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Covalent Immobilization of Candida rugosa Lipase on Epichlorohydrin-Coated Magnetite Nanoparticles: Enantioselective Hydrolysis Studies of Some Racemic Esters and HPLC Analysis

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Abstract

In this study, a new biocatalyst was prepared by immobilizing Candida rugosa lipase epichlorohydrin-functionalized onto the surface of the nanoparticles. Magnetite nanoparticles were obtained by chemical co-precipitation method of Fe2+ and Fe3+, and then the prepared uncoated and coated nanoparticles were characterized by XRD, FT-IR and TGA. Lipase was covalently attached to activated nanoparticles. The catalytic properties of free and immobilized lipases were determined. It was found that the optimum temperature for free and immobilized lipases was 30 °C and 35 °C, respectively. The optimum pH values were found to be 7.0 and 8 for free and immobilized lipases, respectively. Immobilized lipase was found to retain significant activity even after the seventh use. In the final section of the study, optically pure compounds were obtained by carrying out the enantioselective hydrolysis studies of racemic esters by using immobilized lipase. Enantiomeric excesses of the products in the enantioselective hydrolysis of racemic ibuprofen and naproxen methyl ester and racemic butyl mandelate were determined to be 94.93, 77.30 and 68.15, respectively.

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References

  1. Villeneuve, P., Muderhwa, J. M., Graille, J., & Haas, M. (2000). Customizing lipases for biocatalysis: a survey of chemical, physical and molecular biological approaches. Journal of Molecular Catalysis B: Enzymatic, 4–6(9), 113–148.

    Google Scholar 

  2. Cardenas, F., De Castro, M., Sanchez-Montero, J., Sinisterra, J., Valmaseda, M., Elson, S., & Alvarez, E. (2001). Novel microbial lipases: catalytic activity in reactions in organic media. Enzyme Microbial Technology, 2–3(28), 145–154.

    Google Scholar 

  3. Mohamed, M. A., Mohamed, T. M., Mohamed, S. A., & Fahmy, A. S. (2000). Distribution of lipases in the Gramineae. Partial purification and characterization of esterase from Avena fatua. Bioresource Technology, 3(73), 227–234.

    Google Scholar 

  4. Javed, S., Azeem, F., Hussain, S., Rasul, I., Siddique, M. H., Riaz, M., Afzal, M., Kouser, A., & Nadeem, H. (2018). Bacterial lipases: a review on purification and characterization. Progress in Biophysics and Molecular Biology, 132, 23–34.

    CAS  PubMed  Google Scholar 

  5. Zhang, H., Liu, T., Zhu, Y., Hong, L., Li, T., Wang, X., & Fu, Y. (2020). Lipases immobilized on the modified polyporous magnetic cellulose support as an efficient and recyclable catalyst for biodiesel production from Yellow horn seed oil. Renewable Energy, 145, 1246–1254.

    CAS  Google Scholar 

  6. Cheong, L.-Z., Wei, Y., Wang, H., Wang, Z., Su, X., & Shen, C. (2017). Facile fabrication of a stable and recyclable lipase@amine-functionalized ZIF-8 nanoparticles for esters hydrolysis and transesterification. Journal of Nanoparticle Research, 8(19), 280.

    Google Scholar 

  7. Juneidi, I., Hayyan, M., Hashim, M. A., & Hayyan, A. (2017). Pure and aqueous deep eutectic solvents for a lipase-catalysed hydrolysis reaction. Biochemical Engineering Journal, 117, 129–138.

    CAS  Google Scholar 

  8. Urrutia, C., Sangaletti-Gerhard, N., Cea, M., Suazo, A., Aliberti, A., & Navia, R. (2016). Two step esterification–transesterification process of wet greasy sewage sludge for biodiesel production. Bioresource Technology, 200, 1044–1049.

    CAS  PubMed  Google Scholar 

  9. Thangaraj, B., Jia, Z., Dai, L., Liu, D., & Du, W. (2019). Effect of silica coating on Fe3O4 magnetic nanoparticles for lipase immobilization and their application for biodiesel production. Arabian Journal of Chemistry, 8(12), 4694–4706.

