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Review Article

An overview of mammalian and microbial hormone-sensitive lipases (lipolytic family IV): biochemical properties and industrial applications

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Received 20 Jun 2022, Accepted 13 Sep 2022, Published online: 25 Sep 2022

References

  • Alvarez, Y., Esteban-Torres, M., Cortés-Cabrera, Á., Gago, F., Acebrón, I., Benavente, R., Mardo, K., de las Rivas, B., Muñoz, R., & Mancheño, J. M. (2014). Esterase LpEst1 from Lactobacillus plantarum: A Novel and a typical member of the αβ hydrolase superfamily of enzymes. PLoS ONE, 9(3), e92257. https://doi.org/10.1371/journal.pone.0092257
  • Angkawidjaja, C., Koga, Y., Takano, K., & Kanaya, S. (2012). Structure and stability of a thermostable carboxylesterase from the thermoacidophilic archaeon Sulfolobus tokodaii: Structural study on S. tokodaii carboxylesterase. The FEBS Journal, 279(17), 3071–3084. https://doi.org/10.1111/j.1742-4658.2012.08687.x
  • Anthonsen, M. W., Degerman, E., & Holm, C. (1997). Partial purification and identification of hormone-sensitive lipase from chicken adipose tissue. Biochemical and Biophysical Research Communications, 236(1), 94–99. https://doi.org/10.1006/bbrc.1997.6923
  • Arner, P., & Langin, D. (2007). The role of neutral lipases in human adipose tissue lipolysis. Current Opinion in Lipidology, 18(3), 246–250. https://doi.org/10.1097/MOL.0b013e32811e16fb
  • Arpigny, J. L., & Jaeger, K. E. (1999). Bacterial lipolytic enzymes: Classification and properties. The Biochemical Journal, 343(1), 177–183. https://doi.org/10.1042/bj3430177
  • Bassegoda, A., Fillat, A., Pastor, F. I. J., & 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. Applied Microbiology and Biotechnology, 97(19), 8559–8568. https://doi.org/10.1007/s00253-012-4676-x
  • Bassegoda, A., Pastor, F. I. J., & Diaz, P. (2012). Rhodococcus sp. Strain CR-53 LipR, the first member of a new bacterial lipase family (family X) displaying an unusual Y-type oxyanion hole, similar to the Candida antarctica lipase Clan. Applied and Environmental Microbiology, 78(6), 1724–1732. https://doi.org/10.1128/AEM.06332-11
  • Ben Ali, Y., Chahinian, H., Petry, S., Muller, G., Carrière, F., Verger, R., & Abousalham, A. (2004). Might the kinetic behavior of hormone-sensitive lipase reflect the absence of the lid domain? Biochemistry, 43(29), 9298–9306. https://doi.org/10.1021/bi049479o
  • Benavente, R., Esteban-Torres, M., Acebrón, I., de las Rivas, B., Muñoz, R., Álvarez, Y., & Mancheño, J. M. (2013). Structure, biochemical characterization and analysis of the pleomorphism of carboxylesterase Cest-2923 from Lactobacillus plantarum WCFS1. The FEBS Journal, 280(24), 6658–6671. https://doi.org/10.1111/febs.12569
  • Biundo, A., Hromic, A., Pavkov-Keller, T., Gruber, K., Quartinello, F., Haernvall, K., Perz, V., Arrell, M. S., Zinn, M., Ribitsch, D., & Guebitz, G. M. (2016). Characterization of a poly(butylene adipate-co-terephthalate)- hydrolyzing lipase from Pelosinus fermentans. Applied Microbiology and Biotechnology, 100(4), 1753–1764. https://doi.org/10.1007/s00253-015-7031-1
  • Biver, S., & Vandenbol, M. (2013). Characterization of three new carboxylic ester hydrolases isolated by functional screening of a forest soil metagenomic library. Journal of Industrial Microbiology & Biotechnology, 40(2), 191–200. https://doi.org/10.1007/s10295-012-1217-7
  • Blow, D. M., Birktoft, J. J., & Hartley, B. S. (1969). Role of a buried acid group in the mechanism of action of chymotrypsin. Nature, 221(5178), 337–340. https://doi.org/10.1038/221337a0
  • Bornscheuer, U. T. (2002). Microbial carboxyl esterases: Classification, properties and application in biocatalysis. FEMS Microbiology Reviews, 26(1), 73–81. https://doi.org/10.1111/j.1574-6976.2002.tb00599.x
  • Bunterngsook, B., Kanokratana, P., Thongaram, T., Tanapongpipat, S., Uengwetwanit, T., Rachdawong, S., Vichitsoonthonkul, T., & Eurwilaichitr, L. (2010). Identification and characterization of lipolytic enzymes from a peat-swamp forest soil metagenome. Bioscience, Biotechnology, and Biochemistry, 74(9), 1848–1854. https://doi.org/10.1271/bbb.100249
  • Byun, J.-S., Rhee, J.-K., Kim, N. D., Yoon, J., Kim, D.-U., Koh, E., Oh, J.-W., & Cho, H.-S. (2007). Crystal structure of hyperthermophilic esterase EstE1 and the relationship between its dimerization and thermostability properties. BMC Structural Biology, 7(1), 47. https://doi.org/10.1186/1472-6807-7-47
  • Cai, X., Wang, W., Lin, L., He, D., Huang, G., Shen, Y., Wei, W., & Wei, D. (2017). Autotransporter domain-dependent enzymatic analysis of a novel extremely thermostable carboxylesterase with high biodegradability towards pyrethroid pesticides. Scientific Reports, 7(1), 3461. https://doi.org/10.1038/s41598-017-03561-8
  • Castilla, A., Panizza, P., Rodríguez, D., Bonino, L., Díaz, P., Irazoqui, G., & Rodríguez Giordano, S. (2017). A novel thermophilic and halophilic esterase from Janibacter sp. R02, the first member of a new lipase family (Family XVII). Enzyme and Microbial Technology, 98, 86–95. https://doi.org/10.1016/j.enzmictec.2016.12.010
  • Chahiniana, H., & Sarda, L. (2009). Distinction between esterases and lipases: Comparative biochemical properties of sequence-related carboxylesterases. Protein & Peptide Letters, 16(10), 1149–1161. https://doi.org/10.2174/092986609789071333
