Computational design of Candida boidinii xylose reductase for altered cofactor specificity

Protein Science

Volumn 18, Issue 10, 2009, Pages 2125-2138

  Khoury, George A ^a   Fazelinia, Hossein ^a   Chin, Jonathan W ^a   Pantazes, Robert J ^a   Cirino, Patrick C ^a   Maranas, Costas D ^a  

^a The Center for Nanotechnology Education and Utilization   (United States)

Author keywords

Cofactor specificity; Cofactor switching; Computational protein design; IPRO; Nicotinamide; Protein engineering; Xylitol

Indexed keywords

OXIDOREDUCTASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; XYLOSE;

ARTICLE; BINDING AFFINITY; BINDING SITE; CANDIDA BOIDINII; COMPUTER SYSTEM; ENERGY; ENZYME ACTIVITY; HUMAN; HYDROPHOBICITY; MUTATION; NONHUMAN; PREDICTION; PRIORITY JOURNAL;

ALDEHYDE REDUCTASE; BINDING SITES; CANDIDA; COENZYMES; COMPUTATIONAL BIOLOGY; MUTAGENESIS, SITE-DIRECTED; MUTATION; NAD; NADP; SUBSTRATE SPECIFICITY;

CANDIDA BOIDINII;

EID: 70349463121     PISSN: 09618368     EISSN: 1469896X     Source Type: Journal    
DOI: 10.1002/pro.227     Document Type: Article

References (90)

