Modeling the interaction between aldolase and the thrombospondin-related anonymous protein, a key connection of the malaria parasite invasion machinery

Proteins: Structure, Function and Genetics

Volumn 66, Issue 3, 2007, Pages 528-537

  Buscaglia, Carlos A ^a,c   Hol, Wim G J ^b   Nussenzweig, Victor ^a   Cardozo, Timothy ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^c INSTITUTO DE INVESTIGACIONES BIOTECNOLÓGICAS   (Argentina)

Author keywords

Apicomplexa; Flexible docking; Molecular motor; Mutagenesis; Plasmodium; WASp

Indexed keywords

ADHESIN; ALANINE; ASPARTIC ACID; FRUCTOSE 1,6 BISPHOSPHATE; FRUCTOSE BISPHOSPHATE ALDOLASE; MOLECULAR MOTOR; MUTANT PROTEIN; THROMBOSPONDIN; THROMBOSPONDIN RELATED ANONYMOUS PROTEIN; TRYPTOPHAN; UNCLASSIFIED DRUG;

CARBOXY TERMINAL SEQUENCE; CATALYSIS; CELL MOTILITY; CONFERENCE PAPER; CONTROLLED STUDY; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME STRUCTURE; EVOLUTION; HOST PARASITE INTERACTION; MALARIA; MATHEMATICAL MODEL; MUTAGENESIS; NONHUMAN; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; STRUCTURE ACTIVITY RELATION;

ANIMALS; BINDING SITES; CRYSTALLOGRAPHY, X-RAY; FRUCTOSE-BISPHOSPHATE ALDOLASE; HUMANS; KINETICS; LIGANDS; MODELS, MOLECULAR; MUSCLE, SKELETAL; MUTATION; PROTOZOAN PROTEINS; RABBITS;

APICOMPLEXA; MAMMALIA; PLASMODIUM (APICOMPLEXA); PLASMODIUM FALCIPARUM;

EID: 33846223942     PISSN: 08873585     EISSN: 10970134     Source Type: Journal    
DOI: 10.1002/prot.21266     Document Type: Conference Paper

References (48)