  • Choi, Y.-H., Lee, Y.-N., Park, Y.-J., Yoon, S.-J., & Lee, H.-B. (2016). Identification of amino acids related to catalytic function of Sulfolobus solfataricus P1 carboxylesterase by site-directed mutagenesis and molecular modeling. BMB Reports, 49(6), 349–354. https://doi.org/10.5483/bmbrep.2016.49.6.077
  • Chow, J., Kovacic, F., Dall Antonia, Y., Krauss, U., Fersini, F., Schmeisser, C., Lauinger, B., Bongen, P., Pietruszka, J., Schmidt, M., Menyes, I., Bornscheuer, U. T., Eckstein, M., Thum, O., Liese, A., Mueller Dieckmann, J., Jaeger, K.-E., & Streit, W. R. (2012). The metagenome-derived Enzymes LipS and LipT increase the diversity of known lipases. PLoS ONE, 7(10), e47665. https://doi.org/10.1371/journal.pone.0047665
  • Chu, X., He, H., Guo, C., & Sun, B. (2008). Identification of two novel esterases from a marine metagenomic library derived from South China Sea. Applied Microbiology and Biotechnology, 80(4), 615–625. https://doi.org/10.1007/s00253-008-1566-3
  • Cordle, S. R., Colbran, R. J., & Yeaman, S. J. (1986). Hormone-Sensitive lipase from bovine adipose tissue. Biochimica Et Biophysica Acta, 887(1), 51–57. https://doi.org/10.1016/0167-4889(86)90121-7
  • Couto, G. H., Glogauer, A., Faoro, H., Chubatsu, L. S., Souza, E. M., & Pedrosa, F. O. (2010). Isolation of a novel lipase from a metagenomic library derived from mangrove sediment from the south Brazilian coast. Genetics and Molecular Research, 9(1), 514–523. https://doi.org/10.4238/vol9-1gmr738
  • Derewenda, Z. S., Wei, Y., Contreras, J. A., Sheffield, P., Osterlund, T., Derewenda, U., Kneusel, R. E., Matern, U., & Holm, C. (1999). No title found. Nature Structural Biology, 6(4), 340–345. https://doi.org/10.1038/7576
  • 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 1 1edited by D. Rees. Journal of Molecular Biology, 303(5), 761–771. https://doi.org/10.1006/jmbi.2000.4195
  • De Simone, G., Menchise, V., Manco, G., Mandrich, L., Sorrentino, N., Lang, D., Rossi, M., & Pedone, C. (2001). The crystal structure of a hyper-thermophilic carboxylesterase from the archaeon Archaeoglobus fulgidus 1 1edited by R. Huber. Journal of Molecular Biology, 314(3), 507–518. https://doi.org/10.1006/jmbi.2001.5152
  • Dou, S., Kong, X.-D., Ma, B.-D., Chen, Q., Zhang, J., Zhou, J., & Xu, J.-H. (2014). Crystal structures of Pseudomonas putida esterase reveal the functional role of residues 187 and 287 in substrate binding and chiral recognition. Biochemical and Biophysical Research Communications, 446(4), 1145–1150. https://doi.org/10.1016/j.bbrc.2014.03.072
  • 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, 21(5), 871–889. https://doi.org/10.1007/s00792-017-0949-8
  • 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. Biotechnology Letters, 39(4), 577–587. https://doi.org/10.1007/s10529-016-2282-1
  • Fang, Z., Li, J., Wang, Q., Fang, W., Peng, H., Zhang, X., & Xiao, Y. (2014). A novel esterase from a marine metagenomic library exhibiting salt tolerance ability. Journal of Microbiology and Biotechnology, 24(6), 771–780. https://doi.org/10.4014/jmb.1311.11071
  • Febbraio, F., Merone, L., Cetrangolo, G. P., Rossi, M., Nucci, R., & Manco, G. (2011). Thermostable esterase 2 from Alicyclobacillus acidocaldarius as biosensor for the detection of organophosphate pesticides. Analytical Chemistry, 83(5), 1530–1536. https://doi.org/10.1021/ac102025z
  • Feller, G., Thiry, M., & Gerday, C. (1991). Nucleotide sequence of the lipase gene lip2 from the Antarctic psychrotroph Moraxella TA 144 and site-specific mutagenesis of the conserved serine and histidine residues. DNA and Cell Biology, 10(5), 381–388. https://doi.org/10.1089/dna.1991.10.381
  • Fojan, P. (2000). What distinguishes an esterase from a lipase: A novel structural approach. Biochimie, 82(11), 1033–1041. https://doi.org/10.1016/S0300-9084(00)01188-3
  • Fredrikson, G., Strålfors, P., Nilsson, N. O., & Belfrage, P. (1981). Hormone-Sensitive lipase of rat adipose tissue. purification and some properties. The Journal of Biological Chemistry, 256(12), 6311–6320. https://doi.org/10.1016/S0021-9258(19)69164-7
  • Gaur, R., Hemamalini, R., & Khare, S. K. (2017). Lipolytic Enzymes. Current Developments in Biotechnology and Bioengineering, 175–198. Elsevier. https://doi.org/10.1016/B978-0-444-63662-1.00008-7
  • Gobbetti, M., Fox, P. F., & Stepaniak, L. (1997). Isolation and characterization of a tributyrin esterase from Lactobacillus plantarum 2739. Journal of Dairy Science, 80(12), 3099–3106. https://doi.org/10.3168/jds.S0022-0302(97)76280-5
  • Handrick, R., Reinhardt, S., Focarete, M. L., Scandola, M., Adamus, G., Kowalczuk, M., & Jendrossek, D. (2001). A new type of thermoalkalophilic hydrolase of Paucimonas lemoignei with high specificity for amorphous polyesters of short chain-length hydroxyalkanoic acids. The Journal of Biological Chemistry, 276(39), 36215–36224. https://doi.org/10.1074/jbc.M101106200
  • Hardeman, F., & Sara Sjoling, S. (2007). Metagenomic approach for the isolation of a novel low-temperature-active lipase from uncultured bacteria of marine sediment: Low-temperature Lipase by metagenomics. FEMS Microbiology Ecology, 59(2), 524–534. https://doi.org/10.1111/j.1574-6941.2006.00206.x
  • Hitch, T. C. A., & Clavel, T. (2019). A proposed update for the classification and description of bacterial lipolytic enzymes. PeerJ, 7, e7249. https://doi.org/10.7717/peerj.7249
  • Holm C, Kirchgessner T G, Svenson K L, Lusis A J, Belfrage P and Schotz M C. (1988). Nucleotide sequence of rat adipose hormone sensitive lipase cDNA. Nucl Acids Res, 16(20), 9879–9879. doi: 10.1093/nar/16.20.9879.
