Involvement of two positively charged residues of Chlamydomonas reinhardtii glyceraldehyde-3-phosphate dehydrogenase in the assembly process of a bi-enzyme complex involved in CO2 assimilation

European Journal of Biochemistry

Volumn 271, Issue 23-24, 2004, Pages 4737-4744

  Graciet, Emmanuelle ^a,c   Mulliert, Guillermo ^b   Lebreton, Sandrine ^a   Gontero, Brigitte ^a  

^a INSTITUT JACQUES MONOD   (France)

^b Nancy University CNRS   (France)

^c CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

CP12; Glyceraldehyde 3 phosphate dehydrogenase; Phosphoribulokinase; Protein protein interactions; Site directed mutagenesis

Indexed keywords

CARBON DIOXIDE; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; PHOSPHORIBULOKINASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE;

ARTICLE; CHLAMYDOMONAS REINHARDTII; CIRCULAR DICHROISM; ENZYME KINETICS; FLUORESCENCE; GENE MUTATION; MOLECULAR MODEL; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; SITE DIRECTED MUTAGENESIS;

AMINO ACID SEQUENCE; ANIMALS; CARBON DIOXIDE; CATALYSIS; CHLAMYDOMONAS REINHARDTII; GLYCERALDEHYDE-3-PHOSPHATE DEHYDROGENASES; KINETICS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; PHOSPHOTRANSFERASES (ALCOHOL GROUP ACCEPTOR); SEQUENCE HOMOLOGY, AMINO ACID;

CHLAMYDOMONAS; CHLAMYDOMONAS REINHARDTII;

EID: 11244249415     PISSN: 00142956     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1432-1033.2004.04437.x     Document Type: Article

References (40)

