DOI QR코드

DOI QR Code

Bacterial Hormone-Sensitive Lipases (bHSLs): Emerging Enzymes for Biotechnological Applications

  • Kim, T. Doohun (Department of Chemistry, College of Natural Science, Sookmyung Women's University)
  • Received : 2017.08.03
  • Accepted : 2017.09.16
  • Published : 2017.11.28

Abstract

Lipases are important enzymes with biotechnological applications in dairy, detergent, food, fine chemicals, and pharmaceutical industries. Specifically, hormone-sensitive lipase (HSL) is an intracellular lipase that can be stimulated by several hormones, such as catecholamine, glucagon, and adrenocorticotropic hormone. Bacterial hormone-sensitive lipases (bHSLs), which are homologous to the C-terminal domain of HSL, have ${\alpha}/{\beta}-hydrolase$ fold with a catalytic triad composed of His, Asp, and Ser. These bHSLs could be used for a wide variety of industrial applications because of their high activity, broad substrate specificity, and remarkable stability. In this review, the relationships among HSLs, the microbiological origins, the crystal structures, and the biotechnological properties of bHSLs are summarized.

Keywords

References

  1. Casas-Godoy L, Duquesne S, Bordes F, Sandoval G, Marty A. 2012. Lipases: an overview. Methods Mol. Biol. 861: 3-30.
  2. Watt MJ, Steinberg GR. 2008. Regulation and function of triacylglycerol lipases in cellular metabolism. Biochem J. 414: 313-325. https://doi.org/10.1042/BJ20080305
  3. Stergiou PY, Foukis A, Filippou M, Koukouritaki M, Parapouli M, Theodorou LG, et al. 2013. Advances in lipase-catalyzed esterification reactions. Biotechnol. Adv. 31: 1846-1859. https://doi.org/10.1016/j.biotechadv.2013.08.006
  4. Jaeger KE, Eggert T. 2002. Lipases for biotechnology. Curr. Opin. Biotechnol. 13: 390-397. https://doi.org/10.1016/S0958-1669(02)00341-5
  5. Hui DY, Howles PN. 2002. Carboxyl ester lipase: structurefunction relationship and physiological role in lipoprotein metabolism and atherosclerosis. J. Lipid Res. 43: 2017-2030. https://doi.org/10.1194/jlr.R200013-JLR200
  6. Holmquist M. 2000. Alpha/beta-hydrolase fold enzymes:structures, functions and mechanisms. Curr. Protein Pept. Sci. 1: 209-235. https://doi.org/10.2174/1389203003381405
  7. Gupta R, Gupta N, Rathi P. 2004. Bacterial lipases: an overview of production, purification and biochemical properties. Appl. Microbiol. Biotechnol. 64: 763-781. https://doi.org/10.1007/s00253-004-1568-8
  8. Kumar A, Khan A, Malhotra S, Mosurkal R, Dhawan A, Pandey MK, et al. 2016. Synthesis of macromolecular systems via lipase catalyzed biocatalytic reactions: applications and future perspectives. Chem. Soc. Rev. 45: 6855-6887. https://doi.org/10.1039/C6CS00147E
  9. Anobom CD, Pinheiro AS, De-Andrade RA, Aguieiras EC, Andrade GC, Moura MV, et al. 2014. From structure to catalysis: recent developments in the biotechnological applications of lipases. Biomed. Res. Int. 2014: 684506.