  • Hong, K. S., Lim, H. K., Chung, E. J., Park, E. J., Lee, M. H., Kim, J.-C., Choi, G. J., Cho, K. Y., & Lee, S.-W. (2007). Selection and characterization of forest soil metagenome genes encoding lipolytic enzymes. Journal of Microbiology and Biotechnology, 17(10), 1655–1660.
  • Hotta, Y., Ezaki, S., Atomi, H., & Imanaka, T. (2002). Extremely stable and versatile carboxylesterase from a hyperthermophilic archaeon. Applied and Environmental Microbiology, 68(8), 3925–3931. https://doi.org/10.1128/AEM.68.8.3925-3931.2002
  • Huang J, Huo Y, Ji R, Kuang S, Ji C, Xu X and Li J. (2016). Structural insights of a hormone sensitive lipase homologue Est22. Sci Rep, 6(1). doi:10.1038/srep28550.
  • Huang, J., Huo, Y.-Y., Ji, R., Kuang, S., Ji, C., Xu, X.-W., & Li, J. (2016). Structural insights of a hormone sensitive lipase homologue Est22. Scientific Reports, 6(1), 28550. https://doi.org/10.1038/srep28550
  • Hu, Y., Fu, C., Huang, Y., Yin, Y., Cheng, G., Lei, F., Lu, N., Li, J., Ashforth, E. J., Zhang, L., & Zhu, B. (2010). Novel lipolytic genes from the microbial metagenomic library of the South China Sea marine sediment. FEMS Microbiology Ecology, 72(2), 228–237. https://doi.org/10.1111/j.1574-6941.2010.00851.x
  • Huo, Y.-Y., Jian, S.-L., Cheng, H., Rong, Z., Cui, H.-L., & Xu, X.-W. (2018). Two novel deep-sea sediment metagenome-derived esterases: Residue 199 is the determinant of substrate specificity and preference. Microbial Cell Factories, 17(1), 16. https://doi.org/10.1186/s12934-018-0864-4
  • Jaeger, K.-E., & Eggert, T. (2002). Lipases for biotechnology. Current Opinion in Biotechnology, 13(4), 390–397. https://doi.org/10.1016/S0958-1669(02)00341-5
  • Jeon, J. H., Kim, J. T., Lee, H. S., Kim, S.-J., Kang, S. G., Choi, S. H., & Lee, J.-H. (2011). Novel lipolytic enzymes identified from metagenomic library of deep-sea sediment. Evidence-Based Complementary and Alternative Medicine, 2011, 1–9. https://doi.org/10.1155/2011/271419
  • Jeon, J. H., Lee, H. S., Kim, J. T., Kim, S.-J., Choi, S. H., Kang, S. G., & Lee, J.-H. (2012). Identification of a new subfamily of salt-tolerant esterases from a metagenomic library of tidal flat sediment. Applied Microbiology and Biotechnology, 93(2), 623–631. https://doi.org/10.1007/s00253-011-3433-x
  • Jiang, X., Xu, X., Huo, Y., Wu, Y., Zhu, X., Zhang, X., & Wu, M. (2012). Identification and characterization of novel esterases from a deep-sea sediment metagenome. Archives of Microbiology, 194(3), 207–214. https://doi.org/10.1007/s00203-011-0745-2
  • Jiménez, D. J., Montaña, J. S., Álvarez, D., & Baena, S. (2012). A novel cold active esterase derived from Colombian high Andean forest soil metagenome. World Journal of Microbiology & Biotechnology, 28(1), 361–370. https://doi.org/10.1007/s11274-011-0828-x
  • Jin, P., Pei, X., Du, P., Yin, X., Xiong, X., Wu, H., Zhou, X., & Wang, Q. (2012). Overexpression and characterization of a new organic solvent-tolerant esterase derived from soil metagenomic DNA. Bioresource Technology, 116, 234–240. https://doi.org/10.1016/j.biortech.2011.10.087
  • Jochens, H., Hesseler, M., Stiba, K., Padhi, S. K., Kazlauskas, R. J., & Bornscheuer, U. T. (2011). Protein engineering of α/β-hydrolase fold enzymes. ChemBiochem, 12(10), 1508–1517. https://doi.org/10.1002/cbic.201000771
  • Khan, F. I., Lan, D., Durrani, R., Huan, W., Zhao, Z., & Wang, Y. (2017). The lid domain in lipases: Structural and functional determinant of enzymatic properties. Frontiers in Bioengineering and Biotechnology, 5. https://doi.org/10.3389/fbioe.2017.00016
  • Kim, T. D. (2017). Bacterial Hormone-Sensitive Lipases (bHsls): Emerging enzymes for biotechnological applications. Journal of Microbiology and Biotechnology, 27(11), 1907–1915. https://doi.org/10.4014/jmb.1708.08004
  • Kim, Y.-J., Choi, G.-S., Kim, S.-B., Yoon, G.-S., Kim, Y.-S., & Ryu, Y.-W. (2006). Screening and characterization of a novel esterase from a metagenomic library. Protein Expression and Purification, 45(2), 315–323. https://doi.org/10.1016/j.pep.2005.06.008
  • Kim, E.-Y., Oh, K.-H., Lee, M.-H., Kang, C.-H., Oh, T.-K., & Yoon, J.-H. (2009). Novel cold-adapted alkaline lipase from an intertidal flat metagenome and proposal for a new family of bacterial lipases. Applied and Environmental Microbiology, 75(1), 257–260. https://doi.org/10.1128/AEM.01400-08
  • Kim, B., Yoo, W., Huong Luu Le, L. T., Kim, K. K., Kim, H.-W., Lee, J. H., Kim, Y.-O., & Kim, T. D. (2019). Characterization and mutation anaylsis of a cold-active bacterial hormone-sensitive lipase from Salinisphaera sp. P7-4. Archives of Biochemistry and Biophysics, 663, 132–142. https://doi.org/10.1016/j.abb.2019.01.010
