Enzyme promiscuity in the hormone-sensitive lipase family of proteins

Protein and Peptide Letters

Volumn 19, Issue 2, 2012, Pages 144-154

  Manco, Giuseppe ^a   Merone, Luigia ^a   Porzio, Elena ^a   Feng, Yan ^b   Mandrich, Luigi ^a  

^a INSTITUTE OF PROTEIN BIOCHEMISTRY   (Italy)

^b Shanghai Jiao Tong University   (China)

Author keywords

Hormone sensitive lipase family; Promiscuity; hydrolase fold

Indexed keywords

ALPHA HYDROLASE FOLD PROTEIN; BETA HYDROLASE FOLD PROTEIN; HORMONE SENSITIVE LIPASE; HYDROLASE; THIOL ESTER HYDROLASE; UNCLASSIFIED DRUG;

ARTICLE; CATALYSIS; CATALYTIC PROMISCUITY; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME MECHANISM; ENZYME PROMISCUITY; ENZYME SPECIFICITY; ENZYME STRUCTURE; HUMAN; MOLECULAR EVOLUTION; NONHUMAN; PROTEIN FOLD; PROTEIN STRUCTURE; STRUCTURE ANALYSIS; SUBSTRATE PROMISCUITY;

EID: 84858813737     PISSN: 09298665     EISSN: None     Source Type: Journal    
DOI: 10.2174/092986612799080400     Document Type: Article

References (89)

