A novel approach for enhancing the catalytic efficiency of a protease at low temperature: Reduction in substrate inhibition by chemical modification

Biotechnology and Bioengineering

Volumn 103, Issue 4, 2009, Pages 676-686

  Siddiqui, Khawar Sohail ^a   Parkin, Don M ^b   Curmi, Paul M G ^a,c   De Francisci, Davide ^a   Poljak, Anne ^a   Barrow, Kevin ^a   Noble, Malcolm H ^a   Trewhella, Jill ^b   Cavicchioli, Ricardo ^a  

^a UNIVERSITY OF NEW SOUTH WALES   (Australia)

^b UNIVERSITY OF SYDNEY   (Australia)

^c ST VINCENT S HOSPITAL   (Australia)

Author keywords

Allostery; Cold adapted; Enzyme kinetics; Enzyme structure; Function and stability; Savinase; SAXS

Indexed keywords

ALLOSTERY; COLD-ADAPTED; ENZYME STRUCTURE; SAVINASE; SAXS;

CHEMICAL MODIFICATION; ENZYME KINETICS; ENZYMES; GLUCOSE; POLYSACCHARIDES; PRODUCTIVITY; SUBSTRATES;

ENZYME INHIBITION;

AZOCASEIN; CASEIN; DEXTRAN; POLYSACCHARIDE; SUBTILISIN; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; CATALYSIS; ENTHALPY; ENZYME INHIBITION; ENZYME KINETICS; ENZYME MODIFICATION; LOW TEMPERATURE; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEIN FOLDING; PSYCHROPHILE; REDUCTION; TEMPERATURE MEASUREMENT; X RAY CRYSTALLOGRAPHY;

CASEINS; CIRCULAR DICHROISM; DEXTRANS; ENZYME ACTIVATION; ENZYME ACTIVATORS; FICOLL; KINETICS; MODELS, MOLECULAR; PROTEIN STRUCTURE, TERTIARY; SCATTERING, SMALL ANGLE; SERINE ENDOPEPTIDASES; TEMPERATURE;

EID: 67650233754     PISSN: 00063592     EISSN: 10970290     Source Type: Journal    
DOI: 10.1002/bit.22300     Document Type: Article

References (56)

