Different contribution of conserved amino acids to the global properties of triosephosphate isomerases

Proteins: Structure, Function and Bioinformatics

Volumn 82, Issue 2, 2014, Pages 323-335

  Aguirre, Yolanda ^a   Cabrera, Nallely ^a   Aguirre, Beatriz ^a   Pérez Montfort, Ruy ^a   Hernandez Santoyo, Alejandra ^a   Reyes Vivas, Horacio ^b   Enríquez Flores, Sergio ^b   de Gómez Puyou, Marietta Tuena ^a   Gómez Puyou, Armando ^a   Sanchez Ruiz, Jose M ^c   Costas, Miguel ^a  

^a UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

^b SECRETARÍA DE SALUD   (Mexico)

^c UNIVERSITY OF GRANADA   (Spain)

Author keywords

Free energy barriers; Homologous enzymes; Kinetic stability; Protein denaturation; Transition state plasticity

Indexed keywords

AMINO ACID; DIMER; MONOMER; TRIOSEPHOSPHATE ISOMERASE;

AMINO ACID SEQUENCE; ARTICLE; DIFFERENTIAL SCANNING CALORIMETRY; ENERGY TRANSFER; ENZYME KINETICS; ENZYME MECHANISM; ENZYME STABILITY; GIARDIA LAMBLIA; HUMAN; MOLECULAR INTERACTION; MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DENATURATION; PROTEIN FOLDING; TRYPANOSOMA BRUCEI; TRYPANOSOMA CRUZI;

GIARDIA INTESTINALIS; HOMO SAPIENS; TRYPANOSOMA BRUCEI; TRYPANOSOMA CRUZI;

FREE-ENERGY BARRIERS; HOMOLOGOUS ENZYMES; KINETIC STABILITY; PROTEIN DENATURATION; TRANSITION-STATE PLASTICITY;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; CONSERVED SEQUENCE; CRYSTALLOGRAPHY, X-RAY; ENTROPY; ENZYME STABILITY; GIARDIA LAMBLIA; HUMANS; KINETICS; MODELS, MOLECULAR; PROTEIN UNFOLDING; PROTOZOAN PROTEINS; STRUCTURAL HOMOLOGY, PROTEIN; TRIOSE-PHOSPHATE ISOMERASE; TRYPANOSOMA BRUCEI BRUCEI; TRYPANOSOMA CRUZI;

EID: 84892675123     PISSN: 08873585     EISSN: 10970134     Source Type: Journal    
DOI: 10.1002/prot.24398     Document Type: Article

References (46)