1. Looger LL, Dwyer MA, Smith JJ, Hellinga HW (2003) Computational design of receptor and sensor proteins with novel functions. Nature 423:185-190.
2. Kortemme T, Baker D (2004) Computational design of protein-protein interactions. Curr Opin Chem Biol 8:91-97.
3. Ashworth J, Havranek JJ, Duarte CM, Sussman D, Monnat RJ, Stoddard BL, Baker D (2006)Computational redesign of endonuclease DNA binding and cleavage specificity. Nature 441:656-659 (Pubitemid 43927299)
4. Dahiyat BI, Mayo SL (1997) De novo protein design: fully automated sequence selection. Science 278:82-87. (Pubitemid 27446279)
5. Kuhlman B, Dantas G, Ireton GC, Varani G, Stoddard BL, Baker D (2003) Design of a novel globular protein fold with atomic-level accuracy. Science 302:1364-1368. (Pubitemid 37452172)
6. Jiang L, Althoff EA, Clemente FR, Doyle L, Rothlisberger D, Zanghellini A, Gallaher JL, Betker JL, Tanaka F, Barbas CF, Hilvert D, Houk KN, Stoddard BL, Baker D (2008) De novo computational design of retro-aldol enzymes. Science 319:1387-1391. (Pubitemid 351354873)
7. Rothlisberger D, Khersonsky O, Wollacott AM, Jiang L, Dechancie J, Betker J, Gallaher JL, Althoff EA, Zanghellini A, Dym O, Albeck S, Houk KN, Tawfik DS, Baker D (2008) Kemp elimination catalysts by computational enzyme design. Nature 453:190-195. (Pubitemid 351667979)
8. Varadarajan N, Gam J, Olsen MJ, Georgiou G, Iverson BL (2005) Engineering of protease variants exhibiting high catalytic activity and exquisite substrate selectivity. Proc Natl Acad Sci USA 102:6855-6880. (Pubitemid 40675406)
9. Korkegian A, Black ME, Baker D, Stoddard BL (2005) Computational thermostabilization of an enzyme. Science 308:857-860.
10. Johannes TW, Woodyer RD, Zhao H (2005) Directed evolution of a thermostable phosphite dehydrogenase for NAD(P)H regeneration. Appl Environ Microbiol 71:5728-5734.
11. Mclachlan MJ, Johannes TW, Zhao H (2008) Further improvement of phosphite dehydrogenase thermostability by saturation mutagenesis. Biotechnol Bioeng 99:268-274.
12. Hasty J, Mcmillen D, Collins JJ (2002) Engineered gene circuits. Nature 420:224-230.
13. Vercillo NC, Herald KJ, Fox JM, Der BS, Dattelbaum JD (2007) Analysis of ligand binding to a ribose biosensor using site-directed mutagenesis and fluorescence spectroscopy. Protein Sci 16:362-368.
14. Hellinga HW, Marvin JS (1998) Protein engineering and the development of generic biosensors. Trends Biotechnol 16:183-189.
15. Maier NM, Franco P, Lindner W (2001) Separation of enantiomers: needs, challenges, perspectives. J Chromatogr A 906:3-33. (Pubitemid 32056194)
16. Bolon DN, Mayo SL (2001) Enzyme-like proteins by computational design. Proc Natl Acad Sci USA 98:14274-14279.
17. Zanghellini A, Jiang L, Wollacott AM, Cheng G, Meiler J, Althoff EA, Rothlisberger D, Baker D (2006) New algorithms and an in silico benchmark for computational enzyme design. Protein Sci 15:2785-2794. (Pubitemid 44833759)
18. Chockalingam K, Chen ZL, Katzenellenbogen JA, Zhao HM (2005) Directed evolution of specific receptor-ligand pairs for use in the creation of gene switches. Proc Natl Acad Sci USA 102:5691-5696. (Pubitemid 40559621)
19. Koh JT (2002) Engineering selectivity and discrimination into ligand-receptor interfaces. Chem Biol 9:17-23.
20. Tang SY, Fazelinia H, Cirino PC (2008) AraC regulatory protein mutants with altered effector specificity. J Am Chem Soc 130:5267-5271.
21. Moore GL, Maranas CD (2004) Computational challenges in combinatorial library design for protein engineering. AIChE J 50:262-272. (Pubitemid 38366549)
22. Marohnic CC, Bewley MC, Barber MJ (2003) Engineering and characterization of a NADPH-utilizing cytochrome b5 reductase. Biochemistry 42:11170-11182.
23. Woodyer R, Van Der Donk WA, Zhao H (2003) Relaxing the nicotinamide cofactor specificity of phosphite dehydrogenase by rational design. Biochemistry 42:11604-11614. (Pubitemid 37243620)
24. Watanabe S, Kodaki T, Makino K (2005) Complete reversal of coenzyme specificity of xylitol dehydrogenase and increase of thermostability by the introduction of structural zinc. J Biol Chem 280:10340-10349. (Pubitemid 40403056)
