Prediction of distal residue participation in enzyme catalysis

Protein Science

Volumn 24, Issue 5, 2015, Pages 762-778

  Brodkin, Heather R ^a,b,c   Delateur, Nicholas A ^a,d   Somarowthu, Srinivas ^a,e   Mills, Caitlyn L ^a   Novak, Walter R ^b,f   Beuning, Penny J ^a   Ringe, Dagmar ^b   Ondrechen, Mary Jo ^a  

^a NORTHEASTERN UNIVERSITY   (United States)

^b BRANDEIS UNIVERSITY   (United States)

^c Potenza Therapeutics   (United States)

^d MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^e YALE UNIVERSITY   (United States)

^f WABASH COLLEGE   (United States)

Author keywords

alkaline phosphatase; catalytic efficiency; ketosteroid isomerase; nitrile hydratase; partial order optimum likelihood; phosphoglucose isomerase; remote residues

Indexed keywords

ALKALINE PHOSPHATASE; CARBONATE DEHYDRATASE II; ENZYME; GLUCOSE 6 PHOSPHATE ISOMERASE; MANDELATE RACEMASE; NITRILE HYDRATASE; STEROID DELTA ISOMERASE;

ARTICLE; CATALYSIS; CATALYTIC EFFICIENCY; CLINICAL FEATURE; CONTROLLED STUDY; DISTAL RESIDUE; ENZYME ACTIVE SITE; ENZYME KINETICS; ENZYME SPECIFICITY; ENZYME STRUCTURE; ESCHERICHIA COLI; HUMAN; HYDROGEN BOND; MACHINE LEARNING; PHYLOGENETIC TREE; PREDICTION; PRIORITY JOURNAL; PSEUDOMONAS PUTIDA; SITE DIRECTED MUTAGENESIS; STATIC ELECTRICITY; SURFACE PROPERTY; CHEMISTRY; ENZYMOLOGY; GENETICS; PHYLOGENY; PROTEIN CONFORMATION;

CARBONIC ANHYDRASE II; CATALYSIS; ENZYMES; ESCHERICHIA COLI; GLUCOSE-6-PHOSPHATE ISOMERASE; HUMANS; MACHINE LEARNING; PHYLOGENY; PROTEIN CONFORMATION; PSEUDOMONAS PUTIDA; STATIC ELECTRICITY; SURFACE PROPERTIES;

EID: 84943637672     PISSN: 09618368     EISSN: 1469896X     Source Type: Journal    
DOI: 10.1002/pro.2648     Document Type: Article

References (93)