1. Gontero, B., Cardenas, M.L. & Ricard,J. (1988) A functional fiveenzyme complex of chloroplasts involved in the Calvin cycle. Eur. J. Biochem. 173, 437-443.
2. 2-fixing enzyme complex in spinach chloroplasts. Z. Naturforsch. 27b, 925-932.
3. Nicholson, S., Easterby, J.S. & Powls, R. (1987) Properties of a multimeric protein complex from chloroplasts possessing potential activities of NADPH-dependent glyceraldehyde-3-phosphate dehydrogenase and phosphoribulokinase. Eur. J. Biochem. 162, 423-431.
4. Anderson, L.E., Goldhaber-Gordon, I.M., Li, D., Tang, X.Y., Xiang, M. & Prakash, N. (1995) Enzyme-enzyme interaction in the chloroplast: glyceraldehyde-3-phosphate dehydrogenase, triose phosphate isomerase and aldolase. Planta. 196, 245-255.
5. Avilan, L., Gontero, B., Lebreton, S. & Ricard, J. (1997) Memory and imprinting effects in multienzyme complexes - I. Isolation, dissociation, and reassociation of a phosphoribulokinase-glyceraldehyde-3-phosphate dehydrogenase complex from Chlamydomonas reinhardtii chloroplasts. Eur. J. Biochem. 246, 78-84.
6. Nooren, I.M.A. & Thornton, J.M. (2003) Diversity of protein-protein interactions. EMBO J. 22, 3486-3492.
7. Smith, G.R. & Sternberg, MJ. (2002) Prediction of protein-protein interactions by docking methods. Curr. Opin. Struct. Biol. 12, 28-35.
8. Gontero, B., Lebreton, S. & Graciet, E. (2001) Protein-protein interactions in plant metabolism. In Annual Plant Review (McManus, M.T., Laing, W.A. & Allan, A.C., eds), pp. 120-150. Sheffield Academic Press, Sheffield, UK.
9. Romanova, A.K. & Pavlovets, V.V. (1997) Supramolecular complexes of the enzymes participating in photosynthetic carbon dioxide assimilation. Russian J. Plant Physiol. 44, 230-238.
10. Jones, S. & Thornton, J.M. (1996) Principles of protein-protein interactions. Proc. Natl Acad. Sci. USA 93, 13-20.
11. Glaser, F., Steinberg, D.M., Vakser, I.A. & Ben-Tal, N. (2001) Residue frequencies and pairing preferences at protein-protein interfaces. Proteins Struct. Func. Gen. 43, 89-102.
12. Lo Conte, L., Chothia, C. & Janin, J. (1999) The atomic structure of protein-protein recognition sites. J. Mol. Biol. 285, 2177-2198.
13. Gallet, X., Charloteaux, B., Thomas, A. & Brasseur, R. (2000) A fast method to predict protein interaction sites from sequences. J. Mol. Biol. 302, 917-926.
14. Wedel, N., Soll, J. & Paap, B.K. (1997) CP12 provides a new mode of light regulation of Calvin cycle activity in higher plants. Proc. Natl Acad. Sci. USA 94, 10479-10484.
15. Wedel, N. & Soll, J. (1998) Evolutionary conserved light regulation of Calvin cycle activity by NADPH-mediated reversible phosphoribulokinase/CP12/ glyceraldehyde-3- phosphate dehydrogenase complex dissociation. Proc. Natl Acad. Sci. USA 95, 9699-9704.
16. Lebreton, S., Gontero, B., Avilan, L. & Ricard, J. (1997) Information transfer in multienzyme complexes - 1. Thermodynamics of conformational constraints and memory effects in the bienzyme glyceraldehyde-3-phosphate- dehydrogenase-phosphoribulokinase complex of Chlamydomonas reinhardtii chloroplasts. Eur. J. Biochem. 250, 286-295.
17. Lebreton, S., Gontero, B., Avilan, L. & Ricard, J. (1997) Memory and imprinting effects in multienzyme complexes - II. Kinetics of the bienzyme complex from Chlamydomonas reinhardtii and hysteretic activation of chloroplast oxidized phosphoribulokinase. Eur. J. Biochem. 246, 85-91.
18. Lebreton, S. & Gontero, B. (1999) Memory and imprinting in multienzyme complexes: evidence for information transfer from glyceraldehyde-3-phosphate dehydrogenase to phosphoribulo-kinase under reduced state in Chlamydomonas reinhardtii. J. Biol. Chem. 274, 20879-20884.
19. Lebreton, S., Graciet, E. & Gontero, B. (2003) Modulation, via protein-protein interactions, of glyceraldehyde-3- phosphate dehydrogenase activity through redox phosphoribulokinase regulation. J. Biol. Chem. 278, 12078-12084.
20. Graciet, E., Lebreton, S., Camadro, J.M. & Gontero, B. (2002) Thermodynamic analysis of the emergence of new regulatory properties in a phosphoribulokinase-glyceraldehyde 3-phosphate dehydrogenase complex. J. Biol. Chem. 277, 12697-12702.
