Interplay Between Metal Binding and cis/trans Isomerization in Legume Lectins: Structural and Thermodynamic Study of P. angolensis Lectin

Journal of Molecular Biology

Volumn 361, Issue 1, 2006, Pages 153-167

  Garcia Pino, Abel ^a   Buts, Lieven ^a   Wyns, Lode ^a   Loris, Remy ^a  

^a VRIJE UNIVERSITEIT BRUSSEL   (Belgium)

Author keywords

cis peptide; crystal structure; lectin; metal binding; stability

Indexed keywords

ASPARAGINE; METAL; MONOMER; PLANT LECTIN; PROLINE;

AMINO ACID SUBSTITUTION; ARTICLE; BETA CHAIN; BINDING KINETICS; CARBOXY TERMINAL SEQUENCE; CHEMICAL BOND; CIS ISOMER; CIS TRANS ISOMERISM; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; LEGUME; METAL BINDING; METALLATION; MOLECULAR INTERACTION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN FAMILY; PROTEIN STABILITY; PROTEIN STRUCTURE; STRUCTURE ANALYSIS; THERMODYNAMICS; THERMOSTABILITY; TRANS ISOMER;

PTEROCARPUS ANGOLENSIS;

EID: 33745886508     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2006.06.006     Document Type: Article

References (57)