1. Porter CT, Bartlett GJ, Thornton JM, (2004) The catalytic site atlas: a resource of catalytic sites and residues identified in enzymes using structural data. Nucleic Acids Res 32: D129-D133.
2. Lee J, Goodey NM, (2011) Catalytic contributions from remote regions of enzyme structure. Chem Rev 111: 7595-7624.
3. Tong W, Wei Y, Murga LF, Ondrechen MJ, Williams RJ, (2009) Partial order optimum likelihood (POOL): maximum likelihood prediction of protein active site residues using 3D structure and sequence properties. PLoS Comp Biol 5: e1000266.
4. Somarowthu S, Yang H, Hildebrand DGC, Ondrechen MJ, (2011) High-performance prediction of functional residues in proteins with machine learning and computed input features. Biopolymers 95: 390-400.
5. Ondrechen MJ, Clifton JG, Ringe D, (2001) THEMATICS: a simple computational predictor of enzyme function from structure. Proc Natl Acad Sci USA 98: 12473-12478.
6. Ko J, Murga LF, André P, Yang H, Ondrechen MJ, Williams RJ, Agunwamba A, Budil DE, (2005) Statistical criteria for the identification of protein active sites using theoretical microscopic titration curves. Proteins 59: 183-195.
7. Wei Y, Ko J, Murga L, Ondrechen MJ, (2007) Selective prediction of interaction sites in protein structures with THEMATICS. BMC Bioinform 8: 119.
8. Somarowthu S, Ondrechen MJ, (2012) POOL server: machine learning application for functional site prediction in proteins. Bioinformatics 28: 2078-2079.
9. Hildebrand DGC, Yang H, Ondrechen MJ, Williams RJ, (2010) High conservation of amino acids with anomalous protonation behavior. Curr Bioinform 5: 134-140.
10. Capra JA, Laskowski RA, Thornton JM, Singh M, Funkhouser TA, (2009) Predicting protein ligand binding sites by combining evolutionary sequence conservation and 3D structure. PLoS Comput Biol 5: e1000585.
11. Sankararaman S, Sjolander K, (2008) INTREPID: INformation-theoretic TREe traversal for Protein functional site IDentification. Bioinformatics 24: 2445-2452.
12. Johannes TW, Zhao H, (2006) Directed evolution of enzymes and biosynthetic pathways. Curr Opin Microbiol 9: 261-267.
13. Gould SM, Tawfik DS, (2005) Directed evolution of the promiscuous esterase activity of carbonic anhydrase II. Biochemistry 44: 5444-5452.
14. Hsu C-C, Hong Z, Wada M, Franke D, Wong C-H, (2005) Directed evolution of D-sialic acid aldolase to L-3-deoxy-manno-2-octulosonic acid (L-KDO) aldolase. Proc Natl Acad Sci USA 102: 9122-9126.
15. Oue S, Okamoto A, Yano T, Kagamiyama H, (1999) Redesigning the substrate specificity of an enzyme by cumulative effects of the mutations of non-active site residues. J Biol Chem 274: 2344-2349.
16. van den Heuvel RH, van den Berg WA, Rovida S, van Berkel WJ, (2004) Laboratory-evolved vanillyl-alcohol oxidase produces natural vanillin. J Biol Chem 279: 33492-33500.
17. Tomatis PE, Rasia RM, Segovia L, Vila AJ, (2005) Mimicking natural evolution in metallo-beta-lactamases through second-shell ligand mutations. Proc Natl Acad Sci USA 102: 13761-13766.
18. Xu X, Qin XQ, Kantrowitz ER, (1994) Probing the role of histidine-372 in zinc binding and the catalytic mechanism of Escherichia coli alkaline phosphatase by site-specific mutagenesis. Biochemistry 33: 2279-2284.
19. Hehir MJ, Murphy JE, Kantrowitz ER, (2000) Characterization of heterodimeric alkaline phosphatases from Escherichia coli: an investigation of intragenic complementation. J Mol Biol 304: 645-656.
20. Mandecki W, Shallcross MA, Sowadski J, Tomazic-Allen S, (1991) Mutagenesis of conserved residues within the active site of Escherichia coli alkaline phosphatase yields enzymes with increased kcat. Protein Eng 4: 801-804.
21. Muller BH, Lamoure C, Le Du MH, Cattolico L, Lajeunesse E, Lemaitre F, Pearson A, Ducancel F, Menez A, Boulain JC, (2001) Improving Escherichia coli alkaline phosphatase efficacy by additional mutations inside and outside the catalytic pocket. Chembiochem 2: 517-523.
