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Optimization of Synthesis of (S)-Omeprazole Catalyzed by Soybean Pod Peroxidase in Water-in-Oil Microemulsions Using RSM

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Abstract

Response surface methodology (RSM) was used to optimize the oxidizing the omeprazole sulfide to (S)-omeprazole catalyzed by environmentally friendly catalyst soybean pod peroxidase (SPP) in cetyltrimethylammonium bromide (CTAB)/isooctane/n-butyl alcohol/water water-in-oil microemulsions. With the initial concentration of SPP of 3200 U ml−1, the conversion of the omeprazole sulfide, the (S)-omeprazole yield and ee were 93.75%, 91.56% and 96.08%, respectively, under the optimal conditions: Wo of 15.85, the concentration of H2O2 of 22.44 mM and reaction temperature of 49.68 °C, respectively. The proposed mechanism of asymmetric sulfoxidations catalyzed by SPP involves three concomitant mechanisms as follows: (1) a two-electron reduction of SPP-I, (2) a single-electron transfer to SPP-I and (3) nonenzymatic reactions. Based on the proposed mechanism which is reasonable and can express the oxidations, the reaction system includes five enzymatic and two nonenzymatic reactions. With 5.44% of the average relative error, a kinetic model based on the mechanisms fitting observed data very well was established, and the SPP-catalyzed reactions including both the two-electron reduction and the single-electron transfer mechanisms obey ping-pong mechanism with substrate and product inhibition, while nonenzymatic reactions follow a power law. This study has also demonstrated the feasibility of SPP as a substitute with low cost, excellent enantioselectivity and better thermal stability.

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Abbreviations

Sa :

Hydrogen peroxide

A0 :

Initial concentration of hydrogen peroxide, mM

Sb :

5-Methoxy-2-(((4-methoxy-3,5-dimethylpyridin-2-yl)methyl)thio)-1H-benzoimidazole, Omeprazole thioether, 5-methoxy-2-(((4-methoxy-3,5-dimethylpyridin-2-yl)methyl)thio)-1H-benzo[d]imidazole

B0 :

Initial concentration of Sb, mM

Sc :

Cation radical of Sb, Omeprazole sulfide cation

E0 :

Initial concentration of peroxidase, U ml−1

ee:

Enantiomeric excess, %

K1, K10, K19 :

Kinetic parameter, dimensionless

K2, K3, K6 :

Kinetic parameter, mM−1

K4, K5, K7 :

Kinetic parameter, mM−2

K8 :

Kinetic parameter, mM−3

K9 :

Kinetic parameter, h−1 U−1 ml mM1−2K10

K12, K14, K16 :

Kinetic parameter, h−1 U−1 ml mM−1

K11, K13, K15, K17 :

Kinetic parameter, h−1 U−1 ml mM−2

K18 :

Kinetic parameter, h−1 U−1 ml mM1−K19

KK1 KK2:

∑K sum of Kappa constant, dimensionless

PR :

(R)-enantiomer of P

PS :

(S)-enantiomer of P, esomeprazole

P:

5-Methoxy-2-[(4-methoxy-3,5-dimethylpyridin-2-yl) methylsulfinyl]-1H-benzoimidazole, Omeprazole

Q:

H2O

R:

Dication radical of Sb

Wo:

Water/CTAB, mol

Y(i):

Relative residual or yield of Sa, Sb, PS, PR, C and R, for i = 1–6, respectively, dimensionless

Ysimulij :

Simulated residual or yield of Sa, Sb, PS and PR, for i = 1–4, j = 1–12, dimensionless

Yexpi j :

Experimental residual or yield of Sa, Sb, PS and PR, for i = 1–4, j = 1–12, dimensionless

T:

Time, hour

References

  1. Delamare M, Belot S, Caille J-C, Martinet F, Kagan HB, Henryon V (2009) A new titanate/(+)-(1R, 2S)-cis-1-amino-2-indanol system for the asymmetric synthesis of (S)-tenatoprazole. Tetrahedron Lett 50(15):1702–1704

    CAS  Google Scholar 

  2. Dembitsky VM (2003) Oxidation, epoxidation and sulfoxidation reactions catalysed by haloperoxidases. Tetrahedron 26(59):4701–4720

    Google Scholar 

  3. Thomas SM, DiCosimo R, Nagarajan V (2002) Biocatalysis: applications and potentials for the chemical industry. Trends Biotechnol 20(6):238–242