1. Minor DL, Kim PS. Context-dependent secondary structure formation of a designed protein sequence. Nature 1996;380:730-734.
2. Lockless SW, Ranganathan R. Evolutionary conserved pathways of energetic connectivity in protein families. Science 1999;286:295-299.
3. García-Torres I, Cabrera N, Torres-Larios A, Rodríguez-Bolaños M, Díaz-Mazariegos S, Gómez-Puyou A, Pérez-Montfort R. Identification of amino acids that account for long-range interactions in two triosephosphate isomerases from pathogenic trypanosomes. PLoS One 2011;6:e1879.
4. Freire E. The propagation of binding interactions to remote sites in proteins: and analysis of the monoclonal antibody D1.3 to lysozyme. Proc Natl Acad Sci USA 1999;96:10118-10122.
5. Halabi N, Rivoire O, Leibler S, Rangantahan R. Protein sectors: evolutionary units of three-dimensional structure. Cell 2009;138:774-786.
6. Hey Y, Chen Y, Alexander P, Bryan PN, Orban J. NMR structure of two designed proteins with high sequence similarity, but different folds and function. Proc Natl Acad Sci USA 2008;105:14412-14417.
7. Knowles JR. Enzyme catalysis: not different, just better. Nature 1991;350:121-124.
8. Wierenga RK, Kapetaniou EG, Venkatesan R. Triosephosphate isomerase: a highly evolved biocatalyst. Cell Mol Life Sci 2010;67:3961-3982.
9. Waley SG. Refolding of triose phosphate isomerase. Biochem J 1973;135:165-172.
10. Zomosa-Signoret V, Hernández-Alcántara G, Reyes-Vivas H, Martínez-Martínez E, Garza-Ramos G, Pérez-Montfort R, Tuena de Gómez-Puyou M, Gómez-Puyou A. Control of reactivation kinetics of homodimeric triosephosphate isomerase from unfolded monomers. Biochemistry 2003;42:3311-3318.
11. Schneider AS. Triosephosphate isomerase deficiency: historical perspectives and molecular aspects. Baillieres Best Pract Res Clin Haematol 2000;13:119-140.
12. Orosz F, Oláh J, Ovadi J. Triosephosphate isomerase deficiency facts and doubts. IUBMB Life 2006;58:703-715.
13. Orosz F, Oláh J, Ovadi, J. Triosephosphate isomerase deficiency: new insights into an enigmatic disease. Biochim Biophys Acta 2009;1792:1168-1174.
14. Rodríguez-Almazán C, Arreola R, Rodríguez-Larrea D, Aguirre-López B, Tuena de Gómez-Puyou M, Pérez-Montfort R, Costas M, Gómez-Puyou A, Torres-Larios A. Structural basis of triosephosphate isomerase deficiency: mutation E104D is related to alterations of a conserved water network at the dimer interface. J Biol Chem 2008;283:23254-23263.
15. Wierenga RK, Noble MEM, Vriend G, Nauche S, Hol WGJ. Refined 1.83 Å of trypanosomal triosephosphate isomerase crystallized in the presence of 2.4 M ammonium sulphate. A comparison with the structure of the trypanosomal triosephosphate isomerase-glycerol-3-phosphate complex. J Mol Biol 1991;220:995-1015.
16. Maldonado E, Soriano-García M, Moreno A, Cabrera N, Garza-Ramos G, Tuena de Gómez-Puyou M, Gómez-Puyou A, Pérez-Montfort R. Differences in the intersubunit contacts in triosephosphate isomerase from two closely related pathogenic trypanosomes. J Mol Biol 1998;283:193-203.
17. Reyes-Vivas H, Díaz A, Peón J, Mendoza-Hernández G, Hernández-Alcántara G, de la Mora-de la Mora I, Enriquez-Flores S, Domínguez-Ramírez L, López-Velarde G. Disulfide bridges in the mesophilic triosephosphate isomerase from Giardia lamblia are related to oligomerization and activity. J Mol Biol 2007;365:752-763.
18. Borchert TV, Pratt K, Zeelen JP, Callens M, Noble ME, Opperdoes FR, Michels PA, Wierenga RK. Overexpression of trypanosomal triosephosphate isomerase in Escherichia coli and characterisation of a dimer-interface mutant. Eur J Biochem 1993;211:703-710.
19. Ostoa-Saloma P, Garza-Ramos G, Ramírez J, Becker I, Berzunza M, Landa A, Gómez-Puyou A, Tuena de Gómez-Puyou M, Pérez-Montfort R. Cloning, expression, purification and characterization of triosephosphate isomerase from Trypanosoma cruzi. Eur J Biochem 1997;244:700-705.
20. Enriquez-Flores S, Rodríguez-Romero A, Hernández-Alcántara G, Oria-Hernández J, Gutiérrez-Castrellón P, Pérez-Hernández G, de la Mora de la Mora I, Castillo-Villanueva A, García-Torres I, Mendez ST, Gómez-Manzo S, Torres-Arroyo A, López-Velazquez G, Reyes-Vivas H. Determining the molecular mechanism of inactivation by chemical modification of triosephosphate isomerase from the human parasite Giardia lamblia: a study for antiparasitic drug design. Proteins 2011;79:2711-2724.
