Biocatalytic Synthesis of Terpene Esters and their Biological Activity in Human Glioma Cells

Page: [760 - 765] Pages: 6

  • * (Excluding Mailing and Handling)

Abstract

Background: Gliomas are highly malignant brain tumours with high resistance to chemotherapy. Therefore, investigations of new therapeutic molecules with high anti-glioma activity are of great importance.

Objectives: In this work, biocatalytic esterification of terpene alcohols with proven anti-cancer activity was performed to enhance their potency to induce cell death in human glioblastoma multiforme T98G and anaplastic astrocytoma MOGGCCM cell lines in vitro.

Methods and Results: We used primary terpene alcohols and carboxylic acids with a length of two to nine carbon atoms. The structure of the alcohols had an influence on the esterification efficiency, which decreased in the following order: monocyclic > linear > bicyclic. Terpene alcohols and their esters only induced apoptotic cell death, which is highly desirable from a therapeutic point of view, but did not induce autophagy and necrosis. The esterification of perillyl alcohol with butyric acid caused a 4-fold increase in cell death induction in the T98G line. Citronellol valerate, caprylate, and pelargonate and myrtenol butyrate, caprylate and pelargonate also showed higher activity than their alcohol precursors.

Conclusion: We have herein shown that esterification of natural alcohols by biocatalysis can be used for improving the activity of other compounds investigated for their anti-glioma activity.

Keywords: Terpene esters, biocatalysis, esterification, biological activity, apoptosis, glioblastoma.