    CAS  PubMed  Google Scholar 

  4. Carreño MC (1995) Applications of sulfoxides to asymmetric synthesis of biologically active compounds. Chem Rev 95(6):1717–1760

    Google Scholar 

  5. Harris RZ, Newmyer SL, De Montellano PRO (1993) Horseradish peroxidase-catalyzed two-electron oxidations. Oxidation of iodide, thioanisoles, and phenols at distinct sites. Journal of Biological Chemistry 268(3):1637–1645

    CAS  Google Scholar 

  6. Blee E, Schuber F (1989) Mechanism of S-oxidation reactions catalyzed by a soybean hydroperoxide-dependent oxygenase. Biochemistry 28(12):4962–4967

    CAS  Google Scholar 

  7. Van Deurzen MPJ, van Rantwijk F, Sheldon RA (1997) Selective oxidations catalyzed by peroxidases. Tetrahedron 53(39):13183–13220

    Google Scholar 

  8. van de Velde F, Könemann L, van Rantwijk F, Sheldon RA (2000) The rational design of semisynthetic peroxidases. Biotechnol Bioeng 67(1):87–96

    PubMed  Google Scholar 

  9. Zhang Y, Wu Y-Q, Xu N, Zhao Q, Yu H-L, Xu J-H (2019) Engineering of cyclohexanone monooxygenase for the enantioselective synthesis of (S)-omeprazole. ACS Sustainable Chemistry & Engineering 7(7):7218–7226

    CAS  Google Scholar 

  10. Zhang Y, Liu F, Xu N, Wu Y-Q, Zheng Y-C, Zhao Q, Lin G, Yu H-L, Xu J-H (2018) Discovery of two native Baeyer-Villiger monooxygenases for asymmetric synthesis of bulky chiral sulfoxides. Appl Environ Microbiol 84(14):e00638-e718

    PubMed  PubMed Central  Google Scholar 

  11. Ozaki SI, Matsui T, Watanabe Y (1997) Conversion of Myoglobin into a Peroxygenase:? A Catalytic Intermediate of Sulfoxidation and Epoxidation by the F43H/H64L Mutant. J Am Chem Soc 119(28):6666–6667

    CAS  Google Scholar 

  12. Akasaka R, Mashino T, Hirobe M (1993) Cytochrome P450-like Substrate Oxidation Catalyzed by Cytochrome c and Immobilized Cytochrome c. Archives of Biochemistry & Biophysics 301(2):355–360

    CAS  Google Scholar 

  13. Singh P, Prakash R, Shah K (2012) Effect of organic solvents on peroxidases from rice and horseradish: prospects for enzyme based applications. Talanta 97:204–210

    CAS  PubMed  Google Scholar 

  14. Hong ES, Kwon OY, Ryu K (2008) Strong substrate-stabilizing effect of a water-miscible ionic liquid [BMIM][BF 4] in the catalysis of horseradish peroxidase. Biotech Lett 30(3):529–533

    Google Scholar 

  15. Lopez F, Cinelli G, Colella M, De Leonardis A, Palazzo G, Ambrosone L (2014) The role of microemulsions in lipase-catalyzed hydrolysis reactions. Biotechnol Prog 30(2):360–366

    CAS  PubMed  Google Scholar 

  16. Seenivasaperumal M, Federsel H-J, Szab K (2010) Mechanism of the Asymmetric Sulfoxidation in the Esomeprazole Process: Effects of the Imidazole Backbone for the Enantioselection. Adv Synth Catal 351(6):903–919

    Google Scholar 

  17. Amiri S, Shakeri A, Sohrabi MR, Khalajzadeh S, Ghasemi E (2019) Optimization of ultrasonic assisted extraction of fatty acids from Aesculus hippocastanum fruit by response surface methodology. Food Chem 271:762–766

    CAS  PubMed  Google Scholar 

  18. Adachi M, Harada M, Katoh S (2000) Bioaffinity separation of chymotrypsinogen using antigen-antibody reaction in reverse micellar system composed of a nonionic surfactant. Biochem Eng J 4(2):149–151

    CAS  Google Scholar 

  19. Krieger N, Taipa MA, Melo EHM, Lima-Filho JL, Aires-Barros MR, Cabral JMS (1997) Kinetic characterization ofpenicillium citrinum lipase in AOT/lsooctane-reversed micelles. Appl Biochem Biotechnol 67(1–2):87–95