1. Anderson T.A., Cordes M.H., and Sauer R.T. Sequence determinants of a conformational switch in a protein structure. Proc. Natl Acad. Sci. USA 102 (2005) 18344-18349
2. Buxbaum J.N., and Tagoe C.E. The genetics of the amyloidoses. Annu. Rev. Med. 51 (2000) 543-569
3. Booth D.R., Sunde M., Bellotti V., Robinson C.V., Hutchinson W.L., Fraser P.E., et al. Instability, unfolding and aggregation of human lysozyme variants underlying amyloid fibrillogenesis. Nature 385 (1997) 787-793
4. Pepys M.B., Hawkins P.N., Booth D.R., Vigushin D.M., Tennent G.A., Soutar A.K., et al. Human lysozyme gene mutations cause hereditary systemic amyloidosis. Nature 362 (1993) 553-557
5. Jabs A., Weiss M.S., and Hilgenfeld R. Non-proline cis peptide bonds in proteins. J. Mol. Biol. 286 (1999) 291-304
6. Heroux A., White E.L., Ross L.J., and Borhani D.W. Crystal structures of the Toxoplasma gondii hypoxanthine-guanine phosphoribosyltransferase-GMP and -IMP complexes: comparison of purine binding interactions with the XMP complex. Biochemistry 38 (1999) 14485-14494
7. 2+ ions bound: insights into the catalytic mechanism. Biochemistry 38 (1999) 14495-14506
8. Bouckaert J., Dewallef Y., Poortmans F., Wyns L., and Loris R. The structural features of concanavalin A governing non-proline peptide isomerization. J. Biol. Chem. 275 (2000) 19778-19787
9. Guan R.J., Xiang Y., He X.L., Wang C.G., Wang M., Zhang Y., et al. Structural mechanism governing cis and trans isomeric states and an intramolecular switch for cis/trans isomerization of a non-proline peptide bond observed in crystal structures of scorpion toxins. J. Mol. Biol. 341 (2004) 1189-1204
10. Reeke Jr. G.N., Becker J.W., and Edelman G.M. The covalent and three-dimensional structure of concanavalin A. IV. Atomic coordinates, hydrogen bonding, and quaternary structure. J. Biol. Chem. 250 (1975) 1525-1547
11. Bouckaert J., Loris R., Poortmans F., and Wyns L. Crystallographic structure of metal-free concanavalin A at 2.5 A resolution. Proteins: Struct. Funct. Genet. 23 (1995) 510-524
12. Brewer C.F., Brown III R.D., and Koenig S.H. Kinetics of conformational transitions of demetalized Concanavalin A. Biochem. Biophys. Res. Commun. 112 (1983) 595-601
13. Brewer C.F., Brown III R.D., and Koenig S.H. Metal ion binding and conformational transitions in concanavalin A: a structure-function study. J. Biomol. Struct. Dynam. 1 (1983) 961-997
14. 2+ ions. Biochemistry 16 (1977) 3883-3896
15. Lescar J., Loris R., Mitchell E., Gautier C., Chazalet V., Cox V., et al. Isolectins I-A and I-B of Griffonia (Bandeiraea) simplicifolia. Crystal structure of metal-free GS I-B(4) and molecular basis for metal binding and monosaccharide specificity. J. Biol. Chem. 277 (2002) 6608-6614
16. Loris R., Imberty A., Beeckmans S., Van Driessche E., Read J.S., Bouckaert J., et al. Crystal structure of Pterocarpus angolensis lectin in complex with glucose, sucrose, and turanose. J. Biol. Chem. 278 (2003) 16297-16303
17. Loris R., Van Walle I., De Greve H., Beeckmans S., Deboeck F., Wyns L., and Bouckaert J. Structural basis of oligomannose recognition by the Pterocarpus angolensis seed lectin. J. Mol. Biol. 335 (2004) 1227-1240
18. Privalov P.L., and Medved L.V. Domains in the fibrinogen molecule. J. Mol. Biol. 159 (1982) 665-683
19. Privalov P.L. Stability of proteins. Proteins which do not present a single cooperative system. Advan. Protein Chem. 35 (1982) 1-104
20. Rösgen J., and H.H.-J. From macromolecules to man. In: Kemp R.B. (Ed). Handbook of Thermal Analysis and Calorimetry 4 (1999), Elsevier Publ. 1032
21. Loris R., Hamelryck T., Bouckaert J., and Wyns L. Legume lectin structure. Biochim. Biophys. Acta 1383 (1998) 9-36
22. Sharma V., and Surolia A. Analyses of carbohydrate recognition by legume lectins: size of the combining site loops and their primary specificity. J. Mol. Biol. 267 (1997) 433-445
23. Derewenda Z., Yariv J., Helliwell J.R., Kalb A.J., Dodson E.J., Papiz M.Z., et al. The structure of the saccharide-binding site of concanavalin A. EMBO J. 8 (1989) 2189-2193
24. Bouckaert J., Poortmans F., Wyns L., and Loris R. Sequential structural changes upon zinc and calcium binding to metal-free concanavalin A. J. Biol. Chem. 271 (1996) 16144-16150
25. Loris R., Garcia-Pino A., Buts L., Bouckaert J., Beeckmans S., De Greve H., and Wyns L. Crystallization and crystal manipulation of the Pterocarpus angolensis seed lectin. Acta Crystallog. sect. D 61 (2005) 685-689
26. Buts L., Garcia-Pino A., Imberty A., Amiot N., Boons G.J., Beeckmans S., et al. Structural basis for the recognition of complex-type biantennary oligosaccharides by Pterocarpus angolensis lectin. FEBS J. 273 (2006) 2407-2420
27. Moothoo D.N., Canan B., Field R.A., and Naismith J.H. Man alpha1-2 Man alpha-OMe-concanavalin A complex reveals a balance of forces involved in carbohydrate recognition. Glycobiology 9 (1999) 539-545
28. Sinha S., Mitra N., Kumar G., Bajaj K., and Surolia A. Unfolding studies on soybean agglutinin and concanavalin a tetramers: a comparative account. Biophys. J. 88 (2005) 1300-1310
29. Ahmad N., Srinivas V.R., Reddy G.B., and Surolia A. Thermodynamic characterization of the conformational stability of the homodimeric protein, pea lectin. Biochemistry 37 (1998) 16765-16772