22. Schafer SL, Barrett WC, Kallarakal AT, Mitra B, Kozarich JW, Gerlt JA, Clifton JG, Petsko GA, Kenyon GL, (1996) Mechanism of the reaction catalyzed by mandelate racemase: structure and mechanistic properties of the D270N mutant. Biochemistry 35: 5662-5669.
23. Brodkin HR, Novak WR, Milne AC, D'Aquino JA, Karabacak NM, Goldberg IG, Agar JN, Payne MS, Petsko GA, Ondrechen MJ, Ringe D, (2011) Evidence of the participation of remote residues in the catalytic activity of Co-type nitrile hydratase from Pseudomonas putida. Biochemistry 50: 4923-4935.
24. Somarowthu S, Brodkin HR, D'Aquino JA, Ringe D, Ondrechen MJ, Beuning PJ, (2011) A tale of two isomerases: compact versus extended active sites in ketosteroid isomerase and phosphoglucose isomerase. Biochemistry 50: 9283-9295.
25. Walsh JM, Parasuram R, Rajput PR, Rozners E, Ondrechen MJ, Beuning PJ, (2012) Effects of non-catalytic, distal amino acid residues on activity of E. coli DinB (DNA polymerase IV). Environ Mol Mutagen 53: 766-776.
26. Kobayashi M, Shimizu S, (1998) Metalloenzyme nitrile hydratase: structure, regulation, and application to biotechnology. Nat Biotechnol 16: 733-736.
27. Hashimoto Y, Sasaki S, Herai S, Oinuma K, Shimizu S, Kobayashi M, (2002) Site-directed mutagenesis for cysteine residues of cobalt-containing nitrile hydratase. J Inorg Biochem 91: 70-77.
28. Miyanaga A, Fushinobu, S., Ito, K., Shoun, H., Wakagi, T., (2004) Mutational and structural analysis of cobalt-containing nitrile hydratase on substrate and metal binding. Eur J Biochem 271: 429-438.
29. Takarada H, Kawano Y, Hashimoto K, Nakayama H, Ueda S, Yohda M, Kamiya N, Dohmae N, Maeda M, Odaka M, (2006) Mutational study on alphaGln90 of Fe-type nitrile hydratase from Rhodococcus sp. N771. Biosci Biotechnol Biochem 70: 881-889.
30. Endo I, Nojiri M, Tsujimura M, Nakasako M, Nagashima S, Yohda M, Odaka M, (2001) Fe-type nitrile hydratase. J Inorg Biochem 83: 247-253.
31. Jeffery CJ, (1999) Moonlighting proteins. Trends Biochem Sci 24: 8-11.
32. Chaput M, Claes V, Portetelle D, Cludts I, Cravador A, Burny A, Gras H, Tartar A, (1988) The neurotrophic factor neuroleukin is 90% homologous with phosphohexose isomerase. Nature 332: 454-455.
33. Faik P, Walker JIH, Redmill AAM, Morgan MJ, (1988) Mouse glucose-6-phosphate isomerase and neuroleukin have identical 3′ sequences. Nature 332: 455-456.
34. Watanabe H, Takehana K, Date M, Shinozaki T, Raz A, (1996) Tumor cell autocrine motility factor Is the neuroleukin/phosphohexose isomerase polypeptide. Cancer Res 56: 2960-2963.
35. Xu W, Seiter K, Feldman E, Ahmed T, Chiao J, (1996) The differentiation and maturation mediator for human myeloid leukemia cells shares homology with neuroleukin or phosphoglucose isomerase. Blood 87: 4502-4506.
36. Beutler E, West C, Britton HA, Harris J, Forman L, (1997) Glucosephosphate isomerase (GPI) deficiency mutations associated with hereditary nonspherocytic hemolytic anemia (HNSHA). Blood Cells Mol Dis 23: 402-409.
37. Yanagawa T, Funasaka T, Tsutsumi S, Watanabe H, Raz A, (2004) Novel roles of the autocrine motility factor/phosphoglucose isomerase in tumor malignancy. Endocr Relat Cancer 11: 749-759.
38. Read J, Pearce J, Li X, Muirhead H, Chirgwin J, Davies C, (2001) The crystal structure of human phosphoglucose isomerase at 1.6 Å resolution: implications for catalytic mechanism, cytokine activity and haemolytic anaemia. J Mol Biol 309: 447-463.
39. Meng M, Chen YT, Hsiao YY, Itoh Y, Bagdasarian M, (1998) Mutational analysis of the conserved cationic residues of Bacillus stearothermophilus 6-phosphoglucose isomerase. Eur J Biochem 257: 500-505.