    CAS  Google Scholar 

  20. Carvalho CML, Cabral JMS (2000) Reverse micelles as reaction media for lipases. Biochimie 82(11):1063–1085

    CAS  PubMed  Google Scholar 

  21. Chen N, Fan J-B, Xiang J, Chen J, Liang Y (2006) Enzymatic hydrolysis of microcrystalline cellulose in reverse micelles. Biochim Biophys Acta Proteins Proteom 1764(6):1029–1035

    CAS  Google Scholar 

  22. Bru R, Sánchez-Ferrer A, García-Carmona F (1995) Kinetic models in reverse micelles. Biochem J 310(3):721–739

    CAS  PubMed  PubMed Central  Google Scholar 

  23. Hamann H-J, Höft E, Mostowicz D, Mishnev A, Urbańczyk-Lipkowska Z, Chmielewski M (1997) New optically pure sugar hydroperoxides. Synhtesis and use for enantioselective oxygen transfer. Tetrahedron 53(1):185–192

    CAS  Google Scholar 

  24. Goodwin DC, Grover TA, Aust SD (1997) Roles of efficient substrates in enhancement of peroxidase-catalyzed oxidations. Biochemistry 36(1):139–147

    CAS  PubMed  Google Scholar 

  25. Drożdż A, Erfurt K, Bielas R, Chrobok A (2015) Chemo-enzymatic Baeyer-Villiger oxidation in the presence of Candida antarctica lipase B and ionic liquids. New J Chem 39(2):1315–1321

    Google Scholar 

  26. Törnvall U, Fürst CM, Hatti-Kaul R, Hedström M (2009) Mass spectrometric analysis of peptides from an immobilized lipase: focus on oxidative modifications. Rapid Commun Mass Spectrom 23(18):2959–2964

    PubMed  Google Scholar 

  27. Törnvall U, Hedström M, Schillén K, Hatti-Kaul R (2010) Structural, functional and chemical changes in Pseudozyma antarctica lipase B on exposure to hydrogen peroxide. Biochimie 92(12):1867–1875

    PubMed  Google Scholar 

  28. Ji L, Franke A, Brindell M, Oszajca M, Zahl A, van Eldik R (2014) Combined experimental and theoretical study on the reactivity of Compounds I and II in horseradish peroxidase biomimetics. Chem Eur J 20(44):14437–14450

    CAS  PubMed  Google Scholar 

  29. Dunford HB (1991) Horseradish peroxidase: structure and kinetic properties. In: Everse J, Everse KE, Grisham MB (eds) Perozidases in Chemistry and Biology. CRC Press, Boca Raton, pp 1–23

    Google Scholar 

  30. Samuni U, Maimon E, Goldstein S (2018) A kinetic study of the oxidation of hydroxamic acids by compounds I and II of horseradish peroxidase: Effect of transition metal ions. J Coord Chem 71(11–13):1728–1737

    CAS  Google Scholar 

  31. Harris DL, Loew GH (1996) Identification of putative peroxide intermediates of peroxidases by electronic structure and spectra calculations. J Am Chem Soc 118(43):10588–10594

    CAS  Google Scholar 

  32. Perez U, Dunford HB (1990) Transient-state kinetics of the reactions of 1-methoxy-4-(methylthio) benzene with horseradish peroxidase compounds I and II. Biochemistry 29(11):2757–2763

    CAS  PubMed  Google Scholar 

  33. Doerge DR, Cooray NM, Brewster ME (1991) Peroxidase-catalyzed S-oxygenation: mechanism of oxygen transfer for lactoperoxidase. Biochemistry 30(37):8960–8964

    CAS  PubMed  Google Scholar 

  34. Kobayashi S, Nakano M, Kimura T, Schaap AP (1987) On the mechanism of the peroxidase-catalyzed oxygen-transfer reaction. Biochemistry 26(16):5019–5022

    CAS  PubMed  Google Scholar 

  35. Newmyer SL, de Montellano PRO (1995) Horseradish Peroxidase His-42→ Ala, His-42→ Val, and Phe-41→ Ala Mutants histidine catalysis and control of substrate access to the heme iron. J Biol Chem 270(33):19430–19438

    CAS  PubMed  Google Scholar 

  36. Hashimoto S, Tatsuno Y, Kitagawa T (1986) Resonance Raman evidence for oxygen exchange between the FeIV= O heme and bulk water during enzymic catalysis of horseradish peroxidase and its relation with the heme-linked ionization. Proc Natl Acad Sci 83(8):2417–2421