    Google Scholar 

  10. Liu, X., He, D., Li, X., Deng, Y., Deng, J., Li, D., & Ma, L. (2020). Preparation of (S)-2-phenylpropionic acid by CaCl2/CMC nanoparticles immobilized Candida rugosa lipase-catalyzed hydrolysis in micro aqueous mixed organic solvent systems. Journal of Nanoscience and Nanotechnology, 3(20), 1899–1906.

    Google Scholar 

  11. Salihu, A., & Alam, M. Z. (2015). Solvent tolerant lipases: a review. Process Biochemistry, 50(1), 86–96.

    CAS  Google Scholar 

  12. Kumar, A., Dhar, K., Kanwar, S. S., & Arora, P. K. (2016). Lipase catalysis in organic solvents: advantages and applications. Biological Procedures, 1(18), 2.

    Google Scholar 

  13. Mahmod, S. S., Yusof, F., Jami, M. S., Khanahmadi, S., & Shah, H. (2015). Development of an immobilized biocatalyst with lipase and protease activities as a multipurpose cross-linked enzyme aggregate (multi-CLEA). Process Biochemistry, 12(50), 2144–2157.

    Google Scholar 

  14. Sarmah, N., Revathi, D., Sheelu, G., Rani, K. Y., Sridhar, S., Mehtab, V., & Sumana, C. (2018). Recent advances on sources and industrial applications of lipases. Biotechnology Progress, 1(34), 5–28.

    Google Scholar 

  15. Rodrigues, R. C., Virgen-Ortíz, J. J., dos Santos, J. C., Berenguer-Murcia, Á., Alcantara, A. R., Barbosa, O., Ortiz, C., & Fernandez-Lafuente, R. (2019). Immobilization of lipases on hydrophobic supports: immobilization mechanism, advantages, problems, and solutions. Biotechnology Advances, 37(5), 746–770.

    CAS  PubMed  Google Scholar 

  16. Lokha, Y., Arana-Peña, S., Rios, N. S., Mendez-Sanchez, C., Gonçalves, L. R., Lopez-Gallego, F., & Fernandez-Lafuente, R. (2020). Modulating the properties of the lipase from Thermomyces lanuginosus immobilized on octyl agarose beads by altering the immobilization conditions. Enzyme and Microbial Technology, 133, 109461.

    CAS  PubMed  Google Scholar 

  17. Lee, H. R., Chung, M., Kim, M. I., & Ha, S. H. (2017). Preparation of glutaraldehyde-treated lipase-inorganic hybrid nanoflowers and their catalytic performance as immobilized enzymes. Enzyme and Microbial Technology, 105, 24–29.

    CAS  PubMed  Google Scholar 

  18. Zhao, X., Qi, F., Yuan, C., Du, W., & Liu, D. (2015). Lipase-catalyzed process for biodiesel production: enzyme immobilization, process simulation and optimization. Renewable and Sustainable Energy Reviews, 44, 182–197.

    CAS  Google Scholar 

  19. Cui, J. D., Liu, R. L., & Li, L. B. (2016). A facile technique to prepare cross-linked enzyme aggregates of bovine pancreatic lipase using bovine serum albumin as an additive. Korean Journal of Chemical Engineering, 2(33), 610–615.

    Google Scholar 

  20. Liu, D.-M., Chen, J., & Shi, Y.-P. (2018). Advances on methods and easy separated support materials for enzymes immobilization. TrAC, Trends in Analytical Chemistry, 102, 332–342.

    CAS  Google Scholar 

  21. Singh, R., Kumar, M., Mittal, A., & Mehta, P. K. (2016). Microbial enzymes: industrial progress in 21st century. 3 Biotech, 2(6), 174.

    Google Scholar 

  22. Choi, J.-M., Han, S.-S., & Kim, H.-S. (2015). Industrial applications of enzyme biocatalysis: current status and future aspects. Biotechnology Advances, 7(33), 1443–1454.