1. Gefflaut T, Blonski C, Perie J, Willson M. Class I aldolases: substrate specificity, mechanism, inhibitors and structural aspects. Prog Biophys Mol Biol 1995;63:301-340.
2. Kim H, Certa U, Dobeli H, Jakob P, Hol WG. Crystal structure of fructose-1,6-bisphosphate aldolase from the human malaria parasite Plasmodium falciparum. Biochemistry 1998;37:4388-4396.
3. Chudzik DM, Michels PA, de Walque S, Hol WG. Structures of type 2 peroxisomal targeting signals in two trypanosomatid aldolases. J Mol Biol 2000;300:697-707.
4. Hester G, Brenner-Holzach O, Rossi FA, Struck-Donatz M, Winterhalter KH, Smit JD, Piontek K. The crystal structure of fructose-1,6-bisphosphate aldolase from Drosophila melanogaster at 2.5 Å resolution. FEBS Lett 1991;292:237-242.
5. Gamblin SJ, Davies GJ, Grimes JM, Jackson RM, Littlechild JA, Watson HC. Activity and specificity of human aldolases. J Mol Biol 1991;219:573-576.
6. Dalby AR, Tolan DR, Littlechild JA. The structure of human liver fructose-1,6-bisphosphate aldolase. Acta Crystallogr D Biol Crystallogr 2001;57:1526-1533.
7. Arakaki TL, Pezza JA, Cronin MA, Hopkins CE, Zimmer DB, Tolan DR, Allen KN. Structure of human brain fructose 1,6-(bis)phosphate aldolase: linking isozyme structure with function. Protein Sci 2004;13:3077-3084.
8. Dalby A, Dauter Z, Littlechild JA. Crystal structure of human muscle aldolase complexed with fructose 1,6-bisphosphate: mechanistic implications. Protein Sci 1999;8:291-297.
9. Choi KH, Mazurkie AS, Morris AJ, Utheza D, Tolan DR, Allen KN. Structure of a fructose-1,6-bis(phosphate) aldolase liganded to its natural substrate in a cleavage-defective mutant at 2.3 Å. Biochemistry 1999;38:12655-12664.
10. Choi KH, SM J, Hopkins CE, Tolan DR, Allen KN. Snapshots of catalysis: the structure of fructose-1,6-(bis)phosphate aldolase covalently bound to the substrate dihydroxyacetone phosphate. Biochemistry 2001;40:13868-13875.
11. St-Jean M, Lafrance-Vanasse J, Liotard B, Sygusch J. High resolution reaction intermediates of rabbit muscle fructose-1,6-bisphosphate aldolase: substrate cleavage and induced fit. J Biol Chem 2005;280:27262-27270.
12. Sygusch J, Beaudry D, Allaire M. Molecular architecture of rabbit skeletal muscle aldolase at 2.7 Å resolution. Proc Natl Acad Sci USA 1987;84:7846-7850.
13. Berthiaume L, Tolan DR, Sygusch J. Differential usage of the carboxyl-terminal region among aldolase isozymes. J Biol Chem 1993;268:10826-10835.
14. Blom N, Sygusch J. Product binding and role of the C-terminal region in class I D-fructose 1,6-bisphosphate aldolase. Nat Struct Biol 1997;4:36-39.
15. O'Reilly G, Clarke F. Identification of an actin binding region in aldolase. FEBS Lett 1991;321:69-72.
16. Wang J, Morris AJ, Tolan DR, Pagliaro L. The molecular nature of the F-actin binding activity of aldolase revealed with site-directed mutants. J Biol Chem 1996;271:6861-6865.
17. Carr D, Knull H. Aldolase-tubulin interactions: removal of tubulin C-terminals impairs interactions. Biochem Biophys Res Commun 1993;195:289-293.
18. Buscaglia CA, Penesetti D, Tao M, Nussenzweig V. Characterization of an aldolase-binding site in the Wiskott-Aldrich syndrome protein. J Biol Chem 2006;281:1324-1331.
19. Buscaglia CA, Coppens I, Hol WG, Nussenzweig V. Sites of interaction between aldolase and thrombospondin-related anonymous protein in plasmodium. Mol Biol Cell 2003;14:4947-4957.
20. Jewett TJ, Sibley LD. Aldolase forms a bridge between cell surface adhesins and the actin cytoskeleton in apicomplexan parasites. Mol Cell 2003;11:885-894.
21. Kappe SH, Buscaglia CA, Bergman LW, Coppens I, Nussenzweig V. Apicomplexan gliding motility and host cell invasion: overhauling the motor model. Trends Parasitol 2004;20:13-16.
22. Soldati D, Foth BJ, Cowman AF. Molecular and functional aspects of parasite invasion. Trends Parasitol 2004;20:567-574.
23. Kappe S, Bruderer T, Gantt S, Fujioka H, Nussenzweig V, Menard R. Conservation of a gliding motility and cell invasion machinery in Apicomplexan parasites. J Cell Biol 1999;147:937-944.
