., Valerio, C., Lamba, D., Pupillo, P., Trost, P., and Sparla, F. (2010) In vitro characterization of Arabidopsis CP12 isoforms reveals common biochemical and molecular properties. J. Plant Physiol. 167, 939-950
9. Howard, T. P., Lloyd, J. C., and Raines, C. A. (2011) Interspecies variation in the oligomeric states of the higher plant Calvin cycle enzymes glyceraldehyde-3-phosphate dehydrogenase and phosphoribulokinase. J. Exp. Bot. 62, 3799-3805
10. Marri, L., Zaffagnini, M., Collin, V., Issakidis-Bourguet, E., Lemaire, S. D., Pupillo, P., Sparla, F., Miginiac-Maslow, M., and Trost, P. (2009) Prompt and easy activation by specific thioredoxins of Calvin cycle enzymes of Arabidopsis thaliana associated in the GAPDH-CP12/PRK supramolecular complex. Mol. Plant 2, 259-269
11. Fermani, S., Sparla, F., Falini, G., Martelli, P. L., Casadio, R., Pupillo, P., Ripamonti, A., and Trost, P. (2007) Molecular mechanism of thioredoxin regulation in photosynthetic A2B2-glyceraldehyde-3-phosphate dehydrogenase. Proc. Natl. Acad. Sci. U.S.A. 104, 11109-11114 (Pubitemid 47175234)
12. 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 (Pubitemid 43786843)
13. 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 (Pubitemid 351723523)
14. Howard, T. P., Fryer, M. J., Singh, P., Metodiev, M., Lytovchenko, A., Obata, T., Fernie, A. R., Kruger, N. J., Quick, W. P., Lloyd, J. C., and Raines, C. A. (2011) Antisense suppression of the small chloroplast protein CP12 in tobacco alters carbon partitioning and severely restricts growth. Plant Physiol. 157, 620-631
15. Thompson, L. R., Zeng, Q., Kelly, L., Huang, K. H., Singer, A. U., Stubbe, J., and Chisholm, S. W. (2011) Phage auxiliary metabolic genes and the redirection of cyanobacterial host carbon metabolism. Proc. Natl. Acad. Sci. U.S.A. 108, E757-E764
16. Matsumura, H., Kai, A., Maeda, T., Tamoi, M., Satoh, A., Tamura, H., Hirose, M., Ogawa, T., Kizu, N., Wadano, A., Inoue, T., and Shigeoka, S. (2011) Structure basis for the regulation of glyceraldehyde-3-phosphate dehydrogenase activity via the intrinsically disordered protein CP12. Structure 19, 1846-1854
17. 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
18. 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 (Pubitemid 43990938)
19. Ward, J. J., Sodhi, J. S., McGuffin, L. J., Buxton, B. F., and Jones, D. T. (2004) Prediction and functional analysis of native disorder in proteins from the three kingdoms of life. J. Mol. Biol. 26, 635-645 (Pubitemid 38326883)
20. Sun, X., Jones, W. T., Harvey, D., Edwards, P. J., Pascal, S. M., Kirk, C., Considine, T., Sheerin, D. J., Rakonjac, J., Oldfield, C. J., Xue, B., Dunker, A. K., and Uversky, V. N. (2010) N-terminal domains of DELLA proteins are intrinsically unstructured in the absence of interaction with GID1/gibberellic acid receptors. J. Biol. Chem. 285, 11557-11571
21. Cortese, M. S., Uversky, V. N., and Dunker, A. K. (2008) Intrinsic disorder in scaffold proteins. Getting more from less. Prog. Biophys. Mol. Biol. 98, 85-106
22. Tompa, P., and Fuxreiter, M. (2008) Fuzzy complexes. Polymorphism and structural disorder in protein-protein interactions. Trends Biochem. Sci. 33, 2-8
23. Wright, P. E., and Dyson, H. J. (2009) Linking folding and binding, Curr. Opin. Struct. Biol. 19, 31-38
24. Espinoza-Fonseca L. M. (2009) Reconciling binding mechanisms of intrinsically disordered proteins. Biochem. Biophys. Res. Commun. 382, 479-482
25. Boehr, D. D., Nussinov, R., and Wright, P. E. (2009) The role of dynamic conformational ensembles in biomolecular recognition. Nat. Chem. Biol. 5, 789-796
26. Dyson, H. J., and Wright, P. E. (2005) Intrinsically unstructured proteins and their functions, Nat. Rev. Mol. Cell Biol. 6, 197-208 (Pubitemid 40314921)
27. Kjaergaard, M., Teilum, K., and Poulsen, F. M. (2010) Conformational selection in the molten globule state of the nuclear coactivator binding domain of CBP. Proc. Natl. Acad. Sci. U.S.A. 107, 12535-12540
28. Sugase, K., Dyson, H. J., and Wright P. E. (2007) Mechanism of coupled folding and binding of an intrinsically disordered protein. Nature 447, 1021-1025 (Pubitemid 46975749)
29. Wang, T., Darwin, K. H., and Li, H. (2010) Binding-induced folding of prokaryotic ubiquitin-like protein on the Mycobacterium proteasomal ATPase targets substrates for degradation. Nat. Struct. Mol. Biol. 17, 1352-1357
30. Lee, C. W., Martinez-Yamout, M. A., Dyson, H. J., and Wright, P. E. (2010) Structure of the p53 transactivation domain in complex with the nuclear receptor coactivator binding domain of CREB-binding protein. Biochemistry 49, 9964-9971
31. Mohan, A., Oldfield, C. J., Radivojac, P., Vacic, V., Cortese, M. S., Dunker, A. K., and Uversky, V. N. (2006) Analysis of molecular recognition features (MoRFs), J. Mol. Biol. 362, 1043-1059 (Pubitemid 44353519)