1. O'Brien, P.J.; Herschlag, D. Catalytic promiscuity and the evolution of new enzymatic activities. Chem. Biol., 1999, 6, R91-R105. (Pubitemid 29368405)
2. Copley, S.D. Enzymes with extra talents: moonlighting functions and catalytic promiscuity. Curr. Opin. Chem. Biol., 2003, 7, 265-72. (Pubitemid 36514958)
3. Bornscheuer, U. T.; Kazlauskas, R. J., 2006, Hydrolases in Organic Synthesis -Regio-and Stereoselective Biotransformations, 2nd edn. Wiley-VCH, Weinheim.
4. Hult, K.; Berglund, P. Enzyme promiscuity: Mechanism and applications. Trends in Biotech., 2007, 25, 231-238. (Pubitemid 46589665)
5. Tokuriki, N.; Tawfik, D.S. Protein Dynamism and Evolvability. Science, 2009, 324, 203-207.
6. Babbitt, P.C.; Gerlt, J.A. Understanding enzyme superfamilies: Chemistry as the fundamental determinant in the evolution of new catalytic activities. J. Biol. Chem., 1997, 272, 30591-30594. (Pubitemid 27527485)
7. Bornscheuer, U. T.; Kazlauskas, R. J. Catalytic promiscuity in biocatalysis: using old enzymes to form new bonds and follow new pathways. Angew. Chem. Int. Ed., 2004, 43, 6032-6040. (Pubitemid 39611872)
8. Gerlt, J.A.; Babbitt, P.C. Divergent evolution of enzymatic function: mechanistically diverse superfamilies and functionally distinct suprafamilies. Annu. Rev. Biochem., 2001, 70, 209-246. (Pubitemid 32662210)
9. Ekroos, M; Sjögren, T. Structural basis for ligand promiscuity in cytochrome P450 3A4, Proc. Natl. Acad. Sci USA., 2006, 103, 13682-13687. (Pubitemid 44413967)
10. Lampe, J.N.; Brandman, R.; Sivaramakrishnan, S.; and Ortiz de Mantellano, P.R. Two-dimensional NMR and All-atom Molecular Dynamics of Cytochrome P450 CYP119 Reveal Hidden Conformational Substates. J. Biol. Chem., 2010, 285, 9594-9603.
11. Fernández, A.; Tawfik, D.S.; Berkhout, B.; Sanders, R.; Kloczkowski, A.; Sen, T.; Jernigan, B. Protein promiscuity: drug resistance and native functions-HIV-1 case. J. Biomol. Struct. Dyn., 2005, 22, 615-624. (Pubitemid 40703970)
12. Romero, P.A.; and Arnold, F.H. Exploring protein fitness landscapes by directed evolution. Nat. Rev. Mol. Cell Biol., 2009, 10, 866-876.
13. Babtie, A.; Tokuriki, N.; Hollfelder, F. What makes an enzyme promiscuous? Curr. Op. Chem. Biol., 2010, 14, 200-207.
14. van Loo, B.; Jonas, S.; Babtie, A.C.; Benjdia, A.; Berteau, O.; Hyvönen, M.; Hollfelder, F. An efficient, multiply promiscuous hydrolase in the alkaline phosphatase superfamily. Proc. Natl. Acad. Sci. USA., 2010, 107, 2740-2745.
15. Nobeli, I.; Favia, A.D.; Thornton, J.M. Protein promiscuity and its implications for biotechnology. Nature Biotech., 2009, 27, 157-167.
16. Neuberg, C.; and Hirsch, J. Uber ein Kohlenstoffketten knrpfendes Ferment (Carboligase). Biochem. Z, 1921, 115, 282-310.
17. Pocker, Y.; Sarkanen, S. Oxonase and esterase activities of erythrocyte carbonic anhydrase. Biochemistry, 1978, 17, 1110-1118. (Pubitemid 8310769)
18. Pocker, Y.; Stone, J.T. The catalytic versatility of erythrocyte carbonic anhydrase. The enzyme-catalyzed hydrolysis of rhonitrophenyl acetate. J. Am. Chem. Soc., 1965, 87, 5497-5498.
19. D'Ari, R.; Casadesus, J. Underground metabolism. Bioessays, 1998, 20, 181-186. (Pubitemid 28132113)
20. Jensen, R.A. Enzyme recruitment in evolution of new function. Annu. Rev. Microbiol., 1976, 30, 409-425.
21. Patrick,W.M.; Matsumura, I.A. A Study in Molecular Contingency: GlutaminePhosphoribosylpyrophosphate Amidotransferase is a Promiscuous and Evolvable Phosphoribosylanthranilate Isomerase. J. Mol. Biol., 2008, 377, 323-336.
