Design of allosterically regulated protein catalysts

Biochemistry

Volumn 54, Issue 7, 2015, Pages 1444-1456

  Makhlynets, Olga V ^a   Raymond, Elizabeth A ^a   Korendovych, Ivan V ^a  

^a SYRACUSE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CATALYSTS; CHEMICAL DETECTION; ENZYMES; MOBILE SECURITY; POLLUTION DETECTION; PROTEINS;

ALLOSTERIC PROTEINS; ALLOSTERIC REGULATION; CELLULAR PROCESS; DISEASE BIOMARKER; ENVIRONMENTAL POLLUTANTS; EXTERNAL STIMULUS; METAL HOMEOSTASIS; SMALL-MOLECULE BINDINGS;

CATALYST ACTIVITY;

PROTEIN; HYBRID PROTEIN;

ALLOSTERISM; ARTICLE; BINDING SITE; CATALYSIS; CATALYST; ENZYME ACTIVE SITE; LIGAND BINDING; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN ENGINEERING; PROTEIN MODIFICATION; PROTEIN PROCESSING; PROTEIN STRUCTURE; PROTEIN UNFOLDING; ANIMAL; BIOCATALYSIS; CHEMICAL STRUCTURE; CHEMISTRY; GENETICS; HUMAN; METABOLISM; PROCEDURES; PROTEIN TERTIARY STRUCTURE;

ALLOSTERIC REGULATION; ALLOSTERIC SITE; ANIMALS; BIOCATALYSIS; CATALYTIC DOMAIN; HUMANS; MODELS, MOLECULAR; PROTEIN ENGINEERING; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT FUSION PROTEINS;

EID: 84923330873     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi5015248     Document Type: Article

References (98)