30. Schwarz F.P., Puri K.D., Bhat R.G., and Surolia A. Thermodynamics of monosaccharide binding to concanavalin A, pea (Pisum sativum) lectin, and lentil (Lens culinaris) lectin. J. Biol. Chem. 268 (1993) 7668-7677
31. Dalhus B., Saarinen M., Sauer U.H., Eklund P., Johansson K., Karlsson A., et al. Structural basis for thermophilic protein stability: structures of thermophilic and mesophilic malate dehydrogenases. J. Mol. Biol. 318 (2002) 707-721
32. Dams T., Auerbach G., Bader G., Jacob U., Ploom T., Huber R., and Jaenicke R. The crystal structure of dihydrofolate reductase from Thermotoga maritima: molecular features of thermostability. J. Mol. Biol. 297 (2000) 659-672
33. Srinivas V.R., Reddy G.B., Ahmad N., Swaminathan C.P., Mitra N., and Surolia A. Legume lectin family, the 'natural mutants of the quaternary state', provide insights into the relationship between protein stability and oligomerization. Biochim. Biophys. Acta 1527 (2001) 102-111
34. Surolia A., Sharon N., and Schwarz F.P. Thermodynamics of monosaccharide and disaccharide binding to Erythrina corallodendron lectin. J. Biol. Chem. 271 (1996) 17697-17703
35. Hamelryck T.W., Poortmans F., Goossens A., Angenon G., Van Montagu M., Wyns L., and Loris R. Crystal structure of arcelin-5, a lectin-like defense protein from Phaseolus vulgaris. J. Biol. Chem. 271 (1996) 32796-32802
36. Mourey L., Pedelacq J.D., Birck C., Fabre C., Rouge P., and Samama J.P. Crystal structure of the arcelin-1 dimer from Phaseolus vulgaris at 1.9-A resolution. J. Biol. Chem. 273 (1998) 12914-12922
37. Hauri H.P., Kappeler F., Andersson H., and Appenzeller C. ERGIC-53 and traffic in the secretory pathway. J. Cell Sci. 113 (2000) 587-596
38. Velloso L.M., Svensson K., Schneider G., Pettersson R.F., and Lindqvist Y. Crystal structure of the carbohydrate recognition domain of p58/ERGIC-53, a protein involved in glycoprotein export from the endoplasmic reticulum. J. Biol. Chem. 277 (2002) 15979-15984
39. Velloso L.M., Svensson K., Pettersson R.F., and Lindqvist Y. The crystal structure of the carbohydrate-recognition domain of the glycoprotein sorting receptor p58/ERGIC-53 reveals an unpredicted metal-binding site and conformational changes associated with calcium ion binding. J. Mol. Biol. 334 (2003) 845-851
40. Chothia C., and Lesk A.M. The relation between the divergence of sequence and structure in proteins. EMBO J. 5 (1986) 823-826
41. Heinz D.W., Baase W.A., and Matthews B.W. Folding and function of a T4 lysozyme containing 10 consecutive alanines illustrate the redundancy of information in an amino acid sequence. Proc. Natl Acad. Sci. USA 89 (1992) 3751-3755
42. Jones D.T., Moody C.M., Uppenbrink J., Viles J.H., Doyle P.M., Harris C.J., et al. Towards meeting the Paracelsus Challenge: the design, synthesis, and characterization of paracelsin-43, an alpha-helical protein with over 50% sequence identity to an all-beta protein. Proteins: Struct. Funct. Genet. 24 (1996) 502-513
43. Dalal S., Balasubramanian S., and Regan L. Protein alchemy: changing beta-sheet into alpha-helix. Nature Struct. Biol. 4 (1997) 548-552
44. Yuan S.M., and Clarke N.D. A hybrid sequence approach to the paracelsus challenge. Proteins: Struct. Funct. Genet. 30 (1998) 136-143
45. Meyer T., Hendry L., Begitt A., John S., and Vinkemeier U. A single residue modulates tyrosine dephosphorylation, oligomerization, and nuclear accumulation of stat transcription factors. J. Biol. Chem. 279 (2004) 18998-19007
46. Cordes M.H., Walsh N.P., McKnight C.J., and Sauer R.T. Evolution of a protein fold in vitro. Science 284 (1999) 325-328
47. Bates P.A., Dokurno P., Freemont P.S., and Sternberg M.J. Conformational analysis of the first observed non-proline cis-peptide bond occurring within the complementarity determining region (CDR) of an antibody. J. Mol. Biol. 284 (1998) 549-555
48. Ludwig M.L., Pattridge K.A., Metzger A.L., Dixon M.M., Eren M., Feng Y., and Swenson R.P. Control of oxidation-reduction potentials in flavodoxin from Clostridium beijerinckii: the role of conformation changes. Biochemistry 36 (1997) 1259-1280
49. Press W.H., and Vetterling W.T. Numerical Recipes in C: The Art of Scientific Computing. 2nd edit. vol. 2 (1992), Cambridge University Press, Cambridge
50. Marky L.A., and Breslauer K.J. Calculating thermodynamic data for transitions of any molecularity from equilibrium melting curves. Biopolymers 26 (1987) 1601-1620
51. Jancarik J., and Kim S.-H. Sparse matrix sampling: a screening method for crystallization of proteins. J. Appl. Crystallog. 24 (1991) 409-411
52. Otwinowski Z., and Minor W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276 (1997) 307-326
53. McCoy A.J., Grosse-Kunstleve R.W., Storoni L.C., and Read R.J. Likelihood-enhanced fast translation functions. Acta Crystallog. sect. D 61 (2005) 458-464
54. Storoni L.C., McCoy A.J., and Read R.J. Likelihood-enhanced fast rotation functions. Acta Crystallog. sect. D 60 (2004) 432-438
55. Brunger A.T., Adams P.D., Clore G.M., DeLano W.L., Gros P., Grosse-Kunstleve R.W., et al. Crystallography NMR system: a new software suite for macromolecular structure determination. Acta Crystallog. sect. D 54 (1998) 905-921
56. Cambillau C. TURBO-FRODO: Molecular Graphics Program for Silicon Graphics. IRIS 4D Series (1992), Bio-Graphics, Marseille, France
57. Emsley P., and Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallog. sect. D 60 (2004) 2126-2132