22. McLoughlin, S.Y.; Copley, S.D. A compromise required by gene sharing enables survival: Implications for evolution of new enzyme activities. Proc. Natl. Acad. Sci. USA., 2008, 105, 14412-14417.
23. Ohno, S: Evolution by Gene Duplication. New York: Springer-Verlag; 1970, 1-160.
24. Serres, M.H.; Kerr, A.R.W.; McCormack, T.J.; Riley, M. Evolution by leaps: gene duplication in bacteria. Biology Direct, 2009, 4, 46.
25. Aharoni, A.; Gaidukov, L.; Khersonsky, O.; Mc, Q.G.S.; Roodveldt, C.; Tawfik, D.S. The 'evolvability' of promiscuous protein functions. Nat. Genet., 2005, 37, 73-76. (Pubitemid 40070942)
26. Roodvelt, C.; Tawfik, D.S. Shared promiscuous activities and evolutionary features in various members of amidohydrolase superfamily. Biochemistry, 2005, 44, 12728-12736. (Pubitemid 41377312)
27. Bloom, J.D.; Arnold, F.H. In the light of directed evolution: Pathways of adaptive protein evolution. Proc. Natl. Acad. Sci. USA., 2009, 106, 9995-10000.
28. Babbitt, P.C.; Gerlt, J.A. Enzyme (Re)Design: Lessons from Natural Evolution and Computation, J. Biol. Chem., 1997, 272, 30591-30594.
29. Gerlt, J.A.; Babbitt, P.C. Mechanistically diverse enzyme superfamilies: the importance of chemistry in the evolution of catalysis. Curr. Opin. Chem. Biol., 1998, 2, 607-12. (Pubitemid 128645717)
30. Peisajovich, S.G.; Rockah, L.; Tawfik, D.S. Evolution of new protein topologies through multistep gene rearrangements. Nat. Genet., 2006, 38, 168-74. (Pubitemid 43177229)
31. Khersonsky, O.; Roodveldt, C.; Tawfik, D.S. Enzyme promiscuity: evolutionary and mechanistic aspects. Curr. Opin. Chem. Biol., 2006, 10, 498-508. (Pubitemid 44375065)
32. Service, R. Structural biology: a dearth of new folds. Science, 2005, 307, 1555.
33. Bogarad, L. D.; Deem, M. W. A hierarchical approach to protein molecular evolution. Proc. Natl. Acad. Sci. USA, 1999, 96, 2591-2595 (Pubitemid 29148761)
34. Ma, B.; Shatsky, M.; Wolfson, H.J.; Nussinov, R. Multiple diverse ligands binding at a single protein site: A matter of pre-existing populations. Protein Sci., 2002, 11, 184-197. (Pubitemid 34075781)
35. James, L.C.; Roversi, P.; Tawfik, D.S. Antibody multispecificity mediated by conformational diversity. Science, 2003, 299, 1362-1367. (Pubitemid 36254643)
36. Meier, S.; Ozbek, S. A biological cosmos of parallel universes: does protein structural plasticity facilitate evolution? BioEssays, 2007, 29, 1095-1104. (Pubitemid 350057380)
37. Tokuriki, N.; Tawfik, D.S. Protein dynamism and evolvability. Science, 2009, 324, 203-207.
38. Tawfik, D.S. Loop Grafting and the Origins of Enzyme Species. Science, 2006, 311, 475-476. (Pubitemid 43157716)
39. Park, H.S.; Nam, S.H.; Lee, J.K.; Yoon, C.N.; Mannervik, B.; Benkovic, S.J.; Kim, H.S. Design and evolution of new catalytic activity with an existing protein scaffold. Science, 2006, 311, 535-538. (Pubitemid 43157733)
40. Afriat, L.; Roodveldt, C.; Manco, G.; Tawfik, D.S. The Latent Promiscuity of Newly Identified Microbial Lactonases Is Linked to a Recently Diverged Phosphotriesterase. Biochemistry, 2006, 45, 13677-13686. (Pubitemid 44788738)
41. Elias, M.; Dupuy, J.; Merone, L.; Mandrich, L.; Porzio, E.; Moniot, S.; Rochu, D.; Lecomte, C.; Rossi, M.; Masson, P.; Manco, G.; Chabriere, E. Structural basis for natural lactonase and promiscuous phosphotriesterase activities. J. Mol. Biol., 2008, 379, 1017-1028.