  10. Lampidonis AD, Rogdakis E, Voutsinas GE, Stravopodis DJ. 2011. The resurgence of hormone-sensitive lipase (HSL) in mammalian lipolysis. Gene 477: 1-11. https://doi.org/10.1016/j.gene.2011.01.007
  11. Lass A, Zimmermann R, Oberer M, Zechner R. 2011. Lipolysis - a highly regulated multi-enzyme complex mediates the catabolism of cellular fat stores. Prog. Lipid Res. 50: 14-27. https://doi.org/10.1016/j.plipres.2010.10.004
  12. Arner P, Langin D. 2007. The role of neutral lipases in human adipose tissue lipolysis. Curr. Opin. Lipidol. 18: 246-250. https://doi.org/10.1097/MOL.0b013e32811e16fb
  13. Lafontan M, Langin D. 2009. Lipolysis and lipid mobilization in human adipose tissue. Prog. Lipid Res. 48: 275-297. https://doi.org/10.1016/j.plipres.2009.05.001
  14. Yeaman SJ. 2004. Hormone-sensitive lipase - new roles for an old enzyme. Biochem. J. 379: 11-22. https://doi.org/10.1042/bj20031811
  15. Krintel C, Klint C, Lindvall H, Morgelin M, Holm C. 2010. Quarternary structure and enzymological properties of the different hormone-sensitive lipase (HSL) isoforms. PLoS One 5: e11193. https://doi.org/10.1371/journal.pone.0011193
  16. Smith GM, Garton AJ, Aitken A, Yeaman SJ. 1996. Evidence for a multi-domain structure for hormone-sensitive lipase. FEBS Lett. 396: 90-94. https://doi.org/10.1016/0014-5793(96)01076-9
  17. Osterlund T. 2001. Structure-function relationships of hormone-sensitive lipase. Eur. J. Biochem. 268: 1899-1907. https://doi.org/10.1046/j.1432-1327.2001.02097.x
  18. Smith AJ, Sanders MA, Juhlmann BE, Hertzel AV, Bernlohr DA. 2008. Mapping of the hormone-sensitive lipase binding site on the adipocyte fatty acid-binding protein (AFABP). Identification of the charge quartet on the AFABP/aP2 helix-turn-helix domain. J. Biol. Chem. 283: 33536-33543. https://doi.org/10.1074/jbc.M806732200
  19. Jenkins-Kruchten AE, Bennaars-Eiden A, Ross JR, Shen WJ, Kraemer FB, Bernlohr DA. 2003. Fatty acid-binding protein hormone-sensitive lipase interaction. Fatty acid dependence on binding. J. Biol. Chem. 278: 47636-47643. https://doi.org/10.1074/jbc.M307680200
  20. Osterlund T, Contreras JA, Holm C. 1997. Identification of essential aspartic acid and histidine residues of hormone-sensitive lipase: apparent residues of the catalytic triad. FEBS Lett. 403: 259-262. https://doi.org/10.1016/S0014-5793(97)00063-X
  21. Watt MJ, Steinberg GR. 2008. Regulation and function of triacylglycerol lipases in cellular metabolism. Biochem. J. 414: 313-325. https://doi.org/10.1042/BJ20080305
  22. Langin D, Laurell H, Holst LS, Belfrage P, Holm C. 1993. Gene organization and primary structure of human hormone-sensitive lipase: possible significance of a sequence homology with a lipase of Moraxella TA144, an antarctic bacterium. Proc. Natl. Acad. Sci. USA 90: 4897-4901. https://doi.org/10.1073/pnas.90.11.4897
  23. Feller G, Thiry M, Gerday C. 1991. Nucleotide sequence of the lipase gene lip2 from the antarctic psychrotroph Moraxella TA144 and site-specific mutagenesis of the conserved serine and histidine residues. DNA Cell Biol. 10: 381-388. https://doi.org/10.1089/dna.1991.10.381
  24. Reddy PG, Allon R, Mevarech M, Mendelovitz S, Sato Y, Gutnick DL. 1989. Cloning and expression in Escherichia coli of an esterase-coding gene from the oil-degrading bacterium Acinetobacter calcoaceticus RAG-1. Gene 76: 145-152. https://doi.org/10.1016/0378-1119(89)90016-4
  25. Raibaud A, Zalacain M, Holt TG, Tizard R, Thompson CJ. 1991. Nucleotide sequence analysis reveals linked N-acetyl hydrolase, thioesterase, transport, and regulatory genes encoded by the bialaphos biosynthetic gene cluster of Streptomyces hygroscopicus. J. Bacteriol. 173: 4454-4463. https://doi.org/10.1128/jb.173.14.4454-4463.1991
  26. Langin D, Holm C. 1993. Sequence similarities between hormone-sensitive lipase and five prokaryotic enzymes. Trends Biochem. Sci. 18: 466-467. https://doi.org/10.1016/0968-0004(93)90007-A
  27. Choo DW, Kurihara T, Suzuki T, Soda K, Esaki N. 1998. A cold-adapted lipase of an Alaskan psychrotroph, Pseudomonas sp. strain B11-1: gene cloning and enzyme purification and characterization. Appl. Environ. Microbiol. 64: 486-491.
