Origanum vulgare as a Possible Modulator of Testicular Endocrine Function in Mice

Authors: Eva Tvrdá, Barbora Babečková, Michal Ďuračka, Róbert Kirchner, Július Árvay

Abstract:

This study was designed to assess the in vitro effects of Origanum vulgare L. (oregano) extract on the testicular steroidogenesis. We focused on identifying major biomolecules present in the oregano extract, as well as to investigate its in vitro impact on the secretion of cholesterol, testosterone, dehydroepiandrosterone and androstenedione by murine testicular fragments. The extract was subjected to high performance liquid chromatography (HPLC) which identified cyranosid, daidzein, thymol, rosmarinic and trans-caffeic acid among the predominant biochemical components of oregano. For the in vitro experiments, testicular fragments from 20 sexually mature Institute of Cancer Research (ICR) mice were incubated in the absence (control group) or presence of the oregano extract at selected concentrations (10, 100 and 1000 μg/mL) for 24 h. Cholesterol levels were quantified using photometry and the hormones were assessed by ELISA (Enzyme-Linked Immunosorbent Assay). Our data revealed that the release of cholesterol and androstenedione (but not dehydroepiandrosterone and testosterone) by the testicular fragments was significantly impacted by the oregano extract in a dose-dependent fashion. Supplementation of the extract resulted in a significant decline of cholesterol (P < 0.05 in case of 100 μg/mL; P < 0.01 with respect 100 μg/mL extract), as well as androstenedione (P < 0.01 with respect to 100 and 1000 μg/mL extract). Our results suggest that the biomolecules present in Origanum vulgare L. could exhibit a dose-dependent impact on the secretion of male steroids, playing a role in the regulation of testicular steroidogenesis.

Keywords: Mice, Origanum vulgare L., steroidogenesis, testes.

Digital Object Identifier (DOI): doi.org/10.5281/zenodo.3462115

References:

[1] S. Kumar, S. Paul, Y. K. Walia, A. Kumar, and P. Singhal, “Therapeutic potential of medicinal plants: A review,” Journal of Biological and Chemical Chronicles, vol. 1, no. 1, pp. 46-54, 2015.
[2] WHO, “WHO traditional medicine strategy 2002–2005”. Edited by J. D. Quick, J. Sawyer, P. Thorpe, D. Whitney, X. Zhang. World Health Organization, Geneva, 2002.
[3] H. E. Thu, I. N. Mohamed, Z. Hussain, P. A. Jayusman, A. N. Shuid, “Eurycoma longifolia as a potential adoptogen of male sexual health: a systematic review on clinical studies,” Chinese Journal of Natural Medicines, vol. 15, no. 1, pp. 71-80, 2017.
[4] W. H. El–Tantawy, A. Temraz, and O. D. El–Gindi, “Free serum testosterone level in male rats treated with Tribulus alatus extracts,” International Brazilian Journal of Urology, vol. 33, no. 4, pp. 554-558, 2007.
[5] V. R. Ambiye, D. Langade, S. Dongre, P. Aptikar, M. Kulkarni, and A. Dongre, “Clinical Evaluation of the Spermatogenic Activity of the root extract of Ashwagandha (Withania somnifera) in oligospermic males: A pilot study”, Evidence-Based Complementary and Alternative Medicine, vol. 2013, doi: 10.1155/2013/571420, 2013.
[6] A. Morales, “Yohimbine in erectile dysfunction: the facts”, International Journal of Impotence Research, vol. 12, suppl. 1, pp. 70-74, 2000.
[7] M. Fournomiti, A. Kimbaris, I. Mantzourani, S. Plessas, I. Theodoridou, V. Papaemmanouil, I. Kapsiotis, M. Panopoulou, E. Stavropoulou, E. E. Bezirtzoglou, and A. Alexopoulos, “Antimicrobial activity of essential oils of cultivated oregano (Origanum vulgare), sage (Salvia officinalis), and thyme (Thymus vulgaris) against clinical isolates of Escherichia coli, Klebsiella oxytoca, and Klebsiella pneumoniae”, Pakistan Journal of Pharmaceutical Sciences, vol. 44, no. 2, pp. 421-424, 2009.
[8] B. Teixeira, A. Marques, C. Ramos, C. Serrano, O. Matos, N. R. Neng, J. M. Nogueira, J. A. Saraiva, and M. L. Nunes, “Chemical composition and bioactivity of different oregano (Origanum vulgare) extracts and essential oil,” Journal of the Science of Food and Agriculture, vol. 93, no. 11, pp. 2707-2714, 2013.
[9] M. Vazirian, M. Mohammadi, M. H. Farzaei, G. Amin, and Y. Amanzadeh, “Chemical composition and antioxidant activity of Origanum vulgare subsp. vulgare essential oil from Iran”, Research Journal of Pharmacognosy, vol. 2, no. 1, pp. 41-46, 2015.
[10] J. M. García-Beltrán, and M. Á. Esteban, “Properties and applications of plants of Origanum sp. genus,” SM Journal of Biology, vol. 2, no.1, pp. 1006-1015, 2016.
[11] M. Güvenç, M. Cellat, I. Gökçek, I. Yavaş, and Y. Özsoy, “Effects of thymol and carvacrol on sperm quality and oxidant/antioxidant balance in rats,” Archives of Physiology and Biochemistry, vol. 25, pp. 1-8, 2018.
[12] N. A. ElSawy, A. G. Alkushi, W. A. M. Alasmary, M. M. Sinna, E. A. Header, M. A. Elmadbouly, and A. M. E. Ali Sakran, “Does oregano protect against testicular toxicity produced by ethylene glycol in adult male albino rat?” International Journal of Morphology, vol. 37, no. 1, pp. 358-362, 2019.
[13] E. Tvrdá, J. Michalko, I. Matušíková, and N. Lukáč N, “In vitro effects of the Chlamydomonas reinhardtii extract on bovine spermatozoa,” Journal of Microbiology, Biotechnology and Food Sciences, vol. 6, pp. 972-975, 2016.
[14] L. Luksic, J. Árvay, A. Vollmannová, T. Tóth, V. Skrabanja, J. Trcek, M. Germ, and I. Kreft I, “Hydrothermal treatment of Tartary buckwheat grain hinders the transformation of rutin to quercetin,” Journal of Cereal Science, vol. 72, pp. 131-134, 2016.
[15] S. Saeidnia, A. Manayi, and M. Abdollahi, “From in vitro experiments to in vivo and clinical studies; pros and cons,” Current Drug Discovery Technologies, vol. 12, no. 4, pp. 218-224, 2015.
[16] D. Mockute, G. Bernotiene, and A. Judzentiene, “The beta-ocimene chemotype of essential oils of the inflorescences and the leaves with stems from Origanum vulgare ssp. vulgare growing wild in Lithuania,” Biochemical Systematics and Ecology, vol. 31, pp. 269-278, 2003.
[17] C. B. Hollenbach, R. S. Bing, R. Stedile, F. P. da Silva Mello, T. L. Schuch, M. R. Alves Rodrigues, F. B. de Mello, and J. R. Braga de Mello, “Reproductive toxicity assessment of Origanum vulgare essential oil on male Wistar rats,” Acta Scientiae Veterinariae, vol. 43, pp. 1295-1302, 2015.
[18] H. Chen, A. Midzak, L. D. Luo, and B. R. Zirkin, “Aging and decline of androgen production. Leydig cell in health and disease,” Contemporary Endocrinology, vol. 2, pp. 117-131, 2007.
[19] S. Pflieger-Bruss, H. C. Schuppe, and W. B. Schill, “The male reproductive system and its susceptibility to endocrine disrupting chemicals,” Andrologia, vol. 36, pp. 337-345, 2004.
[20] C. H. Song, E. Y. Gong, Js. Park, K. Lee, “Testicular steroidogenesis is locally regulated by androgen via suppression of Nur77,” Biochemical and Biophysical Research Communications, vol. 422, no. 2, pp. 327-332, 2012.
[21] D. M. Kelly, and T. H. Jones. “Testosterone: a metabolic hormone in health and disease,” Journal of Endocrinology, vol. 29, no. 3, pp. 25-45, 2013.
[22] T. Jambor, H. Greifova, A. Kovacik, E. Kovacikova, E. Tvrda, Z. Forgacs, P. Massanyi, and N. Lukac, “Parallel effect of 4-octylphenol and cyclic adenosine monophosphate (cAMP) alters steroidogenesis, cell viability and ROS production in mice Leydig cells,” Chemosphere, vol. 199, pp. 747-754, 2018.
[23] Z. E. Suntres, J. Coccimiglio, and M. Alipour, “The bioactivity and toxicological actions of carvacrol,” Critical Reviews in Food Science and Nutrition, vol. 55, pp. 304-318, 2015.
[24] C. B. Hollenbach, R. Stedile, F. P. da Silva Mello, R. S. Bing, P. P. da Rosa, M. R. Alves Rodrigues, F. B. de Mello, R. A. Zanette, and J. R. Braga de Mello, “Pre- and postnatal evaluation of offspring rats exposed to Origanum vulgare essential oil during mating, gestation and lactation,” Ciência Rural, Santa Maria, vol. 47, no. 1, p. 1-6, 2017.