42. Mandrich, L.; Manco, G. Evolution in the amidohydrolase superfamily: substrate-assisted gain of function in the E183K mutant of a phosphotriesterase-like metal-carboxylesterase. Biochemistry, 2009, 48, 5602-5612.
43. Bornscheuer, U.T.; Kazlauskas, R.J. Catalytic promiscuity in biocatalysis: using old enzymes to form new bonds and follow new pathways. Angew. Chem. Int. Edn. Engl. 2004, 43, 6032-6040. (Pubitemid 39611872)
44. Hult, K.; Berglund, P. Enzyme promiscuity: mechanism and applications. Trends Biotechnol., 2007, 25, 231-238. (Pubitemid 46589665)
45. Toscano, M.D.; Woycechowsky, K.J.; Hilvert, D. Minimalist active-site redesign: teaching old enzymes new tricks. Angew. Chem. Int. Ed. Engl., 2007, 46, 3212-3236. (Pubitemid 46973466)
46. Kazlauskas, R.J. Enhancing catalytic promiscuity for biocatalysis. Curr Opin Chem Biol. 2005, 9, 195-201. (Pubitemid 40462490)
47. Reetz, M. T., Carballeira, J. D., Peyralans, J., Hobenreich, H;. Maichele, A.;. Vogel, A. Expanding the substrate scope of enzymes: combining mutations obtained by CASTing. Chem. Eur. J., 2006, 12, 6031-6038.
48. Eggert, T.; Funke, S. A.; Rao, N. M.; Acharya, P.; Krumm, H.; Reetz, M.T.; Jaeger, K.E .Multiplex-PCR-based recombination as a novel high-fidelity method for directed evolution. ChemBioChem., 2005, 6, 1062-1067. (Pubitemid 40825348)
49. Hamamatsu, N.; Nomiya, Y.; Aita, T.; Nakajima, M.; Husimi, Y.; Shibanaka, Y. Directed evolution by accumulating tailored mutations: thermostabilization of lactate oxidase with less trade-off with catalytic activity. Protein Eng. Des. Sel., 2006, 19, 488-489.
50. Hamamatsu, N.; Suzumura, A.; Nomiya, Y. ; Sato, M.; Aita, T.; Nakajima, M.; Husimi, Y.; Shibanaka, Y. Modified substrate specificity of pyrroloquinoline quinone glucose dehydrogenase by biased mutation assembling with optimized amino acid substitution. Appl. Microbiol. Biotechnol., 2006, 73, 607-617. (Pubitemid 44748950)
51. Turner, N.J. Directed evolution drives the next generation of biocatalysts. Directed evolution drives the next generation of biocatalysts. Nature Chem. Biol., 2009, 5, 567-573
52. Jiang, L.; Althoff, E.A.; Clemente, F.R.; Doyle, L.; Röthlisberger, D.; Zanghellini, A.; Gallaher, J.L.; Betker, J.L.; Tanaka, F.; Barbas, C.F.; Hilvert, D.; Houk, K.N.; Stoddard, B.L.; Baker, D. De novo computational design of retro-aldol enzymes. Science, 2008, 319, 1387-1391. (Pubitemid 351354873)
53. Bolon, D.N.; Mayo, S.L. Enzyme-like proteins by computational design. Proc. Natl. Acad. Sci. USA., 2001, 98, 14274-14279. (Pubitemid 33121382)
54. Rothlisberger, D.; Khersonsky, O.; Wollacott, A.M.; Jiang, L.; DeChancie, J.; Betker, J.; Gallaher, J.L.; Althoff, E.A.; Zanghellini, A.; Dym, O.; Albeck, S.; Houk, K.N.; Tawfik, D.S.; Baker, D. Kemp elimination catalysts by computational enzyme design. Nature, 2008, 453,190-195. (Pubitemid 351667979)
55. Ollis, D.L.; Cheah, E.; Cygler, M.; Dijkstra, B.; Frolow, F.: Franken, S.M.; Harel M.; Remington, S.J.; Silman, I.; Schrag, J.;Sussman, J.L; Verschueren, K.H.G.; Goldman, A. The alpha/beta hydrolase fold. Protein Eng., 1992, 5,197-211.
56. Carr, P.D.; Ollis, D.L. The alpha/beta hydrolase fold. An update. Protein Pept. Lett., 2009, 16, 1137-1148.
57. Holmquist, M. Alpha/Beta-hydrolase fold enzymes: structures, functions and mechanisms. Curr. Protein Pept. Sci., 2000, 1, 209-235.
58. Nardini, M.; Dijkstra, B.W. Alpha/beta hydrolase fold enzymes: the family keeps growing. Curr. Opin. Struct. Biol., 1999, 9, 732-737.