    Google Scholar 

  23. Porter, J. L., Rusli, R. A., & Ollis, D. L. (2016). Directed evolution of enzymes for industrial biocatalysis. Chembiochem., 3(17), 197–203.

    Google Scholar 

  24. Zambrowicz, A., Pokora, M., Setner, B., Dąbrowska, A., Szołtysik, M., Babij, K., Szewczuk, Z., Trziszka, T., Lubec, G., & Chrzanowska, J. (2015). Multifunctional peptides derived from an egg yolk protein hydrolysate: isolation and characterization. Amino Acids, 2(47), 369–380.

    Google Scholar 

  25. Shi, L. (2016). Bioactivities, isolation and purification methods of polysaccharides from natural products: a review. International Journal of Biological Macromolecules, 92, 37–48.

    CAS  PubMed  PubMed Central  Google Scholar 

  26. France, S. P., Hepworth, L. J., Turner, N. J., & Flitsch, S. L. (2016). Constructing biocatalytic cascades: in vitro and in vivo approaches to de novo multi-enzyme pathways. ACS Catalysis, 1(7), 710–724.

    Google Scholar 

  27. Chatzikonstantinou, A. V., Polydera, A. C., Thomou, E., Chalmpes, N., Baroud, T. N., Enotiadis, A., Estevez, L., Patila, M., Hammami, M. A., & Spyrou, K. (2020). Lipase immobilized on magnetic hierarchically porous carbon materials as a versatile tool for the synthesis of bioactive quercetin derivatives. Bioresource Technology Reports., 9, 100372.

    Google Scholar 

  28. Mehta, J., Bhardwaj, N., Bhardwaj, S. K., Kim, K.-H., & Deep, A. (2016). Recent advances in enzyme immobilization techniques: metal-organic frameworks as novel substrates. Coordination Chemistry Reviews, 322, 30–40.

    CAS  Google Scholar 

  29. Küchler, A., Yoshimoto, M., Luginbühl, S., Mavelli, F., & Walde, P. (2016). Enzymatic reactions in confined environments. Nature Nanotechnology, 5(11), 409.

    Google Scholar 

  30. Sigurdardóttir, S. B., Lehmann, J., Ovtar, S., Grivel, J. C., Negra, M. D., Kaiser, A., Pinelo, M., & Catalysis. (2018). Enzyme immobilization on inorganic surfaces for membrane reactor applications: mass transfer challenges, enzyme leakage and reuse of materials. Advanced Synthesis., 14(360), 2578–2607.

    Google Scholar 

  31. Cao, Y., Wen, L., Svec, F., Tan, T., & Lv, Y. (2016). Magnetic AuNP@Fe3O4 nanoparticles as reusable carriers for reversible enzyme immobilization. Chemical Engineering Journal, 286, 272–281.

    CAS  Google Scholar 

  32. Palomo, J. M., Fernández-Lorente, G., Mateo, C., Fuentes, M., Fernández-Lafuente, R., & Guisan, J. M. (2002). Modulation of the enantioselectivity of Candidaantarctica B lipase via conformational engineering. Kinetic resolution of (±)-α-hydroxy-phenylacetic acid derivatives. Tetrahedron: Asymmetry, 12(13), 1337–1345.

    Google Scholar 

  33. Ozyilmaz, E., Etci, K., & Sezgin, M. (2018). Candida rugosa lipase encapsulated with magnetic sporopollenin: design and enantioselective hydrolysis of racemic arylpropanoic acid esters. Preparative Biochemistry & Biotechnology, 10(48), 887–897.

    Google Scholar 

  34. Ozyilmaz, E., Bayrakci, M., & Yilmaz, M. (2016). Improvement of catalytic activity of Candida rugosa lipase in the presence of calix [4] arene bearing iminodicarboxylic/phosphonic acid complexes modified iron oxide nanoparticles. Bioorganic Chemistry, 65, 1–8.