Graphical Abstract

[1]
Jakubowicz-Gil, J.; Langner, E.; Bądziul, D.; Wertel, I.; Rzeski, W. Apoptosis induction in human glioblastoma multiforme t98g cells upon temozolomide and quercetin treatment. Tumour Biol., 2013, 34(4), 2367-2378.
[http://dx.doi.org/10.1007/s13277-013-0785-0] [PMID: 23580181]
[2]
Olivier, C.; Oliver, L.; Lalier, L.; Vallette, F.M. Drug resistance in glioblastoma: the two faces of oxidative stress. Front. Mol. Biosci., 2021, 7, 620677.
[http://dx.doi.org/10.3389/fmolb.2020.620677] [PMID: 33585565]
[3]
Louis, D.N.; Perry, A.; Reifenberger, G.; von Deimling, A.; Figarella-Branger, D.; Cavenee, W.K.; Ohgaki, H.; Wiestler, O.D.; Kleihues, P.; Ellison, D.W. The 2016 World Health Organization classification of tumors of the central nervous system: A summary. Acta Neuropathol., 2016, 131(6), 803-820.
[http://dx.doi.org/10.1007/s00401-016-1545-1] [PMID: 27157931]
[4]
Gupta, A.; Dwivedi, T. Simplified overview of World Health Organization classification update of central nervous system tumors. J. Neurosci. Rural Pract., 2017, 8(4), 629-641.
[http://dx.doi.org/10.4103/jnrp.jnrp_168_17] [PMID: 29204027]
[5]
Wang, J.; Hu, G.; Quan, X. Analysis of the factors affecting the prognosis of glioma patients. Open Med. (Wars.), 2019, 14, 331-335.
[http://dx.doi.org/10.1515/med-2019-0031] [PMID: 30997396]
[6]
Patil, C.G.; Yi, A.; Elramsisy, A.; Hu, J.; Mukherjee, D.; Irvin, D.K.; Yu, J.S.; Bannykh, S.I.; Black, K.L.; Nuño, M. Prognosis of patients with multifocal glioblastoma: A case-control study. J. Neurosurg., 2012, 117(4), 705-711.
[http://dx.doi.org/10.3171/2012.7.JNS12147] [PMID: 22920963]
[7]
Ahmed, R.; Oborski, M.J.; Hwang, M.; Lieberman, F.S.; Mountz, J.M. Malignant gliomas: Current perspectives in diagnosis, treatment, and early response assessment using advanced quantitative imaging methods. Cancer Manag. Res., 2014, 6, 149-170.
[PMID: 24711712]
[8]
Paduch, R.; Kandefer-Szerszeń, M.; Trytek, M.; Fiedurek, J. Terpenes: Substances useful in human healthcare. Arch. Immunol. Ther. Exp. (Warsz.), 2007, 55(5), 315-327.
[http://dx.doi.org/10.1007/s00005-007-0039-1] [PMID: 18219762]
[9]
Burke, Y.D.; Ayoubi, A.S.; Werner, S.R.; McFarland, B.C.; Heilman, D.K.; Ruggeri, B.A.; Crowell, P.L. Effects of the isoprenoids perillyl alcohol and farnesol on apoptosis biomarkers in pancreatic cancer chemoprevention. Anticancer Res., 2002, 22(6A), 3127-3134.
[PMID: 12530055]
[10]
Trytek, M.; Paduch, R.; Pięt, M.; Kozieł, A.; Kandefer-Szerszeń, M.; Szajnecki, Ł.; Gromada, A. Biological activity of oxygenated pinene derivatives on human colon normal and carcinoma cells; Flavour Fragr. J., 2018, pp. 1-10.
[11]
Wojtunik-Kulesza, K.A.; Kasprzak, K.; Oniszczuk, T.; Oniszczuk, A. Natural monoterpenes: Much more than only a scent. Chem. Biodivers., 2019, 16(12), e1900434.
[http://dx.doi.org/10.1002/cbdv.201900434] [PMID: 31587473]
[12]
Erices, J.I.; Torres, Á.; Niechi, I.; Bernales, I.; Quezada, C. Current natural therapies in the treatment against glioblastoma. Phytother. Res., 2018, 32(11), 2191-2201.
[http://dx.doi.org/10.1002/ptr.6170] [PMID: 30109743]
[13]
da Fonseca, C.O.; Simão, M.; Lins, I.R.; Caetano, R.O.; Futuro, D.; Quirico-Santos, T. Efficacy of monoterpene perillyl alcohol upon survival rate of patients with recurrent glioblastoma. J. Cancer Res. Clin. Oncol., 2011, 137(2), 287-293.
[http://dx.doi.org/10.1007/s00432-010-0873-0] [PMID: 20401670]
[14]
Viskupicova, J.; Danihelova, M.; Ondrejovic, M.; Liptaj, T.; Sturdik, E. Lipophilic rutin derivatives for antioxidant protection of oil-based foods. Food Chem., 2010, 123, 45-50.
[http://dx.doi.org/10.1016/j.foodchem.2010.03.125]
[15]
Pedersen, J.N.; Liu, S.; Zhou, Y.; Balle, T.; Xu, X.; Guo, Z. Synergistic effects of binary ionic liquid-solvent systems on enzymatic esterification of esculin. Food Chem., 2020, 310, 125858.
[http://dx.doi.org/10.1016/j.foodchem.2019.125858] [PMID: 31753682]
[16]
Stergiou, P.Y.; Foukis, A.; Filippou, M.; Koukouritaki, M.; Parapouli, M.; Theodorou, L.G.; Hatziloukas, E.; Afendra, A.; Pandey, A.; Papamichael, E.M. Advances in lipase-catalyzed esterification reactions. Biotechnol. Adv., 2013, 31(8), 1846-1859.
[http://dx.doi.org/10.1016/j.biotechadv.2013.08.006] [PMID: 23954307]
[17]
Tamborini, L.; Romano, D.; Pinto, A.; Contente, M.; Iannuzzi, M.C.; Conti, P.; Molinari, F. Biotransformation with whole microbial systems in a continuous flow reactor: Resolution of (RS)-flurbiprofen using Aspergillus oryzae by direct esterification with ethanol in organic solvent. Tetrahedron Lett., 2013, 54, 6090-6093.
[http://dx.doi.org/10.1016/j.tetlet.2013.08.119]
[18]
Kutyła, M.; Trytek, M.; Buczek, K.; Tomaszewska, E.; Muszyński, S. Biomass of a psychrophilic fungus as a biocatalyst for efficient direct esterification of citronellol. BioEnergy Res., 2021.
[http://dx.doi.org/10.1007/s12155-021-10289-x]
[19]
Trytek, M.; Jędrzejewski, K.; Fiedurek, J. Bioconversion of α-pinene by a novel cold-adapted fungus Chrysosporium pannorum. J. Ind. Microbiol. Biotechnol., 2015, 42(2), 181-188.
[http://dx.doi.org/10.1007/s10295-014-1550-0] [PMID: 25487757]
[20]
Sumorek-Wiadro, J.; Zając, A.; Bądziul, D.; Langner, E.; Skalicka-Woźniak, K.; Maciejczyk, A.; Wertel, I.; Rzeski, W.; Jakubowicz-Gil, J. Coumarins modulate the anti-glioma properties of temozolomide. Eur. J. Pharmacol., 2020, 881, 173207.
[http://dx.doi.org/10.1016/j.ejphar.2020.173207] [PMID: 32446712]
[21]
Zając, A.; Sumorek-Wiadro, J.; Langner, E.; Wertel, I.; Maciejczyk, A.; Pawlikowska-Pawlęga, B.; Pawelec, J.; Wasiak, M.; Hułas-Stasiak, M.; Bądziul, D.; Rzeski, W.; Reichert, M.; Jakubowicz-Gil, J. Involvement of PI3K pathway in glioma cell resistance to temozolomide treatment. Int. J. Mol. Sci., 2021, 22(10), 5155.
[http://dx.doi.org/10.3390/ijms22105155] [PMID: 34068110]
[22]
Desai, V.; Bhushan, A. Natural bioactive compounds: Alternative approach to the treatment of glioblastoma multiforme. BioMed Res. Int., 2017, 9363040.
[http://dx.doi.org/10.1155/2017/9363040] [PMID: 29359162]
[23]
Kutyła, M.; Fiedurek, J.; Gromada, A.; Jędrzejewski, K.; Trytek, M. Mutagenesis and adaptation of the psychrotrophic fungus Chrysosporium pannorum A-1 as a method for improving β-pinene bioconversion. Molecules, 2020, 25(11), 2589.
[http://dx.doi.org/10.3390/molecules25112589] [PMID: 32498456]
[24]
Trytek, M.; Fiedurek, J.; Gromada, A. Effect of some abiotic stresses on the biotransformation of α-pinene by a psychrotrophic Chrysosporium pannorum. Biochem. Eng. J., 2016, 112, 86-93.
[http://dx.doi.org/10.1016/j.bej.2016.03.010]
[25]
Diaz, M.D.R.; Gomez, J.M.; Diaz-Suelto, B.; Garcia-Sans, A. Enzymatic synthesis of short-chain esters in n-hexane and supercritical carbon dioxide: effect of the acid chain length. Eng. Life Sci., 2010, 10, 171-176.
[http://dx.doi.org/10.1002/elsc.200900097]
[26]
Jakubowicz-Gil, J.; Bądziul, D.; Langner, E.; Wertel, I.; Zając, A.; Rzeski, W. Temozolomide and sorafenib as programmed cell death inducers of human glioma cells. Pharmacol. Rep., 2017, 69(4), 779-787.
[http://dx.doi.org/10.1016/j.pharep.2017.03.008] [PMID: 28587939]