1. Goodey, N. M. and Benkovic, S. J. (2008) Allosteric regulation and catalysis emerge via a common route Nat. Chem. Biol. 4, 474-482
2. Cui, Q. and Karplus, M. (2008) Allostery and cooperativity revisited Protein Sci. 17, 1295-1307
3. Motlagh, H. N., Wrabi, J. O., Li, J., and Hilser, V. J. (2014) The ensemble nature of allostery Nature 508, 331-339
4. Swain, J. F. and Gierasch, L. M. (2006) The changing landscape of protein allostery Curr. Opin. Struct. Biol. 16, 102-108
5. Korendovych, I. V. and DeGrado, W. F. (2014) Catalytic effciency of designed catalytic proteins Curr. Opin. Struct. Biol. 27, 113-121
6. Kazlauskas, R. J. and Bornscheuer, U. T. (2009) Finding better protein engineering strategies Nat. Chem. Biol. 5, 526-529
7. Wijma, H. J. and Janssen, D. B. (2013) Computational design gains momentum in enzyme catalysis engineering FEBS J. 280, 2948-2960
8. Bornscheuer, U. T., Huisman, G., Kazlauskas, R. J., Lutz, S., Moore, J., and Robins, K. (2012) Engineering the third wave of biocatalysis Nature 485, 185-194
9. Vallée-Bélisle, A. and Plaxco, K. W. (2010) Structure-switching biosensors: Inspired by Nature Curr. Opin. Struct. Biol. 20, 518-526
10. Demaurex, N. and Frieden, M. (2003) Measurement of the free luminal ER Ca2+ concentration with targeted "cameleon" fluorescent proteins Cell Calcium 34, 109-119
11. Lim, W. A. (2010) Designing customized cell signaling circuits Nat. Rev. Mol. Cell Biol. 11, 393-403
12. Chen, Z., Rappert, S., and Zang, A. P. (2013) Rational Design of Allosteric Regulation of Homoserine Dehydrogenase by a Nonnatural Inhibitor l -Lysine ACS Synth. Biol. 10.1021/sb400133g
13. Wright, C. M., Wright, R. C., Eshleman, J. R., and Ostermeier, M. (2011) Protein therapeutic modality founded on molecular regulation Proc. Natl. Acad. Sci. U.S.A. 108, 16206-16211
14. Valdes, G., Schulte, R. W., Ostermeier, M., and Iwamoto, K. (2014) The high-affinity maltose switch MBP317-347 has low affinity for glucose: Implications for targeting tumors with metabolically directed enzyme prodrug therapy Chem. Biol. Drug Des. 83, 266-271
15. Ehrmann, M., Boyd, D., and Beckwith, J. (1990) Genetic analysis of membrane protein topology by a sandwich gene fusion approach Proc. Natl. Acad. Sci. U.S.A. 87, 7574-7578
16. Collinet, B., Hervé, M., Pecorari, F., Minard, P., Eder, O., and Desmadril, M. (2000) Functionally accepted insertions of proteins within protein domains J. Biol. Chem. 275, 17428-17433
17. Betton, J. M., Jacob, J. P., Hofnung, M., and Bromme-Smith, J. K. (1997) Creating a bifunctional protein by insertion of β-lactamase into the maltodextrin-binding protein Nat. Biotechnol. 15, 1276-1279
18. Doi, N., Itaya, M., Yomo, T., Tokura, S., and Yanagawa, H. (1997) Insertion of foreign random sequences of 120 amino acid residues into an active enzyme FEBS Lett. 402, 177-180
19. Biondi, R. M., Baehler, P. J., Reymond, C. D., and Véron, M. (1998) Random insertion of GFP into the cAMP-dependent protein kinase regulatory subunit from Dictyostelium discoideum Nucleic Acids Res. 26, 4946-4952
20. Lee, J., Natarajan, M., Nashine, V. C., Socolich, M., Vo, T., Russ, W. P., Benkovic, S. J., and Ranganathan, R. (2008) Surface sites for engineering allosteric control in proteins Science 322, 438-442
21. Reynolds, K. A., McLaughlin, R. N., and Ranganathan, R. (2011) Hot spots for allosteric regulation on protein surfaces Cell 147, 1564-1575
22. Ostermeier, M. (2005) Engineering allosteric protein switches by domain insertion Protein Eng., Des. Sel. 18, 359-364
23. Kanwar, M., Wright, R. C., Date, A., Tullman, J., and Ostermeier, M. (2013) Protein switch engineering by domain insertion Methods Enzymol. 523, 369-388