25. Kostrzynska M, Sopher CR, Lee H (1998) Mutational analysis of the role of the conserved lysine-270 in the Pichia stipitis xylose reductase. FEMS Microbiol Lett 159:107-112. (Pubitemid 28051352)
26. Leitgeb S, Petschacher B, Wilson DK, Nidetzky B (2005) Fine tuning of coenzyme specificity in family 2 aldo-keto reductases revealed by crystal structures of the Lys-274->Arg mutant of Candida tenuis xylose reductase (AKR2B5) bound to NAD+ and NADP+. FEBS Lett 579:763-767. (Pubitemid 40163998)
27. Petschacher B, Leitgeb S, Kavanagh KL, Wilson DK, Nidetzky B (2005) The coenzyme specificity of Candida tenuis xylose reductase (AKR2B5) explored by site-directed mutagenesis and x-ray crystallography. Biochem J 385:75-83. (Pubitemid 40164025)
28. Liang L, Zhang J, Lin Z (2007) Altering coenzyme specificity of Pichia stipitis xylose reductase by the semirational approach CASTing. Microb Cell Fact 6:36. (Pubitemid 351167795)
29. Banta S, Swanson BA, Wu S, Jarnagin A, Anderson S (2002) Alteration of the specificity of the cofactor-binding pocket of Corynebacterium 2,5-diketo-D-gluconic acid reductase A. Protein Eng 15:131-140. (Pubitemid 34298357)
30. Banta S, Swanson BA, Wu S, Jarnagin A, Anderson S (2002)Optimizing an artificial metabolic pathway: engineering the cofactor specificity of Corynebacterium 2,5-diketo-D-gluconic acid reductase for use in vitamin C biosynthesis. Biochemistry 41:6226-6236. (Pubitemid 34525986)
31. Scrutton NS, Berry A, Perham RN (1990) Redesign of the coenzyme specificity of a dehydrogenase by protein engineering. Nature 343:38-43. (Pubitemid 20036350)
32. Rane MJ, Calvo KC (1997) Reversal of the nucleotide specificity of ketol acid reductoisomerase by site-directed mutagenesis identifies the NADPH binding site. Arch Biochem Biophys 338:83-89.
33. Shiraishi N, Croy C, Kaur J, Campbell WH (1998) Engineering of pyridine nucleotide specificity of nitrate reductase: mutagenesis of recombinant cytochrome b reductase fragment of Neurospora crassa NADPH:Nitrate reductase. Arch Biochem Biophys 358:104-115. (Pubitemid 28471380)
34. Eppink MH, Overkamp KM, Schreuder HA, Van Berkel WJ (1999) Switch of coenzyme specificity of p-hydroxybenzoate hydroxylase. J Mol Biol 292:87-96.
35. Elmore CL, Porter TD (2002) Modification of the nucleotide cofactor-binding site of cytochrome P-450 reductase to enhance turnover with NADH in Vivo. J Biol Chem 277:48960-48964.
36. Kristan K, Stojan J, Adamski J, Rizner TL (2007) Rational design of novel mutants of fungal 17 betahydroxy steroid dehydrogenase. J Biotechnol 129:123-130. (Pubitemid 46400017)
37. Dambe TR, Kuhn AM, Brossette T, Giffhorn F, Scheidig AJ (2006) Crystal structure of NADP(H)-dependent 1,5- anhydro-D-fructose reductase from Sinorhizobium morelense at 2.2 A resolution: construction of a NADH-accepting mutant and its application in rare sugar synthesis. Biochemistry 45:10030-10042. (Pubitemid 44257397)
38. Medina M, Luquita A, Tejero J, Hermoso J, Mayoral T, Sanz-Aparicio J, Grever K, Gomez-Moreno C (2001) Probing the determinants of coenzyme specificity in ferredoxin- NADP+ reductase by site-directed mutagenesis. J Biol Chem 276:11902-11912. (Pubitemid 37385349)
39. Chen R, Greer A, Dean AM (1995) A highly active decarboxylating dehydrogenase with rationally inverted coenzyme specificity. Proc Natl Acad Sci USA 92:11666-11670. (Pubitemid 26014174)
40. Yaoi T, Miyazaki K, Oshima T, Komukai Y, Go M (1996) Conversion of the coenzyme specificity of isocitrate dehydrogenase by module replacement. J Biochem (Tokyo) 119:1014-1018. (Pubitemid 26182385)
41. Zhang L, Ahvazi B, Szittner R, Vrielink A, Meighen E (1999) Change of nucleotide specificity and enhancement of catalytic efficiency in single point mutants of Vibrio harveyi aldehyde dehydrogenase. Biochemistry 38:11440-11447. (Pubitemid 129516721)
42. Holmberg N, Ryde U, Bulow L (1999) Redesign of the coenzyme specificity in L-lactate dehydrogenase from Bacillus stearothermophilus using site-directed mutagenesis and media engineering. Protein Eng 12:851-856. (Pubitemid 29533109)
43. Barber MJ (2000) Altered pyridine nucleotide specificity of spinach nitrate reductase. FASEB J 14:A1416-A1416.
44. Miller SP, Lunzer M, Dean AM (2006) Direct demonstration of an adaptive constraint. Science 314:458-461.
