Stabilization of multimeric enzymes: Strategies to prevent subunit dissociation

Enzyme and Microbial Technology

Volumn 45, Issue 6-7, 2009, Pages 405-418

  Fernandez Lafuente, Roberto ^a  

^a INSTITUTO DE CATÁLISIS Y PETROLEOQUÍMICA   (Spain)

Author keywords

Glyoxyl supports; Heterofunctional supports; Intersubunit disulfide bonds; Modeling the subunit subunit interface; Stabilization of multimeric enzymes

Indexed keywords

GLYOXYL SUPPORTS; HETEROFUNCTIONAL SUPPORTS; INTERSUBUNIT DISULFIDE BONDS; MODELING THE SUBUNIT-SUBUNIT INTERFACE; STABILIZATION OF MULTIMERIC ENZYMES;

CATALYSTS; CROSSLINKING; DISSOCIATION; ENZYME IMMOBILIZATION; STABILIZATION;

ENZYMES;

ADSORPTION; BIOCATALYST; COVALENT BOND; CROSS LINKING; DISSOCIATION; DISULFIDE BOND; ENZYME IMMOBILIZATION; ENZYME INACTIVATION; ENZYME STABILITY; ENZYME STRUCTURE; ENZYME SUBUNIT; INDUSTRIAL PRODUCTION; NONHUMAN; PH; PRESSURE; PROTEIN ENGINEERING; REVIEW;

EID: 70349782241     PISSN: 01410229     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.enzmictec.2009.08.009     Document Type: Review

References (162)

1. Matsuda T., Yamanaka R., and Nakamura K. Recent progress in biocatalysis for asymmetric oxidation and reduction. Tetrahedron Asymmetry 20 (2009) 513-557
2. Tao J., and Xu J.-H. Biocatalysis in development of green pharmaceutical processes. Curr Opin Chem Biol 13 (2009) 43-50
3. Woodley J.M. New opportunities for biocatalysis: making pharmaceutical processes greener. Trends Biotechnol 26 (2008) 321-327
4. Shanmugam K.T., and Ingram L.O. Engineering biocatalysts for production of commodity chemicals. J Mol Microbiol Biotechnol 15 (2008) 8-15
5. Patel R.N. Synthesis of chiral pharmaceutical intermediates by biocatalysis. Coord Chem Rev 252 (2008) 659-701
6. Chen Z., Liu J., and Tao J. Biocatalysis for green chemistry and drug development. Prog Chem 19 (2007) 1919-1927
7. Chen Y., and Wu X. Biocatalysis in drug discovery and development. Prog Chem 19 (2007) 1947-1954
8. Pollard D.J., and Woodley J.M. Biocatalysis for pharmaceutical intermediates: the future is now. Trends Biotechnol 25 (2007) 66-73
9. Robles-Medina A., González-Moreno P.A., Esteban-Cerdán L., and Molina-Grima E. Biocatalysis: towards ever greener biodiesel production. Biotechnol Adv 27 (2009) 398-408
10. Salis A., Pinna M., Monduzzi M., and Solinas V. Biodiesel production from triolein and short chain alcohols through biocatalysis. J Biotechnol 119 (2005) 291-299
11. Kumar R., Singh S., and Singh O.V. Bioconversion of lignocellulosic biomass: biochemical and molecular perspectives. J Ind Microbiol Biotechnol 35 (2008) 377-391
12. Bayer E.A., Lamed R., and Himmel M.E. The potential of cellulases and cellulosomes for cellulosic waste management. Curr Opin Biotechnol 18 (2007) 237-245
13. Zhang Y.-H.P., and Lynd L.R. Toward an aggregated understanding of enzymatic hydrolysis of cellulose: noncomplexed cellulase systems. Biotechnol Bioeng 88 (2004) 797-824
14. Akoh C.C., Chang S.-W., Lee G.-C., and Shaw J.-F. Biocatalysis for the production of industrial products and functional foods from rice and other agricultural produce. J Agric Food Chem 56 (2008) 10445-10451
15. Aravindan R., Anbumathi P., and Viruthagiri T. Lipase applications in food industry. Ind J Biotechnol 6 (2007) 141-158
16. Longo M.A., and Sanromán M.A. Production of food aroma compounds: microbial and enzymatic methodologies. Food Technol Biotechnol 44 (2006) 335-353
17. Greiner R., and Konietzny U. Phytase for food application. Food Technol Biotechnol 44 (2006) 125-140
18. Polizzi K.M., Bommarius A.S., Broering J.M., and Chaparro-Riggers J.F. Stability of biocatalysts. Curr Opin Chem Biol 11 (2007) 220-225
19. Iyer P.V., and Ananthanarayan L. Enzyme stability and stabilization-aqueous and non-aqueous environment. Process Biochem 43 (2008) 1019-1032