24. Guntas, G. and Ostermeier, M. (2004) Creation of an allosteric enzyme by domain insertion J. Mol. Biol. 336, 263-273
25. Graf, R. and Schachman, H. K. (1996) Random circular permutation of genes and expressed polypeptide chains: Application of the method to the catalytic chains of aspartate transcarbamoylase Proc. Natl. Acad. Sci. U.S.A. 93, 11591-11596
26. Krishna, M. M. G. and Englander, S. W. (2005) The N-terminal to C-terminal motif in protein folding and function Proc. Natl. Acad. Sci. U.S.A. 102, 1053-1058
27. Guntas, G., Mitchell, S. F., and Ostermeier, M. (2004) A molecular switch created by in vitro recombination of nonhomologous genes Chem. Biol. 11, 1483-1487
28. Guntas, G., Mansell, T. J., Kim, J. R., and Ostermeier, M. (2005) Directed evolution of protein switches and their application to the creation of ligand-binding proteins Proc. Natl. Acad. Sci. U.S.A. 102, 11224-11229
29. Edwards, W. R., Busse, K., Allemann, R. K., and Jones, D. D. (2008) Linking the functions of unrelated proteins using a novel directed evolution domain insertion method Nucleic Acids Res. 36, e78
30. Edwards, W. R., Williams, A. J., Morris, J. L., Baldwin, A. J., Allemann, R. K., and Jones, D. D. (2010) Regulation of β-lactamase activity by remote binding of heme: Functional coupling of unrelated proteins through domain insertion Biochemistry 49, 6541-6549
31. Fan, F., Binkowski, B. F., Butler, B. L., Stecha, P. F., Lewis, M. K., and Wood, K. V. (2008) Novel genetically encoded biosensors using firefly luciferase ACS Chem. Biol. 3, 346-351
32. Karginov, A. V., Ding, F., Kota, P., Dokholyan, N. V., and Hahn, K. (2010) Engineered allosteric activation of kinases in living cells Nat. Biotechnol. 28, 743-747
33. Chu, P.-H., Tsygankov, D., Berginski, M. E., Dagliyan, O., Gomez, S. M., Elston, T. C., Karginov, A. V., and Hahn, K. M. (2014) Engineered kinase activation reveals unique morphodynamic phenotypes and associated trafficking for Src family isoforms Proc. Natl. Acad. Sci. U.S.A. 111, 12420-12425
34. Karginov, A. V., Tsygankov, D., Berginski, M., Chu, P.-H., Trudeau, E. D., Yi, J. J., Gomez, S., Elston, T. C., and Hahn, K. M. (2014) Dissection motility signaling through activation of specific Src-effector complexes Nat. Chem. Biol. 10, 286-290
35. Dagliyan, O., Shirvanyants, D., Karginov, A. V., Ding, F., Fee, L., Chandrasekaran, S. N., Freisinger, C. M., Smolen, G., Huttenlocker, A., Hahn, K. M., and Dokholyan, N. V. (2013) Rational design of a ligand-controlled protein conformational switch Proc. Natl. Acad. Sci. U.S.A. 110, 6800-6804
36. Tucker, C. L. and Fields, S. (2001) A yeast sensor of ligand binding Nat. Biotechnol. 19, 1042-1046
37. Möglich, A., Ayers, R. A., and Moffat, K. (2009) Structure and signaling mechanism of Per-ARNT-Sim domains Structure 17, 1282-1294
38. Möglich, A., Ayers, R. A., and Moffat, K. (2009) Design and signaling mechanism of light-regulated histidine kinases J. Mol. Biol. 385, 1433-1444
39. Möglich, A., Ayers, R. A., and Moffat, K. (2010) Addition at the molecular level: Signal integration in designed Per-ARNT-Sim receptor proteins J. Mol. Biol. 400, 477-486
40. Kim, S. B., Otani, Y., Umezawa, Y., and Tao, H. (2007) Bioluminescence indicator for determining protein-protein interactions using intramolecular complementation of split click beetle luciferase Anal. Chem. 79, 4820-4826
41. Kim, S. B., Umezawa, Y., Kanno, K. A., and Tao, H. (2008) An integrated-molecule-format multicolor probe for monitoring multiple activities of a bioactive small molecule ACS Chem. Biol. 3, 359-372
42. Hamorsky, K. T., Ensor, C. M., Wei, Y., and Daunert, S. (2008) A bioluminescent molecular switch for glucose Angew. Chem., Int. Ed. 47, 3718-3721