  28. Manco G, Adinolfi E, Pisani FM, Ottolina G, Carrea G, Rossi M. 1998. Overexpression and properties of a new thermophilic and thermostable esterase from Bacillus acidocaldarius with sequence similarity to hormone-sensitive lipase subfamily. Biochem. J. 332: 203-212. https://doi.org/10.1042/bj3320203
  29. Mizuguchi S, Amada K, Haruki M, Imanaka T, Morikawa M, Kanaya S. 1999. Identification of the gene encoding esterase, a homolog of hormone-sensitive lipase, from an oildegrading bacterium, strain HD-1. J. Biochem. 126: 731-737. https://doi.org/10.1093/oxfordjournals.jbchem.a022510
  30. Kanaya S, Koyanagi T, Kanaya E. 1998. An esterase from Escherichia coli with a sequence similarity to hormonesensitive lipase. Biochem. J. 332: 75-80. https://doi.org/10.1042/bj3320075
  31. Manco G, Giosue E, D'Auria S, Herman P, Carrea G, Rossi M. 2000. Cloning, overexpression, and properties of a new thermophilic and thermostable esterase with sequence similarity to hormone-sensitive lipase subfamily from the archaeon Archaeoglobus fulgidus. Arch. Biochem. Biophys. 373: 182-192. https://doi.org/10.1006/abbi.1999.1497
  32. Kulakova L, Galkin A, Nakayama T, Nishino T, Esaki N. 2004. Cold-active esterase from Psychrobacter sp. Ant300:gene cloning, characterization, and the effects of Gly-->Pro substitution near the active site on its catalytic activity and stability. Biochim. Biophys. Acta 1696: 59-65. https://doi.org/10.1016/j.bbapap.2003.09.008
  33. Canaan S, Maurin D, Chahinian H, Pouilly B, Durousseau C, Frassinetti F, et al. 2004. Expression and characterization of the protein Rv1399c from Mycobacterium tuberculosis. A novel carboxyl esterase structurally related to the HSL family. Eur. J. Biochem. 271: 3953-3961. https://doi.org/10.1111/j.1432-1033.2004.04335.x
  34. Deb C, Daniel J, Sirakova TD, Abomoelak B, Dubey VS, Kolattukudy PE. 2006. A novel lipase belonging to the hormone-sensitive lipase family induced under starvation to utilize stored triacylglycerol in Mycobacterium tuberculosis. J. Biol. Chem. 281: 3866-3875. https://doi.org/10.1074/jbc.M505556200
  35. Delorme V, Diomande SV, Dedieu L, Cavalier JF, Carriere F, Kremer L, et al. 2012. MmPPOX inhibits Mycobacterium tuberculosis lipolytic enzymes belonging to the hormonesensitive lipase family and alters mycobacterial growth. PLoS One 7: e46493. https://doi.org/10.1371/journal.pone.0046493
  36. Soror SH, Rao R, Cullum J. 2009. Mining the genome sequence for novel enzyme activity: characterisation of an unusual member of the hormone-sensitive lipase family of esterases from the genome of Streptomyces coelicolor A3 (2). Protein Eng. Des. Sel. 36: 333-339.
  37. Sumby KM, Matthews AH, Grbin PR, Jiranek V. 2009. Cloning and characterization of an intracellular esterase from the wine-associated lactic acid bacterium Oenococcus oeni. Appl. Environ. Microbiol. 75: 6729-6735. https://doi.org/10.1128/AEM.01563-09
  38. Bassegoda A, Fillat A, Pastor FI, Diaz P. 2013. Special Rhodococcus sp. CR-53 esterase Est4 contains a GGG(A)X-oxyanion hole conferring activity for the kinetic resolution of tertiary alcohols. Appl. Microbiol. Biotechnol. 97: 8559-8568. https://doi.org/10.1007/s00253-012-4676-x
  39. Virk AP, Sharma P, Capalash N. 2011. A new esterase, belonging to hormone-sensitive lipase family, cloned from Rheinheimera sp. isolated from industrial effluent. J. Microbiol. Biotechnol. 21: 667-674. https://doi.org/10.4014/jmb.1103.03008
  40. Benavente R, Esteban-Torres M, Acebron I, de Las Rivas B, Munoz R, Alvarez Y, et al. 2013. Structure, biochemical characterization and analysis of the pleomorphism of carboxylesterase Cest-2923 from Lactobacillus plantarum WCFS1. FEBS J. 280: 6658-6671. https://doi.org/10.1111/febs.12569
  41. Alvarez Y, Esteban-Torres M, Cortes-Cabrera A, Gago F, Acebron I, Benavente R, et al. 2014. Esterase LpEst1 from Lactobacillus plantarum: a novel and atypical member of the ${\alpha}$${\beta}$ hydrolase superfamily of enzymes. PLoS One 9: e92257. https://doi.org/10.1371/journal.pone.0092257
  42. Jadeja D, Dogra N, Arya S, Singh G, Singh G, Kaur J. 2016. Characterization of LipN (Rv2970c) of Mycobacterium tuberculosis H37Rv and its probable role in Xenobiotic degradation. J. Cell. Biochem. 117: 390-401. https://doi.org/10.1002/jcb.25285
  43. Li C, Li Q, Zhang Y, Gong Z, Ren S, Li P, Xie J. 2017. Characterization and function of Mycobacterium tuberculosis H37Rv lipase Rv1076 (LipU). Microbiol. Res. 196: 7-16. https://doi.org/10.1016/j.micres.2016.12.005
  44. Lin Y, Li Q, Xie L, Xie J. 2017. Mycobacterium tuberculosis rv1400c encodes functional lipase/esterase. Protein Expr. Purif. 129: 143-149. https://doi.org/10.1016/j.pep.2016.04.013
  45. Dua A, Gupta R. 2017. Functional characterization of hormone-sensitive-like lipase from Bacillus halodurans:synthesis and recovery of pNP-laurate with high yields. Extremophiles DOI: 10.1007/s00792-017-0949-8 [In Press].