45. Bernard N, Johnsen K, Holbrook JJ, Delcour J (1995) D175 discriminates between NADH and NADPH in the coenzyme binding site of Lactobacillus delbrueckii subsp. Bulgaricus D-lactate dehydrogenase. Biochem Biophys Res Commun 208:895-900.
46. Clermont S, Corbier C, Mely Y, Gerard D, Wonacott A, Branlant G (1993) Determinants of coenzyme specificity in glyceraldehyde-3-phosphate dehydrogenase: role of the acidic residue in the fingerprint region of the nucleotide binding fold. Biochemistry 32:10178-10184. (Pubitemid 23312448)
47. Ehrensberger AH, Elling RA, Wilson DK (2006) Structure- guided engineering of xylitol dehydrogenase cosubstrate specificity. Structure 14:567-575.
48. Hsieh JY, Liu GY, Chang GG, Hung HC (2006) Determinants of the dual cofactor specificity and substrate cooperativity of the human mitochondrial NAD(P)(+)- dependent malic enzyme-functional roles of glutamine 362. J Biol Chem 281:23237-23245.
49. Serov AE, Popova AS, Fedorchuk VV, Tishkov VI (2002) Engineering of coenzyme specificity of formate dehydrogenase from Saccharomyces cerevisiae. Biochem J 367:841-847.
50. Chen R, Greer A, Dean AM (1996) Redesigning secondary structure to invert coenzyme specificity in isopropylmalate dehydrogenase. Proc Natl Acad Sci USA 93:12171-12176. (Pubitemid 26367114)
51. Galkin A, Kulakova L, Ohshima T, Esaki N, Soda K (1997) Construction of a new leucine dehydrogenase with preferred specificity for NADP+ by site-directed mutagenesis of the strictly NAD+-specific enzyme. Protein Eng 10:687-690. (Pubitemid 27332076)
52. Saraf MC, Moore GL, Goodey NM, Cao VY, Benkovic SJ, Maranas CD (2006) IPRO: an iterative computational protein library redesign and optimization procedure. Biophys J 90:4167-4180.
53. Kavanagh KL, Klimacek M, Nidetzky B, Wilson DK (2003) Structure of xylose reductase bound to NAD+ and the basis for single and dual co-substrate specificity in family 2 aldo-keto reductases. Biochem J 373:319-326. (Pubitemid 36903204)
54. Jez JM, Penning TM (2001) The aldo-keto reductase (AKR) superfamily: an update. Chem Biol Interact 130:499-525.
55. Kavanagh KL, Klimacek M, Nidetzky B, Wilson DK (2002) The structure of apo and holo forms of xylose reductase, a dimeric aldo-keto reductase from Candida tenuis. Biochemistry 41:8785-8795. (Pubitemid 34777683)
56. Kratzer R, Wilson DK, Nidetzky B (2006) Catalytic mechanism and substrate selectivity of aldo-keto reductases: insights from structure-function studies of Candida tenuis xylose reductase. IUBMB Life 58:499-507. (Pubitemid 44470235)
57. Bohren KM, Grimshaw CE, Lai CJ, Harrison DH, Ringe D, Petsko GA, Gabbay KH (1994)Tyrosine-48 is the proton donor and histidine-110 directs substrate stereochemical selectivity in the reduction reaction of human aldose reductase: enzyme kinetics and crystal structure of the Y48H mutant enzyme. Biochemistry 33:2021-2032. (Pubitemid 24099596)
58. Barski OA, Gabbay KH, Grimshaw CE, Bohren KM (1995) Mechanism of human aldehyde reductase: characterization of the active site pocket. Biochemistry 34:11264-11275.
59. Schlegel BP, Jez JM, Penning TM (1998) Mutagenesis of 3 alpha-hydroxysteroid dehydrogenase reveals a "pushpull" mechanism for proton transfer in aldo-keto reductases. Biochemistry 37:3538-3548.
60. Lee JK, Koo BS, Kim SY (2003) Cloning and characterization of the xyl1 gene, encoding an NADH-preferring xylose reductase from Candida parapsilosis, and its functional expression in Candida tropicalis. Appl Environ Microbiol 69:6179-6188.
61. Werpy T, Petersen G, Aden A, Bozell J, Holladay J, White J, Manheim A (2004) Top value added chemicals from biomass, volume I: results of screening for potential candidates from sugars and synthesiss gas.
62. Cirino PC, Chin JW, Ingram LO (2006) Engineering Escherichia coli for xylitol production from glucosexylose mixtures. Biotechnol Bioeng 95:1167-1176. (Pubitemid 44901332)
63. Chin JW, Khankal R, Monroe CA, Maranas CD, Cirino PC (2009) Analysis of NADPH supply during xylitol production by engineered Escherichia coli. Biotechnol Bioeng 102:209-220.
64. Chenault HK, Whitesides GM (1987) Regeneration of nicotinamide cofactors for use in organic synthesis. Appl Biochem Biotechnol 14:147-197.