1. Argüello MA, Alvarez S, Riera FA, Alvarez R. 2002. Enzymatic cleaning of inorganic ultrafiltration membranes fouled by whey proteins. J Agric Food Chem 50:1951-1958. (Pubitemid 34259994)
2. Bardsley WG, Leff P, Kavanagh J, Waight RD. 1980. Deviations from Michaelis-Menten kinetics. The possibility of complicated curves for simple kinetic schemes and the computer fitting of experimental data for acetylcholinesterase, acid phosphatase, adenosine deaminase, arylsulphatase, benzylamine oxidase, chymotrypsin, fumarase, galactose dehydrogenase, beta-galactosidase, lactate dehydrogenase, peroxidase and xanthine oxidase. Biochem J 187:739-765.
3. Becker S, Palm D, Schinzel R. 1994. Dissecting differential binding in the forward and reverse reaction of Escherichia coli maltodextrin phosphorylase using 2-deoxyglucosyl substrates. J Biol Chem 269:2485-2490.
4. Bode W, Papamokos E, Musil D. 1987. The high-resolution X-ray crystal structure of the complex formed between subtilisin Carlsberg and eglin c, an elastase inhibitor from the leech Hirudo medicinalis. Structural analysis, subtilisin structure and interface geometry. Eur J Biochem 166:673-692.
5. Bonneaux F, Dellacherie E. 1995. Fixation of various aldehydic dextrans onto human hemoglobin: Study of conjugate stability. J Protein Chem 14:1-5.
6. Burton SG, Cowan DA, Woodley JM. 2002. The search for the ideal biocatalyst. Nat Biotechnol 20:37-45.
7. Cavicchioli R, Siddiqui KS, Sowers KR, Andrews D. 2002. Low temperature extremophiles and their applications. Curr Opin Biotechnol 13:253-261. (Pubitemid 35299546)
8. Cavicchioli R, Curmi PMG, Siddiqui KS, Thomas T. 2006. Proteins from psychrophiles. Methods Microbiol 35:395-436.
9. Eschenburg S, Genov N, Peters K, Fittkau S, Stoeva S, Wilson KS, Betzel C. 1998. Crystal structure of subtilisin DY, a random mutant of subtilisin Carlsberg. Eur J Biochem 257:309-318. (Pubitemid 28489475)
10. Feller G, Gerday C. 2003. Psychrophilic enzymes: Hot topics in cold adaptation. Nat Microbiol Rev 1:200-208.
11. Fox RJ, Davis SC, Mundorff EC, Newman LM, Gavrilovic V, Ma SK, Chung LM, Ching C, Tam S, Muley S, Grate J, Gruber J, Whitman JC, Sheldon RA, Huisman GW. 2007. Improving catalytic function by ProSAR-driven enzyme evolution. Nat Biotechnol 25:338-344. (Pubitemid 46398768)
12. Fritz G, Bergmann A, Glatter O. 2000. Evaluation of small-angle scattering data of charged particles using the Generalised Indirect Fourier Transformation (GIFT) technique. J Chem Phys 113:9733-9740. (Pubitemid 32085154)
13. Goody NM, Benkovic SJ. 2008. Allosteric regulation and catalysis emerge via a common route. Nat Chem Biol 4:474-482. (Pubitemid 352019763)
14. Gunasekaran K,Ma B, Nussinov R. 2004. Is allostery an intrinsic property of all dynamic proteins? Proteins 57:433-443.
15. Gupta R, Beg QK, Lorenz P. 2002. Bacterial alkaline proteases: Molecular approaches and industrial applications. Appl Microbiol Biotechnol 59:15-32. (Pubitemid 34809671)
16. Hardy JA, Wells JA. 2004. Searching for new allosteric sites in enzymes. Curr Opin Stuct Biol 14:706-715. (Pubitemid 39592582)
17. Jain SC, Shinde U, Li Y, Inouye M, Berman HM. 1998. The crystal structure of an autoprocessed Ser221Cys-subtilisin E-propeptide complex at 2.0 A resolution. J Mol Biol 284:137-144. (Pubitemid 28524002)
18. Jeffries CM, Whitten AE, Harris SP, Trewhella J. 2008. Small-angle X-ray scattering reveals the N-terminal domain organization of myosin binding protein C. J Mol Biol 377:1186-1199.
19. Kato G, Tan E, Yung J. 1972. Acetylcholinesterase. Kinetic studies on the mechanism of atropine inhibition. J Biol Chem 247:3186-3189.
20. Kazan D, Ertan H, Erarslan A. 1997. Stabilization of Escherichia coli penicillin G acylase against thermal inactivation by cross-linking with dextran dialdehyde polymers. Appl Microbiol Biotechnol 48:191-197. (Pubitemid 27394749)
21. Mahmoud YA, El Souod SM, Niehaus WG. 1995. Purification and characterization of malate dehydrogenase from Cryptococcus neoformans. Arch Biochem Biophys 322:69-75.
22. Marcus CJ, Geller AM, Byrne WL. 1973. Studies on bovine hepatic fructose 1,6-diphosphatase. Substrate inhibition and the kinetic mechanism. J Biol Chem 248:8567-8573.
23. Margesin R, Schinner F. 1999. Biotechnological applications of coldadapted organisms. Heidelberg: Springer-Verlag.
24. Marx JC, Collins T, D'Amico S, Feller G, Gerday C. 2007. Cold-adapted enzymes from marine Antarctic microorganisms. Mar Biotechnol 9: 293-304. (Pubitemid 46878654)
25. Mateo C, Monti R, Pessela BC, Fuentes M, Torres R, Guisán JM, Fernández-Lafuente R. 2004a. Immobilization of lactase from Kluyveromyces lactis greatly reduces the inhibition promoted by glucose. Full hydrolysis of lactose in milk. Biotechnol Prog 20:1259-1262.
26. Mateo C, Palomo JM, van Langen LM, van Rantwijk F, Sheldon RA. 2004b. A new, mild cross-linking methodology to prepare cross-linked enzyme aggregates. Biotechnol Bioeng 86:273-276. (Pubitemid 38560355)
27. Mozhaev VV. 1993. Mechanism-based strategies for protein thermostabilization. Trends Biotechnol 11:88-95.
28. Niday E, Wang C-S, Alaupovic P. 1980. Kinetic evidence for the allosteric substrate inhibition of human erythrocyte acetylcholinesterase. Biochim Biophys Acta 612:67-72. (Pubitemid 10121825)