20. Ó'Fágáin C. Enzyme stabilization-recent experimental progress. Enzyme Microb Technol 33 (2003) 137-149
21. Gershenson A., and Arnold F.H. Enzyme stabilization by directed evolution. Gen Eng 22 (2000) 55-76
22. Wong S.S., and Wong L.-J.C. Chemical crosslinking and the stabilization of proteins and enzymes. Enzyme Microb Technol 14 (1992) 866-874
23. Poltorak O.M., Chukhray E.S., and Torshin I.Y. Dissociative thermal inactivation, stability, and activity of oligomeric enzymes. Biochemistry (Moscow) 63 (1998) 303-311
24. Lencki R.W., Arul J., and Neufeld R.J. Effect of subunit dissociation, denaturation, aggregation, coagulation, and decomposition on enzyme inactivation kinetics: II. Biphasic and grace period behaviour. Biotechnol Bioeng 40 (1992) 1427-1434
25. Poltorak O.M., Chukhrai E.S., and Torshin I.Y. On the influence of interprotein contacts on the active centers and catalytic properties of oligomeric enzymes. Russ J Phys Chem A 74 (2000) S400-S410
26. Barzegar A., Moosavi-Movahedi A.A., Pedersen J.Z., and Miroliaei M. Comparative thermostability of mesophilic and thermophilic alcohol dehydrogenases: stability-determining roles of proline residues and loop conformations. Enzyme Microb Technol 45 (2009) 73-79
27. Carbone V., Hara A., and El-Kabbani O. Structural and functional features of dimeric dihydrodiol dehydrogenase. Cell Mol Life Sci 65 (2008) 1464-1474
28. Lokanath N.K., Shiromizu I., Ohshima N., Nodake Y., Sugahara M., Yokoyama S., et al. Structure of aldolase from Thermus thermophilus HB8 showing the contribution of oligomeric state to thermostability. Acta Cryst Section D: Biol Cryst 60 (2004) 1816-1823
29. Miteva M., Alexov E., and Atanasov B. Numerical simulation of aldolase tetramer stability. Eur Biophys J 28 (1998) 67-73
30. Kumar A.K., and Goswami P. Dissociation and reconstitution studies of a broad substrate specific multimeric alcohol oxidase protein produced by Aspergillus terreus. J Biochem 145 (2009) 259-265
31. Ozimek P., Veenhuis M., and Van Der Klei I.J. Alcohol oxidase: a complex peroxisomal, oligomeric flavoprotein. FEMS Yeast Res 5 (2005) 975-983
32. Prakash K., Prajapati S., Ahmad A., Jain S.K., and Bhakuni V. Unique oligomeric intermediates of bovine liver catalase. Prot Sci 11 (2002) 46-57
33. Bravo J., Verdaguer N., Tormo J., Betzel C., Switala J., Loewen P.C., et al. Crystal structure of catalase HPII from Escherichia coli. Structure 3 (1995) 491-502
34. Matthews B.W. The structure of E. coli β-galactosidase. Comptes Rendus - Biologies 328 (2005) 549-556
35. Becerra M., Cerdán E., and Siso M.I.G. Micro-scale purification of β-galactosidase from Kluyveromyces lactis reveals that dimeric and tetrameric forms are active. Biotechnol Tech 12 (1998) 253-256
36. Ahern T.J., and Klibanov A.M. The mechanism of irreversible enzyme inactivation at 100 °C. Science 228 (1985) 1280-1284
37. Klibanov A.M. Stabilization of enzymes against thermal inactivation. Adv Appl Microbiol 29 (1983) 1-28
38. Poltorak O.M., Chukhrai E.S., Kozlenkov A.A., Chaplin M.F., and Trevan M.D. The putative common mechanism for inactivation of alkaline phosphatase isoenzymes. J Mol Catal B: Enzym 7 (1999) 157-163
39. Pilipenko O.S., Atyaksheva L.F., Poltorak O.M., and Chukhrai E.S. Dissociation and catalytic activity of oligomer forms of β-galactosidases. Russ J Phys Chem A 81 (2007) 990-994
40. Jaenicke R., and Bohm G. The stability of proteins in extreme environments. Curr Opin Struct Biol 8 (1998) 738-748
41. Villeret V., Clantin B., Tricot C., Legrain C., Roovers M., Stalon V., et al. The crystal structure of Pyrococcus furiosus ornithine carbamoyltransferase reveals a key role for oligomerization in enzyme stability at extremely high temperatures. Proc Natl Acad Sci USA 95 (1998) 2801-2806
42. Sterner R., Kleemann G.R., Szadkowski H., Lustig A., Hennig M., and Kirschner K. Phosphoribosyl anthranilate isomerase from Thermotoga maritima is an extremely stable and active homodimer. Prot Sci 5 (1996) 2000-2008