  46. Lee SW, Won K, Lim HK, Kim JC, Choi GJ, Cho KY. 2004. Screening for novel lipolytic enzymes from uncultured soil microorganisms. Appl. Microbiol. Biotechnol. 65: 720-726. https://doi.org/10.1007/s00253-004-1722-3
  47. Rhee JK, Ahn DG, Kim YG, Oh JW. 2005. New thermophilic and thermostable esterase with sequence similarity to the hormone-sensitive lipase family, cloned from a metagenomic library. Appl. Environ. Microbiol. 71: 817-825. https://doi.org/10.1128/AEM.71.2.817-825.2005
  48. Kim YJ, Choi GS, Kim SB, Yoon GS, Kim YS, Ryu YW. 2006. Screening and characterization of a novel esterase from a metagenomic library. Protein Expr. Purif. 45: 315-323. https://doi.org/10.1016/j.pep.2005.06.008
  49. Hong KS, Lim HK, Chung EJ, Park EJ, Lee MH, Kim JC, et al. 2007. Selection and characterization of forest soil metagenome genes encoding lipolytic enzymes. J. Microbiol. Biotechnol. 17: 1655-1660.
  50. Hardeman F, Sjoling S. 2007. Metagenomic approach for the isolation of a novel low-temperature-active lipase from uncultured bacteria of marine sediment. FEMS Microbiol. Ecol. 59: 524-534. https://doi.org/10.1111/j.1574-6941.2006.00206.x
  51. Chu X, He H, Guo C, Sun B. 2008. Identification of two novel esterases from a marine metagenomic library derived from South China Sea. Appl. Microbiol. Biotechnol. 80: 615-625. https://doi.org/10.1007/s00253-008-1566-3
  52. Roh C, Villatte F. 2008. Isolation of a low-temperature adapted lipolytic enzyme from uncultivated microorganism. J. Appl. Microbiol. 105: 116-123. https://doi.org/10.1111/j.1365-2672.2007.03717.x
  53. Nam KH, Kim MY, Kim SJ, Priyadarshi A, Lee WH, Hwang KY. 2009. Structural and functional analysis of a novel EstE5 belonging to the subfamily of hormone-sensitive lipase. Biochem. Biophys. Res. Commun. 379: 553-556. https://doi.org/10.1016/j.bbrc.2008.12.085
  54. Rashamuse K, Ronneburg T, Hennessy F, Visser D, van Heerden E, Piater L, et al. 2009. Discovery of a novel carboxylesterase through functional screening of a preenriched environmental library. J. Appl. Microbiol. 106:1532-1539. https://doi.org/10.1111/j.1365-2672.2008.04114.x
  55. Bunterngsook B, Kanokratana P, Thongaram T, Tanapongpipat S, Uengwetwanit T, Rachdawong S, et al. 2010. Identification and characterization of lipolytic enzymes from a peatswamp forest soil metagenome. Biosci. Biotechnol. Biochem. 74: 1848-1854. https://doi.org/10.1271/bbb.100249
  56. Tao W, Lee MH, Yoon MY, Kim JC, Malhotra S, Wu J, et al. 2011. Characterization of two metagenome-derived esterases that reactivate chloramphenicol by counteracting chloramphenicol acetyltransferase. J. Microbiol. Biotechnol. 21: 1203-1210. https://doi.org/10.4014/jmb.1107.07034
  57. Ko KC, Rim SO, Han Y, Shin BS, Kim GJ, Choi JH, et al. 2012. Identification and characterization of a novel coldadapted esterase from a metagenomic library of mountain soil. J. Ind. Microbiol. Biotechnol. 39: 681-689. https://doi.org/10.1007/s10295-011-1080-y
  58. Jiang X, Xu X, Huo Y, Wu Y, Zhu X, Zhang X, et al. 2012. Identification and characterization of novel esterases from a deep-sea sediment metagenome. Arch. Microbiol. 194: 207-214. https://doi.org/10.1007/s00203-011-0745-2
  59. Jeon JH, Lee HS, Kim JT, Kim SJ, Choi SH, Kang SG, et al. 2012. Identification of a new subfamily of salt-tolerant esterases from a metagenomic library of tidal flat sediment. Appl. Microbiol. Biotechnol. 93: 623-631. https://doi.org/10.1007/s00253-011-3433-x
  60. Biver S, Vandenbol M. 2013. Characterization of three new carboxylic ester hydrolases isolated by functional screening of a forest soil metagenomic library. J. Ind. Microbiol. Biotechnol. 40: 191-200. https://doi.org/10.1007/s10295-012-1217-7