    CAS  PubMed  Google Scholar 

  35. Yuan, X., Zhang, P., Liu, G., Xu, W., & Tang, K. (2019). Lipase-catalyzed hydrolysis of 2-(4-hydroxyphenyl) propionic acid ethyl ester to (R)-(−)-2-(4-hydroxyphenyl) propanoic acid. Chemical Papers, 10(73), 1–8.

    Google Scholar 

  36. Goto, M., Noda, S., Kamiya, N., & Nakashio, F. (1996). Enzymatic resolution of racemic ibuprofen by surfactant-coated lipases in organic media. Biotechnology Letters, 7(18), 839–844.

    Google Scholar 

  37. Chen, J. C., & Tsai, S. W. (2000). Enantioselective synthesis of (S)-ibuprofen ester prodrug in cyclohexane by Candida rugosa lipase immobilized on Accurel MP1000. Biotechnology Progress, 6(16), 986–992.

    Google Scholar 

  38. Yu, H., Wu, J., & Ching, C. B. (2004). Enhanced activity and enantioselectivity of Candida rugosa lipase immobilized on macroporous adsorptive resins for ibuprofen resolution. Biotechnology Letters, 8(26), 629–633.

    Google Scholar 

  39. Marszałł, M. P., & Siódmiak, T. (2012). Immobilization of Candida rugosa lipase onto magnetic beads for kinetic resolution of (R, S)-ibuprofen. Catalysis Communications, 24, 80–84.

    Google Scholar 

  40. Habibi, Z., Mohammadi, M., & Yousefi, M. (2013). Enzymatic hydrolysis of racemic ibuprofen esters using Rhizomucor miehei lipase immobilized on different supports. Process Biochemistry, 4(48), 669–676.

    Google Scholar 

  41. Siódmiak, T., Ziegler-Borowska, M., & Marszałł, M. P. (2013). Lipase-immobilized magnetic chitosan nanoparticles for kinetic resolution of (R, S)-ibuprofen. Journal of Molecular Catalysis B: Enzymatic, 94, 7–14.

    Google Scholar 

  42. Yousefi, M., Mohammadi, M., & Habibi, Z. (2014). Enantioselective resolution of racemic ibuprofen esters using different lipases immobilized on octyl sepharose. Journal of Molecular Catalysis B: Enzymatic, 104, 87–94.

    CAS  Google Scholar 

  43. Lee, E. G., Won, H. S., & Chung, B. H. (2001). Enantioselective hydrolysis of racemic naproxen methyl ester by two-step acetone-treated Candida rugosa lipase. Process Biochemistry, 3(37), 293–298.

    Google Scholar 

  44. Salgın, U., Salgın, S., & Takaç, S. (2007). The enantioselective hydrolysis of racemic naproxen methyl ester in supercritical CO2 using Candida rugosa lipase. The Journal of Supercritical Fluids., 2(43), 310–316.

    Google Scholar 

  45. Cernia, E., Delfini, M., Di Cocco, E., Palocci, C., & Soro, S. (2002). Investigation of lipase-catalysed hydrolysis of naproxen methyl ester: use of NMR spectroscopy methods to study substrate–enzyme interaction. Bioorganic Chemistry, 4(30), 276–284.

    Google Scholar 

  46. Takaç, S., & Mutlu, D. (2007). A parametric study on biphasic medium conditions for the enantioselective production of naproxen by Candida rugosa lipase. Applied Biochemistry and Biotechnology, 1(141), 15–26.

    Google Scholar 

  47. Sahin, O., Erdemir, S., Uyanik, A., & Yilmaz, M. (2009). Enantioselective hydrolysis of (R/S)-Naproxen methyl ester with sol–gel encapculated lipase in presence of calix[n]arene derivatives. Applied Catalysis A: General, 1(369), 36–41.

    Google Scholar 

  48. Tutar, H., Yilmaz, E., Pehlivan, E., & Yilmaz, M. (2009). Immobilization of Candida rugosa lipase on sporopollenin from Lycopodium clavatum. International Journal of Biological Macromolecules, 3(45), 315–320.

