Molecular adaptation strategies to high temperature and thermal denaturation mechanism of the D-trehalose/D-maltose-binding protein from the hyperthermophilic archaeon Thermococcus litoralis

Proteins: Structure, Function and Genetics

Volumn 67, Issue 4, 2007, Pages 1002-1009

  Fessas, Dimitrios ^a   Staiano, Maria ^b   Barbiroli, Alberto ^a   Marabotti, Anna ^c   Schiraldi, Alberto ^a   Varriale, Antonio ^b   Rossi, Mose' ^b   D'Auria, Sabato ^b  

^a UNIVERSITY OF MILAN   (Italy)

^b INSTITUTE OF PROTEIN BIOCHEMISTRY   (Italy)

^c CNR   (Italy)

Author keywords

Archaeon; Differential scanning calorimetry; Periplasmic protein; Trehalose maltose binding protein

Indexed keywords

ABC TRANSPORTER; BINDING PROTEIN; DEXTRO TREHALOSE DEXTRO MALTOSE BINDING PROTEIN; RECOMBINANT PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; DENATURATION; ESCHERICHIA COLI; HYPERTHERMOPHILIC ARCHAEON; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PURIFICATION; PROTEIN STABILITY; PROTEIN STRUCTURE; TEMPERATURE ACCLIMATIZATION; THERMOCOCCUS;

ADAPTATION, BIOLOGICAL; CALORIMETRY, DIFFERENTIAL SCANNING; CARRIER PROTEINS; CRYSTALLOGRAPHY, X-RAY; MODELS, MOLECULAR; PROTEIN DENATURATION; PROTEIN STRUCTURE, TERTIARY; TEMPERATURE; THERMOCOCCUS; TREHALOSE;

ARCHAEA; THERMOCOCCUS LITORALIS;

EID: 34248551438     PISSN: 08873585     EISSN: 10970134     Source Type: Journal    
DOI: 10.1002/prot.21383     Document Type: Article

References (43)