24. Baum J, Richard D, Healer J, Rug M, Krnajski Z, Gilberger TW, Green JL, Holder AA, Cowman AF. A conserved molecular motor drives cell invasion and gliding motility across malaria life cycle stages and other Apicomplexan parasites. J Biol Chem 2006;281: 5197-5208.
25. Menard R. Gliding motility and cell invasion by Apicomplexa: insights from the Plasmodium sporozoite. Cell Microbiol 2001;3: 63-73.
26. Sibley LD. Intracellular parasite invasion strategies. Science 2004;304:248-253.
27. Gaffar FR, Yatsuda AP, Franssen FF, de Vries E. A Babesia bovis merozoite protein with a domain architecture highly similar to the thrombospondin-related anonymous protein (TRAP) present in Plasmodium sporozoites. Mol Biochem Parasitol 2004;136:25-34.
28. Jones ML, Kitson EL, Rayner JC. Plasmodium falciparum erythrocyte invasion: a conserved myosin associated complex. Mol Biochem Parasitol 2006;147:74-84.
29. Schneider ML, Post CB. Solution structure of a band 3 peptide inhibitor bound to aldolase: a proposed mechanism for regulating binding by tyrosine phosphorylation. Biochemistry 1995;34: 16574-16584.
30. Murzin AG, Brenner SE, Hubbard T, Chothia C. SCOP: a structural classification of proteins database for the investigation of sequences and structures. J Mol Biol 1995;247:536-540.
31. Cardozo T, Totrov M, Abagyan R. Homology modeling by the ICM method. Proteins 1995;23:403-414.
32. Abagyan R, Totrov M. Biased probability Monte Carlo conformational searches and electrostatic calculations for peptides and proteins. J Mol Biol 1994;235:983-1002.
33. Totrov M, Abagyan R. Flexible protein-ligand docking by global energy optimization in internal coordinates. Proteins 1997; (Suppl. 1):215-220.
34. Bordner AJ, Abagyan R. Ab initio prediction of peptide-MHC binding geometry for diverse class I MHC allotypes Proteins 2006;63:512-514.
35. Fernandez-Recio J, Totrov M, Abagyan R. Soft protein-protein docking in internal coordinates. Protein Sci 2002;11:280-291.
36. Nemethy G, Gibson KD, Palmer KA, Yoon CN, Paterlini G, Zagari A, Rumsey S, Scherag HA. Energy parameters in polypeptides, Part 10: Improved geometrical parameters and nonbonded interactions for use in the ECEPP/3 algorithm, with application to proline-containing peptides. J Phys Chem 1992;96:6472-6484.
37. Totrov M, Abagyan R. Detailed ab initio prediction of lysozyme-antibody complex with 1.6 Å accuracy. Nat Struct Biol 1994;1: 259-263.
38. Abagyan R, Argos P. Optimal protocol and trajectory visualization for conformational searches of peptides and proteins. J Mol Biol 1992;225:519-532.
39. Metropolis NA, Rosenbluth AW, Rosenbluth NM, Teller AH, Teller E. Equation of state calculations by fast computing machines. J Chem Phys 1953;21:1087-1092.
40. Knapp B, Hundt E, Kupper HA. Plasmodium falciparum aldolase: gene structure and localization. Mol Biochem Parasitol 1990;40:1-4.
41. Alvarez P, Buscaglia CA, Campetella O. Improving protein pharmacokinetics by genetic fusion to simple amino acid sequences. J Biol Chem 2004;279:3375-3381.
42. Maurady A, Zdanov A, de Moissac D, Beaudry D, Sygusch J. A conserved glutamate residue exhibits multifunctional catalytic roles in D-fructose-1,6-bisphosphate aldolases. J Biol Chem 2002;277:9474-9483.
43. Blonski C, De Moissac D, Perie J, Sygusch J. Inhibition of rabbit muscle aldolase by phosphorylated aromatic compounds. Biochem J 1997;323:71-77.
44. Dax C, Coincon M, Sygusch J, Blonski C. Hydroxynaphthaldehyde phosphate derivatives as potent covalent Schiff base inhibitors of fructose-1,6- bisphosphate aldolase. Biochemistry 2005;44:5430-5443.
45. Schindler R, Weichselsdorfer E, Wagner O, Bereiter-Hahn J. Aldolase-localization in cultured cells: cell-type and substrate-specific regulation of cytoskeletal associations. Biochem Cell Biol 2001;79:719-728.
46. Zhou Y, Abagyan R. How and why phosphotyrosine-containing peptides bind to the SH2 and PTB domains. Fold Des 1998; 3:513-522.
47. Fernandez-Recio J, Abagyan R, Totrov M. Improving CAPRI predictions: optimized desolvation for rigid-body docking. Proteins 2005;60:308-313.
48. Fernandez-Recio J, Totrov M, Abagyan R. ICM-DISCO docking by global energy optimization with fully flexible side-chains. Proteins 2003;52:113-117.