    Google Scholar 

  49. Yilmaz, E., Sezgin, M., & Yilmaz, M. (2010). Enantioselective hydrolysis of rasemic naproxen methyl ester with sol–gel encapsulated lipase in the presence of sporopollenin. Journal of Molecular Catalysis B: Enzymatic, 2(62), 162–168.

    Google Scholar 

  50. Palomo, J. M., Fernandez-Lorente, G., Mateo, C., Ortiz, C., Fernandez-Lafuente, R., & Guisan, J. M. (2002). Modulation of the enantioselectivity of lipases via controlled immobilization and medium engineering: hydrolytic resolution of mandelic acid esters. Enzyme and Microbial Technology, 6(31), 775–783.

    Google Scholar 

  51. Ebert, C., Ferluga, G., Gardossi, L., Gianferrara, T., & Linda, P. (1992). Improved lipase-mediated resolution of mandelic acid esters by multivariate investigation of experimental factors. Tetrahedron: Asymmetry, 7(3), 903–912.

    Google Scholar 

  52. Chen, C.-C., & Tsai, S.-W. (2005). Carica papaya lipase: a novel biocatalyst for the enantioselective hydrolysis of (R,S)-naproxen 2,2,2-trifluoroethyl ester. Enzyme and Microbial Technology, 1(36), 127–132.

    Google Scholar 

  53. Francolini, I., Taresco, V., Martinelli, A., & Piozzi, A. (2020). Enhanced performance of Candida rugosa lipase immobilized onto alkyl chain modified-magnetic nanocomposites. Enzyme Microbial Technology, 132, 109439.

    CAS  PubMed  Google Scholar 

  54. Tümtürk, H., Karaca, N., Demirel, G., & Şahin, F. (2007). Preparation and application of poly(N,N-dimethylacrylamide-co-acrylamide) and poly(N-isopropylacrylamide-co-acrylamide)/κ-Carrageenan hydrogels for immobilization of lipase. International Journal of Biological Macromolecules, 3(40), 281–285.

    Google Scholar 

  55. Yildirim, D., & Tükel, S. S. (2013). Immobilized Pseudomonas sp. lipase: A powerful biocatalyst for asymmetric acylation of (±)-2-amino-1-phenylethanols with vinyl acetate. Process Biochemistry, 5(48), 819–830.

    Google Scholar 

  56. Ozmen, E. Y., & Yilmaz, M. (2009). Pretreatment of Candida rugosa lipase with soybean oil before immobilization on β-cyclodextrin-based polymer. Colloids and Surfaces. B, Biointerfaces, 1(69), 58–62.

    Google Scholar 

  57. Rodrigues, R. C., Ortiz, C., Berenguer-Murcia, Á., Torres, R., & Fernández-Lafuente, R. (2013). Modifying enzyme activity and selectivity by immobilization. Chemical Society Reviews, 15(42), 6290–6307.

    Google Scholar 

  58. Srinivas, B., & Ashok, M. Immobilization of enzymes In their economic reuse-a review. International Journal Of Engineering Sciences & Research Technology.

  59. Tartaj, P., del Puerto Morales, M., Veintemillas-Verdaguer, S., González-Carreño, T., & Serna, C. J. (2003). The preparation of magnetic nanoparticles for applications in biomedicine. Journal of Physics D: Applied Physics, 13(36), R182.

    Google Scholar 

  60. Scherer, C., & Figueiredo Neto, A. M. (2005). Ferrofluids: properties and applications. Brazilian Journal of Physics, 3A(35), 718–727.

    Google Scholar 

  61. Batten, S. R., Champness, N. R., Chen, X.-M., Garcia-Martinez, J., Kitagawa, S., Öhrström, L., O’Keeffe, M., Suh, M. P., & Reedijk, J. (2013). Terminology of metal–organic frameworks and coordination polymers (IUPAC Recommendations 2013). Pure and Applied Chemistry, 8(85), 1715–1724.