    CAS  PubMed  PubMed Central  Google Scholar 

  37. Kamble MP, Shinde SD, Yadav GD (2016) Kinetic resolution of (R, S)-α-tetralol catalyzed by crosslinked Candida antarctica lipase B enzyme supported on mesocellular foam: a nanoscale enzyme reactor approach. J Mol Catal B Enzym 132:61–66

    CAS  Google Scholar 

  38. Mathpati AC, Badgujar KC, Bhanage BM (2016) Kinetic modeling and docking study of immobilized lipase catalyzed synthesis of furfuryl acetate. Enzyme Microb Technol 84:1–10

    CAS  PubMed  Google Scholar 

  39. Zhang Y, Zhao Y, Jiang W, Yao Q, Li Z, Gao X, Liu T, Yang F, Wang F, Liu J (2019) Lipase-catalyzed oxidation of cyclohexanone to form ε-caprolactone and kinetic modeling. ACS Sustainable Chemistry & Engineering 7(15):13294–13306

    CAS  Google Scholar 

  40. Zhang Y, Zhao Y, Gao X, Jiang W, Li Z, Yao Q, Yang F, Wang F, Liu J (2019) Kinetic model of the enzymatic Michael addition for synthesis of mitomycin analogs catalyzed by immobilized lipase from T. laibacchii. Molecular Catalysis 466:146–156

    CAS  Google Scholar 

  41. Dai L, Klibanov AM (2000) Peroxidase-catalyzed asymmetric sulfoxidation in organic solvents versus in water. Biotechnol Bioeng 70(3):353–357

    CAS  PubMed  Google Scholar 

  42. Colonna S, Gaggero N, Richelmi C, Pasta P (1999) Recent biotechnological developments in the use of peroxidases. Trends Biotechnol 17(4):163–168

    CAS  PubMed  Google Scholar 

  43. Zhang Y, Kuiying L, Deng Y, Li H, Wang Z, Li D, Gao X, Wang F (2021) Asymmetric Biooxidation using resting cells of Rhodococcus rhodochrous ATCC 4276 mutant QZ-3 for preparation of (S)-omeprazole in a chloroform–water biphasic system using response surface methodology. Catal Lett. https://doi.org/10.1007/s10562-021-03531-w

    Article  Google Scholar 

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Acknowledgements

This work was supported by the National Natural Science Foundation of China [Grant Numbers 21546004 and 21576145], China Scholarship Council (Grant Number: 201908370079) and Shandong Provincial Key R&D Program [Grant Numbers 2019GSF107027, 2019GNC106028 and 2019GSF107033].

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Author notes

  1. Yuanyuan Zhang contributed equally to this work and should be considered co-first authors.

Authors and Affiliations

  1. State Key Laboratory Base for, Eco-Chemical Engineering in College of Chemical Engineering, Qingdao University of Science and Technology, Mail box 70, 53 Zhengzhou Road, Qingdao, 266042, China

    Hui Tang, Yuanyuan Zhang, Depeng Li, Xin Gao & Fanye Wang

  2. William G. Lowrie Department of Chemical and Biomolecular Engineering, The Ohio State University, 151 West Woodruff Avenue, Columbus, OH, 43210, USA

    Hui Tang & Yuanyuan Zhang

  3. Kekulé-Institut Für Organische Chemie und Biochemieder, Rheinischen Friedrich -Wilhelms-Universität Bonn Gerhard-Domagk-Str, 153121, Bonn, Germany

    Depeng Li, Zhiyong Wang & Xin Gao

  4. Department of Pharmaceutical Engineering, College of Chemical Engineering, Qingdao University of Science and Technology, Mail box 70, 53 Zhengzhou Road, Qingdao, 266042, China

    Yashan Deng, Shanshan Du, Zhiyong Wang & Huiling Li

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  1. Hui Tang
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HT and YYZ designed and wrote the manuscript; YSD, DPL, ZYW, HLL, XG, FYW revised the manuscript.

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Correspondence to Yuanyuan Zhang, Xin Gao or Fanye Wang.

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Tang, H., Zhang, Y., Deng, Y. et al. Optimization of Synthesis of (S)-Omeprazole Catalyzed by Soybean Pod Peroxidase in Water-in-Oil Microemulsions Using RSM. Catal Lett 152, 720–731 (2022). https://doi.org/10.1007/s10562-021-03681-x

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