43. Tanaka H., Chinami M., Mizushima T., Ogasahara K., Ota M., Tsukihara T., et al. X-ray crystalline structures of pyrrolidone carboxyl peptidase from a hyperthermophile, Pyrococcus furiosus, and its Cys-free mutant. J Biochem 130 (2001) 107-118
44. Ogasahara K., Ishida M., and Yutani K. Stimulated interaction between α and β subunits of tryptophan synthase from hyperthermophile enhances its thermal stability. J Biol Chem 278 (2003) 8922-8928
45. Eijsink V.G.H., Bjørk A., Gåseidnes S., Sirevåg R., Synstad B., Burg B.V.D., et al. Rational engineering of enzyme stability. J Biotechnol 113 (2004) 105-120
46. 2+ on enzyme stability. J Mol Catal B: Enzym 55 (2008) 142-145
47. Katchalski-Katzir E. Immobilized enzymes-learning from past successes and failures. Trends Biotechnol 11 (1993) 471-478
48. Cao L. Immobilised enzymes: science or art?. Curr Opin Chem Biol 9 (2005) 217-226
49. D'Souza S.F. Immobilized enzymes in bioprocess. Curr Sci 77 (1999) 69-79
50. Taka J., Ogasahara K., Jeyakanthan J., Kunishima N., Kuroishi C., Sugahara M., et al. Stabilization due to dimer formation of phosphoribosyl anthranilate isomerase from Thermus thermophilus HB8: X-ray analysis and DSC experiments. J Biochem 137 (2005) 569-578
51. Bolivar J.M., Wilson L., Ferrarotti S.A., Fernandez-Lafuente R., Guisan J.M., and Mateo C. Stabilization of a formate dehydrogenase by covalent immobilization on highly activated glyoxyl-agarose supports. Biomacromolecules 7 (2006) 669-673
52. Bolivar J.M., Cava F., Mateo C., Rocha-Martín J., Guisán J.M., Berenguer J., et al. Immobilization-stabilization of a new recombinant glutamate dehydrogenase from Thermus thermophilus. Appl Microbiol Biotechnol 80 (2008) 49-58
53. Bolivar J.M., Wilson L., Ferrarotti S.A., Guisán J.M., Fernández-Lafuente R., and Mateo C. Improvement of the stability of alcohol dehydrogenase by covalent immobilization on glyoxyl-agarose. J Biotechnol 125 (2006) 85-94
54. Balny C. High pressure and protein oligomeric dissociation. High Pressure Res 22 (2002) 737-741
55. Jaenicke R. Protein stability and molecular adaption to extreme conditions. Eur J Biochem 202 (1991) 715-728
56. Hei D.J., and Clark D.S. Pressure stabilization of proteins from extreme thermophiles. Appl Environ Microbiol 60 (1994) 932-939
57. Michels P.C., Hei D., and Clark D.S. Pressure effects on enzyme activity and stability at high temperatures. Adv Prot Chem 48 (1996) 341-376
58. Sun M.M.C., Tolliday N., Vetriani C., Robb F.T., and Clark D.S. Pressure-induced thermostabilization of glutamate dehydrogenase from the hyperthermophile Pyrococcus furiosus. Prot Sci 8 (1999) 1056-1063
59. Chang H.-C., Chou W.-Y., and Chang G.-G. Effect of metal binding on the structural stability of pigeon liver malic enzyme. J Biol Chem 277 (2002) 4663-4671
60. Grießler R., Pickl M., D'Auria S., Tanfani F., and Nidetzky B. Oxyanion-mediated protein stabilization: differential roles of phosphate for preventing inactivation of bacterial α-glucan phosphorylases. Biocat Biotrans 19 (2001) 379-398
61. Atyaksheva L.F., Poltorak O.M., and Chukhrai E.S. The effect of the pH value on the thermal stability of bacterial β-galactosidase. Russ J Phys Chem A 76 (2002) 1364-1367
62. Voget C.E., Flores M.V., Faloci M.M., and Ertola R.J.J. Effects of the ionic environment on the stability of Kluyveromyces lactis β-galactosidase. LWT Food Sci Technol 27 (1994) 324-330
63. Ullmann A., and Monod J. On the effect of divalent cations and protein concentration upon renaturation of β-galactosidase from E. coli. Biochem Biophys Res Commun 35 (1969) 35-42
64. Penzol G. Design of biochemical tools for the molecular Engineering of immobilized derivatives of rennin and β-galactosidases. Doctoral dissertation. Universidad Complutense de Madrid; 1996.