    Google Scholar 

  62. Datta, S., Christena, L. R., & Rajaram, Y. R. S. (2013). Enzyme immobilization: an overview on techniques and support materials. 3 Biotech, 1(3), 1–9.

    CAS  Google Scholar 

  63. Lykourinou, V., Chen, Y., Wang, X.-S., Meng, L., Hoang, T., Ming, L.-J., Musselman, R. L., & Ma, S. (2011). Immobilization of MP-11 into a mesoporous metal–organic framework, MP-11@ mesoMOF: a new platform for enzymatic catalysis. Journal of the American Chemical Society, 27(133), 10382–10385.

    Google Scholar 

  64. Rafiei, S., Tangestaninejad, S., Horcajada, P., Moghadam, M., Mirkhani, V., Mohammadpoor-Baltork, I., Kardanpour, R., & Zadehahmadi, F. (2018). Efficient biodiesel production using a lipase@ ZIF-67 nanobioreactor. Chemical Engineering Journal, 334, 1233–1241.

    CAS  Google Scholar 

  65. Maity, D., & Agrawal, D. C. (2007). Synthesis of iron oxide nanoparticles under oxidizing environment and their stabilization in aqueous and non-aqueous media. Journal of Magnetism and Magnetic Materials, 1(308), 46–55.

    Google Scholar 

  66. Axen, R., Drevin, H., & Carlsson, J. (1975). Preparation of modified agarose gels containing thiol groups. Acta Chemica Scandinavica, 29, 471–474.

    Google Scholar 

  67. Yakup Arıca, M., & Bayramoǧlu, G. (2004). Reversible immobilization of tyrosinase onto polyethyleneimine-grafted and Cu(II) chelated poly(HEMA-co-GMA) reactive membranes. Journal of Molecular Catalysis B: Enzymatic, 4(27), 255–265.

    Google Scholar 

  68. Sahoo, B., Sahu, S. K., & Pramanik, P. (2011). A novel method for the immobilization of urease on phosphonate grafted iron oxide nanoparticle. Journal of Molecular Catalysis B: Enzymatic, 3(69), 95–102.

    Google Scholar 

  69. Hung, T.-C., Giridhar, R., Chiou, S.-H., & Wu, W.-T. (2003). Binary immobilization of Candida rugosa lipase on chitosan. Journal of Molecular Catalysis B: Enzymatic, 1(26), 69–78.

    Google Scholar 

  70. Chiou, S.-H., & Wu, W.-T. (2004). Immobilization of Candida rugosa lipase on chitosan with activation of the hydroxyl groups. Biomaterials., 2(25), 197–204.

    Google Scholar 

  71. Takaç, S., & Bakkal, M. (2007). Impressive effect of immobilization conditions on the catalytic activity and enantioselectivity of Candida rugosa lipase toward S-Naproxen production. Process Biochemistry, 6(42), 1021–1027.

    Google Scholar 

  72. Chen, C. S., Fujimoto, Y., Girdaukas, G., & Sih, C. J. (1982). Quantitative analyses of biochemical kinetic resolutions of enantiomers. Journal of the American Chemical Society, 25(104), 7294–7299.

    Google Scholar 

  73. Crini, G., & Morcellet, M. (2002). Synthesis and applications of adsorbents containing cyclodextrins. Journal of Separation Science, 13(25), 789–813.

    Google Scholar 

  74. Santos, J. C., Mijone, P. D., Nunes, G. F. M., Perez, V. H., & de Castro, H. F. (2008). Covalent attachment of Candida rugosa lipase on chemically modified hybrid matrix of polysiloxane–polyvinyl alcohol with different activating compounds. Colloids and Surfaces. B, Biointerfaces, 2(61), 229–236.

    Google Scholar 

  75. Arica, M. Y. (2000). Epoxy-derived pHEMA membrane for use bioactive macromolecules immobilization: Covalently bound urease in a continuous model system. Journal of Applied Polymer Science, 9(77), 2000–2008.