  61. Li PY, Ji P, Li CY, Zhang Y, Wang GL, Zhang XY, et al. 2014. Structural basis for dimerization and catalysis of a novel esterase from the GTSAG motif subfamily of the bacterial hormone-sensitive lipase family. J. Biol. Chem. 289:19031-19041. https://doi.org/10.1074/jbc.M114.574913
  62. Petrovskaya LE, Novototskaya-Vlasova KA, Spirina EV, Durdenko EV, Lomakina GY, Zavialova MG, et al. 2016. Expression and characterization of a new esterase with GCSAG motif from a permafrost metagenomic library. FEMS Microbiol. Ecol. 92: fiw046. https://doi.org/10.1093/femsec/fiw046
  63. Petrovskaya LE, Novototskaya-Vlasova KA, Gapizov SS, Spirina EV, Durdenko EV, Rivkina EM. 2016. New member of the hormone-sensitive lipase family from the permafrost microbial community. Bioengineered 7: 1-4 https://doi.org/10.1080/21655979.2016.1153357
  64. Dukunde A, Schneider D, Lu M, Brady S, Daniel R. 2017. A novel, versatile family IV carboxylesterase exhibits high stability and activity in a broad pH spectrum. Biotechnol. Lett. 39: 577-587. https://doi.org/10.1007/s10529-016-2282-1
  65. Ben Ali Y, Chahinian H, Petry S, Muller G, Lebrun R, Verger R, et al. 2006. Use of an inhibitor to identify members of the hormone-sensitive lipase family. Biochemistry 45:14183-14191. https://doi.org/10.1021/bi0613978
  66. Ascione G, de Pascale D, De Santi C, Pedone C, Dathan NA, Monti SM. 2012. Native expression and purification of hormone-sensitive lipase from Psychrobacter sp. TA144 enhances protein stability and activity. Biochem. Biophys. Res. Commun. 420: 542-546. https://doi.org/10.1016/j.bbrc.2012.03.028
  67. Alvarez Y, Esteban-Torres M, Acebron I, de las Rivas B, Munoz R, Martinez-Ripoll M, et al. 2011. Preliminary X-ray analysis of twinned crystals of the Q88Y25_Lacpl esterase from Lactobacillus plantarum. Acta Crystallogr. F Struct. Biol. Cryst. Commun. 67: 1436-1439. https://doi.org/10.1107/S1744309111036682
  68. Wei Y, Contreras JA, Sheffield P, Osterlund T, Derewenda U, Kneusel RE, et al. 1999. Crystal structure of brefeldin A esterase, a bacterial homolog of the mammalian hormonesensitive lipase. Nat. Struct. Biol. 6: 340-345. https://doi.org/10.1038/7576
  69. De Simone G, Galdiero S, Manco G, Lang D, Rossi M, Pedone C. 2000. A snapshot of a transition state analogue of a novel thermophilic esterase belonging to the subfamily of mammalian hormone-sensitive lipase. J. Mol. Biol. 303:761-771. https://doi.org/10.1006/jmbi.2000.4195
  70. De Simone G, Menchise V, Manco G, Mandrich L, Sorrentino N, Lang D, et al. 2001. The crystal structure of a hyper-thermophilic carboxylesterase from the archaeon Archaeoglobus fulgidus. J. Mol. Biol. 314: 507-518. https://doi.org/10.1006/jmbi.2001.5152
  71. Byun JS, Rhee JK, Kim ND, Yoon J, Kim DU, Koh E, et al. 2007. Crystal structure of hyperthermophilic esterase EstE1 and the relationship between its dimerization and thermostability properties. BMC Struct. Biol. 7: 47 https://doi.org/10.1186/1472-6807-7-47
  72. Nam KH, Kim SJ, Priyadarshi A, Kim HS, Hwang KY. 2009. The crystal structure of an HSL-homolog EstE5 complex with PMSF reveals a unique configuration that inhibits the nucleophile Ser144 in catalytic triads. Biochem. Biophys. Res. Commun. 389: 247-250. https://doi.org/10.1016/j.bbrc.2009.08.123
  73. Angkawidjaja C, Koga Y, Takano K, Kanaya S. 2012. Structure and stability of a thermostable carboxylesterase from the thermoacidophilic archaeon Sulfolobus tokodaii. FEBS J. 279: 3071-3084. https://doi.org/10.1111/j.1742-4658.2012.08687.x
  74. Nam KH, Kim MY, Kim SJ, Priyadarshi A, Kwon ST, Koo BS, et al. 2009. Structural and functional analysis of a novel hormone-sensitive lipase from a metagenome library. Proteins 74: 1036-1040. https://doi.org/10.1002/prot.22313
