A single proline substitution is critical for the thermostabilization of Clostridium beijerinckii alcohol dehydrogenase

Proteins: Structure, Function and Genetics

Volumn 66, Issue 1, 2007, Pages 196-204

  Goihberg, Edi ^a   Dym, Orly ^a   Tel Or, Shoshana ^a   Levin, Inna ^a   Peretz, Moshe ^a   Burstein, Yigal ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

Alcohol dehydrogenase; Entamoeba histolytica; Proline; Site directed mutagenesis; Thermostability; Three dimensional structure

Indexed keywords

ALCOHOL DEHYDROGENASE; GLYCINE; HISTIDINE; PROLINE;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ARTICLE; CIRCULAR DICHROISM; CLOSTRIDIUM; CLOSTRIDIUM BIEJERINCKII; CRYSTALLIZATION; ENTAMOEBA HISTOLYTICA; HEATING; HYDROPHOBICITY; NONHUMAN; PRIORITY JOURNAL; SIGNAL DETECTION; SITE DIRECTED MUTAGENESIS; STRUCTURE ANALYSIS; THERMOANAEROBACTER; THERMOANAEROBACTER BROCKII; THERMOSTABILITY;

ALCOHOL DEHYDROGENASE; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; CIRCULAR DICHROISM; CLOSTRIDIUM BEIJERINCKII; ENZYME STABILITY; HYDROPHOBICITY; MOLECULAR SEQUENCE DATA; PROLINE; RECOMBINANT PROTEINS; TEMPERATURE;

CLOSTRIDIUM BEIJERINCKII; ENTAMOEBA HISTOLYTICA; THERMOANAEROBACTER BROCKII;

EID: 33845679397     PISSN: 08873585     EISSN: 10970134     Source Type: Journal    
DOI: 10.1002/prot.21170     Document Type: Article

References (53)