65. Yeon Woo Ryu, and Ryu D.D.Y. Semisynthetic β-lactam antibiotics synthesizing enzyme from Acetobacter turbidans: purification and properties. Enzyme Microb Technol 9 (1987) 339-344
66. Fernández-Lafuente R., Hernández-Jústiz O., Mateo C., Terreni M., Fernández-Lorente G., Moreno M.A., et al. Biotransformations catalyzed by multimeric enzymes: stabilization of tetrameric ampicillin acylase permits the optimization of ampicillin synthesis under dissociation conditions. Biomacromolecules 2 (2001) 95-104
67. Heller M., Carpenter J.F., and Randolph T.W. Effects of phase separating systems on lyophilized hemoglobin. J Pharm Sci 85 (1996) 1358-1362
68. Timasheff S.N. Control of protein stability and reactions by weakly interacting cosolvents: the simplicity of the complicated. Adv Protein Chem 51 (1998) 355-432
69. Anchordoquy T.J., Izutsu K.-I., Randolph T.W., and Carpenter J.F. Maintenance of quaternary structure in the frozen state stabilizes lactate dehydrogenase during freeze-drying. Arch Biochem Biophys 390 (2001) 35-41
70. Jaenicke R., and Lilie H. Folding and association of oligomeric and multimeric proteins. Adv Protein Chem 53 (2000) 329-401
71. Singleton M., Isupov M., and Littlechild J. X-ray structure of pyrrolidone carboxyl peptidase from the hyperthermophilic archaeon Thermococcus litoralis. Structure 7 (1999) 237-244
72. Kabashima T., Li Y., Kanada N., Ito K., and Yoshimoto T. Enhancement of the thermal stability of pyroglutamyl peptidase I by introduction of an intersubunit disulfide bond. Biochim Biophys Acta: Prot Str Mol Enzym 1547 (2001) 214-220
73. Tamura A., Kojima S., Miura K., and Sturtevant J.M. Effect of an intersubunit disulfide bond on the stability of Streptomyces subtilisin inhibitor. Biochemistry 33 (1994) 14512-14520
74. Gokhale R.S., Agarwalla S., Francis V.S., Santi D.V., and Balaram P. Thermal stabilization of thymidylate synthase by engineering two disulfide bridges across the dimer interface. J Mol Biol 235 (1994) 89-94
75. Velanker S.S., Gokhale R.S., Ray S.S., Gopal B., Parthasarathy S., Santi D.V., et al. Disulfide engineering at the dimer interface of Lactobacillus casei thymidylate synthase: crystal structure of the T155C/E188C/C244T mutant. Prot Sci 8 (1999) 930-933
76. Cunningham A., Watson D.C., and Yaguchi M. Thermostabilization of the Bacillus circulans xylanase by the introduction of disulfide bonds. Prot Eng 7 (1994) 1379-1386
77. Iwakura M., and Honda S. Stability and reversibility of thermal denaturation are greatly improved by limiting terminal flexibility of Escherichia coli dihydrofolate reductase. J Biochem (Tokyo) 119 (1996) 414-420
78. Heikoop J.C., van den Boogaart P., Mulders J.W., and Grootenhuis P.D. Structure-based design and protein engineering of intersubunit disulfide bonds in gonadotropins. Nat Biotechnol 15 (1997) 658-662
79. Dalhus B., Saarinen M., Sauer U.H., Eklund P., Johansson K., Karlsson A., et al. Structural basis for thermophilic protein stability: structures of thermophilic and mesophilic malate dehydrogenases. J Mol Biol 318 (2002) 707-721
80. Bjørk A., Dalhus B., Mantzilas D., Eijsink V.G.H., and Sirevaåg R. Stabilization of a tetrameric malate dehydrogenase by introduction of a disulfide bridge at the dimer-dimer interface. J Mol Biol 334 (2003) 811-821
81. Reznik G.O., Vajda S., Smith C.L., Cantor C.R., and Sano T. Streptavidins with intersubunit crosslinks have enhanced stability. Nat Biotechnol 14 (1996) 1007-1011
82. Nordlund H.R., Laitinen O.H., Uotila S.T.H., Nyholm T., Hytönen V.P., Slotte J.P., et al. Enhancing the thermal stability of avidin: introduction of disulfide bridges between subunit interfaces. J Biol Chem 278 (2003) 2479-2483
83. Das M., Kobayashi M., Yamada Y., Sreeramulu S., Ramakrishnan C., Wakatsuki S., et al. Design of disulfide-linked thioredoxin dimers and multimers through analysis of crystal contacts. J Mol Biol 372 (2007) 1278-1292
84. Ahern T.J., Casal J.I., Petsko G.A., and Klibanov A.M. Control of oligomeric enzyme thermostability by protein engineering. Proc Natl Acad Sci USA 84 (1987) 675-679
85. Peimbert M., Domínguez-Ramírez L., and Fernández-Velasco D.A. Hydrophobic repacking of the dimer interface of triosephosphate isomerase by in silico design and directed evolution. Biochemistry 47 (2008) 5556-5564