43. Buskirk, A. R., Ong, Y.-C., Gartner, Z. J., and Liu, D. R. (2004) Directed evolution of ligand dependence: Small-molecule-activated protein splicing Proc. Natl. Acad. Sci. U.S.A. 101, 10505-10510
44. Skretas, G. and Wood, D. W. (2005) Regulation of protein activity with small-molecule-controlled inteins Protein Sci. 14, 523-532
45. Peck, S. H., Chen, I., and Liu, D. R. (2011) Directed evolution of a small-molecule-triggered intein with improved splicing properties in mammalian cells Chem. Biol. 18, 619-630
46. Kemp, D. S. and Casey, M. L. (1973) Physical organic chemistry of benzisoxazoles. II. Linearity of the Broensted free energy relationship for the base-catalyzed decomposition of benzisoxazoles J. Am. Chem. Soc. 95, 6670-6680
47. Korendovych, I. V., Kulp, D. W., Wu, Y., Cheng, H., Roder, H., and DeGrado, W. F. (2011) Design of a switchable eliminase Proc. Natl. Acad. Sci. U.S.A. 108, 6823-6827
48. Moroz, O. V., Moroz, Y. S., Wu, Y., Olsen, A. B., Cheng, H., Mack, K. L., McLaughlin, J. M., Raymond, E. A., Zhezherya, K., Roder, H., and Korendovych, I. V. (2013) A single mutation in a regulatory protein produces evolvable allosterically regulated catalyst of nonnatural reaction Angew. Chem., Int. Ed. 52, 6246-6249
49. Debler, E. W., Muller, R., Hilvert, D., and Wilson, I. A. (2009) An aspartate and a water molecule mediate efficient acid-base catalysis in a talored antibody pocket Proc. Natl. Acad. Sci. U.S.A. 106, 18539-18544
50. Thorn, S. N., Daniels, R. G., Auditor, M.-T., and Hilvert, D. (1995) Large rate accelerations in antibody catalysis by strategic use of haptenic charge Nature 373, 228-230
51. Genre-Grandpierre, A. and Tellier, C. (1997) Catalysis of the Kemp elimination by antibodies elicitied against a cationic hapten Bioorg. Med. Chem. Lett. 7, 2497-2502
52. Khersonsky, O., Kiss, G., Röthlisberger, D., Dym, O., Albeck, S., Houk, K. N., Baker, D., and Tawfik, D. S. (2012) Bridging the gaps in design methodologies by evolutionary optimization of the stability and proficiency of designed Kemp eliminase KE59 Proc. Natl. Acad. Sci. U.S.A. 109, 10358-10363
53. Privett, H. K., Kiss, G., Lee, T. M., Blomberg, R., Chica, R. A., Thomas, L. M., Hilvert, D., Houk, K. N., and Mayo, S. L. (2012) Iterative approach to computational enzyme design Proc. Natl. Acad. Sci. U.S.A. 109, 3790-3795
54. Blomberg, R., Kries, H., Pinkas, D. M., Mittl, P. R. E., Grütter, M. G., Privett, H. K., Mayo, S. L., and Hilvert, D. (2013) Precision is essential for efficient catalysis in an evolved Kemp eliminase Nature 503, 418-421
55. Chica, R. A., Doucet, N., and Pelletier, J. N. (2005) Semi-rational approaches to engineering enzyme activity: Combining the benefits of directed evolution and rational design Curr. Opin. Biotechnol. 16, 378-384
56. Bolon, D. N. and Mayo, S. (2001) Enzyme-like proteins by computational design Proc. Natl. Acad. Sci. U.S.A. 98, 14272-14279
57. Moroz, Y. S., Dunston, T. T., Makhlynets, O. V., Moroz, O. V., Wu, Y., Yoon, J. H., Olsen, A. B., McLaughlin, J. M., Mack, K. L., Gosavi, P. M., van Nuland, N. A. J., and Korendovych, I. V. (2015) Single mutations in a non-enzymatic protein give rise to various catalytic activities. Manuscript submitted for publication.
58. Richter, F., Blomberg, R., Khare, S. D., Kiss, G., Kuzin, A. P., Smith, A. J. T., Gallaher, J., Pianowski, Z., Helgeson, R. C., Grjasnow, A., Xiao, R., Seetharaman, J., Su, M., Vorobiev, S., Lew, S., Forouhar, F., Kornhaber, G. J., Hunt, J. F., Montelione, G. T., Tong, L., Houk, K. N., Hilvert, D., and Baker, D. (2012) Computational design of catalytic dyads and oxyanion holes for ester hydrolysis J. Am. Chem. Soc. 134, 16197-16206