1. Chakravarty S, Varadarajan R. Elucidation of determinants of protein stability through genome sequence analysis. FEBS Lett 2000;470:65-69.
2. Kumar S, Tsai CJ, Nussinov R. Factors enhancing protein thermostability. Protein Eng 2000;13:179-191.
3. Lehmann M, Loch C, Middendorf A, Studer D, Lassen SF, Pasamontes L, van Loon AP, Wyss M. The consensus concept for thermostability engineering of proteins: further proof of concept. Protein Eng 2002;15:403-411.
4. Menendez-Arias L, Argos P. Engineering protein thermal stability. Sequence statistics point to residue substitutions in α-helices. J Mol Biol 1989;206:397-406.
5. Bogin O, Peretz M, Hacham Y, Korkhin Y, Frolow F, Kalb AJ, Burstein Y. Enhanced thermal stability of Clostridium beijerinckii alcohol dehydrogenase after strategic substitution of amino acid residues with prolines from the homologous thermophilic Thermoanaerobacter brockii alcohol dehydrogenase. Protein Sci 1998;7: 1156-1163.
6. Chen J, Lu Z, Sakon J, Stites WE. Increasing the thermostability of staphylococcal nuclease: implications for the origin of protein thermostability. J Mol Biol 2000;303:125-130.
7. Gerk LP, Leven O, Muller-Hill B. Strengthening the dimerisation interface of Lac repressor increases its thermostability by 40 deg. C. J Mol Biol 2000;299:805-812.
8. Hasegawa J, Shimahara H, Mizutani M, Uchiyama S, Arai H, Ishii M, Kobayashi Y, Ferguson SJ, Sambongi Y, Igarashi Y. Stabilization of Pseudomonas aeruginosa cytochrome c(551) by systematic amino acid substitutions based on the structure of thermophilic Hydrogenobacter thermophilus cytochrome c(552). J Biol Chem 1999;274:37533-37537.
9. Li WT, Shriver JW, Reeve JN. Mutational analysis of differences in thermostability between histones from mesophilic and hyperthermophilic archaea. J Bacteriol 2000;182:812-817.
10. Perl D, Mueller U, Heinemann U, Schmid FX. Two exposed amino acid residues confer thermostability on a cold shock protein. Nat Struct Biol 2000;7:380-383.
11. Shinoda H, Hattori M, Shimizu A, Samejima T, Satoh T. Hydrophobic interactions of Val75 are critical for oligomeric thermostability of inorganic pyrophosphatase from Bacillus stearothermophilus. J Biochem (Tokyo) 1999;125:58-63.
12. Zhu GP, Xu C, Teng MK, Tao LM, Zhu XY, Wu CJ, Hang J, Niu LW, Wang YZ. Increasing the thermostability of D-xylose isomerase by introduction of a proline into the turn of a random coil. Protein Eng 1999;12:635-638.
13. Jaenicke R. Stability and stabilization of globular proteins in solution. J Biotechnol 2000;79:193-203.
14. Matthews BW, Nicholson H, Becktel WJ. Enhanced protein thermostability from site-directed mutations that decrease the entropy of unfolding. Proc Natl Acad Sci USA 1987;84:6663-6667.
15. Hardy F, Vriend G, Veltman OR, van der Vinne B, Venema G, Eijsink VG. Stabilization of Bacillus stearothermophilus neutral protease by introduction of prolines. FEBS Lett 1993;317(1/2): 89-92.
16. Muslin EH, Clark SE, Henson CA. The effect of proline insertions on the thermostability of a barley α-glucosidase. Protein Eng 2002;15:29-33.
17. Sriprapundh D, Vieille C, Zeikus JG. Molecular determinants of xylose isomerase thermal stability and activity: analysis of thermozymes by site-directed mutagenesis. Protein Eng 2000;13:259-265.
18. Stewart RJ, Varghese JN, Garrett TP, Hoj PB, Fincher GB. Mutant barley (1→3,1→4)-β-glucan endohydrolases with enhanced thermostability. Protein Eng 2001;14:245-253.
19. Watanabe K, Kitamura K, Suzuki Y. Analysis of the critical sites for protein thermostabilization by proline substitution in oligo-1,6-glucosidase from Bacillus coagulans ATCC 7050 and the evolutionary consideration of proline residues. Appl Environ Microbiol 1996;62:2066-2073.
20. Watanabe K, Masuda T, Ohashi H, Mihara H, Suzuki Y. Multiple proline substitutions cumulatively thermostabilize Bacillus cereus ATCC7064 oligo-1,6-glucosidase. Irrefragable proof supporting the proline rule. Eur J Biochem 1994;226:277-283.
21. Bogin O, Peretz M, Burstein Y. Thermoanaerobacter brockii alcohol dehydrogenase: characterization of the active site metal and its ligand amino acids Protein Sci 1997;6:450-458.
22. Ismaiel AA, Zhu CX, Colby GD, Chen JS. Purification and characterization of a primary-secondary alcohol dehydrogenase from two strains of Clostridium beijerinckii. J Bacteriol 1993;175:5097-5105.
23. Kumar A, Shen PS, Descoteaux S, Pohl J, Bailey G, Samuelson J. Cloning and expression of an NADP(+)-dependent alcohol dehydrogenase gene of Entamoeba histolytica. Proc Natl Acad Sci USA 1992;89:10188-10192.
24. Lamed RJ, Zeikus JG. Novel NADP-linked alcohol-aldehyde/ ketone oxidoreductase in thermophilic ethanologenic bacteria. Biochem J 1981;195:183-190.
25. Peretz M, Bogin O, Keinan E, Burstein Y. Stereospecificity of hydrogen transfer by the NADP-linked alcohol dehydrogenase from the thermophilic bacterium Thermoanaerobium brockii. Int J Pept Protein Res 1993;42:490-495.
26. Peretz M, Burstein Y. Amino acid sequence of alcohol dehydrogenase from the thermophilic bacterium Thermoanaerobium brockii. Biochemistry 1989;28:6549-6555.