86. Williams J.C., Zeelen J.P., Neubauer G., Vriend G., Backmann J., Michels P.A., et al. Structural and mutagenesis studies of Leishmania triosephosphate isomerase: a point mutation can convert a mesophilic enzyme into a superstable enzyme without losing catalytic power. Prot Eng 12 (1999) 243-250
87. Waldburger C.D., Schildbach J.F., and Sauer R.T. Are buried salt bridges important for protein stability and conformational specificity?. Nat Struct Biol 2 (1995) 122-128
88. Waldburger C.D., Jonsson T., and Sauer R.T. Barriers to protein folding: formation of buried polar interactions is a slow step in acquisition of structure. Proc Natl Acad Sci USA 93 (1996) 2629-2634
89. Bjørk A., Dalhus B., Mantzilas D., Sirevg R., and Eijsink V.G.H. Large improvement in the thermal stability of a tetrameric malate dehydrogenase by single point mutations at the dimer-dimer interface. J Mol Biol 341 (2004) 1215-1226
90. Lebbink J.H.G., Knapp S., Van Der Oost J., Rice D., Ladenstein R., and De Vos W.M. Engineering activity and stability of Thermotoga maritima glutamate dehydrogenase. II: construction of a 16-residue ion-pair network at the subunit interface. J Mol Biol 289 (1999) 357-369
91. Bogin O., Levin I., Hacham Y., Tel-Or S., Peretz M., Frolow F., et al. Structural basis for the enhanced thermal stability of alcohol dehydrogenase mutants from the mesophilic bacterium Clostridium beijerinckii: contribution of salt bridging. Prot Sci 11 (2002) 2561-2574
92. Gerk L.P., Leven O., and Muller-Hill B. Strengthening the dimerisation interface of Lac repressor increases its thermostability by 40 °C. J Mol Biol 299 (2000) 805-812
93. Goihberg E., Dym O., Tel-Or S., Shimon L., Frolow F., Peretz M., et al. Thermal stabilization of the protozoan Entamoeba histolytica alcohol dehydrogenase by a single proline substitution. Proteins 72 (2008) 711-719
94. Griessler R., Schwarz A., Mucha J., and Nidetzky B. Tracking interactions that stabilize the dimer structure of starch phosphorylase from Corynebactorium callunae: roles of Arg234 and Arg242 revealed by sequence analysis and site-directed mutagenesis. Eur J Biochem 270 (2003) 2126-2136
95. Pauly H.E., and Pfleiderer G. Conformation and functional aspects of the reversible dissociation and denaturation of glucose dehydrogenase. Biochemistry 16 (1977) 4599-4604
96. Makino Y., Negoro S., Urabe I., and Okada H. Stability-increasing mutants of glucose dehydrogenase from Bacillus megaterium IWG3. J Biol Chem 264 (1989) 6381-6385
97. Nagao T., Makino Y., Yamamoto K., Urabe I., and Okada H. Stability-increasing mutants of glucose dehydrogenase. FEBS Lett 253 (1989) 113-116
98. Baik S.-H., Ide T., Yoshida H., Kagami O., and Harayama S. Significantly enhanced stability of glucose dehydrogenase by directed evolution. Appl Microbiol Biotechnol 61 (2003) 329-335
99. Baik S.-H., Michel F., Aghajari N., Haser R., and Harayama S. Cooperative effect of two surface amino acid mutations (Q252L and E170K) in glucose dehydrogenase from Bacillus megaterium IWG3 on stabilization of its oligomeric state. Appl Envir Microbiol 71 (2005) 3285-3293
100. Bolivar J.M., Rocha-Martin J., Mateo C., Cava F., Berenguer J., Fernandez-Lafuente R., et al. Coating of soluble and immobilized enzymes with ionic polymers: full stabilization of the quaternary structure of multimeric enzymes. Biomacromolecules 10 (2009) 742-747
101. Andersson M.M., and Hatti-Kaul R. Protein stabilising effect of polyethyleneimine. J Biotechnol 72 (1999) 21-31
102. Bryjak J. Storage stabilization of enzyme activity by poly(ethyleneimine). Bioproc Eng 13 (1995) 177-181
103. Andersson M.M., Breccia J.D., and Hatti-Kaul R. Stabilizing effect of chemical additives against oxidation of lactate dehydrogenase. Biotechnol Appl Biochem 32 (2000) 145-153
104. Torchilin V.P., and Trubetskoy V.S. Stabilization of subunit enzymes by intramolecular crosslinking with bifunctional reagents. Ann N Y Acad Sci 434 (1984) 27-30
105. Fernandez-Lafuente R., Rosell C.M., Rodriguez V., and Guisan J.M. Strategies for enzyme stabilization by intramolecular crosslinking with bifunctional reagents. Enzyme Microb Technol 17 (1995) 517-523