59. Wei, Y. and Hecht, M. H. (2004) Enzyme-like proteins from an unselected library of designed amino acid sequences Protein Eng., Des. Sel. 17, 67-75
60. Raymond, E. A., Mack, K. L., Yoon, J. H., Moroz, O. V., Moroz, Y. S., and Korendovych, I. V. (2015) Design of an allosterically regulated retroaldolase Protein Sci. 10.1002/pro.2622
61. Mack, K. L., Moroz, O. V., Moroz, Y. S., Olsen, A. B., McLaughlin, J. M., and Korendovych, I. V. (2013) Reprogramming EF-hands for design of catalytically amplified lanthanide sensors JBIC, J. Biol. Inorg. Chem. 18, 411-418
62. Zhang, C., Pan, T., Salesse, C., Zhang, D., Miao, L., Wang, L., Gao, Y., Xu, J., Dong, Z., Luo, Q., and Liu, J. (2014) Reversible Ca2+ switch of an engineered allosteric antioxidant selenoenzyme Angew. Chem., Int. Ed. 53, 13536-13539
63. Kiss, G., Çelebi-Ölçüm, N., Moretti, R., Baker, D., and Houk, K. N. (2013) Computational enzyme design Angew. Chem., Int. Ed. 52, 5700-5725
64. Chen-Goodspeed, M., Sogorb, M. A., Wu, F., and Raushel, F. M. (2001) Enhancement, relaxation, and reversal of the stereoselectivity for phosphotriesterase by rational evolution of active site residues Biochemistry 40, 1332-1339
65. Ozaki, S.-I. and de Montellano, P. R. O. (1994) Molecular engineering of horseradish peroxidase. Highly enantioselective sulfoxidation of aryl alkyl sulfides by the F41L mutant J. Am. Chem. Soc. 116, 4487-4488
66. Wells, J. A., Powers, D. B., Bott, R. R., Graycar, T. P., and Estell, D. A. (1987) Designing substrate specificity by protein engineering of electrostatic interactions Proc. Natl. Acad. Sci. U.S.A. 84, 1219-1223
67. Tao, H. and Cornish, V. W. (2002) Milestones in directed enzyme evolution Curr. Opin. Chem. Biol. 6, 858-864
68. Reetz, M. T. (2011) Laboratory evolution of stereoselective enzymes: A prolific source of catalysts for asymmetric reactions Angew. Chem., Int. Ed. 50, 138-174
69. Marletta, M. A. (2006) Raising enzymes from the dead and the secrets they can tell ACS Chem. Biol. 1, 73-74
70. Williams, D. M., Wang, D., and Cole, P. A. (2000) Chemical rescue of a mutant protein-tyrosine kinase J. Biol. Chem. 275, 38127-38130
71. Qiao, Y., Molina, H., Pandey, A., Zhang, J., and Cole, P. A. (2006) Chemical rescue of a mutant enzyme in living cells Science 311, 1293-1297
72. Xia, Y., DiPrimo, N., Keppel, T. R., Vo, B., Fraser, K., Battaile, K. P., Egan, C., Bystroff, C., Lovell, S., Weis, D. D., Anderson, J. C., and Karanicolas, J. (2013) The designability of protein switches by chemical rescue of structure: Mechanisms of inactivation and reactivation J. Am. Chem. Soc. 135, 18840-18849
73. Deckert, K., Budiardjo, S. J., Brunner, L. C., Lovell, S., and Karanicolas, J. (2012) Designing allosteric control into enzymes by chemical rescue of structure J. Am. Chem. Soc. 134, 10055-10060
74. Kohn, J. E. and Plaxco, K. W. (2005) Engineering a signal transduction mechanism for protein-based biosensors Proc. Natl. Acad. Sci. U.S.A. 102, 10841-10845
75. Saghatelian, A., Guckian, K. M., Thayer, D. A., and Ghadiri, M. R. (2003) DNA detection and signal amplification via an engineered allosteric enzyme J. Am. Chem. Soc. 125, 344-345
76. Drake, S. K. and Falke, J. J. (1996) Kinetic tuning of the EF-hand calcium binding motif: The gateway residue independently adjusts (i) barrier height and (ii) equilibrium Biochemistry 35, 1753-1760
77. Drake, S. K., Lee, K. L., and Falke, J. J. (1996) Tuning the equilibrium ion affinity and selectivity of the EF-hand calcium binding motif: Substitutions at the gateway position Biochemistry 35, 6697-6705
78. Rana, S., Pozzi, N., Pelc, L. A., and Di Cera, E. (2011) Redesigning allosteric activation in an enzyme Proc. Natl. Acad. Sci. U.S.A. 108, 5221-5225