  75. Palm GJ, Fernandez-Alvaro E, Bogdanovic X, Bartsch S, Sczodrok J, Singh RK, et al. 2011. The crystal structure of an esterase from the hyperthermophilic microorganism Pyrobaculum calidifontis VA1 explains its enantioselectivity. Appl. Microbiol. Biotechnol. 91: 1061-1072. https://doi.org/10.1007/s00253-011-3337-9
  76. Zheng X, Guo J, Xu L, Li H, Zhang D, Zhang K, et al. 2011. Crystal structure of a novel esterase Rv0045c from Mycobacterium tuberculosis. PLoS One 6: e20506. https://doi.org/10.1371/journal.pone.0020506
  77. Ngo TD, Ryu BH, Ju H, Jang E, Park K, Kim KK, et al. 2013. Structural and functional analyses of a bacterial homologue of hormone-sensitive lipase from a metagenomic library. Acta Crystallogr. D Biol. Crystallogr. 69: 1726-1737. https://doi.org/10.1107/S0907444913013425
  78. Li PY, Chen XL, Ji P, Li CY, Wang P, Zhang Y, et al. 2015. Interdomain hydrophobic interactions modulate the thermostability of microbial esterases from the hormonesensitive lipase family. J. Biol. Chem. 290: 11188-11198. https://doi.org/10.1074/jbc.M115.646182
  79. Huang J, Huo YY, Ji R, Kuang S, Ji C, Xu XW, et al. 2016. Structural insights of a hormone-sensitive lipase homologue Est22. Sci. Rep. 6: 28550. https://doi.org/10.1038/srep28550
  80. Rauwerdink A, Kazlauskas RJ. 2015. How the same core catalytic machinery catalyzes 17 different reactions: the serine-histidine-aspartate catalytic triad of ${\alpha}$/${\beta}$-hydrolase fold enzymes. ACS Catal. 5: 6153-6176. https://doi.org/10.1021/acscatal.5b01539
  81. Marchot P, Chatonnet A. 2012. Enzymatic activity and protein interactions in alpha/beta hydrolase fold proteins:moonlighting versus promiscuity. Protein Pept. Lett. 19:132-143. https://doi.org/10.2174/092986612799080284
  82. Jochens H, Hesseler M, Stiba K, Padhi SK, Kazlauskas RJ, Bornscheuer UT. 2011. Protein engineering of ${\alpha}$/${\beta}$-hydrolase fold enzymes. Chembiochem 12: 1508-1517. https://doi.org/10.1002/cbic.201000771
  83. Mandrich L, Merone L, Pezzullo M, Cipolla L, Nicotra F, Rossi M, et al. 2005. Role of the N terminus in enzyme activity, stability and specificity in thermophilic esterases belonging to the HSL family. J. Mol. Biol. 345: 501-512. https://doi.org/10.1016/j.jmb.2004.10.035
  84. Wang J, Shen WJ, Patel S, Harada K, Kraemer FB. 2005. Mutational analysis of the “regulatory module” of hormonesensitive lipase. Biochemistry 44: 1953-1959. https://doi.org/10.1021/bi049206t
  85. Krintel C, Morgelin M, Logan DT, Holm C. 2009. Phosphorylation of hormone-sensitive lipase by protein kinase A in vitro promotes an increase in its hydrophobic surface area. FEBS J. 276: 4752-4762. https://doi.org/10.1111/j.1742-4658.2009.07172.x
  86. Sherlin D, Anishetty S. 2015. Mechanistic insights from molecular dynamic simulation of Rv0045c esterase in Mycobacterium tuberculosis. J. Mol. Model. 21: 90. https://doi.org/10.1007/s00894-015-2630-4
  87. Manco G, Febbraio F, Adinolfi E, Rossi M. 1999. Homology modeling and active-site residues probing of the thermophilic Alicyclobacillus acidocaldarius esterase 2. Protein Sci. 8: 1789-1796. https://doi.org/10.1110/ps.8.9.1789
  88. Haruki M, Oohashi Y, Mizuguchi S, Matsuo Y, Morikawa M, Kanaya, S. 1999. Identification of catalytically essential residues in Escherichia coli esterase by site-directed mutagenesis. FEBS Lett. 454: 262-266. https://doi.org/10.1016/S0014-5793(99)00813-3
  89. Mandrich L, Menchise V, Alterio V, De Simone G, Pedone C, Rossi M, et al. 2008. Functional and structural features of the oxyanion hole in a thermophilic esterase from Alicyclobacillus acidocaldarius. Proteins 71: 1721-1731.