59. Qian, Z.; Fields, C.J.; Yu, Y.; Lutz, S. Recent progress in engineering alpha/beta hydrolase-fold family members. Biotechnol. J., 2007, 2, 192-200. (Pubitemid 46738871)
60. Bugg, T.D. Diverse catalytic activities in the alpha-beta-hydrolase family of enzymes: activation of H2O, HCN, H2O2, and O2. Bioorg. Chem., 2004, 32, 367-375. (Pubitemid 39277443)
61. Wang ,Q.; Yang, G.; Liu, Y.; Feng, Y. Discrimination of esterase and peptidase activities of acylaminoacyl peptidase from hyperthermophilic Aeropyrum pernix K1 by a single mutation. J. Biol. Chem., 2006, 281, 18618-18625. (Pubitemid 44035521)
62. Kiss, A.L.; Hornung, B.; Rádi, K.; Gengeliczki, Z.; Sztáray, B.; Juhász, T.; Szeltner, Z.; Harmat, V.; Polgár, L. The acylaminoacyl peptidase from Aeropyrum pernix K1 thought to be an exopeptidase displays endopeptidase activity. J. Mol. Biol., 2007, 368, 509-520. (Pubitemid 46505147)
63. Itoh, N.; Kawanami, T.; Liu, J.Q.; Dairi, T.; Miyakoshi, M.; Nitta, C.; Kimoto, Y. Cloning and biochemical characterization of Co(2+)-activated bromoperoxidase-esterase (perhydrolase) from Pseudomonas putida IF-3 strain. Biochim. Biophys. Acta, 2001, 1545, 53-66. (Pubitemid 32124807)
64. Yin de, L.T.; Bernhardt, P.; Morley, K.L.; Jiang, Y.; Cheeseman, J.D.; Purpero, V.; Schrag, J.D.; Kazlauskas, R.J. Switching Catalysis from Hydrolysis to Perhydrolysis in Pseudomonas fluorescens Esterase. Biochemistry, 2010, 49, 1931-1942.
65. Gruber, K.; Gartler, G.; Krammer, B.; Schwab, H.; Kratky C. Reaction mechanism of hydroxynitrile lyases of the α/β-hydrolase superfamily: The 3D structure of the transient enzyme-substrate complex certifies the crucial role of Lys236. J. Biol. Chem., 2004, 279, 20501-20510 . (Pubitemid 38623497)
66. Jochens, H.; Stiba, K.; Savile, C.; Fujii, R.; Yu, J.G.; Gerassenkov, T.; Kazlauskas, R.J.; Bornscheuer, U.T. Converting an esterase into an epoxide hydrolase Angew. Chem. Int. Ed. Eng., 2009, 48, 3532-3535.
67. Bernhardt, P.; Hult, K.; Kazlauskas, R. J. Molecular basis of perhydrolase activity in serine hydrolases. Angew. Chem. Int. Ed. Engl., 2005, 44, 2742-2746. (Pubitemid 40689576)
68. Padhi, S.K.; Fujii, R.; Legatt, G.A.; Fossum, S.L.; Berchtold, R.; Kazlauskas, R.J. Switching from an Esterase to a Hydroxynitrile Lyase Mechanism Requires Only Two Amino Acid Substitutions Chem. Biol., 2010, 17, 863-871.
69. Mandrich, L.; Merone, L.; Manco, G. Structural and kinetic overview of the carboxylesterase EST2 from Alicyclobacillus acidocaldarius: a comparison with the other members of the HSL family. Protein Pept. Lett., 2009, 16, 1189-1200.
70. Manco, G.; Adinolfi, E.; Pisani, F.M.; Ottolina, G.; Carrea, G.; Rossi M. Overexpression and properties of a new thermophilic and thermostable esterase from Bacillus acidocaldarius with sequence similarity to hormone-sensitive lipase subfamily. Biochem. J., 1998, 32, 203-212. (Pubitemid 28239336)
71. Manco, G.; Giosuè, E.; D'Auria, S.; Herman, P.; Carrea, G.; Rossi, M. Cloning, overexpression, and properties of a new thermophilic and thermostable esterase with sequence similarity to hormonesensitive lipase subfamily from the archaeon Archaeoglobus fulgidus. Arch. Biochem. Biophys., 2000, 373, 182-192. (Pubitemid 30046503)
72. Mandrich, L.; Merone, L.; Pezzullo, M.; Cipolla, L.; Nicotra, F.; Rossi, M.; Manco, G. Role of the N terminus in enzyme activity, stability and specificity in thermophilic esterases belonging to the HSL family. J. Mol. Biol., 2005, 345, 501-512. (Pubitemid 39575920)