27. Samuelson J, Zhang WW, Kumar A, Descoteaux S, Shen PS, Bailey G. Primary structures of alcohol and aldehyde dehydrogenase genes of Entamoeba histolytica. Arch Med Res 1992;23:31-33.
28. Peretz M, Bogin O, Tel-Or S, Cohen A, Li G, Chen J-S, Burstein Y. Molecular cloning, nucleotide sequencing, and expression of genes encoding alcohol dehydrogenases from the thermophile Thermoanaerobacter brockii and the mesophile Clostridium beijerinckii. Anaerobe 1997;3:259-270.
29. Shimon LJ, Peretz M, Goihberg E, Burstein Y, Frolow F. Thermophilic alcohol dehydrogenase from the mesophile Entamoeba histolytica: crystallization and preliminary X-ray characterization. Acta Crystallogr D Biol Crystallogr 2002;58 (Part 3):546-548.
30. Bogin O, Levin I, Hacham Y, Tel-Or S, Peretz M, Frolow F, Burstein Y. Structural basis for the enhanced thermal stability of alcohol dehydrogenase mutants from the mesophilic bacterium Clostridium beijerinckii: contribution of salt bridging. Protein Sci 2002;11:2561-2574.
31. Korkhin Y, Kalb AJ, Peretz M, Bogin O, Burstein Y, Frolow F. NADP-dependent bacterial alcohol dehydrogenases: crystal structure, cofactor-binding and cofactor specificity of the ADHs of Clostridium beijerinckii and Thermoanaerobacter brockii. J Mol Biol 1998;278:967-981.
32. Shimon LJW, Goihberg E, Peretz M, Burstein Y, Frolow F. Structure of alcohol dehydrogenase from Entamoeba histolytica. Acta Crystallogr D Biol Crystallogr, 2006;62(Pt5):541-547.
33. Tanaka N, Kusakabe Y, Ito K, Yoshimoto T, Nakamura KT. Crystal structure of formaldehyde dehydrogenase from Pseudomonas putida: the structural origin of the tightly bound cofactor in nicotinoprotein dehydrogenases. J Mol Biol 2002;324:519-533.
34. Esposito L, Sica F, Raia CA, Giordano A, Rossi M, Mazzarella L, Zagari A. Crystal structure of the alcohol dehydrogenase from the hyperthermophilic archaeon Sulfolobus solfataricus at 1.85 A resolution. J Mol Biol 2002;318:463-477.
35. Levin I, Meiri G, Peretz M, Burstein Y, Frolow F. The ternary complex of Pseudomonas aeruginosa alcohol dehydrogenase with NADH and ethylene glycol. Protein Sci 2004;13:1547-1556.
36. Eklund H, Nordstrom B, Zeppezauer E, Soderlund G, Ohlsson I, Boiwe T, Soderberg BO, Tapia O, Branden CI, Akeson A. Three-dimensional structure of horse liver alcohol dehydrogenase at 2-4 A resolution. J Mol Biol 1976;102:27-59.
37. Byrappa S, Gavin DK, Gupta KC. A highly efficient procedure for site-specific mutagenesis of full-length plasmids using Vent DNA polymerase. Genome Res 1995;5:404-407.
38. 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.
39. Sanger F, Coulson AR. A rapid method for determining sequences in DNA by primed synthesis with DNA polymerase. J Mol Biol 1975;94:441-448.
40. Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970;227(5259):680-685.
41. Otwinowski Z, Minor W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol 1997;276:307-326.
42. Storoni LC, McCoy AJ, Read RJ. Likelihood-enhanced fast rotation functions. Acta Crystallogr D Biol Crystallogr 2004;60 (Part 3): 432-438.
43. Brunger AT, Adams PD, Clore GM, DeLano WL, Gros P, Grosse-Kunstleve RW, Jiang JS, Kuszewski J, Nilges M, Pannu NS, Read RJ, Rice LM, Simonson T, Warren GL. Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr D Biol Crystallogr 1998;54 (Part 5): 905-921.
44. Jones TA, Zou JY, Cowan SW, Kjeldgaard M. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr A 1991;47 (Part 2): 110-119.
45. Laskowski RA, MacArthur MW, Moss DS, Thornton JM. PROCHECK: a program to check the stereochemical quality of protein structures. J Appl Cryst 1993;26:283-291.
46. Schimmel PR, Flory PJ. Conformational energies and configurational statistics of copolypeptides containing L-proline. J Mol Biol 1968;34:105-120.
47. Sagermann M, Gay L, Matthews BW. Long-distance conformational changes in a protein engineered by modulated sequence duplication. Proc Natl Acad Sci USA 2003;100:9191-9195.
48. Guy JE, Isupov MN, Littlechild JA. The structure of an alcohol dehydrogenase from the hyperthermophilic archaeon Aeropyrum pernix. J Mol Biol 2003;331:1041-1051.
49. Karplus PA. Hydrophobicity regained. Protein Sci 1997;6:1302-1307.
50. Jackson SE, Moracci M, elMasry N, Johnson CM, Fersht AR. Effect of cavity-creating mutations in the hydrophobic core of chymotrypsin inhibitor 2. Biochemistry 1993;32:11259-11269.
51. Serrano L, Kellis JT, Jr, Cann P, Matouschek A, Fersht AR. The folding of an enzyme. II. Substructure of barnase and the contribution of different interactions to protein stability. J Mol Biol 1992;224:783-804.
52. Magonet E, Hayen P, Delforge D, Delaive E, Remacle J. Importance of the structural zinc atom for the stability of yeast alcohol dehydrogenase. Biochem J 1992;287 (Part 2):361-365.
53. Watanabe S, Kodaki T, Makino K. Complete reversal of coenzyme specificity of xylitol dehydrogenase and increase of thermostability by the introduction of structural zinc. J Biol Chem 2005;280: 10340-10349.