106. Nakajima N., and Ikada Y. Mechanism of amide formation by carbodiimide for bioconjugation in aqueous media. Bioconjug Chem 6 (1995) 123-130
107. Matyash L.F., Ogloblina O.G., and Stepanov V.M. Modification of carboxyl groups in pepsin. Eur J Biochem 35 (1973) 540-545
108. Migneault I., Dartiguenave C., Bertrand M.J., and Waldron K.C. Glutaraldehyde: behavior in aqueous solution, reaction with proteins, and application to enzyme crosslinking. BioTechniques 37 (2004) 790-802
109. Wine Y., Cohen-Hadar N., Freeman A., and Frolow F. Elucidation of the mechanism and end products of glutaraldehyde crosslinking reaction by X-ray structure analysis. Biotechnol Bioengin 98 (2007) 711-718
110. Torchilin V.P., Trubetskoy V.S., Omel'Yanenko V.G., and Martinek K. Stabilization of subunit enzyme by intersubunit crosslinking with bifunctional reagents: studies with glyceraldehyde-3-phosphate dehydrogenase. J Mol Catal 19 (1983) 291-301
111. Kaplan O., and Bakir U. The effect of chemical crosslinking of invertase with dimethyl suberimidate on its pH stability. World J Microbiol Biotechnol 14 (1998) 277-280
112. Cheon Y.-H., Kim G.-J., and Kim H.-S. Stabilization of d-hydantoinase by intersubunit cross-linking. J Mol Catal B: Enzym 11 (2000) 29-35
113. Yamazaki T., Tsugawa W., and Sode K. Increased thermal stability of glucose dehydrogenase by cross-linking chemical modification. Biotechnol Lett 21 (1999) 199-202
114. Fuentes M., Segura R.L., Abian O., Betancor L., Hidalgo A., Mateo C., et al. Determination of protein-protein interactions through aldehyde-dextran intermolecular cross-linking. Proteomics 4 (2004) 2602-2607
115. Fuentes M., Pessela B.C.C., Mateo C., Palomo J.M., Batalla P., Fernández-Lafuente R., et al. Adsorption behavior of bovine serum albumin on lowly activated anionic exchangers suggests a new strategy for solid-phase proteomics. Biomacromolecules 7 (2006) 1357-1361
116. Fuentes M., Mateo C., Pessela B.C.C., Guisán J.M., and Fernandez-Lafuente R. Purification, stabilization, and concentration of very weak protein-protein complexes: shifting the association equilibrium via complex selective adsorption on lowly activated supports. Proteomics 5 (2005) 4062-4069
117. Fuentes M., Pessela B.C.C., Mateo C., Munilla R., Guisán J.M., and Fernandez-Lafuente R. Detection and purification of two antibody-antigen complexes via selective adsorption on lowly activated anion exchangers. J Chromatogr A 1059 (2004) 89-94
118. Fuentes M., Mateo C., Pessela B.C.C., Batalla P., Fernandez-Lafuente R., and Guisán J.M. Solid phase proteomics: dramatic reinforcement of very weak protein-protein interactions. J Chromatogr B 849 (2007) 243-250
119. Mateo C., Palomo J.M., Fernandez-Lorente G., Guisan J.M., and Fernandez-Lafuente R. Improvement of enzyme activity, stability and selectivity via immobilization techniques. Enzyme Microb Technol 40 (2007) 1451-1463
120. Johansson A.C., and Mosbach K. Acrylic copolymers as matrices for the immobilization of enzymes. I. Covalent binding or entrapping of various enzymes to bead formed acrylic copolymers. Biochim Biophys Acta 370 (1974) 339-347
121. Pollak A., Blumenfeld H., Wax M., Baughn R.L., and Whitesides G.M. Enzyme immobilization by condensation copolymerization into cross-linked polyacrylamide gels. J Am Chem Soc 12 (1980) 6324-6336
122. Kennedy J.F., Kalogerakis B., and Cabral J.M.S. Surface immobilization and entrapping of enzymes on glutaraldehyde crosslinked gelatin particles. Enzyme Microb Technol 6 (1984) 127-131
123. Imai K., Shiomi T., Uchida K., and Miya M. Immobilization of enzyme into poly(vinyl alcohol) membrane. Biotechnol Bioeng 28 (1986) 1721-1726
124. Kokufuta E. Novel applications for stimulus-sensitive polymer gels in the preparation of functional immobilized biocatalysts. Adv Polym Sci 110 (1993) 157-177
125. Roy J.J., and Abraham T.E. Strategies in making cross-linked enzyme crystals. Chem Rev 104 (2004) 3705-3721
126. Govardhan C.P. Crosslinking of enzymes for improved stability and performance. Curr Opin Biotechnol 10 (1999) 331-335
127. ®s): stable and recyclable biocatalysts. Biochem Soc Trans 35 (2007) 1583-1587
128. Cao L., Van Rantwijk F., and Sheldon R.A. Cross-linked enzyme aggregates: a simple and effective method for the immobilization of penicillin acylase. Org Lett 2 (2000) 1361-1364