  • Kleeberg, I., Welzel, K., VandenHeuvel, J., Müller, R.-J., & Deckwer, W.-D. (2005). Characterization of a new extracellular hydrolase from Thermobifida fusca degrading aliphatic−aromatic Copolyesters. Biomacromolecules, 6(1), 262–270. https://doi.org/10.1021/bm049582t
  • Ko, K.-C., Rim, S.-O., Han, Y., Shin, B. S., Kim, G.-J., Choi, J. H., & Song, J. J. (2012). Identification and characterization of a novel cold-adapted esterase from a metagenomic library of mountain soil. Journal of Industrial Microbiology & Biotechnology, 39(5), 681–689. https://doi.org/10.1007/s10295-011-1080-y
  • Kovacic, F., Babic, N., Krauss, U., & Jaeger, K.-E. (2019). Classification of lipolytic enzymes from bacteria. In F. Rojo (Ed.), Aerobic utilization of hydrocarbons, oils and lipids (pp. 1–35). Springer International Publishing. https://doi.org/10.1007/978-3-319-39782-5_39-1
  • Kraemer, F. B., & Shen, W.-J. (2002). Hormone-Sensitive lipase. Journal of Lipid Research, 43(10), 1585–1594. https://doi.org/10.1194/jlr.R200009-JLR200
  • Krintel, C., Klint, C., Lindvall, H., Mörgelin, M., & Holm, C. (2010). Quarternary structure and enzymological properties of the different hormone-sensitive lipase (HSL) Isoforms. PLoS ONE, 5(6), e11193. https://doi.org/10.1371/journal.pone.0011193
  • Kumar, L., Singh, B., Adhikari, D. K., Mukherjee, J., & Ghosh, D. (2012). A thermoalkaliphilic halotolerant esterase from Rhodococcus sp. LKE-028 (MTCC 5562): Enzyme purification and characterization. Process Biochemistry, 47(6), 983–991. https://doi.org/10.1016/j.procbio.2012.03.020
  • Lampidonis A D, Argyrokastritis A, Stravopodis D J, Voutsinas G E, Ntouroupi T G, Margaritis L H, Bizelis I and Rogdakis E. (2008). Cloning and functional characterization of the ovine Hormone Sensitive Lipase (HSL) full-length cDNAs: An integrated approach. Gene, 416(1–2), 30–43. doi:10.1016/j.gene.2008.02.026.
  • Lampidonis, A. D., Rogdakis, E., Voutsinas, G. E., & Stravopodis, D. J. (2011). The resurgence of Hormone-Sensitive Lipase (HSL) in mammalian lipolysis. Gene, 477(1–2), 1–11. https://doi.org/10.1016/j.gene.2011.01.007
  • Langin, D., Laurell, H., Holst, L. S., 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. Proceedings of the National Academy of Sciences, 90(11), 4897–4901. https://doi.org/10.1073/pnas.90.11.4897
  • Lee, M. H., Hong, K. S., Malhotra, S., Park, J.-H., Hwang, E. C., Choi, H. K., Kim, Y. S., Tao, W., & Lee, S.-W. (2010). A new esterase EstD2 isolated from plant rhizosphere soil metagenome. Applied Microbiology and Biotechnology, 88(5), 1125–1134. https://doi.org/10.1007/s00253-010-2729-6
  • Lee, M.-H., Lee, C.-H., Oh, T.-K., Song, J. K., & Yoon, J.-H. (2006). Isolation and Characterization of a novel lipase from a metagenomic library of tidal flat sediments: Evidence for a new family of bacterial lipases. Applied and Environmental Microbiology, 72(11), 7406–7409. https://doi.org/10.1128/AEM.01157-06
  • Lee, F. T., Yeaman, S. J., Fredrikson, G., Strålfors, P., & Belfrage, P. (1985). Hormone-Sensitive lipase from swine adipose tissue: Identification and some properties. Comparative Biochemistry and Physiology B, Comparative Biochemistry, 80(3), 609–612. https://doi.org/10.1016/0305-0491(85)90299-8
  • Lenfant, N., Hotelier, T., Velluet, E., Bourne, Y., Marchot, P., & Chatonnet, A. (2012). ESTHER, the database of the α/β-hydrolase fold superfamily of proteins: Tools to explore diversity of functions. Nucleic Acids Research, 41(D1), D423–D429. https://doi.org/10.1093/nar/gks1154
  • Le, L. T. H. L., Yoo, W., Lee, C., Wang, Y., Jeon, S., Kim, K. K., Lee, J. H., & Kim, T. D. (2019). Molecular Characterization of a novel cold-active hormone-sensitive lipase (HaHSL) from Halocynthiibacter Arcticus. Biomolecules, 9(11), 704. https://doi.org/10.3390/biom9110704
  • Li, P.-Y., Chen, X.-L., Ji, P., Li, C.-Y., Wang, P., Zhang, Y., Xie, B.-B., Qin, Q.-L., Su, H.-N., Zhou, B.-C., Zhang, Y.-Z., & Zhang, X.-Y. (2015). Interdomain hydrophobic interactions modulate the thermostability of microbial esterases from the hormone-sensitive lipase family. The Journal of Biological Chemistry, 290(17), 11188–11198. https://doi.org/10.1074/jbc.M115.646182
  • Li, P.-Y., Ji, P., Li, C.-Y., Zhang, Y., Wang, G.-L., Zhang, X.-Y., Xie, B.-B., Qin, Q.-L., Chen, X.-L., Zhou, B.-C., & Zhang, Y.-Z. (2014). Structural basis for dimerization and catalysis of a novel esterase from the GTSAG motif subfamily of the bacterial hormone-sensitive lipase family. The Journal of Biological Chemistry, 289(27), 19031–19041. https://doi.org/10.1074/jbc.M114.574913
  • Lin, Y., Li, Q., Xie, L., & Xie, J. (2017). Mycobacterium tuberculosis rv1400c encodes functional lipase/esterase. Protein Expression and Purification, 129, 143–149. https://doi.org/10.1016/j.pep.2016.04.013