29. Radisky ES, Koshland DE, Jr. 2002. A clogged gutter mechanism for protease inhibitors. Proc Natl Acad Sci USA 99:10316-10321. (Pubitemid 34906973)
30. Rao MB, Tanksale AM, Ghatge MS, Deshpande VV. 1998. Molecular and biotechnological aspects of microbial proteases. Microbiol Mol Biol Rev 62:597-635. (Pubitemid 28415546)
31. Russell AJ, Klibanov AM. 1988. Inhibitor-induced enzyme activation in organic solvents. J Biol Chem 263:11624-11626.
32. Saeki K, Ozaki K, Kobayashi T, Ito S. 2007. Detergent alkaline proteases: Enzymatic properties, genes, and crystal structures. J Biosci Bioeng 103: 501-508. (Pubitemid 47043544)
33. Sangeetha K, Abraham TE. 2008. Preparation and characterization of cross-linked enzyme aggregates (CLEA) of subtilisin for controlled release applications. Int J Biol Macromol 43:314-319.
34. Siddiqui KS, Cavicchioli R. 2005. Improved thermal stability and activity in the cold-adapted lipase B from Candida antarctica following chemical modification with oxidized polysaccharides. Extremophiles 9:471-476.
35. Siddiqui KS, Cavicchioli R. 2006. Cold-adapted enzymes. Annu Rev Biochem 75:403-433.
36. Siddiqui KS, Cavicchioli R, Thomas T. 2002. Thermodynamic activation properties of elongation factor 2 (EF-2) proteins from psychrotolerant and thermophilic Archaea. Extremophiles 6:143-150. (Pubitemid 41490482)
37. Siddiqui KS, Poljak A, Cavicchioli R. 2004. Improved activity and stability of alkaline phosphatases from psychrophilic and mesophilic organisms by chemically modifying aliphatic or amino groups using tetracarboxy- benzophenone derivatives. Cell Mol Biol 50:657-667.
38. Siddiqui KS, Poljak A, Guilhaus M, Feller G, D'Amico S, Gerday C, Cavicchioli R. 2005. The role of disulphide-bridges in the activity and stability of a cold-active a-amylase. J Bacteriol 187:6206-6212. (Pubitemid 41262817)
39. Siddiqui KS, Poljak A, Guilhaus M, De Francisci D, Curmi PM, Feller G, D'Amico S, Gerday C, Uversky VN, Cavicchioli R. 2006. Role of lysine versus arginine in enzyme cold-adaptation: Modifying lysine to homoarginine stabilizes the cold-adapted alpha-amylase from Pseudoalteramonas haloplanktis. Proteins 64:486-501.
40. Siezen RJ, Leunissen JAM. 1997. Subtilases: The superfamily of subtilisinlike serine proteases. Protein Sci 6:501-523. (Pubitemid 27120048)
41. Srimathi S, Jayaraman G, Narayanan PR. 2006. Improved thermodynamic stability of subtilisin Carlsberg by covalent modification. Enzyme Microb Technol 39:301-307.
42. Sundaram PV, Venkatesh R. 1998. Retardation of thermal and urea induced inactivation of alpha-chymotrypsin by modification with carbohydrate polymers. Protein Eng 11:699-705. (Pubitemid 28389161)
43. Svergun DI. 1992. Determination of the regularization parameter in indirect-transform methods using perceptual criteria. J Appl Cryst 25:495-503.
44. Svergun DI. 1999. Restoring low resolution structure of biological macromolecules from solution scattering using simulated annealing. Biophys J 76:2879-2886.
45. Svergun DI, Barberato C, Koch MHJ. 1995. CRYSOL - A program to evaluate X-ray solution scattering of biological macromolecules from atomic coordinates. J Appl Cryst 28:768-773. (Pubitemid 3014671)
46. Taguchi S, Ozaki A, Nonaka T, Mitsui Y, Momose H. 1999. A cold-adapted protease engineered by experimental evolution system. J Biochem (Tokyo) 126:689-693. (Pubitemid 29500388)
47. Taguchi S, Komada S, Momose H. 2000. The complete amino acid substitutions at position 131 that are positively involved in cold adaptation of subtilisin BPN. Appl Environ Microbiol 66:1410-1415. (Pubitemid 30185610)
48. Tindbaek N, Svendsen A, Oestergaard PR, Draborg H. 2004. Engineering a substrate-specific cold-adapted subtilisin. Protein Eng Des Sel 17:149-156.
49. Vazquez SC, Rios Merino LN, MacCormack WP, Fraile ER. 1995. Protease-producing psychrotrophic bacteria isolated from Antarctica. Polar Biol 15:131-135.
50. Venkatesh R, Sundaram PV. 1998. Modulation of stability properties of bovine trypsin after in vitro structural changes with a variety of chemical modifiers. Protein Eng 11:691-698. (Pubitemid 28389160)
51. Volkov VV, Svergun DI. 2003. Uniqueness of ab initio shape determination in small-angle scattering. J Appl Cryst 36:860-864.
52. Wakabayashi M, Fishman WH. 1961. The comparative ability of β-glucuronidase preparations (liver, Escherichia coli, Helix pomatia, and Patella vulgata) to hydrolyze certain steroid glucosiduronic acids. J Biol Chem 236:996-1001.
53. Walker JM. 2002. The protein protocols handbook. New Jersey: Humana Press. p. 1146.
54. Wang C-S. 1997. Inhibition of human erythrocyte lactate dehydrogenase by high concentrations of pyruvate. Eur J Biochem 78:569-574.
55. Wintrode PL, Miyazaki K, Arnold FH. 2000. Cold adaptation of a mesophilic subtilisin-like protease by laboratory evolution. J Biol Chem 275: 31635-31640. (Pubitemid 30782037)
56. Wu Y, Eigenbrot C, Liang WC, Stawicki S, Shia S, Fan B, Ganesan R, Lipari MT, Kirchhofer D. 2007. Structural insight into distinct mechanisms of protease inhibition by antibodies. Proc Natl Acad Sci USA 104: 19784-19789.