40. Meng M, Lin HY, Hsieh CJ, Chen YT, (2001) Functions of the conserved anionic amino acids and those interacting with the substrate phosphate group of phosphoglucose isomerase. FEBS Lett 499: 11-14.
41. Jeffery CJ, Bahnson BJ, Chien W, Ringe D, Petsko GA, (2000) Crystal structure of rabbit phosphoglucose isomerase, a glycolytic enzyme that moonlights as neuroleukin, autocrine motility factor, and differentiation mediator. Biochemistry 39: 955-964.
42. Solomons JTG, Zimmerly EM, Burns S, Krishnamurthy N, Swan MK, Krings S, Muirhead H, Chirgwin J, Davies C, (2004) The crystal structure of mouse phosphoglucose isomerase at 1.6 angstrom resolution and its complex with glucose 6-phosphate reveals the catalytic mechanism of sugar ring opening. J Mol Biol 342: 847-860.
43. Lee JH, Jeffery CJ, (2005) The crystal structure of rabbit phosphoglucose isomerase complexed with D-sorbitol-6-phosphate, an analog of the open chain form of D-glucose-6-phosphate. Protein Sci 14: 727-734.
44. Kraut DA, Sigala PA, Fenn TD, Herschlag D, (2010) Dissecting the paradoxical effects of hydrogen bond mutations in the ketosteroid isomerase oxyanion hole. Proc Natl Acad Sci 107: 1960-1965.
45. Sigala PA, Caaveiro JMM, Ringe D, Petsko GA, Herschlag D, (2009) Hydrogen bond coupling in the ketosteroid isomerase active site. Biochemistry 48: 6932-6939.
46. Kraut DA, Churchill MJ, Dawson PE, Herschlag D, (2009) Evaluating the potential for halogen bonding in the oxyanion hole of ketosteroid isomerase using unnatural amino acid mutagenesis. ACS Chem Biol 4: 269-273.
47. Chakravorty DK, Soudackov AV, Hammes-Schiffer S, (2009) Hybrid quantum/classical molecular dynamics simulations of the proton transfer reactions catalyzed by ketosteroid isomerase: analysis of hydrogen bonding, conformational motions, and electrostatics. Biochemistry 48: 10608-10619.
48. Warshel A, Sharma PK, Chu ZT, Åqvist J, (2007) Electrostatic contributions to binding of transition state analogues can be very different from the corresponding contributions to catalysis: Phenolates binding to the oxyanion hole of ketosteroid isomerase. Biochemistry 46: 1466-1476.
49. Kraut DA, Sigala PA, Pybus B, Liu CW, Ringe D, Petsko GA, Herschlag D, (2006) Testing electrostatic complementarity in enzyme catalysis: hydrogen bonding in the ketosteroid isomerase oxyanion hole. PLoS Biol 4: e99.
50. Hanoian P, Sigala PA, Herschlag D, Hammes-Schiffer S, (2010) Hydrogen bonding in the active site of ketosteroid isomerase: electronic inductive effects and hydrogen bond coupling. Biochemistry 49: 10339-10348.
51. Schwans JP, Kraut DA, Herschlag D, (2009) Determining the catalytic role of remote substrate binding interactions in ketosteroid isomerase. Proc Natl Acad Sci USA 106: 14271-14275.
52. Kim SW, Cha SS, Cho HS, Kim JS, Ha NC, Cho MJ, Joo S, Kim KK, Choi KY, Oh BH, (1997) High-resolution crystal structures of delta5-3-ketosteroid isomerase with and without a reaction intermediate analogue. Biochemistry 36: 14030-14036.
53. Cho HS, Choi G, Choi KY, Oh BH, (1998) Crystal structure and enzyme mechanism of Delta 5-3-ketosteroid isomerase from Pseudomonas testosteroni. Biochemistry 37: 8325-8330.
54. Kim D-H, Jang DS, Nam GH, Choi G, Kim J-S, Ha N-C, Kim M-S, Oh B-H, Choi KY, (2000) Contribution of the hydrogen-bond network involving a tyrosine triad in the active site to the structure and function of a highly proficient ketosteroid isomerase from Pseudomonas putida biotype B. Biochemistry 39: 4581-4589.
55. Nam GH, Jang DS, Cha SS, Lee TH, Kim DH, Hong BH, Yun YS, Oh BH, Choi KY, (2001) Maintenance of alpha-helical structures by phenyl rings in the active-site tyrosine triad contributes to catalysis and stability of ketosteroid isomerase from Pseudomonas putida biotype B. Biochemistry 40: 13529-13537.