  • Liu, X., Zhao, M., Fan, X., & Fu, Y. (2021). Enhanced production of (S)-2-arylpropionic acids by protein engineering and whole-cell catalysis. Frontiers in Bioengineering and Biotechnology, 9, 697677. https://doi.org/10.3389/fbioe.2021.697677
  • Liu, X., Zhou, M., Xing, S., Wu, T., He, H., Bielicki, J. K., & Chen, J. (2021). Identification and Biochemical characterization of a novel hormone-sensitive lipase family esterase Est19 from the antarctic bacterium Pseudomonas sp. E2-15. Biomolecules, 11(11), 1552. https://doi.org/10.3390/biom11111552
  • Li, M., Yang, L.-R., Xu, G., & Wu, J.-P. (2016). Cloning and characterization of a novel lipase from Stenotrophomonas maltophilia GS11: The first member of a new bacterial lipase family XVI. Journal of Biotechnology, 228, 30–36. https://doi.org/10.1016/j.jbiotec.2016.04.034
  • Li, P.-Y., Yao, Q.-Q., Wang, P., Zhang, Y., Li, Y., Zhang, Y.-Q., Hao, J., Zhou, B.-C., Chen, X.-L., Shi, M., Zhang, Y.-Z., & Zhang, X.-Y. (2017). A Novel subfamily esterase with a homoserine transacetylase-like fold but no transferase activity. Applied and Environmental Microbiology, 83(9), 17–e00131. https://doi.org/10.1128/AEM.00131-17
  • Lowe, D. B., Magnuson, S., Qi, N., Campbell, A.-M., Cook, J., Hong, Z., Wang, M., Rodriguez, M., Achebe, F., Kluender, H., Wong, W. C., Bullock, W. H., Salhanick, A. I., Witman-Jones, T., Bowling, M. E., Keiper, C., & Clairmont, K. B. (2004). In vitro SAR of (5-(2H)-isoxazolonyl) ureas, potent inhibitors of hormone-sensitive lipase. Bioorganic & Medicinal Chemistry Letters, 14(12), 3155–3159. https://doi.org/10.1016/j.bmcl.2004.04.015
  • Manco, G., Giosuè, 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. Archives of Biochemistry and Biophysics, 373(1), 182–192. https://doi.org/10.1006/abbi.1999.1497
  • Mandrich, L., Manco, G., Rossi, M., Floris, E., Jansen van den Bosch, T., Smit, G., & Wouters, J. A. (2006). Alicyclobacillus acidocaldarius thermophilic esterase EST2’s activity in milk and cheese models. Applied and Environmental Microbiology, 72(5), 3191–3197. https://doi.org/10.1128/AEM.72.5.3191-3197.2006
  • Mandrich, L., Menchise, V., Alterio, V., De Simone, G., Pedone, C., Rossi, M., & Manco, G. (2008). Functional and structural features of the oxyanion hole in a thermophilic esterase from Alicyclobacillus acidocaldarius. Proteins, 71(4), 1721–1731. https://doi.org/10.1002/prot.21877
  • Mandrich, L., Merone, L., Pezzullo, M., Cipolla, L., Nicotra, F., Rossi, M., & Manco, G. (2005). Role of the N terminus in enzyme activity, stability and specificity in thermophilic esterases belonging to the HSL Family. Journal of Molecular Biology, 345(3), 501–512. https://doi.org/10.1016/j.jmb.2004.10.035
  • Meghji, K., Ward, O. P., & Araujo, A. (1990). Production, purification, and properties of extracellular carboxyl esterases from Bacillus subtilis NRRL 365. Applied and Environmental Microbiology, 56(12), 3735–3740. https://doi.org/10.1128/aem.56.12.3735-3740.1990
  • Miguel-Ruano, V., Rivera, I., Rajkovic, J., Knapik, K., Torrado, A., Otero, J. M., Beneventi, E., Becerra, M., Sánchez-Costa, M., Hidalgo, A., Berenguer, J., González-Siso, M.-I., Cruces, J., Rúa, M. L., & Hermoso, J. A. (2021). Biochemical and Structural Characterization of a novel thermophilic esterase EstD11 provide catalytic insights for the HSL family. Computational and Structural Biotechnology Journal, 19, 1214–1232. https://doi.org/10.1016/j.csbj.2021.01.047
  • Mohamad Tahir, H., Raja Abd Rahman, R. N. Z., Chor Leow, A. T., & Mohamad Ali, M. S. (2020). Expression, characterisation and homology modelling of a novel hormone-sensitive lipase (HSL)-like esterase from Glaciozyma antarctica. Catalysts, 10(1), 58. https://doi.org/10.3390/catal10010058
  • Nacke, H., Will, C., Herzog, S., Nowka, B., Engelhaupt, M., & Daniel, R. (2011). Identification of novel lipolytic genes and gene families by screening of metagenomic libraries derived from soil samples of the German Biodiversity Exploratories: New soil-derived lipolytic genes and gene families. FEMS Microbiology Ecology, 78(1), 188–201. https://doi.org/10.1111/j.1574-6941.2011.01088.x
  • Nagaroor, V., & Gummadi, S. N. (2020). Biochemical characterization of an esterase from Clostridium acetobutylicum with novel GYSMG pentapeptide motif at the catalytic domain. Journal of Industrial Microbiology & Biotechnology, 47(2), 169–181. https://doi.org/10.1007/s10295-019-02253-8