21. Scagliarini, S., Trost, P., Pupillo, P. & Valenti, V. (1993) Light activation and molecular-mass forms of NAD(P)-glyceraldehyde 3-phosphate dehydrogenase of spinach and maize leaves. Planta. 190, 313-319.
22. Baalmann, E., Backhausen, J.E., Kitzmann, C. & Scheibe, R. (1994) Regulation of NADP-dependent glyceraldehyde 3-phosphate dehydrogenase activity in spinach chloroplast. Bot. Acta 107, 313-320.
23. Scheibe, R., Wedel, N., Vetter, S., Emmerlich, V. & Sauermann, S.M. (2002) Co-existence of two regulatory NADP-glyceraldehyde 3-P dehydrogenase complexes in higher plant chloroplasts. Eur. J. Biochem. 269, 5617-5624.
24. Avilan, L., Gontero, B., Lebreton, S. & Ricard, J. (1997) Information transfer in multienzyme complexes. 2. The role of Arg64 of Chlamydomonas reinhardtii phosphoribulokinase in the information transfer between glyceraldehyde-3-phosphate dehydrogenase and phosphoribulokinase. Eur. J. Biochem. 250, 296-302.
25. Bogan, A.A. & Thorn, K.S. (1998) Anatomy of hot spots in protein interfaces. J. Mol. Biol. 280, 1-9.
26. Li, D., Urrutia, M., Smith-Gill, S.J. & Mariuzza, R.A. (2003) Dissection of binding interactions in the complex between the antilysozyme antibody HyHEL-63 and its antigen. Biochemistry 42, 11-22.
27. Li, Y., Li, H., Smith-Gill, S.J. & Mariuzza, R.A. (2000) Three-dimensional structures of the free and antigen-bound Fab from monoclonal antilysozyme antibody HyHEL-63. Biochemistry 39, 6296-6309.
28. Graciet, E., Lebreton, S., Camadro, J.M. & Gontero, B. (2003) Characterization of native and recombinant A4 glyceraldehyde 3-phosphate dehydrogenase. Eur. J. Biochem. 270, 129-136.
29. Graciet, E., Gans, P., Wedel, N., Lebreton, S., Camadro, J.M. & Gontero, B. (2003) The small protein CP12: a protein linker for supramolecular assembly. Biochemistry 42, 8163-8170.
30. Baalmann, E., Backhausen, J.E., Rak, C., Vetter, S. & Scheibe, R. (1995) Reductive modification and nonreductive activation of purified spinach chloroplast NADP-dependent glyceraldehyde-3-phosphate dehydrogenase. Arch. Biochem. Biophys. 324, 201-208.
31. 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.
32. Sali, A. & Blundell, T.L. (1993) Comparative protein modelling by satisfaction of spatial restraints. J. Mol. Biol. 234, 779-815.
33. Case, D.A., Pearlman, D.A., Caldwell, J.W., Cheatham, T.E., Ross, W.S., Simmerling, C.L., Darden, T.A., Merz, K.M., Stanton, R.V., Cheng, A.L., Vincent, J.J., Crowley, M., Tsui, V., Radmer, R.J., Duan, Y., Pitera, J., Massova, I., Seibel, G.L., Singh, U.C., Weiner, P.K. & Koll-man, P.A. (1999) AMBER 6. University of California, San Francisco, CA.
34. Sambrook, J., Fritsch, E.F. & Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual. 2nd edn. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY, USA.
35. Fermani, S., Ripamonti, A., Sabatino, P., Zanotti, G., Scagliarini, S., Sparla, F., Trost, P. & Pupillo, P. (2001) Crystal structure of the non-regulatory A (4) isoform of spinach chloroplast glyceraldehyde-3-phosphate dehydrogenase complexed with NADP. J. Mol. Biol. 314, 527-542.
36. Sparla, F., Fermani, S., Falini, G., Zaffagnini, M., Ripamonti, A., Sabatino, P., Pupillo, P. & Trost, P. (2004) Coenzyme site-directed mutants of photosynthetic A (4)-GAPDH show selectively reduced NADPH-dependent catalysis, similar to regulatory AB-GAPDH inhibited by oxidized thioredoxin. J. Mol. Biol. 340, 1025-1037.
37. Hendsch, Z.S. & Tidor, B. (1994) Do salt bridges stabilize proteins? A continuum electrostatic analysis. Protein Sci. 3, 211-226.
38. Fersht, A.R. (1972) Conformational equilibria in α- and δ-chymotrypsin: the energetics and importance of the salt bridge. J. Mol. Biol. 64, 497-509.
39. Anderson, D.E., Becktel, W.J. & Dahlquist, F.W. (1990) pH-induced denaturation of proteins: a single salt bridge contributes 3-5 kcal/mol to the free energy of folding of T4 lysozyme. Biochemistry 29, 2403-2408.
40. Mouche, F., Gontero, B., Callebaut, I., Mornon, J.P. & Boisset, N. (2002) Striking conformational change suspected within the phosphoribulokinase dimer induced by interaction with GAPDH. J. Biol. Chem. 277, 6743-6749.