73. Manco, G.; Mandrich, L.; Rossi, M. Residues at the active site of the esterase 2 from Alicyclobacillus acidocaldarius involved in substrate specificity and catalytic activity at high temperature. J. Biol. Chem., 2001, 276, 37482-37490.
74. De Simone, G.; Mandrich, L.; Menchise, V.; Giordano, V.; Febbraio, F.; Rossi, M.; Pedone, C.; Manco, G. A substrate-induced switch in the reaction mechanism of a thermophilic esterase: kinetic evidences and structural basis. J. Biol. Chem., 2004, 279, 6815-6823. (Pubitemid 38248823)
75. De Simone, G.; Menchise, V.; Alterio, V.; Mandrich, L.; Rossi, M.; Manco, G.; Pedone, C. The crystal structure of an EST2 mutant unveils structural insights on the H group of the carboxylesterase/ lipase family. J. Mol. Biol., 2004, 343, 137-146. (Pubitemid 39277453)
76. Arpigny, J.L.; Jaeger, K.E. Bacterial lipolytic enzymes: classification and properties. Biochem. J., 1999, 343, 177-183. (Pubitemid 29473893)
77. Mandrich, L.; Manco, G.; Rossi, M.; Floris, E.; Jansen-van den Bosch, T.; Smit, G.; Wouters, J.A. Alicyclobacillus acidocaldarius thermophilic esterase EST2 activity in milk and cheese models. Appl. Environ. Microbiol., 2006, 72, 3191-3197. (Pubitemid 43727966)
78. Nardi, M., Fiez-Vandal, C.; Tailliez, P.; Monnet, V. The EstA esterase is responsible for the main capacity of Lactococcus lactis to synthesize short chain fatty acid esters in vitro. J. Appl. Microbiol., 2002, 93, 994-1002. (Pubitemid 35408574)
79. Fernandez, L.; Beethuyzen, M.M.; Brown, J.; Siezen, R.J.; Coolbear, T.; Holland, R.; Kuipers, O.P. Cloning, characterization, controlled overexpression, and inactivation of the major tributyrin esterase gene of Lactococcus lactis. Appl. Environ. Microbiol., 2000, 66, 1360-1368. (Pubitemid 30185602)
80. Ma, J.; Li, Q.; Song, B.; Liu, D.; Zheng, B.; Zhang, Z.; Feng, Y. Ring-opening polymerization of ε-caprolactone catalyzed by a novel thermophilic esterase from the archaeon Archaeoglobus fulgidus, J. Mol. Catal. B: Enzym., 2009, 56, 151-157.
81. Srivastava, R.K.; Albertsson, A.C. Porous scaffolds from high molecular weight polyesters synthesized via enzyme-catalyzed ring-opening polymerization. Biomacromolecules, 2006, 7, 2531-2538. (Pubitemid 44530490)
82. Khersonsky, O.; Malitsky, S.; Rogachev, I.; Tawfik, D.S. Role of Chemistry versus Substrate Binding in Recruiting Promiscuous Enzyme Functions. Biochemistry, 2011, 50, 2683-2690.
83. Kanaya, S.; Koyanagi, T; Kanaya, E. An esterase from Escherichia coli with a sequence similarity to hormone-sensitive lipase. Biochem. J., 1998, 332, 75-80. (Pubitemid 28239320)
84. Farias, T.; Mandrich, L.; Rossi, M.; Manco, G. Biochemical and thermostability features of acetyl esterase Aes from Escherichia coli. Protein Pept. Lett. 2007, 14, 165-169.
85. Khersonsky, O.; Tawfik, D.S. Enzyme promiscuity: a mechanistic and evolutionary perspective. Annu. Rev. Biochem., 2010, 79, 11.1-11.35.
86. Nath, A.; Atkins, W.M. A quantitative index of substrate promiscuity. Biochemistry, 2008, 47, 157-166.
87. Maillard, N.; Babiak, P.; Syed, S.; Biswas, R.; Mandrich, L.; Manco, G.; Reymond, J.L. Five-substrate cocktail as a sensor array for measuring enzyme activity fingerprints of lipases and esterases. Anal Chem., 2011, 83, 1437-1442.
88. Tawfik, D.S. Messy biology and the origins of evolutionary innovations. Nat. Chem. Biol., 2010, 6, 692-696.
89. Carbonell, P. Molecular signatures-based prediction of enzyme promiscuity. Bioinformatics, 2010, 26, 2012-2019.