  90. Neves Petersen MT, Fojan P, Petersen SB. How do lipases and esterases work: the electrostatic contribution. J. Biotechnol. 85: 115-147.
  91. Kourist R, Krishna S, Patel JS, Bartnek F, Hitchman TS, Weiner DP, et al. 2007. Identification of a metagenomederived esterase with high enantioselectivity in the kinetic resolution of arylaliphatic tertiary alcohols. Org. Biomol. Chem. 5: 3310-3313. https://doi.org/10.1039/b709965g
  92. Rehdorf J, Behrens GA, Nguyen GS, Kourist R, Bornscheuer UT. 2012. Pseudomonas putida esterase contains a GGG(A)Xmotif confering activity for the kinetic resolution of tertiary alcohols. Appl. Microbiol. Biotechnol. 93: 1119-1126. https://doi.org/10.1007/s00253-011-3464-3
  93. Schiefner A, Gerber K, Brosig A, Boos W. 2014 Structural and mutational analyses of Aes, an inhibitor of MalT in Escherichia coli. Proteins 82: 268-277. https://doi.org/10.1002/prot.24383
  94. Truongvan N, Chung HS, Jang SH, Lee C. 2016. Conserved tyrosine 182 residue in hyperthermophilic esterase EstE1 plays a critical role in stabilizing the active site. Extremophiles 20: 187-193. https://doi.org/10.1007/s00792-016-0812-3
  95. Yuhong Z, Shi P, Liu W, Meng K, Bai Y, Wang G, et al. 2009. Lipase diversity in glacier soil based on analysis of metagenomic DNA fragments and cell culture. J. Microbiol. Biotechnol. 19: 888-897. https://doi.org/10.4014/jmb.0812.695
  96. Rhee JK, Kim DY, Ahn DG, Yun JH, Jang SH, Shin HC, et al. 2006. Analysis of the thermostability determinants of hyperthermophilic esterase EstE1 based on its predicted three-dimensional structure. Appl. Environ. Microbiol. 72:3021-3025. https://doi.org/10.1128/AEM.72.4.3021-3025.2006
  97. Pezzullo M, Del Vecchio P, Mandrich L, Nucci R, Rossi M, Manco G. 2013. Comprehensive analysis of surface charged residues involved in thermal stability in Alicyclobacillus acidocaldarius esterase 2. Protein Eng. Des. Sel. 26: 47-58. https://doi.org/10.1093/protein/gzs066
  98. Mandrich L, Merone L, Manco G. 2009. Structural and kinetic overview of the carboxylesterase EST2 from Alicyclobacillus acidocaldarius: a comparison with the other members of the HSL family. Protein Pept. Lett. 16: 1189-1200. https://doi.org/10.2174/092986609789071261
  99. De Santi C, Tutino ML, Mandrich L, Giuliani M, Parrilli E, Del Vecchio P, et al. 2010. The hormone-sensitive lipase from Psychrobacter sp. TA144: new insight in the structural/functional characterization. Biochimie 92: 949-957. https://doi.org/10.1016/j.biochi.2010.04.001
  100. Manco G, Mandrich L, Rossi M. 2001. 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. 276: 37482-37490. https://doi.org/10.1074/jbc.M103017200
  101. De Simone G, Mandrich L, Menchise V, Giordano V, Febbraio F, Rossi M, et al. 2004. A substrate-induced switch in the reaction mechanism of a thermophilic esterase: kinetic evidences and structural basis. J. Biol. Chem. 279: 6815-6823. https://doi.org/10.1074/jbc.M307738200
  102. Li C, Li Q, Zhang Y, Gong Z, Ren S, Li P, et al. 2017. Characterization and function of Mycobacterium tuberculosis H37Rv lipase Rv1076 (LipU). Microbiol. Res. 196: 7-16. https://doi.org/10.1016/j.micres.2016.12.005
  103. Kim S, Joo S, Yoon HC, Ryu Y, Kim KK, Kim TD. 2007. Purification, crystallization and preliminary crystallographic analysis of Est25: a ketoprofen-specific hormone-sensitive lipase. Acta Crystallogr. F Struct. Biol. Cryst. Commun. 63:579-581. https://doi.org/10.1107/S1744309107026152