32. Fuxreiter, M., Simon, I., Friedrich, P., and Tompa, P. (2004) Preformed structural elements feature in partner recognition by intrinsically unstructured proteins. J. Mol. Biol. 338, 1015-1026 (Pubitemid 38542830)
33. Fermani, S., Sparla, F., Marri, L., Thumiger, A., Pupillo, P., Falini, G., and Trost, P. (2010) The crystal structure of photosynthetic glyceraldehyde- 3-phosphate dehydrogenase (isoform A4) from Arabidopsis thaliana in complex with NAD. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 66, 621-626
34. Leslie, A. G. W. (1992) Recent changes to the MOSFLM package for processing film and image plate data. Joint CCP4 + ESF-EAMCB Newsletter on Protein Crystallography 26, 27-33
35. Evans, P. (2006) Scaling and assessment of data quality. Acta Crystallogr.D Biol. Crystallogr. 62, 72-82
36. Otwinowsky, Z., and Minor, W. (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326
37. Navaza, J. (1994) AMoRe. An automated package for molecular replacement. Acta Crystallogr. A 50, 157-163
38. Vagin, A. A., Steiner, R. A., Lebedev, A. A., Potterton, L., McNicholas, S., Long, F., and Murshudov, G. N. (2004) REFMAC5 dictionary: organization of prior chemical knowledge and guidelines for its use. Acta Crystallogr. D Biol. Crystallogr. 60, 2184-2195 (Pubitemid 41742770)
39. Brünger, A. T., Adams, P. D., Clore, G. M., DeLano, W. L., Gros, P., Grosse-Kunstleve, R. W., Jiang, J. S., Kuszewski, J., Nilges, M., Pannu, N. S., Read, R. J., Rice, L. M., Simonson, T., and Warren, G. L. (1998) Crystallography and NMR system (CNS). A new software system for macromolecular structure determination. Acta Crystallogr. D Biol. Crystallogr. 54, 905-921
40. Emsley, P., and Cowtan, K. (2004) Coot. Model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132 (Pubitemid 41742764)
41. Laskowski, R. A., MacArthur, M. W., Moss, D. S., and Thornton, J. M. (1993) PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 26, 283-291
42. Delaglio, F., Grzesiek, S., Vuister, G. W., Zhu, G., Pfeifer, J., and Bax, A. (1995) NMRPipe. A multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR 6, 277-293
43. Johnson, B. A., and Blevins, R. A. (1994) NMRView. A computer program for the visualization and analysis ofNMRdata. J. Biomol.NMR4, 603-614
44. Shen, Y., Delaglio, F., Cornilescu, G., and Bax, A. (2009) TALOS+. A hybrid method for predicting protein backbone torsion angles from NMR chemical shifts. J. Biomol. NMR 44, 213-223
45. Favier, A., and Brutscher, B. (2011) Recovering lost magnetization. Polarization enhancement in biomolecular NMR. J. Biomol. NMR 49, 9-15
46. Case, D. A., Cheatham, T. E., 3rd, Darden, T., Gohlke, H., Luo, R., Merz, K. M., Jr., Onufriev, A., Simmerling, C., Wang, B., and Woods, R. J. (2005) The Amber biomolecular simulation programs. J. Comput. Chem. 26, 1668-1688 (Pubitemid 43076180)
47. Cornell, W. D., Cieplak, P., Bayly, C. I., Gould, I. R., Merz, K. M., Ferguson, D. M., Spellmeyer, D. C., Fox, T., Caldwell, J. W., and Kollman, P. A. (1995) A second generation force field for the simulation of proteins, nucleic acids, and organic molecules. J. Am. Chem. Soc. 117, 5179-5197
48. van Gunsteren, W. F., and Berendsen, H. J. C. (1997) Algorithms for macromolecular dynamics and constraint dynamics. Mol. Physiol. 34, 1311-1327
49. Garner, E., Romero, P., Dunker, A. K., Brown, C., and Obradovic, Z. (1999) Predicting binding regions within disordered proteins. Genome Inform. Ser. Workshop Genome Inform. 10, 41-50
50. Oldfield, C. J., Cheng, Y., Cortese, M. S., Romero, P., Uversky, V. N., and Dunker, A. K. (2005) Coupled folding and binding with α-helix-forming molecular recognition elements. Biochemistry 44, 12454-12470 (Pubitemid 41324337)
51. Graciet, E., Mulliert, G., Lebreton, S., and Gontero, B. (2004) Involvement of two positively charged residues of Chlamydomonas reinhardtii glyceraldehyde-3-phosphate dehydrogenase in the assembly process of a bienzyme complex involved in CO2 assimilation. Eur. J. Biochem. 271, 4737-4744 (Pubitemid 40065575)
52. Erales, J., Mekhalfi, M., Woudstra, M., and Gontero, B. (2011) Molecular mechanism of NADPH-glyceraldehyde-3-phosphate dehydrogenase regulation through the C terminus of CP12 in Chlamydomonas reinhardtii. Biochemistry 50, 2881-2888
53. Erales, J., Lignon, S., and Gontero, B. (2009) CP12 from Chlamydomonas reinhardtii, a permanent specific "chaperone-like" protein of glyceraldehydes-3-phosphate dehydrogenase. J. Biol. Chem. 284, 12735-12744
54. Nicholls, A., Sharp, K. A., and Honig, B. (1991) Protein folding and association. Insights from the interfacial and thermodynamic properties of hydrocarbons. Proteins Struct. Funct. Genet. 11, 281-296
55. Frishman, D., and Argos, P. (1995) Knowledge-based protein secondary structure assignment. Proteins 23, 566-579 (Pubitemid 26009520)