129. Mateo C., Chmura A., Rustler S., Van Rantwijk F., Stolz A., and Sheldon R.A. Synthesis of enantiomerically pure (S)-mandelic acid using an oxynitrilase-nitrilase bienzymatic cascade: a nitrilase surprisingly shows nitrile hydratase activity. Tetrahedron Asymmetry 17 (2006) 320-323
130. Mateo C., Fernandes B., Van Rantwijk F., Stolz A., and Sheldon R.A. Stabilisation of oxygen-labile nitrilases via co-aggregation with poly(ethyleneimine). J Mol Catal B: Enzym 38 (2006) 154-157
131. Wilson L., Illanes A., Abián O., Pessela B.C.C., Fernández-Lafuente R., and Guisán J.M. Co-aggregation of penicillin G acylase and polyionic polymers: an easy methodology to prepare enzyme biocatalysts stable in organic media. Biomacromolecules 5 (2004) 852-857
132. Wilson L., Betancor L., Fernández-Lorente G., Fuentes M., Hidalgo A., Guisán J.M., et al. Cross-linked aggregates of multimeric enzymes: a simple and efficient methodology to stabilize their quaternary structure. Biomacromolecules 5 (2004) 814-817
133. Yoshimoto M., Sakamoto H., Yoshimoto N., Kuboi R., and Nakao K. Stabilization of quaternary structure and activity of bovine liver catalase through encapsulation in liposomes. Enzyme Microb Technol 41 (2007) 849-858
134. Yoshimoto M., Sakamoto H., and Shirakami H. Covalent conjugation of tetrameric bovine liver catalase to liposome membranes for stabilization of the enzyme tertiary and quaternary structures. Coll Surf B: Biointerf 69 (2009) 281-287
135. Fuentes M., Batalla P., Grazu V., Pessela B.C.C., Mateo C., Montes T., et al. Mixed ion exchange supports as useful ion exchangers for protein purification: purification of penicillin G acylase from Escherichia coli. Biomacromolecules 8 (2007) 703-707
136. Pessela B.C.C., Mateo C., Filho M., Carrascosa A., Fernández-Lafuente R., and Guisan J.M. Selective adsorption of large proteins on highly activated IMAC supports in the presence of high imidazole concentrations: purification, reversible immobilization and stabilization of thermophilic α- and β-galactosidases. Enzyme Microb Technol 40 (2007) 242-248
137. Pessela B.C.C., Fuentes M., Mateo C., Munilla R., Carrascosa A.V., Fernandez-Lafuente R., et al. Purification and very strong reversible immobilization of large proteins on anionic exchangers by controlling the support and the immobilization conditions. Enzyme Microb Technol 39 (2006) 909-915
138. Pessela B.C.C., Munilla R., Betancor L., Fuentes M., Carrascosa A.V., Vian A., et al. Ion exchange using poorly activated supports, an easy way for purification of large proteins). J Chromatogr A 1034 (2004) 155-159
139. Fuentes M., Pessela B.C.C., Maquiese J.V., Ortiz C., Segura R.L., Palomo J.M., et al. Reversible and strong immobilization of proteins by ionic exchange on supports coated with sulfate-dextran. Biotechnol Prog 20 (2004) 1134-1139
140. Grunwald P., Freder R., and Gunsser W. Application of polyethylene imine as carrier material for enzyme immobilization. Naturwissenschaften 68 (1981) 525-527
141. Pessela B.C.C., Betancor L., Lopez-Gallego F., Torres R., Dellamora-Ortiz G.M., Alonso-Morales N., et al. Increasing the binding strength of proteins to PEI coated supports by immobilizing at high ionic strength. Enzyme Microb Technol 37 (2005) 295-299
142. Montes T., Grazú V., López-Gallego F., Hermoso J.A., García J.L., Manso I., et al. Genetic modification of the penicillin G acylase surface to improve its reversible immobilization on ionic exchangers. Appl Environ Microbiol 73 (2007) 312-319
143. Filho M., Pessela B.C., Mateo C., Carrascosa A.V., Fernandez-Lafuente R., and Guisán J.M. Reversible immobilization of a hexameric α-galactosidase from Thermus sp. strain T2 on polymeric ionic exchangers. Process Biochem 43 (2008) 1142-1146
144. Pessela B.C.C., Fernández-Lafuente R., Fuentes M., Vián A., García J.L., Carrascosa A.V., et al. Reversible immobilization of a thermophilic β-galactosidase via ionic adsorption on PEI-coated Sepabeads. Enzyme Microb Technol 32 (2003) 369-374
145. Mateo C., Abian O., Fernandez-Lafuente R., and Guisan J.M. Reversible enzyme immobilization via a very strong and nondistorting ionic adsorption on support-polyethylenimine composites. Biotechnol Bioeng 68 (2000) 98-105