  • Nam, K. H., Kim, M.-Y., Kim, S.-J., Priyadarshi, A., Lee, W. H., & Hwang, K. Y. (2009). Structural and functional analysis of a novel EstE5 belonging to the subfamily of hormone-sensitive lipase. Biochemical and Biophysical Research Communications, 379(2), 553–556. https://doi.org/10.1016/j.bbrc.2008.12.085
  • Ngo, T. D., Ryu, B. H., Ju, H., Jang, E., Park, K., Kim, K. K., & Kim, T. D. (2013). Structural and functional analyses of a bacterial homologue of hormone-sensitive lipase from a metagenomic library. Acta Crystallographica Section D, Biological Crystallography, 69(9), 1726–1737. https://doi.org/10.1107/S0907444913013425
  • Ohara, K., Unno, H., Oshima, Y., Hosoya, M., Fujino, N., Hirooka, K., Takahashi, S., Yamashita, S., Kusunoki, M., & Nakayama, T. (2014). Structural insights into the low pH adaptation of a unique carboxylesterase from ferroplasma. The Journal of Biological Chemistry, 289(35), 24499–24510. https://doi.org/10.1074/jbc.M113.521856
  • 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. (1992). The α/β hydrolase fold. Protein Engineering, Design and Selection, 5(3), 197–211. https://doi.org/10.1093/protein/5.3.197
  • Østerlund, T. (2001). Structure-Function relationships of hormone-sensitive lipase: Hormone-sensitive lipase structure. European Journal of Biochemistry, 268(7), 1899–1907. https://doi.org/10.1046/j.1432-1327.2001.02097.x
  • Østerlund, T., Contreras, J. A., & Holm, C. (1997). Identification of essential aspartic acid and histidine residues of hormone-sensitive lipase: Apparent residues of the catalytic triad. FEBS Letters, 403(3), 259–262. https://doi.org/10.1016/S0014-5793(97)00063-X
  • Østerlund, T., Danielsson, B., Degerman, E., Contreras, J. A., Edgren, G., Davis, R. C., Schotz, M. C., & Holm, C. (1996). Domain-Structure analysis of recombinant rat hormone-sensitive lipase. The Biochemical Journal, 319(2), 411–420. https://doi.org/10.1042/bj3190411
  • Ouyang, L.-M., Liu, J.-Y., Qiao, M., & Xu, J.-H. (2013). Isolation and Biochemical Characterization of two novel metagenome-derived esterases. Applied Biochemistry and Biotechnology, 169(1), 15–28. https://doi.org/10.1007/s12010-012-9949-4
  • Palm, G. J., Fernández-Álvaro, E., Bogdanović, X., Bartsch, S., Sczodrok, J., Singh, R. K., Böttcher, D., Atomi, H., Bornscheuer, U. T., & Hinrichs, W. (2011). The crystal structure of an esterase from the hyperthermophilic microorganism Pyrobaculum calidifontis VA1 explains its enantioselectivity. Applied Microbiology and Biotechnology, 91(4), 1061–1072. https://doi.org/10.1007/s00253-011-3337-9
  • Parapouli, M., Foukis, A., Stergiou, P., Koukouritaki, M., Magklaras, P., Gkini, O. A., Papamichael, E. M., Afendra, A., & Hatziloukas, E. (2018). Correction to: Molecular, biochemical and kinetic analysis of a novel, thermostable lipase (LipSm) from Stenotrophomonas maltophilia Psi‑1, the first member of a new bacterial lipase family (XIX). Journal of Biological Research-Thessaloniki, 25(1), 10. https://doi.org/10.1186/s40709-018-0083-5
  • Park, J. E., Jeong, G. S., Lee, H. W., & Kim, H. (2021). Biochemical characterization of a family IV esterase with R-form enantioselectivity from a compost metagenomic library. Applied Biological Chemistry, 64(1), 81. https://doi.org/10.1186/s13765-021-00653-y
  • Park, J.-M., Kang, C.-H., Won, S.-M., Oh, K.-H., & Yoon, J.-H. (2020). Characterization of a novel moderately thermophilic solvent-tolerant esterase isolated from a compost metagenome library. Frontiers in Microbiology, 10, 3069. https://doi.org/10.3389/fmicb.2019.03069
  • Petrovskaya, L. E., Novototskaya-Vlasova, K. A., Gapizov, S. S., Spirina, E. V., Durdenko, E. V., & Rivkina, E. M. (2017). New member of the hormone-sensitive lipase family from the permafrost microbial community. Bioengineered, 8(4), 420–423. https://doi.org/10.1080/21655979.2016.1230571
  • Petrovskaya, L. E., Novototskaya-Vlasova, K. A., Spirina, E. V., Durdenko, E. V., Lomakina, G. Y., Zavialova, M. G., Nikolaev, E. N., & Rivkina, E. M. (2016). Expression and characterization of a new esterase with GCSAG motif from a permafrost metagenomic library. FEMS Microbiology Ecology, 92(5), fiw046. https://doi.org/10.1093/femsec/fiw046
  • Pöhlmann, C., Wang, Y., Humenik, M., Heidenreich, B., Gareis, M., & Sprinzl, M. (2009). Rapid, specific and sensitive electrochemical detection of foodborne bacteria. Biosensors & Bioelectronics, 24(9), 2766–2771. https://doi.org/10.1016/j.bios.2009.01.042
  • Ramnath, L., Sithole, B., & Govinden, R. (2017). Classification of lipolytic enzymes and their biotechnological applications in the pulping industry. Canadian Journal of Microbiology, 63(3), 179–192. https://doi.org/10.1139/cjm-2016-0447