65. Klein P, Kanehisa M, Delisi C (1984) Prediction of protein function from sequence properties. Discriminant analysis of a data base. Biochim Biophys Acta 787:221-226.
66. Cid H, Bunster M, Canales M, Gazitua F (1992) Hydrophobicity and structural classes in proteins. Protein Eng 5:373-375.
67. Krigbaum WR, Komoriya A (1979) Local interactions as a structure determinant for protein molecules: II. Biochim Biophys Acta 576:204-248.
68. Shindyalov IN, Bourne PE (1998) Protein structure alignment by incremental combinatorial extension (CE) of the optimal path. Protein Eng 11:739-747.
69. Berman HM, Westbrook J, Feng Z, Gilliland G, Bhat TN, Weissig H, Shindyalov IN, Bourne PE (2000) The protein data bank. Nucl Acids Res 28:235-242.
70. Arnold K, Bordoli L, Kopp J, Schwede T (2006) The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics 22:195-201. (Pubitemid 43205406)
71. Schwede T, Kopp J, Guex N, Peitsch MC (2003) SWISS-MODEL: an automated protein homology-modeling server. Nucl Acids Res 31:3381-3385. (Pubitemid 37442164)
72. Petschacher B, Nidetzky B (2005) Engineering Candida tenuis xylose reductase for improved utilization of NADH: antagonistic effects of multiple side chain replacements and performance of site-directed mutants under simulated in vivo conditions. Appl Environ Microbiol 71:6390-6393. (Pubitemid 41456943)
73. Henikoff S, Henikoff JG (1992) Amino acid substitution matrices from protein blocks. Proc Natl Acad Sci USA 89:10915-10919.
74. Jonson PH, Petersen SB (2001) A critical view on conservative mutations. Protein Eng 14:397-402.
75. Brooks BR, Bruccoleri RE, Olafson BD, States DJ, Swaminathan S, Karplus M (1983) Charmm - a program for macromolecular energy, minimization, and dynamics calculations. J Comput Chem 4:187-217.
76. Mackerell J, Brooks AD, Brooks B, Nilsson CL, Roux L, Won B, Karplus Y. CHARMM: the energy function and its parameterization with an overview of the program. In: Schleyer PVR, Allinger NL, Ed. (1998) The encyclopedia of computational chemistry. Chichester: Wiley, pp 271-277.
77. Im W, Lee MS, Brooks CL (2003) Generalized born model with a simple smoothing function. J Comput Chem 24:1691-1702
78. Born M (1920) Volumes and hydration warmth of ions. Z Fur Phys 1:45-48.
79. Lee MS, Salsbury FR, Brooks CL (2002) Novel generalized born methods. J Chem Phys 116:10606-10614.
80. Born M (1920) Der aufbau der materie: dreis aufsätze über moderne atomistik und elektronentheorie. Berlin: Springer, 3, 81, 2113.
81. Carugo O, Argos P (1997) NADP-dependent enzymes. I: conserved stereochemistry of cofactor binding. Proteins 28:10-28.
82. Chen R, Li L, Weng Z (2003) ZDOCK: an initial-stage protein-docking algorithm. Proteins 52:80-87.
83. Fazelinia H, Cirino PC, Maranas CD (2007) Extending iterative protein redesign and optimization (IPRO) in protein library design for ligand specificity. Biophys J 92:2120-2130. (Pubitemid 46495273)
84. Tracewell CA, Arnold FH (2009) Directed enzyme evolution: climbing fitness peaks one amino acid at a time. Curr Opin Chem Biol 13:3-9.
85. Dunbrack RL, Karplus M (1993) Backbone-dependent rotamer library for proteins. Application to side-chain prediction. J Mol Biol 230:543-574. (Pubitemid 23161363)
86. Dunbrack RL, Karplus M (1994) Conformational analysis of the backbone-dependent rotamer preferences of protein sidechains. Nat Struct Biol 1:334-340. (Pubitemid 24974858)
87. Metropolis N, Rosenbluth AW, Rosenbluth MN, Teller AH, Teller E (1953) Equation of state calculations by fast computing machines. J Chem Phys 21:1087-1092.
88. Hacker B, Habenicht A, Kiess M, Mattes R (1999) Xylose utilization: cloning and characterization of the xylose reductase from Candida tenuis. Biol Chem 380:1395-1403 (Pubitemid 30021361)
89. Kang MH, Ni H, Jeffries TW (2003) Molecular characterization of a gene for aldose reductase (CbXYL1) from Candida boidinii and its expression in Saccharomyces cerevisiae. Appl Biochem Biotechnol 105:265-276. (Pubitemid 36535194)
90. An YF, Ji JF, Wu WF, Lv A, Huang RB, Wei YT (2005) A rapid and efficient method for multiple-site mutagenesis with a modified overlap extension PCR. Appl Microbiol Biotechnol 68:774-778.