56. Kim S, Choi K, (1995) Identification of active site residues by site-directed mutagenesis of delta 5-3-ketosteroid isomerase from Pseudomonas putida biotype B. J Bacteriol 177: 2602-2605.
57. Kim DH, Nam GH, Jang DS, Choi G, Joo S, Kim JS, Oh BH, Choi KY, (1999) Roles of active site aromatic residues in catalysis by ketosteroid isomerase from Pseudomonas putida biotype B. Biochemistry 38: 13810-13819.
58. Kim S, Joo S, Choi G, Cho H, Oh B, Choi K, (1997) Mutational analysis of the three cysteines and active-site aspartic acid 103 of ketosteroid isomerase from Pseudomonas putida biotype B. J Bacteriol 179: 7742-7747.
59. Kim EE, Wyckoff HW, (1991) Reaction mechanism of alkaline phosphatase based on crystal structures. Two-metal ion catalysis. J Mol Biol 218: 449-464.
60. Andrews LD, Zalatan JG, Herschlag D, (2014) Probing the origins of catalytic discrimination between phosphate and sulfate monoester hydrolysis: comparative analysis of alkaline phosphatase and protein tyrosine phosphatases. Biochemistry 53: 6811-6819.
61. O'Brien PJ, Lassila JK, Fenn TD, Zalatan JG, Herschlag D, (2008) Arginine coordination in enzymatic phosphoryl transfer: evaluation of the effect of Arg166 mutations in Escherichia coli alkaline phosphatase. Biochemistry 47: 7663-7672.
62. Coleman JE, (1992) Structure and mechanism of alkaline phosphatase. Annu Rev Biophys Biomol Struct 21: 441-483.
63. Dealwis CG, Chen L, Brennan C, Mandecki W, Abad-Zapatero C, (1995) 3-D structure of the D153G mutant of Escherichia coli alkaline phosphatase: an enzyme with weaker magnesium binding and increased catalytic activity. Protein Eng 8: 865-871.
64. Matlin AR, Kendall DA, Carano KS, Banzon JA, Klecka SB, Solomon NM, (1992) Enhanced catalysis by active-site mutagenesis at aspartic acid 153 in Escherichia coli alkaline phosphatase. Biochemistry 31: 8196-8200.
65. Wojciechowski CL, Kantrowitz ER, (2003) Glutamic acid residues as metal ligands in the active site of Escherichia coli alkaline phosphatase. Biochim Biophys Acta 1649: 68-73.
66. Tibbitts TT, Murphy JE, Kantrowitz ER, (1996) Kinetic and structural consequences of replacing the aspartate bridge by asparagine in the catalytic metal triad of Escherichia coli alkaline phosphatase. J Mol Biol 257: 700-715.
67. Tibbitts TT, Xu X, Kantrowitz ER, (1994) Kinetics and crystal structure of a mutant Escherichia coli alkaline phosphatase (Asp-369 → Asn): a mechanism involving one zinc per active site. Protein Sci 3: 2005-2014.
68. Ma L, Tibbitts TT, Kantrowitz ER, (1995) Escherichia coli alkaline phosphatase: X-ray structural studies of a mutant enzyme (His-412->Asn) at one of the catalytically important zinc binding sites. Protein Sci 4: 1498-1506.
69. Chaidaroglou A, Brezinski DJ, Middleton SA, Kantrowitz ER, (1988) Function of arginine-166 in the active site of Escherichia coli alkaline phosphatase. Biochemistry 27: 8338-8343.
70. Xu X, Kantrowitz ER, (1991) A water-mediated salt link in the catalytic site of Escherichia coli alkaline phosphatase may influence activity. Biochemistry 30: 7789-7796.
71. Stec B, Hehir MJ, Brennan C, Nolte M, Kantrowitz ER, (1998) Kinetic and X-ray structural studies of three mutant E. coli alkaline phosphatases: insights into the catalytic mechanism without the nucleophile Ser102. J Mol Biol 277: 647-662.
72. Mitra B, Kallarakal AT, Kozarich JW, Gerlt JA, Clifton JG, Petsko GA, Kenyon GL, (1995) Mechanism of the reaction catalyzed by mandelate racemase: importance of electrophilic catalysis by glutamic acid 317. Biochemistry 34: 2777-2787.
73. Landro JA, Kallarakal AT, Ransom SC, Gerlt JA, Kozarich JW, Neidhart DJ, Kenyon GL, (1991) Mechanism of the reaction catalyzed by mandelate racemase. 3. Asymmetry in reactions catalyzed by the H297N mutant. Biochemistry 30: 9274-9281.