1. Brock TD. Life at high temperatures. Science 1985;239:132-138.
2. Jaenicke R.Studies on hyperstable proteins: crystallins from the eye-lens and enzymes from thermophilic bacteria. In: Doniach S, editor. Statistical mechanics, protein structure, and protein substrate interactions. New York: Plenum; 1994. pp 49-62.
3. D'Auria S, Moracci M, Febbraio F, Tanfani F, Nucci R, Rossi M. Structure-function studies on β-glycosidase from Sulfolobus solfataricus. Molecular bases of thermostability. Biochimie 1998;80: 949-957.
4. Xavier KB, Martins LO, Peist R, Kossmann M, Boos W, Santos H. High-affinity maltose/trehalose transport system in the hyperthermophilic archaeon Thermococcus litoralis. J Bacteriol 1996; 178:4773-4777.
5. Diez J, Diederichs K, Greller G, Horlacher R, Boos W, Welte W. The crystal structure of a liganded trehalose/maltose-binding protein from the hyperthermophilic archaeon Thermococcus litoralis at 1.85 A. J Mol Biol 2001;305:905-915.
6. Sun YJ, Rose J, Wang BC, Hsiao CD. The structure of glutamine-binding protein complexed with glutamine at 1.94 angstrom resolution: comparisons with other amino acid binding proteins. J Mol Biol 1998;278:219-229.
7. Horlacher R, Xavier KB, Santos H, DiRuggiero J, Kossmann M, Boos W. Archaeal binding protein-dependent ABC transporter: molecular and biochemical analysis of the trehalose/maltose transport system of the hyperthermophilic archaeon Thermococcus litoralis. J Bacteriol 1998;180:680-689.
8. Herman P, Staiano M, Marabotti A, Varriale A Scire' A, Tanfani F, Vecer J, Rossi M D'Auria S. D-Trehalose/D-Maltose-binding protein from the hyperthermophilic archaeon Thermococcus litoralis: the binding of trehalose and maltose results in different protein conformational states. Proteins 2006;63:754-767.
9. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976;72:248-254.
10. Barone G, Del Vecchio P, Fessas D, Giancola C, Graziano G. THESEUS: a new software package for the handling and analysis of thermal denaturation data of biological macromolecules. J Therm Anal 1992;38:2779-2790.
11. Freire E, Biltonen RL. Statistical mechanical deconvolution of thermal transitions in macromolecules. I. Theory and application to homogeneous systems. Biopolymers 1978;17:463-479.
12. Press WH, Flannery BP, Teukolsky SA, Vetterling WT. Numerical Recipes. Cambridge: Cambridge University Press; 1989.
13. Berman H, Henrick K, Nakamura H. Announcing the worldwide Protein Data Bank. Nat Struct Biol 2003;10:980.
14. Facchiano AM, Colonna G, Ragone R. Helix stabilizing factors and stabilization of thermophilic proteins: an X-ray based study. Protein Eng 1998;11:753-760.
15. Marabotti A, D'Auria S, Rossi M, Facchiano AM. Theoretical model of the three-dimensional structure of a sugar-binding protein from Pyrococcus horikoshii: structural analysis and sugar-binding simulations. Biochem J 2004;380:677-684.
16. Vogt G, Woell S, Argos P. Protein thermal stability, hydrogen bonds and ion pairs. J Mol Biol 1997;269:631-643.
17. Kumar S, Nussinov R. Salt bridge stability in monomelic proteins. J Mol Biol 1999;293:1241-1255.
18. Evdokimov AG, Anderson DE, Routzahn KM, Waugh DS. Structural basis for oligosaccharide recognition by Pyrococcus furiosus maltodextrin-binding protein. J Mol Biol 2001;305:891-904.
19. Aguilar CF, Sanderson I, Moracci M, Ciaramella M, Nucci R, Rossi M, Pearl LH. Crystal structure of the β-glycosidase from the hyperthermophilic archaeon Sulfolobus solfataricus: resilience as a key factor in thermostability. J Mol Biol 1997;271:789-802.
20. Hubbard SJ, Campbell SF, Thornton JM. Molecular recognition. Conformational analysis of limited proteolytic sites and serine proteinase protein inhibitors. J Mol Biol 1991;220:507-530.
21. Sanchez-Ruiz JM, Makhatadze GI. To charge or not to charge? Trends Biotechnol 2001;19:132-135.
22. Loladze W, Ibarra-Molero B, Sanchez-Ruiz JM, Makhatadze GI. Engineering a thermostable protein via optimization of charge-charge interactions on the protein surface. Biochemistry 1999;38:16419-16423.
23. Grimsley GR, Shaw KL, Fee LR, Alston RW, Huyghues-Despointes BM, Thurlkill RL, Scholtz JM, Pace CN. Increasing protein stability by altering long-range coulombic interactions. Protein Sci 1999;8:1843-1849.
24. Spector S, Wang M, Carp SA, Robblee J, Hendsch ZS, Fairman R, Tidor B, Raleigh DP. Rational modification of protein stability by the mutation of charged surface residues. Biochemistry 2000;39: 872-879.
25. Perl D, Mueller U, Heinemann U, Schmid FX. Two exposed amino acid residues confer thermostability on a cold shock protein. Nat Struct Biol 2000;7:373-380.
26. Barone G, Catanzano F, Del Vecchio P, Fessas D, Giancola C, Graziano G. The effect of pH on thermal stability of globular proteins: a critical insight. J Therm Anal 1994;42:383-395.
27. Giancola C, De Sena C, Fessas D, Graziano G, Barone G. DSC studies on bovine serum albumin denaturation. Effects of ionic strength and SDS concentration. Int J Biol Macromol 1997;20: 193-204.
28. Pollegioni L, Iametti S, Fessas D, Caldinelli L, Piubelli L, Barbiroli A, Pilone MS, Bonomi F. Contribution of the dimeric state to the thermal stability of the flavoprotein D-amino acid oxidase. Protein Sci 2003;12:1018-1029.
29. Caldinelli L, Iametti S, Barbiroli A, Bonomi F, Fessas D, Molla G, Pilone MS, Pollegioni L. Dissecting the structural determinants of the stability of cholesterol oxidase containing covalently bound flavin. J Biol Chem 2005;280:22572-22581.
30. Lumry R, Eyring H. Conformation changes of proteins. J Phys Chem 1954;58:110-120.
31. Sanchez-Ruiz J. Theoretical analysis of Lumry-Eyring models in differential scanning calorimetry. Biophys J 1992;61:921-935.
32. D'Auria S, Barone R, Rossi M, Nucci R, Barone G, Fessas D, Bertoli E, Tanfani F. Effects of temperature and SDS on the structure of β-glycosidase from the thermophilic archaeon Sulfolobus solfataricus. Biochem J 1997;323:833-840.
33. Schiraldi A, Piazza L, Fessas D, Riva M. Thermal analyses in foods and food processes. In: Kemp R, editor. Handbook of thermal analysis; 1999. pp 829-921.
34. Edge V, Allewell NM, Sturtevant JM. High-resolution differential scanning calorimetric analysis of the subunits of Escherichia coli aspartate transcarbamoylase. Biochemistry 1985;24:5899-5906.
35. Klibanov AM, Ahern TJ. Thermal stability of proteins. In: Oxender DL and Fox CF editors. Protein engineering. New York: Liss; 1987. pp 213-218.
36. Manly SP, Matthews KS, Sturtevant JM. Thermal denaturation of the core protein of lac repressor. Biochemistry 1985;24:3842-3846.
37. Fessas D, Iametti S, Schiraldi A, Bonomi F. Thermal unfolding of monomeric and dimeric β-lactoglobulins. Eur J Biochem 2001; 268:5439-5448.
38. Barone G, Del Vecchio P, Fessas D, Giancola C, Graziano G. Denaturation of biological macromolecules: new programs for the deconvolution of DSC measurements. In: Russo N, Anastassopoulou J, Barone G editors. Chemistry and properties of biomolecular systems. Amsterdam: Kluwer; 1994. pp 67-78.
39. Shrake A, Ross PD. Origins and consequences of ligand-induced multiphasic thermal protein denaturation. Biopolymers 1992; 32:925-940.
40. Barone G Del Vecchio P, Fessas D, Giancola C, Graziano G, Riccio A. Ligand-induced biphasic thermal denaturation of RNAase A. J Thermal Anal 1994;41:1263-1276.
41. Rees DC, Robertson AD. Some thermodynamic implications for the thermostability of proteins. Protein Sci 2001;10:1187-1194.
42. Ragone R. Phenomenological similarities between protein denaturation and small-molecule dissolution: insights into the mechanism driving the thermal resistance of globular proteins. Proteins: Struct Funct Bioinformat 2004;54:323-332.
43. Kumar S, Nussinov R. Experiment-guided thermodynamic simulations on reversible two-state proteins: implications for protein thermostability. Biophys Chem 2004;111:235-246.