    Google Scholar 

  76. Santra, S., Tapec, R., Theodoropoulou, N., Dobson, J., Hebard, A., & Tan, W. (2001). Synthesis and characterization of silica-coated iron oxide nanoparticles in microemulsion: the effect of nonionic surfactants. Langmuir., 10(17), 2900–2906.

    Google Scholar 

  77. Tural, B., Tarhan, T., & Tural, S. (2014). Covalent immobilization of benzoylformate decarboxylase from Pseudomonas putida on magnetic epoxy support and its carboligation reactivity. Journal of Molecular Catalysis B: Enzymatic, 102, 188–194.

    CAS  Google Scholar 

  78. Wan, M., & Li, J. (1998). Synthesis and electrical–magnetic properties of polyaniline composites. Polymer Chemistry, 15(36), 2799–2805.

    Google Scholar 

  79. Tarducci, C., Kinmond, E. J., Badyal, J. P. S., Brewer, S. A., & Willis, C. (2000). Epoxide-functionalized solid surfaces. Chemistry of Materials, 7(12), 1884–1889.

    Google Scholar 

  80. Schottner, G. (2001). Hybrid sol−gel-derived polymers: applications of multifunctional materials. Chemistry of Materials, 10(13), 3422–3435.

    Google Scholar 

  81. Zhang, Q., Huang, R., & Guo, L.-H. (2009). One-step and high-density protein immobilization on epoxysilane-modified silica nanoparticles. Chinese Science Bulletin, 15(54), 2620–2626.

    Google Scholar 

  82. Wanunu, M., Livne, S., Vaskevich, A., & Rubinstein, I. (2006). Assembly of coordination nanostructures via ligand derivatization of oxide surfaces. Langmuir., 5(22), 2130–2135.

    Google Scholar 

  83. Sun, J., Jiang, Y., Zhou, L., & Gao, J. (2010). Immobilization of Candida antarctica lipase B by adsorption in organic medium. New Biotechnology, 1(27), 53–58.

    Google Scholar 

  84. Jiang, Y., Liu, X., Chen, Y., Zhou, L., He, Y., Ma, L., & Gao, J. (2014). Pickering emulsion stabilized by lipase-containing periodic mesoporous organosilica particles: a robust biocatalyst system for biodiesel production. Bioresource Technology, 153, 278–283.

    CAS  PubMed  Google Scholar 

  85. Kuo, C.-H., Liu, Y.-C., Chang, C.-M. J., Chen, J.-H., Chang, C., & Shieh, C.-J. (2012). Optimum conditions for lipase immobilization on chitosan-coated Fe3O4 nanoparticles. Carbohydrate Polymers, 4(87), 2538–2545.

    Google Scholar 

  86. Lowry, O. H., Rosebrough, N. J., Farr, A. L., & Randall, R. J. (1951). Protein measurement with the Folin phenol reagent. The Journal of Biological Chemistry, 193, 265–275.

    CAS  PubMed  Google Scholar 

  87. Ye, P., Xu, Z.-K., Che, A.-F., Wu, J., & Seta, P. (2005). Chitosan-tethered poly(acrylonitrile-co-maleic acid) hollow fiber membrane for lipase immobilization. Biomaterials., 32(26), 6394–6403.

    Google Scholar 

  88. Phadtare, S., d'Britto, V., Pundle, A., Prabhune, A., & Sastry, M. (2004). Invertase-lipid biocomposite films: preparation, characterization, and enzymatic activity. Biotechnology Progress, 1(20), 156–161.

    Google Scholar 

  89. Öztürk, N., Akgöl, S., Arısoy, M., & Denizli, A. (2007). Reversible adsorption of lipase on novel hydrophobic nanospheres. Separation and Purification Technology, 1(58), 83–90.

    Google Scholar 

  90. Zhu, K., Jutila, A., Tuominen, E. K. J., Patkar, S. A., Svendsen, A., & Kinnunen, P. K. J. (2001). Impact of the tryptophan residues of Humicola lanuginosa lipase on its thermal stability. Biochimica et Biophysica Acta, 2(1547), 329–338.