74. Kallarakal AT, Mitra B, Kozarich JW, Gerlt JA, Clifton JG, Petsko GA, Kenyon GL, (1995) Mechanism of the reaction catalyzed by mandelate racemase: structure and mechanistic properties of the K166R mutant. Biochemistry 34: 2788-2797.
75. Neidhart DJ, Howell PL, Petsko GA, Powers VM, Li RS, Kenyon GL, Gerlt JA, (1991) Mechanism of the reaction catalyzed by mandelate racemase. 2. Crystal structure of mandelate racemase at 2.5-A resolution: identification of the active site and possible catalytic residues. Biochemistry 30: 9264-9273.
76. Lesburg CA, Huang C, Christianson DW, Fierke CA, (1997) Histidine -> carboxamide ligand substitutions in the zinc binding site of carbonic anhydrase II alter metal coordination geometry but retain catalytic activity. Biochemistry 36: 15780-15791.
77. Christianson DW, Cox JD, (1999) Catalysis by metal-activated hydroxide in zinc and manganese metalloenzymes. Annu Rev Biochem 68: 33-57.
78. Kiefer LL, Krebs JF, Paterno SA, Fierke CA, (1993) Engineering a cysteine ligand into the zinc binding site of human carbonic anhydrase II. Biochemistry 32: 9896-9900.
79. Eriksson AE, Jones TA, Liljas A, (1988) Refined structure of human carbonic anhydrase II at 2.0 A resolution. Proteins 4: 274-282.
80. Ippolito JA, Christianson DW, (1993) Structure of an engineered His3Cys zinc binding site in human carbonic anhydrase II. Biochemistry 32: 9901-9905.
81. Venta PJ, Welty RJ, Johnson TM, Sly WS, Tashian RE, (1991) Carbonic anhydrase II deficiency syndrome in a Belgian family is caused by a point mutation at an invariant histidine residue (107 His - Tyr): complete structure of the normal human CA II gene. Am J Hum Genet 49: 1082-1090.
82. Liang Z, Xue Y, Behravan G, Jonsson BH, Lindskog S, (1993) Importance of the conserved active-site residues Tyr7, Glu106 and Thr199 for the catalytic function of human carbonic anhydrase II. Eur J Biochem 211: 821-827.
83. Hilvert D, (2013) Design of protein catalysts. Annu Rev Biochem 82: 447-470.
84. Cha HJ, Jang DS, Jin KS, Lee HJ, B.H. H, Kim E-S, Kim J, Lee HC, Choi KY, Ree M, (2014) Three-dimensional structures of a wild-type ketosteroid isomerase and its single mutant in solution. Sci Advan Mater 6: 2325-2333.
85. Fried SD, Bagchi S, Boxer SG, (2014) Extreme electric fields power catalysis in the active site of ketosteroid isomerase. Science 346: 1510-1514.
86. Berman HM, Westbrook J, Feng Z, Gilliland G, Bhat TN, Weissig H, Shindyalov IN, Bourne PE, (2000) The Protein Data Bank. Nucleic Acids Res 28: 235-242.
87. Ondrechen MJ,. Identification of functional sites based on prediction of charged group behavior. In:, Baxevanis AD, Davison DB, Page RDM, Petsko GA, Stein LD, Stormo GD, Eds. (2004) Current protocols in bioinformatics. Hoboken, NJ: Wiley, pp 8.6.1-8.6.10.
88. Sankararaman S, Kolaczkowski B, Sjolander K, (2009) INTREPID: a web server for prediction of functionally important residues by evolutionary analysis. Nucleic Acids Res 37: W390-W395.
89. Glanville JG, Kirshner D, Krishnamurthy N, Sjolander K, (2007) Berkeley Phylogenomics Group web servers: resources for structural phylogenomic analysis. Nucleic Acids Res 35: W27-W32.
90. Sobolev V, Eyal E, Gerzon S, Potapov V, Babor M, Prilusky J, Edelman M, (2005) SPACE: a suite of tools for protein structure prediction and analysis based on complementarity and environment. Nucleic Acids Res 33: W39-W43.
91. Sobolev V, Sorokine A, Prilusky J, Abola E, Edelman M, (1999) Automated analysis of interatomic contacts in proteins. Bioinformatics 15: 327-332.
92. Chang A, Scheer M, Grote A, Schomburg I, Schomburg D, (2009) BRENDA, AMENDA and FRENDA the enzyme information system: new content and tools in 2009. Nucleic Acids Res 37: D588-592.
93. Brockman RW, Heppel LA, (1968) On the localization of alkaline phosphatase and cyclic phosphodiesterase in Escherichia coli. Biochemistry 7: 2554-2562.