  104. Manco G, Carrea G, Giosue E, Ottolina G, Adamo G, Rossi M. 2002. Modification of the enantioselectivity of two homologous thermophilic carboxylesterases from Alicyclobacillus acidocaldarius and Archaeoglobus fulgidus by random mutagenesis and screening. Extremophiles 6: 325-331. https://doi.org/10.1007/s00792-001-0261-4
  105. Febbraio F, Merone L, Cetrangolo GP, Rossi M, Nucci R, Manco G. 2011. Thermostable esterase 2 from Alicyclobacillus acidocaldarius as biosensor for the detection of organophosphate pesticides. Anal. Chem. 83: 1530-1536. https://doi.org/10.1021/ac102025z
  106. Pohlmann C, Wang Y, Humenik M, Heidenreich B, Gareis M, Sprinzl M. 2009. Rapid, specific and sensitive electrochemical detection of foodborne bacteria. Biosens. Bioelectron. 24:2766-2771. https://doi.org/10.1016/j.bios.2009.01.042
  107. Zhu X, Larsen NA, Basran A, Bruce NC, Wilson IA. 2003. Observation of an arsenic adduct in an acetyl esterase crystal structure. J. Biol. Chem. 278: 2008-2014. https://doi.org/10.1074/jbc.M210103200

Cited by

  1. Biochemical profiles of two thermostable and organic solvent-tolerant esterases derived from a compost metagenome vol.103, pp.8, 2017, https://doi.org/10.1007/s00253-019-09695-1
  2. Molecular Characterization of a Novel Cold-Active Hormone-Sensitive Lipase (HaHSL) from Halocynthiibacter Arcticus vol.9, pp.11, 2019, https://doi.org/10.3390/biom9110704
  3. Crystal structure of PMGL2 esterase from the hormone-sensitive lipase family with GCSAG motif around the catalytic serine vol.15, pp.1, 2017, https://doi.org/10.1371/journal.pone.0226838
  4. Expression, Characterisation and Homology Modelling of a Novel Hormone-Sensitive Lipase (HSL)-Like Esterase from Glaciozyma antarctica vol.10, pp.1, 2017, https://doi.org/10.3390/catal10010058
  5. Characterization of a Novel Moderately Thermophilic Solvent-Tolerant Esterase Isolated From a Compost Metagenome Library vol.10, pp.None, 2017, https://doi.org/10.3389/fmicb.2019.03069
  6. Biochemical characterization of an esterase from Clostridium acetobutylicum with novel GYSMG pentapeptide motif at the catalytic domain vol.47, pp.2, 2017, https://doi.org/10.1007/s10295-019-02253-8
  7. Enzyme Promiscuous Activity: How to Define it and its Evolutionary Aspects vol.27, pp.5, 2017, https://doi.org/10.2174/0929866527666191223141205
  8. Effect of Cysteine Residue Substitution in the GCSAG Motif of the PMGL2 Esterase Active Site on the Enzyme Properties vol.85, pp.6, 2017, https://doi.org/10.1134/s0006297920060085
  9. Crystallization and Preliminary X-ray Diffraction Study of a Novel Bacterial Homologue of Mammalian Hormone-Sensitive Lipase (halip1) from Halocynthiibacter arcticus vol.10, pp.11, 2020, https://doi.org/10.3390/cryst10110963
  10. Structural and Biochemical Characterization of a Cold-Active PMGL3 Esterase with Unusual Oligomeric Structure vol.11, pp.1, 2017, https://doi.org/10.3390/biom11010057
  11. Biochemical and Structural Characterization of a novel thermophilic esterase EstD11 provide catalytic insights for the HSL family vol.19, pp.None, 2017, https://doi.org/10.1016/j.csbj.2021.01.047
  12. Characterization of a Novel Family IV Esterase Containing a Predicted CzcO Domain and a Family V Esterase with Broad Substrate Specificity from an Oil-Polluted Mud Flat Metagenomic Library vol.11, pp.13, 2017, https://doi.org/10.3390/app11135905
  13. Identification and Biochemical Characterization of a Novel Hormone-Sensitive Lipase Family Esterase Est19 from the Antarctic Bacterium Pseudomonas sp. E2-15 vol.11, pp.11, 2017, https://doi.org/10.3390/biom11111552