79. Pineda, A. O., Carell, C. J., Bush, L. A., Prasad, S., Caccia, S., Chen, Z. W., Mathews, F. S., and Di Cera, E. (2004) Molecular dissection of Na+ binding to thrombin J. Biol. Chem. 279, 31842-31853
80. Mathonet, P., Barrios, H., Soumillion, P., and Fastrez, J. (2006) Selection of allosteric β-lactamase mutants featuring an activity regulation by transition metal ions Protein Sci. 15, 2335-2343
81. Wright, C. M., Heins, R. A., and Ostermeier, M. (2007) As easy as flipping a switch? Curr. Opin. Chem. Biol. 11, 342-346
82. Liang, J., Kim, J. R., Boock, J. T., Mansell, T. J., and Ostermeier, M. (2007) Ligand binding and allostery can emerge simultaneously Protein Sci. 16, 929-937
83. Ke, W., Laurent, A. H., Armstrong, M. D., Chen, Y., Smith, W. E., Liang, J., Wright, C. M., Ostermeier, M., and van den Akker, F. (2012) Structure of an engineered β-lactamase maltose binding protein fusion protein: Insights into heterotropic allosteric regulation PLoS One 7, e39168
84. Wright, C. M., Majumdar, A., Tolman, J. R., and Ostermeier, M. (2010) NMR characterization of an engineered domain fusion between maltose binding protein and TEM1 β-lactamase provides insight into its structure and allosteric mechanism Proteins 78, 1423-1430
85. Wu, S., Acevedo, J. P., and Reetz, M. T. (2010) Induced allostery in the directed evolution of an enantioselective Baeyer-Villiger monooxygenase Proc. Natl. Acad. Sci. U.S.A. 107, 2775-2780
86. Looger, L. L., Dwyer, M. A., Smith, J. J., and Hellinga, H. W. (2003) Computational design of receptor and sensor proteins with novel functions Nature 423, 185-190
87. Allert, M., Rizk, S. S., Looger, L. L., and Hellinga, H. W. (2004) Computational design of receptors for an organophosphate surrogate of the nerve agent soman Proc. Natl. Acad. Sci. U.S.A. 101, 7907-7912
88. Schreier, B., Stumpp, C., Wiesner, S., and Höcker, B. (2009) Computational design of ligand binding is not a solved problem Proc. Natl. Acad. Sci. U.S.A. 106, 18491-18496
89. Cross, P. J., Allison, T. M., Dobson, R. C. J., Jamesond, G. B., and Parker, E. J. (2013) Engineering allosteric control to an unregulated enzyme by transfer of a regulatory domain Proc. Natl. Acad. Sci. U.S.A. 110, 2111-2116
90. Baker, A. S. and Deiters, A. (2014) Optical control of protein function through unnatural amino acid mutagenesis and other optogenic approaches ACS Chem. Biol. 9, 1398-1407
91. Davis, L. and Chin, J. W. (2012) Designer proteins: Applications of genetic code expansion in cell biology Nat. Rev. Mol. Cell Biol. 13, 168-182
92. Lang, K. and Chin, J. W. (2014) Cellular incorporation of unnatural amino acids and bioorthogonal labeling of proteins Chem. Rev. 114, 4764-4806
93. Chou, C., Young, D. D., and Deiters, A. (2009) A light-activated DNA polymerase Angew. Chem., Int. Ed. 48, 5950-5953
94. Li, Y., Korolev, S., and Waksman, G. (1998) Crystal structures of open and closed forms of binary and ternary complexes of the large fragment of Thermus aquaticus DNA polymerase I: Structural basis for nucleotide incorporation EMBO J. 17, 7514-7525
95. Kohse, S., Neubauer, A., Pazidis, A., Lochbrunner, S., and Kragl, U. (2013) Photoswitching of enzyme activity by laser-induced pH-jump J. Am. Chem. Soc. 135, 9407-9411
96. Changeux, J.-P. (2013) 50 years of allosteric interactions: The twists and turns of the models Nat. Rev. Mol. Cell Biol. 14, 819-829
97. Ha, J.-H. and Loh, S. N. (2012) Protein conformational switches: From nature to design Chem.-Eur. J. 18, 7984-7999
98. Medintz, I. L. and Deschamps, J. R. (2006) Maltose-binding protein: A versatile platform for prototyping biosensing Curr. Opin. Biotechnol. 17, 17-27