21. Kabsch W. XDS. Acta Crystallogr D Biol Crystallogr 2010;66:125-132.
22. Collaborative Computational Project, Number 4. The CCP4 suite: programs for protein crystallography. Acta Crystallogr D Biol Crystallogr 1994;50:760-763.
23. Evans P. Scaling and assessment of data quality. Acta Crystallogr D Biol Crystallogr 2006;62:72-82.
24. McCoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC, Read RJ. Phaser crystallographic software. J Appl Crystallogr 2007;40:658-674.
25. Adams PD, Afonine PV, Bunkoczi G, Chen VB, Davis IW, Echols N, Headd JJ, Hung LW, Kapral GJ, Grosse-Kunstleve RW, McCoy AJ, Moriarty NW, Oeffner R, Read RJ, Richardson DC, Richardson JS, Terwilliger TC, Zwart PH. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta crystallogr D, Biol crystallogr 2010;66, 213-221.
26. Emsley P, Lohkamp B, Scott WG, Cowtan K. Features and development of Coot. Acta Crystallogr D Biol Crystallogr 2010;66:486-501.
27. Chen VB, Arendall WB, III, Headd JJ, Keedy DA, Immormino RM, Kapral GJ, Murray LW, Richardson JS, Richardson DC. MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr D Biol Crystallogr 2010;66:12-21.
28. Krissinel E, Henrick KJ. Inference of macromolecular assemblies from crystalline state. J Mol Biol 2007;372:774-797.
29. DeLano WL. The PyMOL molecular graphics system. San Carlos, CA: DeLano Scientific, 2002.
30. Costas M, Rodríguez-Larrea D, de Maria L, Borchert T, Gómez-Puyou A, Sánchez-Ruiz JM. Between species variation in the kinetic stability of TIM proteins linked to solvation-barrier free energies. J Mol Biol 2009;385:924-937.
31. Rodríguez-Larrea D, Minning S, Borchert TV, Sanchez-Ruiz JM. Role of solvation barriers in protein kinetic stability. J Mol Biol 2006;360:715-724.
32. Daar IO, Artymiuk PJ, Phillips DC, Maquat LE. Human triose-phosphate isomerase deficiency: a single amino acid subsitution results in a thermolabile enzyme. Proc Natl Acad Sci USA 1986;83:7903-7907.
33. Repiso A, Boren J, Ortega F, Pujades A, Centelles J, Vives-Corrons JL, Climent F, Cascante M, Carreras J. Triosephosphate isomerase deficiency: genetic, enzymatic and metabolic characterization of a new case from Spain. Haematologica 2002;87:ECR12.
34. Sánchez-Ruíz JM. Theoretical analysis of the Lumry-Eyring models in differential scanning calorimetry. Biophys J 1992;61:921-935.
35. Myers JK, Pace CN, Scholtz JM. Denaturant m values and heat capacity changes in accessible surface areas of protein folding. Protein Sci 1995;4:2138-2148.
36. Robertson AD, Murphy KP. Protein structure and the energetics of protein stability. Chem Rev 1997;97:1251-1268.
37. Axe DD. Extreme functional sensitivity in conservative amino acid changes on enzyme exteriors. J Mol Biol 2000;301:585-596.
38. Yanofsky C, Horn V, Thorpe D. Protein structure relationships revealed by mutational analysis. Science 1964;146:1593-1594.
39. Davis BH, Poon AFY, Whitlock MC. Compensatory mutations are repeatable and clustered within proteins. Proc R Soc B 2009;276:1823-1827.
40. Poon A, Davis BH, Chao L. The coupon collector and the suppressor mutation: estimating the number of compensatory mutations by maximum likelihood. Genetics 2005;170:1323-1332.
41. Oria-Hernandez J, Rivero-Rosas H, Ramírez-Silva L. Dichotomic phylogenetic tree of the pyruvate kinase family: K+-dependent and -independent enzymes. J Biol Chem 2006;281:30717-30724.
42. Garza-Ramos G, Cabrera N, Saavedra-Lira E, Tuena de Gómez-Puyou M, Ostoa-Saloma P, Pérez-Montfort R, Gómez Puyou A. Sulfhydryl reagent susceptibility in proteins with high sequence similarity. Triosephosphate isomerase from Tripanosoma brucei, Tripanosoma cruzi and Leishmania mexicana. Eur J Biochem 1998;253:684-691.
43. 8 barrels: catalytic migration from triosephosphate isomerase to thiamine phosphate synthase. J Mol Biol 2012;416:255-270.
44. Gilles HM. Protozoan diseases. New York: Oxford University Press; 1999.
45. Sanchez-Ruiz JM. On promiscuity, changing environments and the possibility of replaying the molecular tape of life. Biochem J 2012;445:e1-e3.
46. Breen S, Kemena C, Vlasov PK, Notredame C, Kondrashov FA. Epistasis as the primary factor en molecular evolution. Nature 2012;490:533-538.