  • Rao, L., Xue, Y., Zheng, Y., Lu, J. R., & Ma, Y. (2013). A novel alkaliphilic bacillus esterase belongs to the 13th bacterial lipolytic enzyme family. PLoS ONE, 8(4), e60645. https://doi.org/10.1371/journal.pone.0060645
  • Rao, L., Xue, Y., Zhou, C., Tao, J., Li, G., Lu, J. R., & Ma, Y. (2011). A thermostable esterase from Thermoanaerobacter tengcongensis opening up a new family of bacterial lipolytic enzymes. Biochimica Et Biophysica Acta (BBA) - Proteins and Proteomics, 1814(12), 1695–1702. https://doi.org/10.1016/j.bbapap.2011.08.013
  • Rashamuse, K., Sanyika, W., Ronneburg, T., & Brady, D. (2012). A feruloyl esterase derived from a leachate metagenome library. BMB Reports, 45(1), 14–19. https://doi.org/10.5483/BMBRep.2012.45.1.14
  • Rauwerdink, A., & Kazlauskas, R. J. (2015). How the same core catalytic machinery catalyzes 17 different reactions: The serine-histidine-aspartate catalytic triad of α/β-hydrolase fold enzymes. ACS Catalysis, 5(10), 6153–6176. https://doi.org/10.1021/acscatal.5b01539
  • Recazens, E., Mouisel, E., & Langin, D. (2021). Hormone-Sensitive lipase: Sixty years later. Progress in Lipid Research, 82, 101084. https://doi.org/10.1016/j.plipres.2020.101084
  • Rehdorf, J., Behrens, G. A., Nguyen, G.-S., Kourist, R., & Bornscheuer, U. T. (2012). Pseudomonas putida esterase contains a GGG(A)X-motif confering activity for the kinetic resolution of tertiary alcohols. Applied Microbiology and Biotechnology, 93(3), 1119–1126. https://doi.org/10.1007/s00253-011-3464-3
  • Rhee, J.-K., Ahn, D.-G., Kim, Y.-G., & Oh, J.-W. (2005). New thermophilic and thermostable esterase with sequence similarity to the hormone-sensitive lipase family, cloned from a metagenomic library. Applied and Environmental Microbiology, 71(2), 817–825. https://doi.org/10.1128/AEM.71.2.817-825.2005
  • Romano, D., Bonomi, F., de Mattos, M. C., de Sousa Fonseca, T., de Oliveira, M. D. C. F., & Molinari, F. (2015). Esterases as stereoselective biocatalysts. Biotechnology Advances, 33(5), 547–565. https://doi.org/10.1016/j.biotechadv.2015.01.006
  • Ruiz, C., Falcocchio, S., Pastor, F. I. J., Saso, L., & Diaz, P. (2007). Helicobacter pylori EstV: Identification, cloning, and characterization of the first lipase isolated from an epsilon-proteobacterium. Applied and Environmental Microbiology, 73(8), 2423–2431. https://doi.org/10.1128/AEM.02215-06
  • Samoylova, Y. V., Sorokina, K. N., Romanenko, M. V., & Parmon, V. N. (2018). Cloning, expression and characterization of the esterase estUT1 from Ureibacillus thermosphaericus which belongs to a new lipase family XVIII. Extremophiles: Life Under Extreme Conditions, 22(2), 271–285. https://doi.org/10.1007/s00792-018-0996-9
  • Sánchez-Carbente, M. D. R., Batista-García, R. A., Sánchez-Reyes, A., Escudero-Garcia, A., Morales-Herrera, C., Cuervo-Soto, L. I., French-Pacheco, L., Fernández-Silva, A., Amero, C., Castillo, E., & Folch-Mallol, J. L. (2017). The first description of a hormone-sensitive lipase from a basidiomycete: Structural insights and biochemical characterization revealed Bjerkandera adusta Ba EstB as a novel esterase. MicrobiologyOpen, 6(4), e00463. https://doi.org/10.1002/mbo3.463
  • Singleton, M., Isupov, M., & Littlechild, J. (1999). X-Ray structure of pyrrolidone carboxyl peptidase from the hyperthermophilic archaeon Thermococcus litoralis. Structure, 7(3), 237–244. https://doi.org/10.1016/S0969-2126(99)80034-3
  • Slee, D. H., Bhat, A. S., Nguyen, T. N., Kish, M., Lundeen, K., Newman, M. J., & McConnell, S. J. (2003). Pyrrolopyrazinedione-Based inhibitors of human hormone-sensitive lipase. Journal of Medicinal Chemistry, 46(7), 1120–1122. https://doi.org/10.1021/jm020460y
  • Soni, S., Sathe, S. S., Odaneth, A. A., Lali, A. M., & Chandrayan, S. K. (2017). SGNH hydrolase-type esterase domain containing Cbes-AcXE2: A novel and thermostable acetyl xylan esterase from Caldicellulosiruptor bescii. Extremophiles, 21(4), 687–697. https://doi.org/10.1007/s00792-017-0934-2
  • Soror, S. H., 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 Engineering, Design and Selection, 22(6), 333–339. https://doi.org/10.1093/protein/gzp009
  • Sumby, K. M., Matthews, A. H., Grbin, P. R., & Jiranek, V. (2009). Cloning and characterization of an intracellular esterase from the wine-associated lactic acid bacterium Oenococcus oeni. Applied and Environmental Microbiology, 75(21), 6729–6735. https://doi.org/10.1128/AEM.01563-09
  • Suzuki, Y., Miyamoto, K., & Ohta, H. (2004). A novel thermostable esterase from the thermoacidophilic archaeon Sulfolobus tokodaii strain 7. FEMS Microbiology Letters, 236(1), 97–102. https://doi.org/10.1111/j.1574-6968.2004.tb09633.x