    Google Scholar 

  91. Janssen, P. H., Monk, C. R., & Morgan, H. W. (1994). A thermophilic, lipolytic Bacillus sp., and continuous assay of its p-nitrophenyl-palmitate esterase activity. FEMS Microbiology Letters, 1–2(120), 195–200.

    Google Scholar 

  92. Abrol, K., Qazi, G. N., & Ghosh, A. K. (2007). Characterization of an anion-exchange porous polypropylene hollow fiber membrane for immobilization of ABL lipase. Journal of Biotechnology, 4(128), 838–848.

    Google Scholar 

  93. Battistel, E., Bianchi, D., Cesti, P., & Pina, C. (1991). Enzymatic resolution of (S)-(+)-naproxen in a continuous reactor. Biotechnology and Bioengineering, 6(38), 659–664.

    Google Scholar 

  94. Lin, H.-Y., & Tsai, S.-W. (2003). Dynamic kinetic resolution of (R, S)-naproxen 2,2,2-trifluoroethyl ester via lipase-catalyzed hydrolysis in micro-aqueous isooctane. Journal of Molecular Catalysis B: Enzymatic, 24–25, 111–120.

    Google Scholar 

  95. Sakaki, K., Giorno, L., & Drioli, E. (2001). Lipase-catalyzed optical resolution of racemic naproxen in biphasic enzyme membrane reactors. Journal of Membrane Science, 1(184), 27–38.

    Google Scholar 

  96. Mao, S., Zhang, Y., Rohani, S., & Ray, A. K. (2012). Chromatographic resolution and isotherm determination of (R,S)-mandelic acid on Chiralcel-OD column. Journal of Separation Science, 17(35), 2273–2281.

    Google Scholar 

  97. Yao, C., Cao, Y., Wu, S., Li, S., & He, B. (2013). An organic solvent and thermally stable lipase from Burkholderia ambifaria YCJ01: Purification, characteristics and application for chiral resolution of mandelic acid. Journal of Molecular Catalysis B: Enzymatic, 85–86, 105–110.

    Google Scholar 

  98. Campbell, R. F., Fitzpatrick, K., Inghardt, T., Karlsson, O., Nilsson, K., Reilly, J. E., & Yet, L. (2003). Enzymatic resolution of substituted mandelic acids. Tetrahedron Letters, 29(44), 5477–5481.

    Google Scholar 

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Acknowledgements

The authors thank to the Scientific and Technical Research Council of Turkey (TUBITAK) and the Scientific Research Projects Unit of Dicle University for their financial support to this work partly achieved from Reşit Çakmak’s Ph.D. thesis, which was prepared under the supervision of Prof Dr. Giray Topal. On the other hand, biochemist Dr. Ercan Çınar studied as a researcher in the section the determination of enzymatic activities of free and immobilized lipases in this doctoral thesis work.

Funding

This research was supported by TUBITAK (grant number:113Z773) and Dicle University (grant number:14-ZEF-16).

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Authors and Affiliations

  1. Medical Laboratory Techniques Program, Vocational School of Health Services, Batman University, 72060, Batman, Turkey

    Reşit Çakmak

  2. Department of Chemistry, Faculty of Education, Dicle University, 21280, Diyarbakır, Turkey

    Giray Topal

  3. Department of Nursing, School of Health Sciences, Batman University, 72060, Batman, Turkey

    Ercan Çınar

Authors
  1. Reşit Çakmak
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  2. Giray Topal
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  3. Ercan Çınar
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Correspondence to Giray Topal.

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Çakmak, R., Topal, G. & Çınar, E. Covalent Immobilization of Candida rugosa Lipase on Epichlorohydrin-Coated Magnetite Nanoparticles: Enantioselective Hydrolysis Studies of Some Racemic Esters and HPLC Analysis. Appl Biochem Biotechnol 191, 1411–1431 (2020). https://doi.org/10.1007/s12010-020-03274-1

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