146. Bolivar J.M., Wilson L., Ferrarotti S.A., Fernandez-Lafuente R., Guisan J.M., and Mateo C. Evaluation of different immobilization strategies to prepare an industrial biocatalyst of formate dehydrogenase from Candida boidinii. Enzyme Microb Technol 40 (2007) 540-546
147. Lopez-Gallego F., Betancor L., Hidalgo A., Dellamora-Ortiz G., Mateo C., Fernández-Lafuente R., et al. Stabilization of different alcohol oxidases via immobilization and post immobilization techniques. Enzyme Microb Technol 40 (2007) 278-284
148. Torres R., Mateo C., Fuentes M., Palomo J.M., Ortiz C., Fernández-Lafuente R., et al. Reversible immobilization of invertase on Sepabeads coated with polyethyleneimine: optimization of the biocatalyst's stability. Biotechnol Prog 18 (2002) 1221-1226
149. Mateo C., Palomo J.M., Fuentes M., Betancor L., Grazu V., López-Gallego F., et al. Glyoxyl agarose: a fully inert and hydrophilic support for immobilization and high stabilization of proteins. Enzyme Microb Technol 39 (2006) 274-280
150. Mateo C., Abian O., Bernedo M., Cuenca E., Fuentes M., Fernandez-Lorente G., et al. Some special features of glyoxyl supports to immobilize proteins. Enzyme Microb Technol 37 (2005) 456-462
151. Mateo C., Grazú V., Pessela B.C.C., Montes T., Palomo J.M., Torres R., et al. Advances in the design of new epoxy supports for enzyme immobilization-stabilization. Biochem Soc Trans 35 (2007) 1593-1601
152. Turkova J., Blaha K., and Malanikova M. Methacrylate gels with epoxide groups as supports for immobilization of enzymes in pH range 3-12. Biochim Biophys Acta 524 (1978) 162-169
153. Grazu V., Betancor L., Montes T., Lopez-Gallego F., Guisan J.M., and Fernandez-Lafuente R. Glyoxyl agarose as a new chromatographic matrix. Enzyme Microb Technol 38 (2006) 960-966
154. Pedroche J., del Mar Yust M., Mateo C., Fernández-Lafuente R., Girón-Calle J., Alaiz M., et al. Effect of the support and experimental conditions in the intensity of the multipoint covalent attachment of proteins on glyoxyl-agarose supports: correlation between enzyme-support linkages and thermal stability. Enzyme Microb Technol 40 (2007) 1160-1166
155. Bolivar J.M., Rocha-Martin J., Mateo C., Cava F., Berenguer J., Vega D., et al. Purification and stabilization of a glutamate dehygrogenase from Thermus thermophilus via oriented multisubunit plus multipoint covalent immobilization. J Mol Catal B: Enzym 58 (2009) 158-163
156. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227 (1970) 680-685
157. Bolivar J.M., Mateo C., Rocha-Martin J., Cava F., Berenguer J., Fernandez-Lafuente R., et al. The adsorption of multimeric enzymes on very lowly activated supports involves more enzyme subunits: stabilization of a glutamate dehydrogenase from Thermus thermophilus by immobilization on heterofunctional supports. Enzyme Microb Technol 44 (2009) 139-144
158. Fernández-Lafuente R., Rodríguez V., Mateo C., Penzol G., Hernández-Justiz O., Irazoqui G., et al. Stabilization of multimeric enzymes via immobilization and post-immobilization techniques. J Mol Catal B: Enzym 7 (1999) 181-189
159. Hidalgo A., Betancor L., Lopez-Gallego F., Moreno R., Berenguer J., Fernández-Lafuente R., et al. Design of an immobilized preparation of catalase from Thermus thermophilus to be used in a wide range of conditions: structural stabilization of a multimeric enzyme. Enzyme Microb Technol 33 (2003) 278-285
160. Betancor L., Hidalgo A., Fernández-Lorente G., Mateo C., Fernández-Lafuente R., and Guisan J.M. Preparation of a stable biocatalyst of bovine liver catalase using immobilization and postimmobilization techniques. Biotechnol Prog 19 (2003) 763-767
161. Pessela B.C., Mateo C., Filho M., Carrascosa A.V., Fernandez-Lafuente R., and Guisán J.M. Stabilization of the quaternary structure of a hexameric alpha-galactosidase from Thermus sp. T2 by immobilization and post-immobilization techniques. Process Biochem 43 (2008) 193-198
162. Pessela B.C.C., Mateo C., Fuentes M., Vian A., García J.L., Carrascosa A.V., et al. Stabilization of a multimeric β-galactosidase from Thermus sp. Strain T2 by immobilization on novel heterofunctional epoxy supports plus aldehyde-dextran cross-linking. Biotechnol Prog 20 (2004) 388-392