  • Tao, W. (2011). Characterization of two metagenome-derived esterases that reactivate chloramphenicol by counteracting chloramphenicol acetyltransferase. Journal of Microbiology and Biotechnology, 21(12), 1203–1210. https://doi.org/10.4014/jmb.1107.07034
  • Torres, S., Baigorí, M. D., Swathy, S. L., Pandey, A., & Castro, G. R. (2009). Enzymatic synthesis of banana flavour (isoamyl acetate) by Bacillus licheniformis S-86 esterase. Food Research International, 42(4), 454–460. https://doi.org/10.1016/j.foodres.2008.12.005
  • Virk, A. P. (2011). A new esterase, belonging to hormone-sensitive lipase family, cloned from Rheinheimera sp. Isolated from industrial effluent. Journal of Microbiology and Biotechnology, 21(7), 667–674. https://doi.org/10.4014/jmb.1103.03008
  • Wagner, U. G., Petersen, E. I., Schwab, H., & Kratky, C. (2009). EstB from Burkholderia gladioli: A novel esterase with a β-lactamase fold reveals steric factors to discriminate between esterolytic and β-lactam cleaving activity. Protein Science, 11(3), 467–478. https://doi.org/10.1110/ps.33002
  • Wang, S. P., Chung, S., Soni, K., Bourdages, H., Hermo, L., Trasler, J., & Mitchell, G. A. (2004). Expression of human hormone-Sensitive Lipase (HSL) in postmeiotic germ cells confers normal fertility to HSL-deficient mice. Endocrinology, 145(12), 5688–5693. https://doi.org/10.1210/en.2004-0919
  • Watt, M. J., & Steinberg, G. R. (2008). Regulation and function of triacylglycerol lipases in cellular metabolism. The Biochemical Journal, 414(3), 313–325. https://doi.org/10.1042/BJ20080305
  • Wu, G., Zhang, S., Zhang, H., Zhang, S., & Liu, Z. (2013). A novel esterase from a psychrotrophic bacterium Psychrobacter celer 3pb1 showed cold-adaptation and salt-tolerance. Journal of Molecular Catalysis B, Enzymatic, 98, 119–126. https://doi.org/10.1016/j.molcatb.2013.10.012
  • Xia, B., Cai, G. H., Yang, H., Wang, S. P., Mitchell, G. A., & Wu, J. W. (2017). Adipose tissue deficiency of hormone-sensitive lipase causes fatty liver in mice. PLoS Genetics, 13(12), e1007110. https://doi.org/10.1371/journal.pgen.1007110
  • Yang, Y., Ghatge, S., & Hur, H.-G. (2019). Characterization of a novel thermostable carboxylesterase from thermoalkaliphilic bacterium Bacillus thermocloaceae. Bioscience, Biotechnology, and Biochemistry, 83(5), 882–891. https://doi.org/10.1080/09168451.2019.1574555
  • Yang, S., Qin, Z., Duan, X., Yan, Q., & Jiang, Z. (2015). Structural insights into the substrate specificity of two esterases from the thermophilic Rhizomucor miehei. Journal of Lipid Research, 56(8), 1616–1624. https://doi.org/10.1194/jlr.M060673
  • Yang S, Qin Z, Duan X, Yan Q and Jiang Z. (2015). Structural insights into the substrate specificity of two esterases from the thermophilic Rhizomucor miehei. Journal of Lipid Research, 56(8), 1616–1624. doi: 10.1194/jlr.M060673.
  • Yan, Q., Yang, S., Duan, X., Xu, H., Liu, Y., & Jiang, Z. (2014). Characterization of a novel hormone-sensitive lipase family esterase from Rhizomucor miehei with tertiary alcohol hydrolysis activity. Journal of Molecular Catalysis B, Enzymatic, 109, 76–84. https://doi.org/10.1016/j.molcatb.2014.08.008
  • Yeaman, S. J. (2004). Hormone-Sensitive lipase—new roles for an old enzyme. The Biochemical Journal, 379(Pt 1), 11–22. https://doi.org/10.1042/BJ20031811
  • Yu, S., Yu, S., Han, W., Wang, H., Zheng, B., & Feng, Y. (2010). A novel thermophilic lipase from Fervidobacterium nodosum Rt17-B1 representing a new subfamily of bacterial lipases. Journal of Molecular Catalysis B, Enzymatic, 66(1–2), 81–89. https://doi.org/10.1016/j.molcatb.2010.03.007
  • Zarafeta, D., Moschidi, D., Ladoukakis, E., Gavrilov, S., Chrysina, E. D., Chatziioannou, A., Kublanov, I., Skretas, G., & Kolisis, F. N. (2016). Metagenomic mining for thermostable esterolytic enzymes uncovers a new family of bacterial esterases. Scientific Reports, 6(1). https://doi.org/10.1038/srep38886
  • Zarafeta, D., Szabo, Z., Moschidi, D., Phan, H., Chrysina, E. D., Peng, X., Ingham, C. J., Kolisis, F. N., & Skretas, G. (2016). EstDZ3: A new esterolytic enzyme exhibiting remarkable thermostability. Frontiers in Microbiology, 7, 7. https://doi.org/10.3389/fmicb.2016.01779
  • Zhang, Y., Lu, W., Wang, J., Chen, M., Zhang, W., Lin, M., Zhou, Z., & Liu, Z. (2021). Characterization of EstDR4, a novel cold-adapted insecticides-metabolizing esterase from Deinococcus radiodurans. Applied Sciences, 11(4), 1864. https://doi.org/10.3390/app11041864
  • Zheng, X., Guo, J., Xu, L., Li, H., Zhang, D., Zhang, K., Sun, F., Wen, T., Liu, S., & Pang, H. (2011). Crystal Structure of a novel esterase Rv0045c from Mycobacterium tuberculosis. PLoS ONE, 6(5), e20506. https://doi.org/10.1371/journal.pone.0020506

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